A Review of Techniques for Biodelivery of Nerve Growth Factor (NGF) to the Brain in Relation to Alzheimer's Disease.
Alzheimer’s disease (AD)
Brain
Delivery
Methods
Nerve growth factor (NGF)
Techniques
Journal
Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103
Informations de publication
Date de publication:
2021
2021
Historique:
entrez:
28
8
2021
pubmed:
29
8
2021
medline:
1
9
2021
Statut:
ppublish
Résumé
Age-dependent progressive neurodegeneration and associated cognitive dysfunction represent a serious concern worldwide. Currently, dementia accounts for the fifth highest cause of death, among which Alzheimer's disease (AD) represents more than 60% of the cases. AD is associated with progressive cognitive dysfunction which affects daily life of the affected individual and associated family. The cognitive dysfunctions are at least partially due to the degeneration of a specific set of neurons (cholinergic neurons) whose cell bodies are situated in the basal forebrain region (basal forebrain cholinergic neurons, BFCNs) but innervate wide areas of the brain. It has been explicitly shown that the delivery of the neurotrophic protein nerve growth factor (NGF) can rescue BFCNs and restore cognitive dysfunction, making NGF interesting as a potential therapeutic substance for AD. Unfortunately, NGF cannot pass through the blood-brain barrier (BBB) and thus peripheral administration of NGF protein is not viable therapeutically. NGF must be delivered in a way which will allow its brain penetration and availability to the BFCNs to modulate BFCN activity and viability. Over the past few decades, various methodologies have been developed to deliver NGF to the brain tissue. In this chapter, NGF delivery methods are discussed in the context of AD.
Identifiants
pubmed: 34453298
doi: 10.1007/978-3-030-74046-7_11
doi:
Substances chimiques
Nerve Growth Factor
9061-61-4
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
167-191Informations de copyright
© 2021. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Ager RR, Davis JL, Agazaryan A, Benavente F, Poon WW, LaFerla FM, Blurton-Jones M (2015) Human neural stem cells improve cognition and promote synaptic growth in two complementary transgenic models of Alzheimer’s disease and neuronal loss. Hippocampus 25(7):813–826. https://doi.org/10.1002/hipo.22405
doi: 10.1002/hipo.22405
pubmed: 25530343
pmcid: 4722865
Albeck DS, Backman C, Veng L, Friden P, Rose GM, Granholm A (1999) Acute application of NGF increases the firing rate of aged rat basal forebrain neurons. Eur J Neurosci 11(7):2291–2304. https://doi.org/10.1046/j.1460-9568.1999.00644.x
doi: 10.1046/j.1460-9568.1999.00644.x
pubmed: 10383618
Allard S, Leon WC, Pakavathkumar P, Bruno MA, Ribeiro-da-Silva A, Cuello AC (2012) Impact of the NGF maturation and degradation pathway on the cortical cholinergic system phenotype. J Neurosci 32(6):2002–2012. https://doi.org/10.1523/JNEUROSCI.1144-11.2012
doi: 10.1523/JNEUROSCI.1144-11.2012
pubmed: 22323714
pmcid: 6621687
Aloe L, Rocco ML, Bianchi P, Manni L (2012) Nerve growth factor: from the early discoveries to the potential clinical use. J Transl Med 10:239. https://doi.org/10.1186/1479-5876-10-239
doi: 10.1186/1479-5876-10-239
pubmed: 23190582
pmcid: 3543237
Aloe L, Rocco ML, Balzamino BO, Micera A (2015) Nerve growth factor: a focus on neuroscience and therapy. Curr Neuropharmacol 13(3):294–303. https://doi.org/10.2174/1570159x13666150403231920
doi: 10.2174/1570159x13666150403231920
pubmed: 26411962
pmcid: 4812798
Aloe L, Rocco ML, Balzamino BO, Micera A (2016) Nerve growth factor: role in growth, differentiation and controlling cancer cell development. J Exp Clin Cancer Res 35(1):116. https://doi.org/10.1186/s13046-016-0395-y
doi: 10.1186/s13046-016-0395-y
pubmed: 27439311
pmcid: 4955168
Altar CA, Bakhit C (1991) Receptor-mediated transport of human recombinant nerve growth factor from olfactory bulb to forebrain cholinergic nuclei. Brain Res 541(1):82–88. https://doi.org/10.1016/0006-8993(91)91077-e
doi: 10.1016/0006-8993(91)91077-e
pubmed: 1851448
Backman C, Rose GM, Hoffer BJ, Henry MA, Bartus RT, Friden P, Granholm AC (1996) Systemic administration of a nerve growth factor conjugate reverses age-related cognitive dysfunction and prevents cholinergic neuron atrophy. J Neurosci 16(17):5437–5442
doi: 10.1523/JNEUROSCI.16-17-05437.1996
Balin BJ, Hudson AP (2018) Herpes viruses and Alzheimer’s disease: new evidence in the debate. Lancet Neurol 17(10):839–841. https://doi.org/10.1016/S1474-4422(18)30316-8
doi: 10.1016/S1474-4422(18)30316-8
pubmed: 30264721
Bartus RT, Dean RL 3rd, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217(4558):408–414
doi: 10.1126/science.7046051
Bernabeu-Zornoza A, Coronel R, Palmer C, Monteagudo M, Zambrano A, Liste I (2019) Physiological and pathological effects of amyloid-beta species in neural stem cell biology. Neural Regen Res 14(12):2035–2042. https://doi.org/10.4103/1673-5374.262571
doi: 10.4103/1673-5374.262571
pubmed: 31397330
pmcid: 6788229
Binder N, Balmford J, Schumacher M (2019) A multi-state model based reanalysis of the Framingham heart study: is dementia incidence really declining? Eur J Epidemiol 34(11):1075–1083. https://doi.org/10.1007/s10654-019-00567-6
doi: 10.1007/s10654-019-00567-6
pubmed: 31612352
Birks JS, Harvey RJ (2018) Donepezil for dementia due to Alzheimer’s disease. Cochrane Database Syst Rev 6:CD001190. https://doi.org/10.1002/14651858.CD001190.pub3
doi: 10.1002/14651858.CD001190.pub3
pubmed: 29923184
Bishop KM, Hofer EK, Mehta A, Ramirez A, Sun L, Tuszynski M, Bartus RT (2008) Therapeutic potential of CERE-110 (AAV2-NGF): targeted, stable, and sustained NGF delivery and trophic activity on rodent basal forebrain cholinergic neurons. Exp Neurol 211(2):574–584. https://doi.org/10.1016/j.expneurol.2008.03.004
doi: 10.1016/j.expneurol.2008.03.004
pubmed: 18439998
pmcid: 2709503
Blondy S, Christou N, David V, Verdier M, Jauberteau MO, Mathonnet M, Perraud A (2019) Neurotrophins and their involvement in digestive cancers. Cell Death Dis 10(2):123. https://doi.org/10.1038/s41419-019-1385-8
doi: 10.1038/s41419-019-1385-8
pubmed: 30741921
pmcid: 6370832
Bonini S, Lambiase A, Rama P, Caprioglio G, Aloe L (2000) Topical treatment with nerve growth factor for neurotrophic keratitis. Ophthalmology 107(7):1347–1351.; Discussion 1351–1342. https://doi.org/10.1016/s0161-6420(00)00163-9
doi: 10.1016/s0161-6420(00)00163-9
pubmed: 10889110
Bourganis V, Kammona O, Alexopoulos A, Kiparissides C (2018) Recent advances in carrier mediated nose-to-brain delivery of pharmaceutics. Eur J Pharm Biopharm 128:337–362. https://doi.org/10.1016/j.ejpb.2018.05.009
doi: 10.1016/j.ejpb.2018.05.009
pubmed: 29733950
Bracci-Laudiero L, Manni L (2014) NGF and immune regulation. In: Kostrzewa RM (ed) Handbook of neurotoxicity. Springer, New York
Bradshaw RA, Mobley W, Rush RA (2017) Nerve growth factor and related substances: a brief history and an introduction to the international NGF meeting series. Int J Mol Sci 18(6):1143. https://doi.org/10.3390/ijms18061143
doi: 10.3390/ijms18061143
pmcid: 5485967
Bruno MA, Cuello AC (2006) Activity-dependent release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by a protease cascade. Proc Natl Acad Sci U S A 103(17):6735–6740. https://doi.org/10.1073/pnas.0510645103
doi: 10.1073/pnas.0510645103
pubmed: 16618925
pmcid: 1458950
Cairns DM, Rouleau N, Parker RN, Walsh KG, Gehrke L, Kaplan DL (2020) A 3D human brain-like tissue model of herpes-induced Alzheimer’s disease. Sci Adv 6(19):eaay8828. https://doi.org/10.1126/sciadv.aay8828
doi: 10.1126/sciadv.aay8828
pubmed: 32494701
pmcid: 7202879
Camarata PJ, Suryanarayanan R, Turner DA, Parker RG, Ebner TJ (1992) Sustained release of nerve growth factor from biodegradable polymer microspheres. Neurosurgery 30(3):313–319. https://doi.org/10.1227/00006123-199203000-00001
doi: 10.1227/00006123-199203000-00001
pubmed: 1620291
Capsoni S, Giannotta S, Cattaneo A (2002) Nerve growth factor and galantamine ameliorate early signs of neurodegeneration in anti-nerve growth factor mice. Proc Natl Acad Sci U S A 99(19):12432–12437. https://doi.org/10.1073/pnas.192442999
doi: 10.1073/pnas.192442999
pubmed: 12205295
pmcid: 129462
Capsoni S, Covaceuszach S, Ugolini G, Spirito F, Vignone D, Stefanini B, Amato G, Cattaneo A (2009) Delivery of NGF to the brain: intranasal versus ocular administration in anti-NGF transgenic mice. J Alzheimers Dis 16(2):371–388. https://doi.org/10.3233/JAD-2009-0953
doi: 10.3233/JAD-2009-0953
pubmed: 19221427
Capsoni S, Brandi R, Arisi I, D’Onofrio M, Cattaneo A (2011) A dual mechanism linking NGF/proNGF imbalance and early inflammation to Alzheimer’s disease neurodegeneration in the AD11 anti-NGF mouse model. CNS Neurol Disord Drug Targets 10(5):635–647
doi: 10.2174/187152711796235032
Capsoni S, Marinelli S, Ceci M, Vignone D, Amato G, Malerba F, Paoletti F, Meli G, Viegi A, Pavone F, Cattaneo A (2012) Intranasal “painless” human nerve growth factor [corrected] slows amyloid neurodegeneration and prevents memory deficits in App X PS1 mice. PLoS One 7(5):e37555. https://doi.org/10.1371/journal.pone.0037555
doi: 10.1371/journal.pone.0037555
pubmed: 22666365
pmcid: 3364340
Capsoni S, Amato G, Vignone D, Criscuolo C, Nykjaer A, Cattaneo A (2013) Dissecting the role of sortilin receptor signaling in neurodegeneration induced by NGF deprivation. Biochem Biophys Res Commun 431(3):579–585. https://doi.org/10.1016/j.bbrc.2013.01.007
doi: 10.1016/j.bbrc.2013.01.007
pubmed: 23313508
pmcid: 3585961
Castle MJ, Baltanas FC, Kovacs I, Nagahara AH, Barba D, Tuszynski MH (2020) Postmortem analysis in a clinical trial of AAV2-NGF gene therapy for Alzheimer’s disease identifies a need for improved vector delivery. Hum Gene Ther 31(7-8):415–422. https://doi.org/10.1089/hum.2019.367
doi: 10.1089/hum.2019.367
pubmed: 32126838
pmcid: 7194314
Cattaneo A, Capsoni S (2019) Painless nerve growth factor: a TrkA biased agonist mediating a broad neuroprotection via its actions on microglia cells. Pharmacol Res 139:17–25. https://doi.org/10.1016/j.phrs.2018.10.028
doi: 10.1016/j.phrs.2018.10.028
pubmed: 30391352
Cattaneo A, Capsoni S, Paoletti F (2008) Towards non invasive nerve growth factor therapies for Alzheimer’s disease. J Alzheimers Dis 15(2):255–283. https://doi.org/10.3233/jad-2008-15210
doi: 10.3233/jad-2008-15210
pubmed: 18953113
Chang DS, Hsu E, Hottinger DG, Cohen SP (2016) Anti-nerve growth factor in pain management: current evidence. J Pain Res 9:373–383. https://doi.org/10.2147/JPR.S89061
doi: 10.2147/JPR.S89061
pubmed: 27354823
pmcid: 4908933
Charles V, Mufson EJ, Friden PM, Bartus RT, Kordower JH (1996) Atrophy of cholinergic basal forebrain neurons following excitotoxic cortical lesions is reversed by intravenous administration of an NGF conjugate. Brain Res 728(2):193–203. https://doi.org/10.1016/0006-8993(96)00398-8
doi: 10.1016/0006-8993(96)00398-8
pubmed: 8864482
Chauhan MB, Chauhan NB (2015) Brain uptake of Neurotherapeutics after intranasal versus intraperitoneal delivery in mice. J Neurol Neurosurg 2:1–9
doi: 10.19104/jnn.2015.91
Chen XQ, Mobley WC (2019) Exploring the pathogenesis of Alzheimer disease in basal forebrain cholinergic neurons: converging insights from alternative hypotheses. Front Neurosci 13:446. https://doi.org/10.3389/fnins.2019.00446
doi: 10.3389/fnins.2019.00446
pubmed: 31133787
pmcid: 6514132
Chen XQ, Fawcett JR, Rahman YE, Ala TA, Frey IW (1998) Delivery of nerve growth factor to the brain via the olfactory pathway. J Alzheimers Dis 1(1):35–44. https://doi.org/10.3233/jad-1998-1102
doi: 10.3233/jad-1998-1102
pubmed: 12214010
Chiaretti A, Genovese O, Riccardi R, Di Rocco C, Di Giuda D, Mariotti P, Pulitano S, Piastra M, Polidori G, Colafati GS, Aloe L (2005) Intraventricular nerve growth factor infusion: a possible treatment for neurological deficits following hypoxic-ischemic brain injury in infants. Neurol Res 27(7):741–746. https://doi.org/10.1179/016164105X35611
doi: 10.1179/016164105X35611
pubmed: 16197811
Chiaretti A, Conti G, Falsini B, Buonsenso D, Crasti M, Manni L, Soligo M, Fantacci C, Genovese O, Calcagni ML, Di Giuda D, Mattoli MV, Cocciolillo F, Ferrara P, Ruggiero A, Staccioli S, Colafati GS, Riccardi R (2017) Intranasal nerve growth factor administration improves cerebral functions in a child with severe traumatic brain injury: a case report. Brain Inj 31(11):1538–1547. https://doi.org/10.1080/02699052.2017.1376760
doi: 10.1080/02699052.2017.1376760
pubmed: 28972396
Cohen S, Levi-Montalcini R (1956) A nerve growth-stimulating factor isolated from snake venom. Proc Natl Acad Sci U S A 42(9):571–574. https://doi.org/10.1073/pnas.42.9.571
doi: 10.1073/pnas.42.9.571
pubmed: 16589907
pmcid: 534252
Cohen S, Levi-Montalcini R, Hamburger V (1954) A nerve growth-stimulating factor isolated from sarcom as 37 and 180. Proc Natl Acad Sci U S A 40(10):1014–1018. https://doi.org/10.1073/pnas.40.10.1014
doi: 10.1073/pnas.40.10.1014
pubmed: 16589582
pmcid: 534215
Corvaglia V, Cilli D, Scopa C, Brandi R, Arisi I, Malerba F, La Regina F, Scardigli R, Cattaneo A (2019) ProNGF is a cell-type-specific mitogen for adult hippocampal and for induced neural stem cells. Stem Cells 37(9):1223–1237. https://doi.org/10.1002/stem.3037
doi: 10.1002/stem.3037
pubmed: 31132299
Covaceuszach S, Capsoni S, Ugolini G, Spirito F, Vignone D, Cattaneo A (2009) Development of a non invasive NGF-based therapy for Alzheimer’s disease. Curr Alzheimer Res 6(2):158–170. https://doi.org/10.2174/156720509787602870
doi: 10.2174/156720509787602870
pubmed: 19355851
Cuello AC, Pentz R, Hall H (2019) The brain NGF metabolic pathway in health and in Alzheimer’s pathology. Front Neurosci 13:62. https://doi.org/10.3389/fnins.2019.00062
doi: 10.3389/fnins.2019.00062
pubmed: 30809111
pmcid: 6379336
Cummings J, Feldman HH, Scheltens P (2019) The “rights” of precision drug development for Alzheimer’s disease. Alzheimers Res Ther 11(1):76. https://doi.org/10.1186/s13195-019-0529-5
doi: 10.1186/s13195-019-0529-5
pubmed: 31470905
pmcid: 6717388
Cummings J, Lee G, Ritter A, Sabbagh M, Zhong K (2020) Alzheimer’s disease drug development pipeline: 2020. Alzheimers Dement (N Y) 6(1):e12050. https://doi.org/10.1002/trc2.12050
doi: 10.1002/trc2.12050
Date I, Ohmoto T, Imaoka T, Ono T, Hammang JP, Francis J, Greco C, Emerich DF (1996) Cografting with polymer-encapsulated human nerve growth factor-secreting cells and chromaffin cell survival and behavioral recovery in hemiparkinsonian rats. J Neurosurg 84(6):1006–1012. https://doi.org/10.3171/jns.1996.84.6.1006
doi: 10.3171/jns.1996.84.6.1006
pubmed: 8847564
de Bellis A, de Bellis M, Aloe L (2018) Long-term non-invasive treatment via intranasal administration of nerve growth factor protects the human brain in frontotemporal dementia associated with corticobasal syndrome: a pilot study. J Alzheimers Dis Rep 2(1):67–77. https://doi.org/10.3233/ADR-180055
doi: 10.3233/ADR-180055
pubmed: 30480250
pmcid: 6159695
de Boer R, Knight AM, Spinner RJ, Malessy MJ, Yaszemski MJ, Windebank AJ (2010) In vitro and in vivo release of nerve growth factor from biodegradable poly-lactic-co-glycolic-acid microspheres. J Biomed Mater Res A 95(4):1067–1073. https://doi.org/10.1002/jbm.a.32900
doi: 10.1002/jbm.a.32900
pubmed: 20878933
pmcid: 2989534
De Luca M, Aiuti A, Cossu G, Parmar M, Pellegrini G, Robey PG (2019) Advances in stem cell research and therapeutic development. Nat Cell Biol 21(7):801–811. https://doi.org/10.1038/s41556-019-0344-z
doi: 10.1038/s41556-019-0344-z
pubmed: 31209293
Denk F, Bennett DL, McMahon SB (2017) Nerve growth factor and pain mechanisms. Annu Rev Neurosci 40:307–325. https://doi.org/10.1146/annurev-neuro-072116-031121
doi: 10.1146/annurev-neuro-072116-031121
pubmed: 28441116
De Rosa R, Garcia AA, Braschi C, Capsoni S, Maffei L, Berardi N, Cattaneo A (2005) Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice. Proc Natl Acad Sci U S A 102(10):3811–3816. https://doi.org/10.1073/pnas.0500195102
doi: 10.1073/pnas.0500195102
pubmed: 15728733
pmcid: 553297
Dou KX, Tan MS, Tan CC, Cao XP, Hou XH, Guo QH, Tan L, Mok V, Yu JT (2018) Comparative safety and effectiveness of cholinesterase inhibitors and memantine for Alzheimer’s disease: a network meta-analysis of 41 randomized controlled trials. Alzheimers Res Ther 10(1):126. https://doi.org/10.1186/s13195-018-0457-9
doi: 10.1186/s13195-018-0457-9
pubmed: 30591071
pmcid: 6309083
Elia CA, Tamborini M, Rasile M, Desiato G, Marchetti S, Swuec P, Mazzitelli S, Clemente F, Anselmo A, Matteoli M, Malosio ML, Coco S (2019) Intracerebral injection of extracellular vesicles from mesenchymal stem cells exerts reduced Abeta plaque burden in early stages of a preclinical model of Alzheimer’s disease. Cells 8(9):1059. https://doi.org/10.3390/cells8091059
doi: 10.3390/cells8091059
pmcid: 6770482
Emerich DF, Hammang JP, Baetge EE, Winn SR (1994a) Implantation of polymer-encapsulated human nerve growth factor-secreting fibroblasts attenuates the behavioral and neuropathological consequences of quinolinic acid injections into rodent striatum. Exp Neurol 130(1):141–150. https://doi.org/10.1006/exnr.1994.1193
doi: 10.1006/exnr.1994.1193
pubmed: 7821389
Emerich DF, Winn SR, Harper J, Hammang JP, Baetge EE, Kordower JH (1994b) Implants of polymer-encapsulated human NGF-secreting cells in the nonhuman primate: rescue and sprouting of degenerating cholinergic basal forebrain neurons. J Comp Neurol 349(1):148–164. https://doi.org/10.1002/cne.903490110
doi: 10.1002/cne.903490110
pubmed: 7852623
Emerich DF, Orive G, Thanos C, Tornoe J, Wahlberg LU (2014) Encapsulated cell therapy for neurodegenerative diseases: from promise to product. Adv Drug Deliv Rev 67–68:131–141. https://doi.org/10.1016/j.addr.2013.07.008
doi: 10.1016/j.addr.2013.07.008
pubmed: 23880505
Erdo F, Bors LA, Farkas D, Bajza A, Gizurarson S (2018) Evaluation of intranasal delivery route of drug administration for brain targeting. Brain Res Bull 143:155–170. https://doi.org/10.1016/j.brainresbull.2018.10.009
doi: 10.1016/j.brainresbull.2018.10.009
pubmed: 30449731
Eriksdotter Jonhagen M, Nordberg A, Amberla K, Backman L, Ebendal T, Meyerson B, Olson L, Seiger, Shigeta M, Theodorsson E, Viitanen M, Winblad B, Wahlund LO (1998) Intracerebroventricular infusion of nerve growth factor in three patients with Alzheimer’s disease. Dement Geriatr Cogn Disord 9 (5):246–257. https://doi.org/10.1159/000017069
Eriksdotter M, Navarro-Oviedo M, Mitra S, Wahlberg L, Linderoth B, Tjernberg LO, Behbahani H (2018) Cerebrospinal fluid from Alzheimer patients affects cell-mediated nerve growth factor production and cell survival in vitro. Exp Cell Res 371(1):175–184. https://doi.org/10.1016/j.yexcr.2018.08.007
doi: 10.1016/j.yexcr.2018.08.007
pubmed: 30092220
pmcid: 30092220
Eriksdotter-Jonhagen M, Linderoth B, Lind G, Aladellie L, Almkvist O, Andreasen N, Blennow K, Bogdanovic N, Jelic V, Kadir A, Nordberg A, Sundstrom E, Wahlund LO, Wall A, Wiberg M, Winblad B, Seiger A, Almqvist P, Wahlberg L (2012) Encapsulated cell biodelivery of nerve growth factor to the Basal forebrain in patients with Alzheimer’s disease. Dement Geriatr Cogn Disord 33(1):18–28. https://doi.org/10.1159/000336051
doi: 10.1159/000336051
pubmed: 22377499
Ernfors P, Ebendal T, Olson L, Mouton P, Stromberg I, Persson H (1989) A cell line producing recombinant nerve growth factor evokes growth responses in intrinsic and grafted central cholinergic neurons. Proc Natl Acad Sci U S A 86(12):4756–4760. https://doi.org/10.1073/pnas.86.12.4756
doi: 10.1073/pnas.86.12.4756
pubmed: 2734317
pmcid: 287352
Estenne-Bouhtou G, Kullander K, Karlsson M, Ebendal T, Hacksell U, Luthman K (1996) Design, synthesis, tandem mass spectrometric sequencing and biological activity of NGF mimetics. Int J Pept Protein Res 48(4):337–346. https://doi.org/10.1111/j.1399-3011.1996.tb00850.x
doi: 10.1111/j.1399-3011.1996.tb00850.x
pubmed: 8919054
Eyjolfsdottir H, Eriksdotter M, Linderoth B, Lind G, Juliusson B, Kusk P, Almkvist O, Andreasen N, Blennow K, Ferreira D, Westman E, Nennesmo I, Karami A, Darreh-Shori T, Kadir A, Nordberg A, Sundstrom E, Wahlund LO, Wall A, Wiberg M, Winblad B, Seiger A, Wahlberg L, Almqvist P (2016) Targeted delivery of nerve growth factor to the cholinergic basal forebrain of Alzheimer’s disease patients: application of a second-generation encapsulated cell biodelivery device. Alzheimers Res Ther 8(1):30. https://doi.org/10.1186/s13195-016-0195-9
doi: 10.1186/s13195-016-0195-9
pubmed: 27389402
pmcid: 4936020
Fahnestock M, Shekari A (2019) ProNGF and neurodegeneration in Alzheimer’s disease. Front Neurosci 13:129. https://doi.org/10.3389/fnins.2019.00129
doi: 10.3389/fnins.2019.00129
pubmed: 30853882
pmcid: 6395390
Fantacci C, Capozzi D, Ferrara P, Chiaretti A (2013) Neuroprotective role of nerve growth factor in hypoxic-ischemic brain injury. Brain Sci 3(3):1013–1022. https://doi.org/10.3390/brainsci3031013
doi: 10.3390/brainsci3031013
pubmed: 24961518
pmcid: 4061878
Ferreira D, Westman E, Eyjolfsdottir H, Almqvist P, Lind G, Linderoth B, Seiger A, Blennow K, Karami A, Darreh-Shori T, Wiberg M, Simmons A, Wahlund LO, Wahlberg L, Eriksdotter M (2015) Brain changes in Alzheimer’s disease patients with implanted encapsulated cells releasing nerve growth factor. J Alzheimers Dis 43(3):1059–1072. https://doi.org/10.3233/JAD-141068
doi: 10.3233/JAD-141068
pubmed: 25147108
Fine A, Dunnett SB, Bjorklund A, Iversen SD (1985) Cholinergic ventral forebrain grafts into the neocortex improve passive avoidance memory in a rat model of Alzheimer disease. Proc Natl Acad Sci U S A 82(15):5227–5230. https://doi.org/10.1073/pnas.82.15.5227
doi: 10.1073/pnas.82.15.5227
pubmed: 3860857
pmcid: 390533
Fischer W, Wictorin K, Bjorklund A, Williams LR, Varon S, Gage FH (1987) Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329(6134):65–68. https://doi.org/10.1038/329065a0
doi: 10.1038/329065a0
pubmed: 3627243
Fjord-Larsen L, Kusk P, Emerich DF, Thanos C, Torp M, Bintz B, Tornoe J, Johnsen AH, Wahlberg LU (2012) Increased encapsulated cell biodelivery of nerve growth factor in the brain by transposon-mediated gene transfer. Gene Ther 19(10):1010–1017. https://doi.org/10.1038/gt.2011.178
doi: 10.1038/gt.2011.178
pubmed: 22113314
Friden PM, Walus LR, Watson P, Doctrow SR, Kozarich JW, Backman C, Bergman H, Hoffer B, Bloom F, Granholm AC (1993) Blood-brain barrier penetration and in vivo activity of an NGF conjugate. Science 259(5093):373–377. https://doi.org/10.1126/science.8420006
doi: 10.1126/science.8420006
pubmed: 8420006
Ganger S, Schindowski K (2018) Tailoring formulations for intranasal nose-to-brain delivery: a review on architecture, physico-chemical characteristics and mucociliary clearance of the nasal olfactory mucosa. Pharmaceutics 10(3):116. https://doi.org/10.3390/pharmaceutics10030116
doi: 10.3390/pharmaceutics10030116
pmcid: 6161189
Gomez D, Martinez JA, Hanson LR, Frey WH 2nd, Toth CC (2012) Intranasal treatment of neurodegenerative diseases and stroke. Front Biosci (Schol Ed) 4:74–89. https://doi.org/10.2741/252
doi: 10.2741/252
Goswami R, Subramanian G, Silayeva L, Newkirk I, Doctor D, Chawla K, Chattopadhyay S, Chandra D, Chilukuri N, Betapudi V (2019) Gene therapy leaves a vicious cycle. Front Oncol 9:297. https://doi.org/10.3389/fonc.2019.00297
doi: 10.3389/fonc.2019.00297
pubmed: 31069169
pmcid: 6491712
Granholm AC, Backman C, Bloom F, Ebendal T, Gerhardt GA, Hoffer B, Mackerlova L, Olson L, Soderstrom S, Walus LR et al (1994) NGF and anti-transferrin receptor antibody conjugate: short and long-term effects on survival of cholinergic neurons in intraocular septal transplants. J Pharmacol Exp Ther 268(1):448–459
pubmed: 8301587
Griffin N, Faulkner S, Jobling P, Hondermarck H (2018) Targeting neurotrophin signaling in cancer: the renaissance. Pharmacol Res 135:12–17. https://doi.org/10.1016/j.phrs.2018.07.019
doi: 10.1016/j.phrs.2018.07.019
pubmed: 30031169
Grill RJ, Blesch A, Tuszynski MH (1997) Robust growth of chronically injured spinal cord axons induced by grafts of genetically modified NGF-secreting cells. Exp Neurol 148(2):444–452. https://doi.org/10.1006/exnr.1997.6704
doi: 10.1006/exnr.1997.6704
pubmed: 9417824
Gu H, Song C, Long D, Mei L, Sun H (2007) Controlled release of recombinant human nerve growth factor (rhNGF) from poly[(lactic acid)-co-(glycolic acid)] microspheres for the treatment of neurodegenerative disorders. Polym Int 56(10):1272–1280. https://doi.org/10.1002/pi.2272
doi: 10.1002/pi.2272
Gu H, Long D, Song C, Li X (2009) Recombinant human NGF-loaded microspheres promote survival of basal forebrain cholinergic neurons and improve memory impairments of spatial learning in the rat model of Alzheimer’s disease with fimbria-fornix lesion. Neurosci Lett 453(3):204–209. https://doi.org/10.1016/j.neulet.2009.02.027
doi: 10.1016/j.neulet.2009.02.027
pubmed: 19429036
Gu G, Zhang W, Li M, Ni J, Wang P (2015) Transplantation of NSC-derived cholinergic neuron-like cells improves cognitive function in APP/PS1 transgenic mice. Neuroscience 291:81–92. https://doi.org/10.1016/j.neuroscience.2015.01.073
doi: 10.1016/j.neuroscience.2015.01.073
pubmed: 25681520
Guo L, Davis BM, Ravindran N, Galvao J, Kapoor N, Haamedi N, Shamsher E, Luong V, Fico E, Cordeiro MF (2020) Topical recombinant human Nerve growth factor (rh-NGF) is neuroprotective to retinal ganglion cells by targeting secondary degeneration. Sci Rep 10(1):3375. https://doi.org/10.1038/s41598-020-60427-2
doi: 10.1038/s41598-020-60427-2
pubmed: 32099056
pmcid: 7042238
Hadlock TA, Sheahan T, Cheney ML, Vacanti JP, Sundback CA (2003) Biologic activity of nerve growth factor slowly released from microspheres. J Reconstr Microsurg 19(3):179–184.; Discussion 185–176. https://doi.org/10.1055/s-2003-39831
doi: 10.1055/s-2003-39831
pubmed: 12806579
Hagg T, Manthorpe M, Vahlsing HL, Varon S (1988) Delayed treatment with nerve growth factor reverses the apparent loss of cholinergic neurons after acute brain damage. Exp Neurol 101(2):303–312. https://doi.org/10.1016/0014-4886(88)90013-1
doi: 10.1016/0014-4886(88)90013-1
pubmed: 3396647
Hampel H, Mesulam MM, Cuello AC, Farlow MR, Giacobini E, Grossberg GT, Khachaturian AS, Vergallo A, Cavedo E, Snyder PJ, Khachaturian ZS (2018) The cholinergic system in the pathophysiology and treatment of Alzheimer’s disease. Brain 141(7):1917–1933. https://doi.org/10.1093/brain/awy132
doi: 10.1093/brain/awy132
pubmed: 29850777
pmcid: 6022632
Hanzel CE, Iulita MF, Eyjolfsdottir H, Hjorth E, Schultzberg M, Eriksdotter M, Cuello AC (2014) Analysis of matrix metallo-proteases and the plasminogen system in mild cognitive impairment and Alzheimer’s disease cerebrospinal fluid. J Alzheimers Dis 40(3):667–678. https://doi.org/10.3233/JAD-132282
doi: 10.3233/JAD-132282
pubmed: 24531161
Hao J, Ebendal T, Xu X, Wiesenfeld-Hallin Z, Eriksdotter Jonhagen M (2000) Intracerebroventricular infusion of nerve growth factor induces pain-like response in rats. Neurosci Lett 286(3):208–212. https://doi.org/10.1016/s0304-3940(00)01107-1
doi: 10.1016/s0304-3940(00)01107-1
pubmed: 10832021
Hayakawa Y, Sakitani K, Konishi M, Asfaha S, Niikura R, Tomita H, Renz BW, Tailor Y, Macchini M, Middelhoff M, Jiang Z, Tanaka T, Dubeykovskaya ZA, Kim W, Chen X, Urbanska AM, Nagar K, Westphalen CB, Quante M, Lin CS, Gershon MD, Hara A, Zhao CM, Chen D, Worthley DL, Koike K, Wang TC (2017) Nerve growth factor promotes gastric tumorigenesis through aberrant cholinergic signaling. Cancer Cell 31(1):21–34. https://doi.org/10.1016/j.ccell.2016.11.005
doi: 10.1016/j.ccell.2016.11.005
pubmed: 27989802
Hayashi Y, Lin HT, Lee CC, Tsai KJ (2020) Effects of neural stem cell transplantation in Alzheimer’s disease models. J Biomed Sci 27(1):29. https://doi.org/10.1186/s12929-020-0622-x
doi: 10.1186/s12929-020-0622-x
pubmed: 31987051
pmcid: 6986162
Hefti F (1986) Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J Neurosci 6(8):2155–2162
doi: 10.1523/JNEUROSCI.06-08-02155.1986
Hefti F, Schneider LS (1989) Rationale for the planned clinical trials with nerve growth factor in Alzheimer’s disease. Psychiatr Dev 7(4):297–315
pubmed: 2487898
Hoffman D, Wahlberg L, Aebischer P (1990) NGF released from a polymer matrix prevents loss of ChAT expression in basal forebrain neurons following a fimbria-fornix lesion. Exp Neurol 110(1):39–44. https://doi.org/10.1016/0014-4886(90)90049-x
doi: 10.1016/0014-4886(90)90049-x
pubmed: 2209780
Hohsfield LA, Ehrlich D, Humpel C (2014) Intravenous infusion of nerve growth factor-secreting monocytes supports the survival of cholinergic neurons in the nucleus basalis of Meynert in hypercholesterolemia Brown-Norway rats. J Neurosci Res 92(3):298–306. https://doi.org/10.1002/jnr.23309
doi: 10.1002/jnr.23309
pubmed: 24323796
Hsu RS, Chen PY, Fang JH, Chen YY, Chang CW, Lu YJ, Hu SH (2019) Adaptable microporous hydrogels of propagating NGF-gradient by injectable building blocks for accelerated axonal outgrowth. Adv Sci (Weinh) 6(16):1900520. https://doi.org/10.1002/advs.201900520
doi: 10.1002/advs.201900520
pmcid: 6702647
Hu X, Li R, Wu Y, Li Y, Zhong X, Zhang G, Kang Y, Liu S, Xie L, Ye J, Xiao J (2020) Thermosensitive heparin-poloxamer hydrogel encapsulated bFGF and NGF to treat spinal cord injury. J Cell Mol Med 24(14):8166–8178. https://doi.org/10.1111/jcmm.15478
doi: 10.1111/jcmm.15478
pubmed: 32515141
pmcid: 7348165
Isaacson LG, Saffran BN, Crutcher KA (1990) Intracerebral NGF infusion induces hyperinnervation of cerebral blood vessels. Neurobiol Aging 11(1):51–55. https://doi.org/10.1016/0197-4580(90)90062-5
doi: 10.1016/0197-4580(90)90062-5
pubmed: 2183082
Isaacson LG, Saffran BN, Crutcher KA (1992) Nerve growth factor-induced sprouting of mature, uninjured sympathetic axons. J Comp Neurol 326(3):327–336. https://doi.org/10.1002/cne.903260302
doi: 10.1002/cne.903260302
pubmed: 1469116
Jonhagen ME (2000) Nerve growth factor treatment in dementia. Alzheimer Dis Assoc Disord 14(Suppl 1):S31–S38. https://doi.org/10.1097/00002093-200000001-00006
doi: 10.1097/00002093-200000001-00006
pubmed: 10850728
Kamei N, Tanaka N, Oishi Y, Hamasaki T, Nakanishi K, Sakai N, Ochi M (2007) BDNF, NT-3, and NGF released from transplanted neural progenitor cells promote corticospinal axon growth in organotypic cocultures. Spine (Phila Pa 1976) 32(12):1272–1278. https://doi.org/10.1097/BRS.0b013e318059afab
doi: 10.1097/BRS.0b013e318059afab
Karami A, Eyjolfsdottir H, Vijayaraghavan S, Lind G, Almqvist P, Kadir A, Linderoth B, Andreasen N, Blennow K, Wall A, Westman E, Ferreira D, Kristoffersen Wiberg M, Wahlund LO, Seiger A, Nordberg A, Wahlberg L, Darreh-Shori T, Eriksdotter M (2015) Changes in CSF cholinergic biomarkers in response to cell therapy with NGF in patients with Alzheimer’s disease. Alzheimers Dement 11(11):1316–1328. https://doi.org/10.1016/j.jalz.2014.11.008
doi: 10.1016/j.jalz.2014.11.008
pubmed: 25676388
Killick-Cole C, Woolley M, Johnson D, Lewis O, Moore P, Fletcher J, Skinner P, Bienemann A, Gill S (2019) SCIDOT-35. A novel model for the optimization of drug-device combinations for the treatment of brain tumors. Neuro-Oncology 21(Supplement_6):vi279–vi279. https://doi.org/10.1093/neuonc/noz175.1171
doi: 10.1093/neuonc/noz175.1171
pmcid: 6846196
Kim HJ, Lee JH, Kim SH (2010) Therapeutic effects of human mesenchymal stem cells on traumatic brain injury in rats: secretion of neurotrophic factors and inhibition of apoptosis. J Neurotrauma 27(1):131–138. https://doi.org/10.1089/neu.2008-0818
doi: 10.1089/neu.2008-0818
pubmed: 19508155
Kim KY, Suh YH, Chang KA (2020) Therapeutic effects of human amniotic epithelial stem cells in a transgenic mouse model of Alzheimer’s disease. Int J Mol Sci 21(7). https://doi.org/10.3390/ijms21072658
Koliatsos VE, Nauta HJ, Clatterbuck RE, Holtzman DM, Mobley WC, Price DL (1990) Mouse nerve growth factor prevents degeneration of axotomized basal forebrain cholinergic neurons in the monkey. J Neurosci 10(12):3801–3813
doi: 10.1523/JNEUROSCI.10-12-03801.1990
Koliatsos VE, Applegate MD, Knusel B, Junard EO, Burton LE, Mobley WC, Hefti FF, Price DL (1991a) Recombinant human nerve growth factor prevents retrograde degeneration of axotomized basal forebrain cholinergic neurons in the rat. Exp Neurol 112(2):161–173. https://doi.org/10.1016/0014-4886(91)90066-l
doi: 10.1016/0014-4886(91)90066-l
pubmed: 2037030
Koliatsos VE, Clatterbuck RE, Nauta HJ, Knusel B, Burton LE, Hefti FF, Mobley WC, Price DL (1991b) Human nerve growth factor prevents degeneration of basal forebrain cholinergic neurons in primates. Ann Neurol 30(6):831–840. https://doi.org/10.1002/ana.410300613
doi: 10.1002/ana.410300613
pubmed: 1789695
Kordower JH, Winn SR, Liu YT, Mufson EJ, Sladek JR Jr, Hammang JP, Baetge EE, Emerich DF (1994) The aged monkey basal forebrain: rescue and sprouting of axotomized basal forebrain neurons after grafts of encapsulated cells secreting human nerve growth factor. Proc Natl Acad Sci U S A 91(23):10898–10902. https://doi.org/10.1073/pnas.91.23.10898
doi: 10.1073/pnas.91.23.10898
pubmed: 7971980
pmcid: 45133
Kurakhmaeva KB, Djindjikhashvili IA, Petrov VE, Balabanyan VU, Voronina TA, Trofimov SS, Kreuter J, Gelperina S, Begley D, Alyautdin RN (2009) Brain targeting of nerve growth factor using poly(butyl cyanoacrylate) nanoparticles. J Drug Target 17(8):564–574. https://doi.org/10.1080/10611860903112842
doi: 10.1080/10611860903112842
pubmed: 19694610
Kwak YD, Brannen CL, Qu T, Kim HM, Dong X, Soba P, Majumdar A, Kaplan A, Beyreuther K, Sugaya K (2006) Amyloid precursor protein regulates differentiation of human neural stem cells. Stem Cells Dev 15(3):381–389. https://doi.org/10.1089/scd.2006.15.381
doi: 10.1089/scd.2006.15.381
pubmed: 16846375
Lambiase A, Rama P, Bonini S, Caprioglio G, Aloe L (1998) Topical treatment with nerve growth factor for corneal neurotrophic ulcers. N Engl J Med 338(17):1174–1180. https://doi.org/10.1056/NEJM199804233381702
doi: 10.1056/NEJM199804233381702
pubmed: 9554857
Lambiase A, Tirassa P, Micera A, Aloe L, Bonini S (2005) Pharmacokinetics of conjunctivally applied nerve growth factor in the retina and optic nerve of adult rats. Invest Ophthalmol Vis Sci 46(10):3800–3806. https://doi.org/10.1167/iovs.05-0301
doi: 10.1167/iovs.05-0301
pubmed: 16186366
Lambiase A, Pagani L, Di Fausto V, Sposato V, Coassin M, Bonini S, Aloe L (2007a) Nerve growth factor eye drop administrated on the ocular surface of rodents affects the nucleus basalis and septum: biochemical and structural evidence. Brain Res 1127(1):45–51. https://doi.org/10.1016/j.brainres.2006.09.102
doi: 10.1016/j.brainres.2006.09.102
pubmed: 17113055
Lambiase A, Coassin M, Sposato V, Micera A, Sacchetti M, Bonini S, Aloe L (2007b) NGF topical application in patients with corneal ulcer does not generate circulating NGF antibodies. Pharmacol Res 56(1):65–69. https://doi.org/10.1016/j.phrs.2007.03.007
doi: 10.1016/j.phrs.2007.03.007
pubmed: 17512750
Lambiase A, Mantelli F, Sacchetti M, Rossi S, Aloe L, Bonini S (2011) Clinical applications of NGF in ocular diseases. Arch Ital Biol 149(2):283–292. https://doi.org/10.4449/aib.v149i2.1363
doi: 10.4449/aib.v149i2.1363
pubmed: 21702001
Lammertink BH, Bos C, Deckers R, Storm G, Moonen CT, Escoffre JM (2015) Sonochemotherapy: from bench to bedside. Front Pharmacol 6:138. https://doi.org/10.3389/fphar.2015.00138
doi: 10.3389/fphar.2015.00138
pubmed: 26217226
pmcid: 4498442
Lee AC, Yu VM, Lowe JB 3rd, Brenner MJ, Hunter DA, Mackinnon SE, Sakiyama-Elbert SE (2003) Controlled release of nerve growth factor enhances sciatic nerve regeneration. Exp Neurol 184(1):295–303. https://doi.org/10.1016/s0014-4886(03)00258-9
doi: 10.1016/s0014-4886(03)00258-9
pubmed: 14637100
Lee HJ, Lee JK, Lee H, Carter JE, Chang JW, Oh W, Yang YS, Suh JG, Lee BH, Jin HK, Bae JS (2012a) Human umbilical cord blood-derived mesenchymal stem cells improve neuropathology and cognitive impairment in an Alzheimer’s disease mouse model through modulation of neuroinflammation. Neurobiol Aging 33(3):588–602. https://doi.org/10.1016/j.neurobiolaging.2010.03.024
doi: 10.1016/j.neurobiolaging.2010.03.024
pubmed: 20471717
Lee HJ, Lim IJ, Park SW, Kim YB, Ko Y, Kim SU (2012b) Human neural stem cells genetically modified to express human nerve growth factor (NGF) gene restore cognition in the mouse with ibotenic acid-induced cognitive dysfunction. Cell Transplant 21(11):2487–2496. https://doi.org/10.3727/096368912X638964
doi: 10.3727/096368912X638964
pubmed: 22526467
LeSauteur L, Wei L, Gibbs BF, Saragovi HU (1995) Small peptide mimics of nerve growth factor bind TrkA receptors and affect biological responses. J Biol Chem 270(12):6564–6569. https://doi.org/10.1074/jbc.270.12.6564
doi: 10.1074/jbc.270.12.6564
pubmed: 7896793
Li XB, Liao GS, Shu YY, Tang SX (2000) Brain delivery of biotinylated NGF bounded to an avidin-transferrin conjugate. J Nat Toxins 9(1):73–83
pubmed: 10701183
Li W, Huang A, Zhong Y, Huang L, Yang J, Zhou C, Zhou L, Zhang Y, Fu G (2020) Laminin-modified gellan gum hydrogels loaded with the nerve growth factor to enhance the proliferation and differentiation of neuronal stem cells. RSC Adv 10(29):17114–17122. https://doi.org/10.1039/D0RA01723J
doi: 10.1039/D0RA01723J
Liao GS, Li XB, Zhang CY, Shu YY, Tang SX (2001) Pharmacological actions of nerve growth factor-transferrin conjugate on the central nervous system. J Nat Toxins 10(4):291–297
pubmed: 11695818
Lim F, Sun AM (1980) Microencapsulated islets as bioartificial endocrine pancreas. Science 210(4472):908–910. https://doi.org/10.1126/science.6776628
doi: 10.1126/science.6776628
pubmed: 6776628
Lipsman N, Meng Y, Bethune AJ, Huang Y, Lam B, Masellis M, Herrmann N, Heyn C, Aubert I, Boutet A, Smith GS, Hynynen K, Black SE (2018) Blood-brain barrier opening in Alzheimer’s disease using MR-guided focused ultrasound. Nat Commun 9(1):2336. https://doi.org/10.1038/s41467-018-04529-6
doi: 10.1038/s41467-018-04529-6
pubmed: 30046032
pmcid: 6060168
Liu H, Wen W, Hu M, Bi W, Chen L, Liu S, Chen P, Tan X (2013) Chitosan conduits combined with nerve growth factor microspheres repair facial nerve defects. Neural Regen Res 8(33):3139–3147. https://doi.org/10.3969/j.issn.1673-5374.2013.33.008
doi: 10.3969/j.issn.1673-5374.2013.33.008
pubmed: 25206635
pmcid: 4158708
Liu X, Li W, Fu X, Xu Y (2017) The immunogenicity and immune tolerance of pluripotent stem cell derivatives. Front Immunol 8:645. https://doi.org/10.3389/fimmu.2017.00645
doi: 10.3389/fimmu.2017.00645
pubmed: 28626459
pmcid: 5454078
Liu PP, Xie Y, Meng XY, Kang JS (2019) History and progress of hypotheses and clinical trials for Alzheimer’s disease. Signal Transduct Target Ther 4:29. https://doi.org/10.1038/s41392-019-0063-8
doi: 10.1038/s41392-019-0063-8
pubmed: 31637009
pmcid: 6799833
Longo FM, Massa SM (2013) Small-molecule modulation of neurotrophin receptors: a strategy for the treatment of neurological disease. Nat Rev Drug Discov 12(7):507–525. https://doi.org/10.1038/nrd4024
doi: 10.1038/nrd4024
pubmed: 23977697
Longo FM, Manthorpe M, Xie YM, Varon S (1997) Synthetic NGF peptide derivatives prevent neuronal death via a p75 receptor-dependent mechanism. J Neurosci Res 48(1):1–17. https://doi.org/10.1002/(sici)1097-4547(19970401)48:1<1::aid-jnr1>3.0.co;2-k
doi: 10.1002/(sici)1097-4547(19970401)48:1<1::aid-jnr1>3.0.co;2-k
pubmed: 9086177
Losurdo M, Pedrazzoli M, D’Agostino C, Elia CA, Massenzio F, Lonati E, Mauri M, Rizzi L, Molteni L, Bresciani E, Dander E, D’Amico G, Bulbarelli A, Torsello A, Matteoli M, Buffelli M, Coco S (2020) Intranasal delivery of mesenchymal stem cell-derived extracellular vesicles exerts immunomodulatory and neuroprotective effects in a 3xTg model of Alzheimer’s disease. Stem Cells Transl Med 9(9):1068–1084. https://doi.org/10.1002/sctm.19-0327
doi: 10.1002/sctm.19-0327
pubmed: 32496649
pmcid: 7445021
Machado A, Ferreira D, Grothe MJ, Eyjolfsdottir H, Almqvist PM, Cavallin L, Lind G, Linderoth B, Seiger A, Teipel S, Wahlberg LU, Wahlund LO, Westman E, Eriksdotter M, Alzheimer’s Disease Neuroimaging Initiative (2020) The cholinergic system in subtypes of Alzheimer’s disease: an in vivo longitudinal MRI study. Alzheimers Res Ther 12(1):51. https://doi.org/10.1186/s13195-020-00620-7
doi: 10.1186/s13195-020-00620-7
pubmed: 32375872
pmcid: 7203806
Mahoney MJ, Saltzman WM (1999) Millimeter-scale positioning of a nerve-growth-factor source and biological activity in the brain. Proc Natl Acad Sci U S A 96(8):4536–4539. https://doi.org/10.1073/pnas.96.8.4536
doi: 10.1073/pnas.96.8.4536
pubmed: 10200297
pmcid: 16367
Mandal A, Pal D, Agrahari V, Trinh HM, Joseph M, Mitra AK (2018) Ocular delivery of proteins and peptides: challenges and novel formulation approaches. Adv Drug Deliv Rev 126:67–95. https://doi.org/10.1016/j.addr.2018.01.008
doi: 10.1016/j.addr.2018.01.008
pubmed: 29339145
pmcid: 5995646
Marcus M, Skaat H, Alon N, Margel S, Shefi O (2015) NGF-conjugated iron oxide nanoparticles promote differentiation and outgrowth of PC12 cells. Nanoscale 7(3):1058–1066. https://doi.org/10.1039/c4nr05193a
doi: 10.1039/c4nr05193a
pubmed: 25473934
Martinez-Serrano A, Bjorklund A (1998) Ex vivo nerve growth factor gene transfer to the basal forebrain in presymptomatic middle-aged rats prevents the development of cholinergic neuron atrophy and cognitive impairment during aging. Proc Natl Acad Sci U S A 95(4):1858–1863. https://doi.org/10.1073/pnas.95.4.1858
doi: 10.1073/pnas.95.4.1858
pubmed: 9465107
pmcid: 19203
Martinez-Serrano A, Fischer W, Soderstrom S, Ebendal T, Bjorklund A (1996) Long-term functional recovery from age-induced spatial memory impairments by nerve growth factor gene transfer to the rat basal forebrain. Proc Natl Acad Sci U S A 93(13):6355–6360. https://doi.org/10.1073/pnas.93.13.6355
doi: 10.1073/pnas.93.13.6355
pubmed: 8692819
pmcid: 39026
McGinley LM, Kashlan ON, Bruno ES, Chen KS, Hayes JM, Kashlan SR, Raykin J, Johe K, Murphy GG, Feldman EL (2018) Human neural stem cell transplantation improves cognition in a murine model of Alzheimer’s disease. Sci Rep 8(1):14776. https://doi.org/10.1038/s41598-018-33017-6
doi: 10.1038/s41598-018-33017-6
pubmed: 30283042
pmcid: 6170460
Menei P, Pean JM, Nerriere-Daguin V, Jollivet C, Brachet P, Benoit JP (2000) Intracerebral implantation of NGF-releasing biodegradable microspheres protects striatum against excitotoxic damage. Exp Neurol 161(1):259–272. https://doi.org/10.1006/exnr.1999.7253
doi: 10.1006/exnr.1999.7253
pubmed: 10683292
Minde J, Toolanen G, Andersson T, Nennesmo I, Remahl IN, Svensson O, Solders G (2004) Familial insensitivity to pain (HSAN V) and a mutation in the NGFB gene. A neurophysiological and pathological study. Muscle Nerve 30(6):752–760. https://doi.org/10.1002/mus.20172
doi: 10.1002/mus.20172
pubmed: 15468048
Mitra S, Behbahani H, Eriksdotter M (2019) Innovative therapy for Alzheimer’s disease-with focus on biodelivery of NGF. Front Neurosci 13:38. https://doi.org/10.3389/fnins.2019.00038
doi: 10.3389/fnins.2019.00038
pubmed: 30804738
pmcid: 6370742
Montero CN, Hefti F (1988) Rescue of lesioned septal cholinergic neurons by nerve growth factor: specificity and requirement for chronic treatment. J Neurosci 8(8):2986–2999
doi: 10.1523/JNEUROSCI.08-08-02986.1988
Montero CN, Hefti F (1989) Intraventricular nerve growth factor administration prevents lesion-induced loss of septal cholinergic neurons in aging rats. Neurobiol Aging 10(6):739–743. https://doi.org/10.1016/0197-4580(89)90011-0
doi: 10.1016/0197-4580(89)90011-0
pubmed: 2628784
Mufson EJ, Conner JM, Kordower JH (1995) Nerve growth factor in Alzheimer’s disease: defective retrograde transport to nucleus basalis. Neuroreport 6(7):1063–1066. https://doi.org/10.1097/00001756-199505090-00028
doi: 10.1097/00001756-199505090-00028
pubmed: 7632896
Nagahara AH, Bernot T, Moseanko R, Brignolo L, Blesch A, Conner JM, Ramirez A, Gasmi M, Tuszynski MH (2009) Long-term reversal of cholinergic neuronal decline in aged non-human primates by lentiviral NGF gene delivery. Exp Neurol 215(1):153–159. https://doi.org/10.1016/j.expneurol.2008.10.004
doi: 10.1016/j.expneurol.2008.10.004
pubmed: 19013154
Nguyen TV, Shen L, Vander Griend L, Quach LN, Belichenko NP, Saw N, Yang T, Shamloo M, Wyss-Coray T, Massa SM, Longo FM (2014) Small molecule p75NTR ligands reduce pathological phosphorylation and misfolding of tau, inflammatory changes, cholinergic degeneration, and cognitive deficits in AbetaPP(L/S) transgenic mice. J Alzheimers Dis 42(2):459–483. https://doi.org/10.3233/JAD-140036
doi: 10.3233/JAD-140036
pubmed: 24898660
pmcid: 4278429
Oh B, Swaminathan V, Malkovskiy A, Santhanam S, McConnell K, George PM (2020) Single-cell encapsulation via click-chemistry alters production of paracrine factors from neural progenitor cells. Adv Sci (Weinh) 7(8):1902573. https://doi.org/10.1002/advs.201902573
doi: 10.1002/advs.201902573
Olson L (1993) NGF and the treatment of Alzheimer’s disease. Exp Neurol 124(1):5–15. https://doi.org/10.1006/exnr.1993.1167
doi: 10.1006/exnr.1993.1167
pubmed: 8282080
Olson L, Nordberg A, von Holst H, Backman L, Ebendal T, Alafuzoff I, Amberla K, Hartvig P, Herlitz A, Lilja A et al (1992) Nerve growth factor affects 11C-nicotine binding, blood flow, EEG, and verbal episodic memory in an Alzheimer patient (case report). J Neural Transm Park Dis Dement Sect 4(1):79–95. https://doi.org/10.1007/BF02257624
doi: 10.1007/BF02257624
pubmed: 1540306
Orive G, Santos E, Poncelet D, Hernandez RM, Pedraz JL, Wahlberg LU, De Vos P, Emerich D (2015) Cell encapsulation: technical and clinical advances. Trends Pharmacol Sci 36(8):537–546. https://doi.org/10.1016/j.tips.2015.05.003
doi: 10.1016/j.tips.2015.05.003
pubmed: 26067102
Orive G, Santos-Vizcaino E, Pedraz JL, Hernandez RM, Vela Ramirez JE, Dolatshahi-Pirouz A, Khademhosseini A, Peppas NA, Emerich DF (2019) 3D cell-laden polymers to release bioactive products in the eye. Prog Retin Eye Res 68:67–82. https://doi.org/10.1016/j.preteyeres.2018.10.002
doi: 10.1016/j.preteyeres.2018.10.002
pubmed: 30342088
Pakzaban P, Geller AI, Isacson O (1994) Effect of exogenous nerve growth factor on neurotoxicity of and neuronal gene delivery by a herpes simplex amplicon vector in the rat brain. Hum Gene Ther 5(8):987–995. https://doi.org/10.1089/hum.1994.5.8-987
doi: 10.1089/hum.1994.5.8-987
pubmed: 7948148
Paradisi M, Alviano F, Pirondi S, Lanzoni G, Fernandez M, Lizzo G, Giardino L, Giuliani A, Costa R, Marchionni C, Bonsi L, Calza L (2014) Human mesenchymal stem cells produce bioactive neurotrophic factors: source, individual variability and differentiation issues. Int J Immunopathol Pharmacol 27(3):391–402. https://doi.org/10.1177/039463201402700309
doi: 10.1177/039463201402700309
pubmed: 25280030
Pardridge WM (2019) Blood-brain barrier and delivery of protein and gene therapeutics to brain. Front Aging Neurosci 11:373. https://doi.org/10.3389/fnagi.2019.00373
doi: 10.3389/fnagi.2019.00373
pubmed: 31998120
Park D, Yang YH, Bae DK, Lee SH, Yang G, Kyung J, Kim D, Choi EK, Lee SW, Kim GH, Hong JT, Choi KC, Lee HJ, Kim SU, Kim YB (2013) Improvement of cognitive function and physical activity of aging mice by human neural stem cells over-expressing choline acetyltransferase. Neurobiol Aging 34(11):2639–2646. https://doi.org/10.1016/j.neurobiolaging.2013.04.026
doi: 10.1016/j.neurobiolaging.2013.04.026
pubmed: 23731954
Pentz R, Iulita MF, Ducatenzeiler A, Bennett DA, Cuello AC (2020) The human brain NGF metabolic pathway is impaired in the pre-clinical and clinical continuum of Alzheimers disease. Mol Psychiatry. https://doi.org/10.1038/s41380-020-0797-2
Piotrowicz A, Shoichet MS (2006) Nerve guidance channels as drug delivery vehicles. Biomaterials 27(9):2018–2027. https://doi.org/10.1016/j.biomaterials.2005.09.042
doi: 10.1016/j.biomaterials.2005.09.042
pubmed: 16239029
Polak JM, Mantalaris S (2008) Stem cells bioprocessing: an important milestone to move regenerative medicine research into the clinical arena. Pediatr Res 63(5):461–466. https://doi.org/10.1203/10.1203/PDR.0b013e31816a8c1c
doi: 10.1203/10.1203/PDR.0b013e31816a8c1c
pubmed: 18427288
Powell EM, Sobarzo MR, Saltzman WM (1990) Controlled release of nerve growth factor from a polymeric implant. Brain Res 515(1–2):309–311. https://doi.org/10.1016/0006-8993(90)90612-f
doi: 10.1016/0006-8993(90)90612-f
pubmed: 2357568
Pramanik S, Sulistio YA, Heese K (2017) Neurotrophin signaling and stem cells-implications for neurodegenerative diseases and stem cell therapy. Mol Neurobiol 54(9):7401–7459. https://doi.org/10.1007/s12035-016-0214-7
doi: 10.1007/s12035-016-0214-7
pubmed: 27815842
Qu M, Jiang X, Zhou X, Wang C, Wu Q, Ren L, Zhu J, Zhu S, Tebon P, Sun W, Khademhosseini A (2020) Stimuli-responsive delivery of growth factors for tissue engineering. Adv Healthc Mater 9(7):e1901714. https://doi.org/10.1002/adhm.201901714
doi: 10.1002/adhm.201901714
pubmed: 32125786
pmcid: 7189772
Rafii MS, Baumann TL, Bakay RA, Ostrove JM, Siffert J, Fleisher AS, Herzog CD, Barba D, Pay M, Salmon DP, Chu Y, Kordower JH, Bishop K, Keator D, Potkin S, Bartus RT (2014) A phase1 study of stereotactic gene delivery of AAV2-NGF for Alzheimer’s disease. Alzheimers Dement 10(5):571–581. https://doi.org/10.1016/j.jalz.2013.09.004
doi: 10.1016/j.jalz.2013.09.004
pubmed: 24411134
Rafii MS, Tuszynski MH, Thomas RG, Barba D, Brewer JB, Rissman RA, Siffert J, Aisen PS, Team ANS (2018) Adeno-associated viral vector (serotype 2)-nerve growth factor for patients with Alzheimer disease: a randomized clinical trial. JAMA Neurol 75(7):834–841. https://doi.org/10.1001/jamaneurol.2018.0233
doi: 10.1001/jamaneurol.2018.0233
pubmed: 29582053
pmcid: 5885277
Razavi S, Seyedebrahimi R, Jahromi M (2019) Biodelivery of nerve growth factor and gold nanoparticles encapsulated in chitosan nanoparticles for schwann-like cells differentiation of human adipose-derived stem cells. Biochem Biophys Res Commun 513(3):681–687. https://doi.org/10.1016/j.bbrc.2019.03.189
doi: 10.1016/j.bbrc.2019.03.189
pubmed: 30982578
Rezai AR, Ranjan M, D’Haese PF, Haut MW, Carpenter J, Najib U, Mehta RI, Chazen JL, Zibly Z, Yates JR, Hodder SL, Kaplitt M (2020) Noninvasive hippocampal blood-brain barrier opening in Alzheimer’s disease with focused ultrasound. Proc Natl Acad Sci U S A 117(17):9180–9182. https://doi.org/10.1073/pnas.2002571117
doi: 10.1073/pnas.2002571117
pubmed: 32284421
pmcid: 7196825
Rocco ML, Soligo M, Manni L, Aloe L (2018) Nerve growth factor: early studies and recent clinical trials. Curr Neuropharmacol 16(10):1455–1465. https://doi.org/10.2174/1570159X16666180412092859
doi: 10.2174/1570159X16666180412092859
pubmed: 29651949
pmcid: 6295934
Rodrigues BDS, Kanekiyo T, Singh J (2020) Nerve growth factor gene delivery across the blood-brain barrier to reduce beta amyloid accumulation in AD mice. Mol Pharm 17(6):2054–2063. https://doi.org/10.1021/acs.molpharmaceut.0c00218
doi: 10.1021/acs.molpharmaceut.0c00218
pubmed: 32315185
Ruozi B, Belletti D, Bondioli L, De Vita A, Forni F, Vandelli MA, Tosi G (2012) Neurotrophic factors and neurodegenerative diseases: a delivery issue. Int Rev Neurobiol 102:207–247. https://doi.org/10.1016/B978-0-12-386986-9.00009-0
doi: 10.1016/B978-0-12-386986-9.00009-0
pubmed: 22748832
Saffran BN, Woo JE, Mobley WC, Crutcher KA (1989) Intraventricular NGF infusion in the mature rat brain enhances sympathetic innervation of cerebrovascular targets but fails to elicit sympathetic ingrowth. Brain Res 492(1-2):245–254. https://doi.org/10.1016/0006-8993(89)90907-4
doi: 10.1016/0006-8993(89)90907-4
pubmed: 2752299
Sakiyama-Elbert SE, Hubbell JA (2000) Controlled release of nerve growth factor from a heparin-containing fibrin-based cell ingrowth matrix. J Control Release 69(1):149–158. https://doi.org/10.1016/s0168-3659(00)00296-0
doi: 10.1016/s0168-3659(00)00296-0
pubmed: 11018553
Sakiyama-Elbert SE, Panitch A, Hubbell JA (2001) Development of growth factor fusion proteins for cell-triggered drug delivery. FASEB J 15(7):1300–1302. https://doi.org/10.1096/fj.00-0564fje
doi: 10.1096/fj.00-0564fje
pubmed: 11344120
Saltzman WM, Mak MW, Mahoney MJ, Duenas ET, Cleland JL (1999) Intracranial delivery of recombinant nerve growth factor: release kinetics and protein distribution for three delivery systems. Pharm Res 16(2):232–240. https://doi.org/10.1023/a:1018824324275
doi: 10.1023/a:1018824324275
pubmed: 10100308
Samal J, Hoban DB, Naughton C, Concannon R, Dowd E, Pandit A (2015) Fibrin-based microsphere reservoirs for delivery of neurotrophic factors to the brain. Nanomedicine (Lond) 10(5):765–783. https://doi.org/10.2217/nnm.14.221
doi: 10.2217/nnm.14.221
Satizabal C, Beiser AS, Seshadri S (2016) Incidence of dementia over three decades in the Framingham heart study. N Engl J Med 375(1):93–94. https://doi.org/10.1056/NEJMc1604823
doi: 10.1056/NEJMc1604823
pubmed: 27406362
pmcid: 6374770
Scheltens P, Blennow K, Breteler MM, de Strooper B, Frisoni GB, Salloway S, Van der Flier WM (2016) Alzheimer’s disease. Lancet 388(10043):505–517. https://doi.org/10.1016/S0140-6736(15)01124-1
doi: 10.1016/S0140-6736(15)01124-1
pubmed: 26921134
Schlachetzki JC, Pizzo DP, Morrissette DA, Winkler J (2014) Intracerebroventricular administration of nerve growth factor induces gliogenesis in sensory ganglia, dorsal root, and within the dorsal root entry zone. Biomed Res Int 2014:704259. https://doi.org/10.1155/2014/704259
doi: 10.1155/2014/704259
pubmed: 24738070
pmcid: 3971563
Schneider L (2020) A resurrection of aducanumab for Alzheimer’s disease. Lancet Neurol 19(2):111–112. https://doi.org/10.1016/S1474-4422(19)30480-6
doi: 10.1016/S1474-4422(19)30480-6
pubmed: 31978357
Secnik J, Schwertner E, Alvarsson M, Hammar N, Fastbom J, Winblad B, Garcia-Ptacek S, Religa D, Eriksdotter M (2020) Cholinesterase inhibitors in patients with diabetes mellitus and dementia: an open-cohort study of ~23 000 patients from the Swedish Dementia registry. BMJ Open Diabetes Res Care 8(1). https://doi.org/10.1136/bmjdrc-2019-000833
Seiger A, Nordberg A, von Holst H, Backman L, Ebendal T, Alafuzoff I, Amberla K, Hartvig P, Herlitz A, Lilja A et al (1993) Intracranial infusion of purified nerve growth factor to an Alzheimer patient: the first attempt of a possible future treatment strategy. Behav Brain Res 57(2):255–261. https://doi.org/10.1016/0166-4328(93)90141-c
doi: 10.1016/0166-4328(93)90141-c
pubmed: 8117429
Simone MD, De Santis S, Vigneti E, Papa G, Amadori S, Aloe L (1999) Nerve growth factor: a survey of activity on immune and hematopoietic cells. Hematol Oncol 17(1):1–10. https://doi.org/10.1002/(sici)1099-1069(199903)17:1<1::aid-hon635>3.0.co;2-l
doi: 10.1002/(sici)1099-1069(199903)17:1<1::aid-hon635>3.0.co;2-l
pubmed: 10440888
Singh AP, Biswas A, Shukla A, Maiti P (2019) Targeted therapy in chronic diseases using nanomaterial-based drug delivery vehicles. Signal Transduct Target Ther 4:33. https://doi.org/10.1038/s41392-019-0068-3
doi: 10.1038/s41392-019-0068-3
pubmed: 31637012
pmcid: 6799838
Skeldal S, Sykes AM, Glerup S, Matusica D, Palstra N, Autio H, Boskovic Z, Madsen P, Castren E, Nykjaer A, Coulson EJ (2012) Mapping of the interaction site between sortilin and the p75 neurotrophin receptor reveals a regulatory role for the sortilin intracellular domain in p75 neurotrophin receptor shedding and apoptosis. J Biol Chem 287(52):43798–43809. https://doi.org/10.1074/jbc.M112.374710
doi: 10.1074/jbc.M112.374710
pubmed: 23105113
pmcid: 3527964
Sochocka M, Zwolinska K, Leszek J (2017) The infectious etiology of Alzheimer’s disease. Curr Neuropharmacol 15(7):996–1009. https://doi.org/10.2174/1570159X15666170313122937
doi: 10.2174/1570159X15666170313122937
pubmed: 28294067
pmcid: 5652018
Son AI, Opfermann JD, McCue C, Ziobro J, Abrahams JH 3rd, Jones K, Morton PD, Ishii S, Oluigbo C, Krieger A, Liu JS, Hashimoto-Torii K, Torii M (2017) An implantable micro-caged device for direct local delivery of agents. Sci Rep 7(1):17624. https://doi.org/10.1038/s41598-017-17912-y
doi: 10.1038/s41598-017-17912-y
pubmed: 29247175
pmcid: 5732160
Song B, Song J, Zhang S, Anderson MA, Ao Y, Yang CY, Deming TJ, Sofroniew MV (2012) Sustained local delivery of bioactive nerve growth factor in the central nervous system via tunable diblock copolypeptide hydrogel depots. Biomaterials 33(35):9105–9116. https://doi.org/10.1016/j.biomaterials.2012.08.060
doi: 10.1016/j.biomaterials.2012.08.060
pubmed: 22985994
Song Z, Wang Z, Shen J, Xu S, Hu Z (2017) Nerve growth factor delivery by ultrasound-mediated nanobubble destruction as a treatment for acute spinal cord injury in rats. Int J Nanomed 12:1717–1729. https://doi.org/10.2147/IJN.S128848
doi: 10.2147/IJN.S128848
Spiegel K, Agrafiotis D, Caprathe B, Davis RE, Dickerson MR, Fergus JH, Hepburn TW, Marks JS, Van Dorf M, Wieland DM et al (1995) PD 90780, a non peptide inhibitor of nerve growth factor’s binding to the P75 NGF receptor. Biochem Biophys Res Commun 217(2):488–494. https://doi.org/10.1006/bbrc.1995.2802
doi: 10.1006/bbrc.1995.2802
pubmed: 7503726
Springer JE, Collier TJ, Notter MF, Loy R, Sladek JR Jr (1988a) Central nervous system grafts of nerve growth factor-rich tissue as an alternative source of trophic support for axotomized cholinergic neurons. Prog Brain Res 78:401–407. https://doi.org/10.1016/s0079-6123(08)60311-8
doi: 10.1016/s0079-6123(08)60311-8
pubmed: 3247438
Springer JE, Collier TJ, Sladek JR Jr, Loy R (1988b) Transplantation of male mouse submaxillary gland increases survival of axotomized basal forebrain neurons. J Neurosci Res 19(3):291–296. https://doi.org/10.1002/jnr.490190303
doi: 10.1002/jnr.490190303
pubmed: 3379646
Sugaya K (2008) Mechanism of glial differentiation of neural progenitor cells by amyloid precursor protein. Neurodegener Dis 5(3-4):170–172. https://doi.org/10.1159/000113693
doi: 10.1159/000113693
pubmed: 18322381
Sydow O, Hansson P, Young D, Meyerson B, Backlund EO, Ebendal T, Farnebo LO, Freedman R, Hamberger B, Hoffer B, Seiger A, Stromberq I, Olson L (1995) Long-term beneficial effects of adrenal medullary autografts supported by nerve growth factor in Parkinson’s disease. Eur J Neurol 2(5):445–454. https://doi.org/10.1111/j.1468-1331.1995.tb00154.x
doi: 10.1111/j.1468-1331.1995.tb00154.x
pubmed: 24283725
Thomas CE, Ehrhardt A, Kay MA (2003) Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 4(5):346–358. https://doi.org/10.1038/nrg1066
doi: 10.1038/nrg1066
pubmed: 12728277
Tirassa P, Triaca V, Amendola T, Fiore M, Aloe L (2003) EGF and NGF injected into the brain of old mice enhance BDNF and ChAT in proliferating subventricular zone. J Neurosci Res 72(5):557–564. https://doi.org/10.1002/jnr.10614
doi: 10.1002/jnr.10614
pubmed: 12749020
Tirassa P, Rosso P, Iannitelli A (2018) Ocular nerve growth factor (NGF) and NGF eye drop application as paradigms to investigate NGF neuroprotective and reparative actions. Methods Mol Biol 1727:19–38. https://doi.org/10.1007/978-1-4939-7571-6_2
doi: 10.1007/978-1-4939-7571-6_2
pubmed: 29222770
Tresco PA, Winn SR, Aebischer P (1992) Polymer encapsulated neurotransmitter secreting cells. Potential treatment for Parkinson’s disease. ASAIO J 38(1):17–23
doi: 10.1097/00002480-199201000-00006
Tuszynski MH (2000) Intraparenchymal NGF infusions rescue degenerating cholinergic neurons. Cell Transplant 9(5):629–636. https://doi.org/10.1177/096368970000900508
doi: 10.1177/096368970000900508
pubmed: 11144960
Tuszynski MH, Gage FH (1995) Bridging grafts and transient nerve growth factor infusions promote long-term central nervous system neuronal rescue and partial functional recovery. Proc Natl Acad Sci U S A 92(10):4621–4625. https://doi.org/10.1073/pnas.92.10.4621
doi: 10.1073/pnas.92.10.4621
pubmed: 7753852
pmcid: 41996
Tuszynski MH, U HS, Amaral DG, Gage FH (1990) Nerve growth factor infusion in the primate brain reduces lesion-induced cholinergic neuronal degeneration. J Neurosci 10(11):3604–3614
doi: 10.1523/JNEUROSCI.10-11-03604.1990
Tuszynski MH, Roberts J, Senut MC, U HS, Gage FH (1996) Gene therapy in the adult primate brain: intraparenchymal grafts of cells genetically modified to produce nerve growth factor prevent cholinergic neuronal degeneration. Gene Ther 3(4):305–314
pubmed: 8732162
Tuszynski MH, Thal L, Pay M, Salmon DP, U HS, Bakay R, Patel P, Blesch A, Vahlsing HL, Ho G, Tong G, Potkin SG, Fallon J, Hansen L, Mufson EJ, Kordower JH, Gall C, Conner J (2005) A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat Med 11(5):551–555. https://doi.org/10.1038/nm1239
doi: 10.1038/nm1239
pubmed: 15852017
Tuszynski MH, Yang JH, Barba D, U HS, Bakay RA, Pay MM, Masliah E, Conner JM, Kobalka P, Roy S, Nagahara AH (2015) Nerve growth factor gene therapy: activation of neuronal responses in Alzheimer disease. JAMA Neurol 72(10):1139–1147. https://doi.org/10.1001/jamaneurol.2015.1807
doi: 10.1001/jamaneurol.2015.1807
pubmed: 26302439
pmcid: 4944824
Varde NK, Pack DW (2004) Microspheres for controlled release drug delivery. Expert Opin Biol Ther 4(1):35–51. https://doi.org/10.1517/14712598.4.1.35
doi: 10.1517/14712598.4.1.35
pubmed: 14680467
Venero JL, Hefti F, Knusel B (1996) Trophic effect of exogenous nerve growth factor on rat striatal cholinergic neurons: comparison between intraparenchymal and intraventricular administration. Mol Pharmacol 49(2):303–310
pubmed: 8632763
Wahlberg LU, Lind G, Almqvist PM, Kusk P, Tornoe J, Juliusson B, Soderman M, Sellden E, Seiger A, Eriksdotter-Jonhagen M, Linderoth B (2012) Targeted delivery of nerve growth factor via encapsulated cell biodelivery in Alzheimer disease: a technology platform for restorative neurosurgery. J Neurosurg 117(2):340–347. https://doi.org/10.3171/2012.2.JNS11714
doi: 10.3171/2012.2.JNS11714
pubmed: 22655593
Wang Z, Wang Z, Lu WW, Zhen W, Yang D, Peng S (2017) Novel biomaterial strategies for controlled growth factor delivery for biomedical applications. NPG Asia Mater 9(10):e435–e435. https://doi.org/10.1038/am.2017.171
doi: 10.1038/am.2017.171
Wang SM, Lee CU, Lim HK (2019) Stem cell therapies for Alzheimer’s disease: is it time? Curr Opin Psychiatry 32(2):105–116. https://doi.org/10.1097/YCO.0000000000000478
doi: 10.1097/YCO.0000000000000478
pubmed: 30557266
Williams LR (1991) Hypophagia is induced by intracerebroventricular administration of nerve growth factor. Exp Neurol 113(1):31–37. https://doi.org/10.1016/0014-4886(91)90143-z
doi: 10.1016/0014-4886(91)90143-z
pubmed: 2044677
Williams LR, Varon S, Peterson GM, Wictorin K, Fischer W, Bjorklund A, Gage FH (1986) Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc Natl Acad Sci U S A 83(23):9231–9235. https://doi.org/10.1073/pnas.83.23.9231
doi: 10.1073/pnas.83.23.9231
pubmed: 3466184
pmcid: 387109
Williams LR, Vahlsing HL, Lindamood T, Varon S, Gage FH, Manthorpe M (1987) A small-gauge cannula device for continuous infusion of exogenous agents into the brain. Exp Neurol 95(3):743–754. https://doi.org/10.1016/0014-4886(87)90313-x
doi: 10.1016/0014-4886(87)90313-x
pubmed: 3545888
Winkler J, Ramirez GA, Kuhn HG, Peterson DA, Day-Lollini PA, Stewart GR, Tuszynski MH, Gage FH, Thal LJ (1997) Reversible Schwann cell hyperplasia and sprouting of sensory and sympathetic neurites after intraventricular administration of nerve growth factor. Ann Neurol 41(1):82–93. https://doi.org/10.1002/ana.410410114
doi: 10.1002/ana.410410114
pubmed: 9005869
Wu K, Meyer EM, Bennett JA, Meyers CA, Hughes JA, King MA (2005) AAV2/5-mediated NGF gene delivery protects septal cholinergic neurons following axotomy. Brain Res 1061(2):107–113. https://doi.org/10.1016/j.brainres.2005.08.056
doi: 10.1016/j.brainres.2005.08.056
pubmed: 16226726
Xhima K, Markham-Coultes K, Nedev H, Heinen S, Saragovi HU, Hynynen K, Aubert I (2020) Focused ultrasound delivery of a selective TrkA agonist rescues cholinergic function in a mouse model of Alzheimer’s disease. Sci Adv 6(4):eaax6646. https://doi.org/10.1126/sciadv.aax6646
doi: 10.1126/sciadv.aax6646
pubmed: 32010781
pmcid: 6976301
Xia B, Lv Y (2018) Dual-delivery of VEGF and NGF by emulsion electrospun nanofibrous scaffold for peripheral nerve regeneration. Mater Sci Eng C Mater Biol Appl 82:253–264. https://doi.org/10.1016/j.msec.2017.08.030
doi: 10.1016/j.msec.2017.08.030
pubmed: 29025656
Xie Y, Ye L, Zhang X, Cui W, Lou J, Nagai T, Hou X (2005) Transport of nerve growth factor encapsulated into liposomes across the blood-brain barrier: in vitro and in vivo studies. J Control Release 105(1–2):106–119. https://doi.org/10.1016/j.jconrel.2005.03.005
doi: 10.1016/j.jconrel.2005.03.005
pubmed: 15893839
Xie Y, Meeker RB, Massa SM, Longo FM (2019) Modulation of the p75 neurotrophin receptor suppresses age-related basal forebrain cholinergic neuron degeneration. Sci Rep 9(1):5273. https://doi.org/10.1038/s41598-019-41654-8
doi: 10.1038/s41598-019-41654-8
pubmed: 30918278
pmcid: 6437186
Xu X, Yu H, Gao S, Ma HQ, Leong KW, Wang S (2002) Polyphosphoester microspheres for sustained release of biologically active nerve growth factor. Biomaterials 23(17):3765–3772. https://doi.org/10.1016/s0142-9612(02)00116-3
doi: 10.1016/s0142-9612(02)00116-3
pubmed: 12109702
Xu D, Wu D, Qin M, Nih LR, Liu C, Cao Z, Ren J, Chen X, He Z, Yu W, Guan J, Duan S, Liu F, Liu X, Li J, Harley D, Xu B, Hou L, Chen ISY, Wen J, Chen W, Pourtaheri S, Lu Y (2019) Efficient delivery of nerve growth factors to the central nervous system for neural regeneration. Adv Mater 31(33):e1900727. https://doi.org/10.1002/adma.201900727
doi: 10.1002/adma.201900727
pubmed: 31125138
Yan Q, Matheson C, Sun J, Radeke MJ, Feinstein SC, Miller JA (1994) Distribution of intracerebral ventricularly administered neurotrophins in rat brain and its correlation with trk receptor expression. Exp Neurol 127(1):23–36. https://doi.org/10.1006/exnr.1994.1076
doi: 10.1006/exnr.1994.1076
pubmed: 8200435
Yang T, Liu H, Tran KC, Leng A, Massa SM, Longo FM (2020a) Small-molecule modulation of the p75 neurotrophin receptor inhibits a wide range of tau molecular pathologies and their sequelae in P301S tauopathy mice. Acta Neuropathol Commun 8(1):156. https://doi.org/10.1186/s40478-020-01034-0
doi: 10.1186/s40478-020-01034-0
pubmed: 32891185
pmcid: 7487850
Yang J, Wu S, Hou L, Zhu D, Yin S, Yang G, Wang Y (2020b) Therapeutic effects of simultaneous delivery of nerve growth factor mRNA and protein via exosomes on cerebral ischemia. Mol Ther Nucleic Acids 21:512–522. https://doi.org/10.1016/j.omtn.2020.06.013
doi: 10.1016/j.omtn.2020.06.013
pubmed: 32682291
pmcid: 7365960
Yi X, Manickam DS, Brynskikh A, Kabanov AV (2014) Agile delivery of protein therapeutics to CNS. J Control Release 190:637–663. https://doi.org/10.1016/j.jconrel.2014.06.017
doi: 10.1016/j.jconrel.2014.06.017
pubmed: 24956489
Zassler B, Humpel C (2006) Transplantation of NGF secreting primary monocytes counteracts NMDA-induced cell death of rat cholinergic neurons in vivo. Exp Neurol 198(2):391–400. https://doi.org/10.1016/j.expneurol.2005.12.009
doi: 10.1016/j.expneurol.2005.12.009
pubmed: 16443222
Zhang W, Wang PJ, Sha HY, Ni J, Li MH, Gu GJ (2014) Neural stem cell transplants improve cognitive function without altering amyloid pathology in an APP/PS1 double transgenic model of Alzheimer’s disease. Mol Neurobiol 50(2):423–437. https://doi.org/10.1007/s12035-014-8640-x
doi: 10.1007/s12035-014-8640-x
pubmed: 24481678
Zhang W, Zhou G, Gao Y, Zhou Y, Liu J, Zhang L, Long A, Zhang L, Tang P (2017) A sequential delivery system employing the synergism of EPO and NGF promotes sciatic nerve repair. Colloids Surf B Biointerfaces 159:327–336. https://doi.org/10.1016/j.colsurfb.2017.07.088
doi: 10.1016/j.colsurfb.2017.07.088
pubmed: 28806665
Zhao YZ, Jiang X, Xiao J, Lin Q, Yu WZ, Tian FR, Mao KL, Yang W, Wong HL, Lu CT (2016) Using NGF heparin-poloxamer thermosensitive hydrogels to enhance the nerve regeneration for spinal cord injury. Acta Biomater 29:71–80. https://doi.org/10.1016/j.actbio.2015.10.014
doi: 10.1016/j.actbio.2015.10.014
pubmed: 26472614
Zhu CW, Livote EE, Scarmeas N, Albert M, Brandt J, Blacker D, Sano M, Stern Y (2013) Long-term associations between cholinesterase inhibitors and memantine use and health outcomes among patients with Alzheimer’s disease. Alzheimers Dement 9(6):733–740. https://doi.org/10.1016/j.jalz.2012.09.015
doi: 10.1016/j.jalz.2012.09.015
pubmed: 23332671
Zhu SP, Wang ZG, Zhao YZ, Wu J, Shi HX, Ye LB, Wu FZ, Cheng Y, Zhang HY, He S, Wei X, Fu XB, Li XK, Xu HZ, Xiao J (2016) Gelatin nanostructured lipid carriers incorporating nerve growth factor inhibit endoplasmic reticulum stress-induced apoptosis and improve recovery in spinal cord injury. Mol Neurobiol 53(7):4375–4386. https://doi.org/10.1007/s12035-015-9372-2
doi: 10.1007/s12035-015-9372-2
pubmed: 26232067
Zilony-Hanin N, Rosenberg M, Richman M, Yehuda R, Schori H, Motiei M, Rahimipour S, Groisman A, Segal E, Shefi O (2019) Neuroprotective effect of nerve growth factor loaded in porous silicon nanostructures in an Alzheimer’s disease model and potential delivery to the brain. Small 15(45):e1904203. https://doi.org/10.1002/smll.201904203
doi: 10.1002/smll.201904203
pubmed: 31482695