Neuroprotective effects of intranasal extracellular vesicles from human platelet concentrates supernatants in traumatic brain injury and Parkinson's disease models.


Journal

Journal of biomedical science
ISSN: 1423-0127
Titre abrégé: J Biomed Sci
Pays: England
ID NLM: 9421567

Informations de publication

Date de publication:
05 Sep 2024
Historique:
received: 24 01 2024
accepted: 11 08 2024
medline: 6 9 2024
pubmed: 6 9 2024
entrez: 5 9 2024
Statut: epublish

Résumé

The burgeoning field of regenerative medicine has significantly advanced with recent findings on biotherapies using human platelet lysates (HPLs), derived from clinical-grade platelet concentrates (PCs), for treating brain disorders. These developments have opened new translational research avenues to explore the neuroprotective effects of platelet-extracellular vesicles (PEVs). Their potential in managing neurodegenerative conditions like traumatic brain injury (TBI) and Parkinson's disease (PD) warrants further exploration. We aimed here to characterize the composition of a PEV preparation isolated from platelet concentrate (PC) supernatant, and determine its neuroprotective potential and neurorestorative effects in cellular and animal models of TBI and PD. We isolated PEVs from the supernatant of clinical-grade PC collected from healthy blood donors utilizing high-speed centrifugation. PEVs were characterized by biophysical, biochemical, microscopic, and LC-MS/MS proteomics methods to unveil biological functions. Their functionality was assessed in vitro using SH-SY5Y neuronal cells, LUHMES dopaminergic neurons, and BV-2 microglial cells, and in vivo by intranasal administration in a controlled cortical impact (CCI)-TBI model using 8-weeks-old male C57/BL6 mice, and in a PD model induced by MPTP in 5-month-old male C57/BL6 mice. PEVs varied in size from 50 to 350 nm, predominantly around 200 nm, with concentrations ranging between 10 The potential of PEV-based therapies in neuroprotection opens new therapeutic avenues for neurodegenerative disorders. The study advocates for clinical trials to establish the efficacy of PEV-based biotherapies in neuroregenerative medicine.

Sections du résumé

BACKGROUND BACKGROUND
The burgeoning field of regenerative medicine has significantly advanced with recent findings on biotherapies using human platelet lysates (HPLs), derived from clinical-grade platelet concentrates (PCs), for treating brain disorders. These developments have opened new translational research avenues to explore the neuroprotective effects of platelet-extracellular vesicles (PEVs). Their potential in managing neurodegenerative conditions like traumatic brain injury (TBI) and Parkinson's disease (PD) warrants further exploration. We aimed here to characterize the composition of a PEV preparation isolated from platelet concentrate (PC) supernatant, and determine its neuroprotective potential and neurorestorative effects in cellular and animal models of TBI and PD.
METHODS METHODS
We isolated PEVs from the supernatant of clinical-grade PC collected from healthy blood donors utilizing high-speed centrifugation. PEVs were characterized by biophysical, biochemical, microscopic, and LC-MS/MS proteomics methods to unveil biological functions. Their functionality was assessed in vitro using SH-SY5Y neuronal cells, LUHMES dopaminergic neurons, and BV-2 microglial cells, and in vivo by intranasal administration in a controlled cortical impact (CCI)-TBI model using 8-weeks-old male C57/BL6 mice, and in a PD model induced by MPTP in 5-month-old male C57/BL6 mice.
RESULTS RESULTS
PEVs varied in size from 50 to 350 nm, predominantly around 200 nm, with concentrations ranging between 10
CONCLUSIONS CONCLUSIONS
The potential of PEV-based therapies in neuroprotection opens new therapeutic avenues for neurodegenerative disorders. The study advocates for clinical trials to establish the efficacy of PEV-based biotherapies in neuroregenerative medicine.

Identifiants

pubmed: 39237980
doi: 10.1186/s12929-024-01072-z
pii: 10.1186/s12929-024-01072-z
doi:

Substances chimiques

Neuroprotective Agents 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

87

Subventions

Organisme : National Science and Technology Council
ID : 111-2314-B-038-025
Organisme : National Science and Technology Council
ID : 112-2923-E-038-001
Organisme : National Science and Technology Council
ID : 112-2811-B-038-048

Informations de copyright

© 2024. The Author(s).

Références

Nebie O, et al. Can the administration of platelet lysates to the brain help treat neurological disorders? Cell Mol Life Sci. 2022;79(7):379.
pubmed: 35750991 pmcid: 9243829 doi: 10.1007/s00018-022-04397-w
Hayon Y, et al. Platelet lysates stimulate angiogenesis, neurogenesis and neuroprotection after stroke. Thromb Haemost. 2013;110(2):323–30.
pubmed: 23765126 doi: 10.1160/TH12-11-0875
Anitua E, et al. Intranasal PRGF-Endoret enhances neuronal survival and attenuates NF-kappaB-dependent inflammation process in a mouse model of Parkinson’s disease. J Control Release. 2015;203:170–80.
pubmed: 25702964 doi: 10.1016/j.jconrel.2015.02.030
Gouel F, et al. The protective effect of human platelet lysate in models of neurodegenerative disease: involvement of the Akt and MEK pathways. J Tissue Eng Regen Med. 2017;11(11):3236–40.
pubmed: 27943621 doi: 10.1002/term.2222
Anitua E, et al. Plasma rich in growth factors (PRGF-Endoret) reduces neuropathologic hallmarks and improves cognitive functions in an Alzheimer’s disease mouse model. Neurobiol Aging. 2014;35(7):1582–95.
pubmed: 24524966 doi: 10.1016/j.neurobiolaging.2014.01.009
Anitua E, et al. Intranasal delivery of plasma and platelet growth factors using PRGF-Endoret system enhances neurogenesis in a mouse model of Alzheimer’s disease. PLoS ONE. 2013;8(9): e73118.
pubmed: 24069173 pmcid: 3777974 doi: 10.1371/journal.pone.0073118
Nebie O, et al. Human platelet lysate biotherapy for traumatic brain injury: preclinical assessment. Brain. 2021;144(10):3142–58.
pubmed: 34086871 pmcid: 8634089 doi: 10.1093/brain/awab205
Delila L, et al. Neuroprotective activity of a virus-safe nanofiltered human platelet lysate depleted of extracellular vesicles in Parkinson’s disease and traumatic brain injury models. Bioeng Transl Med. 2023;8(1): e10360.
pubmed: 36684076 doi: 10.1002/btm2.10360
Chou ML, et al. Tailor-made purified human platelet lysate concentrated in neurotrophins for treatment of Parkinson’s disease. Biomaterials. 2017;142:77–89.
pubmed: 28728000 doi: 10.1016/j.biomaterials.2017.07.018
Nurden AT. Platelets, inflammation and tissue regeneration. Thromb Haemost. 2011;105(S06):S13-33.
pubmed: 21479340
Leiter O, Walker TL. Platelets: the missing link between the blood and brain? Prog Neurobiol. 2019;183: 101695.
pubmed: 31550515 doi: 10.1016/j.pneurobio.2019.101695
Leiter O, Walker TL. Platelets in neurodegenerative conditions-friend or foe? Front Immunol. 2020;11:747.
pubmed: 32431701 pmcid: 7214916 doi: 10.3389/fimmu.2020.00747
Burnouf T, Walker TL. The multifaceted role of platelets in mediating brain function. Blood. 2022;140(8):815–27.
pubmed: 35609283 pmcid: 9412009 doi: 10.1182/blood.2022015970
Blair P, Flaumenhaft R. Platelet α-granules: basic biology and clinical correlates. Blood Rev. 2009;23(4):177–89.
pubmed: 19450911 pmcid: 2720568 doi: 10.1016/j.blre.2009.04.001
Ajoy R, et al. CCL5 promotion of bioenergy metabolism is crucial for hippocampal synapse complex and memory formation. Mol Psychiatry. 2021;26(11):6451–68.
pubmed: 33931731 pmcid: 8760051 doi: 10.1038/s41380-021-01103-3
Ho MH, et al. CCL5 via GPX1 activation protects hippocampal memory function after mild traumatic brain injury. Redox Biol. 2021;46: 102067.
pubmed: 34315111 pmcid: 8327355 doi: 10.1016/j.redox.2021.102067
Leiter O, et al. Platelet-derived exerkine CXCL4/platelet factor 4 rejuvenates hippocampal neurogenesis and restores cognitive function in aged mice. Nat Commun. 2023;14(1):4375.
pubmed: 37587147 pmcid: 10432533 doi: 10.1038/s41467-023-39873-9
Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol. 1967;13(3):269–88.
pubmed: 6025241 doi: 10.1111/j.1365-2141.1967.tb08741.x
Tricarico C, Clancy J, D’Souza-Schorey C. Biology and biogenesis of shed microvesicles. Small GTPases. 2017;8(4):220–32.
pubmed: 27494381 doi: 10.1080/21541248.2016.1215283
György B, et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci. 2011;68(16):2667–88.
pubmed: 21560073 pmcid: 3142546 doi: 10.1007/s00018-011-0689-3
Raposo G, Stahl PD. Extracellular vesicles: a new communication paradigm? Nat Rev Mol Cell Biol. 2019;20(9):509–10.
pubmed: 31324871 doi: 10.1038/s41580-019-0158-7
Nyam-Erdene A, et al. Characterization and chromatographic isolation of platelet extracellular vesicles from human platelet lysates for applications in neuroregenerative medicine. ACS Biomater Sci Eng. 2021;7(12):5823–35.
pubmed: 34846835 doi: 10.1021/acsbiomaterials.1c01226
Bosch G, et al. Effects of platelet-rich plasma on the quality of repair of mechanically induced core lesions in equine superficial digital flexor tendons: a placebo-controlled experimental study. J Orthop Res. 2010;28(2):211–7.
pubmed: 19714688 doi: 10.1002/jor.20980
Duerschmied D, et al. Platelet serotonin promotes the recruitment of neutrophils to sites of acute inflammation in mice. Blood. 2013;121(6):1008–15.
pubmed: 23243271 pmcid: 3567335 doi: 10.1182/blood-2012-06-437392
Jenne C, Urrutia R, Kubes P. Platelets: bridging hemostasis, inflammation, and immunity. Int J Lab Hematol. 2013;35(3):254–61.
pubmed: 23590652 doi: 10.1111/ijlh.12084
Kodali M, et al. Intranasally administered human MSC-derived extracellular vesicles inhibit NLRP3-p38/MAPK signaling after TBI and prevent chronic brain dysfunction. Brain Behav Immun. 2023;108:118–34.
pubmed: 36427808 doi: 10.1016/j.bbi.2022.11.014
Faille D, et al. Endocytosis and intracellular processing of platelet microparticles by brain endothelial cells. J Cell Mol Med. 2012;16(8):1731–8.
pubmed: 21883894 pmcid: 3822686 doi: 10.1111/j.1582-4934.2011.01434.x
Campolo M, Esposito E, Cuzzocrea S. A controlled cortical impact preclinical model of traumatic brain injury. Methods Mol Biol. 2018;1727:385–91.
pubmed: 29222798 doi: 10.1007/978-1-4939-7571-6_30
Mustapha M, Taib CNM. MPTP-induced mouse model of Parkinson’s disease: a promising direction for therapeutic strategies. Bosn J Basic Med Sci. 2021;21(4):422.
pubmed: 33357211 pmcid: 8292858
Widyaningrum R, et al. In vitro evaluation of platelet extracellular vesicles (PEVs) for corneal endothelial regeneration. Platelets. 2022;33(8):1237–50.
pubmed: 35949054 doi: 10.1080/09537104.2022.2105829
Delila L, et al. Extensive characterization of the composition and functional activities of five preparations of human platelet lysates for dedicated clinical uses. Platelets. 2021;32(2):259–72.
pubmed: 33245683 doi: 10.1080/09537104.2020.1849603
Chou ML, et al. Nanofiltration to remove microparticles and decrease the thrombogenicity of plasma: in vitro feasibility assessment. Transfusion. 2015;55(10):2433–44.
pubmed: 25988671 doi: 10.1111/trf.13162
Le NTN, et al. Proteomics of human platelet lysates and insight from animal studies on platelet protein diffusion to hippocampus upon intranasal administration. APL Bioeng. 2024;8(2): 026111.
pubmed: 38726021 pmcid: 11080963 doi: 10.1063/5.0196553
Devos D, et al. Targeting chelatable iron as a therapeutic modality in Parkinson’s disease. Antioxid Redox Signal. 2014;21(2):195–210.
pubmed: 24251381 pmcid: 4060813 doi: 10.1089/ars.2013.5593
Goldie BJ, Barnett MM, Cairns MJ. BDNF and the maturation of posttranscriptional regulatory networks in human SH-SY5Y neuroblast differentiation. Front Cell Neurosci. 2014;8:325.
pubmed: 25360083 pmcid: 4197648 doi: 10.3389/fncel.2014.00325
Zhu X, et al. PDGF-mediated protection of SH-SY5Y cells against Tat toxin involves regulation of extracellular glutamate and intracellular calcium. Toxicol Appl Pharmacol. 2009;240(2):286–91.
pubmed: 19576918 pmcid: 2753679 doi: 10.1016/j.taap.2009.06.020
Lavenius E, et al. Basic FGF and IGF-I promote differentiation of human SH-SY5Y neuroblastoma cells in culture. Growth Factors. 1994;10(1):29–39.
pubmed: 7514011 doi: 10.3109/08977199409019601
Nebie O, et al. Heat-treated human platelet pellet lysate modulates microglia activation, favors wound healing and promotes neuronal differentiation in vitro. Platelets. 2021;32(2):226–37.
pubmed: 32106742 doi: 10.1080/09537104.2020.1732324
Lu J, et al. Extracellular vesicles from endothelial progenitor cells prevent steroid-induced osteoporosis by suppressing the ferroptotic pathway in mouse osteoblasts based on bioinformatics evidence. Sci Rep. 2019;9(1):16130.
pubmed: 31695092 pmcid: 6834614 doi: 10.1038/s41598-019-52513-x
Mahoney-Sánchez L, et al. Ferroptosis and its potential role in the physiopathology of Parkinson’s Disease. Prog Neurobiol. 2021;196: 101890.
pubmed: 32726602 doi: 10.1016/j.pneurobio.2020.101890
Xie Q, et al. Delavatine A, an unusual isoquinoline alkaloid exerts anti-inflammation on LPS-induced proinflammatory cytokines production by suppressing NF-κB activation in BV-2 microglia. Biochem Biophys Res Commun. 2018;502(2):202–8.
pubmed: 29792864 doi: 10.1016/j.bbrc.2018.05.144
Oh W-J, et al. Inhibition of lipopolysaccharide-induced proinflammatory responses by Buddleja officinalis extract in BV-2 microglial cells via negative regulation of NF-κB and ERK1/2 signaling. Molecules. 2013;18(8):9195–206.
pubmed: 23912273 pmcid: 6270610 doi: 10.3390/molecules18089195
Kempuraj D, et al. Neuroinflammation induces neurodegeneration. J Neurol Neurosurg Spine. 2016;1(1):1003.
pubmed: 28127589 pmcid: 5260818
Chen WW, Zhang X, Huang WJ. Role of neuroinflammation in neurodegenerative diseases. Mol Med Rep. 2016;13(4):3391–6.
pubmed: 26935478 pmcid: 4805095 doi: 10.3892/mmr.2016.4948
Valera E, et al. NMDA-induced neuroprotection in hippocampal neurons is mediated through the protein kinase A and CREB (cAMP-response element-binding protein) pathway. Neurochem Int. 2008;53(5):148–54.
pubmed: 18694792 doi: 10.1016/j.neuint.2008.07.007
Saint-Pol J, et al. Targeting and crossing the blood-brain barrier with extracellular vesicles. Cells. 2020;9(4):851.
pubmed: 32244730 pmcid: 7226770 doi: 10.3390/cells9040851
Zhang Y, et al. Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury. J Neurosurg. 2015;122(4):856–67.
pubmed: 25594326 pmcid: 4382456 doi: 10.3171/2014.11.JNS14770
Hayon Y, et al. Platelet microparticles induce angiogenesis and neurogenesis after cerebral ischemia. Curr Neurovasc Res. 2012;9(3):185–92.
pubmed: 22621230 doi: 10.2174/156720212801619018
Hayon Y, et al. Platelet microparticles promote neural stem cell proliferation, survival and differentiation. J Mol Neurosci. 2012;47:659–65.
pubmed: 22290563 doi: 10.1007/s12031-012-9711-y
Tóth EÁ, et al. Formation of a protein corona on the surface of extracellular vesicles in blood plasma. J Extracellular Vesicles. 2021;10(11): e12140.
doi: 10.1002/jev2.12140
Böing AN, et al. Single-step isolation of extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles. 2014;3(1):23430.
doi: 10.3402/jev.v3.23430
Théry C, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018;7(1):1535750.
pubmed: 30637094 pmcid: 6322352 doi: 10.1080/20013078.2018.1535750
Welsh JA, et al. Minimal information for studies of extracellular vesicles (MISEV2023): from basic to advanced approaches. J Extracell Vesicles. 2024;13(2): e12404.
pubmed: 38326288 pmcid: 10850029 doi: 10.1002/jev2.12404
Brennan K, et al. A comparison of methods for the isolation and separation of extracellular vesicles from protein and lipid particles in human serum. Sci Rep. 2020;10(1):1039.
pubmed: 31974468 pmcid: 6978318 doi: 10.1038/s41598-020-57497-7
Aatonen MT, et al. Isolation and characterization of platelet-derived extracellular vesicles. J Extracell Vesicles. 2014;3(1):24692.
doi: 10.3402/jev.v3.24692
Shattil SJ, Newman PJ. Integrins: dynamic scaffolds for adhesion and signaling in platelets. Blood. 2004;104(6):1606–15.
pubmed: 15205259 doi: 10.1182/blood-2004-04-1257
Stockwell BR, et al. Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease. Cell. 2017;171(2):273–85.
pubmed: 28985560 pmcid: 5685180 doi: 10.1016/j.cell.2017.09.021
Samukange WT, et al. Selection of blood, blood components, and blood products as essential medicines in 105 low-and middle-income countries. Transfus Med Rev. 2020;34(2):94–100.
pubmed: 31761652 doi: 10.1016/j.tmrv.2019.10.005
Lin H-C, et al. Platelet-derived microparticles trigger THP-1 monocytic cell aggregation and release of pro-coagulant tissue factor-expressing microparticles in vitro. Transfus Apheres Sci. 2015;53(2):246–52.
doi: 10.1016/j.transci.2015.10.002
Obeid S, et al. NanoBioAnalytical characterization of extracellular vesicles in 75-nm nanofiltered human plasma for transfusion: a tool to improve transfusion safety. Nanomed Nanotechnol Biol Med. 2019;20: 101977.
doi: 10.1016/j.nano.2019.02.026
Burnouf T, et al. Expanding applications of allogeneic platelets, platelet lysates, and platelet extracellular vesicles in cell therapy, regenerative medicine, and targeted drug delivery. J Biomed Sci. 2023;30(1):79.
pubmed: 37704991 pmcid: 10500824 doi: 10.1186/s12929-023-00972-w
Schallmoser K, et al. Production and quality requirements of human platelet lysate: a position statement from the working party on cellular therapies of the international society of blood transfusion. Trends Biotechnol. 2020;38(1):13–23.
pubmed: 31326128 doi: 10.1016/j.tibtech.2019.06.002
Staubach S, et al. Scaled preparation of extracellular vesicles from conditioned media. Adv Drug Deliv Rev. 2021;177: 113940.
pubmed: 34419502 doi: 10.1016/j.addr.2021.113940
Agrahari V, et al. Extracellular microvesicles as new industrial therapeutic frontiers. Trends Biotechnol. 2019;37(7):707–29.
pubmed: 30638682 doi: 10.1016/j.tibtech.2018.11.012
Takov K, Yellon DM, Davidson SM. Comparison of small extracellular vesicles isolated from plasma by ultracentrifugation or size-exclusion chromatography: yield, purity and functional potential. J Extracell Vesicles. 2019;8(1):1560809.
pubmed: 30651940 doi: 10.1080/20013078.2018.1560809
Burnouf T, et al. Platelet microparticles: detection and assessment of their paradoxical functional roles in disease and regenerative medicine. Blood Rev. 2014;28(4):155–66.
pubmed: 24826991 doi: 10.1016/j.blre.2014.04.002
Chen A, et al. The neuroprotective roles of BDNF in hypoxic ischemic brain injury. Biomed Rep. 2013;1(2):167–76.
pubmed: 24648914 doi: 10.3892/br.2012.48
Habtemariam S. The brain-derived neurotrophic factor in neuronal plasticity and neuroregeneration: new pharmacological concepts for old and new drugs. Neural Regen Res. 2018;13(6):983.
pubmed: 29926822 pmcid: 6022464 doi: 10.4103/1673-5374.233438
Schroer AB, et al. Platelet factors attenuate inflammation and rescue cognition in ageing. Nature. 2023;620:1–9.
doi: 10.1038/s41586-023-06436-3
Chen H, et al. Platelet-derived growth factor (PDGF)-BB protects dopaminergic neurons via activation of Akt/ERK/CREB pathways to upregulate tyrosine hydroxylase. CNS Neurosci Ther. 2021;27(11):1300–12.
pubmed: 34346167 pmcid: 8504523 doi: 10.1111/cns.13708
Gustafsson D, et al. The role of BDNF in experimental and clinical traumatic brain injury. Int J Mol Sci. 2021;22(7):3582.
pubmed: 33808272 pmcid: 8037220 doi: 10.3390/ijms22073582
Hyman C, et al. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature. 1991;350(6315):230–2.
pubmed: 2005978 doi: 10.1038/350230a0
Wu F, et al. Platelet derived growth factor promotes the recovery of traumatic brain injury by inhibiting endoplasmic reticulum stress and autophagy-mediated pyroptosis. Front Pharmacol. 2022;13: 862324.
pubmed: 36339541 pmcid: 9629145 doi: 10.3389/fphar.2022.862324
Park C, et al. Platelet factors are induced by longevity factor klotho and enhance cognition in young and aging mice. Nat Aging. 2023;3(9):1067–78.
pubmed: 37587231 pmcid: 10501899 doi: 10.1038/s43587-023-00468-0
Przedborski S, et al. Increased superoxide dismutase activity improves survival of cultured postnatal midbrain neurons. J Neurochem. 1996;67(4):1383–92.
pubmed: 8858919 doi: 10.1046/j.1471-4159.1996.67041383.x
Jung JE, et al. Regulation of Mn-superoxide dismutase activity and neuroprotection by STAT3 in mice after cerebral ischemia. J Neurosci. 2009;29(21):7003–14.
pubmed: 19474327 pmcid: 2712132 doi: 10.1523/JNEUROSCI.1110-09.2009
Nakagawa S, et al. Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci. 2002;22(9):3673–82.
pubmed: 11978843 pmcid: 6758358 doi: 10.1523/JNEUROSCI.22-09-03673.2002
Charest PG, Firtel RA. Big roles for small GTPases in the control of directed cell movement. Biochem J. 2007;401(2):377–90.
pubmed: 17173542 doi: 10.1042/BJ20061432
Lino MM, et al. Engineered extracellular vesicles as brain therapeutics. J Control Release. 2021;338:472–85.
pubmed: 34428481 doi: 10.1016/j.jconrel.2021.08.037
Rebulla P, Prati D. Pathogen reduction for platelets-a review of recent implementation strategies. Pathogens. 2022;11(2):142.
pubmed: 35215085 pmcid: 8879285 doi: 10.3390/pathogens11020142
Nebie O, et al. The neuroprotective activity of heat-treated human platelet lysate biomaterials manufactured from outdated pathogen-reduced (amotosalen/UVA) platelet concentrates. J Biomed Sci. 2019;26(1):89.
pubmed: 31666073 pmcid: 6822406 doi: 10.1186/s12929-019-0579-9
Gouel F, et al. Whole and fractionated human platelet lysate biomaterials-based biotherapy induces strong neuroprotection in experimental models of amyotrophic lateral sclerosis. Biomaterials. 2022;280: 121311.
pubmed: 34952382 doi: 10.1016/j.biomaterials.2021.121311
Johnson J, et al. First-in-human clinical trial of allogeneic, platelet-derived extracellular vesicles as a potential therapeutic for delayed wound healing. J Extracell Vesicles. 2023;12(7): e12332.
pubmed: 37353884 doi: 10.1002/jev2.12332

Auteurs

Liling Delila (L)

Graduate Institute of Biomedical Materials and Tissue Engineering, College of Biomedical Engineering, Taipei Medical University, 250 Wu-Xing Street, Taipei, 11031, Taiwan.
Univ. Lille, Inserm, CHU-Lille, U1172, Lille Neuroscience & Cognition, LiCEND COEN Center, Lille, France.

Ouada Nebie (O)

Graduate Institute of Biomedical Materials and Tissue Engineering, College of Biomedical Engineering, Taipei Medical University, 250 Wu-Xing Street, Taipei, 11031, Taiwan.
Univ. Lille, Inserm, CHU-Lille, U1172, Lille Neuroscience & Cognition, LiCEND COEN Center, Lille, France.
Alzheimer & Tauopathies, Labex DISTALZ, Lille, France.

Nhi Thao Ngoc Le (NTN)

International PhD Program in Biomedical Engineering, College of Biomedical Engineering, Taipei Medical University, Taipei, 11031, Taiwan.

Kelly Timmerman (K)

Univ. Lille, Inserm, CHU-Lille, U1172, Lille Neuroscience & Cognition, LiCEND COEN Center, Lille, France.

Deng-Yao Lee (DY)

Graduate Institute of Biomedical Materials and Tissue Engineering, College of Biomedical Engineering, Taipei Medical University, 250 Wu-Xing Street, Taipei, 11031, Taiwan.

Yu-Wen Wu (YW)

Graduate Institute of Biomedical Materials and Tissue Engineering, College of Biomedical Engineering, Taipei Medical University, 250 Wu-Xing Street, Taipei, 11031, Taiwan.
Biomedical Translation Research Center (BioTReC), Academia Sinica, Taipei, Taiwan.

Ming-Li Chou (ML)

Graduate Institute of Biomedical Materials and Tissue Engineering, College of Biomedical Engineering, Taipei Medical University, 250 Wu-Xing Street, Taipei, 11031, Taiwan.
Institute of Clinical Medicine, National Yang-Ming Chiao Tung University, Taipei, Taiwan.

Luc Buée (L)

Univ. Lille, Inserm, CHU-Lille, U1172, Lille Neuroscience & Cognition, LiCEND COEN Center, Lille, France.
Alzheimer & Tauopathies, Labex DISTALZ, Lille, France.
NeuroTMULille, Lille Neuroscience & Cognition, Lille, France.

Szu-Yi Chou (SY)

Ph.D. Program in Medical Neuroscience, College of Medical Science and Technology, Taipei Medical University and National Health Research Institute, Taipei, 11031, Taiwan.
NeuroTMULille, Taipei Medical University, Taipei, 11031, Taiwan.
Graduate Institute of Neural Regenerative Medicine, College of Medical Science and Technology, Taipei Medical University, Taipei, 11031, Taiwan.
Neuroscience Research Center, Taipei Medical University, Taipei, 11031, Taiwan.
International Master Program in Medical Neuroscience, College of Medical Science and Technology, Taipei Medical University, Taipei, 11031, Taiwan.

David Blum (D)

Univ. Lille, Inserm, CHU-Lille, U1172, Lille Neuroscience & Cognition, LiCEND COEN Center, Lille, France.
Alzheimer & Tauopathies, Labex DISTALZ, Lille, France.
NeuroTMULille, Lille Neuroscience & Cognition, Lille, France.

David Devos (D)

Univ. Lille, Inserm, CHU-Lille, U1172, Lille Neuroscience & Cognition, LiCEND COEN Center, Lille, France. david.devos@chu-lille.fr.
NeuroTMULille, Lille Neuroscience & Cognition, Lille, France. david.devos@chu-lille.fr.
Department of Medical Pharmacology, Expert Center of Parkinson's Disease and ALS, CHU-Lille, Lille, France. david.devos@chu-lille.fr.

Thierry Burnouf (T)

Graduate Institute of Biomedical Materials and Tissue Engineering, College of Biomedical Engineering, Taipei Medical University, 250 Wu-Xing Street, Taipei, 11031, Taiwan. thburnouf@gmail.com.
International PhD Program in Biomedical Engineering, College of Biomedical Engineering, Taipei Medical University, Taipei, 11031, Taiwan. thburnouf@gmail.com.
NeuroTMULille, Taipei Medical University, Taipei, 11031, Taiwan. thburnouf@gmail.com.
International PhD Program in Cell Therapy and Regeneration Medicine, Taipei Medical University, Taipei, 11031, Taiwan. thburnouf@gmail.com.
PhD Program in Graduate Institute of Mind Brain and Consciousness, College of Humanities and Social Sciences, Taipei Medical University, Taipei, Taiwan. thburnouf@gmail.com.

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Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
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Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
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Humans Yoga Low Back Pain Female Male

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