Spinal Cord Injury Leads to Hippocampal Glial Alterations and Neural Stem Cell Inactivation.
Adult neurogenesis
Glial alterations
Neuroinflammation
Spinal cord injury
Journal
Cellular and molecular neurobiology
ISSN: 1573-6830
Titre abrégé: Cell Mol Neurobiol
Pays: United States
ID NLM: 8200709
Informations de publication
Date de publication:
Jan 2022
Jan 2022
Historique:
received:
19
02
2020
accepted:
06
06
2020
pubmed:
17
6
2020
medline:
1
4
2022
entrez:
16
6
2020
Statut:
ppublish
Résumé
The hippocampus encodes spatial and contextual information involved in memory and learning. The incorporation of new neurons into hippocampal networks increases neuroplasticity and enhances hippocampal-dependent learning performances. Only few studies have described hippocampal abnormalities after spinal cord injury (SCI) although cognitive deficits related to hippocampal function have been reported in rodents and even humans. The aim of this study was to characterize in further detail hippocampal changes in the acute and chronic SCI. Our data suggested that neurogenesis reduction in the acute phase after SCI could be due to enhanced death of amplifying neural progenitors (ANPs). In addition, astrocytes became reactive and microglial cells increased their number in almost all hippocampal regions studied. Glial changes resulted in a non-inflammatory response as the mRNAs of the major pro-inflammatory cytokines (IL-1β, TNFα, IL-18) remained unaltered, but CD200R mRNA levels were downregulated. Long-term after SCI, astrocytes remained reactive but on the other hand, microglial cell density decreased. Also, glial cells induced a neuroinflammatory environment with the upregulation of IL-1β, TNFα and IL-18 mRNA expression and the decrease of CD200R mRNA. Neurogenesis reduction may be ascribed at later time points to inactivation of neural stem cells (NSCs) and inhibition of ANP proliferation. The number of granular cells and CA1 pyramidal neurons decreased only in the chronic phase. The release of pro-inflammatory cytokines at the chronic phase might involve neurogenesis reduction and neurodegeneration of hippocampal neurons. Therefore, SCI led to hippocampal changes that could be implicated in cognitive deficits observed in rodents and humans.
Identifiants
pubmed: 32537668
doi: 10.1007/s10571-020-00900-8
pii: 10.1007/s10571-020-00900-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
197-215Subventions
Organisme : RyC-2012-11137 (MINECO)
ID : 11137
Organisme : FEDER funds
ID : SAF-2015-70866-R
Organisme : Ministry of Science and Technology, Argentina
ID : PICT 2017 N0509
Informations de copyright
© 2020. Springer Science+Business Media, LLC, part of Springer Nature.
Références
Adamczyk A et al (2012) GluA3-deficiency in mice is associated with increased social and aggressive behavior and elevated dopamine in striatum. Behav Brain Res 229:265–272. https://doi.org/10.1016/j.bbr.2012.01.007
doi: 10.1016/j.bbr.2012.01.007
pubmed: 22285418
pmcid: 4096766
Alluin O, Karimi-Abdolrezaee S, Delivet-Mongrain H, Leblond H, Fehlings MG, Rossignol S (2011) Kinematic study of locomotor recovery after spinal cord clip compression injury in rats. J Neurotrauma 28:1963–1981. https://doi.org/10.1089/neu.2011.1840
doi: 10.1089/neu.2011.1840
pubmed: 21770755
Arroyo DS et al (2013) Toll-like receptor 2 ligands promote microglial cell death by inducing autophagy. FASEB J: Off Publ Fed Am Soc Exp Biol 27:299–312. https://doi.org/10.1096/fj.12-214312
doi: 10.1096/fj.12-214312
Basso DM, Beattie MS, Bresnahan JC (1996) Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 139:244–256
doi: 10.1006/exnr.1996.0098
Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG (2006) Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 23:635–659. https://doi.org/10.1089/neu.2006.23.635
doi: 10.1089/neu.2006.23.635
pubmed: 16689667
Beattie MS, Hermann GE, Rogers RC, Bresnahan JC (2002) Cell death in models of spinal cord injury. Prog Brain Res 137:37–47
doi: 10.1016/S0079-6123(02)37006-7
Bektas A, Schurman SH, Sen R, Ferrucci L (2018) Aging, inflammation and the environment. Exp Gerontol 105:10–18. https://doi.org/10.1016/j.exger.2017.12.015
doi: 10.1016/j.exger.2017.12.015
pubmed: 29275161
Belarbi K, Arellano C, Ferguson R, Jopson T, Rosi S (2012a) Chronic neuroinflammation impacts the recruitment of adult-born neurons into behaviorally relevant hippocampal networks. Brain, Behav Immun 26:18–23. https://doi.org/10.1016/j.bbi.2011.07.225
doi: 10.1016/j.bbi.2011.07.225
Belarbi K, Jopson T, Tweedie D, Arellano C, Luo W, Greig NH, Rosi S (2012b) TNF-alpha protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation. J Neuroinflamm 9:23. https://doi.org/10.1186/1742-2094-9-23
doi: 10.1186/1742-2094-9-23
Bruel-Jungerman E, Rampon C, Laroche S (2007) Adult hippocampal neurogenesis, synaptic plasticity and memory: facts and hypotheses. Revi Neurosci 18:93–114. https://doi.org/10.1515/revneuro.2007.18.2.93
doi: 10.1515/revneuro.2007.18.2.93
Burda JE, Sofroniew MV (2014) Reactive gliosis and the multicellular response to CNS damage and disease. Neuron 81:229–248. https://doi.org/10.1016/j.neuron.2013.12.034
doi: 10.1016/j.neuron.2013.12.034
pubmed: 3984950
pmcid: 3984950
Chen Q, Xu L, Du T, Hou Y, Fan W, Wu Q, Yan H (2019) Enhanced Expression of PD-L1 on Microglia After Surgical Brain Injury Exerts Self-Protection from Inflammation and Promotes. Neurol Repair Neurochem Res 44:2470–2481. https://doi.org/10.1007/s11064-019-02864-8
doi: 10.1007/s11064-019-02864-8
Chen ZQ et al (2019) Negative regulation of glial Tim-3 inhibits the secretion of inflammatory factors and modulates microglia to antiinflammatory phenotype after experimental intracerebral hemorrhage in rats CNS. Neurosci Therap 25:674–684. https://doi.org/10.1111/cns.13100
doi: 10.1111/cns.13100
Cheyuo C, Aziz M, Wang P (2019) Neurogenesis in neurodegenerative diseases: role of MFG-E8. Front Neurosci 13:569. https://doi.org/10.3389/fnins.2019.00569
doi: 10.3389/fnins.2019.00569
pubmed: 31213977
pmcid: 6558065
Couillard-Despres S et al (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosc 21:1–14. https://doi.org/10.1111/j.1460-9568.2004.03813.x
doi: 10.1111/j.1460-9568.2004.03813.x
Craig A et al (2015) Prospective study of the occurrence of psychological disorders and comorbidities after spinal cord injury. Arch Phys Med Rehabil 96:1426–1434. https://doi.org/10.1016/j.apmr.2015.02.027
doi: 10.1016/j.apmr.2015.02.027
pubmed: 25778773
Cummings BS, Schnellmann RG. (2004). Measurement of cell death in mammalian cells current protocols in pharmacology. Chapter 12:Unit 12, 18, doi:10.1002/0471141755.ph1208s25.
Davidoff GN, Roth EJ, Richards JS (1992) Cognitive deficits in spinal cord injury: epidemiology and outcome. Arch Phys Med Rehabil 73:275–284
doi: 10.1016/0003-9993(92)90006-I
de Almeida FM et al (2011) Human dental pulp cells: a new source of cell therapy in a mouse model of compressive spinal cord injury. J Neurotrauma 28:1939–1949. https://doi.org/10.1089/neu.2010.1317
doi: 10.1089/neu.2010.1317
pubmed: 21609310
Dehler S, Lou WP, Gao L, Skabkin M, Dallenbach S, Neumann A, Martin-Villalba A (2018) An immune-CNS axis activates remote hippocampal stem cells following spinal transection injury. Front Mol Neurosci 11:443. https://doi.org/10.3389/fnmol.2018.00443
doi: 10.3389/fnmol.2018.00443
pubmed: 30618602
pmcid: 6299844
Dolan EJ, Tator CH (1979) A new method for testing the force of clips for aneurysms or experimental spinal cord compression. J Neurosurg 51:229–233. https://doi.org/10.3171/jns.1979.51.2.0229
doi: 10.3171/jns.1979.51.2.0229
pubmed: 448431
Dowler RN, Harrington DL, Haaland KY, Swanda RM, Fee F, Fiedler K (1997) Profiles of cognitive functioning in chronic spinal cord injury and the role of moderating variables. J Int Neuropsychol Soc JINS 3:464–472
doi: 10.1017/S1355617797004645
Dowler RN, O'Brien SA, Haaland KY, Harrington DL, Feel F, Fiedler K (1995) Neuropsychological functioning following a spinal cord injury. Appl Neuropsychol 2:124–129. https://doi.org/10.1080/09084282.1995.9645349
doi: 10.1080/09084282.1995.9645349
pubmed: 16318515
Ehninger D, Kempermann G (2008) Neurogenesis in the adult hippocampus. Cell Tissue Res 331:243–250. https://doi.org/10.1007/s00441-007-0478-3
doi: 10.1007/s00441-007-0478-3
pubmed: 17938969
Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 100:13632–13637. https://doi.org/10.1073/pnas.2234031100
doi: 10.1073/pnas.2234031100
pubmed: 14581618
pmcid: 263865
Encinas JM, Hamani C, Lozano AM, Enikolopov G (2011a) Neurogenic hippocampal targets of deep brain stimulation. J Comp Neurol 519:6–20. https://doi.org/10.1002/cne.22503
doi: 10.1002/cne.22503
pubmed: 21120924
pmcid: 3042399
Encinas JM et al (2011b) Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8:566–579. https://doi.org/10.1016/j.stem.2011.03.010
doi: 10.1016/j.stem.2011.03.010
pubmed: 21549330
pmcid: 3286186
Encinas JM, Sierra A (2012) Neural stem cell deforestation as the main force driving the age-related decline in adult hippocampal neurogenesis. Behav Brain Res 227:433–439. https://doi.org/10.1016/j.bbr.2011.10.010
doi: 10.1016/j.bbr.2011.10.010
pubmed: 22019362
Encinas JM, Vaahtokari A, Enikolopov G (2006) Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci USA 103:8233–8238. https://doi.org/10.1073/pnas.0601992103
doi: 10.1073/pnas.0601992103
pubmed: 16702546
pmcid: 1461404
Felix MS, Popa N, Djelloul M, Boucraut J, Gauthier P, Bauer S, Matarazzo VA (2012) Alteration of forebrain neurogenesis after cervical spinal cord injury in the adult rat. Front Neuroscience 6:45. https://doi.org/10.3389/fnins.2012.00045
doi: 10.3389/fnins.2012.00045
Frank MG, Fonken LK, Annis JL, Watkins LR, Maier SF (2018) Stress disinhibits microglia via down-regulation of CD200R: a mechanism of neuroinflammatory priming. Brain Behav Immun 69:62–73. https://doi.org/10.1016/j.bbi.2017.11.001
doi: 10.1016/j.bbi.2017.11.001
pubmed: 29104062
pmcid: 29104062
Fricker M, Vilalta A, Tolkovsky AM, Brown GC (2013) Caspase inhibitors protect neurons by enabling selective necroptosis of inflamed microglia. J Biol Chem 288:9145–9152. https://doi.org/10.1074/jbc.M112.427880
doi: 10.1074/jbc.M112.427880
pubmed: 23386613
pmcid: 3610987
Garcia-Ovejero D, Gonzalez S, Paniagua-Torija B, Lima A, Molina-Holgado E, De Nicola AF, Labombarda F (2014) Progesterone reduces secondary damage, preserves white matter, and improves locomotor outcome after spinal cord contusion. J Neurotrauma 31:857–871. https://doi.org/10.1089/neu.2013.3162
doi: 10.1089/neu.2013.3162
pubmed: 24460450
pmcid: 3996974
Gebara E et al (2016) Heterogeneity of radial glia-like cells in the adult hippocampus. Stem cells 34:997–1010. https://doi.org/10.1002/stem.2266
doi: 10.1002/stem.2266
pubmed: 26729510
pmcid: 5340291
Gorczynski RM (2005) CD200 and its receptors as targets for immunoregulation. Curr Opin Invest Drugs 6:483–488
Hernangomez M, Klusakova I, Joukal M, Hradilova-Svizenska I, Guaza C, Dubovy P (2016) CD200R1 agonist attenuates glial activation, inflammatory reactions, and hypersensitivity immediately after its intrathecal application in a rat neuropathic pain model. J Neuroinflamm 13:43. https://doi.org/10.1186/s12974-016-0508-8
doi: 10.1186/s12974-016-0508-8
Huttmann K, Sadgrove M, Wallraff A, Hinterkeuser S, Kirchhoff F, Steinhauser C, Gray WP (2003) Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: functional and immunocytochemical analysis. Eu J Neurosci 18:2769–2778
doi: 10.1111/j.1460-9568.2003.03002.x
Iosif RE et al (2006) Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci 26:9703–9712. https://doi.org/10.1523/JNEUROSCI.2723-06.2006
doi: 10.1523/JNEUROSCI.2723-06.2006
pubmed: 16988041
pmcid: 16988041
Joshi M, Fehlings MG (2002a) Development and characterization of a novel, graded model of clip compressive spinal cord injury in the mouse: part 1 Clip Design, behavioral outcomes, and histopathology. J Neurotrauma 19:175–190. https://doi.org/10.1089/08977150252806947
doi: 10.1089/08977150252806947
pubmed: 11893021
Joshi M, Fehlings MG (2002b) Development and characterization of a novel, graded model of clip compressive spinal cord injury in the mouse: part 2 Quantitative neuroanatomical assessment and analysis of the relationships between axonal tracts, residual tissue, and locomotor recovery. J Neurotrauma 19:191–203. https://doi.org/10.1089/08977150252806956
doi: 10.1089/08977150252806956
pubmed: 11893022
Jure I, De Nicola AF, Labombarda F (2019) Progesterone effects on oligodendrocyte differentiation in injured spinal cord. Brain Res 1708:36–46. https://doi.org/10.1016/j.brainres.2018.12.005
doi: 10.1016/j.brainres.2018.12.005
pubmed: 30527678
Jure I, Pietranera L, De Nicola AF, Labombarda F (2017) Spinal cord injury impairs neurogenesis and induces glial reactivity in the hippocampus. Neurochem Res. https://doi.org/10.1007/s11064-017-2225-9
doi: 10.1007/s11064-017-2225-9
pubmed: 28290135
Kempermann G (2011) Seven principles in the regulation of adult neurogenesis. Eur J Neurosci 33:1018–1024. https://doi.org/10.1111/j.1460-9568.2011.07599.x
doi: 10.1111/j.1460-9568.2011.07599.x
pubmed: 21395844
Khan M, Griebel R (1983) Acute spinal cord injury in the rat: comparison of three experimental techniques. Canad J Neurol Sci Le journal canadien des sciences neurologiques 10:161–165
doi: 10.1017/S031716710004484X
Kiyota T, Ingraham KL, Swan RJ, Jacobsen MT, Andrews SJ, Ikezu T (2012) AAV serotype 2/1-mediated gene delivery of anti-inflammatory interleukin-10 enhances neurogenesis and cognitive function in APP+PS1 mice. Gene Ther 19:724–733. https://doi.org/10.1038/gt.2011.126
doi: 10.1038/gt.2011.126
pubmed: 21918553
Kiyota T, Okuyama S, Swan RJ, Jacobsen MT, Gendelman HE, Ikezu T (2010) CNS expression of anti-inflammatory cytokine interleukin-4 attenuates Alzheimer's disease-like pathogenesis in APP+PS1 bigenic mice. FASEB J 24:3093–3102. https://doi.org/10.1096/fj.10-155317
doi: 10.1096/fj.10-155317
pubmed: 20371618
pmcid: 2909296
Kropff E, Yang SM, Schinder AF (2015) Dynamic role of adult-born dentate granule cells in memory processing. Curr Opin Neurobiol 35:21–26. https://doi.org/10.1016/j.conb.2015.06.002
doi: 10.1016/j.conb.2015.06.002
pubmed: 26100379
pmcid: 4641801
Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation The Journal of neuroscience : the official journal of the Society for. Neuroscience 16:2027–2033
doi: 10.1523/JNEUROSCI.16-06-02027.1996
Kuzumaki N et al (2010) Enhanced IL-1beta production in response to the activation of hippocampal glial cells impairs neurogenesis in aged mice. Synapse 64:721–728. https://doi.org/10.1002/syn.20800
doi: 10.1002/syn.20800
pubmed: 20336624
Labombarda F, Gonzalez SL, Lima A, Roig P, Guennoun R, Schumacher M, de Nicola AF (2009) Effects of progesterone on oligodendrocyte progenitors, oligodendrocyte transcription factors, and myelin proteins following spinal cord injury. Glia 57:884–897
doi: 10.1002/glia.20814
Labombarda F et al (2015) A functional progesterone receptor is required for immunomodulation, reduction of reactive gliosis and survival of oligodendrocyte precursors in the injured spinal cord. J Steroid Biochem Mol Biol 154:274–284. https://doi.org/10.1016/j.jsbmb.2015.09.011
doi: 10.1016/j.jsbmb.2015.09.011
pubmed: 26369614
Lazzaro I, Tran Y, Wijesuriya N, Craig A (2013) Central correlates of impaired information processing in people with spinal cord injury. J Clin Neurophysiol 30:59–65. https://doi.org/10.1097/WNP.0b013e31827edb0c
doi: 10.1097/WNP.0b013e31827edb0c
pubmed: 23377444
Lie DC et al (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370–1375. https://doi.org/10.1038/nature04108
doi: 10.1038/nature04108
pubmed: 16251967
Long-Smith CM, Sullivan AM, Nolan YM (2009) The influence of microglia on the pathogenesis of Parkinson's disease. Prog Neurobiol 89:277–287. https://doi.org/10.1016/j.pneurobio.2009.08.001
doi: 10.1016/j.pneurobio.2009.08.001
pubmed: 19686799
Louveau A, Nerriere-Daguin V, Vanhove B, Naveilhan P, Neunlist M, Nicot A, Boudin H (2015) Targeting the CD80/CD86 costimulatory pathway with CTLA4-Ig directs microglia toward a repair phenotype and promotes axonal outgrowth. Glia 63:2298–2312. https://doi.org/10.1002/glia.22894
doi: 10.1002/glia.22894
pubmed: 26212105
Lucassen PJ, Oomen CA, Naninck EF, Fitzsimons CP, van Dam AM, Czeh B, Korosi A (2015) Regulation of Adult Neurogenesis and Plasticity by (Early) Stress Glucocorticoids, and Inflammation. Cold Spring Harbor Perspect Biol 7:a021303. https://doi.org/10.1101/cshperspect.a021303
doi: 10.1101/cshperspect.a021303
Lyons A, Downer EJ, Crotty S, Nolan YM, Mills KH, Lynch MA (2007) CD200 ligand receptor interaction modulates microglial activation in vivo and in vitro: a role for IL-4. J Neurosci 27:8309–8313. https://doi.org/10.1523/JNEUROSCI.1781-07.2007
doi: 10.1523/JNEUROSCI.1781-07.2007
pubmed: 17670977
pmcid: 6673084
Lyons A et al (2009) Decreased neuronal CD200 expression in IL-4-deficient mice results in increased neuroinflammation in response to lipopolysaccharide. Brain Behav Immun 23:1020–1027. https://doi.org/10.1016/j.bbi.2009.05.060
doi: 10.1016/j.bbi.2009.05.060
pubmed: 19501645
Martin-Suarez S, Valero J, Muro-Garcia T, Encinas JM (2019) Phenotypical and functional heterogeneity of neural stem cells in the aged hippocampus. Aging Cell 18:e12958. https://doi.org/10.1111/acel.12958
doi: 10.1111/acel.12958
pubmed: 30989815
pmcid: 6612636
Marques SA, Garcez VF, Del Bel EA, Martinez AM (2009) A simple, inexpensive and easily reproducible model of spinal cord injury in mice: morphological and functional assessment. J Neurosci Methods 177:183–193. https://doi.org/10.1016/j.jneumeth.2008.10.015
doi: 10.1016/j.jneumeth.2008.10.015
pubmed: 19013194
Mathieu P, Piantanida AP, Pitossi F (2010) Chronic expression of transforming growth factor-beta enhances adult neurogenesis. NeuroImmuno Modul 17:200–201. https://doi.org/10.1159/000258723
doi: 10.1159/000258723
Miao EA, Rajan JV, Aderem A (2011) Caspase-1-induced pyroptotic cell death. Immunol Rev 243:206–214. https://doi.org/10.1111/j.1600-065X.2011.01044.x
doi: 10.1111/j.1600-065X.2011.01044.x
pubmed: 21884178
pmcid: 3609431
Mignone JL, Kukekov V, Chiang AS, Steindler D, Enikolopov G (2004) Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 469:311–324. https://doi.org/10.1002/cne.10964
doi: 10.1002/cne.10964
pubmed: 14730584
Moonen G et al (2016) A New Acute Impact-Compression Lumbar Spinal Cord Injury Model in the Rodent. J Neurotrauma 33:278–289. https://doi.org/10.1089/neu.2015.3937
doi: 10.1089/neu.2015.3937
pubmed: 26414192
pmcid: 4744888
Mosher KI, Wyss-Coray T (2014) Microglial dysfunction in brain aging and Alzheimer's disease. Biochem Pharmacol 88:594–604. https://doi.org/10.1016/j.bcp.2014.01.008
doi: 10.1016/j.bcp.2014.01.008
pubmed: 24445162
pmcid: 3972294
Murray RF, Asghari A, Egorov DD, Rutkowski SB, Siddall PJ, Soden RJ, Ruff R (2007) Impact of spinal cord injury on self-perceived pre- and postmorbid cognitive, emotional and physical functioning. Spinal cord 45:429–436. https://doi.org/10.1038/sj.sc.3102022
doi: 10.1038/sj.sc.3102022
pubmed: 17228355
O´Keefe J.(2007). Hippocampal neurophysiology in the behaving animal. In: The Hippocampus Book (eds) Andersen PMR, Amaral D, Bliss T, O´Keefe J. Oxford University Press Oxford, 475–548
Oomen CA, Bekinschtein P, Kent BA, Saksida LM, Bussey TJ (2014) Adult hippocampal neurogenesis and its role in cognition Wiley interdisciplinary reviews. Cognit Sci 5:573–587. https://doi.org/10.1002/wcs.1304
doi: 10.1002/wcs.1304
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
doi: 10.1093/nar/29.9.e45
Pietranera L, Saravia F, Gonzalez Deniselle MC, Roig P, Lima A, De Nicola AF (2006) Abnormalities of the hippocampus are similar in deoxycorticosterone acetate-salt hypertensive rats and spontaneously hypertensive rats. J Neuroendocrinol 18:466–474. https://doi.org/10.1111/j.1365-2826.2006.01436.x
doi: 10.1111/j.1365-2826.2006.01436.x
pubmed: 16684136
Pineda JR, Encinas JM (2016) The Contradictory Effects of Neuronal Hyperexcitation on Adult Hippocampal Neurogenesis. Front Neurosc 10:74. https://doi.org/10.3389/fnins.2016.00074
doi: 10.3389/fnins.2016.00074
Popovich PG, Stuckman S, Gienapp IE, Whitacre CC (2001) Alterations in immune cell phenotype and function after experimental spinal cord injury. J Neurotrauma 18:957–966. https://doi.org/10.1089/089771501750451866
doi: 10.1089/089771501750451866
pubmed: 11565606
Revsin Y, Rekers NV, Louwe MC, Saravia FE, De Nicola AF, de Kloet ER, Oitzl MS (2009) Glucocorticoid receptor blockade normalizes hippocampal alterations and cognitive impairment in streptozotocin-induced type 1 diabetes mice. Neuropsychopharmacology 34:747–758. https://doi.org/10.1038/npp.2008.136
doi: 10.1038/npp.2008.136
pubmed: 18784648
Rosi S et al (2009) Accuracy of hippocampal network activity is disrupted by neuroinflammation: rescue by memantine. Brain 132:2464–2477. https://doi.org/10.1093/brain/awp148
doi: 10.1093/brain/awp148
pubmed: 19531533
pmcid: 2732266
Rosi S, Ramirez-Amaya V, Vazdarjanova A, Worley PF, Barnes CA, Wenk GL (2005) Neuroinflammation alters the hippocampal pattern of behaviorally induced Arc expression. J Neurosci 25:723–731. https://doi.org/10.1523/JNEUROSCI.4469-04.2005
doi: 10.1523/JNEUROSCI.4469-04.2005
pubmed: 15659610
pmcid: 6725337
Rosi S, Vazdarjanova A, Ramirez-Amaya V, Worley PF, Barnes CA, Wenk GL (2006) Memantine protects against LPS-induced neuroinflammation, restores behaviorally-induced gene expression and spatial learning in the rat. Neuroscience 142:1303–1315. https://doi.org/10.1016/j.neuroscience.2006.08.017
doi: 10.1016/j.neuroscience.2006.08.017
pubmed: 16989956
Scheff SW, Rabchevsky AG, Fugaccia I, Main JA, Lumpp JE Jr (2003) Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J Neurotrauma 20:179–193. https://doi.org/10.1089/08977150360547099
doi: 10.1089/08977150360547099
pubmed: 12675971
Sierra A, Beccari S, Diaz-Aparicio I, Encinas JM, Comeau S, Tremblay ME (2014) Surveillance, phagocytosis, and inflammation: how never-resting microglia influence adult hippocampal neurogenesis. Neural Plast 2014:610343. https://doi.org/10.1155/2014/610343
doi: 10.1155/2014/610343
pubmed: 24772353
pmcid: 3977558
Sierra A et al (2010) Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7:483–495. https://doi.org/10.1016/j.stem.2010.08.014
doi: 10.1016/j.stem.2010.08.014
pubmed: 20887954
pmcid: 20887954
Sierra A et al (2015) Neuronal hyperactivity accelerates depletion of neural stem cells and impairs hippocampal neurogenesis. Cell Stem Cell 16:488–503. https://doi.org/10.1016/j.stem.2015.04.003
doi: 10.1016/j.stem.2015.04.003
pubmed: 25957904
pmcid: 4443499
Song H, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417:39–44. https://doi.org/10.1038/417039a
doi: 10.1038/417039a
pubmed: 11986659
Strubreither W, Hackbusch B, Hermann-Gruber M, Stahr G, Jonas HP (1997) Neuropsychological aspects of the rehabilitation of patients with paralysis from a spinal injury who also have a brain injury. Spinal Cord 35:487–492
doi: 10.1038/sj.sc.3100495
Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF (2008) Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11:901–907. https://doi.org/10.1038/nn.2156
doi: 10.1038/nn.2156
pubmed: 18622400
pmcid: 2572641
Vallieres L, Campbell IL, Gage FH, Sawchenko PE (2002) Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci 22:486–492
doi: 10.1523/JNEUROSCI.22-02-00486.2002
van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030–1034. https://doi.org/10.1038/4151030a
doi: 10.1038/4151030a
pubmed: 11875571
Walker DG, Dalsing-Hernandez JE, Campbell NA, Lue LF (2009) Decreased expression of CD200 and CD200 receptor in Alzheimer's disease: a potential mechanism leading to chronic inflammation. Exp Neurol 215:5–19. https://doi.org/10.1016/j.expneurol.2008.09.003
doi: 10.1016/j.expneurol.2008.09.003
pubmed: 18938162
Wu J et al (2014a) Isolated spinal cord contusion in rats induces chronic brain neuroinflammation, neurodegeneration, and cognitive impairment. Involv cell Cycle Activ Cell Cycle 13:2446–2458. https://doi.org/10.4161/cc.29420
doi: 10.4161/cc.29420
Wu J, Zhao Z, Kumar A, Lipinski MM, Loane DJ, Stoica BA, Faden AI (2016) Endoplasmic reticulum stress and disrupted neurogenesis in the brain are associated with cognitive impairment and depressive-like behavior after spinal cord injury. J Neurotrauma 33:1919–1935. https://doi.org/10.1089/neu.2015.4348
doi: 10.1089/neu.2015.4348
pubmed: 27050417
pmcid: 5105355
Wu J et al (2014b) Spinal cord injury causes brain inflammation associated with cognitive and affective changes: role of cell cycle pathways The Journal of neuroscience : the official journal of the Society for. Neuroscience 34:10989–11006. https://doi.org/10.1523/JNEUROSCI.5110-13.2014
doi: 10.1523/JNEUROSCI.5110-13.2014
pubmed: 25122899
pmcid: 4131014