Acute inflammation alters adult hippocampal neurogenesis in a multiple sclerosis mouse model

Journal of Neuroscience Research

Volumn 91, Issue 7, 2013, Pages 890-900

  Giannakopoulou, A ^a   Grigoriadis, N ^b   Bekiari, C ^a   Lourbopoulos, A ^b   Dori, I ^a   Tsingotjidou, A S ^a   Michaloudi, H ^a   Papadopoulos, G C ^a  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b AHEPA UNIVERSITY HOSPITAL   (Greece)

Author keywords

Apoptosis; Differentiation; Experimental autoimmune encephalomyelitis; Progenitor cells; Proliferation

Indexed keywords

BROXURIDINE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN REGION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DISEASE SEVERITY; FEMALE; IMMUNOHISTOCHEMISTRY; MOLECULAR MECHANICS; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NEUROPATHOLOGY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SUBGRANULAR ZONE;

ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CELL CYCLE; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; NEURAL STEM CELLS; NEUROGENESIS; PEPTIDE FRAGMENTS; TIME FACTORS;

EID: 84877922178     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23226     Document Type: Article

References (46)

1. Aharoni R, Arnon R, Eilam R. 2005. Neurogenesis and neuroprotection induced by peripheral immunomodulatory treatment of experimental autoimmune encephalomyelitis. J Neurosci 25:8217-8228.
2. Arnon R, Aharoni R. 2009. Neuroprotection and neurogeneration in MS and its animal model EAE effected by glatiramer acetate. J Neural Transm 116:1443-1449.
3. Attardo A, Fabel K, Krebs J, Haubensak W, Huttner WB, Kempermann G. 2010. Tis21 expression marks not only populations of neurogenic precursor cells but also new postmitotic neurons in adult hippocampal neurogenesis. Cereb Cortex 20:304-314.
4. Belarbi K, Arellano C, Ferguson R, Jopson T, Rosi S. 2012. Chronic neuroinflammation impacts the recruitment of adult-born neurons into behaviorally relevant hippocampal networks. Brain Behav Immun 26:18-23.
5. Brundula V, Rewcastle NB, Metz LM, Bernard CC, Yong VW. 2002. Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain 125:1297-1308.
6. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S, Martino G, Schwartz M. 2006. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31:149-160.
7. Calza L, Giardino L, Pozza M, Bettelli C, Micera A, Aloe L. 1998. Proliferation and phenotype regulation in the subventricular zone during experimental allergic encephalomyelitis: in vivo evidence of a role for nerve growth factor. Proc Natl Acad Sci U S A 95:3209-3214.
8. Cooper-Kuhn CM, Winkler J, Kuhn HG. 2004. Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J Neurosci Res 77:155-165.
9. Das S, Basu A. 2008. Inflammation: a new candidate in modulating adult neurogenesis. J Neurosci Res 86:1199-1208.
10. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O. 2003. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 100:13632-13637.
11. Ekdahl CT, Kokaia Z, Lindvall O. 2009. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158:1021-1029.
12. Gerber J, Bottcher T, Bering J, Bunkowski S, Bruck W, Kuhnt U, Nau R. 2003. Increased neurogenesis after experimental Streptococcus pneumoniae meningitis. J Neurosci Res 73:441-446.
13. Geurts JJ, Bo L, Roosendaal SD, Hazes T, Daniels R, Barkhof F, Witter MP, Huitinga I, van der Valk P. 2007. Extensive hippocampal demyelination in multiple sclerosis. J Neuropathol Exp Neurol 66:819-827.
14. Gold R, Linington C, Lassmann H. 2006. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 129:1953-1971.
15. Gould E, Gross CG. 2002. Neurogenesis in adult mammals: some progress and problems. J Neurosci 22:619-623.
16. Grigoriadis N, Lourbopoulos A, Lagoudaki R, Frischer JM, Polyzoidou E, Touloumi O, Simeonidou C, Deretzi G, Kountouras J, Spandou E, Kotta K, Karkavelas G, Tascos N, Lassmann H. 2011. Variable behavior and complications of autologous bone marrow mesenchymal stem cells transplanted in experimental autoimmune encephalomyelitis. Exp Neurol 230:78-89.
17. Gundersen HJ, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229-263.
18. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, et al. 1988. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis 96:379-394.
19. Guo J, Li H, Yu C, Liu F, Meng Y, Gong W, Yang H, Shen X, Ju G, Li Z, Wang J. 2010. Decreased neural stem/progenitor cell proliferation in mice with chronic/nonremitting experimental autoimmune encephalomyelitis. Neurosignals 18:1-8.
20. Huehnchen P, Prozorovski T, Klaissle P, Lesemann A, Ingwersen J, Wolf SA, Kupsch A, Aktas O, Steiner B. 2011. Modulation of adult hippocampal neurogenesis during myelin-directed autoimmune neuroinflammation. Glia 59:132-142.
21. Iwai M, Sato K, Omori N, Nagano I, Manabe Y, Shoji M, Abe K. 2002. Three steps of neural stem cells development in gerbil dentate gyrus after transient ischemia. J Cereb Blood Flow Metab 22:411-419.
22. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
23. Kuruba R, Hattiangady B, Shetty AK. 2009. Hippocampal neurogenesis and neural stem cells in temporal lobe epilepsy. Epilepsy Behav 14(Suppl 1):65-73.
24. Lugert S, Basak O, Knuckles P, Haussler U, Fabel K, Gotz M, Haas CA, Kempermann G, Taylor V, Giachino C. 2010. Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 6:445-456.
25. Magavi SS, Leavitt BR, Macklis JD. 2000. Induction of neurogenesis in the neocortex of adult mice. Nature 405:951-955.
26. Mellios K, Zacharaki T, Sophou S, Latsari M, Antonopoulos J, Dinopoulos A, Parnavelas JG, Dori I. 2009. Natural and lesion-induced apoptosis in the rat striatum during development. Brain Res 1252:30-44.
27. Nait-Oumesmar B, Picard-Riera N, Kerninon C, Decker L, Seilhean D, Hoglinger GU, Hirsch EC, Reynolds R, Baron-Van Evercooren A. 2007. Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc Natl Acad Sci U S A 104:4694-4699.
28. Papadopoulos D, Dukes S, Patel R, Nicholas R, Vora A, Reynolds R. 2009. Substantial archaeocortical atrophy and neuronal loss in multiple sclerosis. Brain Pathol 19:238-253.
29. Paxinos G, Franklin K. 2001. The mouse brain in stereotaxic coordinates. San Diego: Academic Press.
30. Picard-Riera N, Decker L, Delarasse C, Goude K, Nait-Oumesmar B, Liblau R, Pham-Dinh D, Evercooren AB. 2002. Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci U S A 99:13211-13216.
31. Pluchino S, Muzio L, Imitola J, Deleidi M, Alfaro-Cervello C, Salani G, Porcheri C, Brambilla E, Cavasinni F, Bergamaschi A, Garcia-Verdugo JM, Comi G, Khoury SJ, Martino G. 2008. Persistent inflammation alters the function of the endogenous brainstem cell compartment. Brain 131:2564-2578.
32. Rao SM, Leo GJ, Bernardin L, Unverzagt F. 1991. Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology 41:685-691.
33. Roosendaal SD, Hulst HE, Vrenken H, Feenstra HE, Castelijns JA, Pouwels PJ, Barkhof F, Geurts JJ. 2010. Structural and functional hippocampal changes in multiple sclerosis patients with intact memory function. Radiology 255:595-604.
34. Rovaris M, Filippi M, Minicucci L, Iannucci G, Santuccio G, Possa F, Comi G. 2000. Cortical/subcortical disease burden and cognitive impairment in patients with multiple sclerosis. AJNR Am J Neuroradiol 21:402-408.
35. Russo I, Barlati S, Bosetti F. 2011. Effects of neuroinflammation on the regenerative capacity of brainstem cells. J Neurochem 116:947-956.
36. Saino O, Taguchi A, Nakagomi T, Nakano-Doi A, Kashiwamura S, Doe N, Nakagomi N, Soma T, Yoshikawa H, Stern DM, Okamura H, Matsuyama T. 2010. Immunodeficiency reduces neural stem/progenitor cell apoptosis and enhances neurogenesis in the cerebral cortex after stroke. J Neurosci Res 88:2385-2397.
37. Sajad M, Chawla R, Zargan J, Umar S, Sadaqat M, Khan HA. 2011. Cytokinetics of adult rat SVZ after EAE. Brain Res 1371:140-149.
38. Schwartz M, London A, Shechter R. 2009. Boosting T-cell immunity as a therapeutic approach for neurodegenerative conditions: the role of innate immunity. Neuroscience 158:1133-1142.
39. Sophou S, Dori I, Antonopoulos J, Parnavelas JG, Dinopoulos A. 2006. Apoptosis in the rat basal forebrain during development and following lesions of connections. Eur J Neurosci 24:573-585.
40. Thornton AE, Raz N. 1997. Memory impairment in multiple sclerosis: a quantitative review. Neuropsychology 11:357-366.
41. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
42. Voloboueva LA, Giffard RG. 2011. Inflammation, mitochondria, and the inhibition of adult neurogenesis. J Neurosci Res 89:1989-1996.
43. Wang X, Xu L, Wang H, Zhan Y, Pure E, Feuerstein GZ. 2002. CD44 deficiency in mice protects brain from cerebral ischemia injury. J Neurochem 83:1172-1179.
44. West MJ, Gundersen HJ. 1990. Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296:1-22.
45. Yirmiya R, Goshen I. 2011. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 25:181-213.
46. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N, Cohen H, Kipnis J, Schwartz M. 2006. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 9:268-275.