Inflammation-induced subventricular zone dysfunction leads to olfactory deficits in a targeted mouse model of multiple sclerosis

Journal of Clinical Investigation

Volumn 121, Issue 12, 2011, Pages 4722-4734

  Tepavčević, Vanja ^a,b   Lazarini, Françoise ^c,d   Alfaro Cervello, Clara ^e,f   Kerninon, Christophe ^a,b   Yoshikawa, Kazuaki ^g   Garcia Verdugo, José Manuel ^e,f   Lledo, Pierre Marie ^c,d   Nait Oumesmar, Brahim ^a,b,h   Evercooren, Anne Baron Van ^a,b,h  

^a INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^b INSERM   (France)

^c INSTITUT PASTEUR   (France)

^d CNRS   (France)

^e CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^f UNIVERSITY OF VALENCIA   (Spain)

^g OSAKA UNIVERSITY   (Japan)

^h PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN OLIGODENDROCYTE GLYCOPROTEIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL COUNT; CELL DENSITY; CELL EXPANSION; CELL LINE; CELL POPULATION; CONTROLLED STUDY; CORPUS CALLOSUM; DEMYELINATION; FEMALE; FOREBRAIN; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; OLFACTORY BULB; OLFACTORY MEMORY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMELLING; SMELLING DISORDER; SPINAL CORD; STEM CELL; SUBVENTRICULAR ZONE;

ADULT STEM CELLS; ANIMALS; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINEAGE; CORPUS CALLOSUM; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; INTERNEURONS; LATERAL VENTRICLES; MEMORY, LONG-TERM; MICE; MULTIPLE SCLEROSIS; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; OLFACTION DISORDERS; OLFACTORY BULB; OLIGODENDROGLIA; STEM CELL NICHE; TRANSCRIPTION FACTORS;

EID: 84055217299     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI59145     Document Type: Article

References (54)

1. Alvarez-Buylla A, Lim D. For the long run: maintaining germinal niches in the adult brain. Neuron. 2004;41(5):683-686. (Pubitemid 38326831)
2. Doetsch F, Caillé I, Lim D, García-Verdugo J, Alvarez- Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999;97(6):703-716. (Pubitemid 29278045)
3. Carleton A, Petreanu L, Lansford R, Alvarez-Buylla A, Lledo P. Becoming a new neuron in the adult olfactory bulb. Nat Neurosci. 2003;6(5):507-518. (Pubitemid 36514699)
4. Lazarini F, et al. Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS One. 2009;4(9):e7017.
5. Sultan S, Mandairon N, Kermen F, Garcia S, Sacquet J, Didier A. Learning-dependent neurogenesis in the olfactory bulb determines long-term olfactory memory. FASEB J. 2010;24(7):2355-2363.
6. Menn B, Garcia-Verdugo J, Yaschine C, Gonzalez- Perez O, Rowitch D, Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci. 2006;26(30):7907-7918. (Pubitemid 44315160)
7. Hack M, et al. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci. 2005; 8(7):865-872.
8. Marshall C, Novitch B, Goldman J. Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J Neurosci. 2005; 25(32):7289-7298. (Pubitemid 41129800)
9. Parras C, Hunt C, Sugimori M, Nakafuku M, Rowitch D, Guillemot F. The proneural gene Mash1 specifies an early population of telencephalic oligodendrocytes. J Neurosci. 2007;27(16):4233-4242. (Pubitemid 46640707)
10. Petryniak M, Potter G, Rowitch D, Rubenstein J. Dlx1 and Dlx2 control neuronal versus oligodendroglial cell fate acquisition in the developing forebrain. Neuron. 2007;55(3):417-433. (Pubitemid 47126261)
11. Sanai N, et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature. 2004;427(6976):740-744.
12. Curtis M, et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science. 2007;315(5816):1243-1249. (Pubitemid 46364256)
13. Bédard A, Parent A. Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res. 2004;151(1-2):159-168. (Pubitemid 38887743)
14. Franklin R, Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci. 2008;9(11):839-855.
15. Patrikios P, et al. Remyelination is extensive in a subset of multiple sclerosis patients. Brain. 2006; 129(pt 12):3165-3172. (Pubitemid 44871433)
16. Nait-Oumesmar B, et al. Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc Natl Acad Sci U S A. 2007; 104(11):4694-4699. (Pubitemid 47186287)
17. Wu C, et al. Beta4 tubulin identifies a primitive cell source for oligodendrocytes in the mammalian brain. J Neurosci. 2009;29(24):7649-7657.
18. Demarquay G, Ryvlin P, Royet JP. Olfaction and neurological diseases: a review of the literature [in French]. Rev Neurol (Paris). 2007;163(2):155-167. (Pubitemid 46328254)
19. Nait-Oumesmar B, Decker L, Lachapelle F, Avellana- Adalid V, Bachelin C, Van Evercooren A. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci. 1999;11(12):4357-4366. (Pubitemid 30009267)
20. Aguirre A, Dupree J, Mangin J, Gallo V. A functional role for EGFR signaling in myelination and remyelination. Nat Neurosci. 2007;10(8):990-1002. (Pubitemid 47185206)
21. Jablonska B, et al. Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci. 2010;13(5):541-550.
22. Picard-Riera N, et al. Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci U S A. 2002;99(20):13211- 13216.
23. Pluchino S, et al. Persistent inflammation alters the function of the endogenous brain stem cell compartment. Brain. 2008;131(pt 10):2564-2578.
24. Doetsch F, García-Verdugo J, Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 1997; 17(13):5046-5061. (Pubitemid 27263818)
25. Petreanu L, Alvarez-Buylla A. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci. 2002;22(14):6106-6113. (Pubitemid 35387653)
26. Colak D, et al. Adult neurogenesis requires Smad4- mediated bone morphogenic protein signaling in stem cells. J Neurosci. 2008;28(2):434-446.
27. Roelofs RF, et al. Adult human subventricular, subgranular, and subpial zones contain astrocytes with a specialized intermediate filament cytoskeleton. Glia. 2005;52(4):289-300. (Pubitemid 43076221)
28. Kerschensteiner M, et al. Targeting experimental autoimmune encephalomyelitis lesions to a predetermined axonal tract system allows for refined behavioral testing in an animal model of multiple sclerosis. Am J Pathol. 2004;164(4):1455-1469. (Pubitemid 38387811)
29. Robin A, et al. Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. J Cereb Blood Flow Metab. 2006; 26(1):125-134. (Pubitemid 41818076)
30. Yan Y, Sailor K, Lang B, Park S, Vemuganti R, Dempsey R. Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia. J Cereb Blood Flow Metab. 2007; 27(6):1213-1224. (Pubitemid 46808712)
31. Thored P, Wood J, Arvidsson A, Cammenga J, Kokaia Z, Lindvall O. Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke. 2007;38(11):3032-3039. (Pubitemid 350035699)
32. Whitman M, Fan W, Rela L, Rodriguez-Gil D, Greer C. Blood vessels form a migratory scaffold in the rostral migratory stream. J Comp Neurol. 2009; 516(2):94-104.
33. Gonzalez-Perez O, Jauregui-Huerta F, Galvez-Contreras AY. Immune system modulates the function of adult neural stem cells. Curr Immunol Rev. 2010;6(3):167-173.
34. Guerra-Crespo M, et al. Transforming growth factor- alpha induces neurogenesis and behavioral improvement in a chronic stroke model. Neuroscience. 2009;160(2):470-483.
35. Ekdahl CT, Kokaia Z, Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience. 2009;158(3):1021-1029.
36. Strazielle N, Ghersi-Egea JF. Choroid plexus in the central nervous system: biology and physiopathology. J Neuropathol Exp Neurol. 2000;59(7):561-574. (Pubitemid 30457787)
37. Rowitch D. Glial specification in the vertebrate neural tube. Nat Rev Neurosci. 2004;5(5):409-419. (Pubitemid 38568501)
38. Pastrana E, Cheng L, Doetsch F. Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci U S A. 2009;106(15):6387-6392.
39. Jackson E, et al. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron. 2006;51(2):187-199. (Pubitemid 44063617)
40. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo J, Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron. 2002; 36(6):1021-1034. (Pubitemid 36044505)
41. Gonzalez-Perez O, Romero-Rodriguez R, Soriano- Navarro M, Garcia-Verdugo J, Alvarez-Buylla A. Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells. 2009; 27(8):2032-2043.
42. Butovsky O, et al. Induction and blockage of oligodendrogenesis by differently activated microglia in an animal model of multiple sclerosis. J Clin Invest. 2006;116(4):905-915.
43. Butovsky O, et al. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci. 2006;31(1):149-160. (Pubitemid 43049908)
44. Prozorovski T, et al. Sirt1 contributes critically to the redox-dependent fate of neural progenitors. Nat Cell Biol. 2008;10(4):385-394.
45. Muzio L, et al. Cxcl10 enhances blood cells migration in the sub-ventricular zone of mice affected by experimental autoimmune encephalomyelitis. Mol Cell Neurosci. 2010;43(3):268-280.
46. Rasmussen S, et al. Reversible neural stem cell niche dysfunction in a model of multiple sclerosis. Ann Neurol. 2011;69(5):878-891.
47. Brown DA, Sawchenko PE. Time course and distribution of inflammatory and neurodegenerative events suggest structural bases for the pathogenesis of experimental autoimmune encephalomyelitis. J Comp Neurol. 2007;502(2):236-260. (Pubitemid 46595397)
48. Imayoshi I, et al. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci. 2008; 11(10):1153-1161.
49. Breton-Provencher V, Lemasson M, Peralta MR 3rd, Saghatelyan A. Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci. 2009; 29(48):15245-15257.
50. Linster C, Johnson B, Morse A, Yue E, Leon M. Spontaneous versus reinforced olfactory discriminations. J Neurosci. 2002;22(16):6842-6845. (Pubitemid 35379141)
51. Zivadinov R, Zorzon M, Monti Bragadin L, Pagliaro G, Cazzato G. Olfactory loss in multiple sclerosis. J Neurol Sci. 1999;168(2):127-130. (Pubitemid 29467430)
52. Doty R, Li C, Mannon L, Yousem D. Olfactory dysfunction in multiple sclerosis: relation to longitudinal changes in plaque numbers in central olfactory structures. Neurology. 1999;53(4):880-882. (Pubitemid 29448321)
53. Taupin P. Adult neurogenesis, neuroinflammation and therapeutic potential of adult neural stem cells. Int J Med Sci. 2008;5(3):127-132. (Pubitemid 351880762)
54. Kuwajima T, Nishimura I, Yoshikawa K. Necdin promotes GABAergic neuron differentiation in cooperation with Dlx homeodomain proteins. J Neurosci. 2006;26(20):5383-5392. (Pubitemid 44318390)