Mechanisms of oligodendrocyte regeneration from ventricular-subventricular zone-derived progenitor cells in white matter diseases

Frontiers in Cellular Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Maki, Takakuni ^a   Liang, Anna C ^a   Miyamoto, Nobukazu ^a   Lo, Eng H ^a   Arai, Ken ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Demyeli nation; Multiple sclerosis; Neural stem progenitor cells; Oligodendrocyte precursor cells; Oligodendrogenesis; Subventricular zone; Vascular dementia

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CHEMOKINE RECEPTOR CXCR4; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; NOTCH1 RECEPTOR; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; STROMAL CELL DERIVED FACTOR 1; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; BRAIN DISEASE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CEREBROSPINAL FLUID; EPIGENETICS; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; EXTRACELLULAR MATRIX; GENE EXPRESSION; HISTONE ACETYLATION; HUMAN; MULTIINFARCT DEMENTIA; MULTIPLE SCLEROSIS; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; PROTEIN EXPRESSION; SUBVENTRICULAR ZONE; VASCULARIZATION;

EID: 84891548219     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00275     Document Type: Article

References (116)

1. Arai, K., and Lo, E. H. (2009a). An oligovascular niche: cerebral endothelial cells promote the survival and proliferation of oligodendrocyte precursor cells. J. Neurosci. 29, 4351-4355.doi: 10.1523/jneurosci.0035-09.2009
2. Arai, K., and Lo, E. H. (2009b). Oligovascular signaling in white matter stroke. Biol. Pharm. Bull. 32, 1639-1644.doi: 10.1248/bpb.32.1639
3. Arnett, H. A., Mason, J., Marino, M., Suzuki, K., Matsushima, G. K., and Ting, J. P. (2001). Tnf alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat. Neurosci. 4, 1116-1122.doi: 10.1038/nn738
4. Back, S. A., Tuohy, T. M., Chen, H., Wallingford, N., Craig, A., Struve, J., et al. (2005). Hyaluronan accumulates in demyelinated lesions and inhibits oligoden-drocyte progenitor maturation. Nat. Med. 11, 966-972.doi: 10.1038/nm1279
5. Barca-Mayo, O., and Lu, Q. R. (2012). Fine-tuning oligodendrocyte development by micrornas. Front. Neurosci. 6:13.doi: 10.3389/fnins.2012.00013
6. Baumann, N., and Pham-Dinh, D. (2001). Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol. Rev. 81, 871-927.
7. Bedard, C., Wallman, M. J., Pourcher, E., Parent, A., and Parent, M. (2010). Intense dopamine innervation of the subventricular zone in huntington's disease. Neu-roreport 21, 1074-1079.doi: 10.1097/wnr.0b013e32834052a6
8. Bovetti, S., Hsieh, Y. C., Bovolin, P., Perroteau, I., Kazunori, T., and Puche, A. C. (2007). Blood vessels form a scaffold for neuroblast migration in the adult olfactory bulb. J. Neurosci. 27, 5976-5980.doi: 10.1523/jneurosci.0678-07. 2007
9. Cate, H. S., Sabo, J. K., Merlo, D., Kemper, D., Aumann, T. D., Robinson, J., et al. (2010). Modulation of bone morphogenic protein signalling alters numbers of astrocytes and oligodendroglia in the subventricular zone during cuprizone-induced demyelination. J. Neurochem. 115, 11-22.doi: 10.1111/j.1471-4159. 2010.06660.x
10. Censori, B., Manara, O., Agostinis, C., Camerlingo, M., Casto, L., Galavotti, B., et al. (1996). Dementia after first stroke. Stroke 27, 1205-1210.doi: 10.1161/01.str.27. 7.1205
11. Chew, L. J., Shen, W., Ming, X., Senatorov, V. V. Jr., Chen, H. L., Cheng, Y., et al. (2011). Sry-box containing gene 17 regulates the wnt/beta-catenin signaling pathway in oligodendrocyte progenitor cells. J. Neurosci. 31, 13921-13935.doi: 10.1523/jneurosci.3343-11.2011
12. Chida, Y., Kokubo, Y., Sato, S., Kuge, A., Takemura, S., Kondo, R., et al. (2011). The alterations of oligodendrocyte, myelin in corpus callosum and cognitive dysfunction following chronic cerebral ischemia in rats. Brain Res. 1414, 22-31.doi: 10.1016/j.brainres.2011.07.026
13. Chintawar, S., Cayrol, R., Antel, J., Pandolfo, M., and Prat, A. (2009). Blood-brain barrier promotes differentiation of human fetal neural precursor cells. Stem Cells 27, 838-846.doi: 10.1002/stem.25
14. Costa, M. R., Ortega, F., Brill, M. S., Beckervordersandforth, R., Petrone, C., Schroeder, T., et al. (2011). Continuous live imaging of adult neural stem cell division and lineage progression in vitro. Development 138, 1057-1068.doi: 10. 1242/dev.061663
15. Curtis, M. A., Faull, R. L., and Eriksson, P. S. (2007). The effect of neurodegenera-tive diseases on the subventricular zone. Nat. Rev. Neurosci. 8, 712-723.doi: 10. 1038/nrn2216
16. Curtis, M. A., Low, V. F., and Faull, R. L. (2012). Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventric-ular progenitor proliferation. Dev. Neurobiol. 72, 990-1005.doi: 10.1002/dneu. 22028
17. Dimou, L., Simon, C., Kirchhoff, F., Takebayashi, H., and Gotz, M. (2008). Progeny of olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J. Neurosci. 28, 10434-10442.doi: 10.1523/jneurosci.2831-08. 2008
18. Dugas, J. C., Cuellar, T. L., Scholze, A., Ason, B., Ibrahim, A., Emery, B., et al. (2010). Dicer1 and mir-219 are required for normal oligodendrocyte differentiation and myelination. Neuron 65, 597-611.doi: 10.1016/j.neuron.2010.01. 027
19. Ekonomou, A., Ballard, C. G., Pathmanaban, O. N., Perry, R. H., Perry, E. K., Kalaria, R. N., et al. (2011). Increased neural progenitors in vascular dementia. Neurobiol. Aging 32, 2152-2161.doi: 10.1016/j.neurobiolaging.2010.01. 007
20. Falcao, A. M., Marques, F., Novais, A., Sousa, N., Palha, J. A., and Sousa, J. C. (2012). The path from the choroid plexus to the subventricular zone: go with the flow! Front. Cell. Neurosci. 6:34.doi: 10.3389/fncel.2012.00034
21. Fancy, S. P., Baranzini, S. E., Zhao, C., Yuk, D. I., Irvine, K. A., Kaing, S., et al. (2009). Dysregulation of the wnt pathway inhibits timely myelination and remyelination in the mammalian cns. Genes Dev. 23, 1571-1585.doi: 10. 1101/gad.1806309
22. Fancy, S. P., Glasgow, S. M., Finley, M., Rowitch, D. H., and Deneen, B. (2012). Evidence that nuclear factor ia inhibits repair after white matter injury. Ann. Neurol. 72, 224-233.doi: 10.1002/ana.23590
23. Farkas, E., Luiten, P. G., and Bari, F. (2007). Permanent, bilateral common carotid artery occlusion in the rat: a model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Res. Rev. 54, 162-180.doi: 10.1016/j. brainresrev.2007.01.003
24. Fuentealba, L. C., Obernier, K., and Alvarez-Buylla, A. (2012). Adult neural stem cells bridge their niche. Cell Stem Cell 10, 698-708.doi: 10.1016/j.stem.2012.05. 012
25. Fugger, L., Friese, M. A., and Bell, J. I. (2009). From genes to function: the next challenge to understanding multiple sclerosis. Nat. Rev. Immunol. 9, 408-417.doi: 10.1038/nri2554
26. Goldman, S. A., and Chen, Z. (2011). Perivascular instruction of cell genesis and fate in the adult brain. Nat. Neurosci. 14, 1382-1389.doi: 10.1038/nn.2963
27. Gonzalez-Perez, O., and Alvarez-Buylla, A. (2011). Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res. Rev. 67, 147-156.doi: 10.1016/j.brainresrev.2011.01.001
28. Gonzalez-Perez, O., Romero-Rodriguez, R., Soriano-Navarro, M., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (2009). Epidermal growth factor induces the progeny of subventricular zone type b cells to migrate and differentiate into oligodendrocytes. Stem Cells 27, 2032-2043.doi: 10.1002/stem.119
29. Hack, M. A., Saghatelyan, A., de Chevigny, A., Pfeifer, A., Ashery-Padan, R., Lledo, P. M., et al. (2005). Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat. Neurosci. 8, 865-872.doi: 10.1038/nn1479
30. Hayakawa, K., Pham, L. D., Som, A. T., Lee, B. J., Guo, S., Lo, E. H., et al. (2011). Vascular endothelial growth factor regulates the migration of oligodendrocyte precursor cells. J. Neurosci. 31, 10666-10670.doi: 10.1523/jneurosci.1944-11. 2011
31. Hayakawa, K., Seo, J. H., Pham, L. D., Miyamoto, N., Som, A. T., Guo, S., et al. (2012). Cerebral endothelial derived vascular endothelial growth factor promotes the migration but not the proliferation of oligodendrocyte precursor cells in vitro. Neurosci. Lett. 28, 42-46.doi: 10.1016/j.neulet.2012.02.004
32. Hemberger, M., Dean, W., and Reik, W. (2009). Epigenetic dynamics of stem cells and cell lineage commitment: digging waddington's canal. Nat. Rev. Mol. Cell Biol. 10, 526-537.doi: 10.1038/nrm2727
33. Ihara, M., and Tomimoto, H. (2011). Lessons from a mouse model characterizing features of vascular cognitive impairment with white matter changes. J. Aging Res. 2011, 978761.doi: 10.4061/2011/978761
34. Ihrie, R. A., and Alvarez-Buylla, A. (2011). Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 70, 674-686.doi: 10. 1016/j.neuron.2011.05.004
35. Jablonska, B., Aguirre, A., Raymond, M., Szabo, G., Kitabatake, Y., Sailor, K. A., et al. (2010). Chordin-induced lineage plasticity of adult svz neuroblasts after demyelination. Nat. Neurosci. 13, 541-550.doi: 10.1038/nn.2536
36. Jin, K., Wang, X., Xie, L., Mao, X. O., Zhu, W., Wang, Y., et al. (2006). Evidence for stroke-induced neurogenesis in the human brain. Proc. Natl. Acad. Sci. U S A 103, 13198-13202.doi: 10.1073/pnas.0603512103
37. John, G. R., Shankar, S. L., Shafit-Zagardo, B., Massimi, A., Lee, S. C., Raine, C. S., et al. (2002). Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat. Med. 8, 1115-1121.doi: 10. 1038/nm781
38. Jung, M., Schaefer, A., Steiner, I., Kempkensteffen, C., Stephan, C., Erbersdobler, A., et al. (2010). Robust microrna stability in degraded rna preparations from human tissue and cell samples. Clin. Chem. 56, 998-1006.doi: 10. 1373/clinchem.2009.141580
39. Keough, M. B., and Yong, V. W. (2013). Remyelination therapy for multiple sclerosis. Neurotherapeutics 10, 44-54.doi: 10.1007/s13311-012-0152-7
40. Kojima, T., Hirota, Y., Ema, M., Takahashi, S., Miyoshi, I., Okano, H., et al. (2010). Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells 28, 545-554.doi: 10.1002/stem.306
41. Kokmen, E., Whisnant, J. P., O'Fallon, W. M., Chu, C. P., and Beard, C. M. (1996). Dementia after ischemic stroke: a population-based study in rochester, minnesota (1960-1984). Neurology 46, 154-159.doi: 10.1212/wnl.46.1.154
42. Kokovay, E., Goderie, S., Wang, Y., Lotz, S., Lin, G., Sun, Y., et al. (2010). Adult svz lineage cells home to and leave the vascular niche via differential responses to sdf1/cxcr4 signaling. Cell Stem Cell 7, 163-173.doi: 10.1016/j.stem.2010.05.019
43. Kokovay, E., Wang, Y., Kusek, G., Wurster, R., Lederman, P., Lowry, N., et al. (2012). Vcam1 is essential to maintain the structure of the svz niche and acts as an environmental sensor to regulate svz lineage progression. Cell Stem Cell 11, 220-230.doi: 10.1016/j.stem.2012.06.016
44. Kotter, M. R., Stadelmann, C., and Hartung, H. P. (2011). Enhancing remyelination in disease-canwe wrap it up? Brain 134, 1882-1900.doi: 10.1093/brain/awr014
45. Kutzelnigg, A., Lucchinetti, C. F., Stadelmann, C., Bruck, W., Rauschka, H., Bergmann, M., et al. (2005). Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 128, 2705-2712.doi: 10.1093/brain/ awh641
46. Lazarov, O., and Marr, R. A. (2010). Neurogenesis and alzheimer's disease: at the crossroads. Exp. Neurol. 223, 267-281.doi: 10.1016/j.expneurol.2009.08.009
47. Liu, J., and Casaccia, P. (2010). Epigenetic regulation of oligodendrocyte identity. Trends Neurosci. 33, 193-201.doi: 10.1016/j.tins.2010.01.007
48. Liu, A., Han, Y. R., Li, J., Sun, D., Ouyang, M., Plummer, M. R., et al. (2007). The glial or neuronal fate choice of oligodendrocyte progenitors is modulated by their ability to acquire an epigenetic memory. J. Neurosci. 27, 7339-7343.doi: 10. 1523/jneurosci.1226-07.2007
49. Lu, Q. R., Sun, T., Zhu, Z., Ma, N., Garcia, M., Stiles, C. D., et al. (2002). Common developmental requirement for olig function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75-86.doi: 10.1016/s0092-8674(02)00678-5
50. Lu, Q. R., Yuk, D., Alberta, J. A., Zhu, Z., Pawlitzky, I., Chan, J., et al. (2000). Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bhlh proteins in the mammalian central nervous system. Neuron 25, 317-329.doi: 10. 1016/s0896-6273(00)80897-1
51. Maire, C. L., Wegener, A., Kerninon, C., and Nait Oumesmar, B. (2010). Gain-of-function of olig transcription factors enhances oligodendrogenesis and myelina-tion. Stem Cells 28, 1611-1622.doi: 10.1002/stem.480
52. Marshall, C. A., Novitch, B. G., and Goldman, J. E. (2005). Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J. Neu-rosci. 25, 7289-7298.doi: 10.1523/jneurosci.1924-05.2005
53. Menn, B., Garcia-Verdugo, J. M., Yaschine, C., Gonzalez-Perez, O., Rowitch, D., and Alvarez-Buylla, A. (2006). Origin of oligodendrocytes in the subventricular zone of the adult brain. J. Neurosci. 26, 7907-7918.doi: 10.1523/jneurosci.1299-06. 2006
54. Mercier, F., Kitasako, J. T., and Hatton, G. I. (2002). Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J. Comp. Neurol. 451, 170-188.doi: 10.1002/cne.10342
55. Merkle, F. T., Mirzadeh, Z., and Alvarez-Buylla, A. (2007). Mosaic organization of neural stem cells in the adult brain. Science 317, 381-384.doi: 10.1126/science. 1144914
56. Ming, X., Chew, L. J., and Gallo, V. (2013). Transgenic overexpression of sox17 promotes oligodendrocyte development and attenuates demyelination. J. Neurosci. 33, 12528-12542.doi: 10.1523/jneurosci.0536-13.2013
57. Mirzadeh, Z., Merkle, F. T., Soriano-Navarro, M., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (2008). Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3, 265-278.doi: 10.1016/j.stem.2008.07.004
58. Miyamoto, N., Maki, T., Pham, L. D., Hayakawa, K., Seo, J. H., Mandeville, E. T., et al. (2013a). Oxidative stress interferes with white matter renewal after prolonged cerebral hypoperfusion in mice. Stroke 44, 3516-3521.doi: 10.1161/ strokeaha.113.002813
59. Miyamoto, N., Pham, L. D., Hayakawa, K., Matsuzaki, T., Seo, J. H., Magnain, C., et al. (2013b). Age-related decline in oligodendrogenesis retards white matter repair in mice. Stroke 44, 2573-2578.doi: 10.1161/strokeaha.113.001530
60. Miyamoto, N., Tanaka, R., Shimura, H., Watanabe, T., Mori, H., Onodera, M., et al. (2010). Phosphodiesterase iii inhibition promotes differentiation and survival of oligodendrocyte progenitors and enhances regeneration of ischemic white matter lesions in the adult mammalian brain. J. Cereb. Blood Flow. Metab. 30, 299-310.doi: 10.1038/jcbfm.2009.210
61. Nait-Oumesmar, B., Decker, L., Lachapelle, F., Avellana-Adalid, V., Bachelin, C., and Baron-Van Evercooren, A. (1999). Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur. J. Neurosci. 11, 4357-4366.doi: 10.1046/j.1460-9568. 1999.00873.x
62. Nait-Oumesmar, B., Picard-Riera, N., Kerninon, C., and Baron-Van Evercooren, A. (2008). The role of svz-derived neural precursors in demyelinating diseases: from animal models to multiple sclerosis. J. Neurol. Sci. 265, 26-31.doi: 10. 1016/j.jns.2007.09.032
63. Nait-Oumesmar, B., Picard-Riera, N., Kerninon, C., Decker, L., Seilhean, D., Hoglinger, G. U., et al. (2007). Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc. Natl. Acad. Sci. U S A 104, 4694-4699.doi: 10.1073/pnas.0606835104
64. Nakagomi, T., Molnar, Z., Nakano-Doi, A., Taguchi, A., Saino, O., Kubo, S., et al. (2011). Ischemia-induced neural stem/progenitor cells in the pia mater following cortical infarction. Stem Cells Dev. 20, 2037-2051.doi: 10.1089/scd. 2011.0279
65. Nakagomi, T., Molnar, Z., Taguchi, A., Nakano-Doi, A., Lu, S., Kasahara, Y., et al. (2012). Leptomeningeal-derived doublecortin-expressing cells in poststroke brain. Stem Cells Dev. 21, 2350-2354.doi: 10.1089/scd.2011.0657
66. Nakagomi, T., Taguchi, A., Fujimori, Y., Saino, O., Nakano-Doi, A., Kubo, S., et al. (2009). Isolation and characterization of neural stem/progenitor cells from post-stroke cerebral cortex in mice. Eur. J. Neurosci. 29, 1842-1852.doi: 10.1111/j. 1460-9568.2009.06732.x
67. Nakahara, J., Kanekura, K., Nawa, M., Aiso, S., and Suzuki, N. (2009). Abnormal expression of tip30 and arrested nucleocytoplasmic transport within oligoden-drocyte precursor cells in multiple sclerosis. J. Clin. Invest. 119, 169-181.doi: 10. 1172/JCI35440
68. Nakatani, H., Martin, E., Hassani, H., Clavairoly, A., Maire, C. L., Viadieu, A., et al. (2013). Ascl1/mash1 promotes brain oligodendrogenesis during myelination and remyelination. J. Neurosci. 33, 9752-9768.doi: 10.1523/jneurosci.0805-13. 2013
69. Napoli, I., and Neumann, H. (2010). Protective effects of microglia in multiple sclerosis. Exp. Neurol. 225, 24-28.doi: 10.1016/j.expneurol.2009.04.024
70. Ni, J. W., Matsumoto, K., Li, H. B., Murakami, Y., and Watanabe, H. (1995). Neu-ronal damage and decrease of central acetylcholine level following permanent occlusion of bilateral common carotid arteries in rat. Brain Res. 673, 290-296.doi: 10.1016/0006-8993(94)01436-l
71. Nicolay, D. J., Doucette, J. R., and Nazarali, A. J. (2007). Transcriptional control of oligodendrogenesis. Glia 55, 1287-1299.doi: 10.1002/glia.20540
72. Nunes, M. C., Roy, N. S., Keyoung, H. M., Goodman, R. R., McKhann, G. 2nd, Jiang, L., et al. (2003). Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat. Med. 9, 439-447.doi: 10.1038/nm837
73. Ohab, J. J., Fleming, S., Blesch, A., and Carmichael, S. T. (2006). A neurovascular niche for neurogenesis after stroke. J. Neurosci. 26, 13007-13016.doi: 10. 1523/jneurosci.4323-06.2006
74. Ohira, K., Furuta, T., Hioki, H., Nakamura, K. C., Kuramoto, E., Tanaka, Y., et al. (2010). Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells. Nat. Neurosci. 13, 173-179.doi: 10.1038/nn.2473
75. Olah, M., Amor, S., Brouwer, N., Vinet, J., Eggen, B., Biber, K., et al. (2012). Identification of a microglia phenotype supportive of remyelination. Glia 60, 306-321.doi: 10.1002/glia.21266
76. Ortega, F., Costa, M. R., Simon-Ebert, T., Schroeder, T., Gotz, M., and Berninger, B. (2011). Using an adherent cell culture of the mouse subependymal zone to study the behavior of adult neural stem cells on a single-cell level. Nat. Protoc. 6, 1847-1859.doi: 10.1038/nprot.2011.404
77. Ortega, F., Gascon, S., Masserdotti, G., Deshpande, A., Simon, C., Fischer, J., et al. (2013). Oligodendrogliogenic and neurogenic adult subependymal zone neural stem cells constitute distinct lineages and exhibit differential responsiveness to wnt signalling. Nat. Cell Biol. 15, 602-613.doi: 10.1038/ncb2736
78. Parras, C. M., Hunt, C., Sugimori, M., Nakafuku, M., Rowitch, D., and Guillemot, F. (2007). The proneural gene mash1 specifies an early population of telencephalic oligodendrocytes. J. Neurosci. 27, 4233-4242.doi: 10.1523/jneurosci.0126-07. 2007
79. Paus, T., Zijdenbos, A., Worsley, K., Collins, D. L., Blumenthal, J., Giedd, J. N., et al. (1999). Structural maturation of neural pathways in children and adolescents: in vivo study. Science 283, 1908-1911.doi: 10.1126/science.283.5409. 1908
80. Picard-Riera, N., Decker, L., Delarasse, C., Goude, K., Nait-Oumesmar, B., Liblau, R., et al. (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.doi: 10.1073/pnas. 192314199
81. Plane, J. M., Andjelkovic, A. V., Keep, R. F., and Parent, J. M. (2010). Intact and injured endothelial cells differentially modulate postnatal murine forebrain neural stem cells. Neurobiol. Dis. 37, 218-227.doi: 10.1016/j.nbd.2009.10.008
82. Potzner, M. R., Griffel, C., Lutjen-Drecoll, E., Bosl, M. R., Wegner, M., and Sock, E. (2007). Prolonged sox4 expression in oligodendrocytes interferes with normal myelination in the central nervous system. Mol. Cell Biol. 27, 5316-5326.doi: 10. 1128/mcb.00339-07
83. Pozniak, C. D., Langseth, A. J., Dijkgraaf, G. J., Choe, Y., Werb, Z., and Pleasure, S. J. (2010). Sox10 directs neural stem cells toward the oligodendrocyte lineage by decreasing suppressor of fused expression. Proc. Natl. Acad. Sci. U S A 107, 21795-21800.doi: 10.1073/pnas.1016485107
84. Rasmussen, S., Imitola, J., Ayuso-Sacido, A., Wang, Y., Starossom, S. C., Kivisakk, P., et al. (2011). Reversible neural stem cell niche dysfunction in a model of multiple sclerosis. Ann. Neurol. 69, 878-891.doi: 10.1002/ana.22299
85. Rasmussen, S., Wang, Y., Kivisakk, P., Bronson, R. T., Meyer, M., Imitola, J., et al. (2007). Persistent activation of microglia is associated with neuronal dysfunction of callosal projecting pathways and multiple sclerosis-like lesions in relapsing-remitting experimental autoimmune encephalomyelitis. Brain 130, 2816-2829.doi: 10.1093/brain/awm219
86. Relucio, J., Menezes, M. J., Miyagoe-Suzuki, Y., Takeda, S., and Colognato, H. (2012). Laminin regulates postnatal oligodendrocyte production by promoting oligodendrocyte progenitor survival in the subventricular zone. Glia 60, 1451-1467.doi: 10.1002/glia.22365
87. Roberts, R., Gallagher, J., Spooncer, E., Allen, T. D., Bloomfield, F., and Dexter, T. M. (1988). Heparan sulphate bound growth factors: a mechanism for stromal cell mediated haemopoiesis. Nature 332, 376-378.doi: 10.1038/332376a0
88. Saha, B., Peron, S., Murray, K., Jaber, M., and Gaillard, A. (2013). Cortical lesion stimulates adult subventricular zone neural progenitor cell proliferation and migration to the site of injury. Stem Cell Res. 11, 965-977.doi: 10.1016/j.scr. 2013.06.006
89. Samanta, J., and Kessler, J. A. (2004). Interactions between id and olig proteins mediate the inhibitory effects of bmp4 on oligodendroglial differentiation. Development 131, 4131-4142.doi: 10.1242/dev.01273
90. Sawamoto, K., Wichterle, H., Gonzalez-Perez, O., Cholfin, J. A., Yamada, M., Spassky, N., et al. (2006). New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311, 629-632.doi: 10.1126/science.1119133
91. Scholz, J., Klein, M. C., Behrens, T. E., and Johansen-Berg, H. (2009). Training induces changes in white-matter architecture. Nat. Neurosci. 12, 1370-1371.doi: 10.1038/nn.2412
92. Shen, Q., Goderie, S. K., Jin, L., Karanth, N., Sun, Y., Abramova, N., et al. (2004). Endothelial cells stimulate self-renewal and expand neurogene-sis of neural stem cells. Science 304, 1338-1340.doi: 10.1126/science.109 5505
93. Shen, S., Li, J., and Casaccia-Bonnefil, P. (2005). Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain. J. Cell. Biol. 169, 577-589.doi: 10.1083/jcb.200412101
94. Shen, Q., Wang, Y., Kokovay, E., Lin, G., Chuang, S. M., Goderie, S. K., et al. (2008). Adult svz stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3, 289-300.doi: 10.1016/j.stem.2008.07.026
95. Shibata, M., Ohtani, R., Ihara, M., and Tomimoto, H. (2004). White matter lesions and glial activation in a novel mouse model of chronic cerebral hypoperfusion. Stroke 35, 2598-2603.doi: 10.1161/01.str.0000143725.19053.60
96. Shibata, M., Yamasaki, N., Miyakawa, T., Kalaria, R. N., Fujita, Y., Ohtani, R., et al. (2007). Selective impairment of working memory in a mouse model of chronic cerebral hypoperfusion. Stroke 38, 2826-2832.doi: 10.1161/strokeaha. 107.490151
97. Sloane, J. A., Batt, C., Ma, Y., Harris, Z. M., Trapp, B., and Vartanian, T. (2010). Hyaluronan blocks oligodendrocyte progenitor maturation and remyelination through tlr2. Proc. Natl. Acad. Sci. U S A 107, 11555-11560.doi: 10.1073/pnas. 1006496107
98. Snapyan, M., Lemasson, M., Brill, M. S., Blais, M., Massouh, M., Ninkovic, J., et al. (2009). Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J. Neurosci. 29, 4172-4188.doi: 10.1523/jneurosci.4956-08.2009
99. Sospedra, M., and Martin, R. (2005). Immunology of multiple sclerosis. Annu. Rev. Immunol. 23, 683-747.doi: 10.1146/annurev.immunol.23.021704.115707
100. Soundarapandian, M. M., Selvaraj, V., Lo, U. G., Golub, M. S., Feldman, D. H., Pleasure, D. E., et al. (2011). Zfp488 promotes oligodendrocyte differentiation of neural progenitor cells in adult mice after demyelination. Sci. Rep. 1:2.doi: 10. 1038/srep00002
101. Sugimori, M., Nagao, M., Bertrand, N., Parras, C. M., Guillemot, F., and Nakafuku, M. (2007). Combinatorial actions of patterning and hlh transcription factors in the spatiotemporal control of neurogenesis and gliogenesis in the developing spinal cord. Development 134, 1617-1629.doi: 10.1242/dev.001255
102. Tavazoie, M., Van der Veken, L., Silva-Vargas, V., Louissaint, M., Colonna, L., Zaidi, B., et al. (2008). Specialized vascular niche for adult neural stem cells. Cell Stem Cell 3, 279-288.doi: 10.1016/j.stem.2008.07.025
103. Teng, H., Zhang, Z. G., Wang, L., Zhang, R. L., Zhang, L., Morris, D., et al. (2008). Coupling of angiogenesis and neurogenesis in cultured endothelial cells and neural progenitor cells after stroke. J. Cereb. Blood Flow. Metab. 28, 764-771.doi: 10.1038/sj.jcbfm.9600573
104. Viswanathan, A., Rocca, W. A., and Tzourio, C. (2009). Vascular risk factors and dementia: how to move forward? Neurology 72, 368-374.doi: 10.1212/01.wnl. 0000341271.90478.8e
105. Wakita, H., Tomimoto, H., Akiguchi, I., and Kimura, J. (1994). Glial activation and white matter changes in the rat brain induced by chronic cerebral hypoperfu-sion: an immunohistochemical study. Acta Neuropathol. 87, 484-492.doi: 10. 1007/bf00294175
106. Wakita, H., Tomimoto, H., Akiguchi, I., Matsuo, A., Lin, J. X., Ihara, M., et al. (2002). Axonal damage and demyelination in the white matter after chronic cerebral hypoperfusion in the rat. Brain Res. 924, 63-70.doi: 10.1016/s0006-8993(01)03223-1
107. Wang, S. Z., Dulin, J., Wu, H., Hurlock, E., Lee, S. E., Jansson, K., et al. (2006). An oligodendrocyte-specific zinc-finger transcription regulator cooperates with olig2 to promote oligodendrocyte differentiation. Development 133, 3389-3398.doi: 10.1242/dev.02522
108. Wang, S., Sdrulla, A. D., diSibio, G., Bush, G., Nofziger, D., Hicks, C., et al. (1998). Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21, 63-75.doi: 10.1016/s0896-6273(00)80515-2
109. Whitman, M. C., Fan, W., Rela, L., Rodriguez-Gil, D. J., and Greer, C. A. (2009). Blood vessels form a migratory scaffold in the rostral migratory stream. J. Comp. Neurol. 516, 94-104.doi: 10.1002/cne.22093
110. Wu, M., Hernandez, M., Shen, S., Sabo, J. K., Kelkar, D., Wang, J., et al. (2012). Differential modulation of the oligodendrocyte transcriptome by sonic hedgehog and bone morphogenetic protein 4 via opposing effects on histone acetylation. J. Neurosci. 32, 6651-6664.doi: 10.1523/jneurosci.4876-11.2012
111. Yayon, A., Klagsbrun, M., Esko, J. D., Leder, P., and Ornitz, D. M. (1991). Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64, 841-848.doi: 10.1016/0092-8674(91)90512-w
112. Ye, F., Chen, Y., Hoang, T., Montgomery, R. L., Zhao, X. H., Bu, H., et al. (2009). Hdac1 and hdac2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-tcf interaction. Nat. Neurosci. 12, 829-838.doi: 10.1038/nn. 2333
113. Young, K. M., Psachoulia, K., Tripathi, R. B., Dunn, S. J., Cossell, L., Attwell, D., et al. (2013). Oligodendrocyte dynamics in the healthy adult cns: evidence for myelin remodeling. Neuron 77, 873-885.doi: 10.1016/j.neuron.2013.01.006
114. Zhao, X., He, X., Han, X., Yu, Y., Ye, F., Chen, Y., et al. (2010). Microrna-mediated control of oligodendrocyte differentiation. Neuron 65, 612-626.doi: 10.1016/j. neuron.2010.02.018
115. Zhou, Q., and Anderson, D. J. (2002). The bhlh transcription factors olig2 and olig1 couple neuronal and glial subtype specification. Cell 109, 61-73.doi: 10. 1016/s0092-8674(02)00677-3
116. Zuchero, J. B., and Barres, B. A. (2013). Intrinsic and extrinsic control of oligoden-drocyte development. Curr. Opin. Neurobiol. 23, 914-920.doi: 10.1016/j.conb. 2013.06.005