Strategies for repair of white matter: Influence of osmolarity and microglia on proliferation and apoptosis of oligodendrocyte precursor cells in different basal culture media

Frontiers in Cellular Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Kleinsimlinghaus, Karolina ^a   Marx, Romy ^a,c   Serdar, Meray ^b   Bendix, Ivo ^b   Dietzel, Irmgard D ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

^c FEDERAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (Germany)

Author keywords

Culture medium; Cytokines; Microglia; Oligodendrocyte progenitors; Osmolarity; Proliferation

Indexed keywords

CASPASE 3; CLAUDIN 11; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN BASIC PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; DULBECCO MODIFIED EAGLE MEDIUM; IMMUNOCYTOCHEMISTRY; MICROGLIA; NEUROBASAL MEDIUM; NEWBORN; NICK END LABELING; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; OSMOLARITY; PROTEIN EXPRESSION; RAT; ROSWELL PARK MEMORIAL INSTITUTE MEDIUM; WHITE MATTER;

EID: 84891507128     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00277     Document Type: Article

References (91)

1. Agresti, C., D'Urso, D., and Levi, G. (1996). Reversible inhibitory effects of interferon-gamma and tumour necrosis factor-alpha on oligodendroglial lineage cell proliferation and differentiation in vitro. Eur. J. Neurosci. 8, 1106-1116. doi: 10.1111/j.1460-9568.1996.tb01278.x
2. Andrews, T., Zhang, P., and Bhat, N. R. (1998). TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors. J. Neurosci. Res. 54, 574-583. doi: 10.1002/(SICI)1097-4547(19981201)54:5<574::AID-JNR2>3.3. CO;2-S
3. Armstrong, R. C. (1998). Isolation and characterization of immature oligodendro-cyte lineage cells. Methods 16, 282-292. doi: 10.1006/meth.1998.0685
4. Aslam, M., Kalluri, S. R., Cepok, S., Kraus, V., Buck, D., Srivastava, R., et al. (2010). The antibody response to oligodendrocyte specific protein in multiple sclerosis. J. Neuroimmunol. 221, 81-86. doi: 10.1016/j.jneuroim.2010. 02.008
5. Back, S. A., Gan, X., Li, Y., Rosenberg, P. A., and Volpe, J. J. (1998). Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J. Neurosci. 18, 6241-6253.
6. Bambakidis, N. C., and Miller, R. H. (2004). Transplantation of oligodendrocyte precursors and sonic hedgehog results in improved function and white matter sparing in the spinal cords of adult rats after contusion. Spine J. 4, 16-26. doi: 10.1016/j.spinee.2003.07.004
7. Bansal, R., Miyake, H., Nakamura, I., Eto, H., Gotoh, A., Fujisawa, M., et al. (2002). Fibroblast growth factors and their receptors in oligodendrocyte development: implications for demyelination and remyelination. Dev. Neurosci. 24, 35-46. doi: 10.1159/000064944
8. Barres, B. A., Hart, I. K., Coles, H. S., Burne, J. F., Voyvodic, J. T., Richardson, W. D., et al. (1992). Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70, 31-46. doi: 10.1016/0092-8674(92)90531-G
9. Barres, B. A., Lazar, M. A., and Raff, M. C. (1994). A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120, 1097-1108.
10. Barres, B. A., and Raff, M. C. (1999). Axonal control of oligodendrocyte development. J. Cell Biol. 147, 1123-1128. doi: 10.1083/jcb.147.6.1123
11. Benarroch, E. E. (2009). Oligodendrocytes: susceptibility to injury and involvement in neurologic disease. Neurology 72, 1779-1785. doi: 10.1212/WNL.0b013e3181a6b123
12. Berger, R., and Garnier, Y. (1999). Pathophysiology of perinatal brain damage. Brain Res. Brain Res. Rev. 30, 107-134. doi: 10.1016/S0165-0173(99)00009-0
13. Besnard, F., Perraud, F., Sensenbrenner, M., and Labourdette, G. (1989). Effects of acidic and basic fibroblast growth factors on proliferation and maturation of cultured rat oligodendrocytes. Int. J. Dev. Neurosci. 7, 401-409. doi: 10.1016/0736-5748(89)90061-0
14. Blasi, F., Riccio, M., Brogi, A., Strazza, M., Taddei, M. L., Romagnoli, S., et al. (1999). Constitutive expression of interleukin-1beta (IL-1beta) in rat oligoden-drocytes. Biol. Chem. 380, 259-264. doi: 10.1515/BC.1999.034
15. Bogler, O., Wren, D., Barnett, S. C., Land, H., and Noble, M. (1990). Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells. Proc. Natl. Acad. Sci. U.S.A. 87, 6368-6372. doi: 10.1073/pnas.87.16.6368
16. Bottenstein, J. E., and Sato, G. H. (1979). Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. U.S.A. 76, 514-517. doi: 10.1073/pnas.76.1.514
17. Brewer, G. J., and Cotman, C. W. (1989). Survival and growth of hippocam-pal neurons in defined medium at low density: advantages of a sandwich culture technique or low oxygen. Brain Res. 494, 65-74. doi: 10.1016/0006-8993(89)90144-3
18. Brewer, G. J., Torricelli, J. R., Evege, E. K., and Price, P. J. (1993). Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35, 567-576. doi: 10.1002/jnr. 490350513
19. Bronstein, J. M., Chen, K., Tiwari-Woodruff, S., and Kornblum, H. I. (2000). Developmental expression of OSP/claudin-11. J. Neurosci. Res. 60, 284-290. doi: 10.1002/(SICI)1097-4547(20000501)60:3<284::AID-JNR2>3.0.CO;2-T
20. Buntinx, M., Moreels, M., Vandenabeele, F., Lambrichts, I., Raus, J., Steels, P., et al. (2004). Cytokine-induced cell death in human oligodendroglial cell lines: I. Synergistic effects of IFN-gamma and TNF-alpha on apoptosis. J. Neurosci. Res. 76, 834-845. doi: 10.1002/jnr.20118
21. Cammer, W. (2002). Protection of cultured oligodendrocytes against tumor necrosis factor-alpha by the antioxidants coenzyme Q(10) and N-acetyl cysteine. Brain Res. Bull. 58, 587-592. doi: 10.1016/S0361-9230(02)00830-4
22. Cammer, W., and Zhang, H. (1999). Maturation of oligodendrocytes is more sensitive to TNF alpha than is survival of precursors and immature oligodendrocytes. J. Neuroimmunol. 97, 37-42. doi: 10.1016/S0165-5728(99)00045-4
23. Canoll, P. D., Musacchio, J. M., Hardy, R., Reynolds, R., Marchionni, M. A., and Salzer, J. L. (1996). GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 17, 229-243. doi: 10.1016/S0896-6273(00)80155-5
24. Chen, Y., Balasubramaniyan, V., Peng, J., Hurlock, E. C., Tallquist, M., Li, J., et al. (2007). Isolation and culture of rat and mouse oligodendrocyte precursor cells. Nat. Protoc. 2, 1044-1051. doi: 10.1038/nprot.2007.149
25. Chen, Y., Stevens, B., Chang, J., Milbrandt, J., Barres, B. A., and Hell, J. W. (2008). NS21: re-defined and modified supplement B27 for neuronal cultures. J. Neurosci. Methods 171, 239-247. doi: 10.1016/j.jneumeth.2008.03.013
26. Chew, L. J., King, W. C., Kennedy, A., and Gallo, V. (2005). Interferon-gamma inhibits cell cycle exit in differentiating oligodendrocyte progenitor cells. Glia 52, 127-143. doi: 10.1002/glia.20232
27. Clemente, D., Ortega, M. C., Arenzana, F. J., and de Castro, F. (2011). FGF-2 and Anosmin-1 are selectively expressed in different types of multiple sclerosis lesions. J. Neurosci. 31, 14899-14909. doi: 10.1523/JNEUROSCI.1158-11.2011
28. Dammann, O., and Leviton, A. (1997). Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr. Res. 42, 1-8. doi: 10.1203/00006450-199707000-00001
29. Dincman, T. A., Beare, J. E., Ohri, S. S., and Whittemore, S. R. (2012). Isolation of cortical mouse oligodendrocyte precursor cells. J. Neurosci. Methods 209, 219-226. doi: 10.1016/j.jneumeth.2012.06.017
30. Du Plessis, A. J., and Volpe, J. J. (2002). Perinatal brain injury in the preterm and term newborn. Curr. Opin. Neurol. 15, 151-157. doi: 10.1097/00019052-200204000-00005
31. Dyer, C. A., Hickey, W. F., and Geisert, E. E. J. (1991). Myelin/oligodendrocyte-specific protein: a novel surface membrane protein that associates with micro-tubules. J. Neurosci. Res. 28, 607-613. doi: 10.1002/jnr.490280418
32. Dyer, C. A., and Matthieu, J.-M. (1994). Antibodies to myelin/oligodendrocyte-specific protein and myelin/oligodendrocyte glycoprotein signal distinct changes in the organization of cultured oligodendroglial membrane sheets. J. Neurochem. 62, 777-787. doi: 10.1046/j.1471-4159.1994.62020777.x
33. Ellison, V. J., Mocatta, T. J., Winterbourn, C. C., Darlow, B. A., Volpe, J. J., and Inder, T. E. (2005). The relationship of CSF and plasma cytokine levels to cerebral white matter injury in the premature newborn. Pediatr. Res. 57, 282-286. doi: 10.1203/01.PDR.0000148286.53572.95
34. Favrais, G., van de Looij, Y., Fleiss, B., Ramanantsoa, N., Bonnin, P., Stoltenburg-Didinger, G., et al. (2011). Systemic inflammation disrupts the developmental program of white matter. Ann. Neurol. 70, 550-565. doi: 10.1002/ana.22489
35. Feldhaus, B., Dietzel, I. D., Heumann, R., and Berger, R. (2004a). Effects of interferon-γ and tumor necrosis factor-α on survival and differentiation of oligodendrocyte progenitors. J. Soc. Gynecol. Investig. 11, 89-96. doi: 10.1016/j.jsgi.2003.08.004
36. Feldhaus, B., Dietzel, I. D., Heumann, R., and Berger, R. (2004b). Kortikoide schützen Oligodendrozyten-Vorläuferzellen vor Zytokin-induzierten Schäden. Zentralbl. Gynakol. 126, 282-285. doi: 10.1055/s-2004-822759
37. Folkerth, R. D., Keefe, R. J., Haynes, R. L., Trachtenberg, F. L., Volpe, J. J., and Kinney, H. C. (2004). Interferon-g expression in periventricular leukomalacia in the human brain. Brain Pathol. 14, 265-274. doi: 10.1111/j.1750-3639.2004.tb00063.x
38. Fu, S.-L., Hu, J.-G., Li, Y., Wang, Y.-X., Jin, J.-Q., Xui, X.-M., et al. (2007). A simplified method for generating oligodendrocyte progenitor cells from neural precursor cells isolated from the E16 rat spinal cord. Acta Neurobiol. Exp. (Wars) 67, 367-377. Available online at: http://www.ane.pl/archive.php?vol=67&no=4&id=6728
39. Furusho, M., Dupree, J. L., Nave, K.-A., and Bansal, R. (2012). Fibroblast growth factor receptor signaling in oligodendrocytes regulates myelin sheath thickness. J. Neurosci. 32, 6631-6641. doi: 10.1523/JNEUROSCI.6005-11.2012
40. Furusho, M., Kaga, Y., Ishii, A., Hébert, J. M., and Bansal, R. (2011). Fibroblast growth factor signaling is required for the generation of oligodendrocyte progenitors from the embryonic forebrain. J. Neurosci. 31, 5055-5066. doi: 10.1523/JNEUROSCI.4800-10.2011
41. Gao, L. (2006). Specification of optic nerve oligodendrocyte precursors by retinal ganglion cell axons.J. Neurosci. 26, 7619-7628. doi: 10.1523/JNEUROSCI.0855-06.2006
42. /-cyclic nucleotide 3'-phosphodiesterase (CNPase) in the developing olfactory bulb and subven-tricular zone rostral extension. J. Neurosci. Res. 73, 471-480. doi: 10.1002/ jnr.10678
43. Grinspan, J. B., Stern, J. L., Franceschini, B., and Pleasure, D. (1993). Trophic effects of basic fibroblast growth factor (bFGF) on differentiated oligodendroglia: a mechanism for regeneration of the oligodendroglial lineage. J. Neurosci. Res. 36, 672-680. doi: 10.1002/jnr.490360608
44. He, D., Luo, X., Wei, W., Xie, M., Wang, W., and Yu, Z. (2012). DCPIB, a specific inhibitor of volume-regulated anion channels (VRACs), inhibits astrocyte proliferation and cell cycle progression via G1/S arrest. J. Mol. Neurosci. 46, 249-257. doi: 10.1007/s12031-011-9524-4
45. Hewett, J. A., Hewett, S. J., Winkler, S., and Pfeiffer, S. E. (1999). Inducible nitric oxide synthase expression in cultures enriched for mature oligodendrocytes is due to microglia. J. Neurosci. Res. 56, 189-198. doi: 10.1002/(SICI)1097-4547(19990415)56:2 <189::AID-JNR8> 3.0.CO;2-B
46. Hoenicka, J., Quiñones-Lombraña, A., España-Serrano, L., Alvira-Botero, X., Kremer, L., Pérez-González, R., et al. (2010). The ANKK1 gene associated with addictions is expressed in astroglial cells and upregulated by apomorphine. Biol. Psychiatry 67, 3-11. doi: 10.1016/j.biopsych.2009.08.012
47. Hunter, S. F., and Bottenstein, J. E. (1991). O-2A glial progenitors from mature brain respond to CNS neuronal cell line-derived growth factors. J. Neurosci. Res. 28, 574-582. doi: 10.1002/jnr.490280415
48. Iseki, K., Hagino, S., Zhang, Y., Mori, T., Sato, N., Yokoya, S., et al. (2011). Altered expression pattern of testican-1 mRNA after brain injury. Biomed. Res. 32, 373-378. doi: 10.2220/biomedres.32.373
49. Ishii, A., Furusho, M., and Bansal, R. (2013). Sustained activation of ERK1/2 MAPK in oligodendrocytes and schwann cells enhances myelin growth and stimulates oligodendrocyte progenitor expansion.J. Neurosci. 33, 175-186. doi: 10.1523/JNEUROSCI.4403-12.2013
50. Ishii, A., Fyffe-Maricich, S. L., Furusho, M., Miller, R. H., and Bansal, R. (2012). ERK1/ERK2 MAPK signaling is required to increase myelin thickness independent of oligodendrocyte differentiation and initiation of myelination. J. Neurosci. 32, 8855-8864. doi: 10.1523/JNEUROSCI.0137-12.2012
51. Itoh, K. (2002). Culture of oligodendrocyte precursor cells (NG2+/O1-) and oligodendrocytes (NG2-/O1+) from embryonic rat cerebrum. Brain Res. Protoc. 10, 23-30. doi: 10.1016/S1385-299X(02)00177-0
52. Kadhim, H., Tabarki, B., Verellen, G., De Prez, C., Rona, A. M., and Sebire, G. (2001). Inflammatory cytokines in the pathogenesis of periventricular leuko-malacia. Neurology 56, 1278-1284. doi: 10.1212/WNL.56.10.1278
53. Kahn, M. A., Kumar, S., Liebl, D., Chang, R., Parada, L. F., and de Vellis, J. (1999). Mice lacking NT-3, and its receptor TrkC, exhibit profound deficiencies in CNS glial cells. Glia 26, 153-165. doi: 10.1002/(SICI)1098-1136(199904)26:2 <153::AID-GLIA6> 3.0.CO;2-Z
54. Lang, F., Busch, G. L., Ritter, M., Völkl, H., Waldegger, S., Gulbins, E., et al. (1998). Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 78, 247-306.
55. Levi, G., and Agresti, C. (1991). Cellular interactions and oligodendrocyte differentiation in vitro. Cytotechnology 5, S158. doi: 10.1007/BF00736837
56. Levi, G., Agresti, C, D'Urso, D., and Aloisi, F. (1991). Is the oligodendroglial differentiation of bipotential oligodendrocyte-type 2 astrocyte progenitors promoted by autocrine factors? Neurosci. Lett. 128, 37-41. doi: 10.1016/0304-3940(91)90755-I
57. Levi, G., Aloisi, F., and Wilkin, G. P. (1987). Differentiation of cerebellar bipotential glial precursors into oligodendrocytes in primary culture: developmental profile of surface antigens and mitotic activity. J. Neurosci. Res. 18, 407-417. doi: 10.1002/jnr.490180305
58. Lopes-Cardozo, M., Sykes, J. E., van der Pal, R. H., and van Golde, L. M. (1989). Development of oligodendrocytes. Studies of rat glial cells cultured in chemically-defined medium.J. Dev. Physiol. 12, 117-127.
59. Lü, H.-Z., Wang, Y.-X., Zou, J., Li, Y, Fu, S.-L., Jin, J.-Q., et al. (2010). Differentiation of neural precursor cell-derived oligodendrocyte progenitor cells following transplantation into normal and injured spinal cords. Differentiation 80, 228-240. doi: 10.1016/j.diff.2010.09.179
60. Mann, S. A., Versmold, B., Marx, R., Stahlhofen, S., Dietzel, I. D., Heumann, R., et al. (2008). Corticosteroids reverse cytokine-induced block of survival and differentiation of oligodendrocyte progenitor cells from rats. J. Neuroinflammation 5, 39. doi: 10.1186/1742-2094-5-39
61. McCarthy, K. D., and de Vellis, J. (1980). Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902. doi: 10.1083/jcb.85.3.890
62. McKinnon, R. D., Matsui, T., Aranda, M., and Dubois-Dalcq, M. (1991). A role for fibroblast growth factor in oligodendrocyte development. Ann. N.Y. Acad. Sci. 638, 378-386. doi: 10.1111/j.1749-6632.1991.tb49048.x
63. McKinnon, R. D., Piras, G., Ida, J. A., and Dubois-Dalcq, M. (1993). A role for TGF-beta in oligodendrocyte differentiation. J. Cell Biol. 121, 1397-1407. doi: 10.1083/jcb.121.6.1397
64. Melcangi, R. C., Cavarretta, I., Magnaghi, V., Ciusani, E., and Salmaggi, A. (2000). Corticosteroids protect oligodendrocytes from cytokine-induced cell death. Neuroreport 11, 3969-3972. doi: 10.1097/00001756-200012180-00013
65. Merchán, P., Bribián, A., Sánchez-Camacho, C., Lezameta, M., Bovolenta, P., and de Castro, F. (2007). Sonic hedgehog promotes the migration and proliferation of optic nerve oligodendrocyte precursors. Mol. Cell. Neurosci. 36, 355-368. doi: 10.1016/j.mcn.2007.07.012
66. Miller, B. A., Crum, J. M., Tovar, C. A., Ferguson, A. R., Bresnahan, J. C., and Beattie, M. S. (2007). Developmental stage of oligodendrocytes determines their response to activated microglia in vitro. J Neuroinflammation 4, 28. doi: 10.1186/1742-2094-4-28
67. Molina-Holgado, E., Vela, J. M., Arevalo-Martin, A., Almazan, G., Molina-Holgado, F., Borrell, J., et al. (2002). Cannabinoids promote oligodendrocyte progenitor survival: involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling. J. Neurosci. 22, 9742-9753. Available online at: http://www.jneurosci.org/content/22/22/9742.full
68. Mu, Q. Q., and Dyer, C. (1994). Developmental expression of MOSP in cultured oligodendrocytes. Neurochem. Res. 19, 1033-1038. doi: 10.1007/BF00968713
69. Nery, S., Wichterle, H., and Fishell, G. (2001). Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128, 527-540. Available online at: http://dev.biologists.org/content/128/4/527.abstract
70. Niu, J., Wang, L., Liu, S., Li, C., Kong, J., Shen, H.-Y., et al. (2012). An efficient and economical culture approach for the enrichment of purified oligodendrocyte progenitor cells. J. Neurosci. Methods 209, 241-249. doi: 10.1016/j.jneumeth.2012.05.032
71. Noble, M., Murray, K., Stroobant, P., Waterfield, M. D., and Riddle, P. (1988). Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 333, 560-562. doi: 10.1038/333560a0
72. Pang, Y., Campbell, L., Zheng, B., Fan, L., Cai, Z., and Rhodes, P. (2010). Lipopolysaccharide-activated microglia induce death of oligodendrocyte progenitor cells and impede their development. Neuroscience 166, 464-475. doi: 10.1016/j.neuroscience.2009.12.040
73. Pedraza, C. E., Monk, R., Lei, J., Hao, Q., and Macklin, W. B. (2008). Production, characterization, and efficient transfection of highly pure oligodendrocyte precursor cultures from mouse embryonic neural progenitors. Glia 56, 1339-1352. doi: 10.1002/glia.20702
74. Pringle, N., Collarini, E. J., Mosley, M. J., Heldin, C. H., Westermark, B., and Richardson, W. D. (1989). PDGF A chain homodimers drive proliferation of bipotential (O-2A) glial progenitor cells in the developing rat optic nerve. EMBO. J. 8, 1049-1056.
75. Raff, M. C., Lillien, L. E., Richardson, W. D., Burne, J. F., and Noble, M. D. (1988). Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture. Nature 333, 562-565. doi: 10.1038/333562a0
76. Raff, M. C., Miller, R. H., and Noble, M. (1983). A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303, 390-396. doi: 10.1038/303390a0
77. Romijn, H., van Huizen, F., and Wolters, P. (1984). Towards an improved serum-free, chemically defined medium for long-term culturing of cerebral cortex tissue. Neurosci. Biobehav. Rev. 8, 301-334. doi: 10.1016/0149-7634(84)90055-1
78. Schnitzer, J., and Schachner, M. (1982). Cell type specificity of a neural cell surface antigen recognized by the monoclonal antibody A2B5. Cell Tissue Res. 224, 625-636. doi: 10.1007/BF00213757
79. Selmaj, K., Raine, C. S., Cannella, B., and Brosnan, C. F. (1991). Identification of lymphotoxin and tumor necrosis factor in multiple sclerosis lesions. J. Clin. Invest. 87, 949-954. doi: 10.1172/JCI115102
80. Sher, F., Balasubramaniyan, V., Boddeke, E., and Copray, S. (2008). Oligodendrocyte differentiation and implantation: new insights for remyelinating cell therapy. Curr. Opin. Neurol. 21, 607-614. doi: 10.1097/WCO.0b013e32830f1e50
81. Sloane, J. A., Hinman, J. D., Lubonia, M., Hollander, W., and Abraham, C. R. (2003). Age-dependent myelin degeneration and proteolysis of oligodendrocyte proteins is associated with the activation of calpain-1 in the rhesus monkey. J. Neurochem. 84, 157-168. doi: 10.1046/j.1471-4159.2003.01541.x
82. Spittau, B., Wullkopf, L., Zhou, X., Rilka, J., Pfeifer, D., and Krieglstein, K. (2013). Endogenous transforming growth factor-beta promotes quiescence of primary microglia in vitro. Glia 61, 287-300. doi: 10.1002/glia.22435
83. Sypecka, J., and Sarnowska, A. (2013). Heterogeneity of local tissue microen-vironment influences differentiation of oligodendroglial progenitors. Folia Neuropathol. 51, 103-110. doi: 10.5114/fn.2013.35952
84. Taylor, D. L., Pirianov, G., Holland, S., McGinnity, C. J., Norman, A. L., Reali, C., et al. (2010). Attenuation of proliferation in oligodendrocyte precursor cells by activated microglia. J. Neurosci. Res. 88, 1632-1644. doi: 10.1002/jnr.22335
85. Vela, J. M., Molina-Holgado, E., Arevalo-Martin, A., Almazan, G., and Guaza, C. (2002). Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells. Mol. Cell. Neurosci. 20, 489-502. doi: 10.1006/mcne.2002.1127
86. Vondran, M. W., Clinton-Luke, P., Honeywell, J. Z., and Dreyfus, C. F. (2010). BDNF+/- mice exhibit deficits in oligodendrocyte lineage cells of the basal forebrain. Glia 58, 848-856. doi: 10.1002/glia.20969
87. Wang, Y., Imitola, J., Rasmussen, S., O'Connor, K. C., and Khoury, S. J. (2008). Paradoxical dysregulation of the neural stem cell pathway sonic hedgehog-gli1 in autoimmune encephalomyelitis and multiple sclerosis. Ann. Neurol. 64, 417-427. doi: 10.1002/ana.21457
88. Webber, D. J., van Blitterswijk, M., and Chandran, S. (2009). Neuroprotective effect of oligodendrocyte precursor cell transplantation in a long-term model of periventricular leukomalacia. Am. J. Pathol. 175, 2332-2342. doi: 10.2353/ajpath.2009.090051
89. Yan, H., and Rivkees, S. A. (2002). Hepatocyte growth factor stimulates the proliferation and migration of oligodendrocyte precursor cells. J. Neurosci. Res. 69, 597-606. doi: 10.1002/jnr.10323
90. Yang, Z., Watanabe, M., and Nishiyama, A. (2005). Optimization of oligodendro-cyte progenitor cell culture method for enhanced survival. J. Neurosci. Methods 149, 50-56. doi: 10.1016/j.jneumeth.2005.05.003
91. Zeger, M., Popken, G., Zhang, J., Xuan, S., Lu, Q. R., Schwab, M. H., et al. (2007). Insulin-like growth factor type 1 receptor signaling in the cells of oligodendro-cyte lineage is required for normal in vivo oligodendrocyte development and myelination. Glia 55, 400-411. doi: 10.1002/glia.20469