The effect of glia-glia interactions on oligodendrocyte precursor cell biology during development and in demyelinating diseases

Frontiers in Cellular Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Clemente, Diego ^a   Ortega, María Cristina ^a   Melero Jerez, Carolina ^a   de Castro, Fernando ^a  

^a HOSPITAL NACIONAL DE PARAPLÉJICOS   (Spain)

Author keywords

Astrocytes; Microglia; Molecular cues; Multiple sclerosis; Oligodendrogliogenesis; Remyelination

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR2; COLLAGEN TYPE 1; COLLAGEN TYPE 4; DECORIN; ENTACTIN; FERRITIN; FERROPORTIN; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBRONECTIN; INTERLEUKIN 1BETA; LAMININ; MEGALIN; NERVE CELL ADHESION MOLECULE; NEUROCAN; NEUROTROPHIC FACTOR; PLATELET DERIVED GROWTH FACTOR AA; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEIN CDC42; PROTEOCHONDROITIN SULFATE; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; SONIC HEDGEHOG PROTEIN; TENASCIN; TRANSFERRIN; UNINDEXED DRUG; VIMENTIN;

CELL DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CYTOLOGY; CYTOTOXICITY; DEMYELINATING DISEASE; EXTRACELLULAR MATRIX; GENE EXPRESSION; GLIA CELL; HUMAN; MACROGLIA; MULTIPLE SCLEROSIS; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; REMYELINIZATION; REVIEW;

EID: 84891079549     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00268     Document Type: Review

References (177)

1. Ahrendsen, J. T., and Macklin, W. (2013). Signaling mechanisms regulating myelination in the central nervous system. Neurosci. Bull. 29, 199-215. doi: 10.1007/s12264-013-1322-2
2. Araque, A., and Navarrete, M. (2010). Glial cells in neuronal network function. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 2375-2381. doi: 10.1098/rstb.2009.0313
3. Armstrong, R. C., Le, T. Q., Frost, E. E., Borke, R. C., and Vana, A. C. (2002). Absence of fibroblast growth factor 2 promotes oligodendroglial repopulation of demyelinated white matter. J. Neurosci. 22, 8574-8585.
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 oligodendrocyte progenitor maturation. Nat. Med. 11, 966-972. doi:10.1038/nm1279
5. Baer, A. S., Syed, Y. A., Kang, S. U., Mitteregger, D., Vig, R., Ffrench-Constant, C., et al. (2009). Myelin-mediated inhibition of oligodendrocyte precursor differentiation can be overcome by pharmacological modulation of Fyn-RhoA and protein kinase C signalling. Brain 132, 465-481. doi: 10.1093/brain/awn334
6. Baggiolini, M. (1998). Chemokines and leukocyte traffic. Nature 392, 565-568. doi: 10.1038/33340
7. Banati, R. B., Gehrmann, J., Schubert, P., and Kreutzberg, G. W. (1993). Cytotoxicity of microglia. Glia 7, 111-118. doi: 10.1002/glia.440070117
8. Bansal, R., Kumar, M., Murray, K., Morrison, R. S., and Pfeiffer, S. E. (1996). Regulation of FGF receptors in the oligodendrocyte lineage. Mol. Cell. Neurosci. 7, 263-275. doi: 10.1006/mcne.1996.0020
9. Barkhof, F., Bruck, W., De Groot, C. J., Bergers, E., Hulshof, S., Geurts, J., et al. (2003). Remyelinated lesions in multiple sclerosis: magnetic resonance image appearance. Arch. Neurol. 60, 1073-1081. doi: 10.1001/archneur.60.8.1073
10. Barres, B. A., and Barde, Y. (2000). Neuronal and glial cell biology. Curr. Opin. Neurobiol. 10, 642-648. doi: 10.1016/S0959-4388(00)00134-3
11. 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
12. Barres, B. A., Schmid, R., Sendnter, M., and Raff, M. C. (1993). Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118, 283-295.
13. Bauer, N. G., and Ffrench-Constant, C. (2009). Physical forces in myelination and repair: a question of balance? J. Biol. 8, 78. doi: 10.1186/jbiol169
14. Bento-Abreu, A., Velasco, A., Polo-Hernandez, E., Perez-Reyes, P. L., Tabernero, A., and Medina, J. M. (2008). Megalin is a receptor for albumin in astrocytes and is required for the synthesis of the neurotrophic factor oleic acid. J. Neurochem. 106, 1149-1159. doi: 10.1111/j.1471-4159.2008.05462.x
15. Bertrand, N., and Dahmane, N. (2006). Sonic hedgehog signaling in forebrain development and its interactions with pathways that modify its effects. Trends Cell Biol. 16, 597-605. doi: 10.1016/j.tcb.2006.09.007
16. Besnard, F., Perraud, F., Sensenbrenner, M., and Labourdette, G. (1987). Plateletderived growth factor is a mitogen for glial but not for neuronal rat brain cells in vitro. Neurosci. Lett. 73, 287-292. doi: 10.1016/0304-3940(87)90260-6
17. Block, M. L., Zecca, L., and Hong, J. S. (2007). Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8, 57-69. doi: 10.1038/nrn2038
18. 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
19. Bramow, S., Frischer, J. M., Lassmann, H., Koch-Henriksen, N., Lucchinetti, C. F., Sorensen, P. S., et al. (2010). Demyelination versus remyelination in progressive multiple sclerosis. Brain 133, 2983-2998. doi: 10.1093/brain/awq250
20. Breij, E. C., Brink, B. P., Veerhuis, R., van den Berg, C., Vloet, R., Yan, R., et al. (2008). Homogeneity of active demyelinating lesions in established multiple sclerosis. Ann. Neurol. 63, 16-25. doi: 10.1002/ana.21311
21. Bribián, A., Barallobre, M. J., Soussi-Yanicostas, N., and de Castro, F. (2006). Anosmin-1 modulates the FGF-2-dependent migration of oligodendrocyte precursors in the developing optic nerve. Mol. Cell. Neurosci. 33,2-14. doi: 10.1016/j.mcn.2006.05.009
22. Bribián, A., Esteban, P. F., Clemente, D., Soussi-Yanicostas, N., Thomas, J. L., Zalc, B., et al. (2008). A novel role for anosmin-1 in the adhesion and migration of oligodendrocyte precursors. Dev. Neurobiol. 68, 1503-1516. doi: 10.1002/dneu.20678
23. Butt, A. M., and Dinsdale, J. (2005). Fibroblast growth factor 2 induces loss of adult oligodendrocytes and myelin in vivo. Exp. Neurol. 192, 125-133. doi: 10.1016/j.expneurol.2004.11.007
24. Buttery, P. C., and Ffrench-Constant, C. (1999). Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol. Cell. Neurosci. 14, 199-212. doi: 10.1006/mcne.1999.0781
25. Cao, Y., Gunn, A. J., Bennet, L., Wu, D., George, S., Gluckman, P. D., et al. (2003). Insulin-like growth factor (IGF)-1 suppresses oligodendrocyte caspase-3 activation and increases glial proliferation after ischemia in near-term fetal sheep. J. Cereb. Blood Flow Metab. 23, 739-747. doi: 10.1097/01.WCB.0000067720.12805.6F
26. Cash, E., Zhang, Y., and Rott, O. (1993). Microglia present myelin antigens to T cells after phagocytosis of oligodendrocytes. Cell. Immunol. 147, 129-138. doi: 10.1006/cimm.1993.1053
27. Chang, M. Y., Son, H., Lee, Y. S., and Lee, S. H. (2003). Neurons and astrocytes secrete factors that cause stem cells to differentiate into neurons and astrocytes, respectively. Mol. Cell. Neurosci. 23, 414-426. doi: 10.1016/S1044-7431(03)00068-X
28. Cheepsunthorn, P., Palmer, C., and Connor, J. R. (1998). Cellular distribution of ferritin subunits in postnatal rat brain. J. Comp. Neurol. 400, 73-86. doi: 10.1002/(SICI)1096-9861(19981012)400:1<73::AID-CNE5>3.0.CO;2-Q
29. Chernausek, S. D. (1993). Insulin-like growth factor-I (IGF-I) production by astroglial cells: regulation and importance for epidermal growth factor-induced cell replication. J. Neurosci. Res. 34, 189-197. doi: 10.1002/jnr.490340206
30. Christensen, E. I., and Birn, H. (2002). Megalin and cubilin: multifunctional endocytic receptors. Nat. Rev. Mol. Cell Biol. 3, 256-266. doi:10.1038/nrm778
31. Clemente, D., Esteban, P. F., del Valle, I., Bribián, A., Soussi-Yanicostas, N., Silva, A., et al. (2008). Expression pattern of Anosmin-1 during preand postnatal rat brain development. Dev. Dyn. 237, 2518-2528. doi: 10.1002/dvdy.21659
32. 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
33. Cohen, M. M. Jr. (2003). The hedgehog signaling network. Am. J. Med. Genet. A 123, 5-28. doi: 10.1002/ajmg.a.20495
34. Compston, A., and Coles, A. (2008). Multiple sclerosis. Lancet 372, 1502-1517. doi: 10.1016/S0140-6736(08)61620-7
35. Connor, J. R., and Menzies, S. L. (1996). Relationship of iron to oligodendrocytes and myelination. Glia 17, 83-93. doi: 10.1002/(SICI)1098-1136(199606)17:2<83::AID-GLIA1>3.0.CO;2-7
36. Corley, S. M., Ladiwala, U., Besson, A., and Yong, V. W. (2001). Astrocytes attenuate oligodendrocyte death in vitro through an alpha(6) integrin-laminin-dependent mechanism. Glia 36, 281-294. doi: 10.1002/glia.1116
37. Cui, Q. L., Kuhlmann, T., Miron, V. E., Leong, S. Y., Fang, J., Gris, P., et al. (2013). Oligodendrocyte progenitor cell susceptibility to injury in multiple sclerosis. Am. J. Pathol. 183, 516-525. doi: 10.1016/j.ajpath.2013.04.016
38. Das, S., Varalakshmi, C., Kumari, A. L., Patel, M., and Khar, A. (2001). Target cell induced activation of NK cells in vitro: cytokine production and enhancement of cytotoxic function. Cancer Immunol. Immunother. 50, 428-436. doi: 10.1007/s002620100217
39. Dawson, M. R., Levine, J. M., and Reynolds, R. (2000). NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors? J. Neurosci. Res. 61, 471-479. doi: 10.1002/1097-4547(20000901)61:5<471::AID-JNR1>3.0.CO;2-N
40. de Castro, F., and Bribián, A. (2005). The molecular orchestra of the migration of oligodendrocyte precursors during development. Brain Res. Brain Res. Rev. 49, 227-241. doi: 10.1016/j.brainresrev.2004.12.034
41. de Castro, F., Bribián, A., and Ortega, M. C. (2013). Regulation of oligodendrocyte precursor migration during development, in adulthood and in pathology. Cell. Mol. Life Sci. 70, 4355-4368. doi: 10.1007/s00018-013-1365-6
42. de Castro, F., and Zalc, B. (2013). Migration of myelin-forming cells in the CNS, in Comprehensive Developmental Neuroscience: Cellular Migration and Formation of Neuronal Connections, eds J. L. R. Rubenstein and P. Rakic (Amsterdam: Elsevier), 417-429.
43. del Río-Hortega, P. (1921). Estudios sobre la neuroglía. La glía de escasas radiaciones-oligodendroglía. Boletin Real Soc. Hist. Nat. 21, 63-92.
44. Dessaud, E., McMahon, A. P., and Briscoe, J. (2008). Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135, 2489-2503. doi: 10.1242/dev.009324
45. Dode, C., and Hardelin, J. P. (2009). Kallmann syndrome. Eur. J. Hum. Genet. 17, 139-146. doi: 10.1038/ejhg.2008.206
46. Duke, V. M., Winyard, P. J., Thorogood, P., Soothill, P., Bouloux, P. M., and Woolf, A. S. (1995). KAL, a gene mutated in Kallmann's syndrome, is expressed in the first trimester of human development. Mol. Cell. Endocrinol. 110, 73-79. doi: 10.1016/0303-7207(95)03518-C
47. Durafourt, B. A., Moore, C. S., Blain, M., and Antel, J. P. (2013). Isolating, culturing, and polarizing primary human adult and fetal microglia. Methods Mol. Biol. 1041, 199-211. doi: 10.1007/978-1-62703-520-0_19
48. Durand, B., and Raff, M. (2000). A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays 22, 64-71. doi: 10.1002/(SICI)1521-1878(200001)22:1<64::AID-BIES11>3.0.CO;2-Q
49. Edgar, N., and Sibille, E. (2012). A putative functional role for oligodendrocytes in mood regulation. Transl. Psychiatry 2, e109. doi: 10.1038/tp.2012.34
50. Edwards, J. P., Zhang, X., Frauwirth, K. A., and Mosser, D. M. (2006). Biochemical and functional characterization of three activated macrophage populations. J. Leukoc. Biol. 80, 1298-1307. doi: 10.1189/jlb.0406249
51. Emery, B. (2010). Regulation of oligodendrocyte differentiation and myelination. Science 330, 779-782. doi: 10.1126/science.1190927
52. Fisher, J., Devraj, K., Ingram, J., Slagle-Webb, B., Madhankumar, A. B., Liu, X., et al. (2007). Ferritin: a novel mechanism for delivery of iron to the brain and other organs. Am. J. Physiol. Cell Physiol. 293, C641-C649. doi: 10.1152/ajpcell.00599.2006
53. Fok-Seang, J., Mathews, G. A., Ffrench-Constant, C., Trotter, J., and Fawcett, J. W. (1995). Migration of oligodendrocyte precursors on astrocytes and meningeal cells. Dev. Biol. 171, 1-15. doi: 10.1006/dbio.1995.1255
54. Franklin, R. J., and Ffrench-Constant, C. (2008). Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 9, 839-855. doi: 10.1038/nrn2480
55. Frischer, J. M., Bramow, S., Dal-Bianco, A., Lucchinetti, C. F., Rauschka, H., Schmidbauer, M., et al. (2009). The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 132, 1175-1189. doi: 10.1093/brain/awp070
56. Frohlich, N., Nagy, B., Hovhannisyan, A., and Kukley, M. (2011). Fate of neuronglia synapses during proliferation and differentiation of NG2 cells. J. Anat. 219, 18-32. doi: 10.1111/j.1469-7580.2011.01392.x
57. Frohman, E. M., Racke, M. K., and Raine, C. S. (2006). Multiple sclerosis: the plaque and its pathogenesis. N. Engl. J. Med. 354, 942-955. doi: 10.1056/NEJMra052130
58. Fruhbeis, C., Frohlich, D., Kuo, W. P., Amphornrat, J., Thilemann, S., Saab, A. S., et al. (2013). Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol. 11:e1001604. doi:10.1371/journal.pbio.1001604
59. 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
60. Furusho, M., Kaga, Y., Ishii, A., Hebert, 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
61. Fushimi, S., and Shirabe, T. (2004). Expression of insulin-like growth factors in remyelination following ethidium bromide-induced demyelination in the mouse spinal cord. Neuropathology 24, 208-218. doi: 10.1111/j.1440-1789.2004. 00561.x
62. Gao, L., and Miller, R. H. (2006). Specification of optic nerve oligodendrocyte precursors by retinal ganglion cell axons. J. Neurosci. 26, 7619-7628. doi: 10.1523/JNEUROSCI.0855-06.2006
63. Gard, A. L., Burrell, M. R., Pfeiffer, S. E., Rudge, J. S., and Williams, W. C. (1995). Astroglial control of oligodendrocyte survival mediated by PDGF and leukemia inhibitory factor-like protein. Development 121, 2187-2197.
64. Gianola, S., de Castro, F., and Rossi, F. (2009). Anosmin-1 stimulates outgrowth and branching of developing Purkinje axons. Neuroscience 158, 570-584. doi: 10.1016/j.neuroscience.2008.10.022
65. Goddard, D. R., Berry, M., and Butt, A. M. (1999). In vivo actions of fibroblast growth factor-2 and insulin-like growth factor-I on oligodendrocyte development and myelination in the central nervous system. J. Neurosci. Res. 57, 74-85. doi: 10.1002/(SICI)1097-4547(19990701)57:1<74::AID-JNR8>3.0.CO;2-O
66. Goddard, D. R., Berry, M., Kirvell, S. L., and Butt, A. M. (2001). Fibroblast growth factor-2 inhibits myelin production by oligodendrocytes in vivo. Mol. Cell. Neurosci. 18, 557-569. doi: 10.1006/mcne.2001.1025
67. Goldman, S. A., Nedergaard, M., and Windrem, M. S. (2012). Glial progenitor cellbased treatment and modeling of neurological disease. Science 338, 491-495. doi: 10.1126/science.1218071
68. González-Martínez, D., Kim, S. H., Hu, Y., Guimond, S., Schofield, J., Winyard, P., et al. (2004). Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism. J. Neurosci. 24, 10384-10392. doi: 10.1523/JNEUROSCI.3400-04.2004
69. Gudi, V., Skuljec, J., Yildiz, O., Frichert, K., Skripuletz, T., Moharregh-Khiabani, D., et al. (2011). Spatial and temporal profiles of growth factor expression during CNS demyelination reveal the dynamics of repair priming. PLoS ONE 6:e22623. doi:10.1371/journal.pone.0022623
70. Gutowski, N. J., Newcombe, J., and Cuzner, M. L. (1999). Tenascin-R and C in multiple sclerosis lesions: relevance to extracellular matrix remodelling. Neuropathol. Appl. Neurobiol. 25, 207-214. doi: 10.1046/j.1365-2990.1999.00176.x
71. Gveric, D., Cuzner, M. L., and Newcombe, J. (1999). Insulin-like growth factors and binding proteins in multiple sclerosis plaques. Neuropathol. Appl. Neurobiol. 25, 215-225. doi: 10.1046/j.1365-2990.1999.00187.x
72. Haist, V., Ulrich, R., Kalkuhl, A., Deschl, U., and Baumgartner, W. (2012). Distinct spatio-temporal extracellular matrix accumulation within demyelinated spinal cord lesions in Theiler's murine encephalomyelitis. Brain Pathol. 22, 188-204. doi: 10.1111/j.1750-3639.2011.00518.x
73. Hametner, S., Wimmer, I., Haider, L., Pfeifenbring, S., Bruck, W., and Lassmann, H. (2013). Iron and neurodegeneration in the multiple sclerosis brain. Ann. Neurol. doi:10.1002/ana.23974 [Epub ahead of print].
74. Hanisch, U. K., and Kettenmann, H. (2007). Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10, 1387-1394. doi: 10.1038/nn1997
75. Henderson, A. P., Barnett, M. H., Parratt, J. D., and Prineas, J. W. (2009). Multiple sclerosis: distribution of inflammatory cells in newly forming lesions. Ann. Neurol. 66, 739-753. doi: 10.1002/ana.21800
76. Hibbits, N., Yoshino, J., Le, T. Q., and Armstrong, R. C. (2012). Astrogliosis during acute and chronic cuprizone demyelination and implications for remyelination. ASN Neuro 4, 393-408. doi: 10.1042/AN20120062
77. Hinks, G. L., and Franklin, R. J. (1999). Distinctive patterns of PDGF-A, FGF-2, IGF-I, and TGF-beta1 gene expression during remyelination of experimentallyinduced spinal cord demyelination. Mol. Cell. Neurosci. 14,153-168. doi: 10.1006/mcne.1999.0771
78. Hsieh, C. C., and Papaconstantinou, J. (2004). Akt/PKB and p38 MAPK signaling, translational initiation and longevity in Snell dwarf mouse livers. Mech. Ageing Dev. 125, 785-798. doi: 10.1016/j.mad.2004.07.008
79. Hulet, S. W., Powers, S., and Connor, J. R. (1999). Distribution of transferrin and ferritin binding in normal and multiple sclerotic human brains. J. Neurol. Sci. 165, 48-55. doi: 10.1016/S0022-510X(99)00077-5
80. Jang, E., Lee, S., Kim, J. H., Kim, J. H., Seo, J. W., Lee, W. H., et al. (2013). Secreted protein lipocalin-2 promotes microglial M1 polarization. FASEB J. 27, 1176-1190. doi: 10.1096/fj.12-222257
81. Jeong, S. Y., and David, S. (2003). Glycosylphosphatidylinositol-anchored ceruloplasmin is required for iron efflux from cells in the central nervous system. J. Biol. Chem. 278, 27144-27148. doi: 10.1074/jbc.M301988200
82. Kandel, E. R., Schwartz, J. H., Jessell, T. M., Siegelbaum, S. A., and Hudspeth, A. J. (2013). Principles of Neural Science. New York: McGraw Hill Medical.
83. Kanekiyo, K., Inamori, K., Kitazume, S., Sato, K., Maeda, J, Higuchi, M., et al. (2013). Loss of branched O-mannosyl glycans in astrocytes accelerates remyelination. J. Neurosci. 33, 10037-10047. doi: 10.1523/JNEUROSCI.3137-12.2013
84. Kippert, A., Fitzner, D., Helenius, J., and Simons, M. (2009). Actomyosin contractility controls cell surface area of oligodendrocytes. BMC Cell Biol. 10:71. doi:10.1186i/1471-2121-10-71
85. Kotter, M. R., Li, W. W., Zhao, C., and Franklin, R. J. (2006). Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J. Neurosci. 26, 328-332. doi: 10.1523/JNEUROSCI.2615-05.2006
86. Kotter, M. R., Zhao, C., van Rooijen, N., and Franklin, R. J. (2005). Macrophagedepletion induced impairment of experimental CNS remyelination is associated with a reduced oligodendrocyte progenitor cell response and altered growth factor expression. Neurobiol. Dis. 18, 166-175. doi: 10.1016/j.nbd.2004. 09.019
87. Kuhlmann, T., Miron, V., Cui, Q., Wegner, C., Antel, J., and Bruck, W. (2008). Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131, 1749-1758. doi: 10.1093/brain/awn096
88. Laabs, T. L., Wang, H., Katagiri, Y., McCann, T., Fawcett, J. W., and Geller, H. M. (2007). Inhibiting glycosaminoglycan chain polymerization decreases the inhibitory activity of astrocyte-derived chondroitin sulfate proteoglycans. J. Neurosci. 27, 14494-14501. doi: 10.1523/JNEUROSCI.2807-07.2007
89. Lau, L. W., Keough, M. B., Haylock-Jacobs, S., Cua, R., Doring, A., Sloka, S., et al. (2012). Chondroitin sulfate proteoglycans in demyelinated lesions impair remyelination. Ann. Neurol. 72, 419-432. doi: 10.1002/ana.23599
90. Le Bras, B., Chatzopoulou, E., Heydon, K., Martinez, S., Ikenaka, K., Prestoz, L., et al. (2005). Oligodendrocyte development in the embryonic brain: the contribution of the plp lineage. Int. J. Dev. Biol. 49, 209-220. doi: 10.1387/ijdb.041963bl
91. Leveugle, B., Faucheux, B. A., Bouras, C., Nillesse, N., Spik, G., Hirsch, E. C., et al. (1996). Cellular distribution of the iron-binding protein lactotransferrin in the mesencephalon of Parkinson's disease cases. Acta Neuropathol. 91, 566-572. doi: 10.1007/s004010050468
92. LeVine, S. M. (1997). Iron deposits in multiple sclerosis and Alzheimer's disease brains. Brain Res. 760, 298-303. doi: 10.1016/S0006-8993(97)00470-8
93. Li, W. W., Setzu, A., Zhao, C., and Franklin, R. J. (2005). Minocycline-mediated inhibition of microglia activation impairs oligodendrocyte progenitor cell responses and remyelination in a non-immune model of demyelination. J. Neuroimmunol. 158, 58-66. doi: 10.1016/j.jneuroim.2004.08.011
94. Liu, X., Mashour, G. A., Webster, H. F., and Kurtz, A. (1998). Basic FGF and FGF receptor 1 are expressed in microglia during experimental autoimmune encephalomyelitis: temporally distinct expression of midkine and pleiotrophin. Glia 24, 390-397. doi: 10.1002/(SICI)1098-1136(199812)24:4<390::AIDGLIA4>3.0.CO;2-1
95. Lutz, B., Kuratani, S., Rugarli, E. I., Wawersik, S., Wong, C., Bieber, F. R., et al. (1994). Expression of the Kallmann syndrome gene in human fetal brain and in the manipulated chick embryo. Hum. Mol. Genet. 3, 1717-1723. doi: 10.1093/hmg/3.10.1717
96. Maier, O., van der Heide, T., van Dam, A. M., Baron, W., de Vries, H., and Hoekstra, D. (2005). Alteration of the extracellular matrix interferes with raft association of neurofascin in oligodendrocytes. Potential significance for multiple sclerosis? Mol. Cell. Neurosci. 28, 390-401. doi: 10.1016/j.mcn.2004.09.012
97. Mason, J. L., Langaman, C., Morell, P., Suzuki, K., and Matsushima, G. K. (2001). Episodic demyelination and subsequent remyelination within the murine central nervous system: changes in axonal calibre. Neuropathol. Appl. Neurobiol. 27, 50-58. doi: 10.1046/j.0305-1846.2001.00301.x
98. Mason, J. L., Ye, P., Suzuki, K., D'Ercole, A. J., and Matsushima, G. K. (2000). Insulinlike growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination. J. Neurosci. 20, 5703-5708.
99. Matsushima, G. K., and Morell, P. (2001). The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol. 11, 107-116. doi: 10.1111/j.1750-3639.2001. tb00385.x
100. McCarthy, R. A., and Argraves, W. S. (2003). Megalin and the neurodevelopmental biology of sonic hedgehog and retinol. J. Cell Sci. 116, 955-960. doi: 10.1242/jcs.00313
101. McCarthy, R. A., Barth, J. L., Chintalapudi, M. R., Knaak, C., and Argraves, W. S. (2002). Megalin functions as an endocytic sonic hedgehog receptor. J. Biol. Chem. 277, 25660-25667. doi: 10.1074/jbc.M201933200
102. McKinnon, R. D., Matsui, T., Dubois-Dalcq, M., and Aaronson, S. A. (1990). FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 5, 603-614. doi: 10.1016/0896-6273(90)90215-2
103. McMorris, F. A., Smith, T. M., DeSalvo, S., and Furlanetto, R. W. (1986). Insulin-like growth factor I/somatomedin C: a potent inducer of oligodendrocyte development. Proc. Natl. Acad. Sci. U.S.A. 83, 822-826. doi: 10.1073/pnas.83.3.822
104. Mekki-Dauriac, S., Agius, E., Kan, P., and Cochard, P. (2002). Bone morphogenetic proteins negatively control oligodendrocyte precursor specification in the chick spinal cord. Development 129, 5117-5130.
105. Merchán, P., Bribián, A., Sanchez-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
106. Messersmith, D. J., Murtie, J. C., Le, T. Q., Frost, E. E., and Armstrong, R. C. (2000). Fibroblast growth factor 2 (FGF2) and FGF receptor expression in an experimental demyelinating disease with extensive remyelination. J. Neurosci. Res. 62, 241-256. doi: 10.1002/1097-4547(20001015)62:2<241::AID-JNR9>3.0.CO;2-D
107. Miller, R. H., Dinsio, K., Wang, R., Geertman, R., Maier, C. E., and Hall, A. K. (2004). Patterning of spinal cord oligodendrocyte development by dorsally derived BMP4. J. Neurosci. Res. 76, 9-19. doi: 10.1002/jnr.20047
108. Miller, R. H. (1996). Oligodendrocyte origins. Trends Neurosci. 19, 92-96. doi: 10.1016/S0166-2236(96)80036-1
109. Miller, R. H. (2002). Regulation of oligodendrocyte development in the vertebrate CNS. Prog. Neurobiol. 67, 451-467. doi: 10.1016/S0301-0082(02)00058-8
110. Milner, R., Edwards, G., Streuli, C., and Ffrench-Constant, C. (1996). A role in migration for the alpha V beta 1 integrin expressed on oligodendrocyte precursors. J. Neurosci. 16, 7240-7252.
111. Miron, V. E., Boyd, A., Zhao, J. W., Yuen, T. J., Ruckh, J. M., Shadrach, J. L., et al. (2013). M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat. Neurosci. 16, 1211-1218. doi: 10.1038/nn.3469
112. Miyagi, M., Mikawa, S., Sato, T., Hasegawa, T., Kobayashi, S., Matsuyama, Y., et al. (2012). BMP2, BMP4, noggin, BMPRIA, BMPRIB, and BMPRII are differentially expressed in the adult rat spinal cord. Neuroscience 203, 12-26. doi: 10.1016/j.neuroscience.2011.12.022
113. Moore, C. S., Abdullah, S. L., Brown, A., Arulpragasam, A., and Crocker, S. J. (2011). How factors secreted from astrocytes impact myelin repair. J. Neurosci. Res. 89, 13-21. doi: 10.1002/jnr.22482
114. Morales, C. R., Zeng, J., El Alfy, M., Barth, J. L., Chintalapudi, M. R., McCarthy, R. A., et al. (2006). Epithelial trafficking of sonic hedgehog by megalin. J. Histochem. Cytochem. 54, 1115-1127. doi: 10.1369/jhc.5A6899.2006
115. Murcia-Belmonte, V., Esteban, P. F., García-González, D., and de Castro, F. (2010). Biochemical dissection of anosmin-1 interaction with FGFR1 and components of the extracellular matrix. J. Neurochem. 115, 1256-1265. doi: 10.1111/j.1471-4159.2010.07024.x
116. Nery, S., Wichterle, H., and Fishell, G. (2001). Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128, 527-540.
117. Nguyen, D., and Stangel, M. (2001). Expression of the chemokine receptors CXCR1 and CXCR2 in rat oligodendroglial cells. Brain Res. Dev. Brain Res. 128, 77-81. doi: 10.1016/S0165-3806(01)00128-6
118. Noseworthy, J. H., Lucchinetti, C., Rodríguez, M., and Weinshenker, B. G. (2000). Multiple sclerosis. N. Engl. J. Med. 343, 938-952. doi: 10.1056/NEJM200009283431307
119. O'Meara, R. W., Michalski, J. P., and Kothary, R. (2011). Integrin signaling in oligodendrocytes and its importance in CNS myelination. J. Signal Transduct. 2011, 354091. doi: 10.1155/2011/354091
120. Ortega, M. C., Cases, O., Merchan, P., Kozyraki, R., Clemente, D., and de Castro, F. (2012). Megalin mediates the influence of sonic hedgehog on oligodendrocyte precursor cell migration and proliferation during development. Glia 60, 851-866. doi: 10.1002/glia.22316
121. Passlick, S., Grauer, M., Schafer, C., Jabs, R., Seifert, G., and Steinhauser, C. (2013). Expression of the gamma2-subunit distinguishes synaptic and extrasynaptic GABA(A) receptors in NG2 cells of the hippocampus. J. Neurosci. 33, 12030-12040. doi: 10.1523/JNEUROSCI.5562-12.2013
122. Patani, R., Balaratnam, M., Vora, A., and Reynolds, R. (2007). Remyelination can be extensive in multiple sclerosis despite a long disease course. Neuropathol. Appl. Neurobiol. 33, 277-287. doi: 10.1111/j.1365-2990.2007. 00805.x
123. Patrikios, P., Stadelmann, C., Kutzelnigg, A., Rauschka, H., Schmidbauer, M., Laursen, H., et al. (2006). Remyelination is extensive in a subset of multiple sclerosis patients. Brain 129, 3165-3172. doi: 10.1093/brain/awl217
124. Piaton, G., Williams, A., Seilhean, D., and Lubetzki, C. (2009). Remyelination in multiple sclerosis. Prog. Brain Res. 175, 453-464. doi: 10.1016/S0079-6123(09)17530-1
125. Prineas, J. W., and Connell, F. (1979). Remyelination in multiple sclerosis. Ann. Neurol. 5, 22-31. doi: 10.1002/ana.410050105
126. Prineas, J. W., and Parratt, J. D. (2012). Oligodendrocytes and the early multiple sclerosis lesion. Ann. Neurol. 72, 18-31. doi: 10.1002/ana.23634
127. Qi, Y., Stapp, D., and Qiu, M. (2002). Origin and molecular specification of oligodendrocytes in the telencephalon. Trends Neurosci. 25,223-225. doi: 10.1016/S0166-2236(02)02145-8
128. 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
129. Ransohoff, R. M., and Perry, V. H. (2009). Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27, 119-145. doi: 10.1146/annurev.immunol.021908.132528
130. Rathore, K. I., Redensek, A., and David, S. (2012). Iron homeostasis in astrocytes and microglia is differentially regulated by TNF-alpha and TGF-beta1. Glia 60, 738-750. doi: 10.1002/glia.22303
131. Rawji, K. S., and Yong, V. W. (2013). The benefits and detriments of macrophages/microglia in models of multiple sclerosis. Clin. Dev. Immunol. 2013, 948976. doi: 10.1155/2013/948976
132. Ribeiro, P. F., Ventura-Antunes, L., Gabi, M., Mota, B., Grinberg, L. T., Farfel, J. M., et al. (2013). The human cerebral cortex is neither one nor many: neuronal distribution reveals two quantitatively different zones in the gray matter, three in the white matter, and explains local variations in cortical folding. Front. Neuroanat. 7:28. doi:10.3389/fnana.2013.00028
133. Richardson, W. D., Kessaris, N., and Pringle, N. (2006). Oligodendrocyte wars. Nat. Rev. Neurosci. 7, 11-18. doi: 10.1038/nrn1826
134. Richardson, W. D., Pringle, N., Mosley, M. J., Westermark, B., and Dubois-Dalcq, M. (1988). A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell 53, 309-319. doi: 10.1016/0092-8674(88)90392-3
135. Robinson, S., Tani, M., Strieter, R. M., Ransohoff, R. M., and Miller, R. H. (1998). The chemokine growth-regulated oncogene-alpha promotes spinal cord oligodendrocyte precursor proliferation. J. Neurosci. 18, 10457-10463.
136. Roth, G. A., Spada, V., Hamill, K., and Bornstein, M. B. (1995). Insulin-like growth factor I increases myelination and inhibits demyelination in cultured organotypic nerve tissue. Brain Res. Dev. Brain Res. 88, 102-108. doi: 10.1016/0165-3806(95)00088-U
137. Rottlaender, A., Villwock, H., Addicks, K., and Kuerten, S. (2011). Neuroprotective role of fibroblast growth factor-2 in experimental autoimmune encephalomyelitis. Immunology 133, 370-378. doi: 10.1111/j.1365-2567.2011.03450.x
138. Rouault, T. A., and Cooperman, S. (2006). Brain iron metabolism. Semin. Pediatr. Neurol. 13, 142-148. doi: 10.1016/j.spen.2006.08.002
139. Rowitch, D. H. (2004). Glial specification in the vertebrate neural tube. Nat. Rev. Neurosci. 5, 409-419. doi: 10.1038/nrn1389
140. Ruffini, F., Furlan, R., Poliani, P. L., Brambilla, E., Marconi, P. C., Bergami, A., et al. (2001). Fibroblast growth factor-II gene therapy reverts the clinical course and the pathological signs of chronic experimental autoimmune encephalomyelitis in C57BL/6 mice. Gene Ther. 8, 1207-1213. doi: 10.1038/sj.gt.3301523
141. Satoh, J. I., Tabunoki, H., and Yamamura, T. (2009). Molecular network of the comprehensive multiple sclerosis brain-lesion proteome. Mult. Scler. 15, 531-541. doi: 10.1177/1352458508101943
142. Schnadelbach, O., Blaschuk, O. W., Symonds, M., Gour, B. J., Doherty, P., and Fawcett, J. W. (2000). N-cadherin influences migration of oligodendrocytes on astrocyte monolayers. Mol. Cell. Neurosci. 15,288-302. doi: 10.1006/mcne.1999.0819
143. Schnadelbach, O., and Fawcett, J. W. (2001). Astrocyte influences on oligodendrocyte progenitor migration. Prog. Brain Res. 132, 97-102. doi: 10.1016/S0079-6123(01)32068-X
144. Schonberg, D. L., Goldstein, E. Z., Sahinkaya, F. R., Wei, P., Popovich, P. G., and McTigue, D. M. (2012). Ferritin stimulates oligodendrocyte genesis in the adult spinal cord and can be transferred from macrophages to NG2 cells in vivo. J. Neurosci. 32, 5374-5384. doi: 10.1523/JNEUROSCI.3517-11.2012
145. Schonberg, D. L., and McTigue, D. M. (2009). Iron is essential for oligodendrocyte genesis following intraspinal macrophage activation. Exp. Neurol. 218, 64-74. doi: 10.1016/j.expneurol.2009.04.005
146. Schulz, K., Kroner, A., and David, S. (2012). Iron efflux from astrocytes plays a role in remyelination. J. Neurosci. 32, 4841-4847. doi: 10.1523/JNEUROSCI.5328-11.2012
147. See, J., Zhang, X., Eraydin, N., Mun, S. B., Mamontov, P., Golden, J. A., et al. (2004). Oligodendrocyte maturation is inhibited by bone morphogenetic protein. Mol. Cell. Neurosci. 26, 481-492. doi: 10.1016/j.mcn.2004.04.004
148. See, J. M., and Grinspan, J. B. (2009). Sending mixed signals: bone morphogenetic protein in myelination and demyelination. J. Neuropathol. Exp. Neurol. 68, 595-604. doi: 10.1097/NEN.0b013e3181a66ad9
149. Setzu, A., Lathia, J. D., Zhao, C., Wells, K., Rao, M. S., Ffrench-Constant, C., et al. (2006). Inflammation stimulates myelination by transplanted oligodendrocyte precursor cells. Glia 54, 297-303. doi: 10.1002/glia.20371
150. Sheppard, A. M., Hamilton, S. K., and Pearlman, A. L. (1991). Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J. Neurosci. 11, 3928-3942.
151. Siebert, J. R., and Osterhout, D. J. (2011). The inhibitory effects of chondroitin sulfate proteoglycans on oligodendrocytes. J. Neurochem. 119, 176-188. doi: 10.1111/j.1471-4159.2011.07370.x
152. Siskova, Z., Yong, V. W., Nomden, A., van Strien, M., Hoekstra, D., and Baron, W. (2009). Fibronectin attenuates process outgrowth in oligodendrocytes by mislocalizing MMP-9 activity. Mol. Cell. Neurosci. 42, 234-242. doi: 10.1016/j.mcn.2009.07.005
153. 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
154. Sobel, R. A., and Ahmed, A. S. (2001). White matter extracellular matrix chondroitin sulfate/dermatan sulfate proteoglycans in multiple sclerosis. J. Neuropathol. Exp. Neurol. 60, 1198-1207.
155. Sobel, R. A., and Mitchell, M. E. (1989). Fibronectin in multiple sclerosis lesions. Am. J. Pathol. 135, 161-168.
156. Soussi-Yanicostas, N., de Castro, F., Julliard, A. K., Perfettini, I., Chedotal, A., and Petit, C. (2002). Anosmin-1, defective in the X-linked form of Kallmann syndrome, promotes axonal branch formation from olfactory bulb output neurons. Cell 109, 217-228. doi: 10.1016/S0092-8674(02)00713-4
157. Spassky, N., de Castro, F., Le, B. B., Heydon, K., Queraud-LeSaux, F., Bloch-Gallego, E., et al. (2002). Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J. Neurosci. 22, 5992-6004.
158. Stoffels, J. M., de Jonge, J. C., Stancic, M., Nomden, A., van Strien, M. E., Ma, D., et al. (2013a). Fibronectin aggregation in multiple sclerosis lesions impairs remyelination. Brain 136, 116-131. doi: 10.1093/brain/aws313
159. Stoffels, J. M., Zhao, C., and Baron, W. (2013b). Fibronectin in tissue regeneration: timely disassembly of the scaffold is necessary to complete the build. Cell. Mol. Life Sci. 70, 4243-4253. doi: 10.1007/s00018-013-1350-0
160. Tobin, J. E., Xie, M., Le, T. Q., Song, S. K., and Armstrong, R. C. (2011). Reduced axonopathy and enhanced remyelination after chronic demyelination in fibroblast growth factor 2 (Fgf2)-null mice: differential detection with diffusion tensor imaging. J. Neuropathol. Exp. Neurol. 70, 157-165. doi: 10.1097/NEN.0b013e31820937e4
161. Todorich, B., Pasquini, J. M., Garcia, C. I., Paez, P. M., and Connor, J. R. (2009). Oligodendrocytes and myelination: the role of iron. Glia 57, 467-478. doi: 10.1002/glia.20784
162. Traiffort, E., Moya, K. L., Faure, H., Hassig, R., and Ruat, M. (2001). High expression and anterograde axonal transport of aminoterminal sonic hedgehog in the adult hamster brain. Eur. J. Neurosci. 14, 839-850. doi: 10.1046/j.0953816x.2001.01708.x
163. Tripathi, R. B., Clarke, L. E., Burzomato, V., Kessaris, N., Anderson, P. N., Attwell, D., et al. (2011). Dorsally and ventrally derived oligodendrocytes have similar electrical properties but myelinate preferred tracts. J. Neurosci. 31, 6809-6819. doi: 10.1523/JNEUROSCI.6474-10.2011
164. Tsai, H. H., Frost, E., To, V., Robinson, S., Ffrench-Constant, C., Geertman, R., et al. (2002). The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration. Cell 110, 373-383. doi: 10.1016/S0092-8674(02)00838-3
165. Van Horssen, J., Bo, L., Dijkstra, C. D., and de Vries, H. E. (2006). Extensive extracellular matrix depositions in active multiple sclerosis lesions. Neurobiol. Dis. 24, 484-491. doi: 10.1016/j.nbd.2006.08.005
166. Van Horssen, J., Bo, L., Vos, C. M., Virtanen, I., and de Vries, H. E. (2005). Basement membrane proteins in multiple sclerosis-associated inflammatory cuffs: potential role in influx and transport of leukocytes. J. Neuropathol. Exp. Neurol. 64, 722-729. doi: 10.1097/01.jnen.0000173894.09553.13
167. Verkhratsky, A., and Butt, A. (2007). Glial Neurobiology. Chichester: John Wiley & Sons, Ltd. doi: 10.1002/9780470517796
168. Voss, E. V., Skuljec, J., Gudi, V., Skripuletz, T., Pul, R., Trebst, C., et al. (2012). Characterisation of microglia during deand remyelination: can they create a repair promoting environment? Neurobiol. Dis. 45,519-528. doi: 10.1016/j.nbd.2011.09.008
169. Wilczak, N., Chesik, D., Hoekstra, D., and De Keyser, J. (2008). IGF binding protein alterations on periplaque oligodendrocytes in multiple sclerosis: implications for remyelination. Neurochem. Int. 52, 1431-1435. doi: 10.1016/j.neuint.2008. 03.004
170. Williams, R., Buchheit, C. L., Berman, N. E., and LeVine, S. M. (2012). Pathogenic implications of iron accumulation in multiple sclerosis. J. Neurochem. 120, 7-25. doi: 10.1111/j.1471-4159.2011.07536.x
171. Wood, T. L., Loladze, V., Altieri, S., Gangoli, N., Levison, S. W., Brywe, K. G., et al. (2007). Delayed IGF-1 administration rescues oligodendrocyte progenitors from glutamate-induced cell death and hypoxic-ischemic brain damage. Dev. Neurosci. 29, 302-310. doi: 10.1159/000105471
172. Wynes, M. W., and Riches, D. W. (2003). Induction of macrophage insulin-like growth factor-I expression by the Th2 cytokines IL-4 and IL-13. J. Immunol. 171, 3550-3559.
173. 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
174. Zalc, B., and Fields, R. D. (2000). Do action potentials regulate myelination? Neuroscientist 6, 5-13. doi: 10.1177/107385840000600109
175. 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 oligodendrocyte lineage is required for normal in vivo oligodendrocyte development and myelination. Glia 55, 400-411. doi: 10.1002/glia. 20469
176. Zhang, X., Haaf, M., Todorich, B., Grosstephan, E., Schieremberg, H., Surguladze, N., et al. (2005). Cytokine toxicity to oligodendrocyte precursors is mediated by iron. Glia 52, 199-208. doi: 10.1002/glia.20235
177. Zhang, X., Surguladze, N., Slagle-Webb, B., Cozzi, A., and Connor, J. R. (2006). Cellular iron status influences the functional relationship between microglia and oligodendrocytes. Glia 54, 795-804. doi: 10.1002/glia.20416