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Canadian Association of Neurosciences Review: Regulation of Myelination by Trophic Factors and Neuron-Glial Signaling

Published online by Cambridge University Press:  02 December 2014

Giorgia Melli
Affiliation:
The Neuromuscular Diseases Unit, IRCSS Foundation Neurological Institute Carlo Besta, via Celoria, 11 20133 - Milan, Italy
Ahmet Höke
Affiliation:
Department of Neurology and Neuroscience, Johns Hopkins University, School of Medicine, Baltimore, MD, USA
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Abstract

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Myelination in the nervous system is a tightly regulated process that is mediated by both soluble and non-soluble factors acting on axons and glial cells. This process is bi-directional and involves a variety of neurotrophic and gliotrophic factors acting in paracrine and autocrine manners. Neuron-derived trophic factors play an important role in the control of early proliferation and differentiation of myelinating glial cells. At later stages of development, same molecules may play a different role and act as inducers of myelination rather than cell survival signals for myelinating glial cells. In return, myelinating glial cells provide trophic support for axons and protect them from injury. Chronic demyelination leads to secondary axonal degeneration that is responsible for long-term disability in primary demyelinating diseases such as multiple sclerosis and inherited demyelinating peripheral neuropathies. A better understanding of the molecular mechanisms controlling myelination may yield novel therapeutic targets for demyelinating nervous system disorders.

Résumé:

RÉSUMÉ:

Régulation de la myélinisation par des facteurs trophiques et par la signalisation de la névroglie. La myélinisation du système nerveux est un processus étroitement régulé, qui est médié par des facteurs solubles et non solubles agissant sur les axones et les cellules gliales. Ce processus est bidirectionnel et implique des facteurs neurotrophes et gliotrophes variés agissant de façon paracrine et autocrine. Des facteurs trophiques dérivés des neurones jouent un rôle important dans le contrôle de la prolifération et de la différenciation précoce des cellules gliales myélinisantes. Àdes étapes ultérieures du développement, les mêmes acteurs peuvent jouer un rôle différent et agir comme inducteurs de la myélinisation plutôt que dans la signalisation de la survie cellulaire des cellules gliales myélinisantes. En retour, les cellules gliales myélinisantes fournissent un support trophique aux axones et les protègent de lésions. Une démyélinisation chronique entraî une dégénérescence axonale secondaire qui est responsable de l'invalidité à long terme observée dans les maladies démyélinisantes primaires comme la sclérose en plaques et les neuropathies périphériques démyélinisantes héréditaires. Une meilleure compréhension des mécanismes moléculaires contrôlant la myélinisation pourrait identifier des cibles thérapeutiques nouvelles pour le traitement des maladies démyélinisantes du système nerveux.

Type
Original Articles
Copyright
Copyright © The Canadian Journal of Neurological 2007

References

1. Baumann, N, Pham-Dinh, D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev. 2001 Apr;81(2):871927.CrossRefGoogle ScholarPubMed
2. Sherman, DL, Brophy, PJ. Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci. 2005 Sep;6(9):68390.CrossRefGoogle ScholarPubMed
3. Jessen, KR, Mirsky, R. Signals that determine Schwann cell identity. J Anat. 2002 Apr;200(4):36776.CrossRefGoogle ScholarPubMed
4. Jessen, KR, Mirsky, R. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci. 2005 Sep;6(9):67182.CrossRefGoogle ScholarPubMed
5. Mirsky, R, Jessen, KR, Brennan, A, Parkinson, D, Dong, Z, Meier, C, et al. Schwann cells as regulators of nerve development. J Physiol Paris. 2002 Jan-Mar;96(1-2):1724.CrossRefGoogle ScholarPubMed
6. Nave, KA, Salzer, JL. Axonal regulation of myelination by neuregulin 1. Curr Opin Neurobiol. 2006 Oct;16(5):492500.CrossRefGoogle ScholarPubMed
7. Taveggia, C, Zanazzi, G, Petrylak, A, Yano, H, Rosenbluth, J, Einheber, S, et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron. 2005 Sep 1;47(5):68194.CrossRefGoogle ScholarPubMed
8. Coman, I, Barbin, G, Charles, P, Zalc, B, Lubetzki, C. Axonal signals in central nervous system myelination, demyelination and remyelination. J Neurol Sci. 2005 Jun 15;233(1-2):6771.CrossRefGoogle ScholarPubMed
9. Michailov, GV, Sereda, MW, Brinkmann, BG, Fischer, TM, Haug, B, Birchmeier, C, et al. Axonal neuregulin-1 regulates myelin sheath thickness. Science. 2004 Apr 30;304(5671):7003.CrossRefGoogle ScholarPubMed
10. Aloisi, F. Growth factors. Neurol Sci. 2003 Dec;24 Suppl 5:S2914.CrossRefGoogle ScholarPubMed
11. Jessen, KR, Brennan, A, Morgan, L, Mirsky, R, Kent, A, Hashimoto, Y, et al. The Schwann cell precursor and its fate: a study of cell death and differentiation during gliogenesis in rat embryonic nerves. Neuron. 1994 Mar;12(3):50927.CrossRefGoogle ScholarPubMed
12. Grinspan, JB, Marchionni, MA, Reeves, M, Coulaloglou, M, Scherer, SS. Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: neuregulin receptors and the role of neuregulins. J Neurosci. 1996 Oct 1;16(19):610718.CrossRefGoogle ScholarPubMed
13. Syroid, DE, Maycox, PR, Burrola, PG, Liu, N, Wen, D, Lee, KF, et al. Cell death in the Schwann cell lineage and its regulation by neuregulin. Proc Natl Acad Sci USA. 1996 Aug 20;93(17): 922934.CrossRefGoogle ScholarPubMed
14. Garratt, AN, Britsch, S, Birchmeier, C. Neuregulin, a factor with many functions in the life of a schwann cell. Bioessays. 2000 Nov;22(11):98796.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
15. Morris, JK, Lin, W, Hauser, C, Marchuk, Y, Getman, D, Lee, KF. Rescue of the cardiac defect in ErbB2 mutant mice reveals essential roles of ErbB2 in peripheral nervous system development. Neuron. 1999 Jun;23(2):27383.CrossRefGoogle ScholarPubMed
16. Garratt, AN, Voiculescu, O, Topilko, P, Charnay, P, Birchmeier, C. A dual role of erbB2 in myelination and in expansion of the schwann cell precursor pool. J Cell Biol. 2000 Mar 6;148(5):103546.CrossRefGoogle ScholarPubMed
17. Guertin, AD, Zhang, DP, Mak, KS, Alberta, JA, Kim, HA. Microanatomy of axon/glial signaling during Wallerian degeneration. J Neurosci. 2005 Mar 30;25(13):347887.CrossRefGoogle ScholarPubMed
18. Hammarberg, H, Risling, M, Hokfelt, T, Cullheim, S, Piehl, F. Expression of insulin-like growth factors and corresponding binding proteins (IGFBP 1-6) in rat spinal cord and peripheral nerve after axonal injuries. J Comp Neurol. 1998 Oct 12;400(1):5772.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
19. Meier, C, Parmantier, E, Brennan, A, Mirsky, R, Jessen, KR. Developing Schwann cells acquire the ability to survive without axons by establishing an autocrine circuit involving insulin-like growth factor, neurotrophin-3, and platelet-derived growth factor-BB. J Neurosci. 1999 May 15;19(10):384759.CrossRefGoogle ScholarPubMed
20. Lobsiger, CS, Schweitzer, B, Taylor, V, Suter, U. Platelet-derived growth factor-BB supports the survival of cultured rat Schwann cell precursors in synergy with neurotrophin-3. Glia. 2000 May;30(3):290300.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
21. Oya, T, Zhao, YL, Takagawa, K, Kawaguchi, M, Shirakawa, K, Yamauchi, T, et al. Platelet-derived growth factor-b expression induced after rat peripheral nerve injuries. Glia. 2002 Jun;38(4): 30312.CrossRefGoogle ScholarPubMed
22. Jessen, KR, Mirsky, R. Schwann cells and their precursors emerge as major regulators of nerve development. Trends Neurosci. 1999 Sep;22(9):40210.CrossRefGoogle ScholarPubMed
23. Compston, A, Zajicek, J, Sussman, J, Webb, A, Hall, G, Muir, D, et al. Glial lineages and myelination in the central nervous system. J Anat. 1997 Feb;190 (Pt 2):161200.CrossRefGoogle ScholarPubMed
24. Noble, M, Murray, K, Stroobant, P, Waterfield, MD, Riddle, P. Plateletderived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature. 1988 Jun 9;333(6173):5602.CrossRefGoogle ScholarPubMed
25. Laeng, P, Decimo, D, Pettmann, B, Janet, T, Labourdette, G. Retinoic acid regulates the development of oligodendrocyte precursor cells in vitro. J Neurosci Res. 1994 Dec 15;39(6):61333.CrossRefGoogle ScholarPubMed
26. Barres, BA, Raff, MC, Gaese, F, Bartke, I, Dechant, G, Barde, YA. A crucial role for neurotrophin-3 in oligodendrocyte development. Nature. 1994 Jan 27;367(6461):3715.CrossRefGoogle ScholarPubMed
27. Barres, BA, Raff, MC. Control of oligodendrocyte number in the developing rat optic nerve. Neuron. 1994 May;12(5):93542.CrossRefGoogle ScholarPubMed
28. Fernandez, PA, Tang, DG, Cheng, L, Prochiantz, A, Mudge, AW, Raff, MC. Evidence that axon-derived neuregulin promotes oligodendrocyte survival in the developing rat optic nerve. Neuron. 2000 Oct;28(1):8190.CrossRefGoogle ScholarPubMed
29. Colognato, H, Baron, W, Avellana-Adalid, V, Relvas, JB, Baron-Van Evercooren, A, Georges-Labouesse, E, et al. CNS integrins switch growth factor signalling to promote target-dependent survival. Nat Cell Biol. 2002 Nov;4(11):83341.CrossRefGoogle ScholarPubMed
30. Kim, JY, Sun, Q, Oglesbee, M, Yoon, SO. The role of ErbB2 signaling in the onset of terminal differentiation of oligodendrocytes in vivo. J Neurosci. 2003 Jul 2;23(13):556171.CrossRefGoogle ScholarPubMed
31. Wang, S, Sdrulla, AD, diSibio, G, Bush, G, Nofziger, D, Hicks, C, et al. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron. 1998 Jul;21(1):6375.CrossRefGoogle ScholarPubMed
32. Hu, QD, Ang, BT, Karsak, M, Hu, WP, Cui, XY, Duka, T, et al. F3/contactin acts as a functional ligand for Notch during oligodendrocyte maturation. Cell. 2003 Oct 17;115(2):16375.CrossRefGoogle ScholarPubMed
33. Fanarraga, ML, Griffiths, IR, Zhao, M, Duncan, ID. Oligodendrocytes are not inherently programmed to myelinate a specific size of axon. J Comp Neurol. 1998 Sep 14;399(1):94100.3.0.CO;2-5>CrossRefGoogle Scholar
34. Friede, RL, Bischhausen, R. How are sheath dimensions affected by axon caliber and internode length? Brain Res. 1982 Mar 11; 235(2):33550.CrossRefGoogle ScholarPubMed
35. Friede, RL, Miyagishi, T. Adjustment of the myelin sheath to changes in axon caliber. Anat Rec. 1972 Jan;172(1):114.CrossRefGoogle ScholarPubMed
36. Hoke, A, Ho, T, Crawford, TO, LeBel, C, Hilt, D, Griffin, JW. Glial cell line-derived neurotrophic factor alters axon schwann cell units and promotes myelination in unmyelinated nerve fibers. J Neurosci. 2003 Jan 15;23(2):5617.CrossRefGoogle ScholarPubMed
37. Colello, RJ, Pott, U. Signals that initiate myelination in the developing mammalian nervous system. Mol Neurobiol. 1997 Aug;15(1):83100.CrossRefGoogle ScholarPubMed
38. Elder, GA, Friedrich, VL Jr., Lazzarini, RA. Schwann cells and oligodendrocytes read distinct signals in establishing myelin sheath thickness. J Neurosci Res. 2001 Sep 15;65(6):4939.CrossRefGoogle ScholarPubMed
39. Chan, JR, Watkins, TA, Cosgaya, JM, Zhang, C, Chen, L, Reichardt, LF, et al. NGF controls axonal receptivity to myelination by Schwann cells or oligodendrocytes. Neuron. 2004 Jul 22;43(2): 18391.CrossRefGoogle ScholarPubMed
40. Chan, JR, Cosgaya, JM, Wu, YJ, Shooter, EM. Neurotrophins are key mediators of the myelination program in the peripheral nervous system. Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):146618.CrossRefGoogle ScholarPubMed
41. Cosgaya, JM, Chan, JR, Shooter, EM. The neurotrophin receptor p75NTR as a positive modulator of myelination. Science. 2002 Nov 8;298(5596):12458.CrossRefGoogle ScholarPubMed
42. Notterpek, L. Neurotrophins in myelination: a new role for a puzzling receptor. Trends Neurosci. 2003 May;26(5):2324.CrossRefGoogle ScholarPubMed
43. Mirsky, R, Jessen, KR. The neurobiology of Schwann cells. Brain Pathol. 1999 Apr;9(2):293311.CrossRefGoogle ScholarPubMed
44. Voyvodic, JT. Target size regulates calibre and myelination of sympathetic axons Nature . 1989;342(6248): 4303.Google Scholar
45. Iwase, T, Jung, CG, Bae, H, Zhang, M, Soliven, B. Glial cell linederived neurotrophic factor-induced signaling in Schwann cells. J Neurochem. 2005 Sep;94(6):148899.CrossRefGoogle ScholarPubMed
46. Esper, RM, Loeb, JA. Rapid axoglial signaling mediated by neuregulin and neurotrophic factors. J Neurosci. 2004 Jul 7;24(27):621827.CrossRefGoogle ScholarPubMed
47. Stankoff, B, Aigrot, MS, Noel, F, Wattilliaux, A, Zalc, B, Lubetzki, C. Ciliary neurotrophic factor (CNTF) enhances myelin formation: a novel role for CNTF and CNTF-related molecules. J Neurosci. 2002 Nov 1;22(21):92217.CrossRefGoogle ScholarPubMed
48. Cellerino, A, Carroll, P, Thoenen, H, Barde, YA. Reduced size of retinal ganglion cell axons and hypomyelination in mice lacking brain-derived neurotrophic factor. Mol Cell Neurosci. 1997;9(5-6):397408.CrossRefGoogle ScholarPubMed
49. Esper, RM, Pankonin, MS, Loeb, JA. Neuregulins: versatile growth and differentiation factors in nervous system development and human disease. Brain Res Brain Res Rev. 2006 Aug;51(2): 16175.CrossRefGoogle ScholarPubMed
50. Falls, DL. Neuregulins: functions, forms, and signaling strategies. Exp Cell Res. 2003 Mar 10;284(1):1430.CrossRefGoogle ScholarPubMed
51. ffrench-Constant, C, Colognato, H, Franklin, RJ. Neuroscience. The mysteries of myelin unwrapped. Science. 2004 Apr 30; 304(5671):6889.CrossRefGoogle ScholarPubMed
52. Bermingham-McDonogh, O, YT, Xu, Marchionni, MA, Scherer, SS. Neuregulin expression in PNS neurons: isoforms and regulation by target interactions. Mol Cell Neurosci. 1997;10(3-4):18495.CrossRefGoogle ScholarPubMed
53. Chen, S, Velardez, MO, Warot, X, Yu, ZX, Miller, SJ, Cros, D, et al. Neuregulin 1-erbB signaling is necessary for normal myelination and sensory function. J Neurosci. 2006 Mar 22;26(12):307986.CrossRefGoogle ScholarPubMed
54. Chun, SJ, Rasband, MN, Sidman, RL, Habib, AA, Vartanian, T. Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J Cell Biol. 2003 Oct 27;163(2):397408.CrossRefGoogle ScholarPubMed
55. Ishibashi, T, Dakin, KA, Stevens, B, Lee, PR, Kozlov, SV, Stewart, CL, et al. Astrocytes promote myelination in response to electrical impulses. Neuron. 2006 Mar 16;49(6):82332.CrossRefGoogle ScholarPubMed
56. Waxman, SG, Ritchie, JM. Molecular dissection of the myelinated axon. Ann Neurol. 1993 Feb;33(2):12136.CrossRefGoogle ScholarPubMed
57. Poliak, S, Peles, E. The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci. 2003 Dec;4(12):96880.CrossRefGoogle ScholarPubMed
58. Salzer, JL. Polarized domains of myelinated axons. Neuron. 2003 Oct 9;40(2):297318.CrossRefGoogle ScholarPubMed
59. Vabnick, I, Novakovic, SD, Levinson, SR, Schachner, M, Shrager, P. The clustering of axonal sodium channels during development of the peripheral nervous system. J Neurosci. 1996 Aug 15;16(16): 491422.CrossRefGoogle ScholarPubMed
60. Vabnick, I, Messing, A, Chiu, SY, Levinson, SR, Schachner, M, Roder, J, et al. Sodium channel distribution in axons of hypomyelinated and MAG null mutant mice. J Neurosci Res. 1997 Oct 15; 50(2):32136.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
61. Arroyo, EJ, Sirkowski, EE, Chitale, R, Scherer, SS. Acute demyelination disrupts the molecular organization of peripheral nervous system nodes. J Comp Neurol. 2004 Nov 22; 479(4):42434.CrossRefGoogle ScholarPubMed
62. Dugandzija-Novakovic, S, Koszowski, AG, Levinson, SR, Shrager, P. Clustering of Na+ channels and node of Ranvier formation in remyelinating axons. J Neurosci. 1995 Jan;15(1 Pt 2):492503.CrossRefGoogle ScholarPubMed
63. Kaplan, MR, Cho, MH, Ullian, EM, Isom, LL, Levinson, SR, Barres, BA. Differential control of clustering of the sodium channels Na(v)1.2 and Na(v)1.6 at developing CNS nodes of Ranvier. Neuron. 2001 Apr;30(1):10519.CrossRefGoogle ScholarPubMed
64. Kaplan, MR, Meyer-Franke, A, Lambert, S, Bennett, V, Duncan, ID, Levinson, SR, et al. Induction of sodium channel clustering by oligodendrocytes. Nature. 1997 Apr 17;386(6626):7248.CrossRefGoogle ScholarPubMed
65. Eshed, Y, Feinberg, K, Poliak, S, Sabanay, H, Sarig-Nadir, O, Spiegel, I, et al. Gliomedin mediates Schwann cell-axon interaction and the molecular assembly of the nodes of Ranvier. Neuron. 2005 Jul 21;47(2):21529.CrossRefGoogle ScholarPubMed
66. de Waegh, SM, Lee, VM, Brady, ST. Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell. 1992 Feb 7; 68(3):45163.CrossRefGoogle ScholarPubMed
67. Brady, ST, Witt, AS, Kirkpatrick, LL, de Waegh, SM, Readhead, C, PH, Tu, et al. Formation of compact myelin is required for maturation of the axonal cytoskeleton. J Neurosci. 1999 Sep 1; 19(17):727888.CrossRefGoogle ScholarPubMed
68. Sanchez, I, Hassinger, L, Paskevich, PA, Shine, HD, Nixon, RA. Oligodendroglia regulate the regional expansion of axon caliber and local accumulation of neurofilaments during development independently of myelin formation. J Neurosci. 1996 Aug 15; 16(16):5095105.CrossRefGoogle ScholarPubMed
69. Henderson, CE. Role of neurotrophic factors in neuronal development. Curr Opin Neurobiol. 1996 Feb;6(1):6470.CrossRefGoogle ScholarPubMed
70. Moore, MW, Klein, RD, Farinas, I, Sauer, H, Armanini, M, Phillips, H, et al. Renal and neuronal abnormalities in mice lacking GDNF. Nature. 1996 Jul 4;382(6586):769.CrossRefGoogle ScholarPubMed
71. Wilkins, A, Majed, H, Layfield, R, Compston, A, Chandran, S. Oligodendrocytes promote neuronal survival and axonal length by distinct intracellular mechanisms: a novel role for oligodendrocyte-derived glial cell line-derived neurotrophic factor. J Neurosci. 2003 Jun 15;23(12):496774.CrossRefGoogle ScholarPubMed
72. De Stefano, N, Matthews, PM, Fu, L, Narayanan, S, Stanley, J, Francis, GS, et al. Axonal damage correlates with disability in patients with relapsing-remitting multiple sclerosis. Results of a longitudinal magnetic resonance spectroscopy study. Brain. 1998 Aug;121 (Pt 8):146977.CrossRefGoogle ScholarPubMed
73. Ferguson, B, Matyszak, MK, Esiri, MM, Perry, VH. Axonal damage in acute multiple sclerosis lesions. Brain. 1997 Mar;120 (Pt 3): 3939.CrossRefGoogle ScholarPubMed
74. Sarchielli, P, Greco, L, Stipa, A, Floridi, A, Gallai, V. Brain-derived neurotrophic factor in patients with multiple sclerosis. J Neuroimmunol. 2002 Nov;132(1-2):1808.CrossRefGoogle ScholarPubMed
75. Linker, RA, Maurer, M, Gaupp, S, Martini, R, Holtmann, B, Giess, R, et al. CNTF is a major protective factor in demyelinating CNS disease: a neurotrophic cytokine as modulator in neuroinflammation. Nat Med. 2002 Jun;8(6):6204.CrossRefGoogle Scholar
76. Kuhlmann, T, Remington, L, Cognet, I, Bourbonniere, L, Zehntner, S, Guilhot, F, et al. Continued administration of ciliary neurotrophic factor protects mice from inflammatory pathology in experimental autoimmune encephalomyelitis. Am J Pathol. 2006 Aug;169(2):58498.CrossRefGoogle ScholarPubMed
77. Baron, W, Colognato, H, ffrench-Constant, C. Integrin-growth factor interactions as regulators of oligodendroglial development and function. Glia. 2005 Mar;49(4):46779.CrossRefGoogle ScholarPubMed