Class 3 semaphorins influence oligodendrocyte precursor recruitment and remyelination in adult central nervous system

Brain

Volumn 134, Issue 4, 2011, Pages 1156-1167

  Piaton, Gabrile ^a   Aigrot, Marie Stéphane ^a   Williams, Anna ^b   Moyon, Sarah ^a   Tepavcevic, Vanja ^a   Moutkine, Imane ^a   Gras, Julien ^a   Matho, Katherine S ^a   Schmitt, Alain ^c   Soellner, Heidi ^d   Huber, Andrea B ^d   Ravassard, Philippe ^a   Lubetzki, Catherine ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c INSTITUT COCHIN   (France)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

gain and loss of function; oligodendrocyte precursor cell; recruitment; remyelination; semaphorin

Indexed keywords

ANTIBODY; GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; NEUROPILIN; PLEXIN; SEMAPHORIN 3A; SEMAPHORIN 3F;

ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CELL SELECTION; CELL STRAIN HEK293; CENTRAL NERVOUS SYSTEM; CYTOMEGALOVIRUS; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOHISTOCHEMISTRY; INJECTION; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REMYELINIZATION; SPINAL CORD; STEM CELL; TRANSMISSION ELECTRON MICROSCOPY; VESICULAR STOMATITIS VIRUS;

ANIMALS; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MYELIN BASIC PROTEINS; MYELIN SHEATH; OLIGODENDROGLIA; SEMAPHORINS; SPINAL CORD; STATISTICS, NONPARAMETRIC;

EID: 79953653879     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr022     Document Type: Article

References (57)

1. Adams RH, Lohrum M, Klostermann A, Betz H, Puschel AW. The che-morepulsive activity of secreted semaphorins is regulated by furin-dependent proteolytic processing. EMBO J 1997; 16: 6077-86. (Pubitemid 27458327)
2. Aguirre A, Dupree JL, Mangin JM, Gallo V. A functional role for EGFR signaling in myelination and remyelination. Nat Neurosci 2007; 10: 990-1002. (Pubitemid 47185206)
3. Back SA, Tuohy TM, Chen H, Wallingford N, Craig A, Struve J, et al. Hyaluronan accumulates in demyelinated lesions and inhibits oligo-dendrocyte progenitor maturation. Nat Med 2005; 11: 966-72. (Pubitemid 41294442)
4. Bribian A, Barallobre MJ, Soussi-Yanicostas N, de Castro F. Anosmin-1 modulates the FGF-2-dependent migration of oligodendrocyte precursors in the developing optic nerve. Mol Cell Neurosci 2006; 33: 2-14. (Pubitemid 44308463)
5. Bruce CC, Zhao C, Franklin RJ. Remyelination-an effective means of neuroprotection. Horm Behav 2010; 57: 56-62.
6. Carbajal KS, Schaumburg C, Strieter R, Kane J, Lane TE. Migration of engrafted neural stem cells is mediated by CXCL12 signaling through CXCR4 in a viral model of multiple sclerosis. Proc Natl Acad Sci USA 2010; 107: 11068-73.
7. Castaing M, Guerci A, Mallet J, Czernichow P, Ravassard P, Scharfmann R. Efficient restricted gene expression in beta cells by lentivirus-mediated gene transfer into pancreatic stem/progenitor cells. Diabetologia 2005; 48: 709-19. (Pubitemid 40591227)
8. Chang A, Tourtellotte WW, Rudick R, Trapp BD. Premyelinating oligo-dendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 2002; 346: 165-73. (Pubitemid 34438882)
9. Charles P, Reynolds R, Seilhean D, Rougon G, Aigrot MS, Niezgoda A, et al. Re-expression of PSA-NCAM by demyelinated axons: an inhibitor of remyelination in multiple sclerosis? Brain 2002; 125: 1972-9.
10. Chen G, Sima J, Jin M, Wang KY, Xue XJ, Zheng W, et al. Semaphorin-3A guides radial migration of cortical neurons during development. Nat Neurosci 2008; 11: 36-44.
11. Compston A, Coles A. Multiple sclerosis. Lancet 2008; 372: 1502-17.
12. Crawford DK, Mangiardi M, Xia X, Lopez-Valdes HE, Tiwari-Woodruff SK. Functional recovery of callosal axons following demye-lination: a critical window. Neuroscience 2009; 164: 1407-21.
13. De Castro F, Bribian A. The molecular orchestra of the migration of oligodendrocyte precursors during development. Brain Res Brain Res Rev 2005; 49: 227-41. (Pubitemid 41160392)
14. De Wit J, De Winter F, Klooster J, Verhaagen J. Semaphorin 3A displays a punctate distribution on the surface of neuronal cells and interacts with proteoglycans in the extracellular matrix. Mol Cell Neurosci 2005; 29: 40-55. (Pubitemid 40603879)
15. Dziembowska M, Tham TN, Lau P, Vitry S, Lazarini F, Dubois-Dalcq M. A role for CXCR4 signaling in survival and migration of neural and oligodendrocyte precursors. Glia 2005; 50: 258-69. (Pubitemid 40769855)
16. Franklin RJ. Why does remyelination fail in multiple sclerosis? Nat Rev Neurosci 2002; 3: 705-14. (Pubitemid 135706676)
17. Gu C, Rodriguez ER, Reimert DV, Shu T, Fritzsch B, Richards LJ, et al. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell 2003; 5: 45-57. (Pubitemid 36827341)
18. Irvine KA, Blakemore WF. Remyelination protects axons from demyelination-associated axon degeneration. Brain 2008; 131: 1464-77. (Pubitemid 351806463)
19. Jarjour AA, Manitt C, Moore SW, Thompson KM, Yuh SJ, Kennedy TE. Netrin-1 is a chemorepellent for oligodendrocyte precursor cells in the embryonic spinal cord. J Neurosci 2003; 23: 3735-44. (Pubitemid 36958480)
20. John GR, Shankar SL, Shafit-Zagardo B, Massimi A, Lee SC, Raine CS, et al. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat Med 2002; 8: 1115-21. (Pubitemid 35175966)
21. Klinghoffer RA, Hamilton TG, Hoch R, Soriano P. An allelic series at the PDGFalphaR locus indicates unequal contributions of distinct signaling pathways during development. Dev Cell 2002; 2: 103-13. (Pubitemid 34065910)
22. Kornek B, Storch MK, Weissert R, Wallstroem E, Stefferl A, Olsson T, et al. Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am J Pathol 2000; 157: 267-76. (Pubitemid 30641742)
23. Kusy S, Funkelstein L, Bourgais D, Drabkin H, Rougon G, Roche J, et al. Redundant functions but temporal and regional regulation of two alternatively spliced isoforms of semaphorin 3F in the nervous system. Mol Cell Neurosci 2003; 24: 409-18. (Pubitemid 37311304)
24. Lubetzki C, Goujet-Zalc C, Gansmuller A, Monge M, Brillat A, Zalc B. Morphological, biochemical, and functional characterization of bulk isolated glial progenitor cells. J Neurochem 1991; 56: 671-80. (Pubitemid 21902013)
25. Lucchinetti C, Bruck W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H. A quantitative analysis of oligodendrocytes in multiple sclerosis lesions. A study of 113 cases. Brain 1999; 122 (Pt 12): 2279-95.
26. Maeda Y, Solanky M, Menonna J, Chapin J, Li W, Dowling P. Platelet-derived growth factor-alpha receptor-positive oligodendroglia are frequent in multiple sclerosis lesions. Ann Neurol 2001; 49: 776-85. (Pubitemid 32530245)
27. Mi S, Miller RH, Tang W, Lee X, Hu B, Wu W, et al. Promotion of central nervous system remyelination by induced differentiation of oligodendrocyte precursor cells. Ann Neurol 2009; 65: 304-15.
28. Miller RH, Mi S. Dissecting demyelination. Nat Neurosci 2007; 10: 1351-4. (Pubitemid 350014684)
29. Nave KA, Trapp BD. Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 2008; 31: 535-61.
30. Okada A, Tominaga M, Horiuchi M, Tomooka Y. Plexin-A4 is expressed in oligodendrocyte precursor cells and acts as a mediator of sema-phorin signals. Biochem Biophys Res Commun 2007; 352: 158-63. (Pubitemid 44821108)
31. Omari KM, John GR, Sealfon SC, Raine CS. CXC chemokine receptors on human oligodendrocytes: implications for multiple sclerosis. Brain 2005; 128: 1003-15. (Pubitemid 40675456)
32. Omari KM, Lutz SE, Santambrogio L, Lira SA, Raine CS. Neuroprotection and remyelination after autoimmune demyelination in mice that indu-cibly overexpress CXCL1. Am J Pathol 2009; 174: 164-76.
33. Pasterkamp RJ, Verhaagen J. Semaphorins in axon regeneration: developmental guidance molecules gone wrong? Philos Trans R Soc Lond B Biol Sci 2006; 361: 1499-511. (Pubitemid 44450207)
34. Patel JR, McCandless EE, Dorsey D, Klein RS. CXCR4 promotes differentiation of oligodendrocyte progenitors and remyelination. Proc Natl Acad Sci USA 2010; 107: 11062-7.
35. Patrikios P, Stadelmann C, Kutzelnigg A, Rauschka H, Schmidbauer M, Laursen H, et al. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006; 129: 3165-72. (Pubitemid 44871433)
36. Penderis J, Shields SA, Franklin RJ. Impaired remyelination and depletion of oligodendrocyte progenitors does not occur following repeated episodes of focal demyelination in the rat central nervous system. Brain 2003; 126: 1382-91. (Pubitemid 36644383)
37. Perier O, Gregoire A. Electron microscopic features of multiple sclerosis lesions. Brain 1965; 88: 937-52.
38. Piaton G, Williams A, Seilhean D, Lubetzki C. Remyelination in multiple sclerosis. Prog Brain Res 2009; 175: 453-64.
39. Prestoz L, Chatzopoulou E, Lemkine G, Spassky N, Lebras B, Kagawa T, et al. Control of axonophilic migration of oligodendrocyte precursor cells by Eph-ephrin interaction. Neuron Glia Biol 2004; 1: 73-83.
40. Prineas JW, Connell F. Remyelination in multiple sclerosis. Ann Neurol 1979; 5: 22-31. (Pubitemid 9083248)
41. Raine CS, Wu E. Multiple sclerosis: remyelination in acute lesions. J Neuropathol Exp Neurol 1993; 52: 199-204. (Pubitemid 23136018)
42. Rist JM, Franklin RJ. Taking ageing into account in remyelination-based therapies for multiple sclerosis. J Neurol Sci 2008; 274: 64-7.
43. Russ HA, Bar Y, Ravassard P, Efrat S. In vitro proliferation of cells derived from adult human beta-cells revealed by cell-lineage tracing. Diabetes 2008; 57: 1575-83.
44. Smith KJ, Blakemore WF, McDonald WI. The restoration of conduction by central remyelination. Brain 1981; 104: 383-404. (Pubitemid 12183328)
45. Spassky N, de Castro F, Le Bras B, Heydon K, Queraud-LeSaux F, Bloch-Gallego E, et al. Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J Neurosci 2002; 22: 5992-6004. (Pubitemid 35387643)
46. Sugimoto Y, Taniguchi M, Yagi T, Akagi Y, Nojyo Y, Tamamaki N. Guidance of glial precursor cell migration by secreted cues in the developing optic nerve. Development 2001; 128: 3321-30. (Pubitemid 32910384)
47. Takamatsu H, Okuno T, Kumanogoh A. Regulation of immune cell responses by semaphorins and their receptors. Cell Mol Immunol 2010; 7: 83-8.
48. Tsai HH, Frost E, To V, Robinson S, Ffrench-Constant C, Geertman R, et al. The chemokine receptor CXCR2 controls positioning of oligo-dendrocyte precursors in developing spinal cord by arresting their migration. Cell 2002; 110: 373-83.
49. Vana AC, Flint NC, Harwood NE, Le TQ, Fruttiger M, Armstrong RC. Platelet-derived growth factor promotes repair of chronically demyeli-nated white matter. J Neuropathol Exp Neurol 2007; 66: 975-88. (Pubitemid 350060366)
50. Williams A, Piaton G, Aigrot MS, Belhadi A, Theaudin M, Petermann F, et al. Semaphorin 3A and 3F: key players in myelin repair in multiple sclerosis? Brain 2007; 130: 2554-65. (Pubitemid 47511713)
51. Wolswijk G. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J Neurosci 1998; 18: 601-9. (Pubitemid 28041896)
52. Wolswijk G, Riddle PN, Noble M. Coexistence of perinatal and adult forms of a glial progenitor cell during development of the rat optic nerve. Development 1990; 109: 691-8. (Pubitemid 20228663)
53. Woodruff RH, Fruttiger M, Richardson WD, Franklin RJ. Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol Cell Neurosci 2004; 25: 252-62. (Pubitemid 38344108)
54. Yee JK, Miyanohara A, LaPorte P, Bouic K, Burns JC, Friedmann T. A general method for the generation of high-titer, pantropic retroviral vectors: highly efficient infection of primary hepatocytes. Proc Natl Acad Sci USA 1994; 91: 9564-8. (Pubitemid 24297955)
55. Zennou V, Petit C, Guetard D, Nerhbass U, Montagnier L, Charneau P. HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 2000; 101: 173-85. (Pubitemid 32004745)
56. Zhang Y, Argaw AT, Gurfein BT, Zameer A, Snyder BJ, Ge C, et al. Notch1 signaling plays a role in regulating precursor differentiation during CNS remyelination. Proc Natl Acad Sci USA 2009; 106: 19162-7.
57. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 1997; 15: 871-5.