Insufficient OPC migration into demyelinated lesions is a cause of poor remyelination in MS and mouse models

Acta Neuropathologica

Volumn 125, Issue 6, 2013, Pages 841-859

  Boyd, Amanda ^a   Zhang, Hui ^a   Williams, Anna ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Migration; Oligodendrocyte precursor cell; Remyelination; Semaphorin

Indexed keywords

SEMAPHORIN 3A; SEMAPHORIN 3F;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; DEMYELINATION; FEMALE; HUMAN; HUMAN TISSUE; MALE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REMYELINIZATION; STEM CELL;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CASE-CONTROL STUDIES; CELL MOVEMENT; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; MULTIPLE SCLEROSIS; NEURAL STEM CELLS; NEUROPILIN-1; OLIGODENDROGLIA; REGENERATION; SEMAPHORINS;

EID: 84878527176     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-013-1112-y     Document Type: Article

References (57)

1. Behar O, Golden JA, Mashimo H, Schoen FJ, Fishman MC (1996) Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature 383(6600):525-528
2. Caillava C, Vandenbosch R, Jablonska B, Deboux C, Spigoni G, Gallo V, Malgrange B, Baron-Van Evercooren A (2011) Cdk2 loss accelerates precursor differentiation and remyelination in the adult central nervous system. J Cell Biol 193(2):397-407. doi: 10.1083/jcb.201004146
3. Carbajal KS, Miranda JL, Tsukamoto MR, Lane TE (2011) CXCR4 signaling regulates remyelination by endogenous oligodendrocyte progenitor cells in a viral model of demyelination. Glia 59(12):1813-1821. doi: 10.1002/glia.21225
4. Catalano SM, Messersmith EK, Goodman CS, Shatz CJ, Chedotal A (1998) Many major CNS axon projections develop normally in the absence of semaphorin III. Mol Cell Neurosci 11(4):173-182
5. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD (2000) NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 20(17):6404-6412
6. Chang A, Tourtellotte WW, Rudick R, Trapp BD (2002) Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 346(3):165-173
7. Crandall JE, Dibble C, Butler D, Pays L, Ahmad N, Kostek C, Puschel AW, Schwarting GA (2000) Patterning of olfactory sensory connections is mediated by extracellular matrix proteins in the nerve layer of the olfactory bulb. J Neurobiol 45(4):195-206
8. De Stefano N, Matthews PM, Filippi M, Agosta F, De Luca M, Bartolozzi ML, Guidi L, Ghezzi A, Montanari E, Cifelli A, Federico A, Smith SM (2003) Evidence of early cortical atrophy in MS: relevance to white matter changes and disability. Neurology 60(7):1157-1162
9. Eickholt BJ, Morrow R, Walsh FS, Doherty P (1997) Structural features of collapsin required for biological activity and distribution of binding sites in the developing chick. Mol Cell Neurosci 9(5-6):358-371. doi: 10.1006/mcne.1997.0636
10. Fancy SP, Baranzini SE, Zhao C, Yuk DI, Irvine KA, Kaing S, Sanai N, Franklin RJ, Rowitch DH (2009) Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 23(13):1571-1585
11. Fancy SP, Harrington EP, Yuen TJ, Silbereis JC, Zhao C, Baranzini SE, Bruce CC, Otero JJ, Huang EJ, Nusse R, Franklin RJ, Rowitch DH (2011) Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat Neurosci 14(8):1009-1016. doi: 10.1038/nn.2855
12. Franklin RJ, Ffrench-Constant C (2008) Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 9(11):839-855
13. Fritzsching B, Haas J, Konig F, Kunz P, Fritzsching E, Poschl J, Krammer PH, Bruck W, Suri-Payer E, Wildemann B (2011) Intracerebral human regulatory T cells: analysis of CD4+ CD25+ FOXP3+ T cells in brain lesions and cerebrospinal fluid of multiple sclerosis patients. PLoS One 6(3):e17988. doi: 10.1371/journal.pone.0017988
14. Funfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS, Edgar J, Brinkmann BG, Kassmann CM, Tzvetanova ID, Mobius W, Diaz F, Meijer D, Suter U, Hamprecht B, Sereda MW, Moraes CT, Frahm J, Goebbels S, Nave KA (2012) Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485(7399):517-521. doi: 10.1038/nature11007
15. Giger RJ, Urquhart ER, Gillespie SK, Levengood DV, Ginty DD, Kolodkin AL (1998) Neuropilin-2 is a receptor for semaphorin IV: insight into the structural basis of receptor function and specificity. Neuron 21(5):1079-1092
16. Gu C, Rodriguez ER, Reimert DV, Shu T, Fritzsch B, Richards LJ, Kolodkin AL, Ginty DD (2003) Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell 5(1):45-57
17. Huang JK, Jarjour AA, Nait Oumesmar B, Kerninon C, Williams A, Krezel W, Kagechika H, Bauer J, Zhao C, Evercooren AB, Chambon P, Ffrench-Constant C, Franklin RJ (2011) Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat Neurosci 14(1):45-53
18. Kaneko S, Iwanami A, Nakamura M, Kishino A, Kikuchi K, Shibata S, Okano HJ, Ikegami T, Moriya A, Konishi O, Nakayama C, Kumagai K, Kimura T, Sato Y, Goshima Y, Taniguchi M, Ito M, He Z, Toyama Y, Okano H (2006) A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat Med 12(12):1380-1389. doi: 10.1038/nm1505
19. Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, Bekku Y, Yagi T, Fujisawa H (1997) Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19(5):995-1005
20. Kotter MR, Setzu A, Sim FJ, Van Rooijen N, Franklin RJ (2001) Macrophage depletion impairs oligodendrocyte remyelination following lysolecithin-induced demyelination. Glia 35(3):204-212
21. Kuhlmann T, Goldschmidt T, Antel J, Wegner C, Konig F, Metz I, Bruck W (2009) Gender differences in the histopathology of MS? J Neurol Sci 286(1-2):86-91. doi: 10.1016/j.jns.2009.07.014
22. Lau P, Verrier JD, Nielsen JA, Johnson KR, Notterpek L, Hudson LD (2008) Identification of dynamically regulated microRNA and mRNA networks in developing oligodendrocytes. J Neurosci 28(45):11720-11730. doi: 10.1523/JNEUROSCI.1932- 08.2008
23. Lee KK, de Repentigny Y, Saulnier R, Rippstein P, Macklin WB, Kothary R (2006) Dominant-negative beta1 integrin mice have region-specific myelin defects accompanied by alterations in MAPK activity. Glia 53(8):836-844. doi: 10.1002/glia.20343
24. Lee MA, Blamire AM, Pendlebury S, Ho KH, Mills KR, Styles P, Palace J, Matthews PM (2000) Axonal injury or loss in the internal capsule and motor impairment in multiple sclerosis. Arch Neurol 57(1):65-70
25. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, Liu Y, Tsingalia A, Jin L, Zhang PW, Pellerin L, Magistretti PJ, Rothstein JD (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487(7408):443-448. doi: 10.1038/nature11314
26. Liang WC, Dennis MS, Stawicki S, Chanthery Y, Pan Q, Chen Y, Eigenbrot C, Yin J, Koch AW, Wu X, Ferrara N, Bagri A, Tessier-Lavigne M, Watts RJ, Wu Y (2007) Function blocking antibodies to neuropilin-1 generated from a designed human synthetic antibody phage library. J Mol Biol 366(3):815-829. doi: S0022-2836(06)01550-610.1016/j.jmb.2006.11.021
27. Lucchinetti C, Bruck W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H (1999) A quantitative analysis of oligodendrocytes in multiple sclerosis lesions. A study of 113 cases. Brain 122(Pt 12):2279-2295
28. Majed HH, Chandran S, Niclou SP, Nicholas RS, Wilkins A, Wing MG, Rhodes KE, Spillantini MG, Compston A (2006) A novel role for Sema3A in neuroprotection from injury mediated by activated microglia. J Neurosci 26(6):1730-1738
29. Mi S, Lee X, Hu Y, Ji B, Shao Z, Yang W, Huang G, Walus L, Rhodes K, Gong BJ, Miller RH, Pepinsky RB (2011) Death receptor 6 negatively regulates oligodendrocyte survival, maturation and myelination. Nat Med 17(7):816-821. doi: 10.1038/nm.2373
30. Mi S, Miller RH, Tang W, Lee X, Hu B, Wu W, Zhang Y, Shields CB, Zhang Y, Miklasz S, Shea D, Mason J, Franklin RJ, Ji B, Shao Z, Chedotal A, Bernard F, Roulois A, Xu J, Jung V, Pepinsky B (2009) Promotion of central nervous system remyelination by induced differentiation of oligodendrocyte precursor cells. Ann Neurol 65(3):304-315
31. Olah M, Amor S, Brouwer N, Vinet J, Eggen B, Biber K, Boddeke HW (2012) Identification of a microglia phenotype supportive of remyelination. Glia 60(2):306-321
32. Omoto M, Yoshida S, Miyashita H, Kawakita T, Yoshida K, Kishino A, Kimura T, Shibata S, Tsubota K, Okano H, Shimmura S (2012) The semaphorin 3A inhibitor SM-345431 accelerates peripheral nerve regeneration and sensitivity in a murine corneal transplantation model. PLoS One 7(11):e47716. doi: 10.1371/journal. pone.0047716
33. Pan Q, Chanthery Y, Liang WC, Stawicki S, Mak J, Rathore N, Tong RK, Kowalski J, Yee SF, Pacheco G, Ross S, Cheng Z, Le Couter J, Plowman G, Peale F, Koch AW, Wu Y, Bagri A, Tessier-Lavigne M, Watts RJ (2007) Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 11(1):53-67. doi: S1535-6108(06)00367-9
34. Patani R, Balaratnam M, Vora A, Reynolds R (2007) Remyelination can be extensive in multiple sclerosis despite a long disease course. Neuropathol Appl Neurobiol 33(3):277-287
35. Patrikios P, Stadelmann C, Kutzelnigg A, Rauschka H, Schmidbauer M, Laursen H, Sorensen PS, Bruck W, Lucchinetti C, Lassmann H (2006) Remyelination is extensive in a subset of multiple sclerosis patients. Brain 129(Pt 12):3165-3172
36. Perier O, Gregoire A (1965) Electron microscopic features of multiple sclerosis lesions. Brain 88(5):937-952
37. Piaton G, Aigrot MS, Williams A, Moyon S, Tepavcevic V, Moutkine I, Gras J, Matho KS, Schmitt A, Soellner H, Huber AB, Ravassard P, Lubetzki C (2011) Class 3 semaphorins influence oligodendrocyte precursor recruitment and remyelination in adult central nervous system. Brain 134(Pt 4):1156-1167
38. Prineas JW, Barnard RO, Kwon EE, Sharer LR, Cho ES (1993) Multiple sclerosis: remyelination of nascent lesions. Ann Neurol 33(2):137-151
39. Prinz F, Schlange T, Asadullah K (2011) Believe it or not: how much can we rely on published data on potential drug targets? Nat Rev 10(9):712
40. Raine CS, Wu E (1993) Multiple sclerosis: remyelination in acute lesions. J Neuropathol Exp Neurol 52(3):199-204
41. Ruckh JM, Zhao JW, Shadrach JL, van Wijngaarden P, Rao TN, Wagers AJ, Franklin RJ (2012) Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 10(1):96-103
42. Sabo JK, Aumann TD, Merlo D, Kilpatrick TJ, Cate HS (2011) Remyelination is altered by bone morphogenic protein signaling in demyelinated lesions. J Neurosci 31(12):4504-4510. doi: 10.1523/JNEUROSCI.5859-10.2011
43. Spassky N, de Castro F, Le Bras B, Heydon K, Queraud-LeSaux F, Bloch-Gallego E, Chedotal A, Zalc B, Thomas JL (2002) Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J Neurosci 22(14):5992-6004
44. Stephens LA, Malpass KH, Anderton SM (2009) Curing CNS autoimmune disease with myelin-reactive Foxp3+ Treg. Eur J Immunol 39(4):1108-1117
45. Sugimoto Y, Taniguchi M, Yagi T, Akagi Y, Nojyo Y, Tamamaki N (2001) Guidance of glial precursor cell migration by secreted cues in the developing optic nerve. Development 128(17):3321-3330
46. Syed YA, Hand E, Mobius W, Zhao C, Hofer M, Nave KA, Kotter MR (2011) Inhibition of CNS remyelination by the presence of semaphorin 3A. J Neurosci 31(10):3719-3728. doi: 10.1523/JNEUROSCI.4930-10.2011
47. Taniguchi M, Yuasa S, Fujisawa H, Naruse I, Saga S, Mishina M, Yagi T (1997) Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 19(3):519-530
48. Trapp BD, Bo L, Mork S, Chang A (1999) Pathogenesis of tissue injury in MS lesions. J Neuroimmunol 98(1):49-56
49. Turbic A, Leong SY, Turnley AM (2011) Chemokines and inflammatory mediators interact to regulate adult murine neural precursor cell proliferation, survival and differentiation. PLoS One 6(9):e25406. doi: 10.1371/journal.pone. 0025406
50. Vooijs M, Jonkers J, Berns A (2001) A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO Rep 2(4):292-297. doi: 10.1093/embo-reports/kve064
51. Vora P, Pillai P, Mustapha J, Kowal C, Shaffer S, Bose R, Namaka M, Frost EE (2012) CXCL1 regulation of oligodendrocyte progenitor cell migration is independent of calcium signaling. Exp Neurol 236(2):259-267. doi: 10.1016/j.expneurol.2012.04.012
52. Voss EV, Skuljec J, Gudi V, Skripuletz T, Pul R, Trebst C, Stangel M (2012) Characterisation of microglia during de- and remyelination: can they create a repair promoting environment? Neurobiol Dis 45(1):519-528
53. Weiss JM, Bilate AM, Gobert M, Ding Y, Curotto de Lafaille MA, Parkhurst CN, Xiong H, Dolpady J, Frey AB, Ruocco MG, Yang Y, Floess S, Huehn J, Oh S, Li MO, Niec RE, Rudensky AY, Dustin ML, Littman DR, Lafaille JJ (2012) Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells. J Exp Med 209(10):1723-1742. doi: 10.1084/jem.20120914
54. Williams A, Piaton G, Aigrot MS, Belhadi A, Theaudin M, Petermann F, Thomas JL, Zalc B, Lubetzki C (2007) Semaphorin 3A and 3F: key players in myelin repair in multiple sclerosis? Brain 130(Pt 10):2554-2565
55. Woodruff RH, Fruttiger M, Richardson WD, Franklin RJ (2004) Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol Cell Neurosci 25(2):252-262
56. Yadav M, Louvet C, Davini D, Gardner JM, Martinez-Llordella M, Bailey-Bucktrout S, Anthony BA, Sverdrup FM, Head R, Kuster DJ, Ruminski P, Weiss D, Von Schack D, Bluestone JA (2012) Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J Exp Med 209(10):1713-1722. doi: 10.1084/jem.20120822
57. Zachary I (2005) Neuroprotective role of vascular endothelial growth factor: signalling mechanisms, biological function, and therapeutic potential. Neurosignals 14(5):207-221. doi: 8863710.1159/000088637