Full-length and fragmented netrin-1 in multiple sclerosis plaques are inhibitors of oligodendrocyte precursor cell migration

American Journal of Pathology

Volumn 183, Issue 3, 2013, Pages 673-680

  Bin, Jenea M ^a   Rajasekharan, Sathyanath ^a   Kuhlmann, Tanja ^b   Hanes, Ilana ^a   Marcal, Nathalie ^a   Han, Dong ^a   Rodrigues, Sonia P ^a   Leong, Soo Yuen ^a   Newcombe, Jia ^c   Antel, Jack P ^a   Kennedy, Timothy E ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NETRIN 1;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; ASTROCYTE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MULTIPLE SCLEROSIS; NERVE FIBER GROWTH; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REMYELINIZATION; WHITE MATTER;

ADULT; AGED; ANIMALS; BRAIN; CELL MOVEMENT; CHICKENS; CHILD; FEMALE; HEK293 CELLS; HUMANS; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; NERVE GROWTH FACTORS; OLIGODENDROGLIA; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; STEM CELLS; TUMOR SUPPRESSOR PROTEINS;

EID: 84883143062     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.06.004     Document Type: Article

References (49)

1. K. Lai Wing Sun, J.P. Correia, and T.E. Kennedy Netrins: versatile extracellular cues with diverse functions Development 138 2011 2153 2169
2. S.W. Moore, M. Tessier-Lavigne, and T.E. Kennedy Netrins and their receptors Adv Exp Med Biol 621 2007 17 31
3. A.A. Jarjour, C. Manitt, S.W. Moore, K.M. Thompson, S.J. Yuh, and T.E. Kennedy Netrin-1 is a chemorepellent for oligodendrocyte precursor cells in the embryonic spinal cord J Neurosci 23 2003 3735 3744
4. Y. Sugimoto, M. Taniguchi, T. Yagi, Y. Akagi, Y. Nojyo, and N. Tamamaki Guidance of glial precursor cell migration by secreted cues in the developing optic nerve Development 128 2001 3321 3330
5. H.H. Tsai, M. Tessier-Lavigne, and R.H. Miller Netrin 1 mediates spinal cord oligodendrocyte precursor dispersal Development 130 2003 2095 2105
6. S. Rajasekharan, K.A. Baker, K.E. Horn, A.A. Jarjour, J.P. Antel, and T.E. Kennedy Netrin 1 and Dcc regulate oligodendrocyte process branching and membrane extension via Fyn and RhoA Development 136 2009 415 426
7. S. Rajasekharan, J.M. Bin, J.P. Antel, and T.E. Kennedy A central role for RhoA during oligodendroglial maturation in the switch from netrin-1 mediated chemorepulsion to process elaboration J Neurochem 113 2010 1589 1597
8. A.A. Jarjour, S.J. Bull, M. Almasieh, S. Rajasekharan, K.A. Baker, J. Mui, J.P. Antel, A. Di Polo, and T.E. Kennedy Maintenance of axo-oligodendroglial paranodal junctions requires DCC and netrin-1 J Neurosci 28 2008 11003 11014
9. C. Manitt, M.A. Colicos, K.M. Thompson, E. Rousselle, A.C. Peterson, and T.E. Kennedy Widespread expression of netrin-1 by neurons and oligodendrocytes in the adult mammalian spinal cord J Neurosci 21 2001 3911 3922
10. T. Goldschmidt, J. Antel, F.B. Konig, W. Bruck, and T. Kuhlmann Remyelination capacity of the MS brain decreases with disease chronicity Neurology 72 2009 1914 1921
11. R. Patani, M. Balaratnam, A. Vora, and R. Reynolds Remyelination can be extensive in multiple sclerosis despite a long disease course Neuropathol Appl Neurobiol 33 2007 277 287
12. J.M. Gensert, and J.E. Goldman Endogenous progenitors remyelinate demyelinated axons in the adult CNS Neuron 19 1997 197 203
13. V.E. Miron, T. Kuhlmann, and J.P. Antel Cells of the oligodendroglial lineage, myelination, and remyelination Biochim Biophys Acta 1812 2011 184 193
14. G. Piaton, A. Williams, D. Seilhean, and C. Lubetzki Remyelination in multiple sclerosis Prog Brain Res 175 2009 453 464
15. R.H. Miller, and S. Mi Dissecting demyelination Nat Neurosci 10 2007 1351 1354
16. G. Piaton, M.S. Aigrot, A. Williams, S. Moyon, V. Tepavcevic, I. Moutkine, J. Gras, K.S. Matho, A. Schmitt, H. Soellner, A.B. Huber, P. Ravassard, and C. Lubetzki Class 3 semaphorins influence oligodendrocyte precursor recruitment and remyelination in adult central nervous system Brain 134 2011 1156 1167
17. A. Williams, G. Piaton, M.S. Aigrot, A. Belhadi, M. Theaudin, F. Petermann, J.L. Thomas, B. Zalc, and C. Lubetzki Semaphorin 3A and 3F: key players in myelin repair in multiple sclerosis? Brain 130 2007 2554 2565
18. R.C. Armstrong Isolation and characterization of immature oligodendrocyte lineage cells Methods 16 1998 282 292
19. V.E. Miron, C.G. Jung, H.J. Kim, T.E. Kennedy, B. Soliven, and J.P. Antel FTY720 modulates human oligodendrocyte progenitor process extension and survival Ann Neurol 63 2008 61 71
20. K. Wosik, J. Antel, T. Kuhlmann, W. Bruck, B. Massie, and J. Nalbantoglu Oligodendrocyte injury in multiple sclerosis: a role for p53 J Neurochem 85 2003 635 644
21. T.E. Kennedy, H. Wang, W. Marshall, and M. Tessier-Lavigne Axon guidance by diffusible chemoattractants: a gradient of netrin protein in the developing spinal cord J Neurosci 26 2006 8866 8874
22. T.E. Kennedy, T. Serafini, J.R. de la Torre, and M. Tessier-Lavigne Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord Cell 78 1994 425 435
23. F. Mille, F. Llambi, C. Guix, C. Delloye-Bourgeois, C. Guenebeaud, S. Castro-Obregon, D.E. Bredesen, C. Thibert, and P. Mehlen Interfering with multimerization of netrin-1 receptors triggers tumor cell death Cell Death Differ 16 2009 1344 1351
24. K.E. Horn, S.D. Glasgow, D. Gobert, S.J. Bull, T. Luk, J. Girgis, M.E. Tremblay, D. McEachern, J.F. Bouchard, M. Haber, E. Hamel, P. Krimpenfort, K.K. Murai, A. Berns, G. Doucet, C.A. Chapman, E.S. Ruthazer, and T.E. Kennedy DCC expression by neurons regulates synaptic plasticity in the adult brain Cell Rep 3 2013 173 185
25. S. Rajasekharan, and T.E. Kennedy The netrin protein family Genome Biol 10 2009 239
26. K. Keino-Masu, M. Masu, L. Hinck, E.D. Leonardo, S.S. Chan, J.G. Culotti, and M. Tessier-Lavigne Deleted in colorectal cancer (DCC) encodes a netrin receptor Cell 87 1996 175 185
27. E.D. Leonardo, L. Hinck, M. Masu, K. Keino-Masu, S.L. Ackerman, and M. Tessier-Lavigne Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors Nature 386 1997 833 838
28. E. Stein, Y. Zou, M. Poo, and M. Tessier-Lavigne Binding of DCC by netrin-1 to mediate axon guidance independent of adenosine A2B receptor activation Science 291 2001 1976 1982
29. R.K. Tadagavadi, W. Wang, and G. Ramesh Netrin-1 regulates Th1/Th2/Th17 cytokine production and inflammation through UNC5B receptor and protects kidney against ischemia-reperfusion injury J Immunol 185 2010 3750 3758
30. A. Colavita, and J.G. Culotti Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans Dev Biol 194 1998 72 85
31. K. Hong, L. Hinck, M. Nishiyama, M.M. Poo, M. Tessier-Lavigne, and E. Stein A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion Cell 97 1999 927 941
32. K. Keleman, and B.J. Dickson Short- and long-range repulsion by the Drosophila Unc5 netrin receptor Neuron 32 2001 605 617
33. W. Wang, W.B. Reeves, and G. Ramesh Netrin-1 and kidney injury, I: netrin-1 protects against ischemia-reperfusion injury of the kidney Am J Physiol Renal Physiol 294 2008 F739 F747
34. P.V. Ranganathan, C. Jayakumar, R. Mohamed, Z. Dong, and G. Ramesh Netrin-1 regulates the inflammatory response of neutrophils and macrophages, and suppresses ischemic acute kidney injury by inhibiting COX-2-mediated PGE2 production Kidney Int 83 2013 1087 1098
35. P.V. Ranganathan, C. Jayakumar, and G. Ramesh Netrin-1-treated macrophages protect the kidney against ischemia-reperfusion injury and suppress inflammation by inducing M2 polarization Am J Physiol Renal Physiol 304 2013 F948 F957
36. C.M. Aherne, C.B. Collins, J.C. Masterson, M. Tizzano, T.A. Boyle, J.A. Westrich, J.A. Parnes, G.T. Furuta, J. Rivera-Nieves, and H. Eltzschig Neuronal guidance molecule netrin-1 attenuates inflammatory cell trafficking during acute experimental colitis Gut 61 2012 695 705
37. Y. Han, Y. Shao, Z. Lin, Y.L. Qu, H. Wang, Y. Zhou, W. Chen, Y. Chen, W.L. Chen, F.R. Hu, W. Li, and Z. Liu Netrin-1 simultaneously suppresses corneal inflammation and neovascularization Invest Ophthalmol Vis Sci 53 2012 1285 1295
38. V. Mirakaj, D. Gatidou, C. Potzsch, K. Konig, and P. Rosenberger Netrin-1 signaling dampens inflammatory peritonitis J Immunol 186 2011 549 555
39. V. Mirakaj, C.A. Thix, S. Laucher, C. Mielke, J.C. Morote-Garcia, M.A. Schmit, J. Henes, K.E. Unertl, D. Kohler, and P. Rosenberger Netrin-1 dampens pulmonary inflammation during acute lung injury Am J Respir Crit Care Med 181 2010 815 824
40. C. Mutz, V. Mirakaj, D.A. Vagts, P. Westermann, K. Waibler, K. Konig, T. Iber, G. Noldge-Schomburg, and P. Rosenberger The neuronal guidance protein netrin-1 reduces alveolar inflammation in a porcine model of acute lung injury Crit Care 14 2010 R189
41. N.P. Ly, K. Komatsuzaki, I.P. Fraser, A.A. Tseng, P. Prodhan, K.J. Moore, and T.B. Kinane Netrin-1 inhibits leukocyte migration in vitro and in vivo Proc Natl Acad Sci U S A 102 2005 14729 14734
42. P. Ranganathan, C. Jayakumar, M. Santhakumar, and G. Ramesh Netrin-1 regulates colon-kidney cross talk through suppression of IL-6 function in a mouse model of DSS-colitis Am J Physiol Renal Physiol 304 2013 F1187 F1197
43. J.M. van Gils, M.C. Derby, L.R. Fernandes, B. Ramkhelawon, T.D. Ray, K.J. Rayner, S. Parathath, E. Distel, J.L. Feig, J.I. Alvarez-Leite, A.J. Rayner, T.O. McDonald, K.D. O'Brien, L.M. Stuart, E.A. Fisher, A. Lacy-Hulbert, and K.J. Moore The neuroimmune guidance cue netrin-1 promotes atherosclerosis by inhibiting the emigration of macrophages from plaques Nat Immunol 13 2012 136 143
44. B. Ramkhelawon, Y. Yang, J.M. van Gils, B. Hewing, K.J. Rayner, S. Parathath, L. Guo, S. Oldebeken, J.L. Feig, E.A. Fisher, and K.J. Moore Hypoxia induces netrin-1 and unc5b in atherosclerotic plaques: mechanism for macrophage retention and survival Arterioscler Thromb Vasc Biol 33 2013 1180 1188
45. C. Delloye-Bourgeois, D. Goldschneider, A. Paradisi, G. Therizols, S. Belin, S. Hacot, M. Rosa-Calatrava, J.Y. Scoazec, J.J. Diaz, A. Bernet, and P. Mehlen Nucleolar localization of a netrin-1 isoform enhances tumor cell proliferation Sci Signal 5 2012 ra57
46. M. Koch, J.R. Murrell, D.D. Hunter, P.F. Olson, W. Jin, D.R. Keene, W.J. Brunken, and R.E. Burgeson A novel member of the netrin family, beta-netrin, shares homology with the beta chain of laminin: identification, expression, and functional characterization J Cell Biol 151 2000 221 234
47. K. Low, M. Culbertson, F. Bradke, M. Tessier-Lavigne, and M.H. Tuszynski Netrin-1 is a novel myelin-associated inhibitor to axon growth J Neurosci 28 2008 1099 1108
48. C. Manitt, K.M. Thompson, and T.E. Kennedy Developmental shift in expression of netrin receptors in the rat spinal cord: predominance of UNC-5 homologues in adulthood J Neurosci Res 77 2004 690 700
49. C. Manitt, D. Wang, T.E. Kennedy, and D.R. Howland Positioned to inhibit: netrin-1 and netrin receptor expression after spinal cord injury J Neurosci Res 84 2006 1808 1820