The collapsin response mediator protein 5 onconeural protein is expressed in Schwann cells under axonal signals and regulates Axon-Schwann cell interactions

Journal of Neuropathology and Experimental Neurology

Volumn 71, Issue 4, 2012, Pages 298-311

  Camdessanché, Jean Philippe ^a,b,c,d   Ferraud, Karine ^a,c,d   Boutahar, Nadia ^a,d   Lassablière, François ^a   Mutter, Marie ^a,b   Touret, Monique ^b   Kolattukudy, Pappachan ^e   Honnorat, Jérôme ^b,c   Antoine, Jean Christophe ^a,b,c,d  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c HÔPITAL NEUROLOGIQUE   (France)

^d UNIVERSITY HOSPITAL OF SAINT ETIENNE   (France)

^e UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

CRMP5; Paraneoplastic neurologic syndromes; Peripheral neuropathy; Schwann cells

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN 5; CYCLIC AMP; FORSKOLIN; NEU DIFFERENTIATION FACTOR; SEMAPHORIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CELL MATURATION; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; ELECTRON MICROSCOPY; MORPHOMETRICS; MYELINATION; NERVE FIBER; NERVE REGENERATION; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SCHWANN CELL; SCIATIC NERVE; UPREGULATION; WESTERN BLOTTING;

AMIDOHYDROLASES; ANIMALS; ANIMALS, NEWBORN; AXONS; CELL COMMUNICATION; CELLS, CULTURED; COCULTURE TECHNIQUES; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; RATS; SCHWANN CELLS; SIGNAL TRANSDUCTION;

EID: 84859029361     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e31824d1df2     Document Type: Article

References (56)

1. Vincent A, Irani SR. Caspr2 antibodies inpatients with thymomas. J Thorac Oncol 2010;5:S277-80
2. Antoine JC, Honnorat J, Camdessanche JP, et al. Paraneoplastic anti-CV2 antibodies react with peripheral nerve and are associated with a mixed axonal and demyelinating peripheral neuropathy. Ann Neurol 2001;49: 214-21 (Pubitemid 32157997)
3. Honnorat J, Cartalat-Carel S, Ricard D, et al. Onco-neural antibodies and tumour type determine survival and neurological symptoms in paraneoplastic neurological syndromes with Hu or CV2/CRMP5 antibodies. J Neurol Neurosurg Psychiatry 2009;80:412-16
4. Hamajima N, Matsuda K, Sakata S, et al. A novel gene family defined by human dihydropyrimidinase and three related proteins with differential tissue distribution. Gene 1996;180:157-63 (Pubitemid 26417923)
5. Wang LH, Strittmatter SM. A family ofrat CRMP genes is differentially expressed in the nervous system. J Neurosci 1996;16:6197-6207 (Pubitemid 26313994)
6. Byk T, Dobransky T, Cifuentes-Diaz C, et al. Identification and molecular characterization of Unc-33Ylike phosphoprotein (Ulip), a putative mammalian homolog of the axonal guidance-associated unc-33 gene product. J Neurosci 1996;16:688-701
7. Goshima Y, Nakamura F, Strittmatter P, et al. Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 1995;376:509-14
8. Charrier E, Reibel S, Rogemond V, et al. Collapsin response mediator proteins (CRMPs): Involvement in nervous system development and adult neurodegenerative disorders. Mol Neurobiol 2003;28:51-64
9. Brown M, Jacobs T, Eickholt B, et al. alpha2-Chimaerin, cyclin-dependent kinase 5/p35, and its target collapsin response mediator protein-2 are essential components in semaphorin 3A-induced growth-cone collapse. J Neurosci 2004;24:8994-9004 (Pubitemid 39372244)
10. Mimura F, Yamagishi S, Arimura N, et al. Myelin-associated glycoprotein inhibits microtubule assembly by a Rho-kinase-dependent mechanism. J Biol Chem 2006;281:15970-79 (Pubitemid 43848490)
11. Rogemond V, Auger C, Giraudon P, et al. Processing and nuclear localization of CRMP2 during brain development induce neurite outgrowth inhibition. J Biol Chem 2008;283:14751-61
12. Zhou FQ, Cohan CS. How actin filaments and microtubules steer growth cones to their targets. J Neurobiol 2004;58:84-91 (Pubitemid 37543340)
13. Cole AR, Knebel A, Morrice NA, et al. GSK-3 phosphorylation ofthe Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J Biol Chem 2004;279:50176-80 (Pubitemid 39577830)
14. Arimura N, Inagaki N, Chihara K, et al. Phosphorylation ofcollapsin response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse. J Biol Chem 2000;275: 23973-80 (Pubitemid 30624686)
15. Ricard D, Stankoff B, Bagnard D, et al. Differential expression ofcollapsin response mediator proteins (CRMP/ULIP) in subsets of oligodendrocytes in the postnatal rodent brain. Mol Cell Neurosci 2000;16: 324-37
16. Ricard D, Rogemond V, Charrier E, et al. Isolation and expression pattern of human Unc-33-like phosphoprotein 6/collapsin response mediator protein 5 (Ulip6/CRMP5): Coexistence with Ulip2/CRMP2 in Sema3a-sensitive oligodendrocytes. J Neurosci 2001;21:7203-14 (Pubitemid 32846968)
17. Fukada M, Watakabe I, Yuasa-Kawada J, et al. Molecular characterization ofCRMP5, a novel member of the collapsin response mediator protein family. J Biol Chem 2000;275:37957-65 (Pubitemid 32004917)
18. Inatome R, Tsujimura T, Hitomi T, et al. Identification of CRAM, anovel unc-33 gene family protein that associates with CRMP3 and proteintyrosine kinase(s) in the developing rat brain. J Biol Chem 2000;275: 27291-302
19. Brot S, Rogemond V, Perrot V, et al. CRMP5 interacts with tubulin to inhibit neurite outgrowth, thereby modulating the function of CRMP2. J Neurosci 2010;30:10639-54
20. Veyrac A, Giannetti N, Charrier E, et al. Expression ofcollapsin response mediator proteins 1, 2 and 5 is differentially regulated in newly generated and mature neurons of the adult olfactory system. Eur J Neurosci 2005; 21:2635-48 (Pubitemid 40835107)
21. Yamashita N, Mosinger B, Roy A, et al. CRMP5 regulates dendritic development and synaptic plasticity in the cerebellar Purkinje cells. J Neurosci 2011;31:1773-79
22. Brockes JP, Raff MC. Studies oncultured rat Schwann cells. II. Comparison with a rat Schwann cell line. In Vitro 1979;15:772-78 (Pubitemid 10170783)
23. Seilheimer B, Schachner M. Studies ofadhesion molecules mediating interactions between cells of peripheral nervous system indicate a major role for L1 in mediating sensory neuron growth on Schwann cells in culture. J Cell Biol 1988;107:341-51
24. Bretin S, Reibel S, Charrier E, et al. Differential expression ofCRMP1, CRMP2A, CRMP2B, and CRMP5 in axons or dendrites of distinct neurons in the mouse brain. J Comp Neurol 2005;486:1-17 (Pubitemid 40571646)
25. Jessen KR, Mirsky R. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 2005;6:671-82 (Pubitemid 43160316)
26. Simons M, Trotter J. Wrapping itup: The cell biology of myelination. Curr Opin Neurobiol 2007;17:533-40
27. Le Douarin N, Dulac C, Dupin E, et al. Glial cell lineages inthe neural crest. Glia 1991;4:175-84
28. Zorick TS, Lemke G. Schwann cell differentiation. Curr Opin Cell Biol 1996;8:870-76 (Pubitemid 26399949)
29. Jessen KR, Mirsky R. Developmental regulation inthe Schwann cell lineage. Adv Exp Med Biol 1999;468:3-12
30. Mirsky R, Jessen KR. Schwann cell development, differentiation and myelination. Curr Opin Neurobiol 1996;6:89-96 (Pubitemid 26103367)
31. D'Antonio M, Michalovich D, Paterson M, et al. Gene profiling and bioinformatic analysis of Schwann cell embryonic development and myelination. Glia 2006;53:501-15
32. Chen ZL, Yu WM, Strickland S. Peripheral regeneration. Annu Rev Neurosci 2007;30:209-33 (Pubitemid 47218756)
33. Scherer SS. The biology and pathobiology of Schwann cells. Curr Opin Neurol 1997;10:386-97 (Pubitemid 27445627)
34. Akassoglou K, Yu WM, Akpinar P, et al. Fibrin inhibits peripheral nerve remyelination by regulating Schwann cell differentiation. Neuron 2002; 33:861-75 (Pubitemid 34246353)
35. Stoll G, Muller HW. Nerve injury, axonal degeneration and neural regeneration: Basic insights. Brain Pathol 1999;9:313-25 (Pubitemid 29157718)
36. Maurel P, Salzer JL. Axonal regulation ofSchwann cell proliferation and survival and the initial events of myelination requires PI 3-kinase activity. J Neurosci 2000;20:4635-45 (Pubitemid 30396629)
37. Winseck AK, Caldero J, Ciutat D, et al. In vivo analysis ofSchwann cell programmed cell death in the embryonic chick: Regulation by axons and glial growth factor. J Neurosci 2002;22:4509-21 (Pubitemid 37465667)
38. Touma E, Kato S, Fukui K, et al. Calpain-mediated cleavage ofcollapsin response mediator protein(CRMP)-2 during neurite degeneration in mice. Eur J Neurosci 2007;26:3368-81 (Pubitemid 350243516)
39. Coleman M. Axon degeneration mechanisms: Commonality amid diversity. Nat Rev Neurosci 2005;6:889-98 (Pubitemid 41568730)
40. Jiang SX, Kappler J, Zurakowski B, et al. Calpain cleavage ofcollapsin response mediator proteins in ischemic mouse brain. Eur J Neurosci 2007; 26:801-9 (Pubitemid 47274611)
41. Hou ST, Jiang SX, Desbois A, et al. Calpain-cleaved collapsin response mediator protein-3 induces neuronal death after glutamate toxicity and cerebral ischemia. J Neurosci 2006;26:2241-49 (Pubitemid 44699033)
42. Nave KA, Salzer JL. Axonal regulation ofmyelination by neuregulin 1. Curr Opin Neurobiol 2006;16:492-500
43. Michailov GV, Sereda MW, Brinkmann BG, et al. Axonal neuregulin-1 regulates myelin sheath thickness. Science 2004;304:700-3 (Pubitemid 38560869)
44. Taveggia C, Zanazzi G, Petrylak A, et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 2005;47:681-94 (Pubitemid 41208007)
45. Cheng L, Mudge AW. Cultured Schwann cells constitutively express the myelin protein P0. Neuron 1996;16:309-19 (Pubitemid 26072364)
46. Morgan L, Jessen KR, Mirsky R. The effects ofcAMP on differentiation of cultured Schwann cells: Progression from an early phenotype (04+) to a myelin phenotype (P0+, GFAP-, N-CAM-, NGF-receptor-) depends on growth inhibition. J Cell Biol 1991;112:457-67 (Pubitemid 21926000)
47. Dong Z, Dean C, Walters JE, et al. Response ofSchwann cells to mitogens in vitro is determined by pre-exposure to serum, time in vitro, and developmental age. Glia 1997;20:219-30 (Pubitemid 27324308)
48. Bermingham JR Jr, Shumas S, Whisenhunt T, et al. Modification ofrepresentational difference analysis applied to the isolation of forskolinregulated genes from Schwann cells. J Neurosci Res 2001;63:516-24 (Pubitemid 32193709)
49. Yamashita N, Morita A, Uchida Y, et al. Regulation ofspine development by semaphorin3A through cyclin-dependent kinase 5 phosphorylation of collapsin response mediator protein 1. J Neurosci 2007;27: 12546-54 (Pubitemid 350127813)
50. Su KY, Chien WL, Fu WM, et al. Mice deficient incollapsin response mediator protein-1 exhibit impaired long-term potentiation and impaired spatial learning and memory. J Neurosci 2007;27:2513-24
51. Hotta A, Inatome R, Yuasa-Kawada J, et al. Critical role ofcollapsin response mediator protein-associated molecule CRAM for filopodia and growth cone development in neurons. Mol Biol Cell 2005;16:32-9 (Pubitemid 40024288)
52. Yuasa-Kawada J, Suzuki R, Kano F, et al. Axonal morphogenesis controlled byantagonistic roles of two CRMP subtypes in microtubule organization. Eur J Neurosci 2003;17:2329-43 (Pubitemid 36793742)
53. Inagaki N, Chihara K, Arimura N, et al. CRMP-2 induces axons incultured hippocampal neurons. Nat Neurosci 2001;4:781-82 (Pubitemid 32702507)
54. Hoffman PN, Cleveland DW, Griffin JW, et al. Neurofilament gene expression: Amajor determinant of axonal caliber. Proc Natl Acad Sci USA 1987;84:3472-76 (Pubitemid 17085426)
55. Shea TB, Chan WK, Kushkuley J, et al. Organizational dynamics, functions, and pathobiological dysfunctions of neurofilaments. Results Probl Cell Differ 2009;48:29-45
56. Hahn AF, Whitaker JN, Kachar B, et al. P2, P1, and P0myelin protein expression in developing rat sixth nerve: A quantitative immunocytochemical study. J Comp Neurol 1987;260:501-12