Skip to main content
SpringerLink
Log in

Collapsin response mediator proteins (CRMPs)

Involvement in nervous system development and adult neurodegenerative disorders

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

The members of the collapsin response mediator protein (CRMP) family—five cytosolic phosphoproteins—are highly expressed throughout brain development. The first member to be cloned, CRMP2, was identified as an intracellular messenger required for the growth cone-collapse induced by semaphorin 3A (Sema3A). A rapidly expanding body of study indicates that the functions of CRMPs are not solely limited to the signaling transduction of the Sema3A guidance cue. They are probably involved in multiple cellular and molecular events involved in apoptosis/proliferation, cell migration, and differentiation. In the adult brain, the expression of CRMPs is dramatically downregulated. However, they remain expressed in structures that retain their capacity for differentiation and plasticity and also in a subpopulation of oligodendrocytes (CRMP2 and CRMP5). Moreover, the expression of CRMPs is altered in neurodegenerative diseases, and these proteins may be of key importance in the physiopathology of the adult nervous system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Goshima Y., Nakamura F., Strittmatter P., and Strittmatter S.M. (1995) Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 376(6540), 509–514.

    Article  PubMed  CAS  Google Scholar 

  2. Luo Y., Raible D., and Raper J.A. (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75(2), 217–227.

    Article  PubMed  CAS  Google Scholar 

  3. Minturn J.E., Geschwind D.H., Fryer H.J.L., and Hockfield S. (1995) Early postmitotic neurons transiently express TOAD-64, a neural specific protein. J. Comp. Neurol. 355(3), 369–379.

    Article  PubMed  CAS  Google Scholar 

  4. Minturn J.E., Fryer H.J.L., Geschwind D.H., and Hockfield S. (1995) TOAD-64, a gene expressed early in neuronal differentiation in the rat, is related to unc-33, a C. elegans gene involved in axon outgrowth. J. Neurosci. 15(10), 6757–6766.

    PubMed  CAS  Google Scholar 

  5. Gaetano C., Matsuo T., and Thiele C.J. (1997) Identification and characterisation of a retinoïc acid-regulated human homologue of the hUlip from neuroblastoma cells. J. Biol. Chem. 272(18), 12,195–12,201.

    Article  CAS  Google Scholar 

  6. Scott B.W., Wang S., Burnham W.M., De Boni U., and Wojtowicz J.M. (1998) Kindling-induced neurogenesis in the dentate gyrus of the rat. Neurosci. Lett. 248(2), 73–76.

    Article  PubMed  CAS  Google Scholar 

  7. Nacher J., Rosell D.R., and McEwen B.S. (2000) Widespread expression of rat collapsin response-mediated protein 4 in the telencephalon and other areas of the adult rat central nervous system. J. Comp. Neurol. 424(4), 628–639.

    Article  PubMed  CAS  Google Scholar 

  8. Cameron H.A. and McKay R.D. (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435(4), 406–417.

    Article  PubMed  CAS  Google Scholar 

  9. Byk T., Dobransky T., Cifluentes-Diaz C., and Sobel A. (1996) Identification and molecular characterization of Unc-33-like phosphoprotein (Ulip), a putative mammalian homolog of the axonal guidance-associated unc-33 gene product. J. Neurosci. 16(2), 688–701.

    PubMed  CAS  Google Scholar 

  10. Wang L.H. and Strittmatter S.M. (1996) A family of rat CRMP genes is differentially expressed in the nervous system. J. Neurosci. 16(19), 6197–6207.

    PubMed  CAS  Google Scholar 

  11. Hamajima N., Matsuda K., Sakata S., Tamaki M., and Nonaka M. (1996) A novel gene family defined by human dihydropyrimidinase and three related proteins with differential tissue distribution. Gene 180(1–2), 157–163.

    Article  PubMed  CAS  Google Scholar 

  12. Byk T., Ozon S., and Sobel A. (1998) The Ulip family phosphoproteins. Eur. J. Biochem. 254(1), 14–24.

    Article  PubMed  CAS  Google Scholar 

  13. Horiuchi M., El Far O., and Betz H. (2000) Ulip6, a novel unc-33 and dihydropyrimidinase related protein highly expressed in developing rat brain. FEBS Lett. 480(2–3), 283–286.

    Article  PubMed  CAS  Google Scholar 

  14. Fukada M., Watakabe I., Yuasa-Kawada J., Kawachi H., Kuroiwa A., Matsuda Y., et al. (2000) Molecular characterization of CRMP5, a novel member of the collapsin response mediator protein family. J. Biol. Chem. 275(48), 37,957–37,965.

    Article  CAS  Google Scholar 

  15. Inatome R., Tsujimura T., Hitomi T., Hermann P., Kuroda S., Yamamura H., et al. (2000) Identification of CRAM, a novel Unc33 gene family that associates with CRMP3 and protein-tyrosine kinase(s) in the developing rat brain. J. Biol. Chem. 275(35), 27,291–27,302.

    CAS  Google Scholar 

  16. Ricard D., Rogemond V., Charrier E., Aguera M., Bagnard D., Belin M.F., et al. (2001) 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. 21(18), 7203–7214.

    PubMed  CAS  Google Scholar 

  17. Quach T.T., Rong Y., Belin M.F., Duchemin A.M., Akakoa H., Ding S., et al. (1997) Molecular cloning and expression of a new unc-33 like cDNA from rat brain and its relation to paraneoplastic neurological syndromes. Brain Res. Mol. Brain Res. 46(1–2), 329–332.

    Article  PubMed  CAS  Google Scholar 

  18. Antoine J.C., Honnorat J., Vocanson C., Koenig F., Aguera M., Belin M.F. (1993) Posterior uveitis, paraneoplastic encephalomyelitis and auto-antibodies reacting with developmental protein of brain and retina. J. Neurol. Sci. 117(1–2), 215–223.

    Article  PubMed  CAS  Google Scholar 

  19. Honnorat J., Antoine J.C., Derrington E.A., Aguera M., and Belin M.F. (1996) Antibodies to a subpopulation of glial cells and a 66 kD developmental protein in patients with paraneoplastic neurological syndromes. J. Neurol. Neurosurg. Psychiatry 61(3), 270–278.

    PubMed  CAS  Google Scholar 

  20. Honnorat J., Rogemond, V., Byk T., Kusters I., Aguera M., Ricard D., Rogemend V., et al. (1999) Ulip/CRMP proteins are recognized by autoantibodies in paraneoplasic neurological syndromes. Eur. J. Neurosci. 11(12), 4226–4232.

    Article  PubMed  CAS  Google Scholar 

  21. Quach T.T., Mosinger B. Jr, Ricard D., Copeland N.G., Gilbert D.J., Jenkins N.A., et al. (2000) Collapsin response mediator protein-3/unc-33-like protein-4 gene: organization, chromosomal mapping and expression in the developing mouse brain. Gene 242(1–2), 175–182.

    Article  PubMed  CAS  Google Scholar 

  22. Wang L.H. and Strittmatter S.M. (1997) Brain CRMP forms heterotetramers similar to liver dihydropyrimidinase. J. Neurochem. 69(6), 2261–2269.

    Article  PubMed  CAS  Google Scholar 

  23. Kamata T., Subleski M., Hara Y., Yuhki N., Kung H., Copeland N.G., Jenkins N.A., Yoshimura T., Modi W., and Copeland T.D. (1998) Isolation and characterization of a bovine neural specific protein (CRMP-2) cDNA homologous to unc-33, a C. elegans gene implicated in axonal outgrowth and guidance. Brain Res. Mol. Brain Res. 54(2), 219–236.

    Article  PubMed  CAS  Google Scholar 

  24. Takemoto T., Sasaki Y., Hamajima N., Goshima Y., Nonaka M., and Kimura H. (2000) Cloning and characterization of the Caenorhabditis elegans CeCRMP/DHP-1 and -2; common ancestors of CRMP and dihydropyrimidinase? Gene 261(2), 259–267.

    Article  PubMed  CAS  Google Scholar 

  25. Geschwind D.H., Kelly G.M., Fryer H., Feeser-Bhatt H., and Hockfield S. (1996) Identification and characterization of novel developmentally regulated proteins in rat spinal cord. Brain Res. Dev. Brain Res. 97(1), 62–75.

    Article  PubMed  CAS  Google Scholar 

  26. Honnorat J., Aguera M., Zalc B., Goujet C., Quach T., Antoine J.C., et al. (1998) POP66, a paraneoplastic encephalomyelitis-related antigen, is a marker of adult oligodendrocytes. J. Neuropathol. Exp. Neurol. 57(4), 311–322.

    Article  PubMed  CAS  Google Scholar 

  27. Yoshida H., Watanabe A., and Ihara Y. (1998) CRMP-2 is associated with neurofibrillary tangles in Alzheimer’s disease. J. Biol. Chem. 273(16), 9761–9768.

    Article  PubMed  CAS  Google Scholar 

  28. Kamata T., Daar I.O., Subleski M., Copeland T., Kung H.F., and Xu R.H. (1998) Xenopus CRMP-2 is an early response gene to neural induction. Brain Res. Mol. Brain Res. 57(2), 201–210.

    Article  PubMed  CAS  Google Scholar 

  29. Ricard D., Stankoff B., Bagnard D., Aguera M., Rogemond V., Antoine J.C., et al. (2000) Differential expression of CRMP/Ulip proteins in subsets of oligodendrocytes in the post-natal rodent brain. Mol. Cell. Neurosci. 16(4), 324–337.

    Article  PubMed  CAS  Google Scholar 

  30. Pasterkamp R.J., De Winter F., Holtmaat A.J.G.D., and Verhaagen J. (1998) Evidence for a role of the chemorepellent semaphorin III and its receptor neuropilin-1 in the regeneration of primary olfactory axons. J. Neurosci. 18(23), 9962–9976.

    PubMed  CAS  Google Scholar 

  31. Jourdan F., Veyrac A., Charrier E., Reymond-Marron I., Aguera M., Belin M. F., et al. (2002) Differential neuronal expression of Ulip/CRMP in the regenerating olfactory epithelium following lesions of the olfactory nerve in the adult mouse. Abstract 3rd Forum of European Neuroscience, Paris, 2002.

  32. Antoine J.C., Honnorat J., Camdessanche J.P., Magistris M., Absi L., Mosnier J.F., et al. (2001) Paraneoplastic anti-CV2 antibodies react with peripheral nerve and are associated with a mixed axonal and demyelinating peripheral neuropathy. Ann. Neurol. 49(2), 214–221.

    Article  PubMed  CAS  Google Scholar 

  33. Taketo M.M., Araki Y., Matsunaga A., Yokoi A., Tsuchida J., Nishina Y., et al. (1997) Mapping of eight testis specific genes to mouse chromosomes. Genomics 46(1), 138–142.

    Article  PubMed  CAS  Google Scholar 

  34. Kato Y., Hamajima N., Inagaki H., Okumura N., Koji T., Sasaki M., et al. (1998) Post-meiotic expression of the mouse dihydropyrimidinase related protein 3 gene during spermiogenesis. Mol. Reprod. Dev. 51(1), 105–111.

    Article  PubMed  CAS  Google Scholar 

  35. Branda C.S. and Stern M. J. (2000) Mechanisms controlling sex myoblast migration in Caenorhabditis elegans hermaphrodites. Dev. Biol. 226(1), 137–151.

    Article  PubMed  CAS  Google Scholar 

  36. Ito T., Kagoshima M., Sasaki Y., Li C., Udaka N., Kitsukawa T., et al. (2000) Repulsive axon guidance molecule Sema3A inhibits branching morphogenesis of fetal mouse lung. Mech. Dev. 97(1–2), 35–45.

    Article  PubMed  CAS  Google Scholar 

  37. Rouzaut A., Lopez-Moratalla N., and De Miguel C. (2000) Differential gene expression in the activation and maturation of human monocytes. Arch. Biochem. Biophys. 374(2), 153–160.

    Article  PubMed  CAS  Google Scholar 

  38. Inagaki N., Chihara K., Arimura N., Menager C., Kawano Y., Matsuo N., et al. (2001) CRMP-2 induces axons in cultured hippocampal neurons. Nat. Neurosci. 4(8), 781–782.

    Article  PubMed  CAS  Google Scholar 

  39. Lee S., Kim J.H., Lee C.S., Kim J.H., Kim Y., Heo K., et al. (2002) Collapsin response mediator protein-2 inhibits neuronal phospholipase D(2) activity by direct interaction. J. Biol. Chem. 277(8), 6542–6549.

    Article  PubMed  CAS  Google Scholar 

  40. Hedgecock E.M., Culotti J.G., Thomson J.N., and Perkins L.A. (1985) Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev. Biol. 111(1), 158–170.

    Article  PubMed  CAS  Google Scholar 

  41. Bagnard D., Lohrum M., Uziel D., Püschel A.W., and Bolz J. (1998) Semaphorins as attractive and repulsive guidance signals during the development of cortical projections. Development 125(24), 5043–5053.

    PubMed  CAS  Google Scholar 

  42. Tessier-lavigne M. and Goodman C.S. (1996) The molecular biology of axon guidance. Science 274(5290), 1123–1133.

    Article  PubMed  CAS  Google Scholar 

  43. Liu B.P. and Strittmatter S.M. (2001) Semaphorinmediated axonal guidance via Rho-related G proteins. Curr. Opin. Cell. Biol. 13(5), 619–626.

    Article  PubMed  CAS  Google Scholar 

  44. He Z. and Tessier-Lavigne M. (1997) Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell 90(4), 739–751.

    Article  PubMed  CAS  Google Scholar 

  45. Kolodkin A.L., Levengood D.V., Rowe E.G., Tai Y.T., Giger R.J., and Ginty D.D. (1997) Neuropilin is a semaphorin III receptor. Cell 90(4), 753–762.

    Article  PubMed  CAS  Google Scholar 

  46. Takahashi T., Fournier A., Nakamura F., Wang L.H., Murakami Y., Kalb R.G., et al. (1999) Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99(1), 59–69.

    Article  PubMed  CAS  Google Scholar 

  47. Nakamura F., Kalb R.G., and Strittmatter S. M. (2000) Molecular basis of semaphorin-mediated axon guidance. J. Neurobiol. 44(2), 219–229.

    Article  PubMed  CAS  Google Scholar 

  48. Rohm B., Ottemeyer A., Lohrum M., and Püschel A.W. (2000) Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A. Mech. Dev. 93(1–2), 95–104.

    Article  PubMed  CAS  Google Scholar 

  49. Takahashi T. and Strittmatter S.M. (2001) Plexin A1 autoinhibition by the plexin sema domain. Neuron 29(2), 429–439.

    Article  PubMed  CAS  Google Scholar 

  50. Mitsui N., Inatome R., Takahashi S., Goshima Y., Yamamura H., and Yanagi S. (2002) Involvement of Fes/FPS tyrosine kinase in semaphorin3A signaling. EMBO J. 21(13), 3274–3285.

    Article  PubMed  CAS  Google Scholar 

  51. Moolenaar W.H. (2000) Development of our current understanding of bioactive lysophospholipids. Ann. NY Acad. Sci. 905, 1–10.

    Article  PubMed  CAS  Google Scholar 

  52. Chun J., Weiner J.A., Fukushima N., Contos J.J., Zhang G., Kimura Y., et al. (2000) Neurobiology of receptor-mediated lysophospholipid signaling. From the first lysophospholipid receptor to roles in nervous system function and development. Ann. NY Acad. Sci. 905, 110–117.

    Article  PubMed  CAS  Google Scholar 

  53. Arimura N., Inagaki N., Chihara K., Ménager C., Nakamura N., Iwamatsu A., et al. (2000) Phosphorylation of CRMP-2 by Rho-kinase:evidence for two separate signaling pathways for growth cone collapse. J. Biol. Chem. 275(31), 23,973–23,980.

    Article  CAS  Google Scholar 

  54. Jin Z. and Strittmatter S.M. (1997) Rac1 mediates collapsin1 induced growth cone collapse. J. Neurosci. 17(16), 6256–6263.

    PubMed  CAS  Google Scholar 

  55. Kuhn T.B., Brown M.D., Wilcox C.L., Raper J.A., and Bamburg J.R. (1999) Myelin and collapsin-1 induce motor neuron growth cone collapse through different pathways: inhibition of collapse by opposing mutants of Rac1. J. Neurosci. 19(6), 1965–1975.

    PubMed  CAS  Google Scholar 

  56. Nishiki T., Narumiya S., Morii N., Yamamoto M., Fujiwara M., Kamata Y., et al. (1990) ADP-ribosylation of the rho/rac proteins induces growth inhibition, neurite outgrowth and acetylcholine esterase in cultured PC-12 cells. Biochem. Biophys. Res. Commun. 167(1), 265–272.

    Article  PubMed  CAS  Google Scholar 

  57. Jalink K., Van Corven E.J., Hengeveld T., Morii N., Narumiya S., and Moolenaar W.H. (1994) Inhibition of lysophosphatidate-and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell. Biol. 126(3), 801–810.

    Article  PubMed  CAS  Google Scholar 

  58. Tigyi G., Fischer D.J., Sebok A., Yang C., Dyer D.L., and Miledi R. (1996) Lysophosphatidic acid-induced neurite retraction in PC12 cells: control by phosphoinositide-Ca2+ signaling and Rho. J. Neurochem. 66(2), 537–548.

    Article  PubMed  CAS  Google Scholar 

  59. Amano M., Chihara K., Nakamura N., Fukata Y., Yano T., Shibata M., et al. (1998) Myosin II activation promotes neurite retraction during the action of Rho and Rho-kinase Genes Cells 3(3), 177–188.

    Article  PubMed  CAS  Google Scholar 

  60. Kranenburg O., Poland M., Van Horck F.P., Drechsel D., Hall A., and Moolenaar W.H. (1999) Activation of RhoA by lysophosphatidic acid and G alpha12/13 subunits in neuronal cells: induction of neurite retraction. Mol. Biol. Cell. 10(6), 1851–1857.

    PubMed  CAS  Google Scholar 

  61. Hall C., Brown M., Jacobs T., Ferrari G., Cann N., Teo M., et al. (2001) Collapsin response mediator protein switches RhoA and Rac1 morphology in N1E-115 neuroblastoma cells and is regulated by Rho kinase. J. Biol. Chem. 276(46), 43,482–43,486.

    Article  CAS  Google Scholar 

  62. Leung T., Ng Y., Cheong A., Ng C.H., Tan I., Hall C., et al. (2002) p80 ROKalpha binding protein is a navel variant of CRMP1 which associates with CRMP2 and modulates Rho-A-induced neuronal morphology. FEBS Lett. 523(3), 445–449.

    Article  Google Scholar 

  63. Cole R.N. and Hart G.W. (2001) Cytosolic O-glycosylation is abundant in nerve terminals. J. Neurochem. 79(5), 1080–1089.

    Article  PubMed  CAS  Google Scholar 

  64. Li W., Herman R.K., and Shaw J.E. (1992) Analysis of the Caenorhabditis elegans axonal guidance and outgrowth gene unc-33. Genetics 132(3), 675–689.

    PubMed  CAS  Google Scholar 

  65. Gu Y. and Ihara Y. (2000) Evidence that CRMP2 is involved in the dynamics of microtubules. J. Biol. Chem. 275(24), 17,917–17,920.

    Article  CAS  Google Scholar 

  66. Fukata Y., Itoh T.J., Kimura T., Ménager C., Nishimura T., Shiromizu T., et al. (2002) CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nature Cell. Biol. 4(8), 583–591.

    PubMed  CAS  Google Scholar 

  67. Fukata Y., Kimura T., and Kaibuchi K. (2002) Axon specification in hippocampal neurons. Neurosci. Res. 43(4), 305–315.

    Article  PubMed  CAS  Google Scholar 

  68. Goshima Y., Kawakami T., Hori H., Sugiyama Y., Takasawa S., Hashimoto Y., et al. (1997) A novel action of collapsin: collapsin-1 increases antero- and retrograde axoplasmic transport independently of growth cone collapse. J. Neurobiol. 33(3), 316–328.

    Article  PubMed  CAS  Google Scholar 

  69. Shirvan A., Fleminger G., Shina R., He Z., Brudo I., Melamed E., et al. (1999) Semaphorins as mediators of neuronal apoptosis. J. Neurochem. 73(3), 961–971.

    Article  PubMed  CAS  Google Scholar 

  70. Galiardini V. and Fankhauser C. (1999) Semaphorin III can induce death in sensory neurons. Mol. Cell. Neurosci. 14(4–5), 301–316.

    Article  Google Scholar 

  71. Barzilai A., Zilkha-Falb R., Daily D., Stern N., Offen D., Ziv I., et al. (2000) The molecular mechanism of dopamine-induced apoptosis: identification and characterization of genes that mediate dopamine toxicity. J. Neural Transm. Suppl. 60, 59–76.

    PubMed  Google Scholar 

  72. Bagnard D., Vaillant C., Khuth S., Dufay N., Lohrum M., Püschel A., et al. (2001) Sema3A/VEGF165 balance mediates migration and apoptosis of neural progenitor cells by the recrutment of shared receptors. J. Neurosci. 21(10), 3332–3341.

    PubMed  CAS  Google Scholar 

  73. Franken S., Junghans U., Rosslenbroich V., Baader S.L., Hoffman R., Gieselmann V., et al. (2002) Collapsin Response Mediator Proteins of neonatal brain interact with chondroitin sulfate. J. Biol. Chem. 278(5), 3241–3250.

    Article  PubMed  CAS  Google Scholar 

  74. Bermingham J.R. Jr, Shumas S., Whisenhunt T., Rosenfeld M.G., and Scherer S.S. (2001) Modification of representational difference analysis applied to the isolation of forskolin-regulated genes from Schwann cells. J. Neurosci. Res. 63(6), 516–524.

    Article  PubMed  CAS  Google Scholar 

  75. Weiner J.A., Hecht J.H., and Chun J. (1998) Lysophosphatidic receptor gene vzg-1/lpA1/edg-2 is expressed by mature oligodendrocytes during myelination in the postnatal murine brain. J. Comp. Neurol. 398(4), 587–598.

    Article  PubMed  CAS  Google Scholar 

  76. Cervera P., Tirard M., Barron S., Allard J., Trottier S., Lacombe J., et al. (2002) Immunohistological localization of the myelinating cell-specific receptor LP (A1). Glia 38(2), 126–136.

    Article  PubMed  Google Scholar 

  77. Stankoff B., Barron S., Allard J., Barbin G., Noel F., Aigrot M.S., et al. (2002) Oligodendroglial expression of Edg-2 receptor: developmental analysis and pharmacological responses to lysophosphatidic acid. Mol. Cell. Neurosci. 20(3), 415–428.

    Article  PubMed  CAS  Google Scholar 

  78. Weiner J.A. and Chun J. (1999) Schwann cells survival mediated by the signaling phospholipid lysophosphatidic acid. Proc. Natl. Acad. Sci. USA 96(9), 5233–5238.

    Article  PubMed  CAS  Google Scholar 

  79. Möller T., Musante D.B., and Ransom B.R. (1999) Lysophosphatidic acid-induced calcium signals in cultured rat oligodendrocytes. NeuroReport 10(14), 2929–2932.

    Article  PubMed  Google Scholar 

  80. Weiner J.A., Fukushima N., Contos J.J., and Chun J. (2001) Regulation of Schwann cells morphology and adhesion by receptor-mediated lysophosphatidic acid signaling. J. Neurosci. 21(18), 7069–7078.

    PubMed  CAS  Google Scholar 

  81. Yoshimura Y., Shinkawa T., Taoka M., Kobayashi K., Isobe T., and Yamauchi T. (2002) Identification of protein substrates of Ca(2+)/calmodulin-dependent protein kinase Il in the postsynaptic density by protein sequencing and mass spectrometry. Biochem. Biophys. Res. Commun. 290(3), 948–954.

    Article  PubMed  CAS  Google Scholar 

  82. Wong C.C. and Leung M.S. (2001) Effects of neonatal hypothyroidism on the expressions of growth cone proteins and axon guidance molecules related genes in the hippocampus. Mol. Cell. Endocrinol. 184(1–2), 143–150.

    Article  PubMed  CAS  Google Scholar 

  83. Lubec G., Nonaka M., Krapfenbauer K., Gratzer M., Cairns N., and Fountoulakis M. (1999) Expression of the dihydropyrimidinase related protein 2 (DRP-2) in Down syndrome and Alzheimer’s disease brain is downregulated at the mRNA and dysregulated at the protein level. J. Neural Transm. Suppl. 57, 161–177.

    PubMed  CAS  Google Scholar 

  84. Gu Y., Hamajima N., and Ihara Y. (2000) Neurofibrillary tangle associated CRMP-2 is highly phosphorylated on thr-509, ser-518 and ser-552. Biochemistry 39(15), 4267–4275.

    Article  PubMed  CAS  Google Scholar 

  85. Castegna A., Aksenov M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., et al. (2002) Proteomic identification of oxidatively modified proteins in Alzheimer’s disease brain. Part II: dihydropyrimidinase-related-protein 2, alpha-enolase and heat shock cognate 71. J. Neurochem. 82(6), 1524–1532.

    Article  PubMed  CAS  Google Scholar 

  86. Bulliard C., Zurbriggen R., Tornare J., Faty M., Dastoor Z., and Dreyer J.L. (1997) Purification of a dichlorophenol-indophenol oxidoreductase from rat and bovine synaptic membranes: tight complex association of a glyceraldehyde-3-phosphate dehydrogenase isoform, TOAD64, enolase-gamma and aldolase C. Biochem. J. 324, 555–563.

    PubMed  CAS  Google Scholar 

  87. Rogemond V. and Honnorat J. (2000) Anti-CV2 autoantibodies and paraneoplastic neurological syndromes. Clin. Rev. Allergy Immunol. 19(1), 51–59.

    Article  PubMed  CAS  Google Scholar 

  88. Yu Z., Kryzer T.J., Griesmann G.E., Kim K., Benarroch E.E., and Lennon V.A. (2001) CRMP-5 neuronal autoantibody: marker of lung cancer and thymoma-related autoimmunity. Ann. Neurol. 49(2), 146–154.

    Article  PubMed  CAS  Google Scholar 

  89. Shih J.Y., Yang S.C., Hong T.M., Yuan A., Chen J.J., Yu C.J., et al. (2001) Collapsin response mediator protein-1 and the invasion and metastasis of cancer cells. J. Natl. Cancer Inst. 93(18), 1392–1400.

    Article  PubMed  CAS  Google Scholar 

  90. Eickholt B.J., Mackenzie S.L., Graham A., Walsh F.S., and Doherty P. (1999) Evidence for collapsin-1 functioning in the control of neural crest migration in both trunk and hindbrain regions. Development 126(10), 2181–2189.

    PubMed  CAS  Google Scholar 

  91. Miao H.Q., Soker S., Feiner L., Alonso J.L., Raper J.A., Klagsbrun M. (1999) Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J. Cell. Biol. 146(1), 233–242.

    Article  PubMed  CAS  Google Scholar 

  92. Johnston-Wilson N.L., Sims C.D., Hofmann J.P., Anderson L., Shore A.D., Torrey E.F., et al. (2000) Disease-specific alterations in frontal cortex brain proteins in schizophrenia, bipolar disorder, and major depressive disorder. The Stanley Neuropathology Consortium. Mol. Psychiatry 5(2), 142–149.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut National de la Santé et de la Recherche Médicale U 433, Hôpital Neurologique, 59 Bd Pinel, 69003, Lyon, France

    Emmanuelle Charrier, Sophie Reibel, Véronique Rogemond, Michèle Aguera, Nicole Thomasset & Jérôme Honnorat

Authors
  1. Emmanuelle Charrier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sophie Reibel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Véronique Rogemond
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michèle Aguera
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicole Thomasset
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jérôme Honnorat
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jérôme Honnorat.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Charrier, E., Reibel, S., Rogemond, V. et al. Collapsin response mediator proteins (CRMPs). Mol Neurobiol 28, 51–63 (2003). https://doi.org/10.1385/MN:28:1:51

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1385/MN:28:1:51

Index Entries

Search

Navigation