Localized role of CRMP1 and CRMP2 in neurite outgrowth and growth cone steering

Developmental Neurobiology

Volumn 72, Issue 12, 2012, Pages 1528-1540

  Higurashi, Masakazu ^a   Iketani, Masumi ^a   Takei, Kohtaro ^a   Yamashita, Naoya ^a   Aoki, Reina ^a   Kawahara, Nobutaka ^a   Goshima, Yoshio ^a  

^a YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

CALI; CRMP1; CRMP2; Growth cone steering; Neurite outgrowth

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN 1; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; PHOSPHOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHICKEN; CYTOSKELETON; EMBRYO; GROWTH CONE; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; NERVE FIBER GROWTH; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SPINAL GANGLION;

ANIMALS; CHICK EMBRYO; GROWTH CONES; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NERVE TISSUE PROTEINS; NEURITES; NEUROGENESIS; PHOSPHOPROTEINS;

EID: 84865763268     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22017     Document Type: Article

References (46)

1. Arimura N, Inagaki N, Chihara K, Menager C, Nakamura N, Amano M, Iwamatsu A, et al. 2000. Phosphorylation of collapsin response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse. J Biol Chem 275: 23973-23980.
2. Arimura N, Menager C, Kawano Y, Yoshimura T, Kawabata S, Hattori A, Fukata Y, et al. 2005. Phosphorylation by Rho kinase regulates CRMP-2 activity in growth cones. Mol Cell Biol 25: 9973-9984.
3. Buck KB, Zheng JQ. 2002. Growth cone turning induced by direct local modification of microtubule dynamics. J Neurosci 22: 9358-9367.
4. Buel GR, Rush J, Ballif BA. 2010. Fyn promotes phosphorylation of collapsin response mediator protein 1 at tyrosine 504, a novel, isoform-specific regulatory site. J Cell Biochem 111: 20-28.
5. Challacombe JF, Snow DM, Letourneau PC. 1997. Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue. J Neurosci 17: 3085-3095.
6. Charrier E, Mosinger B, Meissirel C, Aguera M, Rogemond V, Reibel S, Salin P, et al. 2006. Transient alterations in granule cell proliferation, apoptosis and migration in postnatal developing cerebellum of CRMP1-/- mice. Genes Cells 11: 1337-1352.
7. Deo RC, Schmidt EF, Elhabazi A, Togashi H, Burley SK, Strittmatter SM. 2004. Structural bases for CRMP function in plexin-dependent semaphorin3A signaling. EMBO J 23: 9-22.
8. Fan J, Raper JA. 1995. Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron 14: 263-274.
9. Fukada M, Watakabe I, Yuasa-Kawada J, Kawachi H, Kuroiwa A, Matsuda Y, Noda M. 2000. Molecular characterization of CRMP5, a novel member of the collapsin response mediator protein family. J Biol Chem 275: 37957-37965.
10. Fukata M, Watanabe T, Noritake J, Nakagawa M, Yamaga M, Kuroda S, Matsuura Y, et al. 2002a. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109: 873-885.
11. Fukata Y, Itoh TJ, Kimura T, Menager C, Nishimura T, Shiromizu T, Watanabe H, et al. 2002b. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol 4: 583-591.
12. Goshima Y, Nakamura F, Strittmatter P, Strittmatter SM. 1995. Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 376: 509-514.
13. Hamajima N, Matsuda K, Sakata S, Tamaki N, Sasaki M, Nonaka M. 1996. A novel gene family defined by human dihydropyrimidinase and three related proteins with differential tissue distribution. Gene 180: 157-163.
14. Hensley K, Christov A, Kamat S, Zhang XC, Jackson KW, Snow S, Post J. 2010. Proteomic identification of binding partners for the brain metabolite lanthionine ketimine (LK) and documentation of LK effects on microglia and motoneuron cell cultures. J Neurosci 30: 2979-2988.
15. Hu L, Papoian GA. 2010. Mechano-chemical feedbacks regulate actin mesh growth in lamellipodial protrusions. Biophys J 98: 1375-1384.
16. Inagaki N, Chihara K, Arimura N, Menager C, Kawano Y, Matsuo N, Nishimura T, et al. 2001. CRMP-2 induces axons in cultured hippocampal neurons. Nat Neurosci 4: 781-782.
17. Jay DG. 1988. Selective destruction of protein function by chromophore-assisted laser inactivation. Proc Natl Acad Sci USA 85: 5454-5458.
18. Kawano Y, Yoshimura T, Tsuboi D, Kawabata S, Kaneko-Kawano T, Shirataki H, Takenawa T, et al. 2005. CRMP-2 is involved in kinesin-1-dependent transport of the Sra-1/WAVE1 complex and axon formation. Mol Cell Biol 25: 9920-9935.
19. Kimura T, Watanabe H, Iwamatsu A, Kaibuchi K. 2005. Tubulin and CRMP-2 complex is transported via Kinesin-1. J Neurochem 93: 1371-1382.
20. Koester MP, Muller O, Pollerberg GE. 2007. Adenomatous polyposis coli is differentially distributed in growth cones and modulates their steering. J Neurosci 27: 12590-12600.
21. Liao JC, Roider J, Jay DG. 1994. Chromophore-assisted laser inactivation of proteins is mediated by the photogeneration of free radicals. Proc Natl Acad Sci USA 91: 2659-2663.
22. Lowery LA, Van Vactor D. 2009. The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol 10: 332-343.
23. Mack TG, Koester MP, Pollerberg GE. 2000. The microtubule-associated protein MAP1B is involved in local stabilization of turning growth cones. Mol Cell Neurosci 15: 51-65.
24. Mimura F, Yamagishi S, Arimura N, Fujitani M, Kubo T, Kaibuchi K, Yamashita T. 2006. Myelin-associated glycoprotein inhibits microtubule assembly by a Rho-kinase-dependent mechanism. J Biol Chem 281: 15970-15979.
25. Nakamura M, Zhou XZ, Lu KP. 2001. Critical role for the EB1 and APC interaction in the regulation of microtubule polymerization. Curr Biol 11: 1062-1067.
26. Nishimura T, Fukata Y, Kato K, Yamaguchi T, Matsuura Y, Kamiguchi H, Kaibuchi K. 2003. CRMP-2 regulates polarized Numb-mediated endocytosis for axon growth. Nat Cell Biol 5: 819-826.
27. Quach TT, Duchemin AM, Rogemond V, Aguera M, Honnorat J, Belin MF, Kolattukudy PE. 2004. Involvement of collapsin response mediator proteins in the neurite extension induced by neurotrophins in dorsal root ganglion neurons. Mol Cell Neurosci 25: 433-443.
28. Rahajeng J, Giridharan SS, Naslavsky N, Caplan S. 2010. Collapsin response mediator protein-2 (Crmp2) regulates trafficking by linking endocytic regulatory proteins to dynein motors. J Biol Chem 285: 31918-31922.
29. Rosslenbroich V, Dai L, Baader SL, Noegel AA, Gieselmann V, Kappler J. 2005. Collapsin response mediator protein-4 regulates F-actin bundling. Exp Cell Res 310: 434-444.
30. Schmidt EF, Strittmatter SM. 2007. The CRMP family of proteins and their role in Sema3A signaling. Adv Exp Med Biol 600: 1-11.
31. Su KY, Chien WL, Fu WM, Yu IS, Huang HP, Huang PH, Lin SR, et al. 2007. Mice deficient in collapsin response mediator protein-1 exhibit impaired long-term potentiation and impaired spatial learning and memory. J Neurosci 27: 2513-2524.
32. Takei K, Chan TA, Wang FS, Deng H, Rutishauser U, Jay DG. 1999. The neural cell adhesion molecules L1 and NCAM-180 act in different steps of neurite outgrowth. J Neurosci 19: 9469-9479.
33. Takei K, Tokushige N, Cai W, Mikoshiba K. 2000. Indirect visualization of protein loading in living DRG neurons by concomitant trituration loading of fluorescence-labeled dextran. Bioimages 8: 5-9.
34. Tojima T, Hines JH, Henley JR, Kamiguchi H. 2011. Second messengers and membrane trafficking direct and organize growth cone steering. Nat Rev Neurosci 12: 191-203.
35. Uchida Y, Ohshima T, Sasaki Y, Suzuki H, Yanai S, Yamashita N, Nakamura F, et al. 2005. Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 10: 165-179.
36. Uchida Y, Ohshima T, Yamashita N, Ogawara M, Sasaki Y, Nakamura F, Goshima Y. 2009. Semaphorin3A signaling mediated by Fyn-dependent tyrosine phosphorylation of collapsin response mediator protein 2 at tyrosine 32. J Biol Chem 284: 27393-27401.
37. Wang FS, Wolenski JS, Cheney RE, Mooseker MS, Jay DG. 1996. Function of myosin-V in filopodial extension of neuronal growth cones. Science 273: 660-663.
38. Wang LH, Strittmatter SM. 1996. A family of rat CRMP genes is differentially expressed in the nervous system. J Neurosci 16: 6197-6207.
39. Yamashita N, Mosinger B, Roy A, Miyazaki M, Ugajin K, Nakamura F, Sasaki Y, et al. 2011. CRMP5 (collapsin response mediator protein 5) regulates dendritic development and synaptic plasticity in the cerebellar Purkinje cells. J Neurosci 31: 1773-1779.
40. Yamashita N, Uchida Y, Ohshima T, Hirai S, Nakamura F, Taniguchi M, Mikoshiba K, et al. 2006. Collapsin response mediator protein 1 mediates reelin signaling in cortical neuronal migration. J Neurosci 26: 13357-13362.
41. Yamashita N, Morita A, Uchida Y, Nakamura F, Usui H, Ohshima T, Taniguchi M, et al. 2007. Regulation of spine development by semaphorin3A through cyclin-dependent kinase 5 phosphorylation of collapsin response mediator protein 1. J Neurosci 27: 12546-12554.
42. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K. 2005. GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120: 137-149.
43. Yuan XB, Jin M, Xu X, Song YQ, Wu CP, Poo MM, Duan S. 2003. Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat Cell Biol 5: 38-45.
44. Yuasa-Kawada J, Suzuki R, Kano F, Ohkawara T, Murata M, Noda M. 2003. Axonal morphogenesis controlled by antagonistic roles of two CRMP subtypes in microtubule organization. Eur J Neurosci 17: 2329-2343.
45. Zheng JQ, Wan JJ, Poo MM. 1996. Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 16: 1140-1149.
46. Zhou FQ, Cohan CS. 2004. How actin filaments and microtubules steer growth cones to their targets. J Neurobiol 58: 84-91.