CRMP5 (Collapsin Response Mediator Protein 5) regulates dendritic development and synaptic plasticity in the cerebellar purkinje cells

Journal of Neuroscience

Volumn 31, Issue 5, 2011, Pages 1773-1779

  Yamashita, Naoya ^a   Mosinger, Bedrich ^b   Roy, Arpita ^b   Miyazaki, Mari ^a   Ugajin, Kozue ^a   Nakamura, Fumio ^a   Sasaki, Yukio ^a   Yamaguchi, Kazuhiko ^c   Kolattukudy, Pappachan ^b   Goshima, Yoshio ^a  

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

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

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALBINDIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN 5; PHOSPHOPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MATURATION; CELL STRAIN HEK293; CELL STRUCTURE; CEREBELLUM; CONTROLLED STUDY; DENDRITE; DENDRITIC CELL; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VIVO STUDY; LONG TERM DEPRESSION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PURKINJE CELL; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

AMIDOHYDROLASES; ANIMALS; ANIMALS, NEWBORN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CEREBELLUM; DENDRITES; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; LONG-TERM SYNAPTIC DEPRESSION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONAL PLASTICITY; POLYMERASE CHAIN REACTION; PURKINJE CELLS; RECEPTOR, TRKB; SYNAPTIC TRANSMISSION;

EID: 79551508311     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5337-10.2011     Document Type: Article

References (43)

1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377-388.
2. Bretin S, Reibel S, Charrier E, Maus-Moatti M, Auvergnon N, Thevenoux A, Glowinski J, Rogemond V, Prémont J, Honnorat J, Gauchy C (2005) Differential expression of CRMP1, CRMP2A, CRMP2B, and CRMP5 in axons or dendrites of distinct neurons in the mouse brain. J Comp Neurol 486:1-17.
3. Brot S, Rogemond V, Perrot V, Chounlamountri N, Auger C, Honnorat J, Moradi-Améli M (2010) CRMP5 interacts with tubulin to inhibit neurite outgrowth, thereby modulating the function of CRMP2. J Neurosci 30:10639-10654.
4. Byk T, Dobransky T, Cifuentes-Diaz C, 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 16:688-701. (Pubitemid 26028828)
5. Carter AR, Chen C, Schwartz PM, Segal RA (2002) Brain-derived neurotrophic factor modulates cerebellar plasticity and synaptic ultrastructure. J Neurosci 22:1316-1327.
6. Charrier E, Mosinger B, Meissirel C, Aguera M, Rogemond V, Reibel S, Salin P, Chounlamountri N, Perrot V, Belin MF, Goshima Y, Honnorat J, Thomasset N, Kolattukudy P (2006) Transient alterations in granule cell proliferation, apoptosis and migration in postnatal developing cerebellum of CRMP1-/- mice. Genes Cells 11:1337-1352.
7. Chen YT, Collins LL, Uno H, Chang C (2005) Deficits in motor coordination with aberrant cerebellar development in mice lacking testicular orphan nuclear receptor 4. Mol Cell Biol 25:2722-2732.
8. Cheung ZH, Chin WH, Chen Y, Ng YP, Ip NY (2007) Cdk5 is involved in BDNF-stimulated dendritic growth in hippocampal neurons. PLoS Biol 5:e63.
9. Cross SA, Salomao DR, Parisi JE, Kryzer TJ, Bradley EA, Mines JA, Lam BL, Lennon VA (2003) Paraneoplastic autoimmune optic neuritis with retinitis defined by CRMP-5-IgG. Ann Neurol 54:38-50.
10. 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. (Pubitemid 32004917)
11. Fukata Y, Itoh TJ, Kimura T, Ménager C, Nishimura T, Shiromizu T, Watanabe H, Inagaki N, Iwamatsu A, Hotani H, Kaibuchi K (2002) CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol 4:583-591.
12. Gao WQ, Zheng JL, Karihaloo M (1995) Neurotrophin-4/5 (NT-4/5) and brain-derived neurotrophic factor (BDNF) act at later stages of cerebellar granule cell differentiation. J Neurosci 15:2656-2667.
13. 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.
14. 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. (Pubitemid 26417923)
15. Hirai H, Launey T (2000) The regulatory connection between the activity of granule cell NMDA receptors and dendritic differentiation of cerebellar Purkinje cells. J Neurosci 20:5217-5224. (Pubitemid 30457718)
16. Honnorat J, Antoine JC (2007) Paraneoplastic neurological syndromes. Orphanet J Rare Dis 2:22.
17. Horch HW, Katz LC (2002) BDNF release from single cells elicits local dendritic growth in nearby neurons. Nat Neurosci 5:1177-1184.
18. Hotta A, Inatome R, Yuasa-Kawada J, Qin Q, Yamamura H, Yanagi S (2005) Critical role of collapsin response mediator protein-associated molecule CRAM for filopodia and growth cone development in neurons. Mol Biol Cell 16:32-39. (Pubitemid 40024288)
19. Inatome R, Tsujimura T, Hitomi T, Mitsui N, Hermann P, Kuroda S, Yamamura H, Yanagi S (2000) Identification of CRAM, a novel unc-33 gene family protein that associates with CRMP3 and protein-tyrosine kinase(s) in the developing rat brain. J Biol Chem 275:27291-27302.
20. Ito M (1986) Long-term depression as a memory process in the cerebellum. Neurosci Res 3:531-539.
21. Koekkoek SK, Yamaguchi K, Milojkovic BA, Dortland BR, Ruigrok TJ, Maex R, De Graaf W, Smit AE, VanderWerf F, Bakker CE, Willemsen R, Ikeda T, Kakizawa S, Onodera K, Nelson DL, Mientjes E, Joosten M, De Schutter E, Oostra BA, Ito M, De Zeeuw CI (2005) Deletion of FMR1 in Purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in Fragile X syndrome. Neuron 47:339-352.
22. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:880-884.
23. Liou YC, Sun A, Ryo A, Zhou XZ, Yu ZX, Huang HK, Uchida T, Bronson R, Bing G, Li X, Hunter T, Lu KP (2003) Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature 424:556-561.
24. Luo L (2000) Rho GTPases in neuronal morphogenesis. Nat Rev Neurosci 1:173-180.
25. McKay BE, Turner RW (2005) Physiological and morphological development of the rat cerebellar Purkinje cell. J Physiol 567:829-850.
26. Minturn JE, Fryer HJ, Geschwind DH, 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 15:6757-6766.
27. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci U S A 90:8424-8428.
28. Pittock SJ, Kryzer TJ, Lennon VA (2004) Paraneoplastic antibodies coexist and predict cancer, not neurological syndrome. Ann Neurol 56:715-719.
29. 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.
30. Quach TT, Massicotte G, Belin MF, Honnorat J, Glasper ER, Devries AC, Jakeman LB, Baudry M, Duchemin AM, Kolattukudy PE (2008) CRMP3 is required for hippocampal CA1 dendritic organization and plasticity. FASEB J 22:401-409.
31. Raymond LA, Blackstone CD, Huganir RL (1993) Phosphorylation of amino acid neurotransmitter receptors in synaptic plasticity. Trends Neurosci 16:147-153.
32. Ricard D, Rogemond V, Charrier E, Aguera M, Bagnard D, Belin MF, Thomasset N, Honnorat J (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 21:7203-7214.
33. -/-mice reveals a role for neurotrophins in CNS patterning. Neuron 19:269-281.
34. Shimada A, Mason CA, Morrison ME (1998) TrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells. J Neurosci 18:8559-8570. (Pubitemid 28491723)
35. Su KY, Chien WL, Fu WM, Yu IS, Huang HP, Huang PH, Lin SR, Shih JY, Lin YL, Hsueh YP, Yang PC, Lin SW (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.
36. Uchida Y, Ohshima T, Sasaki Y, Suzuki H, Yanai S, Yamashita N, Nakamura F, Takei K, Ihara Y, Mikoshiba K, Kolattukudy P, Honnorat J, Goshima Y (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.
37. Wang LH, Strittmatter SM (1996) A family of rat CRMP genes is differentially expressed in the nervous system. J Neurosci 16:6197-6207. (Pubitemid 26313994)
38. Wang LH, Strittmatter SM (1997) Brain CRMP forms heterotetramers similar to liver dihydropyrimidinase. J Neurochem 69:2261-2269.
39. Yamashita N, Uchida Y, Ohshima T, Hirai S, Nakamura F, Taniguchi M, Mikoshiba K, Honnorat J, Kolattukudy P, Thomasset N, Takei K, Takahashi T, Goshima Y (2006) Collapsin response mediator protein 1 mediates reelin signaling in cortical neuronal migration. J Neurosci 26:13357-13362.
40. Yamashita N, Morita A, Uchida Y, Nakamura F, Usui H, Ohshima T, Taniguchi M, Honnorat J, Thomasset N, Takei K, Takahashi T, Kolattukudy P, Goshima Y (2007) Regulation of spine development by semaphorin3A through cyclin-dependent kinase 5 phosphorylation of collapsin response mediator protein 1. J Neurosci 27:12546-12554.
41. 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. (Pubitemid 40094609)
42. Yu Z, Kryzer TJ, Griesmann GE, Kim K, Benarroch EE, Lennon VA (2001) CRMP-5 neuronal autoantibody: marker of lung cancer and thymoma-related autoimmunity. Ann Neurol 49:146-154. (Pubitemid 32157990)
43. 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. (Pubitemid 36793742)