Cdk5-mediated phosphorylation of CRMP-2 enhances its interaction with CaV2.2

FEBS Letters

Volumn 586, Issue 21, 2012, Pages 3813-3818

  Brittain, Joel M ^a   Wang, Yuying ^a   Eruvwetere, Omotore ^a   Khanna, Rajesh ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CaV2.2; Cdk5; CRMP 2; Interaction; Phosphorylation; RhoK

Indexed keywords

CALCIUM CHANNEL CAV2.2; CALCIUM CHANNEL N TYPE; CALCIUM ION; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; CYCLIN DEPENDENT KINASE 5; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CALCIUM CURRENT; CALCIUM TRANSPORT; CONTROLLED STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; CALCIUM CHANNELS, N-TYPE; CEREBRAL CORTEX; CYCLIN-DEPENDENT KINASE 5; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HIPPOCAMPUS; IMMUNOPRECIPITATION; MUTATION; NERVE TISSUE PROTEINS; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PRIMARY CELL CULTURE; RATS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84868092963     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.09.022     Document Type: Article

References (37)

1. Y. Goshima, F. Nakamura, P. Strittmatter, and S.M. Strittmatter Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33 Nature 376 1995 509 514
2. E.M. Hedgecock, J.G. Culotti, J.N. Thomson, and L.A. Perkins Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes Dev. Biol. 111 1985 158 170
3. D.H. Geschwind, and S. Hockfield Identification of proteins that are developmentally regulated during early cerebral corticogenesis in the rat J. Neurosci. 9 1989 4303 4317
4. J.E. Minturn, H.J. Fryer, D.H. Geschwind, and S. Hockfield 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 1995 6757 6766
5. T. Byk, T. Dobransky, C. Cifuentes-Diaz, and A. Sobel 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 1996 688 701
6. N. Hamajima, K. Matsuda, S. Sakata, N. Tamaki, M. Sasaki, and M. Nonaka A novel gene family defined by human dihydropyrimidinase and three related proteins with differential tissue distribution Genes Cells 180 1996 157 163
7. K. Kitamura, M. Takayama, N. Hamajima, M. Nakanishi, M. Sasaki, Y. Endo, T. Takemoto, H. Kimura, M. Iwaki, and M. Nonaka Characterization of the human dihydropyrimidinase-related protein 2 (DRP-2) gene DNA Res. 6 1999 291 297
8. Morris, D.H., Dubnau, J., Park, J.H. and Rawls, J.M. Jr. (2012). Divergent functions through alternative splicing: roles of the Drosophila CRMP gene in pyrimidine metabolism, brain and behavior. Genetics 191, 1227-1238.
9. Hensley, K., Venkova, K., Christov, A., Gunning, W. and Park, J. (2011). Collapsin response mediator protein-2: an emerging pathologic feature and therapeutic target for neurodisease indications. Mol. Neurobiol. 43, 180-191.
10. E.F. Schmidt, and S.M. Strittmatter The CRMP family of proteins and their role in Sema3A signaling Adv. Exp. Med. Biol. 600 1-11 2007 1 11
11. J.M. Brittain, A.D. Piekarz, Y. Wang, T. Kondo, T.R. Cummins, and R. Khanna An atypical role for collapsin response mediator protein 2 (CRMP-2) in neurotransmitter release via interaction with presynaptic voltage-gated Ca2+ channels J. Biol. Chem. 284 2009 31375 31390
12. X.X. Chi, B.S. Schmutzler, J.M. Brittain, C.M. Hingtgen, G.D. Nicol, and R. Khanna Regulation of N-type voltage-gated calcium (CaV2.2) channels and transmitter release by collapsin response mediator protein-2 (CRMP-2) in sensory neurons J. Cell Sci. 23 2009 4351 4362
13. Y. Wang, J.M. Brittain, S.M. Wilson, and R. Khanna Emerging roles of collapsin response mediator proteins (CRMPs) as regulators of voltage-gated calcium channels and synaptic transmission Commun. Integr. Biol. 3 2010 1 4
14. L.D. Hirning, A.P. Fox, E.W. McCleskey, B.M. Olivera, S.A. Thayer, R.J. Miller, and R.W. Tsien Dominant role of N-type Ca2+ channels in evoked release of norepinephrine from sympathetic neurons Transl. Neurosci. 239 1988 57 61
15. E.F. Stanley Single calcium channels and acetylcholine release at a presynaptic nerve terminal Neuron 11 1993 1007 1011
16. E.F. Stanley Presynaptic calcium channels and the transmitter release mechanism Ann. N. Y. Acad. Sci. 681 368-72 1993 368 372
17. J.M. Brittain, D.B. Duarte, S.M. Wilson, W. Zhu, C. Ballard, P.L. Johnson, N. Liu, W. Xiong, M.S. Ripsch, Y. Wang, J.C. Fehrenbacher, S.D. Fitz, M. Khanna, C.K. Park, B.S. Schmutzler, B.M. Cheon, M.R. Due, T. Brustovetsky, N.M. Ashpole, A. Hudmon, S.O. Meroueh, C.M. Hingtgen, N. Brustovetsky, R.R. Ji, J.H. Hurley, X. Jin, A. Shekhar, X.M. Xu, G.S. Oxford, M.R. Vasko, F.A. White, and R. Khanna Suppression of inflammatory and neuropathic pain by uncoupling CRMP-2 from the presynaptic Ca(2+) channel complex Nat. Med. 17 2011 822 829
18. Wilson, S.M., Brittain, J.M., Piekarz, A.D., Ballard, C.J., Ripsch, M.S., Cummins, T.R., Hurley, J.H., Khanna, M., Hammes, N.M., Samuels, B.C., White, F.A. and Khanna, R. (2011). Further insights into the antinociceptive potential of a peptide disrupting the N-type calcium channel-CRMP-2 signaling complex. Channels (Austin.) 5, 449-456.
19. 2+ channel complex demonstrates efficacy in animal models of migraine and AIDS therapy-induced neuropathy Transl. Neurosci. 3 2012 8
20. H. Saegusa, T. Kurihara, S. Zong, A. Kazuno, Y. Matsuda, T. Nonaka, W. Han, H. Toriyama, and T. Tanabe Suppression of inflammatory and neuropathic pain symptoms in mice lacking the N-type Ca2+ channel EMBO J. 20 2001 2349 2356
21. S. Hatakeyama, M. Wakamori, M. Ino, N. Miyamoto, E. Takahashi, T. Yoshinaga, K. Sawada, K. Imoto, I. Tanaka, T. Yoshizawa, Y. Nishizawa, Y. Mori, T. Niidome, and S. Shoji Differential nociceptive responses in mice lacking the alpha(1B) subunit of N-type Ca(2+) channels Neuroreport 12 2001 2423 2427
22. T. Yoshimura, Y. Kawano, N. Arimura, S. Kawabata, A. Kikuchi, and K. Kaibuchi GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity Genes Cells 120 2005 137 149
23. N. Arimura, N. Inagaki, K. Chihara, C. Menager, N. Nakamura, M. Amano, A. Iwamatsu, Y. Goshima, and K. Kaibuchi Phosphorylation of collapsin response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse J. Biol. Chem. 275 2000 23973 23980
24. N. Arimura, C. Menager, Y. Kawano, T. Yoshimura, S. Kawabata, A. Hattori, Y. Fukata, M. Amano, Y. Goshima, M. Inagaki, N. Morone, J. Usukura, and K. Kaibuchi Phosphorylation by Rho kinase regulates CRMP-2 activity in growth cones Mol. Cell Biol. 25 2005 9973 9984
25. S.T. Hou, S.X. Jiang, A. Aylsworth, G. Ferguson, J. Slinn, H. Hu, T. Leung, J. Kappler, and K. Kaibuchi CaMKII phosphorylates collapsin response mediator protein 2 and modulates axonal damage during glutamate excitotoxicity J. Neurochem. 111 2009 870 878
26. Y. Uchida, T. Ohshima, N. Yamashita, M. Ogawara, Y. Sasaki, F. Nakamura, and Y. Goshima Semaphorin3A signaling mediated by Fyn-dependent tyrosine phosphorylation of collapsin response mediator protein 2 at tyrosine 32 J. Biol. Chem. 284 2009 27393 27401
27. M. Varrin-Doyer, P. Vincent, S. Cavagna, N. Auvergnon, N. Noraz, V. Rogemond, J. Honnorat, M. Moradi-Ameli, and P. Giraudon Phosphorylation of collapsin response mediator protein 2 on Tyr-479 regulates CXCL12-induced T lymphocyte migration J. Biol. Chem. 284 2009 13265 13276
28. Y. Uchida, T. Ohshima, Y. Sasaki, H. Suzuki, S. Yanai, N. Yamashita, F. Nakamura, K. Takei, Y. Ihara, K. Mikoshiba, P. Kolattukudy, J. Honnorat, and Y. Goshima 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 2005 165 179
29. A.R. Cole, F. Causeret, G. Yadirgi, C.J. Hastie, H. McLauchlan, E.J. McManus, F. Hernandez, B.J. Eickholt, M. Nikolic, and C. Sutherland Distinct priming kinases contribute to differential regulation of collapsin response mediator proteins by glycogen synthase kinase-3 in vivo J. Biol. Chem. 281 2006 16591 16598
30. Y. Wang, J.M. Brittain, B.W. Jarecki, K.D. Park, S.M. Wilson, B. Wang, R. Hale, S.O. Meroueh, T.R. Cummins, and R. Khanna In silico docking and electrophysiological characterization of lacosamide binding sites on collapsin response mediator protein 2 (CRMP-2) identifies a pocket important in modulating sodium channel slow inactivation J. Biol. Chem. 285 2010 25296 25307
31. Brittain, J., Wilson, S.M., Wang, Y. and Khanna, R. (2012). Regulation of CREB signaling through L-Type Ca2+ channels by Nipsnap-2. Channels 6, 94-102.
32. S. Patrakitkomjorn, D. Kobayashi, T. Morikawa, M.M. Wilson, N. Tsubota, A. Irie, T. Ozawa, M. Aoki, N. Arimura, K. Kaibuchi, H. Saya, and N. Araki Neurofibromatosis type 1 (NF1) tumor suppressor, neurofibromin, regulates the neuronal differentiation of PC12 cells via its associating protein, CRMP-2 J. Biol. Chem. 283 2008 9399 9413
33. M. Uehata, T. Ishizaki, H. Satoh, T. Ono, T. Kawahara, T. Morishita, H. Tamakawa, K. Yamagami, J. Inui, M. Maekawa, and S. Narumiya Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension Nature 389 1997 990 994
34. J. Lew, Q.Q. Huang, Z. Qi, R.J. Winkfein, R. Aebersold, T. Hunt, and J.H. Wang A brain-specific activator of cyclin-dependent kinase 5 Nature 371 1994 423 426
35. B.A. Samuels, Y.P. Hsueh, T. Shu, H. Liang, H.C. Tseng, C.J. Hong, S.C. Su, J. Volker, R.L. Neve, D.T. Yue, and L.H. Tsai Cdk5 promotes synaptogenesis by regulating the subcellular distribution of the MAGUK family member CASK Neuron 56 2007 823 837
36. M. Brown, T. Jacobs, B. Eickholt, G. Ferrari, M. Teo, C. Monfries, R.Z. Qi, T. Leung, L. Lim, and C. Hall 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. 24 2004 8994 9004
37. S.C. Su, J. Seo, J.Q. Pan, B.A. Samuels, A. Rudenko, M. Ericsson, R.L. Neve, D.T. Yue, and L.H. Tsai Regulation of N-type voltage-gated calcium channels and presynaptic function by cyclin-dependent kinase 5 Neuron 75 2012 675 687