Collapsin response mediator protein-2 is a calmodulin-binding protein

Cellular and Molecular Life Sciences

Volumn 66, Issue 3, 2009, Pages 526-536

  Zhang, Z ^a   Majava, V ^b   Greffier, A ^b   Hayes, R L ^a,c   Kursula, P ^b   Wang, K K W ^a,c  

^a BANYAN BIOMARKERS INC   (United States)

^b UNIVERSITY OF OULU   (Finland)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Calmodulin; Calmodulin binding protein; CRMP 2; Oligomerization; Proteolysis

Indexed keywords

CALMODULIN BINDING PROTEIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2;

ARTICLE; BINDING SITE; BIOLOGICAL ACTIVITY; BIOTINYLATION; CELL LYSATE; CELL REGENERATION; CELL STRAIN HEK293; ELUTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; ISOTHERMAL TITRATION CALORIMETRY; NERVE CELL DIFFERENTIATION; OLIGOMERIZATION; PLASMID; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; SURFACE PLASMON RESONANCE; TANDEM MASS SPECTROMETRY;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CALMODULIN; CALMODULIN-BINDING PROTEINS; CALPAIN; CELL LINE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURONS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN ISOFORMS; RATS; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT;

EID: 59349108979     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-008-8362-1     Document Type: Article

References (43)

1. Bretin, S., Reibel, S., Charrier, E., Maus-Moatti, M., Auvergnon, N., Thevenoux, A., Glowinski, J., Rogemond, V., Premont, J., Honnorat, J. and 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
2. Wang, L. H. and Strittmatter, S. M. (1996) A family of rat CRMP genes is differentially expressed in the nervous system. J. Neurosci. 16, 6197-6207
3. Fukata, Y., Itoh, T. J., Kimura, T., Menager, C., Nishimura, T., Shiromizu, T., Watanabe, H., Inagaki, N., Iwamatsu, A., Hotani, H. and Kaibuchi, K. (2002) CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4, 583-591
4. Fukata, Y., Kimura, T. and Kaibuchi, K. (2002) Axon specification in hippocampal neurons. Neurosci. Res. 43, 305-15
5. Wang, L. H. and Strittmatter, S. M. (1997) Brain CRMP forms heterotetramers similar to liver dihydropyrimidinase. J. Neurochem. 69, 2261-2269
6. Jiang, S. X., Kappler, J., Zurakowski, B., Desbois, A., Aylsworth, A. and Hou, S. T. (2007) Calpain cleavage of collapsin response mediator proteins in ischemic mouse brain. Eur. J. Neurosci. 26, 801-809
7. Zhang, Z., Ottens, A. K., Sadasivan, S., Kobeissy, F. H., Fang, T., Hayes, R. L. and Wang, K. K. (2007) Calpain-mediated collapsin response mediator protein-1, -2, and -4 proteolysis after neurotoxic and traumatic brain injury. J. Neurotrauma 24, 460-472
8. Gu, Y., Hamajima, N. and Ihara, Y. (2000) Neurofibrillary tangle-associated collapsin response mediator protein-2 (CRMP-2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry (Mosc) 39, 4267-4275
9. Kobeissy, F. H., Ottens, A. K., Zhang, Z., Liu, M. C., Denslow, N. D., Dave, J. R., Tortella, F. C., Hayes, R. L. and Wang, K. K. (2006) Novel differential neuroproteomics analysis of traumatic brain injury in rats. Mol. Cell Proteomics 5, 1887-1898
10. Majava, V., Loytynoja, N., Chen, W. Q., Lubec, G. and Kursula, P. (2008) Crystal and solution structure, stability and post-translational modifications of collapsin response mediator protein 2. FEBS J. 275, 4583-4596
11. 2+/calmodulin signaling system in the neural response to excitability. Involvement of neuronal and glial cells. Prog. Neurobiol. 58, 207-232
12. Czogalla, A. and Sikorski, A. F. (2005) Spectrin and calpain: a 'target' and a 'sniper' in the pathology of neuronal cells. Cell Mol. Life Sci. 62, 1913-1924
13. Haeseleer, F., Imanishi, Y., Sokal, I., Filipek, S. and Palczewski, K. (2002) Calcium-binding proteins: intracellular sensors from the calmodulin superfamily. Biochem. Biophys. Res. Commun. 290, 615-623
14. O'Day, D. H. and Myre, M. A. (2004) Calmodulin-binding domains in Alzheimer's disease proteins: extending the calcium hypothesis. Biochem. Biophys. Res. Commun. 320, 1051-1054
15. Wang, K. K. W., Villalobo, A. and Roufogalis, B. D. (1989) Calmodulin-binding proteins as calpain substrates. Biochem. J. 262, 693-706
16. Xia, Z. and Storm, D. R. (2005) The role of calmodulin as a signal integrator for synaptic plasticity. Nat. Rev. Neurosci. 6, 267-276
17. Johnson, G. V., Greenwood, J. A., Costello, A. C. and Troncoso, J. C. (1991) The regulatory role of calmodulin in the proteolysis of individual neurofilament proteins by calpain. Neurochem. Res. 16, 869-873
18. Zhang, Z., Ottens, A. K., Golden, E. C., Hayes, R. L. and Wang, K. K. (2006) Using calmodulin-affinity capture to study the rat brain calmodulin binding proteome and its vulnerability to calpain and caspase proteolysis. Calcium Binding Proteins 1, 125-134
19. 2+-calmodulin affinity chromatography and tandem mass spectrometry. J. Proteome Res. 5, 669-687
20. Ikura, M. and Ames, J. B. (2006) Genetic polymorphism and protein conformational plasticity in the calmodulin superfamily: two ways to promote multifunctionality. Proc. Natl. Acad. Sci. USA 103, 1159-1164
21. Yap, K. L., Kim, J., Truong, K., Sherman, M., Yuan, T. and Ikura, M. (2000) Calmodulin target database. J. Struct. Funct. Genomics 1, 8-14
22. Majava, V., Petoukhov, M. V., Hayashi, N., Pirila, P., Svergun, D. I. and Kursula, P. (2008) Interaction between the C-terminal region of human myelin basic protein and calmodulin:Analysis of complex formation and solution structure. BMC Struct Biol. 8, 10
23. Stenmark, P., Ogg, D., Flodin, S., Flores, A., Kotenyova, T., Nyman, T., Nordlund, P. and Kursula, P. (2007) The structure of human collapsin response mediator protein 2, a regulator of axonal growth. J. Neurochem. 101, 906-917
24. Radivojac, P., Vucetic, S., O'Connor, T. R., Uversky, V. N., Obradovic, Z. and Dunker, A. K. (2006) Calmodulin signaling: analysis and prediction of a disorder-dependent molecular recognition. Proteins 63, 398-410
25. Libich, D. S., Hill, C. M., Haines, J. D. and Harauz, G. (2003) Myelin basic protein has multiple calmodulin-binding sites. Biochem. Biophys. Res. Commun. 308, 313-319
26. 2+ signal transduction by members of the calpacitin protein family. J. Neurosci. Res. 58, 107-119
27. Krucker, T., Siggins, G. R., McNamara, R. K., Lindsley, K. A., Dao, A., Allison, D. W., De Lecea, L., Lovenberg, T. W., Sutcliffe, J. G. and Gerendasy, D. D. (2002) Targeted disruption of RC3 reveals a calmodulin-based mechanism for regulating metaplasticity in the hippocampus. J. Neurosci. 22, 5525-5535
28. van Dalen, J. J.,Gerendasy, D. D., de Graan, P. N., Schrama, L. H. and Gruol, D. L. (2003) Calcium dynamics are altered in cortical neurons lacking the calmodulin-binding protein RC3. Eur. J. Neurosci. 18, 13-22
29. Rogemond, V., Auger, C., Giraudon, P., Becchi, M., Auvergnon, N., Belin, M. F., Honnorat, J. and Moradi-Ameli, M. (2008) Processing and nuclear localization of CRMP2 during brain development induce neurite outgrowth inhibition. J. Biol. Chem. 283, 14751-14761
30. Kawano,Y., Yoshimura, T., Tsuboi, D., Kawabata, S., Kaneko-Kawano, T., Shirataki, H., Takenawa, T. and Kaibuchi, K. (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
31. Gungabissoon, R. A. and Bamburg, J. R. (2003) Regulation of growth cone actin dynamics by ADF/cofilin. J. Histochem. Cytochem. 51, 411-420
32. Rosslenbroich, V., Dai, L., Baader, S. L., Noegel, A. A., Gieselmann, V. and Kappler, J. (2005) Collapsin response mediator protein-4 regulates F-actin bundling. Exp. Cell Res. 310, 434-444
33. Arimura, N., Menager, C., Fukata, Y. and Kaibuchi, K. (2004) Role of CRMP-2 in neuronal polarity. J. Neurobiol. 58, 34-47
34. Yoshimura, T., Kawano, Y., Arimura, N., Kawabata, S., Kikuchi, A. and Kaibuchi, K. (2005) GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120, 137-149
35. Chung, M. A., Lee, J. E., Lee, J. Y., Ko, M. J., Lee, S. T. and Kim, H. J. (2005) Alteration of collapsin response mediator protein-2 expression in focal ischemic rat brain. Neuroreport. 16, 1647-1653
36. Harris, A. S., Croall, D. E. and Morrow, J. S. (1989) Calmodulin regulates fodrin susceptibility to cleavage by calcium-dependent protease I. J. Biol. Chem. 264, 17401-17408
37. 2+-activated neutral protease in human platelets. Biochem. Int. 6, 767-775
38. Tsunekawa, S., Takahashi, K., Abe, M., Hiwada, K., Ozawa, K. and Murachi, T. (1989) Calpain proteolysis of free and bound forms of calponin, a troponin T-like protein in smooth muscle. FEBS Lett. 250, 493-496
39. Croall, D. E., Chacko, S. and Wang, Z. (1996) Cleavage of caldesmon and calponin by calpain: Substrate recognition is not dependent on calmodulin binding domains. Biochim. Biophys. Acta 1298, 276-284
40. Zhang, S., Ehlers, M. D., Bernhardt, J. P., Su, C. T. and Huganir, R. L. (1998) Calmodulin mediates calcium-dependent inactivation of N-methyl-D-aspartate receptors. Neuron 21, 443-453
41. Dent, E. W. and Gertler, F. B. (2003) Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40, 209-227
42. Tahimic, C. G., Tomimatsu, N., Nishigaki, R., Fukuhara, A., Toda, T., Kaibuchi, K., Shiota, G., Oshimura, M. and Kurimasa, A. (2006) Evidence for a role of collapsin response mediator protein-2 in signaling pathways that regulate the proliferation of non-neuronal cells. Biochem. Biophys. Res. Commun. 340, 1244-1250
43. Touma, E., Kato, S., Fukui, K. and Koike, T. (2007) Calpain-mediated cleavage of collapsin response mediator protein (CRMP)-2 during neurite degeneration in mice. Eur. J. Neurosci. 26, 3368-3381