Insights into the oligomerization of CRMPs: Crystal structure of human collapsin response mediator protein 5

Journal of Neurochemistry

Volumn 125, Issue 6, 2013, Pages 855-868

  Ponnusamy, Rajesh ^a,b   Lohkamp, Bernhard ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

analytical gel filtration; collapsin response mediator protein 5; crystal structure; differential scanning fluorimetry; growth cone guidance; oligomerization

Indexed keywords

AMIDASE; CALCIUM ION; COLLAPSIN RESPONSE MEDIATOR PROTEIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN 1; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; COLLAPSIN RESPONSE MEDIATOR PROTEIN 5; DIHYDROPYRIMIDINASE; HETERO OLIGOMER; HETEROTETRAMER; HOMOTETRAMER; MAGNESIUM ION; OLIGOMER; TETRAMER; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CHEMICAL BOND; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HUMAN; HYDROGEN BOND; MOLECULAR INTERACTION; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SALT BRIDGE; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

CALCIUM; CATALYTIC DOMAIN; CATIONS, DIVALENT; CRYSTALLOGRAPHY, X-RAY; ENZYME ASSAYS; HUMANS; MAGNESIUM; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS;

EID: 84878758337     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12188     Document Type: Article

References (55)

1. Battye T. G. G., Kontogiannis L., Johnson O., Powell H. R., and, Leslie A. G. W., (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67, 271-281.
2. Berg K., Puntervoll P., Valdersnes S., and, Goksøyr A., (2011) Responses in the brain proteome of Atlantic cod (Gadus morhua) exposed to methylmercury. Aquat. Toxicol. 100, 51-65.
3. Brenner S., (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
4. Brittain J. M., Piekarz A. D., Wang Y., Kondo T., Cummins T. R., and, Khanna R., (2009) An Atypical Role for Collapsin Response Mediator Protein 2 (CRMP-2) in Neurotransmitter Release via Interaction with Presynaptic Voltage-gated Calcium Channels. J. Biol. Chem. 284, 31375-31390.
5. Brot S., Rogemond V., Perrot V., Chounlamountri N., Auger C., Honnorat J., and, Moradi-Améli M., (2010) CRMP5 Interacts with Tubulin to Inhibit Neurite Outgrowth, Thereby Modulating the Function of CRMP2. J. Neurosci. 30, 10639-10654.
6. Camdessanché J.-P., Ferraud K., Boutahar N., Lassablière F., Mutter M., Touret M., Kolattukudy P., Honnorat J., and, Antoine J.-C., (2012) The Collapsin Response Mediator Protein 5 Onconeural Protein Is Expressed in Schwann Cells Under Axonal Signals and Regulates Axon-Schwann Cell Interactions. J. Neuropathol. Exp. Neurol. 71, 298-311.
7. Charbaut E., Curmi P. A., Ozon S., Lachkar S., Redeker V., and, Sobel A., (2001) Stathmin Family Proteins Display Specific Molecular and Tubulin Binding Properties. J. Biol. Chem. 276, 16146-16154.
8. Charrier E., Reibel S., Rogemond V., Aguera M., Thomasset N., and, Honnorat J., (2003) Collapsin response mediator proteins (CRMPs): involvement in nervous system development and adult neurodegenerative disorders. Mol. Neurobiol. 28, 51-64.
9. Cowtan K., (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62, 1002-1011.
10. Davis I. W., Leaver-Fay A., Chen V. B., et al,. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383.
11. Deo R. C., Schmidt E. F., Elhabazi A., Togashi H., Burley S. K., and, Strittmatter S. M., (2004) Structural bases for CRMP function in plexin-dependent semaphorin3A signaling. EMBO J. 23, 9-22.
12. Emsley P., Lohkamp B., Scott W. G., and, Cowtan K., (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501.
13. Ericsson U. B., Hallberg B. M., DeTitta G. T., Dekker N., and, Nordlund P., (2006) Thermofluor-based high-throughput stability optimization of proteins for structural studies. Anal. Biochem. 357, 289-298.
14. Evans P. R., (2006) Scaling and data assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62, 72-82.
15. Fukada M., Watakabe I., Yuasa-Kawada J., Kawachi H., Kuroiwa A., Matsuda Y., and, Noda M., (2000) Molecular Characterization of CRMP5, a Novel Member of the Collapsin Response Mediator Protein Family. J. Biol. Chem. 275, 37957-37965.
16. Fukata Y., Itoh T. J., Kimura T., et al,. (2002) CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4, 583-591.
17. Gojkovic Z., Jahnke K., Schnackerz K. D., and, Piškur J., (2000) PYD2 encodes 5,6-dihydropyrimidine amidohydrolase, which participates in a novel fungal catabolic pathway. J. Mol. Biol. 295, 1073-1087.
18. 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, 509-514.
19. Gräslund S., Sagemark J., Berglund H., et al,. (2008) The use of systematic N- and C-terminal deletions to promote production and structural studies of recombinant proteins. Protein Expr. Purif. 58, 210-221.
20. Henderson M. J., Ward K., Simmonds H. A., Duley J. A., and, Davies P. M., (1993) Dihydropyrimidinase deficiency presenting in infancy with severe developmental delay. J. Inherit. Metab. Dis. 16, 574-576.
21. 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, 283-286.
22. Hotta A., Inatome R., Yuasa-Kawada J., Qin Q., Yamamura H., and, 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.
23. Huang C.-Y., Hsu C.-C., Chen M.-C., and, Yang Y.-S., (2009) Effect of metal binding and posttranslational lysine carboxylation on the activity of recombinant hydantoinase. J. Biol. Inorg. Chem. 14, 111-121.
24. Inatome R., Tsujimura T., Hitomi T., Mitsui N., Hermann P., Kuroda S. I., Yamamura H., and, 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.
25. 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.
26. 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.
27. Krieger E., Joo K., Lee J., Lee J., Raman S., Thompson J., Tyka M., Baker D., and, Karplus K., (2009) Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins 77, 114-122.
28. Krissinel E., and, Henrick K., (2007) Inference of Macromolecular Assemblies from Crystalline State. J. Mol. Biol. 372, 774-797.
29. Laurie A. T. R., and, Jackson R. M., (2005) Q-SiteFinder: an energy-based method for the prediction of protein-ligand binding sites. Bioinformatics 21, 1908-1916.
30. Lohkamp B., Andersen B., Piskur J., and, Dobritzsch D., (2006) The crystal structures of dihydropyrimidinases reaffirm the close relationship between cyclic amidohydrolases and explain their substrate specificity. J. Biol. Chem. 281, 13762-13776.
31. Lovell S. C., Davis I. W., Arendall W. B., de Bakker P. I. W., Word J. M., Prisant M. G., Richardson J. S., and, Richardson D. C., (2003) Structure validation by Cα geometry: φ, ψ and Cβ deviation. Proteins 50, 437-450.
32. Majava V., Löytynoja 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.
33. Martínez-Rodríguez S., Martínez-Gómez A. I., Clemente-Jimínez J. M., Rodríguez-Vico F., García- Ruíz J. M., Las Heras-Vázquez F. J., and, Gavira J. A., (2010) Structure of dihydropyrimidinase from Sinorhizobium meliloti CECT4114: New features in an amidohydrolase family member. J. Struct. Biol. 169, 200-208.
34. McCoy A. J., Grosse-Kunstleve R. W., Adams P. D., Winn M. D., Storoni L. C., and, Read R. J., (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674.
35. Meyronet D., Massoma P., Thivolet F., Chalabreysse L., Rogemond V., Schlama A., Honnorat J., and, Thomasset N., (2008) Extensive Expression of Collapsin Response Mediator Protein 5 (CRMP5) is a Specific Marker of High-grade Lung Neuroendocrine Carcinoma. Am. J. Surg. Pathol. 32, 1699-1708.
36. Murshudov G. N., Skubak P., Lebedev A. A., Pannu N. S., Steiner R. A., Nicholls R. A., Winn M. D., Long F., and, Vagin A. A., (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367.
37. Noble M., Lewis S. A., and, Cowan N. J., (1989) The microtubule binding domain of microtubule-associated protein MAP1B contains a repeated sequence motif unrelated to that of MAP2 and tau. J. Cell Biol. 109, 3367-3376.
38. Prilusky J., Felder C. E., Zeev-Ben-Mordehai T., Rydberg E. H., Man O., Beckmann J. S., Silman I., and, Sussman J. L., (2005) FoldIndex©: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21, 3435-3438.
39. Punta M., Coggill P. C., Eberhardt R. Y., et al,. (2012) The Pfam protein families database. Nucleic Acids Res. 40, D290-D301.
40. Ricard D., Rogemond V., Charrier E., Aguera M., Bagnard D., Belin M.-F., Thomasset N., and, 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.
41. Rogemond V. r., and, Honnorat J. r. m., (2000) Anti-CV2 autoantibodies and paraneoplastic neurological syndromes. Clin. Rev. Allergy Immunol. 19, 51-59.
42. 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.
43. Studier F. W., (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207-234.
44. Su K.-Y., Chien W.-L., Fu W.-M., 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.
45. Taghian K., Lee J. Y., and, Petratos S., (2012) Phosphorylation and Cleavage of the Family of Collapsin Response Mediator Proteins May Play a Central Role in Neurodegeneration after CNS Trauma. J. Neurotrauma 29, 1728-1735.
46. Tsuboi D., Hikita T., Qadota H., Amano M., and, Kaibuchi K., (2005) Regulatory machinery of UNC-33 Ce-CRMP localization in neurites during neuronal development in Caenorhabditis elegans. J. Neurochem. 95, 1629-1641.
47. Veyrac A., Giannetti N., Charrier E., Reymond-Marron I., Aguera M., Rogemond V., Honnorat J., and, Jourdan F., (2005) Expression of collapsin response mediator proteins 1, 2 and 5 is differentially regulated in newly generated and mature neurons of the adult olfactory system. Eur. J. Neurosci. 21, 2635-2648.
48. Veyrac A., Reibel S., Sacquet J., Mutin M., Camdessanche J.-P., Kolattukudy P., Honnorat J., and, Jourdan F., (2011) CRMP5 Regulates Generation and Survival of Newborn Neurons in Olfactory and Hippocampal Neurogenic Areas of the Adult Mouse Brain. PLoS ONE 6, e23721.
49. Wang L.-H., and, Strittmatter S. M., (1997) Brain CRMP Forms Heterotetramers Similar to Liver Dihydropyrimidinase. J. Neurochem. 69, 2261-2269.
50. Werry C., Götz F., Wurster U., Stangel M., Giess R., Heidenreich F., and, Windhagen A., (2009) Paraneoplastic autoimmune encephalitis associated with CV2/CRMP-5 IgG antineuronal antibodies in a patient with thymoma. J. Neurol. 256, 129-131.
51. Wilkins M. R., Gasteiger E., Bairoch A., Sanchez J. C., Williams K. L., Appel R. D., and, Hochstrasser D. F., (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol. Biol. 112, 531-552.
52. Yamashita N., Mosinger B., Roy A., Miyazaki M., Ugajin K., Nakamura F., Sasaki Y., Yamaguchi K., Kolattukudy P., and, Goshima Y., (2011) CRMP5 (Collapsin Response Mediator Protein 5) Regulates Dendritic Development and Synaptic Plasticity in the Cerebellar Purkinje Cells. J. Neurosci. 31, 1773-1779.
53. 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, 146-154.
54. 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.
55. Zhang Z., Majava V., Greffier A., Hayes R., Kursula P., and, Wang K., (2009) Collapsin response mediator protein-2 is a calmodulin-binding protein. Cell. Mol. Life Sci. 66, 526-536.