Structural basis for the association of MAP6 protein with microtubules and its regulation by calmodulin

Journal of Biological Chemistry

Volumn 288, Issue 34, 2013, Pages 24910-24922

  Lefèvre, Julien ^a,b   Savarin, Philippe ^a,b,e   Gans, Pierre ^c   Hamon, Loïc ^a,b   Clément, Marie Jeanne ^a,b   David, Marie Odile ^a,b   Bosc, Christophe ^d   Andrieux, Annie ^d   Curmi, Patrick A ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^d UNIV GRENOBLE ALPES   (France)

^e UNIVERSITÉ PARIS 13   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; BIOCHEMICAL ASSAY; COLD CONDITIONS; MICROTUBULE STABILITY; MICROTUBULE-BINDING DOMAINS; PROTEIN FRAGMENTS; STRUCTURAL BASIS; STRUCTURAL DATA;

AMINO ACIDS; BINDING ENERGY; CALCIUM; MANGANESE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

CALMODULIN;

AMINO ACID; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CALMODULIN; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 6; NOCODAZOLE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CELL CULTURE; CHEMICAL ANALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; IN VITRO STUDY; MEMBRANE STABILIZATION; MICROTUBULE; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; RAT; REGULATORY MECHANISM; STOICHIOMETRY; STRUCTURE ANALYSIS;

CALMODULIN; MAP6; MAPS; MICROTUBULES; NMR; STOP; TUBULIN;

ANIMALS; CALMODULIN; HELA CELLS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RATS; TUBULIN;

EID: 84883199117     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.457267     Document Type: Article

References (52)

1. Webb, B. C., and Wilson, L. (1980) Cold-stable microtubules from brain. Biochemistry 19, 1993-2001
2. Baas, P. W., and Heidemann, S. R. (1986) Microtubule reassembly from nucleating fragments during the regrowth of amputated neurites. J. Cell Biol. 103, 917-927
3. Baas, P. W., Slaughter, T., Brown, A., and Black, M. M. (1991) Microtubule dynamics in axons and dendrites. J. Neurosci. Res. 30, 134-153
4. Guillaud, L., Bosc, C., Fourest-Lieuvin, A., Denarier, E., Pirollet, F., Lafanechère, L., and Job, D. (1998) STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells. J. Cell Biol. 142, 167-179
5. Galiano, M. R., Bosc, C., Schweitzer, A., Andrieux, A., Job, D., and Hallak, M. E. (2004) Astrocytes and oligodendrocytes express different STOP protein isoforms. J. Neurosci. Res. 78, 329-337
6. Margolis, R. L., Rauch, C. T., and Job, D. (1986) Purification and assay of a 145-kDa protein (STOP145) with microtubule-stabilizing and motility behavior. Proc. Natl. Acad. Sci. U.S.A. 83, 639-643
7. Margolis, R. L., Rauch, C. T., Pirollet, F., and Job, D. (1990) Specific association of STOP protein with microtubules in vitro and with stable microtubules in mitotic spindles of cultured cells. EMBO J. 9, 4095-4102
8. Bosc, C., Cronk, J. D., Pirollet, F., Watterson, D. M., Haiech, J., Job, D., and Margolis, R. L. (1996) Cloning, expression, and properties of the microtubule-stabilizing protein STOP. Proc. Natl. Acad. Sci. U.S.A. 93, 2125-2130
9. Denarier, E., Fourest-Lieuvin, A., Bosc, C., Pirollet, F., Chapel, A., Margolis, R. L., and Job, D. (1998) Nonneuronal isoforms of STOP protein are responsible for microtubule cold stability in mammalian fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 95, 6055-6060
10. Denarier, E., Aguezzoul, M., Jolly, C., Vourc'h, C., Roure, A., Andrieux, A., Bosc, C., and Job, D. (1998) Genomic structure and chromosomal mapping of the mouse STOP gene (Mtap6). Biochem. Biophys. Res. Commun. 243, 791-796
11. Aguezzoul, M., Andrieux, A., and Denarier, E. (2003) Overlap of promoter and coding sequences in the mouse STOP gene (Mtap6). Genomics 81, 623-627
12. Andrieux, A., Salin, P. A., Vernet, M., Kujala, P., Baratier, J., Gory-Fauré, S., Bosc, C., Pointu, H., Proietto, D., Schweitzer, A., Denarier, E., Klumperman, J., and Job, D. (2002) The suppression of brain cold-stable microtubules in mice induces synaptic defects associated with neuroleptic-sensitive behavioral disorders. Genes Dev. 16, 2350-2364
13. Delotterie, D., Ruiz, G., Brocard, J., Schweitzer, A., Roucard, C., Roche, Y., Suaud-Chagny, M. F., Bressand, K., and Andrieux, A. (2010) Chronic administration of atypical antipsychotics improves behavioral and synaptic defects of STOP null mice. Psychopharmacology 208, 131-141
14. Shimizu, H., Iwayama, Y., Yamada, K., Toyota, T., Minabe, Y., Nakamura, K., Nakajima, M., Hattori, E., Mori, N., Osumi, N., and Yoshikawa, T. (2006) Genetic and expression analyses of the STOP (MAP6) gene in schizophrenia. Schizophr. Res. 84, 244-252
15. Choi, K. H., Zepp, M. E., Higgs, B. W., Weickert, C. S., and Webster, M. J. (2009) Expression profiles of schizophrenia susceptibility genes during human prefrontal cortical development. J. Psychiatry Neurosci. 34, 450-458
16. Martins-De-Souza, D., Dias-Neto, E., Schmitt, A., Falkai, P., Gormanns, P., Maccarrone, G., Turck, C. W., and Gattaz, W. F. (2010) Proteome analysis of schizophrenia brain tissue. World J. Biol. Psychiatry 11, 110-120
17. Benardais, K., Kasem, B., Couegnas, A., Samama, B., Fernandez, S., Schaeffer, C., Antal, M. C., Job, D., Schweitzer, A., Andrieux, A., Giersch, A., Nehlig, A., and Boehm, N. (2010) Loss of STOP protein impairs peripheral olfactory neurogenesis. PLoS One 5, e12753
18. Delphin, C., Bouvier, D., Seggio, M., Couriol, E., Saoudi, Y., Denarier, E., Bosc, C., Valiron, O., Bisbal, M., Arnal, I., and Andrieux, A. (2012) MAP6-F is a temperature sensor that directly binds to and protects microtubules from cold-induced depolymerization. J. Biol. Chem. 287, 35127-35138
19. Bosc, C., Frank, R., Denarier, E., Ronjat, M., Schweitzer, A., Wehland, J., and Job, D. (2001) Identification of novel bifunctional calmodulin-binding and microtubule-stabilizing motifs in STOP proteins. J. Biol. Chem. 276, 30904-30913
20. Job, D., Fischer, E. H., and Margolis, R. L. (1981) Rapid disassembly of cold-stable microtubules by calmodulin. Proc. Natl. Acad. Sci. U.S.A. 78, 4679-4682
21. Job, D., Rauch, C. T., Fischer, E. H., and Margolis, R. L. (1982) Recycling of cold-stable microtubules: evidence that cold stability is due to substoichiometric polymer blocks. Biochemistry 21, 509-515
22. 2+-calmodulin binding interactions of the microtubule-associated protein F-STOP. Biochemistry 42, 11484-11493
23. Castoldi, M., and Popov, A. V. (2003) Purification of brain tubulin through two cycles of polymerization-depolymerization in a high-molarity buffer. Protein Expr. Purif. 32, 83-88
24. Chernov, K. G., Curmi, P. A., Hamon, L., Mechulam, A., Ovchinnikov, L. P., and Pastré, D. (2008) Atomic force microscopy reveals binding of mRNA to microtubules mediated by two major mRNP proteins YB-1 and PABP. FEBS Lett. 582, 2875-2881
25. Grzesiek, S., and Bax, A. (1993) Amino acid type determination in the sequential assignment procedure of uniformly 13C/15N-enriched proteins. J. Biomol. NMR 3, 185-204
26. Johnson, B. A., and Blevins, R. A. (1994)NMRView: A computer program for the visualization and analysis of NMRdata. J. Biomol. NMR4, 603-614
27. Favier, A., and Brutscher, B. (2011) Recovering lost magnetization: polarization enhancement in biomolecular NMR. J. Biomol. NMR 49, 9-15
28. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
29. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graph 14, 33-38, 27-28
30. Lieuvin, A., Labbé, J. C., Dorée, M., and Job, D. (1994) Intrinsic microtubule stability in interphase cells. J. Cell Biol. 124, 985-996
31. Chernov, K. G., Mechulam, A., Popova, N. V., Pastre, D., Nadezhdina, E. S., Skabkina, O. V., Shanina, N. A., Vasiliev, V. D., Tarrade, A., Melki, J., Joshi, V., Baconnais, S., Toma, F., Ovchinnikov, L. P., and Curmi, P. A. (2008) YB-1 promotes microtubule assembly in vitro through interaction with tubulin and microtubules. BMC Biochem. 9, 23
32. 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 6, 135-140
33. Lefèvre, J., Chernov, K. G., Joshi, V., Delga, S., Toma, F., Pastré, D., Curmi, P. A., and Savarin, P. (2011) The C terminus of tubulin, a versatile partner for cationic molecules: binding of Tau, polyamines, and calcium. J. Biol. Chem. 286, 3065-3078
34. Ban, C., Ramakrishnan, B., Ling, K. Y., Kung, C., and Sundaralingam, M. (1994) Structure of the recombinant Paramecium tetraurelia calmodulin at 1.68 A resolution. Acta Crystallogr. D Biol. Crystallogr. 50, 50-63
35. Bonnet, C., Denarier, E., Bosc, C., Lazereg, S., Denoulet, P., and Larcher, J. C. (2002) Interaction of STOP with neuronal tubulin is independent of polyglutamylation. Biochem. Biophys. Res. Commun. 297, 787-793
36. Al-Bassam, J., Ozer, R. S., Safer, D., Halpain, S., and Milligan, R. A. (2002) MAP2 and tau bind longitudinally along the outer ridges of microtubule protofilaments. J. Cell Biol. 157, 1187-1196
37. Moores, C. A., Perderiset, M., Francis, F., Chelly, J., Houdusse, A., and Milligan, R. A. (2004) Mechanism of microtubule stabilization by doublecortin. Mol. Cell 14, 833-839
38. Makarov, A. A., Tsvetkov, P. O., Villard, C., Esquieu, D., Pourroy, B., Fahy, J., Braguer, D., Peyrot, V., and Lafitte, D. (2007) Vinflunine, a novel microtubule inhibitor, suppresses calmodulin interaction with the microtubule-associated protein STOP. Biochemistry 46, 14899-14906
39. 2+-and calmodulin-dependent flipflop mechanism in microtubule assembly-disassembly. FEBS Lett. 132, 141-143
40. Baratier, J., Peris, L., Brocard, J., Gory-Fauré, S., Dufour, F., Bosc, C., Fourest-Lieuvin, A., Blanchoin, L., Salin, P., Job, D., and Andrieux, A. (2006) Phosphorylation of microtubule-associated protein STOP by calmodulin kinase II. J. Biol. Chem. 281, 19561-19569
41. He, L., Hou, Z., and Qi, R. Z. (2008) Calmodulin binding and Cdk5 phosphorylation of p35 regulate its effect on microtubules. J. Biol. Chem. 283, 13252-13260
42. Lee, Y. C., and Wolff, J. (1984) The calmodulin-binding domain on microtubule-associated protein 2. J. Biol. Chem. 259, 8041-8044
43. Kotani, S., Nishida, E., Kumagai, H., and Sakai, H. (1985) Calmodulin inhibits interaction of actin with MAP2 and Tau, two major microtubule- associated proteins. J. Biol. Chem. 260, 10779-10783
44. Padilla, R., Maccioni, R. B., and Avila, J. (1990) Calmodulin binds to a tubulin binding site of the microtubule-associated protein tau. Mol. Cell Biochem. 97, 35-41
45. Meador, W. E., Means, A. R., and Quiocho, F. A. (1993) Modulation of calmodulin plasticity in molecular recognition on the basis of x-ray structures. Science 262, 1718-1721
46. 2+-calmodulin-dependent kinase kinase. Nat. Struct. Biol. 6, 819-824
47. McIlroy, B. K., Walters, J. D., Blackshear, P. J., and Johnson, J. D. (1991) Phosphorylation-dependent binding of a synthetic MARCKS peptide to calmodulin. J. Biol. Chem. 266, 4959-4964
48. Blackshear, P. J. (1993) The MARCKS family of cellular protein kinase C substrates. J. Biol. Chem. 268, 1501-1504
49. Minami, Y., Kawasaki, H., Suzuki, K., and Yahara, I. (1993) The calmodulin-binding domain of the mouse 90-kDa heat shock protein. J. Biol. Chem. 268, 9604-9610
50. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948
51. Livingstone, C. D., and Barton, G. J. (1993) Protein sequence alignments: a strategy for the hierarchical analysis of residue conservation. Comput. Appl. Biosci. 9, 745-756
52. Mulder, F. A., Schipper, D., Bott, R., and Boelens, R. (1999) Altered flexibility in the substrate-binding site of related native and engineered highalkaline Bacillus subtilisins. J. Mol. Biol. 292, 111-123