Conformation of the calmodulin-binding domain of metabotropic glutamate receptor subtype 7 and its interaction with calmodulin

Journal of Biochemistry

Volumn 149, Issue 4, 2011, Pages 463-474

  Isozumi, Noriyoshi ^a   Iida, Yoshinori ^a   Nakatomi, Akiko ^b   Nemoto, Nobuaki ^c   Yazawa, Michio ^b   Ohki, S ^a  

^a JAPAN ADVANCED INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c JEOL LTD   (Japan)

Author keywords

calmodulin; interaction; metabotropic glutamate receptor 7; multiple conformations; pre binding

Indexed keywords

CALCIUM ION; CALMODULIN; METABOTROPIC RECEPTOR 7; PEPTIDE; TRIFLUOROETHANOL;

ARTICLE; CIRCULAR DICHROISM; ENZYME MECHANISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; SURFACE PLASMON RESONANCE;

EID: 79953173950     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvr006     Document Type: Article

References (51)

1. Nakanishi, S. (1992) Molecular diversity of glutamate receptors and implications for brain function. Science 258, 597-603
2. Conn, P.J. and Pin, J.P. (1997) Pharmacology and func-tions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37, 205-237 (Pubitemid 27238875)
3. Nakanishi, S., Nakajima, Y., Masu, M., Ueda, Y., Nakahara, K., Watanabe, D., Yamaguchi, S., Kawabata, S., and Okada, M. (1998) Glutamate recep-tor: brain function and signal transduction. Brain Res. Brain Res. Rev. 26, 230-235 (Pubitemid 28318078)
4. Schoepp, D.D. (2001) Unveiling the functions of pre-synaptic metabotropic glutamate receptors in the central nervous system. J. Pharmacol. Exp. Ther. 299, 12-20 (Pubitemid 32905113)
5. Enz, R. (2006) The trick of the tail: protein-protein interactions of metabotropic glutamate receptors. BioEssay 29, 60-73
6. Kinoshita, A., Shigemoto, R., Ohishi, H., van der Putten, H., and Mizuno, N. (1998) Immunohistochemical localization of metabotropic glu-tamate receptors, mGluR 7a and mGluR 7b, in the cen-tral nervous system of the adult rat and mouse: a light and electron microscopic study. J. Comp. Neurol. 393, 332-352 (Pubitemid 28164590)
7. Lanthorn, T.H., Ganong, A.H., and Cotman, C.W. (1984) 2-Amino-4-phosphonobutyrate selectively blocks mossy fiber-CA3 responses in guinea pig but not rat hippocampus. Brain Res. 290, 174-178 (Pubitemid 14219431)
8. Bradley, S.R., Levey, A.I., Hersch, S.M., and Conn, P.J. (1996) Immunocytochemical localization of group III metabotropic glutamate receptors in the hippocampus with subtype-specific antibodies. J. Neurosci. 16, 2044-2056 (Pubitemid 26144017)
9. Masugi, M., Yokoi, M., Shigemoto, R., Muguruma, K., Watanabe, Y., Sansig, G., van der Putter, H., and Nakanishi, S. (1999) Metabotropic glutamate receptor subtype 7 ablation causes deficit in fear response and conditioned taste aversion. J. Neurosci. 19, 955-963 (Pubitemid 29066158)
10. O'Connor, V., El Far, O., Bofill-Cardona, E., Nanoff, C., Freissmuth, M., Karschin, A., Airas, J.M., Betz, H., and Boehm, S. (1999) Calmodulin dependence of presynaptic metabotropic glutamate receptor signaling. Science 286, 1180-1184
11. Nakajima, Y., Yamamoto, T., Nakayama, T., and Nakanishi, S. (1999) A relationship between protein kinase C phosphorylation and calmodulin binding to the metabotropic glutamate receptor subtype 7. J. Biol. Chem. 274, 27573-27577
12. Sorensen, S.D., Macek, T.A., Cai, Z., Saugstad, J.A., and Conn, P.J. (2002) Dissociation of protein kinase-mediated regulation of metabotropic glutamate receptor (mGluR 7) interactions with calmodulin and regulation of mGluR 7 function. Mol. Pharmacol. 61, 1303-1312 (Pubitemid 34575740)
13. El Far, O., Bofill-Cardona, E., Airas, J.M., O'Connor, V., Boehm, S., Freissmuth, M., Nanoff, C., and Betz, H. (2001) Mapping of calmodulin and Gβγ binding domains within the C-terminal region of the metabotropic glutam-ate receptor 7A. J. Biol. Chem. 276, 30662-30669
14. Ishida, H. and Vogel, H.J. (2006) Protein-peptide inter-action studies demonstrate the versatility of calmodulin target protein binding. Protein Pept. Lett. 13, 455-465
15. Chin, D. and Means, A.R. (2000) Calmodulin: a proto-typical calcium sensor. Trends Cell Biol. 10, 322-328
16. Rhoads, A.R. and Friedberg, F. (1997) Sequence motifs for calmodulin recognition. FASEB J. 11, 331-340 (Pubitemid 27193937)
17. 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
18. Meador, W.E., Means, A.R., and Quiocho, F.A. (1992) Target enzyme recognition by calmodulin: 2.4 a structure of a calmodulin-peptide complex. Science 257, 1251-1255
19. Scheschonka, A., Findlow, S., Schemm, R., El Far, O., Caldwell, J.H., Crump, M.P., Holden-Dye, K., O'Connor, V., Betz, H., and Werner, J.M. (2008) Structural determinants of calmodulin binding to the intracellular C-terminal domain of the metabotropic glu-tamate receptor 7A. J. Biol. Chem. 283, 5577-5588
20. Mal, T.K., Skrynnikov, N.R., Yap, K.L., Kay, L.E., and Ikura, M. (2002) Detecting protein kinase recognition modes of calmodulin by residual dipolar couplings in solution NMR. Biochemistry 41, 12899-12906 (Pubitemid 35215771)
21. Airas, J.M., Betz, H., and El Far, O. (2001) PKC phos-phorylation of a conserved serine residue in the C-terminus of group III metabotropic glutamate recep-tors inhibits calmodulin binding. FEBS Lett. 494, 60-63 (Pubitemid 32289372)
22. Isozumi, N. and Ohki, S. (2010) Expression and purifi-cation of metabotropic glutamate receptor 7 peptides. Protein Expr. Purif. 73, 46-50
23. Putkey, J.A., Slaughter, G.R., and Means, R. (1985) Bacterial expression and characterization of proteins derived from the chicken calmodulin cDNA and a cal-modulin processed gene. J. Biol. Chem. 260, 4704-4712 (Pubitemid 15034606)
24. Sorensen, B.R. and Shea, M.A. (1998) Interactions be-tween domains of apo calmodulin alter calcium binding and stability. Biochemistry 37, 4244-4253 (Pubitemid 28166447)
25. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMR Pipe: a multidimen-sional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
26. Godard, T.D. and Kneller, D.G. (2006) SPARKY Version 3.113., University of California, San Francisco
27. Yang, J.J., Buck, M., Pitkeathly, M., Kotik, M., Haynie, D.T., Dobson, C.M., and Radford, S.E. (1995) Conformational properties of four peptides spanning the sequence ofhen lysozyme. J. Mol. Biol. 252, 483-491
28. Itzhaki, L.S., Neira, J.L., Ruiz-Sanz, J., de Part Gay, G., and Fersht, A.R. (1995) Search for nucleation sites in smaller fragments of chymotrypsin inhibitor 2. J. Mol. Biol. 254, 289-304
29. Schleiff, E., Schmitz, A., McIlhinney, R.A., Manenti, S., and Vergeres, G (1996) Myristoylation does not modu-late the properties of MARCKS-related protein (MRP) in solution. J. Biol. Chem. 271, 26794-26802 (Pubitemid 26359089)
30. Weinreb, P.H., Zhen, W., Poon, A.W., Conway, K.A., and Lansbury, P.T. Jr (1996) NACP, a protein impli-cated in Alzheimer's disease and learning, is natively unfolded. Biochemistry 35, 13709-13715 (Pubitemid 26363912)
31. 2+-calmodulin. FEBS Lett. 421, 203-207 (Pubitemid 28045754)
32. Urbauer, J.L., Short, J.H., Dow, L.K., and Wand, A.J. (1995) Structual analysis of a novel interaction by cal-modulin: high-affinity binding of a peptide in the absence ofcalcium. Biochemistry 34, 8099-8109
33. +-dependent and-in-dependent interactions between calmodulin and its bind-ing domain of inducible nitric oxide synthase. FEBS Lett. 431, 210-214 (Pubitemid 28334218)
34. Wishart, D.S., Sykes, B.D., and Richards, F.M. (1992) The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31, 1647-1651
35. Gellman, S.H. (1991) On the role ofmethionine residue in the sequence-independent recognition of nonpolar protein surfaces. Biochemistry 30, 6633-6636
36. Zhang, M. and Vogel, H.J. (1994) The calmodulin-binding domain of caldesmon binds to cal-modulin in an α-helical conformation. Biochemistry 33, 1163-1171 (Pubitemid 24072446)
37. Siivari, K., Zhang, M., Palmer, A.G. III, and Vogel, H.J. (1995) NMR studies of the methionine methyl groups in calmodulin. FEBS Lett. 366, 104-108
38. Andreasen, T.J., Luetje, C.W., Heideman, W., and Storm, D.R. (1983) Purification of a novel calmodulin binding protein from bovine cerebral cortex membranes. Biochemistry 22, 4615-4618 (Pubitemid 13016989)
39. Baudier, J., Deloulme, J.C., Van Dorsselaer, A., and Matthes, H.W. (1991) Purification and characterization of a brain-specific protein kinase C substrate, neurogra-nin (p17). Identification of a consensus amino acid sequence between neurogranin and neuromodulin (GAP43) that corresponds to the protein kinase C phos-phorylation site and the calmodulin-binding domain. J. Biol. Chem. 266, 229-237 (Pubitemid 21906113)
40. Slemmon, J.R., Morgan, J.I., Fullerton, S.M., Danho, W., Hilbush, B.S., and Wengenack, T.M. (1996) Camstatins are peptide antagonists of calmodulin based upon a conserved structural motif in PEP-19, neurogranin, and neuromodu-lin. J. Biol. Chem. 271, 15911-15917 (Pubitemid 26236200)
41. +-binding protein. Biochemistry 36, 1295-1305 (Pubitemid 27074953)
42. 2+. J. Biol. Chem. 271, 22679-22686 (Pubitemid 26304711)
43. Dasgupta, M., Honeycutt, T., and Blumenthal, D.K. (1989) The gamma-subunit of skeletal muscle phosphor-ylase kinase contains two noncontiguous domains that act in concert to bind calmodulin. J. Biol. Chem. 264, 17156-17163 (Pubitemid 19255546)
44. Yamniuk, A.P. and Vogel, H.J. (2004) Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol. Biotechnol. 27, 33-57
45. Yuan, T., Walsh, M.P., Sutherland, C., Fabian, H., and Vogel, H.J. (1999) Calcium-dependent and-independent interaction of the calmodulin-binding domain of cyclic nucleotide phosphodiesterase with calmodulin. Biochemistry 38, 1446-1455
46. Bahler, M. and Rhoads, A. (2001) Calmodulin signaling via the IQ motif. FEBS Lett. 513, 107-113 (Pubitemid 34242986)
47. Houdusse, A. and Cohen, C. (1995) Target sequence recognition by the calmodulin superfamily: implications from light cahin binding to the regulatory domain of scallop myosin. Proc. Natl. Acad. Sci. 92, 10644-10647
48. Ishida, H., Borman, M.A., Ostrander, J., Vogel, H.J., and MacDonald, J.A. (2008) Solution structure of the calponin homology (CH) domain from the smoothelin-like 1 protein. J. Biol. Chem. 283, 20569-20578
49. Vetter, S.W. and Leclerc, E. (2003) Novel aspects of calmodulin target recognition and activation. Eur. J. Biochem. 270, 404-414 (Pubitemid 36177307)
50. Mal, T.K., Skrynnikov, N.R., Yap, K.L., Kay, L.E., and Ikura, M. (2002) Detecting protein kinase recognition modes of calmodulin by residual dipolar couplings in solution NMR. Biochemistry 41, 12899-12906 (Pubitemid 35215771)
51. Schneggenburger, R. and Neher, E. (2005) Presynaptic calcium and control of vesicle fusion. Curr. Opin. Neurobiol. 15, 266-274 (Pubitemid 40806437)