Structural analysis of the voltage-dependent calcium channel β subunit functional core and its complex with the α1 interaction domain

Neuron

Volumn 42, Issue 3, 2004, Pages 387-399

  Opatowsky, Yarden ^a   Chen, Chien Chang ^b   Campbell, Kevin P ^b,c   Hirsch, Joel A ^a,b  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE; PROTEIN SUBUNIT; VOLTAGE GATED CALCIUM CHANNEL;

ARTICLE; CELL MEMBRANE; COMPLEX FORMATION; CRYSTALLOGRAPHY; ELECTROPHYSIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM CHANNELS; MOLECULAR SEQUENCE DATA; PROTEIN SUBUNITS; RABBITS;

EID: 2342666133     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(04)00250-8     Document Type: Article

References (83)

1. Abrahams J.P., Leslie A.G.W. Methods used in the structure determination of bovine mitochondrial F-1 ATPase. Acta Crystallogr. D. 52:1996;30-42
2. Andersen C.A., Palmer A.G., Brunak S., Rost B. Continuum secondary structure captures protein flexibility. Structure. 10:2002;175-184
3. Ball S.L., Powers P.A., Shin H.S., Morgans C.W., Peachey N.S., Gregg R.G. Role of the beta(2) subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Invest. Ophthalmol. Vis. Sci. 43:2002;1595-1603
4. 2+ channel expression at the cell surface by the small G-protein kir/Gem. Nature. 411:2001;701-706
5. Berrou L., Klein H., Bernatchez G., Parent L. A specific tryptophan in the I-II linker is a key determinant of beta-subunit binding and modulation in Ca(V)2.3 calcium channels. Biophys. J. 83:2002;1429-1442
6. 2+ channel alpha1 subunit contains an endoplasmic reticulum retention signal antagonized by the beta subunit. Neuron. 25:2000;177-190. a
7. Bichet D., Lecomte C., Sabatier J.M., Felix R., De Waard M. Reversibility of the Ca(2+) channel alpha(1)-beta subunit interaction. Biochem. Biophys. Res. Commun. 277:2000;729-735. b
8. Bohm G., Muhr R., Jaenicke R. Quantitative analysis of protein far UV circular dichroism spectra by neural networks. Protein Eng. 5:1992;191-195
9. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.-S., Kuszewki J., Nilges M., Pannu N.S., et al. Crystallography & NMR system. a new software suite for macromolecular structure determination Acta Crystallogr. D. 54:1998;905-921
10. Budisa N., Steipe B., Demange P., Eckerskorn C., Kellermann J., Huber R. High-level biosynthetic substitution of methionine in proteins by its analogs 2-aminohexanoic acid, selenomethionine, telluromethionine and ethionine in Escherichia coli. Eur. J. Biochem. 230:1995;788-796
11. Budnik V., Koh Y.H., Guan B., Hartmann B., Hough C., Woods D., Gorczyca M. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron. 17:1996;627-640
12. Canti C., Page K.M., Stephens G.J., Dolphin A.C. Identification of residues in the N terminus of alpha1B critical for inhibition of the voltage-dependent calcium channel by Gbeta gamma. J. Neurosci. 19:1999;6855-6864
13. Canti C., Davies A., Berrow N.S., Butcher A.J., Page K.M., Dolphin A.C. Evidence for two concentration-dependent processes for beta-subunit effects on alpha1B calcium channels. Biophys. J. 81:2001;1439-1451
14. Catterall W.A. Molecular properties of sodium and calcium channels. J. Bioenerg. Biomembr. 28:1996;219-230
15. Cens T., Dalle C., Charnet P. Expression of beta subunit modulates surface potential sensing by calcium channels. Pflugers Arch. 435:1998;865-867
16. Cens T., Restituito S., Galas S., Charnet P. Voltage and calcium use the same molecular determinants to inactivate calcium channels. J. Biol. Chem. 274:1999;5483-5490
17. 2+ channels. J. Biol. Chem. 270:1995;30036-30044
18. Chien A.J., Gao T., Perez-Reyes E., Hosey M.M. Membrane targeting of L-type calcium channels. Role of palmitoylation in the subcellular localization of the beta2a subunit. J. Biol. Chem. 273:1998;23590-23597
19. Cornet V., Bichet D., Sandoz G., Marty I., Brocard J., Bourinet E., Mori Y., Villaz M., De Waard M. Multiple determinants in voltage-dependent P/Q calcium channels control their retention in the endoplasmic reticulum. Eur. J. Neurosci. 16:2002;883-895
20. 2+ channel regulation by a conserved beta subunit domain. Neuron. 13:1994;495-503
21. 2+ channels. FEBS Lett. 380:1996;272-276
22. Dimitratos S.D., Woods D.F., Stathakis D.G., Bryant P.J. Signaling pathways are focused at specialized regions of the plasma membrane by scaffolding proteins of the MAGUK family. Bioessays. 21:1999;912-921
23. Dolphin A.C. β subunits of voltage-gated calcium channels. J. Bioenerg. Biomembr. 35:2003;599-620. a
24. Dolphin A.C. G protein modulation of voltage-gated calcium channels. Pharmacol. Rev. 55:2003;607-627. b
25. Esnouf R.M. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr. D. 55:1999;938-940
26. Finlin B.S., Crump S.M., Satin J., Andres D.A. Regulation of voltage-gated calcium channel activity by the Rem and Rad GTPases. Proc. Natl. Acad. Sci. USA. 100:2003;14469-14474
27. Geib S., Sandoz G., Mabrouk K., Matavel A., Marchot P., Hoshi T., Villaz M., Ronjat M., Miquelis R., Leveque C., de Waard M. Use of a purified and functional recombinant calcium-channel beta4 subunit in surface-plasmon resonance studies. Biochem. J. 364:2002;285-292
28. Hanada T., Lin L., Tibaldi E.V., Reinherz E.L., Chishti A.H. GAKIN, a novel kinesin-like protein associates with the human homologue of the Drosophila discs large tumor suppressor in T lymphocytes. J. Biol. Chem. 275:2000;28774-28784
29. 2+ channel beta subunit as a basis for understanding its functional properties. FEBS Lett. 445:1999;366-370
30. 2+ channels. J. Bioenerg. Biomembr. 35:2003;621-637
31. 2+-channel beta 4 subunit. Proc. Natl. Acad. Sci. USA. 100:2003;307-312
32. Jiang Y., Lee A., Chen J., Cadene M., Chait B.T., MacKinnon R. Crystal structure and mechanism of a calcium-gated potassium channel. Nature. 417:2002;515-522. a
33. Jiang Y., Lee A., Chen J., Cadene M., Chait B.T., MacKinnon R. The open pore conformation of potassium channels. Nature. 417:2002;523-526. b
34. Jones S.W. Overview of voltage-dependent calcium channels. J. Bioenerg. Biomembr. 30:1998;299-312
35. Jones T.A., Zou J.-Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A. 47:1991;110-119
36. Kim E., Naisbitt S., Hsueh Y.P., Rao A., Rothschild A., Craig A.M., Sheng M. GKAP, a novel synaptic protein that interacts with the guanylate kinase-like domain of the PSD-95/SAP90 family of channel clustering molecules. J. Cell Biol. 136:1997;669-678
37. Kraulis P.J. Molscript - a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:1991;946-950
38. Kuo A., Gulbis J.M., Antcliff J.F., Rahman T., Lowe E.D., Zimmer J., Cuthbertson J., Ashcroft F.M., Ezaki T., Doyle D.A. Crystal structure of the potassium channel KirBac1.1 in the closed state. Science. 300:2003;1922-1926
39. Laskowski R.A., Macarthur M.W., Moss D.S., Thornton J.M. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:1993;283-291
40. Leipe D.D., Koonin E.V., Aravind L. Evolution and classification of P-loop kinases and related proteins. J. Mol. Biol. 333:2003;781-815
41. Lo Conte L., Chothia C., Janin J. The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285:1999;2177-2198
42. Luo P., Baldwin R.L. Mechanism of helix induction by trifluoroethanol. a framework for extrapolating the helix-forming properties of peptides from trifluoroethanol/water mixtures back to water Biochemistry. 36:1997;8413-8421
43. Marquart A.F.V. Alpha-1-beta interaction in voltage-gated cardiac L-type calcium channels. FEBS Lett. 407:1997;137-140
44. Mathew D., Gramates L.S., Packard M., Thomas U., Bilder D., Perrimon N., Gorczyca M., Budnik V. Recruitment of scribble to the synaptic scaffolding complex requires GUK-holder, a novel DLG binding protein. Curr. Biol. 12:2002;531-539
45. McGee A.W., Dakoji S.R., Olsen O., Bredt D.S., Lim W.A., Prehoda K.E. Structure of the SH3-guanylate kinase module from PSD-95 suggests a mechanism for regulated assembly of MAGUK scaffolding proteins. Mol. Cell. 8:2001;1291-1301
46. Meinhart A., Alonso J.C., Strater N., Saenger W. Crystal structure of the plasmid maintenance system epsilon/zeta. functional mechanism of toxin zeta and inactivation by epsilon 2 zeta 2 complex formation Proc. Natl. Acad. Sci. USA. 100:2003;1661-1666
47. Merritt E.A., Bacon D.J. Raster3D. photorealistic molecular graphics Carter C.W. Jr., Sweet R.M. Methods in Enzymology, Volume 277. 1997;505-524 Academic Press, New York
48. Morris R.J., Perrakis A., Lamzin V.S. ARP/wARP and automatic interpretation of protein electron density maps. Methods Enzymol. 374:2003;229-244
49. Murata K., Odahara N., Kuniyasu A., Sato Y., Nakayama H., Nagayama K. Asymmetric arrangement of auxiliary subunits of skeletal muscle voltage-gated l-type Ca(2+) channel. Biochem. Biophys. Res. Commun. 282:2001;284-291
50. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D. 53:1997;240-255
51. Nicholls A., Sharp K.A., Honig B. Protein folding and association. insights from the interfacial and thermodynamic properties of hydrocarbons Proteins. 11:1991;281-296
52. Nishida M., MacKinnon R. Structural basis of inward rectification. cytoplasmic pore of the G protein-gated inward rectifier GIRK1 at 1.8 Å resolution Cell. 111:2002;957-965
53. Olcese R., Qin N., Schneider T., Neely A., Wei X., Stefani E., Birnbaumer L. The amino terminus of a calcium channel beta subunit sets rates of channel inactivation independently of the subunit's effect on activation. Neuron. 13:1994;1433-1438
54. Opatowsky Y., Chomsky-Hecht O., Kang M.G., Campbell K.P., Hirsch J.A. The voltage-dependent calcium channel beta subunit contains two stable interacting domains. J. Biol. Chem. 278:2003;52323-52332
55. Opatowsky Y., Chomsky-Hecht O., Hirsch J.A. Expression, purification, and crystallization of a functional core of the voltage dependent calcium channel β subunit. Acta Crystallogr. D. in press:2004
56. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Carter C.W. Jr., Sweet R.M. Methods in Enzymology, Volume 276. 1997;307-326 Academic Press, New York
57. Pace C.N., Scholtz J.M. A helix propensity scale based on experimental studies of peptides and proteins. Biophys. J. 75:1998;422-427
58. Pragnell M., De Waard M., Mori Y., Tanabe T., Snutch T.P., Campbell K.P. Calcium channel beta-subunit binds to a conserved motif in the I-II cytoplasmic linker of the alpha 1-subunit. Nature. 368:1994;67-70
59. 2+ channel inactivation gate. J. Neurosci. 20:2000;9046-9052
60. Restituito S., Cens T., Rousset M., Charnet P. Ca(2+) channel inactivation heterogeneity reveals physiological unbinding of auxiliary beta subunits. Biophys. J. 81:2001;89-96
61. Schreiber G. Kinetic studies of protein-protein interactions. Curr. Opin. Struct. Biol. 12:2002;41-47
62. Sekulic N., Shuvalova L., Spangenberg O., Konrad M., Lavie A. Structural characterization of the closed conformation of mouse guanylate kinase. J. Biol. Chem. 277:2002;30236-30243
63. 2+ channel by electron cryomicroscopy. Proc. Natl. Acad. Sci. USA. 99:2002;10370-10375
64. Shatsky M., Nussinov R., Wolfson H.J. Flexible protein alignment and hinge detection. Proteins. 48:2002;242-256
65. Stehle T., Schulz G.E. Refined structure of the complex between guanylate kinase and its substrate GMP at 2.0 Å resolution. J. Mol. Biol. 224:1992;1127-1141
66. 2+ channel amino terminus contributes determinants for beta subunit-mediated voltage-dependent inactivation properties. J. Physiol. 525:2000;377-390
67. Stotz S.C., Jarvis S.E., Zamponi G.W. Functional roles of cytoplasmic loops and pore lining transmembrane helices in the voltage-dependent inactivation of HVA calcium channels. J. Physiol. 554:2004;263-273
68. Takeuchi M., Hata Y., Hirao K., Toyoda A., Irie M., Takai Y. SAPAPs. A family of PSD-95/SAP90-associated proteins localized at postsynaptic density. J. Biol. Chem. 272:1997;11943-11951
69. Tanabe T., Takeshima H., Mikami A., Flockerzi V., Takahashi H., Kangawa K., Kojima M., Matsuo H., Hirose T., Numa S. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature. 328:1987;313-318
70. Tareilus E., Roux M., Qin N., Olcese R., Zhou J., Stefani E., Birnbaumer L. A Xenopus oocyte beta subunit. evidence for a role in the assembly/expression of voltage-gated calcium channels that is separate from its role as a regulatory subunit Proc. Natl. Acad. Sci. USA. 94:1997;1703-1708
71. Tavares G.A., Panepucci E.H., Brunger A.T. Structural characterization of the intramolecular interaction between the SH3 and guanylate kinase domains of PSD-95. Mol. Cell. 8:2001;1313-1325
72. Terwilliger T.C. Solve and resolve. automated structure solution and density modification Methods Enzymol. 374:2003;22-37
73. Vagin A., Teplyakov A. An approach to multi-copy search in molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 56:2000;1622-1624
74. Van Duyne G.D., Standaert R.F., Karplus P.A., Schreiber S.L., Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229:1993;105-124
75. 2+ channels. role in channel function Trends Neurosci. 21:1998;148-154
76. 2+ channel alpha(1a) subunit. J. Biol. Chem. 273:1998;2361-2367
77. 2+ channel activation. J. Biol. Chem. 274:1999;12383-12390
78. Wang M.C., Collins R.F., Ford R.C., Berrow N.S., Dolphin A.C., Kitmitto A. The three-dimensional structure of the cardiac L-type voltage-gated calcium channel. comparison with the skeletal muscle form reveals a common architectural motif J. Biol. Chem. 279:2003;7159-7168
79. Ward Y., Spinelli B., Quon M.J., Chen H., Ikeda S.R., Kelly K. Phosphorylation of critical serine residues in gem separates cytoskeletal reorganization from down-regulation of calcium channel activity. Mol. Cell. Biol. 24:2004;651-661
80. 2+ channel beta subunits with the alpha 1 subunit interaction domain. J. Biol. Chem. 270:1995;18088-18093
81. 2+ channel using electron cryo-microscopy. J. Mol. Biol. 332:2003;171-182
82. Wu X., Knudsen B., Feller S.M., Zheng J., Sali A., Cowburn D., Hanafusa H., Kuriyan J. Structural basis for the specific interaction of lysine-containing proline-rich peptides with the N-terminal SH3 domain of c-Crk. Structure. 3:1995;215-226
83. Yang A.S., Honig B. Free energy determinants of secondary structure formation. I. alpha-helices J. Mol. Biol. 252:1995;351-365