Alanine-Scanning Mutagenesis Defines a Conserved Energetic Hotspot in the CaVα1 AID-CaVβ Interaction Site that Is Critical for Channel Modulation

Structure

Volumn 16, Issue 2, 2008, Pages 280-294

  Van Petegem, Filip ^a   Duderstadt, Karl E ^a   Clark, Kimberly A ^a   Wang, Michelle ^a   Minor Jr , Daniel L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

PROTEINS; SIGNALING

Indexed keywords

ALANINE; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL ALPHA1; VOLTAGE GATED CALCIUM CHANNEL BETA;

ARTICLE; BINDING SITE; COMPLEX FORMATION; ELECTROPHYSIOLOGY; ISOTHERMAL TITRATION CALORIMETRY; MUTAGENESIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; THERMODYNAMICS;

ALANINE; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM CHANNELS; CALCIUM CHANNELS, L-TYPE; CALORIMETRY; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RABBITS; RATS; THERMODYNAMICS;

EID: 38949120535     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2007.11.010     Document Type: Article

References (70)

1. Arkin M.R., and Wells J.A. Small-molecule inhibitors of protein-protein interactions: progressing towards the dream. Nat. Rev. Drug Discov. 3 (2004) 301-317
2. 2+ channel expression at the cell surface by the small G-protein kir/Gem. Nature 411 (2001) 701-706
3. Bell D.C., Butcher A.J., Berrow N.S., Page K.M., Brust P.F., Nesterova A., Stauderman K.A., Seabrook G.R., Nurnberg B., and Dolphin A.C. Biophysical properties, pharmacology, and modulation of human, neuronal L-type (α(1D), Ca(V)1.3) voltage-dependent calcium currents. J. Neurophysiol. 85 (2001) 816-827
4. Berrou L., Bernatchez G., and Parent L. Molecular determinants of inactivation within the I-II linker of α1E (CaV2.3) calcium channels. Biophys. J. 80 (2001) 215-228
5. Berrou L., Dodier Y., Raybaud A., Tousignant A., Dafi O., Pelletier J.N., and Parent L. The C-terminal residues in the α-interacting domain (AID) helix anchor CaV β subunit interaction and modulation of CaV2.3 channels. J. Biol. Chem. 280 (2005) 494-505
6. 2+ channel α1 subunit contains an endoplasmic reticulum retention signal antagonized by the β subunit. Neuron 25 (2000) 177-190
7. Bogan A.A., and Thorn K.S. Anatomy of hot spots in protein interfaces. J. Mol. Biol. 280 (1998) 1-9
8. Bouchard C., Price R.B., Moneypenny C.G., Thompson L.F., Zillhardt M., Stalheim L., and Anderson P.A. Cloning and functional expression of voltage-gated ion channel subunits from cnidocytes of the Portuguese Man O'War Physalia physalis. J. Exp. Biol. 209 (2006) 2979-2989
9. 2+ channel β subunit gene Cchb4 is associated with ataxia and seizures in the lethargic (lh) mouse. Cell 88 (1997) 385-392
10. Butcher A.J., Leroy J., Richards M.W., Pratt W.S., and Dolphin A.C. The importance of occupancy rather than affinity of CaV{β} subunits for the calcium channel I-II linker in relation to calcium channel function. J. Physiol. 574 (2006) 387-398
11. Canti C., Davies A., Berrow N.S., Butcher A.J., Page K.M., and Dolphin A.C. Evidence for two concentration-dependent processes for β-subunit effects on α1B calcium channels. Biophys. J. 81 (2001) 1439-1451
12. Cantí C., Davies A., and Dolphin A.C. Calcium channel α2δ subunits: structure, functions, and target site for drugs. Curr. Neuropharmacol. 1 (2003) 209-217
13. 2+ channels. Annu. Rev. Cell Dev. Biol. 16 (2000) 521-555
14. 2+ channels. Nature 429 (2004) 675-680
15. Chien A.J., Carr K.M., Shirokov R.E., Rios E., and Hosey M.M. Identification of palmitoylation sites within the L-type calcium channel β2a subunit and effects on channel function. J. Biol. Chem. 271 (1996) 26465-26468
16. Clackson T., and Wells J.A. A hot spot of binding energy in a hormone-receptor interface. Science 267 (1995) 383-386
17. Colecraft H.M., Alseikhan B., Takahashi S.X., Chaudhuri D., Mittman S., Yegnasubramanian V., Alvania R.S., Johns D.C., Marban E., and Yue D.T. Novel functional properties of Ca(2+) channel β subunits revealed by their expression in adult rat heart cells. J. Physiol. 541 (2002) 435-452
18. Dafi O., Berrou L., Dodier Y., Raybaud A., Sauve R., and Parent L. Negatively charged residues in the N-terminal of the AID helix confer slow voltage dependent inactivation gating to CaV1.2. Biophys. J. 87 (2004) 3181-3192
19. Desrosiers D.C., and Peng Z.Y. A binding free energy hot spot in the ankyrin repeat protein GABPβ mediated protein-protein interaction. J. Mol. Biol. 354 (2005) 375-384
20. 2+ channels. FEBS Lett. 380 (1996) 272-276
21. Dolphin A.C. β subunits of voltage-gated calcium channels. J. Bioenerg. Biomembr. 35 (2003) 599-620
22. Dolphin A.C. G protein modulation of voltage-gated calcium channels. Pharmacol. Rev. 55 (2003) 607-627
23. Edelhoch H. Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 6 (1967) 1948-1954
24. Geib S., Sandoz G., Mabrouk K., Matavel A., Marchot P., Hoshi T., Villaz M., Ronjat M., Miquelis R., Leveque C., et al. Use of a purified and functional recombinant calcium-channel β4 subunit in surface-plasmon resonance studies. Biochem. J. 364 (2002) 285-292
25. Grabner M., Bachmann A., Rosenthal F., Striessnig J., Schultz C., Tautz D., and Glossmann H. Insect calcium channels. Molecular cloning of an α 1-subunit from housefly (Musca domestica) muscle. FEBS Lett. 339 (1994) 189-194
26. Grabner M., Wang Z., Mitterdorfer J., Rosenthal F., Charnet P., Savchenko A., Hering S., Ren D., Hall L.M., and Glossmann H. Cloning and functional expression of a neuronal calcium channel β subunit from house fly (Musca domestica). J. Biol. Chem. 269 (1994) 23668-23674
27. Gregg R.G., Messing A., Strube C., Beurg M., Moss R., Behan M., Sukhareva M., Haynes S., Powell J.A., Coronado R., et al. Absence of the β subunit (cchb1) of the skeletal muscle dihydropyridine receptor alters expression of the α 1 subunit and eliminates excitation-contraction coupling. Proc. Natl. Acad. Sci. USA 93 (1996) 13961-13966
28. Harry J.B., Kobrinsky E., Abernethy D.R., and Soldatov N.M. New short splice variants of the human cardiac Cavβ2 subunit: redefining the major functional motifs implemented in modulation of the Cav1.2 channel. J. Biol. Chem. 279 (2004) 46367-46372
29. 2+ channels. Biophys. J. 93 (2007) 834-845
30. Hering S. β-subunits: fine tuning of Ca(2+) channel block. Trends Pharmacol. Sci. 23 (2002) 509-513
31. Herlitze S., Hockerman G.H., Scheuer T., and Catterall W.A. Molecular determinants of inactivation and G protein modulation in the intracellular loop connecting domains I and II of the calcium channel α1A subunit. Proc. Natl. Acad. Sci. USA 94 (1997) 1512-1516
32. Hidalgo P., Gonzalez-Gutierrez G., Garcia-Olivares J., and Neely A. The α1-β-subunit interaction that modulates calcium channel activity is reversible and requires a competent α-interaction domain. J. Biol. Chem. 281 (2006) 24104-24110
33. Hille B. Ion Channels of Excitable Membranes. Third Edition (2001), Sinauer Associates, Sunderland, MA
34. 2+ channel α 1 subunits from the marine ray Discopyge ommata. Proc. Natl. Acad. Sci. USA 90 (1993) 3787-3791
35. Hullin R., Khan I.F., Wirtz S., Mohacsi P., Varadi G., Schwartz A., and Herzig S. Cardiac L-type calcium channel β-subunits expressed in human heart have differential effects on single channel characteristics. J. Biol. Chem. 278 (2003) 21623-21630
36. Jencks W.P. On the attribution of additivity of binding energies. Proc. Natl. Acad. Sci. USA 78 (1981) 4046-4050
37. Jeziorski M.C., Greenberg R.M., Clark K.S., and Anderson P.A. Cloning and functional expression of a voltage-gated calcium channel α1 subunit from jellyfish. J. Biol. Chem. 273 (1998) 22792-22799
38. Jeziorski M.C., Greenberg R.M., and Anderson P.A. Cloning and expression of a jellyfish calcium channel β subunit reveal functional conservation of the α1-β interaction. Receptors Channels 6 (1999) 375-386
39. Kohn A.B., Anderson P.A., Roberts-Misterly J.M., and Greenberg R.M. Schistosome calcium channel β subunits. Unusual modulatory effects and potential role in the action of the antischistosomal drug praziquantel. J. Biol. Chem. 276 (2001) 36873-36876
40. Kohn A.B., Lea J., Roberts-Misterly J.M., Anderson P.A., and Greenberg R.M. Structure of three high voltage-activated calcium channel α1 subunits from Schistosoma mansoni. Parasitology 123 (2001) 489-497
41. 2+ channel cause myotonia in Caenorhabditis elegans. EMBO J. 16 (1997) 6066-6076
42. Leroy J., Richards M.W., Butcher A.J., Nieto-Rostro M., Pratt W.S., Davies A., and Dolphin A.C. Interaction via a key tryptophan in the I-II linker of N-type calcium channels is required for β1 but not for palmitoylated β2, implicating an additional binding site in the regulation of channel voltage-dependent properties. J. Neurosci. 25 (2005) 6984-6996
43. Maltez J.M., Nunziato D.A., Kim J., and Pitt G.S. Essential Ca(V) β modulatory properties are AID-independent. Nat. Struct. Mol. Biol. 12 (2005) 372-377
44. Murakami M., Fleischmann B., De Felipe C., Freichel M., Trost C., Ludwig A., Wissenbach U., Schwegler H., Hofmann F., Hescheler J., et al. Pain perception in mice lacking the β3 subunit of voltage-activated calcium channels. J. Biol. Chem. 277 (2002) 40342-40351
45. 2+ channel β3 subunit. J. Biol. Chem. 278 (2003) 43261-43267
46. 2+ channels in neurons. Proc. Natl. Acad. Sci. USA 95 (1998) 12010-12015
47. Neely A., Wei X., Olcese R., Birnbaumer L., and Stefani E. Potentiation by the β subunit of the ratio of the ionic current to the charge movement in the cardiac calcium channel. Science 262 (1993) 575-578
48. Opatowsky Y., Chomsky-Hecht O., Kang M.G., Campbell K.P., and Hirsch J.A. The voltage-dependent calcium channel β subunit contains two stable interacting domains. J. Biol. Chem. 278 (2003) 52323-52332
49. Opatowsky Y., Chen C.C., Campbell K.P., and Hirsch J.A. Structural analysis of the voltage-dependent calcium channel β subunit functional core and its complex with the α1 interaction domain. Neuron 42 (2004) 387-399
50. Perez-Reyes E., Castellano A., Kim H.S., Bertrand P., Baggstrom E., Lacerda A.E., Wei X.Y., and Birnbaumer L. Cloning and expression of a cardiac/brain β subunit of the L-type calcium channel. J. Biol. Chem. 267 (1992) 1792-1797
51. Pitt G.S. Calmodulin and CaMKII as molecular switches for cardiac ion channels. Cardiovasc. Res. 73 (2007) 641-647
52. Pragnell M., De Waard M., Mori Y., Tanabe T., Snutch T.P., and Campbell K.P. Calcium channel β-subunit binds to a conserved motif in the I-II cytoplasmic linker of the α 1-subunit. Nature 368 (1994) 67-70
53. Reichmann D., Rahat O., Cohen M., Neuvirth H., and Schreiber G. The molecular architecture of protein-protein binding sites. Curr. Opin. Struct. Biol. 17 (2007) 67-76
54. Restituito S., Cens T., Rousset M., and Charnet P. Ca(2+) channel inactivation heterogeneity reveals physiological unbinding of auxiliary β subunits. Biophys. J. 81 (2001) 89-96
55. Rottbauer W., Baker K., Wo Z.G., Mohideen M.A., Cantiello H.F., and Fishman M.C. Growth and function of the embryonic heart depend upon the cardiac-specific L-type calcium channel α1 subunit. Dev. Cell 1 (2001) 265-275
56. Schredelseker J., Di Biase V., Obermair G.J., Felder E.T., Flucher B.E., Franzini-Armstrong C., and Grabner M. The β 1a subunit is essential for the assembly of dihydropyridine-receptor arrays in skeletal muscle. Proc. Natl. Acad. Sci. USA 102 (2005) 17219-17224
57. Spafford J.D., Chen L., Feng Z.P., Smit A.B., and Zamponi G.W. Expression and modulation of an invertebrate presynaptic calcium channel α1 subunit homolog. J. Biol. Chem. 278 (2003) 21178-21187
58. Spafford J.D., Van Minnen J., Larsen P., Smit A.B., Syed N.I., and Zamponi G.W. Uncoupling of calcium channel α1 and β subunits in developing neurons. J. Biol. Chem. 279 (2004) 41157-41167
59. 2+ channels. J. Gen. Physiol. 126 (2005) 365-377
60. Tareilus E., Roux M., Qin N., Olcese R., Zhou J., Stefani E., and Birnbaumer L. A Xenopus oocyte β 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
61. Van Petegem F., and Minor Jr. D.L. The structural biology of voltage-gated calcium channel function and regulation. Biochem. Soc. Trans. 34 (2006) 887-893
62. Van Petegem F., Clark K.A., Chatelain F.C., and Minor Jr. D.L. Structure of a complex between a voltage-gated calcium channel β-subunit and an α-subunit domain. Nature 429 (2004) 671-675
63. Velazquez Campoy A., and Freire E. ITC in the post-genomic era? Priceless. Biophys. Chem. 115 (2005) 115-124
64. 2+ channel α 1A subunit. J. Biol. Chem. 273 (1998) 2361-2367
65. -/- embryos impairs cardiac development and contraction with secondary defects in vascular maturation. Circ. Res. 99 (2006) 749-757
66. Wells J.A. Systematic mutational analyses of protein-protein interfaces. Methods Enzymol. 202 (1991) 390-411
67. 2+ channel β subunits with the α 1 subunit interaction domain. J. Biol. Chem. 270 (1995) 18088-18093
68. Yamaguchi H., Okuda M., Mikala G., Fukasawa K., and Varadi G. Cloning of the β(2a) subunit of the voltage-dependent calcium channel from human heart: cooperative effect of α(2)/δ and β(2a) on the membrane expression of the α(1C) subunit. Biochem. Biophys. Res. Commun. 267 (2000) 156-163
69. Young K., Lin S., Sun L., Lee E., Modi M., Hellings S., Husbands M., Ozenberger B., and Franco R. Identification of a calcium channel modulator using a high throughput yeast two-hybrid screen. Nat. Biotechnol. 16 (1998) 946-950
70. Zoccola D., Tambutte E., Senegas-Balas F., Michiels J.F., Failla J.P., Jaubert J., and Allemand D. Cloning of a calcium channel α1 subunit from the reef-building coral, Stylophora pistillata. Gene 227 (1999) 157-167