Conservation of Ca2+/calmodulin regulation across Na and Ca 2+ channels

Cell

Volumn 157, Issue 7, 2014, Pages 1657-1670

  Ben Johny, Manu ^a   Yang, Philemon S ^a   Niu, Jacqueline ^a   Yang, Wanjun ^a   Joshi Mukherjee, Rosy ^a   Yue, David T ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CALMODULIN; SODIUM CHANNEL NAV1.5; CALCIUM; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CLONE; CONTROLLED STUDY; HEART MUSCLE; MODULATION; MUSCLE CHANNELOPATHY; MUTATION; MYOTONIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SKELETAL MUSCLE; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; GUINEA PIG; HUMAN; METABOLISM; MOLECULAR GENETICS; MUSCLE CELL; MYOBLAST; PHYLOGENY; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CALCIUM CHANNELS; CALMODULIN; GUINEA PIGS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUSCLE CELLS; MYOBLASTS; PHYLOGENY; RATS; SEQUENCE ALIGNMENT; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84903155994     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.04.035     Document Type: Article

References (79)

1. P.J. Adams, and T.P. Snutch Calcium channelopathies: voltage-gated calcium channels Subcell. Biochem. 45 2007 215 251
2. 2+ channel inactivation in controlling heart excitation Proc. Natl. Acad. Sci. USA 99 2002 17185 17190
3. J. Babitch Channel hands Nature 346 1990 321 322
4. H. Bazzazi, M. Ben Johny, P.J. Adams, T.W. Soong, and D.T. Yue Continuously tunable Ca(2+) regulation of RNA-edited CaV1.3 channels Cell Rep. 5 2013 367 377
5. M. Ben Johny, D.N. Yue, and D.T. Yue A novel FRET-based assay reveals 1:1 stoichiometry of apocalmodulin binding across voltage-gated Ca and Na ion channels Biophys J. 102 2012 125a 126a
6. M. Ben Johny, P.S. Yang, H. Bazzazi, and D.T. Yue Dynamic switching of calmodulin interactions underlies Ca2+ regulation of CaV1.3 channels Nature Commun. 4 2013 1717
7. M.J. Berridge Calcium signalling remodelling and disease Biochem. Soc. Trans. 40 2012 297 309
8. D.M. Bers, C.W. Patton, and R. Nuccitelli A practical guide to the preparation of Ca(2+) buffers Methods Cell Biol. 99 2010 1 26
9. S. Biswas, I. Deschênes, D. Disilvestre, Y. Tian, V.L. Halperin, and G.F. Tomaselli Calmodulin regulation of Nav1.4 current: role of binding to the carboxyl terminus J. Gen. Physiol. 131 2008 197 209
10. S. Biswas, D. DiSilvestre, Y. Tian, V.L. Halperin, and G.F. Tomaselli Calcium-mediated dual-mode regulation of cardiac sodium channel gating Circ. Res. 104 2009 870 878
11. S. Biswas, D.A. DiSilvestre, P. Dong, and G.F. Tomaselli Mechanisms of a human skeletal myotonia produced by mutation in the C-terminus of NaV1.4: is Ca2+ regulation defective? PLoS ONE 8 2013 e81063
12. J.G. Borst, and B. Sakmann Facilitation of presynaptic calcium currents in the rat brainstem J. Physiol. 513 1998 149 155
13. F. Bosmans, M.F. Martin-Eauclaire, and K.J. Swartz Deconstructing voltage sensor function and pharmacology in sodium channels Nature 456 2008 202 208
14. P. Brehm, and R. Eckert Calcium entry leads to inactivation of calcium channel in Paramecium Science 202 1978 1203 1206
15. S.C. Cannon From mutation to myotonia in sodium channel disorders Neuromuscul. Disord. 7 1997 241 249
16. B. Chagot, F. Potet, J.R. Balser, and W.J. Chazin Solution NMR structure of the C-terminal EF-hand domain of human cardiac sodium channel NaV1.5 J. Biol. Chem. 284 2009 6436 6445
17. S.H. Chao, Y. Suzuki, J.R. Zysk, and W.Y. Cheung Activation of calmodulin by various metal cations as a function of ionic radius Mol. Pharmacol. 26 1984 75 82
18. T. Clausen In isolated skeletal muscle, excitation may increase extracellular K+ 10-fold; how can contractility be maintained? Exp. Physiol. 96 2011 356 368
19. L. Crotti, C.N. Johnson, E. Graf, G.M. De Ferrari, B.F. Cuneo, M. Ovadia, J. Papagiannis, M.D. Feldkamp, S.G. Rathi, and J.D. Kunic et al. Calmodulin mutations associated with recurrent cardiac arrest in infants Circulation 127 2013 1009 1017
20. M. de Leon, Y. Wang, L. Jones, E. Perez-Reyes, X. Wei, T.W. Soong, T.P. Snutch, and D.T. Yue Essential Ca(2+)-binding motif for Ca(2+)-sensitive inactivation of L-type Ca2+ channels Science 270 1995 1502 1506
21. C.D. DeMaria, T.W. Soong, B.A. Alseikhan, R.S. Alvania, and D.T. Yue Calmodulin bifurcates the local Ca2+ signal that modulates P/Q-type Ca2+ channels Nature 411 2001 484 489
22. I. Deschênes, N. Neyroud, D. DiSilvestre, E. Marbán, D.T. Yue, and G.F. Tomaselli Isoform-specific modulation of voltage-gated Na(+) channels by calmodulin Circ. Res. 90 2002 E49 E57
23. K. Dunlap Calcium channels are models of self-control J. Gen. Physiol. 129 2007 379 383
24. R. Eckert, and J.E. Chad Inactivation of Ca channels Prog. Biophys. Mol. Biol. 44 1984 215 267
25. M.G. Erickson, B.A. Alseikhan, B.Z. Peterson, and D.T. Yue Preassociation of calmodulin with voltage-gated Ca(2+) channels revealed by FRET in single living cells Neuron 31 2001 973 985
26. M.D. Feldkamp, L. Yu, and M.A. Shea Structural and energetic determinants of apo calmodulin binding to the IQ motif of the Na(V)1.2 voltage-dependent sodium channel Structure 19 2011 733 747
27. R.I. Herzog, C. Liu, S.G. Waxman, and T.R. Cummins Calmodulin binds to the C terminus of sodium channels Nav1.4 and Nav1.6 and differentially modulates their functional properties J. Neurosci. 23 2003 8261 8270
28. B. Hille Ionic Channels of Excitable Membranes Third Edition 2001 Sinauer Associates Sunderland, MA
29. +-dependent inactivation Neuron 73 2012 304 316
30. J.P. Imredy, and D.T. Yue Submicroscopic Ca2+ diffusion mediates inhibitory coupling between individual Ca2+ channels Neuron 9 1992 197 207
31. 2+ channels Neuron 12 1994 1301 1318
32. L.Y. Jan, and Y.N. Jan Voltage-sensitive ion channels Cell 56 1989 13 25
33. J. Kim, S. Ghosh, H. Liu, M. Tateyama, R.S. Kass, and G.S. Pitt Calmodulin mediates Ca2+ sensitivity of sodium channels J. Biol. Chem. 279 2004 45004 45012
34. 2+ channels Neuron 41 2004 745 754
35. T. Kubota, M. Kinoshita, R. Sasaki, F. Aoike, M.P. Takahashi, S. Sakoda, and K. Hirose New mutation of the Na channel in the severe form of potassium-aggravated myotonia Muscle Nerve 39 2009 666 673
36. A. Lee, S.T. Wong, D. Gallagher, B. Li, D.R. Storm, T. Scheuer, and W.A. Catterall Ca2+/calmodulin binds to and modulates P/Q-type calcium channels Nature 399 1999 155 159
37. 2+ channel family Neuron 39 2003 951 960
38. W.B. Limpitikul, I.E. Dick, R. Joshi-Mukherjee, M.T. Overgaard, A.L. George, and D.T. Yue Calmodulin mutations associated with long QT syndrome prevent inactivation of cardiac L-type Ca2+ currents and promote proarrhythmic behavior in ventricular myocytes J. Mol. Cell. Cardiol 74 2014 115 124
39. S. Linse, and S. Forsén Determinants that govern high-affinity calcium binding Adv. Second Messenger Phosphoprotein Res. 30 1995 89 151
40. A. Mahajan, D. Sato, Y. Shiferaw, A. Baher, L.H. Xie, R. Peralta, R. Olcese, A. Garfinkel, Z. Qu, and J.N. Weiss Modifying L-type calcium current kinetics: consequences for cardiac excitation and arrhythmia dynamics Biophys. J. 94 2008 411 423
41. V.Z. Miloushev, J.A. Levine, M.A. Arbing, J.F. Hunt, G.S. Pitt, and A.G. Palmer 3rd Solution structure of the NaV1.2 C-terminal EF-hand domain J. Biol. Chem. 284 2009 6446 6454
42. M. Mori, T. Konno, T. Ozawa, M. Murata, K. Imoto, and K. Nagayama Novel interaction of the voltage-dependent sodium channel (VDSC) with calmodulin: does VDSC acquire calmodulin-mediated Ca2+-sensitivity? Biochemistry 39 2000 1316 1323
43. M.X. Mori, M.G. Erickson, and D.T. Yue Functional stoichiometry and local enrichment of calmodulin interacting with Ca2+ channels Science 304 2004 432 435
44. 2+ sensor for Ca2+ -dependent inactivation of L-type calcium channels Neuron 22 1999 549 558
45. B.Z. Peterson, J.S. Lee, J.G. Mulle, Y. Wang, M. de Leon, and D.T. Yue Critical determinants of Ca(2+)-dependent inactivation within an EF-hand motif of L-type Ca(2+) channels Biophys. J. 78 2000 1906 1920
46. G.S. Pitt, R.D. Zühlke, A. Hudmon, H. Schulman, H. Reuter, and R.W. Tsien Molecular basis of calmodulin tethering and Ca2+-dependent inactivation of L-type Ca2+ channels J. Biol. Chem. 276 2001 30794 30802
47. F. Potet, B. Chagot, M. Anghelescu, P.C. Viswanathan, S.Z. Stepanovic, S. Kupershmidt, W.J. Chazin, and J.R. Balser Functional Interactions between Distinct Sodium Channel Cytoplasmic Domains through the Action of Calmodulin J. Biol. Chem. 284 2009 8846 8854
48. R.R. Preston, J.A. Kink, R.D. Hinrichsen, Y. Saimi, and C. Kung Calmodulin mutants and Ca(2+)-dependent channels in Paramecium Annu. Rev. Physiol. 53 1991 309 319
49. B. Prod'hom, D. Pietrobon, and P. Hess Direct measurement of proton transfer rates to a group controlling the dihydropyridine-sensitive Ca2+ channel Nature 329 1987 243 246
50. M.F. Sarhan, C.C. Tung, F. Van Petegem, and C.A. Ahern Crystallographic basis for calcium regulation of sodium channels Proc. Natl. Acad. Sci. USA 109 2012 3558 3563
51. V.N. Shah, T.L. Wingo, K.L. Weiss, C.K. Williams, J.R. Balser, and W.J. Chazin Calcium-dependent regulation of the voltage-gated sodium channel hH1: intrinsic and extrinsic sensors use a common molecular switch Proc. Natl. Acad. Sci. USA 103 2006 3592 3597
52. P.C. Sternweis, and A.G. Gilman Aluminum: a requirement for activation of the regulatory component of adenylate cyclase by fluoride Proc. Natl. Acad. Sci. USA 79 1982 4888 4891
53. W. Stühmer, F. Conti, H. Suzuki, X.D. Wang, M. Noda, N. Yahagi, H. Kubo, and S. Numa Structural parts involved in activation and inactivation of the sodium channel Nature 339 1989 597 603
54. M.R. Tadross, R.W. Tsien, and D.T. Yue Ca2+ channel nanodomains boost local Ca2+ amplitude Proc. Natl. Acad. Sci. USA 110 2013 15794 15799
55. H.L. Tan, S. Kupershmidt, R. Zhang, S. Stepanovic, D.M. Roden, A.A. Wilde, M.E. Anderson, and J.R. Balser A calcium sensor in the sodium channel modulates cardiac excitability Nature 415 2002 442 447
56. J.S. Trimmer, S.S. Cooperman, W.S. Agnew, and G. Mandel Regulation of muscle sodium channel transcripts during development and in response to denervation Dev. Biol. 142 1990 360 367
57. F. Van Petegem, P.A. Lobo, and C.A. Ahern Seeing the forest through the trees: towards a unified view on physiological calcium regulation of voltage-gated sodium channels Biophys. J. 103 2012 2243 2251
58. S. Wagner, and L.S. Maier Modulation of cardiac Na(+) and Ca(2+) currents by CaM and CaMKII J. Cardiovasc. Electrophysiol. 17 Suppl 1 2006 S26 S33
59. C. Wang, B.C. Chung, H. Yan, S.Y. Lee, and G.S. Pitt Crystal structure of the ternary complex of a NaV C-terminal domain, a fibroblast growth factor homologous factor, and calmodulin Structure 20 2012 1167 1176
60. T.L. Wingo, V.N. Shah, M.E. Anderson, T.P. Lybrand, W.J. Chazin, and J.R. Balser An EF-hand in the sodium channel couples intracellular calcium to cardiac excitability Nat. Struct. Mol. Biol. 11 2004 219 225
61. F.F. Wu, E. Gordon, E.P. Hoffman, and S.C. Cannon A C-terminal skeletal muscle sodium channel mutation associated with myotonia disrupts fast inactivation J. Physiol. 565 2005 371 380
62. 2+-dependent inactivation of Ca(v)1.3 channels by calcium binding proteins of auditory hair cells J. Neurosci. 26 2006 10677 10689
63. J. Zhou, R. Olcese, N. Qin, F. Noceti, L. Birnbaumer, and E. Stefani Feedback inhibition of Ca2+ channels by Ca2+ depends on a short sequence of the C terminus that does not include the Ca2+ -binding function of a motif with similarity to Ca2+ -binding domains Proc. Natl. Acad. Sci. USA 94 1997 2301 2305
64. T. Zimmer, and R. Surber SCN5A channelopathies - an update on mutations and mechanisms Prog. Biophys. Mol. Biol. 98 2008 120 136
65. 1C subunit Proc. Natl. Acad. Sci. USA 95 1998 3287 3294
66. R.D. Zühlke, G.S. Pitt, K. Deisseroth, R.W. Tsien, and H. Reuter Calmodulin supports both inactivation and facilitation of L-type calcium channels Nature 399 1999 159 162
67. R.D. Zühlke, G.S. Pitt, R.W. Tsien, and H. Reuter Ca2+-sensitive inactivation and facilitation of L-type Ca2+ channels both depend on specific amino acid residues in a consensus calmodulin-binding motif in the(alpha)1C subunit J. Biol. Chem. 275 2000 21121 21129
68. 2+/calmodulin-dependent protein kinase II in guinea-pig ventricular myocytes Cardiovasc. Res. 85 2010 454 463
69. O. Arnaiz, and L. Sperling ParameciumDB in 2011: new tools and new data for functional and comparative genomics of the model ciliate Paramecium tetraurelia Nucleic Acids Res. 39 Database issue 2011 D632 D636
70. V1.5 gating by multiple phosphorylation sites J. Biol. Chem. 287 2012 19856 19869
71. D.A. Benson, I. Karsch-Mizrachi, D.J. Lipman, J. Ostell, and D.L. Wheeler GenBank Nucleic Acids Res. 33 Database issue 2005 D34 D38
72. 2+ channels J. Neurosci. 24 2004 6334 6342
73. R.C. Edgar MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 32 2004 1792 1797
74. 2+ channel CaM preassociation Neuron 39 2003 97 107
75. I.V. Grigoriev, H. Nordberg, I. Shabalov, A. Aerts, M. Cantor, D. Goodstein, A. Kuo, S. Minovitsky, R. Nikitin, and R.A. Ohm et al. The genome portal of the Department of Energy Joint Genome Institute Nucleic Acids Res. 40 Database issue 2012 D26 D32
76. J.A. Powell, L. Petherbridge, and B.E. Flucher Formation of triads without the dihydropyridine receptor alpha subunits in cell lines from dysgenic skeletal muscle J. Cell Biol. 134 1996 375 387
77. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods Mol. Biol. Evol. 28 2011 2731 2739
78. UniProt Consortium Update on activities at the Universal Protein Resource (UniProt) in 2013 Nucleic Acids Res. 41 Database issue 2013 D43 D47
79. +)-channel inactivation Proc. Natl. Acad. Sci. USA 89 1992 10910 10914