Perturbation of sodium channel structure by an inherited Long QT Syndrome mutation

Nature Communications

Volumn 3, Issue , 2012, Pages

  Glaaser, Ian W ^a   Osteen, Jeremiah D ^a   Puckerin, Akil ^a   Sampson, Kevin J ^a   Jin, Xiangshu ^b,c   Kass, Robert S ^a  

^a Columbia University Medical Center ^*  (United States)

^b NewYork Presbyterian Hospital   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METAL ION; POLYPEPTIDE; SODIUM CHANNEL NAV1.5; TRYPTOPHAN; MUTANT PROTEIN; SODIUM CHANNEL; SODIUM CHANNEL PROTEIN TYPE 5 SUBUNIT ALPHA;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEART ARRHYTHMIA; LONG QT SYNDROME; MUTATION; NUCLEAR MAGNETIC RESONANCE; PROTEIN INTERACTION; CELL MEMBRANE; CHANNEL GATING; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HEART; HEART MUSCLE; HEART MUSCLE CONDUCTION SYSTEM; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

AMINO ACID MOTIFS; CELL MEMBRANE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEART; HEART CONDUCTION SYSTEM; HUMANS; ION CHANNEL GATING; LONG QT SYNDROME; MODELS, MOLECULAR; MUTANT PROTEINS; MUTATION; MYOCARDIUM; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SODIUM CHANNELS;

EID: 84857730542     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1717     Document Type: Article

References (37)

1. Catterall, W. A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26, 13-25 (2000).
2. Nerbonne, J. M. & Kass, R. S. Molecular physiology of cardiac repolarization. Physiol. Rev. 85, 1205-1253 (2005). (Pubitemid 41362269)
3. Vassilev, P. M., Scheuer, T. & Catterall, W. A. Identifcation of an intracellular peptide segment involved in sodium channel inactivation. Science 241, 1658-1661 (1988).
4. West, J. W. et al. A cluster of hydrophobic amino acid residues required for fast Na(+)-channel inactivation. Proc. Natl Acad. Sci. USA 89, 10910-10914 (1992).
5. Fontaine, B. et al. Hyperkalemic periodic paralysis and the adult muscle sodium channel alpha-subunit gene. Science 250, 1000-1002 (1990). (Pubitemid 120031809)
6. Ptacek, L. J. et al. Identifcation of a mutation in the gene causing hyperkalemic periodic paralysis. Cell 67, 1021-1027 (1991). (Pubitemid 121001515)
7. Cannon, S. C. & Strittmatter, S. M. Functional expression of sodium channel mutations identifed in families with periodic paralysis. Neuron 10, 317-326 (1993). (Pubitemid 23079552)
8. Lossin, C., Wang, D. W., Rhodes, T. H., Vanoye, C. G. & George, A. L. Jr. Molecular basis of an inherited epilepsy. Neuron 34, 877-884 (2002). (Pubitemid 34722278)
9. George, A. L. Jr. Inherited channelopathies associated with epilepsy. Epilepsy Curr. 4, 65-70 (2004).
10. George, A. L. Jr. Inherited disorders of voltage-gated sodium channels. J. Clin. Invest. 115, 1990-1999 (2005). (Pubitemid 41134134)
11. Zimmer, T. & Surber, R. SCN5A channelopathies-an update on mutations and mechanisms. Prog. Biophys. Mol. Biol. 98, 120-136 (2008).
12. Wang, Q. et al. SCN5A mutations associated with an inherited cardiac arrhythmia, long QT syndrome. Cell 80, 805-811 (1995).
13. Bennett, P. B., Yazawa, K., Makita, N. & George, A. L. Jr. Molecular mechanism for an inherited cardiac arrhythmia. Nature 376, 683-685 (1995).
14. Kass, R. S. Sodium channel inactivation in heart: a novel role of the carboxy-terminal domain. J. Cardiovasc. Electrophysiol. 17 (Suppl 1), S21-S25 (2006).
15. + channel. Circulation 99, 3165-3171 (1999). (Pubitemid 29289083)
16. + channel activity through interactions between alpha-and beta1-subunits. Circ. Res. 83, 141-146 (1998). (Pubitemid 28354458)
17. Rivolta, I. et al. Inherited Brugada and long QT-3 syndrome mutations of a single residue of the cardiac sodium channel confer distinct channel and clinical phenotypes. J. Biol. Chem. 276, 30623-30630 (2001).
18. Bezzina, C. et al. A single Na(+) channel mutation causing both long QT and Brugada syndrome. Circ. Res. 85, 1206-1213 (1999). (Pubitemid 30430627)
19. Veldkamp, M. W. et al. Two distinct congenital arrhythmias evoked by a multidysfunctional Na(+) channel. Circ. Res. 86, E91-E97 (2000).
20. Cormier, J. W., Rivolta, I., Tateyama, M., Yang, A. S. & Kass, R. S. Secondary structure of the human cardiac Na+ channel C terminus: evidence for a role of helical structures in modulation of channel inactivation. J. Biol. Chem. 277, 9233-9241 (2002). (Pubitemid 34953004)
21. V1.5. J. Biol. Chem. 284, 6436-6445 (2009).
22. V1.2 C-terminal EF-hand domain. J. Biol. Chem. 284, 6446-6454 (2009).
23. + channel inactivation gate is a molecular complex: a novel role of the COOH-terminal domain. J. Gen. Physiol. 123, 155-165 (2004). (Pubitemid 38176607)
24. Bankston, J. R. et al. A novel LQT-3 mutation disrupts an inactivation gate complex with distinct rate-dependent phenotypic consequences. Channels 1, 273-280 (2007).
25. Biswas, S., DiSilvestre, D., Tian, Y., Halperin, V. L. & Tomaselli, G. F. Calcium-mediated dual-mode regulation of cardiac sodium channel gating. Circ. Res. 104, 870-878 (2009).
26. Wingo, T. L. et al. An EF-hand in the sodium channel couples intracellular calcium to cardiac excitability. Nat. Struct. Mol. Biol. 11, 219-225 (2004). (Pubitemid 38282766)
27. Shah, V. N. et al. 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, 3592-3597 (2006). (Pubitemid 43376600)
28. Potet, F. et al. Functional interactions between distinct sodium channel cytoplasmic domains through the action of calmodulin. J. Biol. Chem. 284, 8846-8854 (2009).
29. Taraska, J. W., Puljung, M. C., Olivier, N. B., Flynn, G. E. & Zagotta, W. N. Mapping the structure and conformational movements of proteins with transition metal ion FRET. Nat. Methods 6, 532-537 (2009).
30. Taraska, J. W., Puljung, M. C. & Zagotta, W. N. Short-distance probes for protein backbone structure based on energy transfer between bimane and transition metal ions. Proc. Natl Acad. Sci. USA 106, 16227-16232 (2009).
31. Glaaser, I. W., Bankston, J. R., Liu, H., Tateyama, M. & Kass, R. S. A carboxyl-terminal hydrophobic interface is critical to sodium channel function. Relevance to inherited disorders. J. Biol. Chem. 281, 24015-24023 (2006). (Pubitemid 44274175)
32. 2+ sensitivity of sodium channels. J. Biol. Chem. 279, 45004-45012 (2004). (Pubitemid 39430914)
33. V1.5. J. Mol. Biol. 406, 106-119 (2011).
34. Sarhan, M. F., Van Petegem, F. & Ahern, C. A. A double tyrosine motif in the cardiac sodium channel domain III-IV linker couples calcium-dependent calmodulin binding to inactivation gating. J. Biol. Chem. 284, 33265-33274 (2009).
35. Sun, W., Barchi, R. L. & Cohen, S. A. Probing sodium channel cytoplasmic domain structure. Evidence for the interaction of the rSkM1 amino and carboxyl termini. J. Biol. Chem. 270, 22271-22276 (1995).
36. de Vries, S. J. et al. HADDOCK vs. HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets. Proteins 69, 726-733 (2007). (Pubitemid 350210131)
37. de Vries, S. J., van Dijk, M. & Bonvin, A. M. The HADDOCK web server for data-driven biomolecular docking. Nat. Protoc. 5, 883-897 (2010).