Caveolin-3 suppresses late sodium current by inhibiting nNOS-dependent S-nitrosylation of SCN5A

Journal of Molecular and Cellular Cardiology

Volumn 61, Issue , 2013, Pages 102-110

  Cheng, Jianding ^a,b   Valdivia, Carmen R ^a   Vaidyanathan, Ravi ^a   Balijepalli, Ravi C ^a   Ackerman, Michael J ^c   Makielski, Jonathan C ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c MAYO CLINIC   (United States)

Author keywords

Caveolin 3; Long QT syndrome; LQT9; Nitric oxide synthase; Sodium current; Sudden infant death syndrome

Indexed keywords

ALPHA1 SYNTROPHIN; CAVEOLIN 3; NEURAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE; SODIUM CHANNEL NAV1.5; SYNTROPHIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; LONG QT SYNDROME; LONG QT SYNDROME 9; NITROSYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM; SODIUM CURRENT;

CAVEOLIN-3; LONG QT SYNDROME; LQT9; NITRIC OXIDE SYNTHASE; SODIUM CURRENT; SUDDEN INFANT DEATH SYNDROME;

ANIMALS; CAVEOLIN 3; HEK293 CELLS; HUMANS; LONG QT SYNDROME; MEMBRANE POTENTIALS; MUTATION, MISSENSE; MYOCYTES, CARDIAC; NAV1.5 VOLTAGE-GATED SODIUM CHANNEL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; S-NITROSOTHIOLS; SODIUM;

RATTUS;

EID: 84880332939     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.03.013     Document Type: Article

References (32)

1. Westermann M., Steiniger F., Richter W. Belt-like localisation of caveolin in deep caveolae and its re-distribution after cholesterol depletion. Histochem Cell Biol 2005, 123:613-620.
2. Balijepalli R.C., Kamp T.J. Caveolae, ion channels and cardiac arrhythmias. Prog Biophys Mol Biol 2008, 98:149-160.
3. Parton R.G., Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol 2007, 8:185-194.
4. Li S., Galbiati F., Volonte D., Sargiacomo M., Engelman J.A., Das K., et al. Mutational analysis of caveolin-induced vesicle formation. Expression of caveolin-1 recruits caveolin-2 to caveolae membranes. FEBS Lett 1998, 434:127-134.
5. Vatta M., Ackerman M.J., Ye B., Makielski J.C., Ughanze E.E., Taylor E.W., et al. Mutant caveolin-3 induces persistent late sodium current and is associated with long-QT syndrome. Circulation 2006, 114:2104-2112.
6. Cronk L.B., Ye B., Kaku T., Tester D.J., Vatta M., Makielski J.C., et al. Novel mechanism for sudden infant death syndrome: persistent late sodium current secondary to mutations in caveolin-3. Heart Rhythm 2007, 4:161-166.
7. Ahern G.P., Hsu S.F., Klyachko V.A., Jackson M.B. Induction of persistent sodium current by exogenous and endogenous nitric oxide. J Biol Chem 2000, 275:28810-28815.
8. Ueda K., Valdivia C., Medeiros-Domingo A., Tester D.J., Vatta M., Farrugia G., et al. Syntrophin mutation associated with long QT syndrome through activation of the nNOS-SCN5A macromolecular complex. Proc Natl Acad Sci U S A 2008, 105:9355-9360.
9. Cheng J., Van Norstrand D.W., Medeiros-Domingo A., Valdivia C., Tan B.H., Ye B., et al. Alpha1-syntrophin mutations identified in sudden infant death syndrome cause an increase in late cardiac sodium current. Circ Arrhythm Electrophysiol 2009, 2:667-676.
10. Venema V.J., Ju H., Zou R., Venema R.C. Interaction of neuronal nitric-oxide synthase with caveolin-3 in skeletal muscle. Identification of a novel caveolin scaffolding/inhibitory domain. J Biol Chem 1997, 272:28187-28190.
11. Sunada Y., Ohi H., Hase A., Ohi H., Hosono T., Arata S., et al. Transgenic mice expressing mutant caveolin-3 show severe myopathy associated with increased nNOS activity. Hum Mol Genet 2001, 10:173-178.
12. Tan B.H., Pundi K.N., Van Norstrand D.W., Valdivia C.R., Tester D.J., Medeiros-Domingo A., et al. Sudden infant death syndrome-associated mutations in the sodium channel beta subunits. Heart Rhythm 2010, 7:771-778.
13. Yarbrough T.L., Lu T., Lee H.C., Shibata E.F. Localization of cardiac sodium channels in caveolin-rich membrane domains: regulation of sodium current amplitude. Circ Res 2002, 90:443-449.
14. Arking D.E., Pfeufer A., Post W., Kao W.H., Newton-Cheh C., Ikeda M., et al. A common genetic variant in the NOS1 regulator NOS1AP modulates cardiac repolarization. Nat Genet 2006, 38:644-651.
15. Aarnoudse A.J., Newton-Cheh C., de Bakker P.I., Straus S.M., Kors J.A., Hofman A., et al. Common NOS1AP variants are associated with a prolonged QTc interval in the Rotterdam Study. Circulation 2007, 116:10-16.
16. Lehtinen A.B., Newton-Cheh C., Ziegler J.T., Langefeld C.D., Freedman B.I., Daniel K.R., et al. Association of NOS1AP genetic variants with QT interval duration in families from the Diabetes Heart Study. Diabetes 2008, 57:1108-1114.
17. Chang K.C., Barth A.S., Sasano T., Kizana E., Kashiwakura Y., Zhang Y., et al. CAPON modulates cardiac repolarization via neuronal nitric oxide synthase signaling in the heart. Proc Natl Acad Sci U S A 2008, 105:4477-4482.
18. Kao W.H., Arking D.E., Post W., Rea T.D., Sotoodehnia N., Prineas R.J., et al. Genetic variations in nitric oxide synthase 1 adaptor protein are associated with sudden cardiac death in US white community-based populations. Circulation 2009, 119:940-951.
19. Osawa M., Kimura R., Hasegawa I., Mukasa N., Satoh F. SNP association and sequence analysis of the NOS1AP gene in SIDS. Leg Med (Tokyo) 2009, 11(Suppl. 1):S307-S308.
20. Jamshidi Y., Nolte I.M., Dalageorgou C., Zheng D., Johnson T., Bastiaenen R., et al. Common variation in the NOS1AP gene is associated with drug-induced QT prolongation and ventricular arrhythmia. J Am Coll Cardiol 2012, 60:841-850.
21. Frohnwieser B., Chen L.Q., Schreibmayer W., Kallen R.G. Modulation of the human cardiac sodium channel alpha-subunit by cAMP-dependent protein kinase and the responsible sequence domain. J Physiol (Lond) 1997, 498(Pt. 2):309-318.
22. Palygin O.A., Pettus J.M., Shibata E.F. Regulation of caveolar cardiac sodium current by a single Gsalpha histidine residue. Am J Physiol Heart Circ Physiol 2008, 294:H1693-H1699.
23. + channel antagonist inhibits hypertrophic signaling without reducing cardiac contractility. Circ Res 2012, 110:669-674.
24. Pfleger C., Ebeling G., Blasche R., Patton M., Patel H.H., Kasper M., et al. Detection of caveolin-3/caveolin-1/P2X7R complexes in mice atrial cardiomyocytes in vivo and in vitro. Histochem Cell Biol 2012, 138:231-241.
25. Gazzerro E., Bonetto A., Minetti C. Caveolinopathies: translational implications of caveolin-3 in skeletal and cardiac muscle disorders. Handb Clin Neurol 2011, 101:135-142.
26. Ye B., Balijepalli R.C., Foell J.D., Kroboth S., Ye Q., Luo Y.H., et al. Caveolin-3 associates with and affects the function of hyperpolarization-activated cyclic nucleotide-gated channel 4. Biochemistry 2008, 47:12312-12318.
27. Garg V., Sun W., Hu K. Caveolin-3 negatively regulates recombinant cardiac K(ATP) channels. Biochem Biophys Res Commun 2009, 385:472-477.
28. 2+ channels. J Biol Chem 2011, 286:2433-2444.
29. Tsutsumi Y.M., Horikawa Y.T., Jennings M.M., Kidd M.W., Niesman I.R., Yokoyama U., et al. Cardiac-specific overexpression of caveolin-3 induces endogenous cardiac protection by mimicking ischemic preconditioning. Circulation 2008, 118:1979-1988.
30. Tsutsumi Y.M., Kawaraguchi Y., Horikawa Y.T., Niesman I.R., Kidd M.W., Chin-Lee B., et al. Role of caveolin-3 and glucose transporter-4 in isoflurane-induced delayed cardiac protection. Anesthesiology 2010, 112:1136-1145.
31. Makielski J.C., Farley A.L. Na(+) current in human ventricle: implications for sodium loading and homeostasis. J Cardiovasc Electrophysiol 2006, 17(Suppl. 1):S15-S20.
32. Hale S.L., Shryock J.C., Belardinelli L., Sweeney M., Kloner R.A. Late sodium current inhibition as a new cardioprotective approach. J Mol Cell Cardiol 2008, 44:954-967.