The interaction of caveolin 3 protein with the potassium inward rectifier channel Kir2.1: Physiology and pathology related to long QT syndrome 9 (LQT9)

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17472-17480

  Vaidyanathan, Ravi ^a   Vega, Amanda L ^a,c   Song, Chunhua ^a   Zhou, Qing ^a   Tan, Bihua ^a   Berger, Stuart ^b   Makielski, Jonathan C ^a   Eckhardt, Lee L ^a  

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

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICAL PROPERTIES; CELL SURFACE EXPRESSION; GOLGI COMPARTMENTS; HETEROLOGOUS EXPRESSION; MOLECULAR DISTANCES; PROTEIN LOCATIONS; VENTRICULAR MYOCYTES; WESTERN-BLOT ANALYSIS;

CELL MEMBRANES;

PROTEINS;

CAVEOLIN 3; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN TISSUE; LONG QT SYNDROME; LONG QT SYNDROME 9; LOSS OF FUNCTION MUTATION; MOLECULAR PATHOLOGY; NONHUMAN; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; WESTERN BLOTTING;

ARRHYTHMIAS, BASIC STUDIES; CARDIOMYOPATHY; CAVEOLIN; ELECTROPHYSIOLOGY; ION CHANNELS; LONG QT SYNDROME (LQTS); POTASSIUM CHANNELS;

ANIMALS; CAVEOLIN 3; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GOLGI APPARATUS; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; LONG QT SYNDROME; MEMBRANE POTENTIALS; MICROSCOPY, FLUORESCENCE; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; MYOCYTES, CARDIAC; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN BINDING; PROTEIN TRANSPORT;

RATTUS;

EID: 84879034942     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.435370     Document Type: Article

References (32)

1. Schwartz, P. J., Crotti, L., and Insolia, R. (2012) Long-QT syndrome. From genetics to management. Circ. Arrhythm. Electrophysiol. 5, 868-877
2. Song, K. S., Scherer, P. E., Tang, Z., Okamoto, T., Li, S., Chafel, M., Chu, C., Kohtz, D. S., and Lisanti, M. P. (1996) Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J. Biol. Chem. 271, 15160-15165 (Pubitemid 26197582)
3. Cohen, A. W., Hnasko, R., Schubert, W., and Lisanti, M. P. (2004) Role of caveolae and caveolins in health and disease. Physiol. Rev. 84, 1341-1379 (Pubitemid 39287953)
4. Balijepalli, R. C., and Kamp, T. J. (2008) Caveolae, ion channels and cardiac arrhythmias. Prog. Biophys. Mol. Biol. 98, 149-160
5. Vatta, M., Ackerman, M. J., Ye, B., Makielski, J. C., Ughanze, E. E., Taylor, E. W., Tester, D. J., Balijepalli, R. C., Foell, J. D., Li, Z., Kamp, T. J., and Towbin, J. A. (2006) Mutant caveolin-3 induces persistent late sodium current and is associated with long-QT syndrome. Circulation 114, 2104-2112 (Pubitemid 44747890)
6. Leonoudakis, D., Conti, L. R., Anderson, S., Radeke, C. M., McGuire, L. M., Adams, M. E., Froehner, S. C., Yates, J. R., 3rd, and Vandenberg, C. A. (2004) Protein trafficking and anchoring complexes revealed by proteomic analysis of inward rectifier potassium channel (Kir2.x)-associated proteins. J. Biol. Chem. 279, 22331-22346 (Pubitemid 38679430)
7. Anumonwo, J. M., and Lopatin, A. N. (2010) Cardiac strong inward rectifier potassium channels. J. Mol. Cell Cardiol. 48, 45-54
8. Miake, J., Marbán, E., and Nuss, H. B. (2003) Functional role of inward rectifier current in heart probed by Kir2.1 overexpression and dominant-negative suppression. J. Clin. Invest. 111, 1529-1536 (Pubitemid 38063285)
9. Plaster, N. M., Tawil, R., Tristani-Firouzi, M., Canún, S., Bendahhou, S., Tsunoda, A., Donaldson, M. R., Iannaccone, S. T., Brunt, E., Barohn, R., Clark, J., Deymeer, F., George, A. L., Jr., Fish, F. A., Hahn, A., Nitu, A., Ozdemir, C., Serdaroglu, P., Subramony, S. H., Wolfe, G., Fu, Y. H., and Ptácek, L. J. (2001) Mutations in Kir2.1 cause the developmental and episodic electrical phenotypes of Andersen's syndrome. Cell 105, 511-519 (Pubitemid 32520856)
10. Tristani-Firouzi, M., Jensen, J. L., Donaldson, M. R., Sansone, V., Meola, G., Hahn, A., Bendahhou, S., Kwiecinski, H., Fidzianska, A., Plaster, N., Fu, Y. H., Ptacek, L. J., and Tawil, R. (2002) Functional and clinical characterization of KCNJ2 mutations associated with LQT7 (Andersen syndrome). J. Clin. Invest. 110, 381-388 (Pubitemid 34847970)
11. Leonoudakis, D., Conti, L. R., Radeke, C. M., McGuire, L. M., and Vandenberg, C. A. (2004) A multiprotein trafficking complex composed of SAP97, CASK, Veli, and Mint1 is associated with inward rectifier Kir2 potassium channels. J. Biol. Chem. 279, 19051-19063 (Pubitemid 38623336)
12. Leonoudakis, D., Mailliard, W., Wingerd, K., Clegg, D., and Vandenberg, C. (2001) Inward rectifier potassium channel Kir2.2 is associated with synapse-associated protein SAP97. J. Cell Sci. 114, 987-998 (Pubitemid 32266269)
13. Eckhardt, L. L., Farley, A. L., Rodriguez, E., Ruwaldt, K., Hammill, D., Tester, D. J., Ackerman, M. J., and Makielski, J. C. (2007) KCNJ2 mutations in arrhythmia patients referred for LQT testing. A mutation T305A with novel effect on rectification properties. Heart Rhythm 4, 323-329 (Pubitemid 46323455)
14. Deleted in proof
15. Pu, J. L., Ye, B., Kroboth, S. L., McNally, E. M., Makielski, J. C., and Shi, N. Q. (2008) Cardiac sulfonylurea receptor short form-based channels confer a glibenclamide-insensitive KATP activity. J. Mol. Cell Cardiol. 44, 188-200
16. 2+)-activated Cl-channel Ano1/TMEM16A. J. Biol. Chem. 286, 1381-1388
17. Hamill, O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391, 85-100 (Pubitemid 11012976)
18. Delisle, B. P., Anderson, C. L., Balijepalli, R. C., Anson, B. D., Kamp, T. J., and January, C. T. (2003) Thapsigargin selectively rescues the trafficking defective LQT2 channels G601S and F805C. J. Biol. Chem. 278, 35749-35754 (Pubitemid 37102351)
19. Galbiati, F., Volonte, D., Minetti, C., Chu, J. B., and Lisanti, M. P. (1999) Phenotypic behavior of caveolin-3 mutations that cause autosomal dominant limb girdle muscular dystrophy (LGMD-1C). Retention of LGMD-1C caveolin-3 mutants within the Golgi complex. J. Biol. Chem. 274, 25632-25641 (Pubitemid 129530737)
20. Romanenko, V. G., Rothblat, G. H., and Levitan, I. (2002) Modulation of endothelial inward-rectifier K+ current by optical isomers of cholesterol. Biophys. J. 83, 3211-3222 (Pubitemid 36041940)
21. Wang, Z., Yue, L., White, M., Pelletier, G., and Nattel, S. (1998) Differential distribution of inward rectifier potassium channel transcripts in human atrium versus ventricle. Circulation 98, 2422-2428 (Pubitemid 28549786)
22. Cheng, J., PhD, Valdivia, C. M., Vaiyanathan, R. P., Balejepalli, R. P., Ackerman, M., and Makielski, J. M. (2013) J. Mol. Cell. Cardiol., in press
23. Ueda, K., Valdivia, C., Medeiros-Domingo, A., Tester, D. J., Vatta, M., Farrugia, G., Ackerman, M. J., and Makielski, J. C. (2008) Syntrophin mutation associated with long QT syndrome through activation of the nNOS-SCN5A macromolecular complex. Proc. Natl. Acad. Sci. U.S.A. 105, 9355-9360
24. Cui, S., Ho, W. K., Kim, S. T., and Cho, H. (2010) Agonist-induced localization of Gq-coupled receptors and G protein-gated inwardly rectifying K+ (GIRK) channels to caveolae determines receptor specificity of phosphatidylinositol 4,5-bisphosphate signaling. J. Biol. Chem. 285, 41732-41739
25. Gómez, R., Caballero, R., Barana, A., Amorós, I., Calvo, E., López, J. A., Klein, H., Vaquero, M., Osuna, L., Atienza, F., Almendral, J., Pinto, A., Tamargo, J., and Delpón, E. (2009) Nitric oxide increases cardiac IK1 by nitrosylation of cysteine 76 of Kir2.1 channels. Circ. Res. 105, 383-392
26. Couchoux, H., Allard, B., Legrand, C., Jacquemond, V., and Berthier, C. (2007) Loss of caveolin-3 induced by the dystrophy-associated P104L mutation impairs L-type calcium channel function in mouse skeletal muscle cells. J. Physiol. 580, 745-754 (Pubitemid 46909031)
27. Petitprez, S., Zmoos, A. F., Ogrodnik, J., Balse, E., Raad, N., El-Haou, S., Albesa, M., Bittihn, P., Luther, S., Lehnart, S. E., Hatem, S. N., Coulombe, A., and Abriel, H. (2011) SAP97 and dystrophin macromolecular complexes determine two pools of cardiac sodium channels Nav1.5 in cardiomyocytes. Circ. Res. 108, 294-304
28. Vaidyanathan, R., Taffet, S. M., Vikstrom, K. L., and Anumonwo, J. M. (2010) Regulation of cardiac inward rectifier potassium current (I(K1)) by synapse-associated protein-97. J. Biol. Chem. 285, 28000-28009
29. Milstein, M. L., Musa, H., Balbuena, D. P., Anumonwo, J. M., Auerbach, D. S., Furspan, P. B., Hou, L., Hu, B., Schumacher, S. M., Vaidyanathan, R., Martens, J. R., and Jalife, J. (2012) Dynamic reciprocity of sodium and potassium channel expression in a macromolecular complex controls cardiac excitability and arrhythmia. Proc. Natl. Acad. Sci. U.S.A. 109, E2134-2143
30. Tomaselli, G. F., and Zipes, D. P. (2004) What causes sudden death in heart failure? Circ. Res. 95, 754-763 (Pubitemid 39390577)
31. Beuckelmann, D. J., Näbauer, M., and Erdmann, E. (1993) Alterations of K+ currents in isolated human ventricular myocytes from patients with terminal heart failure. Circ. Res. 73, 379-385 (Pubitemid 23212118)
32. Hare, J. M., Lofthouse, R. A., Juang, G. J., Colman, L., Ricker, K. M., Kim, B., Senzaki, H., Cao, S., Tunin, R. S., and Kass, D. A. (2000) Contribution of caveolin protein abundance to augmented nitric oxide signaling in conscious dogs with pacing-induced heart failure. Circ. Res. 86, 1085-1092 (Pubitemid 30367868) Development