Syntaxin-1A inhibits K ATP channels by interacting with specific conserved motifs within sulfonylurea receptor 2A

Journal of Molecular and Cellular Cardiology

Volumn 51, Issue 5, 2011, Pages 790-802

  Chao, Christin ^a   Liang, Tao ^a   Kang, Youhou ^a   Lin, Xianguang ^a   Xie, Huanli ^a   Feng, Zhong Ping ^a   Gaisano, Herbert Y ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

ATP sensitive potassium channel; Kir6.2; SNARE; SUR2A; Syntaxin 1A

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; HETERODIMER; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; SULFONYLUREA RECEPTOR; SULFONYLUREA RECEPTOR 2A; SYNTAXIN 1A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRAIN HEK293; CHANNEL GATING; CONTROLLED STUDY; DIMERIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNOPRECIPITATION; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE BINDING FOLD; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ADENOSINE TRIPHOSPHATE; AMINO ACID MOTIFS; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BINDING SITES; CELL MEMBRANE; CONSERVED SEQUENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HUMANS; KATP CHANNELS; MALE; MICE; MICROSCOPY, FLUORESCENCE; MYOCYTES, CARDIAC; OLIGOPEPTIDES; PATCH-CLAMP TECHNIQUES; PLASMIDS; POTASSIUM; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, DRUG; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SYNTAXIN 1;

RATTUS;

EID: 80053277935     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.08.011     Document Type: Article

References (41)

1. Nichols C.G. KATP channels as molecular sensors of cellular metabolism. Nature 2006, 440:470-476.
2. Flagg T.P., Nichols C.G. Sarcolemmal K(ATP) channels: what do we really know?. J Mol Cell Cardiol 2005, 39:61-70.
3. Moreau C., Prost A.L., Derand R., Vivaudou M. SUR, ABC proteins targeted by KATP channel openers. J Mol Cell Cardiol 2005, 38:951-963.
4. Higgins C.F., Linton K.J. The ATP switch model for ABC transporters. Nat Struct Mol Biol 2004, 11:918-926.
5. Park S., Lim B.B., Perez-Terzic C., Mer G., Terzic A. Interaction of asymmetric ABCC9-encoded nucleotide binding domains determines KATP channel SUR2A catalytic activity. J Proteome Res 2008, 7:1721-1728.
6. Campbell J.D., Sansom M.S., Ashcroft F.M. Potassium channel regulation. EMBO Rep 2003, 4:1038-1042.
7. Matsuo M., Dabrowski M., Ueda K., Ashcroft F.M. Mutations in the linker domain of NBD2 of SUR inhibit transduction but not nucleotide binding. EMBO J 2002, 21:4250-4258.
8. Zingman L.V., Alekseev A.E., Bienengraeber M., Hodgson D., Karger A.B., Dzeja P.P., et al. Signaling in channel/enzyme multimers: ATPase transitions in SUR module gate ATP-sensitive K+ conductance. Neuron 2001, 31:233-245.
9. Zingman L.V., Hodgson D.M., Bienengraeber M., Karger A.B., Kathmann E.C., Alekseev A.E., et al. Tandem function of nucleotide binding domains confers competence to sulfonylurea receptor in gating ATP-sensitive K+ channels. J Biol Chem 2002, 277:14206-14210.
10. Light P.E., Bladen C., Winkfein R.J., Walsh M.P., French R.J. Molecular basis of protein kinase C-induced activation of ATP-sensitive potassium channels. Proc Natl Acad Sci U S A 2000, 97:9058-9063.
11. Liu G.X., Hanley P.J., Ray J., Daut J. Long-chain acyl-coenzyme A esters and fatty acids directly link metabolism to K(ATP) channels in the heart. Circ Res 2001, 88:918-924.
12. Ribalet B., John S.A., Xie L.H., Weiss J.N. Regulation of the ATP-sensitive K channel Kir6.2 by ATP and PIP(2). J Mol Cell Cardiol 2005, 39:71-77.
13. Jovanovic S., Jovanovic A. High glucose regulates the activity of cardiac sarcolemmal ATP-sensitive K+ channels via 1,3-bisphosphoglycerate: a novel link between cardiac membrane excitability and glucose metabolism. Diabetes 2005, 54:383-393.
14. Han J., So I., Kim E.Y., Earm Y.E. ATP-sensitive potassium channels are modulated by intracellular lactate in rabbit ventricular myocytes. Pflugers Arch 1993, 425:546-548.
15. Carrasco A.J., Dzeja P.P., Alekseev A.E., Pucar D., Zingman L.V., Abraham M.R., et al. Adenylate kinase phosphotransfer communicates cellular energetic signals to ATP-sensitive potassium channels. Proc Natl Acad Sci U S A 2001, 98:7623-7628.
16. Crawford R.M., Ranki H.J., Botting C.H., Budas G.R., Jovanovic A. Creatine kinase is physically associated with the cardiac ATP-sensitive K+ channel in vivo. FASEB J 2002, 16:102-104.
17. Zlatkovic J., Arrell D.K., Kane G.C., Miki T., Seino S., Terzic A. Proteomic profiling of KATP channel-deficient hypertensive heart maps risk for maladaptive cardiomyopathic outcome. Proteomics 2009, 9:1314-1325.
18. Jovanovic S., Du Q., Crawford R.M., Budas G.R., Stagljar I., Jovanovic A. Glyceraldehyde 3-phosphate dehydrogenase serves as an accessory protein of the cardiac sarcolemmal K(ATP) channel. EMBO Rep 2005, 6:848-852.
19. Jovanovic S., Du Q., Sukhodub A., Jovanovic A. M-LDH physically associated with sarcolemmal K ATP channels mediates cytoprotection in heart embryonic H9C2 cells. Int J Biochem Cell Biol 2009, 41:2295-2301.
20. Kang Y., Leung Y.M., Manning-Fox J.E., Xia F., Xie H., Sheu L., et al. Syntaxin-1A inhibits cardiac KATP channels by its actions on nucleotide binding folds 1 and 2 of sulfonylurea receptor 2A. J Biol Chem 2004, 279:47125-47131.
21. Kang Y., Ng B., Leung Y.M., He Y., Xie H., Lodwick D., et al. Syntaxin-1A actions on sulfonylurea receptor 2A can block acidic pH-induced cardiac K(ATP) channel activation. J Biol Chem 2006, 281:19019-19028.
22. Ng B., Kang Y., Xie H., Sun H., Gaisano H.Y. Syntaxin-1A inhibition of P-1075, cromakalim, and diazoxide actions on mouse cardiac ATP-sensitive potassium channel. Cardiovasc Res 2008, 80:365-374.
23. Giblin J.P., Cui Y., Clapp L.H., Tinker A. Assembly limits the pharmacological complexity of ATP-sensitive potassium channels. J Biol Chem 2002, 277:13717-13723.
24. Kang Y., Zhang Y., Liang T., Leung Y.M., Ng B., Xie H., et al. ATP modulates interaction of syntaxin-1A with sulfonylurea receptor 1 to regulate pancreatic {beta}-cell KATP channels. J Biol Chem 2011, 286:5876-5883.
25. Pasyk E.A., Kang Y., Huang X., Cui N., Sheu L., Gaisano H.Y. Syntaxin-1A binds the nucleotide-binding folds of sulphonylurea receptor 1 to regulate the KATP channel. J Biol Chem 2004, 279:4234-4240.
26. Chao C.C., Mihic A., Tsushima R.G., Gaisano H.Y. SNARE protein regulation of cardiac potassium channels and atrial natriuretic factor secretion. J Mol Cell Cardiol 2011, 50:401-407.
27. Biemans-Oldehinkel E., Doeven M.K., Poolman B. ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett 2006, 580:1023-1035.
28. Moody J.E., Millen L., Binns D., Hunt J.F., Thomas P.J. Cooperative, ATP-dependent association of the nucleotide binding cassettes during the catalytic cycle of ATP-binding cassette transporters. J Biol Chem 2002, 277:21111-21114.
29. Vergani P., Lockless S.W., Nairn A.C., Gadsby D.C. CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains. Nature 2005, 433:876-880.
30. Hiraoka M., Furukawa T. Functional modulation of cardiac ATP-sensitive K(+) channels. News Physiol Sci 1998, 13:131-137.
31. Nichols C.G., Lederer W.J. Adenosine triphosphate-sensitive potassium channels in the cardiovascular system. Am J Physiol 1991, 261:H1675-H1686.
32. Budas G.R., Jovanovic S., Crawford R.M., Jovanovic A. Hypoxia-induced preconditioning in adult stimulated cardiomyocytes is mediated by the opening and trafficking of sarcolemmal KATP channels. FASEB J 2004, 18:1046-1048.
33. Gumina R.J., Pucar D., Bast P., Hodgson D.M., Kurtz C.E., Dzeja P.P., et al. Knockout of Kir6.2 negates ischemic preconditioning-induced protection of myocardial energetics. Am J Physiol Heart Circ Physiol 2003, 284:H2106-H2113.
34. Zhang H., Flagg T.P., Nichols C.G. Cardiac sarcolemmal KATP channels: latest twists in a questing tale!. J Mol Cell Cardiol 2009, 48(1):71-75.
35. Zingman L.V., Alekseev A.E., Hodgson-Zingman D.M., Terzic A. ATP-sensitive potassium channels: metabolic sensing and cardioprotection. J Appl Physiol 2007, 103:1888-1893.
36. Billman G.E. The cardiac sarcolemmal ATP-sensitive potassium channel as a novel target for anti-arrhythmic therapy. Pharmacol Ther 2008, 120:54-70.
37. Chao C.C., Mihic A., Tsushima R.G., Gaisano H.Y. SNARE protein regulation of cardiac potassium channels and atrial natriuretic factor secretion. J Mol Cell Cardiol 2010, 50:401-407.
38. Wang C., Castro A.F., Wilkes D.M., Altenberg G.A. Expression and purification of the first nucleotide-binding domain and linker region of human multidrug resistance gene product: comparison of fusions to glutathione S-transferase, thioredoxin and maltose-binding protein. Biochem J 1999, 338(Pt 1):77-81.
39. Couet J., Li S., Okamoto T., Ikezu T., Lisanti M.P. Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 1997, 272:6525-6533.
40. Li S., Okamoto T., Chun M., Sargiacomo M., Casanova J.E., Hansen S.H., et al. Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J Biol Chem 1995, 270:15693-15701.
41. Frangioni J.V., Neel B.G. Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal Biochem 1993, 210:179-187.