Activation of the KATP channel by Mg-nucleotide interaction with SUR1

Journal of General Physiology

Volumn 136, Issue 4, 2010, Pages 389-405

  Proks, Peter ^a   De Wet, Heidi ^a   Ashcroft, Frances M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; DRUG RECEPTOR; INWARDLY RECTIFYING POTASSIUM CHANNEL; SULFONYLUREA RECEPTOR; UK ATP 1 POTASSIUM CHANNEL; UK-ATP-1 POTASSIUM CHANNEL;

ANIMAL; ARTICLE; CHANNEL GATING; GENETICS; HYDROLYSIS; KINETICS; METABOLISM; OOCYTE; PATCH CLAMP; RAT; XENOPUS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; HYDROLYSIS; ION CHANNEL GATING; KATP CHANNELS; KINETICS; OOCYTES; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RECEPTORS, DRUG; XENOPUS;

EID: 77957838073     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201010475     Document Type: Article

References (52)

1. Abraham, M.R., V.A. Selivanov, D.M. Hodgson, D. Pucar, L.V Zingman, B. Wieringa, P.P. Dzeja, A.E. Alekseev, and A. Terzic. 2002. Coupling of cell energetics with membrane metabolic sensing. Integrative signaling through creatine kinase phosphotransfer disrupted by M-CK gene knock-out. J. Biol. Chem. 277:24427-24434. doi: 10.1074/jbc.M201777200 (Pubitemid 34951966)
2. Aittoniemi, J., C. Fotinou, T.J. Craig, H. de Wet, P. Proks, and F.M. Ashcroft. 2009. Review. SUR1: a unique ATP-binding cassette protein that functions as an ion channel regulator. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364:257-267. doi:10.1098/rstb.2008.0142
3. Alekseev, A.E., P.A. Brady, and A. Terzic. 1998. Ligand-insensitive state of cardiac ATP-sensitive K+ channels. Basis for channel opening. J. Gen. Physiol. 111:381-394. doi:10.1085/jgp.111.2.381 (Pubitemid 28113083)
4. Antcliff, J.F., S. Haider, P. Proks, M.S.P. Sansom, and F.M. Ashcroft. 2005. Functional analysis of a structural model of the ATP-bind- ing site of the KATP channel Kir6.2 subunit. EMBOJ. 24:229-239. doi:10.1038/sj.emboj.7600487 (Pubitemid 40216128)
5. Ashcroft, F.M. 2007. The Walter B. Cannon Physiology in Perspective Lecture, 2007. ATP-sensitive K+ channels and disease: from molecule to malady. Am. J. Physiol. Endocrinol. Metab. 293:E880-E889. doi:10.1152/ajpendo.00348.2007 (Pubitemid 47535818)
6. ATP channels. Science. 282:1141-1144. doi:10.1126/science.282.5391.1141
7. ATP channel: separate roles of Kir6.2 and SUR1 subunit phosphorylation. EMBO J. 18:4722-4732. doi:10.1093/emboj/18.17.4722 (Pubitemid 29415526)
8. Bienengraeber, M., T.M. Olson, V.A. Selivanov, E.C. Kathmann, F. O'Cochlain, F. Gao, A.B. Karger, J.D. Ballew, D.M. Hodgson, L.V. Zingman, et al. 2004. ABCC9 mutations identified in human dilated cardiomyopathy disrupt catalytic KATP channel gating. Nat. Genet. 36:382-387.
9. Bokvist, K., C. Ammälä, F.M. Ashcroft, P.O. Berggren, O. Larsson, and P. Rorsman. 1991. Separate processes mediate nucleotideinduced inhibition and stimulation of the ATP-regulated K+- channels in mouse pancreatic β-cells. Proc Biol Sci. 243:139-144. doi:10.1098/rspb.1991.0022
10. Clement, J.P., IV, K. Kunjilwar, G. Gonzalez, M. Schwanstecher, U. Panten, L. Aguilar-Bryan, and J. Bryan. 1997. Association and stoichiometry of KATP channel subunits. Neuron. 18:827-838. doi:10.1016/S0896-6273(00)80321-9 (Pubitemid 27232792)
11. Dabrowski, M., S. Trapp, and F.M. Ashcroft. 2003. Pyridine nucleotide regulation of the KATP channel Kir6.2/SUR1 expressed in Xenopus oocytes. J. Physiol. 550:357-363. doi:10.1113/jphysiol.2003.041715 (Pubitemid 36889297)
12. Davies, N.W., N.B. Standen, and P.R. Stanfield. 1992. The effect of intracellular pH on ATP-dependent potassium channels of frog skeletal muscle. J. Physiol. 445:549-568.
13. de Wet, H., M.V. Mikhailov, C. Fotinou, M. Dreger, T.J. Craig, C. Vénien-Bryan, and F.M. Ashcroft. 2007. Studies of the ATPase activity of the ABC protein SUR1. FEBS J. 274:3532-3544. doi:10 .1111/j.1742-4658.2007. 05879.x
14. ATP requires distinct functional domains of the cytoplasmic C terminus of the pore-forming subunit. Proc. Natl. Acad. Sci. USA. 95:13953-13958. doi:10.1073/pnas.95.23.13953 (Pubitemid 28523079)
15. ATP channel. Biophys. J. 80:719-728. doi:10.1016/S0006-3495(01)76051-1
16. Fan, Z., and J.C. Makielski. 1997. Anionic phospholipids activate ATP-sensitive potassium channels. J. Biol. Chem. 272:5388-5395. doi:10.1074/jbc.272.9.5388 (Pubitemid 27102355)
17. + channels in an operational state. Pflugers Arch. 407:238-240. doi:10.1007/BF00580683
18. + channels in guinea pig ventricular myocytes. J. Membr. Biol. 136:289-302. (Pubitemid 24005389)
19. + channel in rat pancreatic β-cells. Am. J. Physiol. 257:C1119-C1127.
20. + currents expressed in Xenopus oocytes. J. Physiol. 498:87-98.
21. ATP channel activation by Mg-ADP and diazoxide. EMBO J. 16:1145-1152. doi:10.1093/ emboj/16.6.1145
22. ATP channel by interaction with its SUR1 subunit. Proc. Natl. Acad. Sci. USA. 95:7185-7190. doi:10.1073/pnas.95.12.7185 (Pubitemid 28278128)
23. Hopkins, W.F., S. Fatherazi, B. Peter-Riesch, B.E. Corkey, and D.L. Cook. 1992. Two sites for adenine-nucleotide regulation of ATP- sensitive potassium channels in mouse pancreatic β-cells and HIT cells. J. Membr. Biol. 129:287-295.
24. John, S.A., J.N. Weiss, and B. Ribalet. 2001. Regulation of cloned ATP-sensitive K channels by adenine nucleotides and sulfonylureas: interactions between SUR1 and positively charged domains on Kir6.2. J. Gen. Physiol. 118:391-405. doi:10.1085/jgp.118.4.391 (Pubitemid 32980002)
25. ATP channel inhibition by ATP. J. Gen. Physiol. 119:105-116. doi:10.1085/jgp.119.1.105 (Pubitemid 34074597)
26. Lin, Y.F., Y.N. Jan, and L.Y. Jan. 2000. Regulation of ATP-sensitive potassium channel function by protein kinase A-mediated phosphorylation in transfected HEK293 cells. EMBO J. 19:942-955. doi:10.1093/emboj/19.5.942
27. Magleby, K.L., and B.S. Pallotta. 1983. Burst kinetics of single calcium-activated potassium channels in cultured rat muscle. J. Physiol. 344:605-623.
28. 4 mediates closure of pancreatic beta-cell ATP-sensitive potassium channels by interaction with 1 of 4 identical sites. Diabetes. 49:1413-1418. doi:10.2337/diabetes.49.9.1413
29. Masia, R., J.C. Koster, S. Tumini, F. Chiarelli, C. Colombo, C.G. Nichols, and F. Barbetti. 2007. An ATP-binding mutation (G334D) in KCNJ11 is associated with a sulfonylurea-insensitive form of developmental delay, epilepsy, and neonatal diabetes. Diabetes. 56:328-336. doi:10.2337/db06-1275
30. Matsuo, M., K. Tanabe, N. Kioka, T. Amachi, and K. Ueda. 2000. Different binding properties and affinities for ATP and ADP among sulfonylurea receptor subtypes, SUR1, SUR2A, and SUR2B. J. Biol. Chem. 275:28757-28763. doi:10.1074/jbc.M004818200
31. ATP channel complex Kir6.2-SUR1. EMBO J. 24:4166-4175. doi:10.1038/sj.emboj.7600877 (Pubitemid 41752885)
32. ATP channels as metabolic sensors in acute metabolic changes. J. Mol. Cell. Cardiol. 38:917-925. doi:10.1016/j.yjmcc.2004.11.019 (Pubitemid 40725939)
33. Nichols, C.G., S.L. Shyng, A. Nestorowicz, B. Glaser, J.P. Clement IV, G. Gonzalez, L. Aguilar-Bryan, M.A. Permutt, and J. Bryan. 1996. Adenosine diphosphate as an intracellular regulator of insulin secretion. Science. 272:1785-1787. doi:10.1126/science.272.5269.1785
34. -ATP channels in pancreatic β-cells by trypsin. Pflugers Arch. 424:63-72. doi:10.1007/BF00375103
35. ATP channel gating and its regulation. Prog. Biophys. Mol. Biol. 99:7-19. doi:10.1016/j.pbiomolbio.2008.10.002
36. Proks, P., C.E. Capener, P. Jones, and F.M. Ashcroft. 2001. Mutations within the P-loop of Kir6.2 modulate the intraburst kinetics of the ATP-sensitive potassium channel. J. Gen. Physiol. 118:341-353. doi:10.1085/jgp.118.4.341 (Pubitemid 32979999)
37. Proks, P., C. Girard, S. Haider, A.L. Gloyn, A.T. Hattersley, M.S.P. Sansom, and F.M. Ashcroft. 2005a. A gating mutation at the internal mouth of the Kir6.2 pore is associated with DEND syndrome. EMBO Reep. 6:470-475. doi:10.1038/sj.embor.7400393 (Pubitemid 40767081)
38. Proks, P., C. Girard, and F.M. Ashcroft. 2005b. Functional effects of KCNJ11 mutations causing neonatal diabetes: enhanced activation by MgATP. Hum. Mol. Genet. 14:2717-2726. doi:10.1093/hmg/ddi305 (Pubitemid 41300644)
39. Proks, P., K. Shimomura, T.J. Craig, C.A. Girard, and F.M. Ashcroft. 2007. Mechanism of action of a sulphonylurea receptor SUR1 mutation (F132L) that causes DEND syndrome. Hum. Mol. Genet. 16:2011-2019. doi:10.1093/hmg/ddm149 (Pubitemid 47354884)
40. + channel revealed with oil-gate concentration jump method. Am. J. Physiol. 257:H1624-H1633.
41. ATP channel activity via cAMPdependent protein kinase in insulin-secreting cell lines. J. Gen. Physiol. 94:693-717. doi:10.1085/jgp.94.4.693
42. Rosado, J.A., and S.O. Sage. 2000. A role for the actin cytoskeleton in the initiation and maintenance of store-mediated calcium entry in human platelets. Trends Cardiovasc. Med. 10:327-332. doi:10.1016/S1050-1738(01)00073-1 (Pubitemid 32451679)
43. + channel in mouse beta-cells. Br. J. Pharmacol. 111:302-310.
44. ATP channels. Science. 282:1138-1141. doi:10.1126/science.282.5391.1138
45. ATP channel activity by diazoxide and MgADP. Distinct functions of the two nucleotide binding folds of the sulfonylurea receptor. J. Gen. Physiol. 110:643-654. doi:10.1085/jgp.110.6.643 (Pubitemid 27524605)
46. Silberberg, S.D., and K.L. Magleby. 1993. Preventing errors when estimating single channel properties from the analysis of current fluctuations. Biophys. J. 65:1570-1584. doi:10.1016/S0006-3495(93)81196-2
47. Tarasov, A.I., H.J. Welters, S. Senkel, G.U. Ryffel, A.T. Hattersley, N.G. Morgan, and F.M. Ashcroft. 2006. A Kir6.2 mutation causing neonatal diabetes impairs electrical activity and insulin secretion from INS-1 beta-cells. Diabetes. 55:3075-3082. doi:10.2337/db06-0637 (Pubitemid 44923645)
48. ATP channel gating and implications for channel inhibition by ATP. J. Gen. Physiol. 112:333-349.
49. + channels in the absence of the sulphonylurea receptor. Nature. 387:179-183. doi:10.1038/387179a0 (Pubitemid 27209432)
50. 2+-independent ATP binding of the sulfonylurea receptor SURI. J. Biol. Chem. 272:22983-22986. doi:10.1074/jbc.272.37.22983 (Pubitemid 27392419)
51. Xie, L.H., M. Takano, M. Kakei, M. Okamura, and A. Noma. 1999. Wortmannin, an inhibitor of phosphatidylinositol kinases, blocks the MgATP-dependent recovery of Kir6.2/ SUR2A channels. J. Physiol. 514:655-665. doi:10.1111/j.1469-7793.1999.655ad.x (Pubitemid 29060312)
52. Zingman, L.V., A.E. Alekseev, M. Bienengraeber, D. Hodgson, A.B. Karger, P.P. Dzeja, and A. Terzic. 2001. Signaling in channel/ enzyme multimers: ATPase transitions in SUR module gate ATP-sensitive K+ conductance. Neuron. 31:233-245. doi:10.1016/S0896-6273(01)00356-7 (Pubitemid 32762977)