Reinterpreting the action of ATP analogs on KATP channels

Journal of Biological Chemistry

Volumn 288, Issue 26, 2013, Pages 18894-18902

  Ortiz, David ^a   Gossack, Lindsay ^a   Quasts, Ulrich ^b   Bryan, Joseph ^a  

^a PACIFIC NORTHWEST RESEARCH INSTITUTE   (United States)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATP-ASE ACTIVITY; CELLULAR METABOLISM; CHANNEL ACTIVITY; CONFORMATIONAL SWITCHING; ENZYMATIC ACTIVITIES; MEMBRANE POTENTIALS; NUCLEOTIDE BINDING; TRANSMEMBRANE FLUX;

HYDROLYSIS;

SWITCHING;

ADENOSINE TRIPHOSPHATE; ADENYLATE CYCLASE; ADENYLYLIMIDODIPHOSPHATE; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; POTASSIUM CHANNEL; SULFONYLUREA RECEPTOR 1;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL METABOLISM; CONFORMATIONAL TRANSITION; DIMERIZATION; DISSOCIATION CONSTANT; ENZYME ACTIVITY; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; STEADY STATE;

ABC TRANSPORTER; ABCC8; ALLOSTERIC REGULATION; ATP ANALOGS; KATP CHANNELS; LIGAND-BINDING PROTEIN; NEONATAL DIABETES; NUCLEOSIDE NUCLEOTIDE ANALOGS; POTASSIUM CHANNELS; SULFONYLUREAS;

ADENOSINE TRIPHOSPHATE; ADENYLYL IMIDODIPHOSPHATE; ALLOSTERIC SITE; ATP-BINDING CASSETTE TRANSPORTERS; DIABETES MELLITUS; DIMERIZATION; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; HYDROLYSIS; INHIBITORY CONCENTRATION 50; MUTATION; PICHIA; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, DRUG; SULFONYLUREA COMPOUNDS;

BACTERIA (MICROORGANISMS);

EID: 84879577910     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.476887     Document Type: Article

References (62)

1. Aguilar-Bryan, L., and Bryan, J. (1999) Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocr. Rev. 20, 101-135 (Pubitemid 29339588)
2. Pratt, E. B., and Shyng, S. L. (2011) ATP activates ATP-sensitive potassium channels composed of mutant sulfonylurea receptor 1 and Kir6.2 with diminished PIP2 sensitivity. Channels (Austin) 5, 314-319
3. Pratt, E. B., Tewson, P., Bruederle, C. E., Skach, W. R., and Shyng, S. L. (2011) N-terminal transmembrane domain of SUR1 controls gating of Kir6.2 by modulating channel sensitivity to PIP2. J. Gen. Physiol. 137, 299-314
4. Shyng, S. L., Barbieri, A., Gumusboga, A., Cukras, C., Pike, L., Davis, J. N., Stahl, P. D., and Nichols, C. G. (2000) Modulation of nucleotide sensitivity of ATP-sensitive potassium channels by phosphatidylinositol-4- phosphate 5-kinase. Proc. Natl. Acad. Sci. U.S.A. 97, 937-941 (Pubitemid 30070413)
5. Shyng, S. L., and Nichols, C. G. (1998) Membrane phospholipid control of nucleotide sensitivity of KATP channels. Science 282, 1138-1141
6. Baukrowitz, T., and Fakler, B. (2000) KATP channels gated by intracellular nucleotides and phospholipids. Eur. J. Biochem. 267, 5842-5848
7. Baukrowitz, T., Schulte, U., Oliver, D., Herlitze, S., Krauter, T., Tucker, S. J., Ruppersberg, J. P., and Fakler, B. (1998) PIP2 and PIP as determinants for ATP inhibition of KATP channels. Science 282, 1141-1144 (Pubitemid 28516246)
8. Enkvetchakul, D., Loussouarn, G., Makhina, E., Shyng, S. L., and Nichols, C. G. (2000) The kinetic and physical basis of KATP channel gating: toward a unified molecular understanding. Biophys. J. 78, 2334-2348 (Pubitemid 30313793)
9. + channel. A molecular probe for the mechanism of ATP-sensitive inhibition. J. Gen. Physiol. 114, 251-269
10. Bränström, R., Corkey, B. E., Berggren, P. O., and Larsson, O. (1997) Evidence for a unique long chain acyl-CoA ester binding site on the ATP-regulated potassium channel in mouse pancreatic beta cells. J. Biol. Chem. 272, 17390-17394
11. Bränström, R., Leibiger, I. B., Leibiger, B., Corkey, B. E., Berggren, P. O., and Larsson, O. (1998) Long chain coenzyme A esters activate the pore-forming subunit (Kir6. 2) of the ATP-regulated potassium channel. J. Biol. Chem. 273, 31395-31400
12. Gribble, F. M., Proks, P., Corkey, B. E., and Ashcroft, F. M. (1998) Mechanism of cloned ATP-sensitive potassium channel activation by oleoyl-CoA. J. Biol. Chem. 273, 26383-26387 (Pubitemid 28471642)
13. Bränström, R., Aspinwall, C. A., Välimäki, S., Ostensson, C. G., Tibell, A., Eckhard, M., Brandhorst, H., Corkey, B. E., Berggren, P. O., and Larsson, O. (2004) Long-chain CoA esters activate human pancreatic beta-cell KATP channels: potential role in Type 2 diabetes. Diabetologia 47, 277-283
14. Schulze, D., Rapedius, M., Krauter, T., and Baukrowitz, T. (2003) Long-chain acyl-CoA esters and phosphatidylinositol phosphates modulate ATP inhibition of KATP channels by the same mechanism. J. Physiol. 552, 357-367 (Pubitemid 37321835)
15. Riedel, M. J., Boora, P., Steckley, D., de Vries, G., and Light, P. E. (2003) Kir6.2 polymorphisms sensitize beta-cell ATP-sensitive potassium channels to activation by acyl CoAs: a possible cellular mechanism for increased susceptibility to type 2 diabetes? Diabetes 52, 2630-2635 (Pubitemid 37210554)
16. Best, L., Jarman, E., and Brown, P. D. (2011)Adual action of saturated fatty acids on electrical activity in rat pancreatic beta-cells. Role of volume-regulated anion channel and KATP channel currents. J. Physiol. 589, 1307-1316
17. de Wet, H., Mikhailov, M. V., Fotinou, C., Dreger, M., Craig, T. J., Vénien-Bryan, C., and Ashcroft, F. M. (2007) Studies of the ATPase activity of the ABC protein SUR1. FEBS J. 274, 3532-3544
18. Mikhailov, M. V., Campbell, J. D., de Wet, H., Shimomura, K., Zadek, B., Collins, R. F., Sansom, M. S., Ford, R. C., and Ashcroft, F. M. (2005) 3-D structural and functional characterization of the purified KATP channel complex Kir6.2-SUR1. EMBO J. 24, 4166-4175 (Pubitemid 41752885)
19. Zingman, L. V., Alekseev, A. E., Bienengraeber, M., Hodgson, D., Karger, A. B., Dzeja, P. P., and Terzic, A. (2001) Signaling in channel/enzyme multimers: ATPase transitions in SUR module gate ATP-sensitive K+conductance. Neuron 31, 233-245 (Pubitemid 32762977)
20. Aittoniemi, J., Fotinou, C., Craig, T. J., de Wet, H., Proks, P., and Ashcroft, F. M. (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
21. + channel channel/enzyme multimer: metabolic gating in the heart. J. Mol. Cell. Cardiol. 38, 895-905
22. Matsuo, M., Kimura, Y., and Ueda, K. (2005) KATP channel interaction with adenine nucleotides. J. Mol. Cell. Cardiol. 38, 907-916 (Pubitemid 40725938)
23. + channels in rat ventricular myocytes are blocked and inactivated by internal divalent cations. Pflugers Arch. 410, 313-320
24. + channel in rat ventricular myocytes. J. Membr. Biol. 101, 83-92
25. Dunne, M. J. (1989) Protein phosphorylation is required for diazoxide to open ATP-sensitive potassium channels in insulin (RINm5F) secreting cells. FEBS Lett. 250, 262-266
26. Dunne, M. J., Aspinall, R. J., and Petersen, O. H. (1990) The effects of cromakalim on ATP-sensitive potassium channels in insulin-secreting cells. Br. J. Pharmacol. 99, 169-175 (Pubitemid 20033804)
27. 2+ ions. J. Physiol. 416, 349-367
28. + channels in guinea pig cardiac myocytes. Am. J. Physiol. 258, H45-50
29. + channels in rat ventromedial hypothalamic neurons. Proc. Biol. Sci. 247, 121-124
30. Schwanstecher, M., Sieverding, C., Dörschner, H., Gross, I., Aguilar-Bryan, L., Schwanstecher, C., and Bryan, J. (1998) Potassium channel openers require ATP to bind to and act through sulfonylurea receptors. EMBO J. 17, 5529-5535 (Pubitemid 28445964)
31. Ortiz, D., Voyvodic, P., Gossack, L., Quast, U., and Bryan, J. (2012) Two Neonatal diabetes mutations on transmembrane helix 15 of SUR1 increase affinity for ATP and ADP at nucleotide binding domain 2. J. Biol. Chem. 287, 17985-17995
32. Higgins, C. F., and Linton, K. J. (2004) The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 11, 918-926 (Pubitemid 39315294)
33. Rees, D. C., Johnson, E., and Lewinson, O. (2009) ABC transporters: the power to change. Nat. Rev. Mol. Cell. Biol. 10, 218-227
34. Dawson, R. J., and Locher, K. P. (2007) Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett. 581, 935-938 (Pubitemid 46282725)
35. Oldham, M. L., and Chen, J. (2011) Snapshots of the maltose transporter during ATP hydrolysis. Proc. Natl. Acad. Sci. U.S.A. 108, 15152-15156
36. Hohl, M., Briand, C., Grütter, M. G., and Seeger, M. A. (2012) Crystal structure of a heterodimeric ABC transporter in its inward-facing conformation. Nat. Struct. Mol. Biol. 19, 395-402
37. Lubelski, J., van Merkerk, R., Konings, W. N., and Driessen, A. J. (2006) Nucleotide-binding sites of the heterodimeric LmrCD ABC-multidrug transporter of Lactococcus lactis are asymmetric. Biochemistry 45, 648-656 (Pubitemid 43100429)
38. Procko, E., Ferrin-O'Connell, I., Ng, S. L., and Gaudet, R. (2006) Distinct structural and functional properties of the ATPase sites in an asymmetric ABC transporter. Mol. Cell. 24, 51-62 (Pubitemid 44466678)
39. Qin, L., Zheng, J., Grant, C. E., Jia, Z., Cole, S. P., and Deeley, R. G. (2008) Residues responsible for the asymmetric function of the nucleotide binding domains of multidrug resistance protein 1. Biochemistry 47, 13952-13965
40. Procko, E., O'Mara, M. L., Bennett, W. F., Tieleman, D. P., and Gaudet, R. (2009) The mechanism of ABC transporters: general lessons from structural and functional studies of an antigenic peptide transporter. FASEB J. 23, 1287-1302
41. Christesen, H. B. T., Sjöblad, S., Brusgaard, K., Papadopoulou, D., and Jacobsen, B. B. (2005) Permanent neonatal diabetes in a child with an ABCC8 gene mutation. Hormone Res. 64, Suppl. 1, 135
42. Babenko, A. P. (2008) A novel ABCC8 (SUR1)-dependent mechanism of metabolism-excitation uncoupling. J. Biol. Chem. 283, 8778-8782
43. Tombline, G., Bartholomew, L. A., Tyndall, G. A., Gimi, K., Urbatsch, I. L., and Senior, A. E. (2004) Properties of P-glycoprotein with mutations in the "catalytic carboxylate" glutamate residues. J. Biol. Chem. 279, 46518-46526 (Pubitemid 39518295)
44. Orelle, C., Dalmas, O., Gros, P., Di Pietro, A., and Jault, J. M. (2003) The conserved glutamate residue adjacent to the Walker-B motif is the catalytic base for ATP hydrolysis in the ATP-binding cassette transporter BmrA. J. Biol. Chem. 278, 47002-47008 (Pubitemid 37452283)
45. Oldham, M. L., Khare, D., Quiocho, F. A., Davidson, A. L., and Chen, J. (2007) Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450, 515-521 (Pubitemid 350190241)
46. Smith, P. C., Karpowich, N., Millen, L., Moody, J. E., Rosen, J., Thomas, P. J., and Hunt, J. F. (2002) ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell 10, 139-149 (Pubitemid 34876568)
47. Moody, J. E., Millen, L., Binns, D., Hunt, J. F., and Thomas, P. J. (2002) Cooperative, ATP-dependent association of the nucleotide binding cassettes during the catalytic cycle of ATP-binding cassette transporters. J. Biol. Chem. 277, 21111-21114 (Pubitemid 34952244)
48. Aleksandrov, L., Aleksandrov, A. A., Chang, X. B., and Riordan, J. R. (2002) The first nucleotide binding domain of cystic fibrosis transmembrane conductance regulator is a site of stable nucleotide interaction, whereas the second is a site of rapid turnover. J. Biol. Chem. 277, 15419-15425 (Pubitemid 34967805)
49. Aleksandrov, L., Mengos, A., Chang, X., Aleksandrov, A., and Riordan, J. R. (2001) Differential interactions of nucleotides at the two nucleotide binding domains of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 276, 12918-12923
50. Löffler-Walz, C., and Quast, U. (1998) Binding of KATP channel modulators in rat cardiac membranes. Br. J. Pharmacol. 123, 1395-1402
51. Wyman, J., and Gill, S.J.(1990) Binding and Linkage: Functional Chemistry of Biological Macromolecules, University Science Books, Mill Valley, CA
52. Männikkö, R., Flanagan, S. E., Sim, X., Segal, D., Hussain, K., Ellard, S., Hattersley, A. T., and Ashcroft, F. M. (2011) Mutations of the same conserved glutamate residue in NBD2 of the sulfonylurea receptor 1 subunit of the KATP channel can result in either hyperinsulinism or neonatal diabetes. Diabetes 60, 1813-1822
53. Yount, R. G. (1975) ATP analogs. Adv. Enzymol. Relat. Areas Mol. Biol. 43, 1-56
54. Hehl, S., and Neumcke, B. (1994) KATP channels of mouse skeletal muscle: mechanism of channel blockage by AMP-PNP. Eur. Biophys. J. 23, 231-237
55. + channels in isolated membrane patches. J. Physiol. 419, 193-211
56. + channel in mouse beta-cells. Br. J. Pharmacol. 111, 302-310
57. Proks, P., de Wet, H., and Ashcroft, F. M. (2010) Activation of the KATP channel by Mg-nucleotide interaction with SUR1. J. Gen. Physiol. 136, 389-405
58. Schwanstecher, M., Löser, S., Brandt, C., Scheffer, K., Rosenberger, F., and Panten, U. (1992) Adenine nucleotide-induced inhibition of binding of sulphonylureas to their receptor in pancreatic islets. Br. J. Pharmacol. 105, 531-534
59. Matsuo, M., Kioka, N., Amachi, T., and Ueda, K. (1999) ATP binding properties of the nucleotide-binding folds of SUR1. J. Biol. Chem. 274, 37479-37482
60. 2+- independent ATP binding of the sulfonylurea receptor SUR1. J. Biol. Chem. 272, 22983-22986
61. Cheng, Y., and Prusoff, W. H. (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099-3108
62. Hung, L. W., Wang, I. X., Nikaido, K., Liu, P. Q., Ames, G. F., and Kim, S. H. (1998) Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396, 703-707