Two neonatal diabetes mutations on transmembrane helix 15 of SUR1 increase affinity for ATP and ADP at nucleotide binding domain 2

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 17985-17995

  Ortiz, David ^a,b   Voyvodic, Peter ^b   Gossack, Lindsay ^b   Quast, Ulrich ^c   Bryan, Joseph ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b PACIFIC NORTHWEST RESEARCH INSTITUTE   (United States)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; FACINGS; INSULIN; METABOLISM;

ATP-BINDING CASSETTE; HYDROLYTIC CONDITIONS; MEMBRANE POTENTIALS; NUCLEOTIDE AFFINITY; NUCLEOTIDE-BINDING DOMAIN; PANCREATIC BETA CELLS; SULFONYLUREA RECEPTORS; TRANSMEMBRANE HELICES;

NUCLEOTIDES;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DIAZOXIDE; GLIBENCLAMIDE; MAGNESIUM ION; SULFONYLUREA RECEPTOR 1;

ALLOSTERISM; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CHANNEL GATING; CONCENTRATION RESPONSE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DIMERIZATION; HYDROLYSIS; NUCLEOTIDE BINDING DOMAIN 1; NUCLEOTIDE BINDING DOMAIN 2; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR BINDING;

EID: 84861538639     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.349019     Document Type: Article

References (54)

1. Aguilar-Bryan, L., and Bryan, J. (1999) Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocr. Rev. 20, 101-135 (Pubitemid 29339588)
2. Aguilar-Bryan, L., and Bryan, J. (2008) Neonatal diabetes mellitus. Endocr. Rev. 29, 265-291 (Pubitemid 351679699)
3. Babenko, A. P., Polak, M., Cavé, H., Busiah, K., Czernichow, P., Scharfmann, R., Bryan, J., Aguilar-Bryan, L., Vaxillaire, M., and Froguel, P. (2006) Activating mutations in the ABCC8 gene in neonatal diabetes mellitus. N. Engl. J. Med. 355, 456-466 (Pubitemid 44162273)
4. Rafiq, M., Flanagan, S. E., Patch, A. M., Shields, B. M., Ellard, S., and Hattersley, A. T. (2008) Effective treatment with oral sulfonylureas in patients with diabetes due to sulfonylurea receptor 1 (SUR1) mutations. Diabetes Care 31, 204-209 (Pubitemid 351213320)
5. Babenko, A. P., and Bryan, J. (2003) SUR domains that associate with and gate KATP pores define a novel gatekeeper. J. Biol. Chem. 278, 41577-41580 (Pubitemid 37310410)
6. Aller, S. G., Yu, J., Ward, A., Weng, Y., Chittaboina, S., Zhuo, R., Harrell, P. M., Trinh, Y. T., Zhang, Q., Urbatsch, I. L., and Chang, G. (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718-1722
7. Dawson, R. J., and Locher, K. P. (2006) Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185 (Pubitemid 44387602)
8. Kreimer, D. I., Chai, K. P., and Ferro-Luzzi Ames, G. (2000) Nonequivalence of the nucleotide-binding subunits of an ABC transporter, the histidine permease, and conformational changes in the membrane complex. Biochemistry 39, 14183-14195
9. Manciu, L., Chang, X. B., Buyse, F., Hou, Y. X., Gustot, A., Riordan, J. R., and Ruysschaert, J. M. (2003) Intermediate structural states involved in MRP1-mediated drug transport. Role of glutathione. J. Biol. Chem. 278, 3347-3356 (Pubitemid 36801249)
10. Mannering, D. E., Sharma, S., and Davidson, A. L. (2001) Demonstration of conformational changes associated with activation of the maltose transport complex. J. Biol. Chem. 276, 12362-12368
11. Sonveaux, N., Vigano, C., Shapiro, A. B., Ling, V., and Ruysschaert, J. M. (1999) Ligand-mediated tertiary structure changes of reconstituted P-glycoprotein. A tryptophan fluorescence quenching analysis. J. Biol. Chem. 274, 17649-17654
12. Higgins, C. F., and Linton, K. J. (2004) The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 11, 918-926 (Pubitemid 39315294)
13. Rees, D. C., Johnson, E., and Lewinson, O. (2009) ABC transporters: the power to change. Nat. Rev. Mol. Cell Biol. 10, 218-227
14. 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)
15. 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)
16. 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
17. 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
18. Matsuo, M., Tanabe, K., Kioka, N., Amachi, T., and Ueda, K. (2000) Different binding properties and affinities for ATP and ADP among sulfonylurea receptor subtypes, SUR1, SUR2A, and SUR2B. J. Biol. Chem. 275, 28757-28763
19. 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
20. 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 (Pubitemid 47052393)
21. Hambrock, A., Löffler-Walz, C., and Quast, U. (2002) Glibenclamide binding to sulphonylurea receptor subtypes. Dependence on adenine nucleotides. Br. J. Pharmacol. 136, 995-1004
22. Schwanstecher, M., Löser, S., Rietze, I., and Panten, U. (1991) Phosphate and thiophosphate group donating adenine and guanine nucleotides inhibit glibenclamide binding to membranes from pancreatic islets. Naunyn Schmiedebergs Arch Pharmacol. 343, 83-89
23. 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
24. 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)
25. 2+ and ATP dependence of KATP channel modulator binding to the recombinant sulphonylurea receptor, SUR2B. Br J. Pharmacol. 125, 577-583
26. Babenko, A. P. (2008) A novel ABCC8 (SUR1)-dependent mechanism of metabolism-excitation uncoupling. J. Biol. Chem. 283, 8778-8782
27. 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)
28. Chloupková, M., Pickert, A., Lee, J. Y., Souza, S., Trinh, Y. T., Connelly, S. M., Dumont, M. E., Dean, M., and Urbatsch, I. L. (2007) Expression of 25 human ABC transporters in the yeast Pichia pastoris and characterization of the purified ABCC3 ATPase activity. Biochemistry 46, 7992-8003 (Pubitemid 47051635)
29. Doyle, S. A. (2005) High-throughput cloning for proteomics research. Methods Mol. Biol. 310, 107-113
30. Lerner-Marmarosh, N., Gimi, K., Urbatsch, I. L., Gros, P., and Senior, A. E. (1999) Large scale purification of detergent-soluble P-glycoprotein from Pichia pastoris cells and characterization of nucleotide binding properties of wild-type, Walker A, and Walker B mutant proteins. J. Biol. Chem. 274, 34711-34718 (Pubitemid 129509511)
31. Urbatsch, I. L., Beaudet, L., Carrier, I., and Gros, P. (1998) Mutations in either nucleotide-binding site of P-glycoprotein (Mdr3) prevent vanadate trapping of nucleotide at both sites. Biochemistry 37, 4592-4602 (Pubitemid 28217177)
32. Schwanstecher, M., Löser, S., Chudziak, F., Bachmann, C., and Panten, U. (1994) Photoaffinity labeling of the cerebral sulfonylurea receptor using a novel radioiodinated azidoglibenclamide analogue. J. Neurochem. 63, 698-708 (Pubitemid 24233708)
33. Wang, Z., Stalcup, L. D., Harvey, B. J., Weber, J., Chloupkova, M., Dumont, M. E., Dean, M., and Urbatsch, I. L. (2006) Purification and ATP hydrolysis of the putative cholesterol transporters ABCG5 and ABCG8. Biochemistry 45, 9929-9939 (Pubitemid 44257438)
34. Löffler-Walz, C., and Quast, U. (1998) Binding of KATP channel modulators in rat cardiac membranes. Br J. Pharmacol. 123, 1395-1402 (Pubitemid 28143140)
35. Dawson, R. J., and Locher, K. P. (2007) Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMPPNP. FEBS Lett. 581, 935-938 (Pubitemid 46282725)
36. 2+-independent ATP binding of the sulfonylurea receptor SUR1. J. Biol. Chem. 272, 22983-22986
37. Bryan, J., Vila-Carriles, W. H., Zhao, G., Babenko, A. P., and Aguilar-Bryan, L. (2004) Toward linking structure with function in ATP-sensitive K+ channels. Diabetes 53, Suppl. 3, S104-S112 (Pubitemid 39564531)
38. Bryan, J., Crane, A., Vila-Carriles, W. H., Babenko, A. P., and Aguilar-Bryan, L. (2005) Insulin secretagogues, sulfonylurea receptors and KATP channels. Curr. Pharm. Des. 11, 2699-2716 (Pubitemid 41051879)
39. Ashfield, R., Gribble, F. M., Ashcroft, S. J., and Ashcroft, F. M. (1999) Identification of the high-affinity tolbutamide site on the SUR1 subunit of the KATP channel. Diabetes 48, 1341-1347 (Pubitemid 29241036)
40. Babenko, A. P., Gonzalez, G., and Bryan, J. (1999) The tolbutamide site of SUR1 and a mechanism for its functional coupling to KATP channel closure. FEBS Lett. 459, 367-376 (Pubitemid 29467370)
41. Hambrock, A., Kayar, T., Stumpp, D., and Osswald, H. (2004) Effect of two amino acids in TM17 of Sulfonylurea receptor SUR1 on the binding of ATP-sensitive K+ channel modulators. Diabetes 53, Suppl. 3, S128-S134 (Pubitemid 39564534)
42. Schwanstecher, M., Brandt, C., Behrends, S., Schaupp, U., and Panten, U. (1992) Effect of MgATP on pinacidil-induced displacement of glibenclamide from the sulphonylurea receptor in a pancreatic beta-cell line and rat cerebral cortex. Br. J. Pharmacol. 106, 295-301
43. Babenko, A. P., Gonzalez, G., and Bryan, J. (2000) Pharmaco-topology of sulfonylurea receptors. Separate domains of the regulatory subunits of KATP channel isoforms are required for selective interaction with K+ channel openers. J. Biol. Chem. 275, 717-720 (Pubitemid 30051106)
44. Moreau, C., Jacquet, H., Prost, A. L., D'hahan, N., and Vivaudou, M. (2000) The molecular basis of the specificity of action of KATP channel openers. EMBO J. 19, 6644-6651 (Pubitemid 32011657)
45. Alberty, R. A. (2003) Thermodynamics of Biochemical Reactions, pp. 5-11, John Wiley & Sons, Inc., Hoboken, NJ
46. Shyng, S., Ferrigni, T., and Nichols, C. G. (1997) Regulation of KATP channel activity by diazoxide and MgADP. Distinct functions of the two nucleotide binding folds of the sulfonylurea receptor. J. Gen. Physiol. 110, 643-654 (Pubitemid 27524605)
47. Kim, I. W., Peng, X. H., Sauna, Z. E., FitzGerald, P. C., Xia, D., Müller, M., Nandigama, K., and Ambudkar, S. V. (2006) The conserved tyrosine residues 401 and 1044 in ATP sites of human P-glycoprotein are critical for ATP binding and hydrolysis. Evidence for a conserved subdomain, the A-loop in the ATP-binding cassette. Biochemistry 45, 7605-7616 (Pubitemid 43894952)
48. Ambudkar, S. V., Kim, I. W., Xia, D., and Sauna, Z. E. (2006) The A-loop, a novel conserved aromatic acid subdomain upstream of the Walker A motif in ABC transporters, is critical for ATP binding. FEBS Lett. 580, 1049-1055 (Pubitemid 43185285)
49. + channels that are inhibited by ATP in an insulin-secreting cell line. FEBS Lett. 208, 59-62
50. + channel in rat ventricular myocytes. J. Membr. Biol. 101, 83-92
51. + channels in rat pancreatic B-cells is modulated by ADP. FEBS Lett. 208, 63-66
52. + channels in isolated membrane patches. J. Physiol. 419, 193-211
53. Misler, S., Falke, L. C., Gillis, K., and McDaniel, M. L. (1986) A metabolite-regulated potassium channel in rat pancreatic B cells. Proc. Natl. Acad. Sci. U.S.A. 83, 7119-7123 (Pubitemid 16002380)
54. Rosano, T. G., Clayson, K. J., and Strandjord, P. E. (1976) Evaluation of adenosine 5′-monophosphate and fluoride as adenylate kinase inhibitors in the creatine kinase assay. Clin. Chem. 22, 1078-1083