Engineered interaction between SUR1 and Kir6.2 that enhances ATP sensitivity in KATP channels

Journal of General Physiology

Volumn 140, Issue 2, 2012, Pages 175-187

  Pratt, Emily B ^a   Zhou, Qing ^a   Gay, Joel W ^a   Shyng, Show Ling ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; DRUG RECEPTOR; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; POTASSIUM; SULFONYLUREA RECEPTOR;

AMINO ACID SUBSTITUTION; ANIMAL; ARTICLE; CELL STRAIN COS1; CERCOPITHECUS; CHANNEL GATING; CRICETULUS; GENETICS; HAMSTER; METABOLISM; PROTEIN DOMAIN; RAT; STRUCTURE ACTIVITY RELATION;

ADENOSINE TRIPHOSPHATE; AMINO ACID SUBSTITUTION; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CERCOPITHECUS AETHIOPS; COS CELLS; CRICETINAE; CRICETULUS; ION CHANNEL GATING; KATP CHANNELS; POTASSIUM; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RATS; RECEPTORS, DRUG; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84866172544     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201210803     Document Type: Article

References (46)

1. Aguilar-Bryan, L., and J. Bryan. 1999. Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocr. Rev. 20:101-135. http://dx.doi.org/10.1210/er.20.2.101
2. Antcliff, J.F., S. Haider, P. Proks, M.S. Sansom, and F.M. Ashcroft. 2005. Functional analysis of a structural model of the ATP-binding site of the KATP channel Kir6.2 subunit. EMBO J. 24:229-239. http://dx.doi.org/10.1038/sj.emboj.7600487
3. Ashcroft, F.M. 1988. Adenosine 5'-triphosphate-sensitive potassium channels. Annu. Rev. Neurosci. 11:97-118. http://dx.doi.org/10.1146/annurev.ne.11.030188.000525
4. Ashcroft, F.M. 2005. ATP-sensitive potassium channelopathies: focus on insulin secretion. J. Clin. Invest. 115:2047-2058. http://dx.doi.org/10.1172/JCI25495
5. Babenko, A.P. 2005. K(ATP) channels " vingt ans après" : ATG to PDB to Mechanism. J. Mol. Cell. Cardiol. 39:79-98. http://dx.doi.org/10.1016/j.yjmcc.2004.12.004
6. Babenko, A.P., and J. Bryan. 2003. Sur domains that associate with and gate KATP pores define a novel gatekeeper. J. Biol. Chem. 278:41577-41580. http://dx.doi.org/10.1074/jbc.C300363200
7. Barrett-Jolley, R., C. Dart, and N.B. Standen. 1999. Direct block of native and cloned (Kir2.1) inward rectifier K+ channels by chloroethylclonidine. Br. J. Pharmacol. 128:760-766. http://dx.doi.org/10.1038/sj.bjp.0702819
8. Baukrowitz, T., U. Schulte, D. Oliver, S. Herlitze, T. Krauter, S.J. Tucker, J.P. Ruppersberg, and B. Fakler. 1998. PIP2 and PIP as determinants for ATP inhibition of KATP channels. Science. 282:1141- 1144. http://dx.doi.org/10.1126/science.282.5391.1141
9. Cartier, E.A., L.R. Conti, C.A. Vandenberg, and S.L. Shyng. 2001. Defective trafficking and function of KATP channels caused by a sulfonylurea receptor 1 mutation associated with persistent hyperinsulinemic hypoglycemia of infancy. Proc. Natl. Acad. Sci. USA. 98:2882-2887. http://dx.doi.org/10.1073/pnas.051499698
10. Chan, K.W., H. Zhang, and D.E. Logothetis. 2003. N-terminal transmembrane domain of the SUR controls trafficking and gating of Kir6 channel subunits. EMBO J. 22:3833-3843. http://dx.doi.org/10.1093/emboj/cdg376
11. Cukras, C.A., I. Jeliazkova, and C.G. Nichols. 2002. The role of NH2-terminal positive charges in the activity of inward rectifier KATP channels. J. Gen. Physiol. 120:437-446. http://dx.doi.org/10.1085/jgp.20028621
12. Enkvetchakul, D., G. Loussouarn, E. Makhina, S.L. Shyng, and C.G. Nichols. 2000. The kinetic and physical basis of K(ATP) channel gating: toward a unified molecular understanding. Biophys. J. 78:2334- 2348. http://dx.doi.org/10.1016/S0006-3495(00)76779-8
13. Fan, Z., and J.C. Makielski. 1997. Anionic phospholipids activate ATP-sensitive potasium channels. J. Biol. Chem. 272:5388-5395. http://dx.doi.org/10.1074/jbc.272.9.5388
14. Gloyn, A.L., E.R. Pearson, J.F. Antcliff, P. Proks, G.J. Bruining, A.S. Slingerland, N. Howard, S. Srinivasan, J.M. Silva, J. Molnes, et al. 2004. Activating mutations in the gene encoding the ATPsensitive potassium-channel subunit Kir6.2 and permanent neonatal diabetes. N. Engl. J. Med. 350:1838-1849. http://dx.doi.org/10.1056/NEJMoa032922
15. Hansen, S.B., X. Tao, and R. MacKinnon. 2011. Structural basis of PIP2 activation of the classical inward rectifier K+ channel Kir2.2. Nature. 477:495-498. http://dx.doi.org/10.1038/nature10370
16. Hilgemann, D.W., and R. Ball. 1996. Regulation of cardiac Na+,Ca2+ exchange and KATP potassium channels by PIP2. Science. 273:956- 959. http://dx.doi.org/10.1126/science.273.5277.956
17. Inagaki, N., T. Gonoi, J.P. Clement IV, N. Namba, J. Inazawa, G. Gonzalez, L. Aguilar-Bryan, S. Seino, and J. Bryan. 1995. Reconstitution of IKATP: an inward rectifier subunit plus the sulfonylurea receptor. Science. 270:1166-1170. http://dx.doi.org/10.1126/science.270.5239.1166
18. Koster, J.C., M.S. Remedi, C. Dao, and C.G. Nichols. 2005. ATP and sulfonylurea sensitivity of mutant ATP-sensitive K+ channels in neonatal diabetes: implications for pharmacogenomic therapy. Diabetes. 54:2645-2654. http://dx.doi.org/10.2337/diabetes.54.9.2645
19. Koster, J.C., H.T. Kurata, D. Enkvetchakul, and C.G. Nichols. 2008. DEND mutation in Kir6.2 (KCNJ11) reveals a flexible N-terminal region critical for ATP-sensing of the KATP channel. Biophys. J. 95:4689-4697. http://dx.doi.org/10.1529/biophysj.108.138685
20. Lin, C.W., Y.W. Lin, F.F. Yan, J. Casey, M. Kochhar, E.B. Pratt, and S.L. Shyng. 2006a. Kir6.2 mutations associated with neonatal diabetes reduce expression of ATP-sensitive K+ channels: implications in disease mechanism and sulfonylurea therapy. Diabetes. 55:1738-1746. http://dx.doi.org/10.2337/db05-1571
21. Lin, Y.W., T. Jia, A.M. Weinsoft, and S.L. Shyng. 2003. Stabilization of the activity of ATP-sensitive potassium channels by ion pairs formed between adjacent Kir6.2 subunits. J. Gen. Physiol. 122:225-237. http://dx.doi.org/10.1085/jgp.200308822
22. Lin, Y.W., C. MacMullen, A. Ganguly, C.A. Stanley, and S.L. Shyng. 2006b. A novel KCNJ11 mutation associated with congenital hyperinsulinism reduces the intrinsic open probability of beta-cell ATP-sensitive potassium channels. J. Biol. Chem. 281:3006-3012. http://dx.doi.org/10.1074/jbc.M511875200
23. Lin, Y.W., J.D. Bushman, F.F. Yan, S. Haidar, C. MacMullen, A. Ganguly, C.A. Stanley, and S.L. Shyng. 2008. Destabilization of ATP-sensitive potassium channel activity by novel KCNJ11 mutations identified in congenital hyperinsulinism. J. Biol. Chem. 283:9146-9156. http://dx.doi.org/10.1074/jbc.M708798200
24. Loussouarn, G., L.J. Pike, F.M. Ashcroft, E.N. Makhina, and C.G. Nichols. 2001. Dynamic sensitivity of ATP-sensitive K(+) channels to ATP. J. Biol. Chem. 276:29098-29103. http://dx.doi.org/10.1074/jbc.M102365200
25. Macmullen, C.M., Q. Zhou, K.E. Snider, P.H. Tewson, S.A. Becker, A.R. Aziz, A. Ganguly, S.L. Shyng, and C.A. Stanley. 2011. Diazoxide-unresponsive congenital hyperinsulinism in children with dominant mutations of the β-cell sulfonylurea receptor SUR1. Diabetes. 60:1797-1804. http://dx.doi.org/10.2337/ db10-1631
26. Mikhailov, M.V., J.D. Campbell, H. de Wet, K. Shimomura, B. Zadek, R.F. Collins, M.S. Sansom, R.C. Ford, and F.M. Ashcroft. 2005. 3-D structural and functional characterization of the purified KATP channel complex Kir6.2-SUR1. EMBO J. 24:4166-4175. http://dx.doi.org/10.1038/sj.emboj.7600877
27. Nichols, C.G. 2006. KATP channels as molecular sensors of cellular metabolism. Nature. 440:470-476. http://dx.doi.org/10.1038/nature04711
28. Pinney, S.E., C. MacMullen, S. Becker, Y.W. Lin, C. Hanna, P. Thornton, A. Ganguly, S.L. Shyng, and C.A. Stanley. 2008. Clinical characteristics and biochemical mechanisms of congenital hyperinsulinism associated with dominant KATP channel mutations. J. Clin. Invest. 118:2877-2886. http://dx.doi.org/10.1172/JCI35414
29. Pratt, E.B., F.F. Yan, J.W. Gay, C.A. Stanley, and S.L. Shyng. 2009. Sulfonylurea receptor 1 mutations that cause opposite insulin secretion defects with chemical chaperone exposure. J. Biol. Chem. 284:7951-7959. http://dx.doi.org/10.1074/jbc.M807012200
30. Pratt, E.B., P. Tewson, C.E. Bruederle, W.R. Skach, and S.L. Shyng. 2011. N-terminal transmembrane domain of SUR1 controls gating of Kir6.2 by modulating channel sensitivity to PIP2. J. Gen. Physiol. 137:299-314. http://dx.doi.org/10.1085/jgp.201010557
31. Proks, P., J.F. Antcliff, J. Lippiat, A.L. Gloyn, A.T. Hattersley, and F.M. Ashcroft. 2004. Molecular basis of Kir6.2 mutations associated with neonatal diabetes or neonatal diabetes plus neurological features. Proc. Natl. Acad. Sci. USA. 101:17539-17544. http://dx.doi.org/10.1073/pnas.0404756101
32. Proks, P., A.L. Arnold, J. Bruining, C. Girard, S.E. Flanagan, B. Larkin, K. Colclough, A.T. Hattersley, F.M. Ashcroft, and S. Ellard. 2006. A heterozygous activating mutation in the sulphonylurea receptor SUR1 (ABCC8) causes neonatal diabetes. Hum. Mol. Genet. 15:1793-1800. http://dx.doi.org/10.1093/hmg/ddl101
33. Schulze, D., T. Krauter, H. Fritzenschaft, M. Soom, and T. Baukrowitz. 2003. Phosphatidylinositol 4,5-bisphosphate (PIP2) modulation of ATP and pH sensitivity in Kir channels. A tale of an active and a silent PIP2 site in the N terminus. J. Biol. Chem. 278:10500-10505. http://dx.doi.org/10.1074/jbc.M208413200.
34. Schwappach, B., N. Zerangue, Y.N. Jan, and L.Y. Jan. 2000. Molecular basis for K(ATP) assembly: transmembrane interactions mediate association of a K+ channel with an ABC transporter. Neuron. 26:155-167. http://dx.doi.org/10.1016/S0896-6273(00)81146-0
35. Shyng, S.L., and C.G. Nichols. 1998. Membrane phospholipid control of nucleotide sensitivity of KATP channels. Science. 282:1138-1141. http://dx.doi.org/10.1126/science.282.5391.1138.
36. Shyng, S.L., Q. Sha, T. Ferrigni, A.N. Lopatin, and C.G. Nichols. 1996. Depletion of intracellular polyamines relieves inward rectification of potassium channels. Proc. Natl. Acad. Sci. USA. 93:12014-12019. http://dx.doi.org/10.1073/pnas.93.21.12014.
37. Shyng, S., T. Ferrigni, and C.G. Nichols. 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. http://dx.doi.org/10.1085/jgp.110.6.643.
38. Sigworth, F.J. 1980. The variance of sodium current fluctuations at the node of Ranvier. J. Physiol. 307:97-129.
39. Tammaro, P., P. Proks, and F.M. Ashcroft. 2006. Functional effects of naturally occurring KCNJ11 mutations causing neonatal diabetes on cloned cardiac KATP channels. J. Physiol. 571:3-14. http://dx.doi.org/10.1113/jphysiol.2005.099168.
40. Tucker, S.J., F.M. Gribble, C. Zhao, S. Trapp, and F.M. Ashcroft. 1997. Truncation of Kir6.2 produces ATP-sensitive K+ channels in the absence of the sulphonylurea receptor. Nature. 387:179-183. http://dx.doi.org/10.1038/387179a0.
41. Tucker, S.J., F.M. Gribble, P. Proks, S. Trapp, T.J. Ryder, T. Haug, F. Reimann, and F.M. Ashcroft. 1998. Molecular determinants of KATP channel inhibition by ATP. EMBO J. 17:3290-3296. http://dx.doi.org/10.1093/emboj/17.12.3290.
42. Wang, C., K. Wang, W. Wang, Y. Cui, and Z. Fan. 2002. Compromised ATP binding as a mechanism of phosphoinositide modulation of ATP-sensitive K+ channels. FEBS Lett. 532:177-182. http://dx.doi.org/10.1016/S0014-5793(02)03671-2.
43. Whorton, M.R., and R. MacKinnon. 2011. Crystal structure of the mammalian GIRK2 K+ channel and gating regulation by G proteins, PIP2, and sodium. Cell. 147:199-208. http://dx.doi.org/10.1016/j.cell.2011.07.046.
44. Yan, F., C.W. Lin, E. Weisiger, E.A. Cartier, G. Taschenberger, and S.L. Shyng. 2004. Sulfonylureas correct trafficking defects of ATP-sensitive potassium channels caused by mutations in the sulfonylurea receptor. J. Biol. Chem. 279:11096-11105. http://dx.doi.org/10.1074/jbc.M312810200.
45. Yan, F.F., Y.W. Lin, C. MacMullen, A. Ganguly, C.A. Stanley, and S.L. Shyng. 2007. Congenital hyperinsulinism associated ABCC8 mutations that cause defective trafficking of ATP-sensitive K+ channels: identification and rescue. Diabetes. 56:2339-2348. http://dx.doi.org/10.2337/db07-0150.
46. Zerangue, N., B. Schwappach, Y.N. Jan, and L.Y. Jan. 1999. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron. 22:537-548. http://dx.doi.org/10.1016/S0896-6273(00)80708-4.