SUR1: A unique ATP-binding cassette protein that functions as an ion channel regulator

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1514, 2009, Pages 257-267

  Aittoniemi, Jussi ^a   Fotinou, Constantina ^a   Craig, Tim J ^a   De Wet, Heidi ^a   Proks, Peter ^a   Ashcroft, Frances M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

ATP binding cassette (ABC) transporter; Diabetes; Insulin secretion; K ATP channel; Sulphonylurea receptor

Indexed keywords

DIABETES; ENZYME ACTIVITY; HORMONE; ION; METABOLISM; MOLECULAR ANALYSIS; MUTATION; NEONATE; POTASSIUM; PROTEIN; PUBLIC HEALTH; SECRETION; UREA;

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

CHEMICAL STRUCTURE; DIABETES MELLITUS; GENETICS; HUMAN; METABOLISM; MUTATION; PROTEIN CONFORMATION; REVIEW;

ATP-BINDING CASSETTE TRANSPORTERS; DIABETES MELLITUS; HUMANS; MODELS, MOLECULAR; MUTATION; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN CONFORMATION; RECEPTORS, DRUG;

EID: 61449365340     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2008.0142     Document Type: Review

References (77)

1. Abdulhadi-Atwan, M., Bushman, J. D., Tornovsky-Babaey, S., Perry, A., Abu-Libdeh, A., Glaser, B., Shyng, S. L. & Zangen, D. H. 2008 Novel de novo mutation in SUR1 presenting as HI in infancy followed by overt diabetes in early adolescence. Diabetes 57, 1935-1940. (doi: 10.2337/db08-0159)
2. Ashcroft, F. M. 2005 ATP-sensitive potassium channelopathies: focus on insulin secretion. J. Clin. Invest. 115, 2047-2058. (doi:10.1172/JCI25495)
3. + channels and disease: from molecule to malady. Am. J. Physiol. Endocrinol. Metab. 293, E880-E889. (doi:10.1152/ajpendo. 00348.2007)
4. ATP channel. Diabetes 48, 1341-1347. (doi:10.2337/diabetes.48.6.1341)
5. Babenko, A. P. 2008 A novel ABCC8 (SUR1)-dependent mechanism of metabolism-excitation uncoupling. J. Biol. Chem. 283, 8778-8782. (doi:10.1074/jbc.C700243200)
6. ATP pores define a novel gatekeeper. J. Biol. Chem. 278, 41 577-41 580. (doi:10.1074/jbc. C300363200)
7. ATP channel isoforms. J. Biol. Chem. 274, 11587-11592. (doi:10.1074/jbc.274.17. 11587)
8. Babenko, A. P. et al. 2006 Activating mutations in the ABCC8 gene in neonatal diabetes mellitus. N. Engl. J. Med. 355, 456-466. (doi:10.1056/NEJMoa055068)
9. ATP channel complex. FASEB J. 14, 1943-1952. (doi:10.1096/fj.00-0027com)
10. Campbell, J. D., Sansom, M. S. & Ashcroft, F. M. 2003 Potassium channel regulation. EMBO Rep. 4, 1038-1042. (doi:10.1038/sj.embor. 7400003)
11. Chan, K. W., Zhang, H. & Logothetis, D. E. 2003 N-terminal transmembrane domain of the SUR controls trafficking and gating of Kir6 channel subunits. EMBO J. 22, 3833-3843. (doi:10.1093/emboj/cdg376)
12. Chang, X. B., Hou, Y. X. & Riordan, J. R. 1998 Stimulation of ATPase activity of purified multidrug resistance-associated protein by nucleoside diphosphates. J. Biol. Chem. 273, 23 844-23 848. (doi:10.1074/jbc.273.37. 23844)
13. ATP channel subunits. Neuron 18, 827-838. (doi:10.1016/S0896-6273(00) 80321-9)
14. Cole, S. P. & Deeley, R. G. 1998 Multidrug resistance mediated by the ATP-binding cassette transporter protein MRP. Bioessays 20, 931-940. (doi:10.1002/(SICI)1521-1878(199811)20:11<931::AID-BIES8>3.0. CO;2-J)
15. ATP channel subunit essential for cell protection against ischemia. EMBO J. 21, 3936-3948. (doi:10.1093/emboj/cdf388)
16. + channel in vivo. FASEB J. 16, 102-104.
17. ATP channels by its actions on the sulfonylurea receptor 1 nucleotide-binding folds-1 and -2. J. Biol. Chem. 279, 53 259-53 265. (doi:10.1074/jbc.M410171200)
18. Dawson, R. J. & Locher, K. P. 2006 Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185. (doi:10.1038/nature05155)
19. Dawson, R. J. & Locher, K. P. 2007 Structure of the multidrug ABC transporter Savl866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett. 581, 935-938. (doi:10.1016/j.febslet.2007.01.073)
20. de Wet, H., Mikhailov, M. V., Fotinou, C., Dreger, M., Craig, T. J., Venien-Bryan, C. & Ashcroft, F. M. 2007a Studies of the ATPase activity of the ABC protein SUR1. FEBS J. 274, 3532-3544. (doi:10.1111/j.1742-4658.2007. 05879.x)
21. de Wet, H. et al. 2007b Increased ATPase activity produced by mutations at arginine-1380 in nucleotide-binding domain 2 of ABCC8 causes neonatal diabetes. Proc. Natl Acad. Sci. USA 104, 18 988-18 992.
22. de Wet, H., Proks, P., Lafond, M., Aittoniemi, J., Sansom, M. S. P., Flanagan, S. E., Pearson, E. R., Hattersley, A. T. & Ashcroft, F. M. 2008 A mutation (R826W) in nucleotide-binding domain 1 of ABCC8 reduces ATPase activity and causes transient neonatal diabetes. EMBO Rep. 9, 648-654. (doi:10.1038/embor.2008.71)
23. Dean, M. 2002 The human ATP-binding cassette (ABC) transporter superfamily. National Library of Medicine (US), NCBI. See http://www.ncbi.nlm. nih.gov/books/bv.fcgi?rid=mono-001.chapter.137.
24. Deeley, R. G., Westlake, C. & Cole, S. P. 2006 Trans-membrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol. Rev. 86, 849-899. (doi:10.1152/physrev. 00035.2005)
25. ATP channel inhibition by ATP requires distinct functional domains of the cytoplasmic C terminus of the pore-forming subunit. Proc. Natl Acad. Sci. USA 95, 13 953-13 958. (doi:10.1073/pnas.95.23.13953)
26. Dunne, M. J., Cosgrove, K. E., Shepherd, R. M., Aynsley-Green, A. & Lindley, K. J. 2004 Hyperinsulinism in infancy: from basic science to clinical disease. Physiol. Rev. 84, 239-275. (doi:10.1152/physrev.00022. 2003)
27. Ellard, S. et al. 2007 Permanent neonatal diabetes caused by dominant, recessive, or compound heterozygous SUR1 mutations with opposite functional effects. Am. J. Hum. Genet. 81, 375-382. (doi:10.1086/519174)
28. Gadsby, D. C., Vergani, P. & Csanady, L. 2006 The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440, 477-483. (doi: 10.1038/nature04712)
29. ATP channels of the endocrine pancreas. Diabetes 52, 767-776. (doi:10.2337/diabetes. 52.3.767)
30. ATP channel subunits Kir6.2 (KCNJ11) and SUR1 (ABCC8) in diabetes mellitus and hyperinsulinism. Hum. Mutat. 27, 220-231. (doi:10.1002/humu.20292)
31. Gribble, F. M., Tucker, S. J. & Ashcroft, F. M. 1997 The essential role of the Walker A motifs of SUR1 in K-ATP channel activation by Mg-ADP and diazoxide. EMBO J. 16, 1145-1152. (doi:10.1093/emboj/16.6.1145)
32. Gribble, F. M., Proks, P., Corkey, B. E. & Ashcroft, F. M. 1998 Mechanism of cloned ATP-sensitive potassium channel activation by oleoyl-CoA. J. Biol. Chem. 273, 26 383-26 387. (doi:10.1074/jbc.273.41.26383)
33. Haider, S., Antcliff, J. F., Proks, P., Sansom, M. S. & Ashcroft, F. M. 2005 Focus on Kir6.2: a key component of the ATP-sensitive potassium channel. J. Mol. Cell. Cardiol. 38, 927-936. (doi:10.1016/j.yjmcc.2005.01. 007)
34. ATP channels. Br. J. Pharmacol. 144, 551-557. (doi:10.1038/sj.bjp.0706082)
35. Hattersley, A. T. & Ashcroft, F. M. 2005 Activating mutations in Kir6.2 and neonatal diabetes: new clinical syndromes, new scientific insights, and new therapy. Diabetes 54, 2503-2513. (doi:10.2337/diabetes.54. 9.2503)
36. Hollenstein, K., Dawson, R. J. & Locher, K. P. 2007 Structure and mechanism of ABC transporter proteins. Curr. Opin. Struct. Biol. 17, 412-418. (doi:10.1016/j.sbi. 2007.07.003)
37. ATP) conductance in rat pancreatic A-cells. J. Physiol. 527(Pt 1), 109-120. (doi:10.1111/j.1469-7793.2000.00109.x)
38. ATP channels and insulin secretion disorders. Am. J. Physiol. Endocrinol. Metab. 283, E207-E216.
39. ATP channel. EMBO Rep. 6, 848-852. (doi:10.1038/sj.embor.7400489)
40. Kikuta, T., Ohara-Imaizumi, M., Nakazaki, M., Nishiwaki, C., Nakamichi, Y., Tei, C., Aguilar-Bryan, L., Bryan, J. & Nagamatsu, S. 2005 Docking and fusion of insulin secretory granules in SUR1 knock out mouse beta-cells observed by total internal reflection fluorescence microscopy. FEBS Lett. 579, 1602-1606. (doi:10.1016/j.febslet.2005.01.074)
41. ATP channels induces profound neonatal diabetes. Cell 100, 645-654. (doi:10.1016/S0092-8674(00)80701-1)
42. Linton, K. J. & Higgins, C. F. 2007 Structure and function of ABC transporters: the ATP switch provides flexible control. Pflugers Arch. 453, 555-567. (doi:10.1007/s00424-006-0126-x)
43. Locher, K. P. 2009 Structure and mechanism of ATP-binding cassette transporters. Phil. Trans. R. Soc. B 364, 239-245. (doi:10.1098/rstb.2008.0125)
44. + channel. Mol. Cell. Biol. 18, 1652-1659.
45. Mao, Q., Leslie, E. M., Deeley, R. G. & Cole, S. P. 1999 ATPase activity of purified and reconstituted multidrug resistance protein MRP1 from drug-selected H69AR cells. Biochim. Biophys. Acta 1461, 69-82. (doi:10.1016/S0005-2736(99)00150-9)
46. ATP channels by SUR1 and SUR2A. J. Mol. Cell. Cardiol. 39, 491-501. (doi: 10.1016/j.yjmcc.2005.03.009)
47. Masia, R., De Leon, D. D., MacMullen, C., McKnight, H., Stanley, C. A. & Nichols, C. G. 2007 A mutation in the TMD0-L0 region of sulfonylurea receptor-1 (L225P) causes permanent neonatal diabetes mellitus (PNDM). Diabetes 56, 1357-1362. (doi:10.2337/db06-1746)
48. Matsuo, M., Kioka, N., Amachi, T. & Ueda, K. 1999 ATP binding properties of the nucleotide-binding folds of SUR1. J. Biol. Chem. 274, 37 479-37 482. (doi:10.1074/jbc.274.52.37479)
49. McDevitt, C. A., Collins, R. F., Conway, M., Modok, S., Storm, J., Kerr, I. D., Ford, R. C. & Callaghan, R. 2006 Purification and 3D structural analysis of oligomeric human multidrug transporter ABCG2. Structure 14, 1623-1632. (doi:10.1016/j.str.2006.08.014)
50. ATP channel complex Kir6.2-SUR1. EMBO J. 24, 4166-4175. (doi:10.1038/sj. emboj.7600877)
51. Muallem, D. & Vergani, P. 2009 ATP hydrolysis-driven gating in cystic fibrosis transmembrane conductance regulator. Phil. Trans. R. Soc. B 364, 247-255. (doi:10. 1098/rstb.2008.0191)
52. Nakazaki, M., Crane, A., Hu, M., Seghers, V., Ullrich, S., Aguilar-Bryan, L. & Bryan, J. 2002 cAMP-activated protein kinase-independent potentiation of insulin secretion by cAMP is impaired in SUR1 null islets. Diabetes 51, 3440-3449. (doi:10.2337/diabetes.51.12.3440)
53. ATP channels as molecular sensors of cellular metabolism. Nature 440, 470-476. (doi: 10.1038/nature048711)
54. ATP channel. J. Biol. Chem. 279, 4234-4240. (doi: 10. 1074/jbc.M309667200)
55. Pearson, E. R. et al. 2006 Switching from insulin to oral sulfonylureas in patients with diabetes due to Kir6.2 mutations. N. Engl. J. Med. 355, 467-477. (doi:10.1056/NEJMoa061759)
56. ATP channels is mediated by Kir6.2. Proc. Natl Acad. Sci. USA 94, 11 716-11 720. (doi:10.1073/pnas.94.21.11716)
57. Proks, P. et al. 2006a A heterozygous activating mutation in the sulphonylurea receptor SUR1 (ABCC8) causes neonatal diabetes. Hum. Mol. Genet. 15, 1793-1800. (doi: 10.1093/hmg/dd1101)
58. Proks, P., Girard, C., Baevre, H., Njolstad, P. R. & Ashcroft, F. M. 2006b Functional effects of mutations at F35 in the NH2-terminus of Kir6.2 (KCNJ11), causing neonatal diabetes, and response to sulfonylurea therapy. Diabetes 55, 1731-1737. (doi:10.2337/db05-1420)
59. Proks, P., Shimomura, K., Craig, T. J., Girard, C. A. & Ashcroft, F. M. 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)
60. 2+/ATP reveals a non-productive catalytic site. J. Mol. Biol. 359, 940-949. (doi:10.1016/j.jmb.2006.04.005)
61. Reimann, F., Tucker, S. J., Proks, P. & Ashcroft, F. M. 1999 Involvement of the n-terminus of Kir6.2 in coupling to the sulphonylurea receptor. J. Physiol. 518(Pt 2), 325-336. (doi: 10.1111/j.1469-7793.1999.0325p.x)
62. ATP channels containing SUR2A or SUR2B subunits to nucleotides and pinacidil. Mol. Pharmacol. 58, 1318-1325.
63. + channel with an ABC transporter. Neuron 26, 155-167. (doi:10.1016/S0896-6273(00)81146-0)
64. 2+ channel in insulin granule exocytosis. J. Biol. Chem. 279, 7956-7961. (doi:10.1074/jbc.M309068200)
65. 2+ signals in insulin granule exocytosis. Diabetes 53(Suppl. 3), S59-S62. (doi:10. 2337/diabetes.53.suppl-3. S59)
66. Shield, J. P., Flanagan, S. E., Mackay, D. J., Harries, L. W., Proks, P., Girard, C., Ashcroft, F. M., Temple, I. K. & Ellard, S. 2008 Mosaic paternal uniparental isodisomy and an ABCC8 gene mutation in a patient with permanent neonatal diabetes and hemihypertrophy. Diabetes 57, 255-258. (doi:10.2337/db07-0999)
67. Sudhof, T. C. 2004 The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547. (doi:10.1146/annurev.neuro.26. 041002.131412)
68. Tammaro, P., Girard, C., Molnes, J., Njolstad, P. R. & Ashcroft, F. M. 2005 Kir6.2 mutations causing neonatal diabetes provide new insights into Kir6.2-SUR1 interactions. EMBO J. 24, 2318-2330. (doi:10.1038/sj. emboj.7600715)
69. ATP channels. J. Physiol. 571, 3-14. (doi:10.1113/jphysiol.2005.099168)
70. ATP channels. J. Biol. Chem. 277, 17 139-17 146. (doi:10.1074/jbc.M200363200)
71. + channels in the absence of the sulphonylurea receptor. Nature 387, 179-183. (doi: 10.1038/387179a0)
72. Vila-Carriles, W. H., Zhao, G. & Bryan, J. 2007 Defining a binding pocket for sulfonylureas in ATP-sensitive potassium channels. FASEB J. 21, 18-25. (doi:10.1096/fj.06-6730hyp)
73. Ward, A., Reyes, C. L., Yu, J., Roth, C. B. & Chang, G. 2007 Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc. NatlAcad. Sci. USA 104, 19 005-19 010. (doi:10.1073/pnas. 0709388104)
74. Yan, F., Lin, C. W., Weisiger, E., Carrier, E. A., Taschenberger, G. & Shyng, S. L. 2004 Sulfonylureas correct trafficking defects of ATP-sensitive potassium channels caused by mutations in the sulfonylurea receptor. J. Biol. Chem. 279, 11096-11105. (doi:10.1074/jbc. M312810200)
75. Yan, F. F., Casey, J. & Shyng, S. L. 2006 Sulfonylureas correct trafficking defects of disease-causing ATP-sensitive potassium channels by binding to the channel complex. J. Biol. Chem. 281, 33 403-33 413. (doi:10.1074/jbc. M605195200)
76. ATP channels. Neuron 22, 537-548. (doi:10.1016/S0896- 6273(00) 80708-4)
77. + conductance. Neuron 31, 233-245. (doi:10.1016/S0896-6273(01)00356-7)