Interaction of asymmetric ABCC9-encoded nucleotide binding domains determines K ATP channel SUR2A catalytic activity

Journal of Proteome Research

Volumn 7, Issue 4, 2008, Pages 1721-1728

  Park, Sungjo ^a   Lim, Bernard B C ^a   Perez Terzic, Carmen ^a   Mer, Georges ^b   Terzic, Andre ^a  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

ABC proteins; Atomic force microscopy; ATP sensitive K + channel; Circular dichroism; Dynamic light scattering

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; NUCLEOTIDE BINDING PROTEIN; POTASSIUM CHANNEL; RECOMBINANT PROTEIN; SULFONYLUREA RECEPTOR 2A; UNCLASSIFIED DRUG; ABCC9 PROTEIN, MOUSE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL;

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING SITE; CATALYSIS; CIRCULAR DICHROISM; COMPLEX FORMATION; ENZYME ACTIVITY; GENETIC CODE; LIGHT SCATTERING; MOLECULAR MODEL; NANOANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; STRUCTURE ACTIVITY RELATION; TRANSMISSION ELECTRON MICROSCOPY; AMINO ACID SUBSTITUTION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HYDROGEN BOND; LIGHT; METABOLISM; MOUSE; PROTEIN TERTIARY STRUCTURE; RADIATION SCATTERING; ULTRASTRUCTURE; ULTRAVIOLET SPECTROPHOTOMETRY;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID SUBSTITUTION; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BINDING SITES; CATALYSIS; CIRCULAR DICHROISM; HYDROGEN BONDING; KATP CHANNELS; LIGHT; MICE; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SCATTERING, RADIATION; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 45549105672     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr7007847     Document Type: Article

References (75)

1. Dean, M. The genetics of ATP-binding cassette transporters. Methods Enzymol. 2005, 400, 409-429.
2. Linton, K. J. Structure and function of ABC transporters. Physiology (Bethesda) 2007, 22, 122-130.
3. Higgins, C. F.; Linton, K. J. The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 2004, 11, 918-926.
4. Biemans-Oldehinkel, E.; Doeven, M. K.; Poolman, B. ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett. 2006, 580, 1023-1035.
5. Oram, J. F.; Vaughan, A. M. ATP-Binding cassette cholesterol transporters and cardiovascular disease. Circ. Res. 2006, 99, 1031- 1043.
6. Solbach, T. F.; Konig, J.; Fromm, M. F.; Zolk, O. ATP-binding cassette transporters in the heart. Trends Cardiovasc. Med. 2006, 16, 7-15.
7. + conductance. Neuron 2001, 31, 233-245.
8. + channel channel/enzyme multimer: metabolic gating in the heart. J. Mol. Cell. Cardiol. 2005, 38, 895-905.
9. Walker, 1. E.; Saraste, M.; Runswick, M. J.; Gay, N. J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982, 1, 945-951.
10. Higgins, C. F. ABC transporters: physiology, structure and mechanism-an overview. Res. Microbiol. 2001, 152, 205-210.
11. Ashcroft, F. M. From molecule to malady. Nature 2006, 440, 440- 447.
12. ATP channel complex Kir6.2-SUR1. EMBO J. 2005, 24, 4166-4175.
13. + channels. Neuron 1996, 16, 1011-1017.
14. Bienengraeber, M; Alekseev, A. E.; Abraham, M. R.; Carrasco, A. J.; Moreau, C; Vivaudou, M; Dzeja, P. P.; Terzic, A. ATPase activity of the sulfonylurea receptor: a catalytic function for the KATP channel complex. FASEB J. 2000, 14, 1943-1952.
15. ATP channels by SUR1 and SUR2A. J. Mol. Cell. Cardiol. 2005, 39, 491-501.
16. + channels. J. Biol. Chem. 2002, 277, 14206-14210.
17. ATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 1995, 270, 1166-1170.
18. + channel modulator binding to sulfonylurea receptors SUR2A and SUR2B: opposite effects of MgADP. Mol. Pharmacol. 1999, 55, 832-840.
19. + channel subunits Kir6.2 and SUR2A. J. Mol. Cell. Cardiol. 1999, 31, 425-434.
20. ATP channels. Circ. Res. 2002, 90, 554-561.
21. + channels. Pflugers Arch. 2006, 453, 703-718.
22. Zingman, L. V.; Hodgson, D. M.; Bast, P. H.; Kane, G. C; Perez- Terzic, C; Gumina, R. J.; Pucar, D.; Bienengraeber, M.; Dzeja, P. P.; Miki, T.; Seino, S.; Alekseev, A. E.; Terzic, A. Kir6.2 is required for adaptation to stress. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 13278- 13283.
23. Ashcroft, F. M. ATP-sensitive potassium channelopathies: focus on insulin secretion.J. Clin. Invest. 2005, 115, 2047-2058.
24. ATP channels in health and disease. J. Mol. Cell. Cardiol. 2005, 38, 937-943.
25. ATP channel openers. J. Mol. Cell. Cardiol. 2005, 38, 951-963.
26. ATP channels as molecular sensors of cellular metabolism. Nature 2006, 440, 470-176.
27. Hambrock, A.; de Oliveira Franz, C. B.; Hiller, S.; Grenz, A.; Ackermann, S.; Schulze, D. U.; Drews, G.; Osswald, H. Resveratrol binds to the sulfonylurea receptor (SUR) and induces apoptosis in a SUR subtype-specific manner. J. Biol. Chem. 2007, 282, 3347- 3356.
28. ATP channel causes maladaptive remodeling and heart failure in hypertension. Hum. Mol. Genet. 2006, 15, 2285-2297.
29. + channels in pressure overload- induced congestive heart failure revealed in KCNJ11 Kir6.2-null mutant. J. Physiol. 2006, 577, 1053-1065.
30. Du, Q.; Jovanovic, S.; Clelland, A.; Sukhodub, A.; Budas, G.; Phelan, K.; Murray-Tait, V.; Malone, L.; Jovanovic, A. Overexpression of SUR2A generates a cardiac phenotype resistant to ischemia. FASEB J. 2006, 20, 1131-1141.
31. Carrasco, A. J.; Dzeja, P. P.; Alekseev, A. E.; Pucar, D.; Zingman, L. V.; Abraham, M. R.; Hodgson, D.; Bienengraeber, M.; Puceat, M.; Janssen, E.; Wieringa, B.; Terzic, A. Adenylate kinase phos- photransfer communicates cellular energetic signals to ATP- sensitive potassium channels. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 7623-7628.
32. Abraham, M. R.; Selivanov, V. A.; Hodgson, D. M.; Pucar, D.; Zingman, L. V.; Wieringa, B.; Dzeja, P. P.; Alekseev, A. E.; Terzic, A. Coupling of cell energetics with membrane metabolic sensing. Integrative signaling through creatine kinase phosphotransfer disrupted by M-CK gene knock-out.J. Biol. Chem. 2002, 277, 24427-24434.
33. ATP channels integrated with creatine and adenylate kinases: amplification, tuning and sensing of energetic signals in the compartmentalized cellular environment. Mol. Cell. Biochem. 2004, 256-257, 243-256.
34. ATP channel gating. Nat. Genet. 2004, 36, 382-387.
35. Ueda, K.; Komine, J.; Matsuo, M.; Seino, S.; Amachi, T. Cooperative binding of ATP and MgADP in the sulfonylurea receptor is modulated by glibenclamide. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 1268-1272.
36. ATP channel interaction with adenine nucleotides. J. Mol. Cell. Cardiol. 2005, 38, 907-916.
37. Miroux, B.; Walker, J. E. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 1996, 260, 289- 298.
38. Chifflet, S.; Torriglia, A.; Chiesa, R.; Tolosa, S. A method for the determination of inorganic phosphate in the presence of labile organic phosphate and high concentrations of protein: application to lens ATPases. Anal. Biochem. 1988, 168, 1-4.
39. Park, S.; Ajtai, K.; Burghardt, T. P. Inhibition of myosin ATPase by metal fluoride complexes. Biochim. Biophys. Acta 1999, 1430, 127- 140.
40. Gakh, O.; Adamec, J.; Gacy, A. M.; Twesten, R. D.; Owen, W. G.; Isaya, G. Physical evidence that yeast frataxin is an iron storage protein. Biochemistry 2002, 41, 6798-6804.
41. Greenfield, N. J. Using circular dichroism spectra to estimate protein secondary structure. Nat. Protocols 2006, 1, 2876-2890.
42. Perez-Terzic, C.; Gacy, A. M.; Bortolon, R.; Dzeja, P. P.; Puceat, M.; Jaconi, M.; Prendergast, F. G.; Terzic, A. Structural plasticity of the cardiac nuclear pore complex in response to regulators of nuclear import. Circ. Res. 1999, 84, 1292-1301.
43. Kuznetsov, V. Y.; Ivanov, Y. D.; Bykov, V. A.; Saunin, S. A.; Fedorov, I. A.; Lemeshko, S. V.; Hoa, H. B.; Archakov, A. I. Atomic force microscopy detection of molecular complexes in multiprotein P450cam containing monooxygenase system. Proteomics 2002, 2, 1699-1705.
44. Frederix, P. L.; Akiyama, T.; Staufer, U.; Gerber, C.; Fotiadis, D.; Muller, D. J.; Engel, A. Atomic force bio-analytics. Curr. Opin. Chem. Biol. 2003, 7, 641-647.
45. 2receptor. Eur. J. Pharmacol. 2005, 518, 107-110.
46. Perez-Terzic, C.; Faustino, R. S.; Boorsma, B. J.; Arrell, D. K.; Niederlander, N. J.; Behfar, A.; Terzic, A. Stem cells transform into a cardiac phenotype with remodeling of the nuclear transport machinery. Nat. Clin. Pract. Cardiovasc. Med. 2007, 4, S68-76.
47. Perez-Terzic, C; Behfar, A.; Mery, A.; van Deursen, J. M.; Terzic, A.; Puceat, M. Structural adaptation of the nuclear pore complex in stem cell-derived cardiomyocytes. Circ. Res. 2003, 92, 444-452.
48. Zaitseva, J.; Jenewein, S.; Jumpertz, T.; Holland, I. B.; Schmitt, L. H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J. 2005, 24, 1901- 1910.
49. Sali, A.; Blundell, T. L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234, 779-815.
50. Davis, G. D.; Elisee, C; Newham, D. M.; Harrison, R. G. New fusion protein systems designed to give soluble expression in Escherichia coli. Biotechnol. Bioeng. 1999, 65, 382-388.
51. De Marco, V.; Stier, G.; Blandin, S.; de Marco, A. The solubility and stability of recombinant proteins are increased by their fusion to NusA. Biochem. Biophys. Res. Commun. 2004, 322, 766-771.
52. Sreerama, N.; Woody, R. W. Computation and analysis of protein circular dichroism spectra. Methods Enzymol. 2004, 383, 318-351.
53. Greenfield, N. J. Circular dichroism analysis for protein-protein interactions. Methods Mol. Biol. 2004, 261, 55-78.
54. Wang, H.; Yang, Y.; Schofield, M. J.; Du, C; Fridman, Y.; Lee, S. D.; Larson, E. D.; Drummond, J. T.; Alani, E.; Hsieh, P.; Erie, D. A. DNA bending and unbending by MutS govern mismatch recognition and specificity. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 14822- 14827.
55. Fotiadis, D.; Jastrzebska, B.; Philippsen, A.; Muller, D. J.; Palczewski, K.; Engel, A. Structure of the rhodopsin dimer: a working model for G-protein-coupIed receptors. Curr. Opin. Struct. Biol. 2006, 16, 252-259.
56. Moody, J. E.; Millen, L.; Binns, D.; Hunt, J. F.; Thomas, P. J. Cooperative, ATP-dependent association of the nucleotide binding cassettes during the catalytic cycle of ATP-binding cassette transporters. J. Biol. Chem. 2002, 277, 21111-21114.
57. Hopfner, K. P.; Karcher, A.; Shin, D. S.; Craig, L.; Arthur, L. M.; Carney, J. P.; Tainer, J. A. Structural biology of Rad50 ATPase: ATP- driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 2000, 101, 789-800.
58. Smith, P. C; Karpowich, N.; Millen, L.; Moody, J. E.; Rosen, J.; Thomas, P. J.; Hunt, J. F. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell 2002, 10, 139-149.
59. Campbell, J. D.; Sansom, M. S.; Ashcroft, F. M. Potassium channel regulation. EMBO Rep. 2003, 4, 1038-1042.
60. Chen, J.; Lu, G.; Lin, J.; Davidson, A. L.; Quiocho, F. A. A tweezers- like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol. Cell 2003, 12, 651-661.
61. Procko, E.; Ferrin-O'Connell, I.; Ng, S. L.; Gaudet, R. Distinct structural and functional properties of the ATPase sites in an asymmetric ABC transporter. Mol. Cell 2006, 24, 51-62.
62. Tombline, G.; Bartholomew, L.; Gimi, K.; Tyndall, G. A.; Senior, A. E. Synergy between conserved ABC signature Ser residues in P-glycoprotein catalysis. J. Biol. Chem. 2004, 279, 5363-5373.
63. ATP channels. Mol. Psychiatry 2003, 8, 253-254.
64. ATP channel mutation confers risk for vein of Marshall adrenergic atrial fibrillation. Nat. Clin. Pract. Cardiovasc. Med. 2007, 4, 110-116.
65. Zaitseva, J.; Oswald, C; Jumpertz, T.; Jenewein, S.; Wiedenmann, A.; Holland, I. B.; Schmitt, L. A structural analysis of asymmetry required for catalytic activity of an ABC-ATPase domain dimer. EMBO J. 2006, 25, 3432-3443.
66. Roosbeek, S.; Caster, H.; Liu, Q. Z.; Berne, P. F.; Duverger, N.; Christiaens, B.; Vandekerckhove, J.; Peelman, F.; Labeur, C; Rosseneu, M. Expression and activity of the nucleotide-binding domains of the human ABCA1 transporter. Protein Expression Purif. 2004, 35, 102-110.
67. Ramaen, O.; Sizun, C; Pamlard, O.; Jacquet, E.; Lallemand, J. Y. Attempts to characterize the NBD heterodimer of MRP1: transient complex formation involves Gly771 of the ABC signature sequence but does not enhance the intrinsic ATPase activity. Biochem. J. 2005, 391, 481-490.
68. ATP channels. J. Biol. Chem. 2000, 275, 3360-3364.
69. de Wet, H.; Mikhailov, M. V.; Fotinou, C; Dreger, M.; Craig, T. J.; Venien-Bryan, C; Ashcroft, F. M. Studies of the ATPase activity of the ABC protein SUR1. FEBS J. 2007, 274, 3532-3544.
70. Sokolova, A. V.; Kreplak, L.; Wedig, T.; Mucke, N.; Svergun, D. I.; Herrmann, H.r Aebi, U.; Strelkov, S. V. Monitoring intermediate filament assembly by small-angle x-ray scattering reveals the molecular architecture of assembly intermediates. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 16206-16211.
71. Palleros, D. R.; Welch, W. J.; Fink, A. L. Interaction of hsp70 with unfolded proteins: effects of temperature and nucleotides on the kinetics of binding. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 5719- 5723.
72. Sharma, S.; Davis, J. A.; Ayvaz, T.; Traxler, B.; Davidson, A. L. Functional reassembly of the Escherichia coli maltose transporter following purification of a MalF-MalG subassembly. J. Bacterial. 2005, 187, 2908-2911.
73. Wang, Z.; Stalcup, L. D.; Harvey, B. I.; Weber, J.; Chloupkova, M.; Dumont, M. E.; Dean, M.; Urbatsch, I. L. Purification and ATP hydrolysis of the putative cholesterol transporters ABCG5 and ABCG8. Biochemistry 2006, 45, 9929-9939.
74. Kidd, J. F.; Ramjeesingh, M.; Stratford, F.; Huan, L. J.; Bear, C. E. A heteromeric complex of the two nucleotide binding domains of cystic fibrosis transmembrane conductance regulator (CFTR) mediates ATPase activity. J. Biol. Chem. 2004, 279, 41664-41669.
75. Biswas-Fiss, E. E. Interaction of the nucleotide binding domains and regulation of the ATPase activity of the human retina specific ABC transporter, ABCR. Biochemistry 2006, 45, 3813-3823.