On the mechanism of MgATP-dependent gating of CFTR Cl- channels

Journal of General Physiology

Volumn 121, Issue 1, 2003, Pages 17-36

  Vergani, Paola ^a   Nairn, Angus C ^a   Gadsby, David C ^a  

^a NONE

Author keywords

ABC transporters; ATP binding and hydrolysis; Catalytic site mutations; Nonhydrolyzable analogs; Single channels kinetics

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE DERIVATIVE; ADENOSINE TRIPHOSPHATE MAGNESIUM; CHLORIDE; CHLORIDE CHANNEL; NUCLEOTIDE; PHOSPHATE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CHANNEL GATING; CHEMICAL BINDING; CHEMICAL STRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYSTIC FIBROSIS; DIMERIZATION; ENZYME ACTIVE SITE; GENE MUTATION; HUMAN; HYDROLYSIS; KINETICS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PHOSPHORYLATION; XENOPUS;

EID: 0037246832     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.20028673     Document Type: Article

References (78)

1. Aleksandrov, A.A., X. Chang, L. Aleksandrov, and J.R. Riordan. 2000. The non-hydrolytic pathway of cystic fibrosis transmembrane conductance regulator ion channel gating. J. Physiol. 528:259-265.
2. Aleksandrov, A.A., and J.R. Riordan. 1998. Regulation of CFTR ion channel gating by MgATP. FEBS Lett. 431:97-101.
3. Aleksandrov, L., A.A. Aleksandrov, X.B. Chang, and J.R. Riordan. 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.
4. Aleksandrov, L., A. Mengos, X.-B. Chang, A. Aleksandrov, and J.R. Riordan. 2001. Differential interactions of nucleotides at the two nucleotide binding domains of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 276:12918-12923.
5. Anderson, M.P., H.A. Berger, D.P. Rich, R.J. Gregory, A.E. Smith, and M.J. Welsh. 1991. Nucleoside triphosphates are required to open the CFTR chloride channel. Cell. 67:775-784.
6. Anderson, M.P., and M.J. Welsh. 1992. Regulation by ATP and ADP of CFTR chloride channels that contain mutant nucleotide-binding domains. Science. 257:1701-1704.
7. Armstrong, S., L. Tabernero, H. Zhang, M. Hermodson, and C. Stauffacher. 1998. Powering the ABC transporters: the 2.5 Å crystal structure of the ABC domain of RBSA. Pediatr. Pulmonol. 17:91-92.
8. Basso, C., P. Vergani, A.C. Nairn, and D.C. Gadsby. 2002. NBD1 might remain nucleotide-bound throughout CFTR channel gating cycle. Biophys. J. 82:12a.
9. - channel gating to an ATP hydrolysis cycle. Neuron. 12:473-482.
10. Carson, M.R., S.M. Travis, and M.J. Welsh. 1995. The two nucleotide-binding domains of cystic fibrosis transmembrane conductance regulator (CFTR) have distinct functions in controlling channel activity. J. Biol. Chem. 270:1711-1717.
11. Carson, M.R., and M.J. Welsh. 1993. 5′-Adenylylimidodiphosphate does not activate CFTR chloride channels in cell-free patches of membrane. Am. J. Physiol. 265: L27-L32.
12. Carson, M.R., and M.J. Welsh. 1995. Structural and functional similarities between the nucleotide-binding domains of CFTR and GTP-binding proteins. Biophys. J. 69:2443-2448.
13. Chan, K.W., L. Csanády, D. Seto-Young, A.C. Nairn, and D.C. Gadsby. 2000. Severed molecules functionally define the boundaries of the cystic fibrosis transmembrane conductance regulator's NH(2)-terminal nucleotide binding domain. J. Gen. Physiol. 116:163-180.
14. Chang, G., and C.B. Roth. 2001. Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science. 293:1793-1800.
15. Chen, J., S. Sharma, F.A. Quiocho, and A.L. Davidson. 2001. Trapping the transition state of an ATP-binding cassette transporter: evidence for a concerted mechanism of maltose transport. Proc. Natl. Acad. Sci. USA. 98:1525-1530.
16. Cheng, S.H., D.P. Rich, J. Marshall, R.J. Gregory, M.J. Welsh, and A.E. Smith. 1991. Phosphorylation of the R domain by cAMP-dependent protein kinase regulates the CFTR chloride channel. Cell. 66:1027-1036.
17. Cotten, J.F., and M.J. Welsh. 1998. Covalent modification of the nucleotide binding domains of cystic fibrosis transmembrane conductance regulatory. J. Biol. Chem. 273:31873-31879.
18. Csanády, L. 2000. Rapid kinetic analysis of multichannel records by a simultaneous fit to all dwell-time histograms. Biophys. J. 78:785-799.
19. Csanády, L., K.W. Chan, D. Seto-Young, D.C. Kopsco, A.C. Nairn, and D.C. Gadsby. 2000. Severed channels probe regulation of gating of cystic fibrosis transmembrane conductance regulator by its cytoplasmic domains. J. Gen. Physiol. 116:477-500.
20. Del Castillo, J., and B. Katz. 1957. Interaction at end-plate receptors between different choline derivatives. Proceedings of the Royal Society of London, series B. 146:369-381.
21. Diederichs, K., J. Diez, G. Greller, C. Muller, J. Breed, C. Schnell, C. Vonrhein, W. Boos, and W. Welte. 2000. Crystal structure of MalK, the ATPase subunit of the trehalose/maltose ABC transporter of the archaeon Thermococcus litoralis. EMBO J. 19:5951-5961.
22. Dousmanis, A.G., A.C. Nairn, and D.C. Gadsby. 2002. Distinct Mg(2+)-dependent steps rate limit opening and closing of a single CFTR Cl(-) channel. J. Gen. Physiol. 119:545-559.
23. Fersht, A. 1999. Structure and Mechanism in Protein Science. W. H. Freeman and Company, New York, NY. 631 pp.
24. Gadsby, D.C., and A.C. Nairn. 1994. Regulation of CFTR channel gating. Trends Biochem. Sci. 19:513-518.
25. Gadsby, D.C., and A.C. Nairn. 1999. Control of CFTR channel gating by phosphorylation and nucleotide hydrolysis. Physiol. Rev. 79:S77-S107.
26. Gao, M., H.R. Cui, D.W. Loe, C.E. Grant, K.C. Almquist, S.P. Cole, and R.G. Deeley. 2000. Comparison of the functional characteristics of the nucleotide binding domains of multidrug resistance protein 1. J. Biol. Chem. 275:13098-13108.
27. Gaudet, R., and D.C. Wiley. 2001. Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J. 20:4964-4972.
28. Guex, N., and M.C. Peitsch. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 18:2714-2723.
29. Gunderson, K.L., and R.R. Kopito. 1994. Effects of pyrophosphate and nucleotide analogs suggest a role for ATP hydrolysis in cystic fibrosis transmembrane regulator channel gating. J. Biol. Chem. 269:19349-19353.
30. Gunderson, K.L., and R.R. Kopito. 1995. Conformational states of CFTR associated with channel gating: the role ATP binding and hydrolysis. Cell. 82:231-239.
31. Hopfner, K.P., A. Karcher, D.S. Shin, L. Craig, L.M. Arthur, J.P. Carney, and J.A. Tainer. 2000. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell. 101:789-800.
32. Hou, Y., L. Cui, J.R. Riordan, and X.B. Chang. 2000. Allosteric interactions between the two non-equivalent nucleotide binding domains of multidrug resistance protein MRP1. J. Biol. Chem. 275:20280-20287.
33. Hou, Y.X., L. Cui, J.R. Riordan, and X.B. Chang. 2002. ATP binding to the first nucleotide-binding domain of multidrug resistance protein MRP1 increases binding and hydrolysis of ATP and trapping of ADP at the second domain. J. Biol. Chem. 277:5110-5119.
34. Hrycyna, C.A., M. Ramachandra, U.A. Germann, P.W. Cheng, I. Pastan, and M.M. Gottesman. 1999. Both ATP sites of human P-glycoprotein are essential but not symmetric. Biochemistry. 38:13887-13899.
35. Hung, L.W., I.X. Wang, K. Nikaido, P.Q. Liu, G.F. Ames, and S.H. Kim. 1998. Crystal structure of the ATP-binding subunit of an ABC transporter. Nature. 396:703-707.
36. Hunke, S., M. Mourez, M. Jehanno, E. Dassa, and E. Schneider. 2000. ATP modulates subunit-subunit interactions in an ATP-binding cassette transporter (MalFGK2) determined by site-directed chemical cross-linking. J. Biol. Chem. 275:15526-15534.
37. Hwang, T.C., G. Nagel, A.C. Nairn, and D.C. Gadsby. 1994. Regulation of the gating of cystic fibrosis transmembrane conductance regulator Cl channels by phosphorylation and ATP hydrolysis. Proc. Natl. Acad. Sci. USA. 91:4698-4702.
38. - channel gating by ATP binding and hydrolysis. Proc. Natl. Acad. Sci. USA. 97:8675-8680.
39. Jackson, M.B., B.S. Wong, C.E. Morris, H. Lecar, and C.N. Christian. 1983. Successive openings of the same acetylcholine receptor channel are correlated in open time. Biophys. J. 42:109-114.
40. Jones, P.M., and A.M. George. 1999. Subunit interactions in ABC transporters: towards a functional architecture. FEMS Microbiol. Lett. 179:187-202.
41. Junop, M.S., G. Obmolova, K. Rausch, P. Hsieh, and W. Yang. 2001. Composite active site of an ABC ATPase: MutS uses ATP to verify mismatch recognition and authorize DNA repair. Mol. Cell. 7:1-12.
42. Kaczmarek, L.K., K.R. Jennings, F. Strumwasser, A.C. Nairn, U. Walter, F.D. Wilson, and P. Greengard. 1980. Microinjection of catalytic subunit of cyclic AMP-dependent protein kinase enhances calcium action potentials of bag cell neurons in cell culture. Proc. Natl. Acad. Sci. USA. 77:7487-7491.
43. Karpowich, N., O. Martsinkevich, L. Millen, Y.R. Yuan, P.L. Dai, K. MacVey, P.J. Thomas, and J.F. Hunt. 2001. Crystal structures of the MIJ1267 ATP binding cassette reveal an induced-fit effect at the ATPase active site of an ABC transporter. Structure (Camb.). 9:571-586.
44. Koronakis, E., C. Hughes, I. Milisav, and V. Koronakis. 1995. Protein exporter function and in vitro ATPase activity are correlated in ABC-domain mutants of HlyB. Mol. Microbiol. 16:87-96.
45. Li, C., M. Ramjeesingh, W. Wang, E. Garami, M. Hewryk, D. Lee, J.M. Rommens, K. Galley, and C.E. Bear. 1996. ATPase activity of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 271:28463-28468.
46. Linsdell, P., and J.W. Hanrahan. 1998. Adenosine triphosphatedependent asymmetry of anion permeation in the cystic fibrosis transmembrane conductance regulator chloride channel. J. Gen. Physiol. 111:601-614.
47. Locher, K.P., A.T. Lee, and D.C. Rees. 2002. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science. 296:1091-1098.
48. Loo, T.W., and D.M. Clarke. 2001. Cross-linking of human multidrug resistance p-glycoprotein by the substrate, tris-(2-maleimidoethyl)amine, is altered by atp hydrolysis, evidence for rotation of a transmembrane helix. J. Biol. Chem. 276:31800-31805.
49. Manavalan, P., D.G. Dearborn, J.M. McPherson, and A.E. Smith. 1995. Sequence homologies between nucleotide binding regions of CFTR and G-proteins suggest structural and functional similarities. FEBS Lett. 366:87-91.
50. Mathews, C.J., J.A. Tabcharani, and J.W. Hanrahan. 1998. The CFTR chloride channel: nucleotide interactions and temperature-dependent gating. J. Membr. Biol. 163:55-66.
51. Matsuo, M., N. Kioka, T. Amachi, and K. Ueda. 1999. ATP binding properties of the nucleotide-binding folds of SUR1. J. Biol. Chem. 274:37479-37482.
52. Matsuo, M., K. Tanabe, N. Kioka, T. Amachi, and K. Ueda. 2000. Different binding properties and affinities for ATP and ADP among sulfonylurea receptor subtypes, SUR1, SUR2A, and SUR2B. J. Biol. Chem. 275:28757-28763.
53. Moody, J.E., L. Millen, D. Binns, J.F. Hunt, and P.J. Thomas. 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.
54. Picciotto, M.R., J.A. Cohn, G. Bertuzzi, P. Greengard, and A.C. Nairn. 1992. Phosphorylation of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 267:12742-12752.
55. Powe, A.C.J., L. Al-Nakkash, M. Li, and T.C. Hwang. 2002. Mutation of Walker-A lysine 464 in cystic fibrosis transmembrane conductance regulator reveals functional interaction between its nucleotide-binding domains. J. Physiol. 539:333-346.
56. Qu, Q., and F.J. Sharom. 2001. FRET analysis indicates that the two ATPase active sites of the P-glycoprotein multidrug transporter are closely associated. Biochemistry. 40:1413-1422.
57. Quinton, P.M., and M.M. Reddy. 1992. Control of CFTR chloride conductance by ATP levels through non-hydrolytic binding. Nature. 360:79-81.
58. Ramjeesingh, M., C. Li, E. Garami, L.J. Huan, K. Galley, Y. Wang, and C.E. Bear. 1999. Walker mutations reveal loose relationship between catalytic and channel-gating activities of purified CFTR (cystic fibrosis transmembrane conductance regulator). Biochemistry. 38:1463-1468.
59. Riordan, J.R., J.M. Rommens, B. Kerem, N. Alon, R. Rozmahel, Z. Grzelczak, J. Zielenski, S. Lok, N. Plavsic, and J.L. Chou. 1989. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science. 245:1066-1073.
60. Schneider, E., and S. Hunke. 1998. ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains. FEMS Microbiol. Rev. 22:1-20.
61. - channel gating by ADP and ATP analogues. J. Gen. Physiol. 105:329-361.
62. Senior, A.E., and S. Bhagat. 1998. P-glycoprotein shows strong catalytic cooperativity between the two nucleotide sites. Biochemistry. 37:831-836.
63. Sheppard, D.N., and M.J. Welsh. 1999. Structure and function of the CFTR chloride channel. Physiol. Rev. 79:S23-S45.
64. Szabó, K., G. Szakács, T. Hegeds, and B. Sarkadi. 1999. Nucleotide occlusion in the human cystic fibrosis transmembrane conductance regulator. Different patterns in the two nucleotide binding domains. J. Biol. Chem. 274:12209-12212.
65. - channel in CHO cells stably expressing the cystic fibrosis gene. Nature. 352:628-631.
66. Ueda, K., N. Inagaki, and S. Seino. 1997. MgADP antagonism to Mg2+-independent ATP binding of the sulfonylurea receptor SUR1. J. Biol. Chem. 272:22983-22986.
67. Ueda, K., J. Komine, M. Matsuo, S. Seino, and T. Amachi. 1999. Cooperative binding of ATP and MgADP in the sulfonylurea receptor is modulated by glibenclamide. Proc. Natl. Acad. Sci. USA. 96:1268-1272.
68. Urbatsch, I.L., L. Beaudet, I. Carrier, and P. Gros. 1998. Mutations in either nucleotide-binding site of P-glycoprotein (Mdr3) prevent vanadate trapping of nucleotide at both sites. Biochemistry. 37:4592-4602.
69. Urbatsch, I.L., B. Sankaran, J. Weber, and A.E. Senior. 1995. P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J. Biol. Chem. 270:19383-19390.
70. Venglarik, C.J., B.D. Schultz, R.A. Frizzell, and R.J. Bridges. 1994. ATP alters current fluctuations of cystic fibrosis transmembrane conductance regulator: evidence for a three-state activation mechanism. J. Gen. Physiol. 104:123-146.
71. - channel gating of Walker A lysine mutation K464A imply allosteric interaction between NBDs. Biophys. J. 82:240a.
72. Walker, J.E., M. Saraste, M.J. Runswick, and N.J. Gay. 1982. 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. 1:945-951.
73. Weber, J., S.T. Hammond, S. Wilke-Mounts, and A.E. Senior. 1998. Mg2+ coordination in catalytic sites of F1-ATPase. Biochemistry. 37:608-614.
74. Weinreich, F., J.R. Riordan, and G. Nagel. 1999. Dual effects of ADP and adenylylimidodiphosphate on CFTR channel kinetics show binding to two different nucleotide binding sites. J. Gen. Physiol. 114:55-70.
75. - channels: a kinetic analysis of channel regulation. Biophys. J. 66:1398-1403.
76. Yount, R.G. 1971. Adenylyl imidodiphosphate, an adenosine triphosphate analog containing a P-N-P linkage. Biochemistry. 10:2484-2489.
77. Yuan, Y.R., S. Blecker, O. Martsinkevich, L. Millen, P.J. Thomas, and J.F. Hunt. 2001. The crystal structure of the mj0796 atp-binding cassette, implications for the structural consequences of atp hydrolysis in the active site of an abc transporter. J. Biol. Chem. 276:32313-32321.
78. Zeltwanger, S., F. Wang, G.T. Wang, K.D. Gillis, and T.C. Hwang. 1999. Gating of cystic fibrosis transmembrane conductance regulator chloride channels by adenosine triphosphate hydrolysis. Quantitative analysis of a cyclic gating scheme. J. Gen. Physiol. 113:541-554.