Conformational changes in the catalytically inactive nucleotide-binding site of CFTR

Journal of General Physiology

Volumn 142, Issue 1, 2013, Pages 61-73

  Csanády, Lászlócsanady ^a   Mihályi, Csaba ^a   Szollosi, Andras ^a   Töröcsik, Beáta ^a   Vergani, Paola ^b  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CFTR PROTEIN, HUMAN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR;

ACTION POTENTIAL; ANIMAL; BINDING SITE; CHANNEL GATING; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MISSENSE MUTATION; PROTEIN TERTIARY STRUCTURE; XENOPUS;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HUMANS; ION CHANNEL GATING; MUTATION, MISSENSE; PROTEIN STRUCTURE, TERTIARY; XENOPUS;

EID: 84880024804     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201210954     Document Type: Article

References (33)

1. 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. http://dx.doi.org/10.1074/jbc .M111713200
2. Anderson, M.P., D.P. Rich, R.J. Gregory, A.E. Smith, and M.J. Welsh. 1991. Generation of cAMP-activated chloride currents by expression of CFTR. Science. 251:679-682. http://dx.doi.org/10.1126/ science.1704151
3. Artur, L., P. Chaves, and D.C. Gadsby. 2011. Extent of nucleotidebinding domain (NBD) separation when a CFTR channel closes. Biophys. J. 100:265a-266a. http://dx.doi.org/10.1016/j.bpj.2010 .12.1662
4. Basso, C., P. Vergani, A.C. Nairn, and D.C. Gadsby. 2003. Prolonged nonhydrolytic interaction of nucleotide with CFTR's NH2-terminal nucleotide binding domain and its role in channel gating. J. Gen. Physiol. 122:333-348. http://dx.doi.org/10.1085/jgp .200308798
5. Cai, Z., T.S. Scott-Ward, and D.N. Sheppard. 2003. Voltagedependent gating of the cystic fibrosis transmembrane conductance regulator Cl→ channel. J. Gen. Physiol. 122:605-620. http:// dx.doi.org/10.1085/jgp.200308921
6. 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 NH2-terminal nucleotide binding domain. J. Gen. Physiol. 116:163-180. http://dx.doi.org/10.1085/jgp.116.2.163
7. Changeux, J.P., and S.J. Edelstein. 2005. Allosteric mechanisms of signal transduction. Science. 308:1424-1428. http://dx.doi.org/10.1126/science.1108595
8. Colquhoun, D., and F.J. Sigworth. 1995. Fitting and statistical analysis of single-channel records. In Single Channel Recording. Second edition. B. Sakmann and E. Neher, editors. Plenum Press, New York. 483-587.
9. Csanády, L. 2000. Rapid kinetic analysis of multichannel records by a simultaneous fit to all dwell-time histograms. Biophys. J. 78:785-799. http://dx.doi.org/10.1016/S0006-3495(00)76636-7
10. Csanády, L. 2006. Statistical evaluation of ion-channel gating models based on distributions of log-likelihood ratios. Biophys. J. 90: 3523-3545. http://dx.doi.org/10.1529/biophysj.105.075135
11. 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. http://dx.doi.org/10.1085/jgp.116.3.477
12. Csanády, L., K.W. Chan, A.C. Nairn, and D.C. Gadsby. 2005. Functional roles of nonconserved structural segments in CFTR's NH2- terminal nucleotide binding domain. J. Gen. Physiol. 125:43-55. http://dx.doi.org/10.1085/jgp.200409174
13. Csanády, L., P. Vergani, and D.C. Gadsby. 2010. Strict coupling between CFTR's catalytic cycle and gating of its Cl- ion pore revealed by distributions of open channel burst durations. Proc. Natl. Acad. Sci. USA. 107:1241-1246. http://dx.doi.org/10.1073/ pnas.0911061107
14. Dawson, R.J.P., and K.P. Locher. 2007. Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett. 581:935-938. http://dx.doi.org/ 10.1016/j.febslet.2007.01.073
15. Fersht, A. 2002. Structure and Mechanism in Protein Science. Fourth edition. W.H. Freeman and Company, New York. 650 pp.
16. Hohl, M., C. Briand, M.G. Grütter, and M.A. Seeger. 2012. Crystal structure of a heterodimeric ABC transporter in its inward-facing conformation. Nat. Struct. Mol. Biol. 19:395-402. http://dx.doi.org/ 10.1038/nsmb.2267
17. Hollenstein, K., R.J. Dawson, and K.P. Locher. 2007. Structure and mechanism of ABC transporter proteins. Curr. Opin. Struct. Biol. 17:412-418. http://dx.doi.org/10.1016/j.sbi.2007.07.003
18. Ishihara, H., and M.J. Welsh. 1997. Block by MOPS reveals a conformation change in the CFTR pore produced by ATP hydrolysis. Am. J. Physiol. 273:C1278-C1289.
19. 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. http://dx.doi.org/10.1016/S0006-3495(83)84375-6
20. Jih, K.Y., and T.C. Hwang. 2013. Vx-770 potentiates CFTR function by promoting decoupling between the gating cycle and ATP hydrolysis cycle. Proc. Natl. Acad. Sci. USA. 110:4404-4409. http:// dx.doi.org/10.1073/pnas.1215982110
21. Jih, K.Y., Y. Sohma, and T.C. Hwang. 2012a. Nonintegral stoichiometry in CFTR gating revealed by a pore-lining mutation. J. Gen. Physiol. 140:347-359. http://dx.doi.org/10.1085/jgp.201210834
22. Jih, K.Y., Y. Sohma, M. Li, and T.C. Hwang. 2012b. Identification of a novel post-hydrolytic state in CFTR gating. J. Gen. Physiol. 139:359-370. http://dx.doi.org/10.1085/jgp.201210789
23. Lewis, H.A., S.G. Buchanan, S.K. Burley, K. Conners, M. Dickey, M. Dorwart, R. Fowler, X. Gao, W.B. Guggino, W.A. Hendrickson, et al. 2004. Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J. 23: 282-293. http://dx.doi.org/10.1038/sj.emboj.7600040
24. Monod, J., J. Wyman, and J.P. Changeux. 1965. On the nature of allosteric transitions: A plausible model. J. Mol. Biol. 12:88-118. http://dx.doi.org/10.1016/S0022-2836(65)80285-6
25. Procko, E., M.L. O'mara, W.F.D. Bennett, D.P. Tieleman, and R. Gaudet. 2009. The mechanism of ABC transporters: general lessons from structural and functional studies of an antigenic peptide transporter. FASEB J. 23:1287-1302. http://dx.doi.org/10 .1096/fj.08-121855
26. Riordan, J.R., J.M. Rommens, B. Kerem, N. Alon, R. Rozmahel, Z. Grzelczak, J. Zielenski, S. Lok, N. Plavsic, J.L. Chou, et al. 1989. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science. 245:1066-1073. http://dx.doi.org/10.1126/science.2475911
27. Smith, P.C., N. Karpowich, L. Millen, J.E. Moody, J. Rosen, P.J. Thomas, and J.F. Hunt. 2002. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell. 10:139-149. http://dx.doi.org/10.1016/ S1097-2765(02)00576-2
28. Szollosi, A., P. Vergani, and L. Csanády. 2010. Involvement of F1296 and N1303 of CFTR in induced-fit conformational change in response to ATP binding at NBD2. J. Gen. Physiol. 136:407-423. http://dx.doi.org/10.1085/jgp.201010434
29. Szollosi, A., D.R. Muallem, L. Csanády, and P. Vergani. 2011. Mutant cycles at CFTR's non-canonical ATP-binding site support little interface separation during gating. J. Gen. Physiol. 137:549-562. http://dx.doi.org/10.1085/jgp.201110608
30. Tsai, M.F., M. Li, and T.C. Hwang. 2010. Stable ATP binding mediated by a partial NBD dimer of the CFTR chloride channel. J. Gen. Physiol. 135:399-414. http://dx.doi.org/10.1085/jgp.201010399
31. Vergani, P., A.C. Nairn, and D.C. Gadsby. 2003. On the mechanism of MgATP-dependent gating of CFTR Cl→ channels. J. Gen. Physiol. 121:17-36. http://dx.doi.org/10.1085/jgp.20028673
32. Vergani, P., S.W. Lockless, A.C. Nairn, and D.C. Gadsby. 2005. CFTR channel opening by ATP-driven tight dimerization of its nucleotide- binding domains. Nature. 433:876-880. http://dx.doi.org/ 10.1038/nature03313
33. Zhou, Z., X. Wang, M. Li, Y. Sohma, X. Zou, and T.C. Hwang. 2005. High affinity ATP/ADP analogues as new tools for studying CFTR gating. J. Physiol. 569:447-457. http://dx.doi.org/10.1113/jphys iol.2005.095083