Nonintegral stoichiometry in CFTR gating revealed by a pore-lining mutation

Journal of General Physiology

Volumn 140, Issue 4, 2012, Pages 347-359

  Jih, Kang Yang ^a,b   Sohma, Yoshiro ^c   Hwang, Tzyh Chang ^a,b  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHLORIDE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL; ARTICLE; CHANNEL GATING; CHEMISTRY; CHO CELL; CRICETULUS; GENETICS; HAMSTER; HYDROLYSIS; METABOLISM; MISSENSE MUTATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CHLORIDES; CHO CELLS; CRICETINAE; CRICETULUS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HYDROLYSIS; ION CHANNEL GATING; MUTATION, MISSENSE; PROTEIN STRUCTURE, TERTIARY;

EID: 84870795585     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201210834     Document Type: Article

References (39)

1. Aleksandrov, A.A., L. Aleksandrov, and J.R. Riordan. 2002. Nucleoside triphosphate pentose ring impact on CFTR gating and hydrolysis. FEBS Lett. 518:183-188. http://dx.doi.org/10.1016/S0014-5793(02)02698-4
2. Aller, S.G., J. Yu, A. Ward, Y. Weng, S. Chittaboina, R. Zhuo, P.M. Harrell, Y.T. Trinh, Q. Zhang, I.L. Urbatsch, and G. Chang. 2009. Structure of P-glycoprotein reveals a molecular basis for polyspecific drug binding. Science. 323:1718-1722. http://dx.doi.org/10.1126/science.1168750
3. Bai, Y., M. Li, and T.C. Hwang. 2010. Dual roles of the sixth transmembrane segment of the CFTR chloride channel in gating and permeation. J. Gen. Physiol. 136:293-309. http://dx.doi.org/10.1085/jgp.201010480
4. Bai, Y., M. Li, and T.C. Hwang. 2011. Structural basis for the channel function of a degraded ABC transporter, CFTR (ABCC7). J. Gen. Physiol. 138:495-507. http://dx.doi.org/10.1085/jgp.201110705
5. Bompadre, S.G., T. Ai, J.H. Cho, X. Wang, Y. Sohma, M. Li, and T.C. Hwang. 2005a. CFTR gating I: Characterization of the ATPdependent gating of a phosphorylation-independent CFTR channel (ΔR-CFTR). J. Gen. Physiol. 125:361-375. http://dx.doi.org/10.1085/jgp.200409227
6. Bompadre, S.G., J.H. Cho, X. Wang, X. Zou, Y. Sohma, M. Li, and T.C. Hwang. 2005b. CFTR gating II: Effects of nucleotide binding on the stability of open states. J. Gen. Physiol. 125:377-394. http://dx.doi.org/10.1085/jgp.200409228
7. 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. http://dx.doi.org/10.1074/jbc.270.4.1711
8. 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
9. Csanády, L., D. Seto-Young, K.W. Chan, C. Cenciarelli, B.B. Angel, J. Qin, D.T. McLachlin, A.N. Krutchinsky, B.T. Chait, A.C. Nairn, and D.C. Gadsby. 2005. Preferential phosphorylation of R-domain serine 768 dampens activation of CFTR channels by PKA. J. Gen. Physiol. 125:171-186. http://dx.doi.org/10.1085/jgp.200409076
10. Csanády, L., A.C. Nairn, and D.C. Gadsby. 2006. Thermodynamics of CFTR channel gating: a spreading conformational change initiates an irreversible gating cycle. J. Gen. Physiol. 128:523-533. http://dx.doi.org/10.1085/jgp.200609558
11. 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
12. Cui, G., Z.R. Zhang, A.R. O'Brien, B. Song, and N.A. McCarty. 2008. Mutations at arginine 352 alter the pore architecture of CFTR. J. Membr. Biol. 222:91-106. http://dx.doi.org/10.1007/s00232-008-9105-9
13. Dawson, R.J., and K.P. Locher. 2006. Structure of a bacterial multidrug ABC transporter. Nature. 443:180-185. http://dx.doi.org/10.1038/nature05155
14. Gadsby, D.C., T.C. Hwang, T. Baukrowitz, G. Nagel, M. Horie, and A.C. Nairn. 1994. Regulation of CFTR channel gating. Jpn. J. Physiol. 44:S183-S192.
15. 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. http://dx.doi.org/10.1093/emboj/20.17.4964
16. 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.
17. 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. http://dx.doi.org/10.1016/0092-8674(95)90310-0
18. Hollenstein, K., D.C. Frei, and K.P. Locher. 2007. Structure of an ABC transporter in complex with its binding protein. Nature. 446:213-216. http://dx.doi.org/10.1038/nature05626
19. Hwang, T.C., G. Nagel, A.C. Nairn, and D.C. Gadsby. 1994. Regulation of the gating of cystic fibrosis transmembrane conductance regulator C1 channels by phosphorylation and ATP hydrolysis. Proc. Natl. Acad. Sci. USA. 91:4698-4702. http://dx.doi.org/10.1073/pnas.91.11.4698
20. 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.
21. Ivetac, A., J.D. Campbell, and M.S. Sansom. 2007. Dynamics and function in a bacterial ABC transporter: simulation studies of the BtuCDF system and its components. Biochemistry. 46:2767-2778. http://dx.doi.org/10.1021/bi0622571
22. Jih, K.Y., Y. Sohma, M. Li, and T.C. Hwang. 2012. 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. 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 MJ1267 ATP binding cassette reveal an induced-fit effect at the ATPase active site of an ABC transporter. Structure. 9:571-586. http://dx.doi.org/10.1016/S0969-2126(01)00617-7
24. Khare, D., M.L. Oldham, C. Orelle, A.L. Davidson, and J. Chen. 2009. Alternating access in maltose transporter mediated by rigid-body rotations. Mol. Cell. 33:528-536. http://dx.doi.org/10.1016/j.molcel.2009.01.035
25. Kopeikin, Z., Y. Sohma, M. Li, and T.C. Hwang. 2010. On the mechanism of CFTR inhibition by a thiazolidinone derivative. J. Gen. Physiol. 136:659-671. http://dx.doi.org/10.1085/jgp.201010518
26. 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
27. Mense, M., P. Vergani, D.M. White, G. Altberg, A.C. Nairn, and D.C. Gadsby. 2006. In vivo phosphorylation of CFTR promotes formation of a nucleotide-binding domain heterodimer. EMBO J. 25:4728-4739. http://dx.doi.org/10.1038/sj.emboj.7601373
28. 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
29. Ostedgaard, L.S., O. Baldursson, and M.J. Welsh. 2001. Regulation of the cystic fibrosis transmembrane conductance regulator Clchannel by its R domain. J. Biol. Chem. 276:7689-7692. http://dx.doi.org/10.1074/jbc.R100001200
30. Richard, E.A., and C. Miller. 1990. Steady-state coupling of ionchannel conformations to a transmembrane ion gradient. Science. 247:1208-1210. http://dx.doi.org/10.1126/science.2156338
31. 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
32. 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
33. Tsai, M.F., H. Shimizu, Y. Sohma, M. Li, and T.C. Hwang. 2009. State-dependent modulation of CFTR gating by pyrophosphate. J. Gen. Physiol. 133:405-419. http://dx.doi.org/10.1085/jgp.200810186
34. Tsai, M.F., K.Y. Jih, H. Shimizu, M. Li, and T.C. Hwang. 2010a. Optimization of the degenerated interfacial ATP binding site improves the function of disease-related mutant cystic fibrosis transmembrane conductance regulator (CFTR) channels. J. Biol. Chem. 285:37663-37671. http://dx.doi.org/10.1074/jbc.M110.172817
35. Tsai, M.F., M. Li, and T.C. Hwang. 2010b. 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
36. - channels. J. Gen. Physiol. 121:17-36. http://dx.doi.org/10.1085/jgp.20028673
37. 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
38. Zhou, Z., S. Hu, and T.C. Hwang. 2001. Voltage-dependent flickery block of an open cystic fibrosis transmembrane conductance regulator (CFTR) channel pore. J. Physiol. 532:435-448. http://dx.doi.org/10.1111/j.1469-7793.2001.0435f.x
39. Zhou, Z., X. Wang, H.Y. Liu, X. Zou, M. Li, and T.C. Hwang. 2006. The two ATP binding sites of cystic fibrosis transmembrane conductance regulator (CFTR) play distinct roles in gating kinetics and energetics. J. Gen. Physiol. 128:413-422. http://dx.doi.org/10.1085/jgp.200609622