Cysteine scanning of CFTR's first transmembrane segment reveals its plausible roles in gating and permeation

Biophysical Journal

Volumn 104, Issue 4, 2013, Pages 786-797

  Gao, Xiaolong ^a,b   Bai, Yonghong ^a,b   Hwang, Tzyh Chang ^a,b,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE; CYSTEINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; MESYLIC ACID DERIVATIVE; METHANETHIOSULFONATE;

ANIMAL; ARTICLE; CELL MEMBRANE; CHANNEL GATING; CHEMISTRY; CHO CELL; CRICETULUS; DRUG EFFECT; GENETICS; HAMSTER; METABOLISM; MISSENSE MUTATION; PERMEABILITY; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CELL MEMBRANE; CHLORIDES; CHO CELLS; CRICETINAE; CRICETULUS; CYSTEINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ION CHANNEL GATING; MESYLATES; MUTATION, MISSENSE; PERMEABILITY; PROTEIN STRUCTURE, TERTIARY;

EID: 84874150515     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.12.048     Document Type: Article

References (55)

1. J.R. Riordan, J.M. Rommens, B. Kerem, N. Alon, R. Rozmahel, Z. Grzelczak, J. Zielenski, S. Lok, N. Plavsic, and J.L. Chou Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA Science 245 1989 1066 1073
2. C.E. Bear, and C.H. Li J.R. Riordan Purification and functional reconstitution of the cystic fibrosis transmembrane conductance regulator (CFTR) Cell 68 1992 809 818
3. M. Dean, and T. Annilo Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates Annu. Rev. Genomics Hum. Genet. 6 2005 123 142
4. D.C. Gadsby, P. Vergani, and L. Csanády The ABC protein turned chloride channel whose failure causes cystic fibrosis Nature 440 2006 477 483
5. T.Y. Chen, and T.C. Hwang CLC-0 and CFTR: chloride channels evolved from transporters Physiol. Rev. 88 2008 351 387
6. T.C. Hwang, and D.N. Sheppard Gating of the CFTR Cl- channel by ATP-driven nucleotide-binding domain dimerisation J. Physiol. 587 2009 2151 2161
7. M.F. Tsai, and H. Shimizu T.C. Hwang State-dependent modulation of CFTR gating by pyrophosphate J. Gen. Physiol. 133 2009 405 419
8. M.F. Tsai, M. Li, and T.C. Hwang Stable ATP binding mediated by a partial NBD dimer of the CFTR chloride channel J. Gen. Physiol. 135 2010 399 414
9. I. Szollosi, and S.J. King M.T. Naughton Tachycardia in adults with cystic fibrosis is associated with normal autonomic function Intern. Med. J. 41 2011 455 461
10. K.Y. Jih, and Y. Sohma T.C. Hwang Identification of a novel post-hydrolytic state in CFTR gating J. Gen. Physiol. 139 2012 359 370
11. D.C. Rees, E. Johnson, and O. Lewinson ABC transporters: the power to change Nat. Rev. Mol. Cell Biol. 10 2009 218 227
12. Y. Bai, M. Li, and T.C. Hwang Structural basis for the channel function of a degraded ABC transporter, CFTR (ABCC7) J. Gen. Physiol. 138 2011 495 507
13. W. Wang, and P. Linsdell Alternating access to the transmembrane domain of the ATP-binding cassette protein cystic fibrosis transmembrane conductance regulator (ABCC7) J. Biol. Chem. 287 2012 10156 10165
14. K.Y. Jih, and T.C. Hwang Nonequilibrium gating of CFTR on an equilibrium theme Physiology (Bethesda) 27 2012 351 361
15. C. Alexander, and A. Ivetac D.C. Dawson Cystic fibrosis transmembrane conductance regulator: using differential reactivity toward channel-permeant and channel-impermeant thiol-reactive probes to test a molecular model for the pore Biochemistry 48 2009 10078 10088
16. Y. Bai, M. Li, and T.C. Hwang Dual roles of the sixth transmembrane segment of the CFTR chloride channel in gating and permeation J. Gen. Physiol. 136 2010 293 309
17. J.J. Zhou, and M.S. Li P. Linsdell Regulation of conductance by the number of fixed positive charges in the intracellular vestibule of the CFTR chloride channel pore J. Gen. Physiol. 135 2010 229 245
18. F. Qian, Y. El Hiani, and P. Linsdell Functional arrangement of the 12th transmembrane region in the CFTR chloride channel pore based on functional investigation of a cysteine-less CFTR variant Pflugers Arch 462 2011 559 571
19. G.G. Wilson, and A. Karlin The location of the gate in the acetylcholine receptor channel Neuron 20 1998 1269 1281
20. A.M. Engh, and M. Maduke Cysteine accessibility in ClC-0 supports conservation of the ClC intracellular vestibule J. Gen. Physiol. 125 2005 601 617
21. J.M. Pascual, and D. Wang D.C. De Vivo Structural signatures and membrane helix 4 in GLUT1: inferences from human blood-brain glucose transport mutants J. Biol. Chem. 283 2008 16732 16742
22. Y. El Hiani, and P. Linsdell Changes in accessibility of cytoplasmic substances to the pore associated with activation of the cystic fibrosis transmembrane conductance regulator chloride channel J. Biol. Chem. 285 2010 32126 32140
23. Y. Norimatsu, and A. Ivetac M.S. Sansom Cystic fibrosis transmembrane conductance regulator: a molecular model defines the architecture of the anion conduction path and locates a "bottleneck" in the pore Biochemistry 51 2012 2199 2212
24. E.J. Beck, and Y. Yang V. Raghuram Conformational changes in a pore-lining helix coupled to cystic fibrosis transmembrane conductance regulator channel gating J. Biol. Chem. 283 2008 4957 4966
25. M.H. Akabas, and C. Kaufmann P. Archdeacon Amino acid residues lining the chloride channel of the cystic fibrosis transmembrane conductance regulator J. Biol. Chem. 269 1994 14865 14868
26. W. Wang, and P. Linsdell Relative movements of transmembrane regions at the outer mouth of the cystic fibrosis transmembrane conductance regulator channel pore during channel gating J. Biol. Chem. 287 2012 32136 32146
27. R.J. Dawson, and K.P. Locher Structure of a bacterial multidrug ABC transporter Nature 443 2006 180 185
28. R.J. Dawson, and K.P. Locher Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP FEBS Lett. 581 2007 935 938
29. A. Ward, and C.L. Reyes G. Chang Flexibility in the ABC transporter MsbA: alternating access with a twist Proc. Natl. Acad. Sci. USA 104 2007 19005 19010
30. S.G. Aller, and J. Yu G. Chang Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding Science 323 2009 1718 1722
31. M. Hohl, and C. Briand M.A. Seeger Crystal structure of a heterodimeric ABC transporter in its inward-facing conformation Nat. Struct. Mol. Biol. 19 2012 395 402
32. J.P. Mornon, P. Lehn, and I. Callebaut Atomic model of human cystic fibrosis transmembrane conductance regulator: membrane-spanning domains and coupling interfaces Cell. Mol. Life Sci. 65 2008 2594 2612
33. A.W. Serohijos, and T. Hegedus J.R. Riordan Phenylalanine-508 mediates a cytoplasmic-membrane domain contact in the CFTR 3D structure crucial to assembly and channel function Proc. Natl. Acad. Sci. USA 105 2008 3256 3261
34. J.P. Mornon, P. Lehn, and I. Callebaut Molecular models of the open and closed states of the whole human CFTR protein Cell. Mol. Life Sci. 66 2009 3469 3486
35. W. Wang, Y. El Hiani, and P. Linsdell Alignment of transmembrane regions in the cystic fibrosis transmembrane conductance regulator chloride channel pore J. Gen. Physiol. 138 2011 165 178
36. Y. Li, and W.P. Yu T.Y. Chen Oxidation and reduction control of the inactivation gating of Torpedo ClC-0 chloride channels Biophys. J. 88 2005 3936 3945
37. X. Liu, and C. Alexander D.C. Dawson Variable reactivity of an engineered cysteine at position 338 in cystic fibrosis transmembrane conductance regulator reflects different chemical states of the thiol J. Biol. Chem. 281 2006 8275 8285
38. L. Csanady Rapid kinetic analysis of multichannel records by a simultaneous fit to all dwell-time histograms Biophys. J. 78 2000 785 799
39. T. Ma, and J.R. Thiagarajah A.S. Verkman Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion J. Clin. Invest. 110 2002 1651 1658
40. Z. Kopeikin, and Y. Sohma T.C. Hwang On the mechanism of CFTR inhibition by a thiazolidinone derivative J. Gen. Physiol. 136 2010 659 671
41. H. Lindley A study of the kinetics of the reaction between thiol compounds and choloracetamide Biochem. J. 74 1960 577 584
42. X. Liu, and Z.R. Zhang D.C. Dawson CFTR: a cysteine at position 338 in TM6 senses a positive electrostatic potential in the pore Biophys. J. 87 2004 3826 3841
43. S. Zeltwanger, and F. Wang T.C. Hwang Gating of cystic fibrosis transmembrane conductance regulator chloride channels by adenosine triphosphate hydrolysis. Quantitative analysis of a cyclic gating scheme J. Gen. Physiol. 113 1999 541 554
44. P. Vergani, A.C. Nairn, and D.C. Gadsby On the mechanism of MgATP-dependent gating of CFTR Cl-channels J. Gen. Physiol. 121 2003 17 36
45. Z. Zhou, S. Hu, and T.C. Hwang Voltage-dependent flickery block of an open cystic fibrosis transmembrane conductance regulator (CFTR) channel pore J. Physiol. 532 2001 435 448
46. Y. Liu, and M. Holmgren G. Yellen Gated access to the pore of a voltage-dependent K+ channel Neuron 19 1997 175 184
47. J.J. Zhou, M. Fatehi, and P. Linsdell Identification of positive charges situated at the outer mouth of the CFTR chloride channel pore Pflugers Arch 457 2008 351 360
48. S.S. Smith, and E.D. Steinle D.C. Dawson Cystic fibrosis transmembrane conductance regulator. Physical basis for lyotropic anion selectivity patterns J. Gen. Physiol. 114 1999 799 818
49. P. Linsdell Mechanism of chloride permeation in the cystic fibrosis transmembrane conductance regulator chloride channel Exp. Physiol. 91 2006 123 129
50. N.A. McCarty, and Z.R. Zhang Identification of a region of strong discrimination in the pore of CFTR Am. J. Physiol. Lung Cell. Mol. Physiol. 281 2001 L852 L867
51. C.N. Aubin, and P. Linsdell Positive charges at the intracellular mouth of the pore regulate anion conduction in the CFTR chloride channel J. Gen. Physiol. 128 2006 535 545
52. J.A. Tabcharani, and J.M. Rommens J.W. Hanrahan Multi-ion pore behaviour in the CFTR chloride channel Nature 366 1993 79 82
53. J.F. Cotten, and M.J. Welsh Cystic fibrosis-associated mutations at arginine 347 alter the pore architecture of CFTR. Evidence for disruption of a salt bridge J. Biol. Chem. 274 1999 5429 5435
54. J. Kyte, and R.F. Doolittle A simple method for displaying the hydropathic character of a protein J. Mol. Biol. 157 1982 105 132
55. S.H. White, and W.C. Wimley Membrane protein folding and stability: physical principles Annu. Rev. Biophys. Biomol. Struct. 28 1999 319 365