Relative movements of transmembrane regions at the outer mouth of the cystic fibrosis transmembrane conductance regulator channel pore during channel gating

Journal of Biological Chemistry

Volumn 287, Issue 38, 2012, Pages 32136-32146

  Wang, Wuyang ^a   Linsdell, Paul ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHANNEL ACTIVATION; CHANNEL GATING; CHANNEL OPENING; CHANNEL PORE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATORS; DISULFIDE BOND FORMATION; DISULFIDE BONDS; NUCLEOTIDE-BINDING DOMAIN; PATCH CLAMP RECORDING; RELATIVE LOCATION; RELATIVE MOVEMENT; SIDE-CHAINS; STATE DEPENDENCE; STRUCTURAL INFORMATION; THREE-DIMENSIONAL STRUCTURE; TRANSMEMBRANE REGIONS; TRANSMEMBRANES;

AMINO ACIDS; CYTOLOGY; ELECTROPHYSIOLOGY; PROTEINS; THREE DIMENSIONAL;

COVALENT BONDS;

CYSTEINE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; CROSS LINKING; DISULFIDE BOND; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN STRUCTURE; TRANSMEMBRANE 11; TRANSMEMBRANE 6;

ANIMALS; CADMIUM; CELL LINE; CELL MEMBRANE; CRICETINAE; CROSS-LINKING REAGENTS; CYSTEINE; DISULFIDES; EXCITATORY AMINO ACID ANTAGONISTS; HUMANS; ION TRANSPORT; IONS; MODELS, BIOLOGICAL; PATCH-CLAMP TECHNIQUES; PROTEIN CONFORMATION;

EID: 84866429140     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.385096     Document Type: Article

References (40)

1. O'Sullivan, B. P., and Freedman, S. D. (2009) Cystic fibrosis. Lancet 373, 1891-1904
2. Rees, D. C., Johnson, E., and Lewinson, O. (2009) ABC transporters. The power to change. Nat. Rev. Mol. Cell Biol. 10, 218-227
3. Gadsby, D. C., Vergani, P., and Csanády, L. (2006) The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440, 477-483
4. - channel by ATP-driven nucleotide-binding domain dimerisation. J. Physiol. 587, 2151-2161
5. Muallem, D., and Vergani, P. (2009) ATP hydrolysis-driven gating in cystic fibrosis transmembrane conductance regulator. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 247-255
6. Linsdell, P. (2006) Mechanism of chloride permeation in the cystic fibrosis transmembrane conductance regulator chloride channel. Exp. Physiol. 91, 123-129
7. Bai, Y., Li, M., Hwang, T. C. (2011) Structural basis for the channel function of a degraded ABC transporter, CFTR (ABCC7). J. Gen. Physiol. 138, 495-507
8. Wang, W., and Linsdell, P. (2012) Conformational change opening the CFTR chloride channel pore coupled to ATP-dependent channel gating. Biochim. Biophys. Acta 1818, 851-860
9. Wang, W., and Linsdell, P. (2012) Alternating access to the transmembrane domain of the ATP-binding cassette protein cystic fibrosis transmembrane conductance regulator (ABCC7). J. Biol. Chem. 287, 10156-10165
10. Kos, V., and Ford, R. C. (2009) The ATP-binding cassette family. A structural perspective. Cell Mol. Life Sci. 66, 3111-3126
11. Locher, K. P. (2009) Review. Structure and mechanism of ATP-binding cassette transporters. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 239-245
12. Rosenberg, M. F., O'Ryan, L. P., Hughes, G., Zhao, Z., Aleksandrov, L. A., Riordan, J. R., and Ford, R. C. (2011) The cystic fibrosis transmembrane conductance regulator (CFTR). Three-dimensional structure and localization of a channel gate. J. Biol. Chem. 286, 42647-42654
13. Ge, N., Muise, C. N., Gong, X., and Linsdell, P. (2004) Direct comparison of the functional roles played by different membrane spanning regions in the cystic fibrosis transmembrane conductance regulator chloride channel pore. J. Biol. Chem. 279, 55283-55289 (Pubitemid 40066525)
14. Aubin, C. N., and Linsdell, P. (2006) Positive charges at the intracellular mouth of the pore regulate anion conduction in the CFTR chloride channel. J. Gen. Physiol. 128, 535-545 (Pubitemid 44664631)
15. Fatehi, M., and Linsdell, P. (2009) Novel residues lining the CFTR chloride channel pore identified by functional modification of introduced cysteines. J. Membr. Biol. 228, 151-164
16. Qian, F., El Hiani, Y., and Linsdell, P. (2011) Functional arrangement of the 12th transmembrane region in the CFTR chloride channel pore based on functional investigation of a cysteine-less CFTR variant. Pflügers Arch. 462, 559-571
17. Zhou, J. J., Fatehi, M., and Linsdell, P. (2008) Identification of positive charges situated at the outer mouth of the CFTR chloride channel pore. Pflügers Arch 457, 351-360
18. Zhou, J. J., Li, M. S., Qi, J., and Linsdell, P. (2010) Regulation of conductance by the number of fixed positive charges in the intracellular vestibule of the CFTR chloride channel pore J. Gen. Physiol. 135, 229-245
19. Wang, W., El Hiani, Y., and Linsdell, P. (2011) Alignment of transmembrane regions in the cystic fibrosis transmembrane conductance regulator chloride channel pore. J. Gen. Physiol. 138, 165-178
20. Fatehi, M., and Linsdell, P. (2008) State-dependent access of anions to the cystic fibrosis transmembrane conductance regulator chloride channel pore. J. Biol. Chem. 283, 6102-6109
21. El Hiani, Y., and Linsdell, P. (2010) 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, 32126-32140
22. Zhang, Z. R., Song, B., and McCarty, N. A. (2005) State-dependent chemical reactivity of an engineered cysteine reveals conformational changes in the outer vestibule of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 280, 41997-42003 (Pubitemid 43023168)
23. Beck, E. J., Yang, Y., Yaemsiri, S., and Raghuram, V. (2008) Conformational changes in a pore-lining helix coupled to cystic fibrosis transmembrane conductance regulator channel gating. J. Biol. Chem. 283, 4957-4966
24. Bai, Y., Li, M., Hwang, T. C. (2010) Dual roles of the sixth transmembrane segment of the CFTR chloride channel in gating and permeation. J. Gen. Physiol. 136, 293-309
25. Norimatsu, Y., Ivetac, A., Alexander, C., Kirkham, J., O'Donnell, N., Dawson, D. C., and Sansom, M. S. (2012) 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, 2199-2212
26. Mense, M., Vergani, P., White, D. M., Altberg, G., Nairn, A. C., and Gadsby, D. C. (2006) In vivo phosphorylation of CFTR promotes formation of a nucleotide-binding domain heterodimer. EMBO J. 25, 4728-4739 (Pubitemid 44607019)
27. Li, M. S., Demsey, A. F., Qi, J., and Linsdell, P. (2009) Cysteine-independent inhibition of the CFTR chloride channel by the cysteine-reactive reagent sodium (2-sulphonatoethyl) methanethiosulphonate (MTSES). Br. J. Pharmacol. 157, 1065-1071
28. Holstead, R. G., Li, M. S., and Linsdell, P. (2011) Functional differences in pore properties between wild-type and cysteine-less forms of the CFTR chloride channel. J. Membr. Biol. 243, 15-23
29. Smith, S. S., Liu, X., Zhang, Z. R., Sun, F., Kriewall, T. E., McCarty, N. A., and Dawson, D. C. (2001) CFTR. Covalent and noncovalent modification suggests a role for fixed charges in anion conduction. J. Gen. Physiol. 118, 407-431 (Pubitemid 32980003)
30. Fatehi, M., St Aubin, C. N., and Linsdell, P. (2007) On the origin of asymmetric interactions between permeant anions and the CFTR chloride channel pore. Biophys. J. 92, 1241-1253 (Pubitemid 46203185)
31. + channel can be trapped in the open state by an intersubunit metal bridge. Neuron 21, 617-621
32. Neale, E. J., Elliott, D. J., Hunter, M., and Sivaprasadarao, A. (2003) Evidence for intersubunit interactions between S4 and S5 transmembrane segments of the Shaker potassium channel. J. Biol. Chem. 278, 29079-29085 (Pubitemid 36935822)
33. Sobolevsky, A. I., Yelshansky, M. V., and Wollmuth, L. P. (2004) The outer pore of the glutamate receptor channel has 2-fold rotational symmetry. Neuron 41, 367-378 (Pubitemid 38221041)
34. Clarke, C. E., Veale, E. L., Wyse, K., Vandenberg, J. I., and Mathie, A. (2008) The M1P1 loop of TASK3 K2P channels apposes the selectivity filter and influences channel function. J. Biol. Chem. 283, 16985-16992
35. 2+ coordination. Pflügers Arch. 458, 259-272
36. Li, M. S., Holstead, R. G., Wang, W., and Linsdell, P. (2011) Regulation of CFTR chloride channel macroscopic conductance by extracellular bicarbonate. Am. J. Physiol. Cell Physiol. 300, C65-C74
37. Gong, X., and Linsdell, P. (2003) Molecular determinants and role of an anion binding site in the external mouth of the CFTR chloride channel pore. J. Physiol. 549, 387-397 (Pubitemid 36701752)
38. Zhou, J. J., Fatehi, M., and Linsdell, P. (2007) Direct and indirect effects of mutations at the outer mouth of the CFTR chloride channel pore. J. Membr. Biol. 216, 129-142
39. Gupta, J., Evagelidis, A., Hanrahan, J. W., and Linsdell, P. (2001) Asymmetric structure of the cystic fibrosis transmembrane conductance regulator chloride channel pore suggested by mutagenesis of the twelfth transmembrane region. Biochemistry 40, 6620-6627 (Pubitemid 32552785)
40. Cheung, M., and Akabas, M. H. (1996) Identification of CFTR channel-lining residues in and flanking the M6 membrane-spanning semgent. Biophys. J. 70, 2688-2695 (Pubitemid 26000967)