State-dependent modulation of CFTR gating by pyrophosphate

Journal of General Physiology

Volumn 133, Issue 4, 2009, Pages 405-419

  Tsai, Ming Feng ^a,b   Shimizu, Hiroyasu ^a,b   Sohma, Yoshiro ^b,c,d   Li, Min ^b   Hwang, Tzyh Chang ^a,b  

^a Department of Medical Pharmacology and Physiology ^*

^b UNIVERSITY OF MISSOURI   (United States)

^c OSAKA MEDICAL COLLEGE   (Japan)

^d KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; MAGNESIUM ION; MAGNESIUM PYROPHOSPHATE; NUCLEOTIDE BINDING PROTEIN; PYROPHOSPHATE; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; MAGNESIUM DERIVATIVE; PROTEIN BINDING; PYROPHOSPHORIC ACID DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CHANNEL GATING; CONTROLLED STUDY; DIMERIZATION; ELECTROPHYSIOLOGY; INDUCED MUTATION; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; STEADY STATE; ANIMAL; CHEMISTRY; CHO CELL LINE; COMPARATIVE STUDY; CRICETULUS; HAMSTER; HUMAN; METABOLISM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DIPHOSPHATES; HUMANS; ION CHANNEL GATING; MAGNESIUM COMPOUNDS; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING;

EID: 64549132504     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200810186     Document Type: Article

References (58)

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, L., A. Mengos, X. 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.
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. Aleksandrov, and J.R. Riordan. 2008. Mg2+-dependent ATP occlusion at the first nucleotide-binding domain (NBD1) of CFTR does not require the second (NBD2). Biochem. J. 416: 129 - 136.
5. 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.
6. 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.
7. Anderson, W.B., and R.C. Nordlie. 1967. Inorganic pyrophosphateglucose phosphotransferase activity associated with alkaline phosphatase of Escherichia coli. J. Biol. Chem. 242: 114 - 119.
8. 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.
9. Baukrowitz, T., T.C. Hwang, A.C. Nairn, and D.C. Gadsby. 1994. Coupling of CFTR Cl- channel gating to an ATP hydrolysis cycle. Neuron. 12: 473 - 482.
10. Berger, A.L., M. Ikuma, J.F. Hunt, P.J. Thomas, and M.J. Welsh. 2002. Mutations that change the position of the putative gamma-phosphate linker in the nucleotide binding domains of CFTR alter channel gating. J. Biol. Chem. 277: 2125 - 2131.
11. 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 (Δ R-CFTR). J. Gen. Physiol. 125: 361 - 375.
12. 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.
13. Bompadre, S.G., Y. Sohma, M. Li, and T.C. Hwang. 2007. G551D and G1349D, two CF-associated mutations in the signature sequences of CFTR, exhibit distinct gating defects. J. Gen. Physiol. 129: 285 - 298.
14. Bompadre, S.G., M. Li, and T.C. Hwang. 2008. Mechanism of G551D-CFTR (cystic fibrosis transmembrane conductance regulator) potentiation by a high affinity ATP analog. J. Biol. Chem. 283: 5364 - 5369.
15. Cai, Z., A. Taddei, and D.N. Sheppard. 2006. Differential sensitivity of the cystic fibrosis (CF)-associated mutants G551D and G1349D to potentiators of the cystic fibrosis transmembrane conductance regulator (CFTR) Cl- channel. J. Biol. Chem. 281: 1970 - 1977.
16. Carnal, N.W., and C.C. Black. 1979. Pyrophosphate-dependent 6-phosphofructokinase, a new glycolytic enzyme in pineapple leaves. Biochem. Biophys. Res. Commun. 86: 20 - 26.
17. Carson, M.R., M.C. Winter, S.M. Travis, and M.J. Welsh. 1995. Pyrophosphate stimulates wild-type and mutant cystic fibrosis transmembrane conductance regulator Cl- channels. J. Biol. Chem. 270: 20466 - 20472.
18. Chen, J., G. Lu, J. Lin, A.L. Davidson, and F.A. Quiocho. 2003. A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol. Cell. 12: 651 - 661.
19. Chen, T.Y., and T.C. Hwang. 2008. CLC-0 and CFTR: chloride channels evolved from transporters. Physiol. Rev. 88: 351 - 387.
20. Clark, G.M., and R. Morley. 1976. Inorganic pyro-compounds M a ((X 2 O 7 ) b ). Chem. Soc. Rev. 5: 269 - 295.
21. Coric, T., P. Zhang, N. Todorovic, and C.M. Canessa. 2003. The extracellular domain determines the kinetics of desensitization in acid-sensitive ion channel 1. J. Biol. Chem. 278: 45240 - 45247.
22. Cotten, J.F., L.S. Ostedgaard, M.R. Carson, and M.J. Welsh. 1996. Effect of cystic fibrosis-associated mutations in the fourth intracellular loop of cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 271: 21279 - 21284.
23. Csanady, 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.
24. - channel. J. Gen. Physiol. 119: 545 - 559.
25. Gadsby, D.C., P. Vergani, and L. Csanady. 2006. The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature. 440: 477 - 483.
26. 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.
27. 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.
28. Higgins, C.F., and K.J. Linton. 2004. The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 11: 918 - 926.
29. 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.
30. Hwang, T.C., G. Nagel, A.C. Nairn, and D.C. Gadsby. 1994. Regulation of the gating of cystic fibrosis transmembrane con- ductance regulator C1 channels by phosphorylation and ATP hydrolysis. Proc. Natl. Acad. Sci. USA. 91: 4698 - 4702.
31. - channel gating by ATP binding and hydrolysis. Proc. Natl. Acad. Sci. USA. 97: 8675 - 8680.
32. Lansdell, K.A., J.F. Kidd, S.J. Delaney, B.J. Wainwright, and D.N. Sheppard. 1998. Regulation of murine cystic fibrosis transmembrane conductance regulator Cl- channels expressed in Chinese hamster ovary cells. J. Physiol. 512: 751 - 764.
33. 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.
34. Lewis, H.A., X. Zhao, C. Wang, J.M. Sauder, I. Rooney, B.W. Noland, D. Lorimer, M.C. Kearins, K. Conners, B. Condon, et al. 2005. Impact of the deltaF508 mutation in first nucleotide-binding domain of human cystic fibrosis transmembrane conductance regulator on domain folding and structure. J. Biol. Chem. 280: 1346 - 1353.
35. 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.
36. 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.
37. Nagel, G., T.C. Hwang, K.L. Nastiuk, A.C. Nairn, and D.C. Gadsby. 1992. The protein kinase A-regulated cardiac Cl- channel resembles the cystic fibrosis transmembrane conductance regulator. Nature. 360: 81 - 84.
38. Nordlie, R.C., J.D. Foster, and A.J. Lange. 1999. Regulation of glucose production by the liver. Annu. Rev. Nutr. 19: 379 - 406.
39. Powe, A.C. Jr., 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.
40. 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.
41. 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.
42. - channel gating by ADP and ATP analogues. J. Gen. Physiol. 105: 329 - 361.
43. Schultz, B.D., R.J. Bridges, and R.A. Frizzell. 1996. Lack of conventional ATPase properties in CFTR chloride channel gating. J. Membr. Biol. 151: 63 - 75.
44. Scott-Ward, T.S., Z. Cai, E.S. Dawson, A. Doherty, A.C. Da Paula, H. Davidson, D.J. Porteous, B.J. Wainwright, M.D. Amaral, D.N. Sheppard, and A.C. Boyd. 2007. Chimeric constructs endow the human CFTR Cl- channel with the gating behavior of murine CFTR. Proc. Natl. Acad. Sci. USA. 104: 16365 - 16370.
45. 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.
46. Stratford, F.L., M. Ramjeesingh, J.C. Cheung, L.J. Huan, and C.E. Bear. 2007. The Walker B motif of the second nucleotide-binding domain (NBD2) of CFTR plays a key role in ATPase activity by the NBD1-NBD2 heterodimer. Biochem. J. 401: 581 - 586.
47. Szabo, K., G. Szakacs, 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.
48. Tombline, G., L. Bartholomew, K. Gimi, G.A. Tyndall, and A.E. Senior. 2004. Synergy between conserved ABC signature Ser residues in P-glycoprotein catalysis. J. Biol. Chem. 279: 5363 - 5373.
49. Thibodeau, P.H., C.A. Brautiqam, M. Machius, and P.J. Thomas. 2005. Side chain and backbone contributions of Phe508 to CFTR folding. Nat. Struct. Mol. Biol. 12: 10 - 16.
50. - channels. J. Gen. Physiol. 121: 17 - 36.
51. 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.
52. 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.
53. 2+ -gated chloride channel. J. Gen. Physiol. 133: 69 - 77.
54. Winter, M.C., D.N. Sheppard, M.R. Carson, and M.J. Welsh. 1994. Effect of ATP concentration on CFTR Cl- channels: a kinetic analys is of channel regulation. Biophys. J. 66: 1398 - 1403.
55. Zaitseva, J., S. Jenewein, T. Jumpertz, I.B. Holland, and L. Schmitt. 2005. H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J. 24: 1901 - 1910.
56. 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.
57. 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.
58. 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.