Converting nonhydrolyzable nucleotides to strong cystic fibrosis transmembrane conductance regulator (CFTR) agonists by gain of function (GOF) mutations

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17122-17133

  Okeyo, George ^a   Wang, Wei ^a   Wei, Shipeng ^a   Kirk, Kevin L ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATORS; ENZYMATIC ACTIVITIES; GAIN-OF FUNCTION; LIGAND-GATED ION CHANNELS; NUCLEOTIDE-BINDING DOMAIN; SIGNATURE SEQUENCES; TIGHTLY-COUPLED;

BIOCHEMISTRY; BIOLOGY;

NUCLEOTIDES;

CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR GENE; GAIN OF FUNCTION MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; WILD TYPE;

ABC TRANSPORTER; ALLOSTERIC REGULATION; ATP; ATPASES; CFTR; CYSTIC FIBROSIS; ION CHANNELS; LIGAND; LIGAND-BINDING PROTEIN;

ADENOSINE TRIPHOSPHATE; ADENYLYL IMIDODIPHOSPHATE; BINDING SITES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HEK293 CELLS; HUMANS; HYDROLYSIS; ION CHANNEL GATING; MEMBRANE POTENTIALS; MUTATION, MISSENSE; PATCH-CLAMP TECHNIQUES; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84879066653     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.442582     Document Type: Article

References (44)

1. - channel by ATP-driven nucleotide-binding domain dimerisation. J. Physiol. 587, 2151-2161
2. Vergani P, Lockless SW, Nairn AC, and Gadsby DC (2005) CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains. Nature 433, 876-880 (Pubitemid 40314897)
3. Berger, A. L., Ikuma, M., and Welsh, M. J. (2005) Normal gating of CFTR requires ATP binding to both nucleotide-binding domains and hydrolysis at the second nucleotide-binding domain. Proc. Natl. Acad. Sci. U.S.A. 102, 455-460 (Pubitemid 40116788)
4. Aleksandrov, L., Aleksandrov, A. A., Chang, X. B., and Riordan, J. R. (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 (Pubitemid 34967805)
5. 2-terminal nucleotide binding domain and its role in channel gating. J. Gen. Physiol. 122, 333-348
6. - ion pore revealed by distributions of open channel burst durations. Proc. Natl. Acad. Sci. U.S.A. 107, 1241-1246
7. Cheng, S. H., Rich, D. P., Marshall, J., Gregory, R. J., Welsh, M. J., and Smith, A. E. (1991) Phosphorylation of the R domain by cAMP-dependent protein kinase regulates the CFTR chloride channel. Cell 66, 1027-1036 (Pubitemid 121001734)
8. Mathews, C. J., Tabcharani, J. A., Chang, X. B., Jensen, T. J., Riordan, J. R., and Hanrahan, J. W. (1998) Dibasic protein kinase A sites regulate bursting rate and nucleotide sensitivity of the cystic fibrosis transmembrane conductance regulator chloride channel. J. Physiol. 508, 365-377 (Pubitemid 28203953)
9. Gunderson, K. L., and Kopito, R. R. (1995) Conformational states of CFTR associated with channel gating. The role ATP binding and hydrolysis. Cell 82, 231-239
10. - channels. J. Gen. Physiol. 121, 17-36
11. Hennager, D. J., Ikuma, M., Hoshi, T., and Welsh, M. J. (2001) A conditional probability analysis of cystic fibrosis transmembrane conductance regulator gating indicates that ATP has multiple effects during the gating cycle. Proc. Natl. Acad. Sci. U.S.A. 98, 3594-3599 (Pubitemid 32220890)
12. Bompadre, S. G., Sohma, Y., Li, M., and Hwang, T.-C. (2007) G551D and G1349D, two CF-associated mutations in the signature sequences of CFTR, exhibit distinct gating defects. J. Gen. Physiol. 129, 285-298 (Pubitemid 46506980)
13. Wang, W., Wu, J., Bernard, K., Li, G., Wang, G., Bevensee, M. O., and Kirk, K. L. (2010) ATP-independent CFTR channel gating and allosteric modulation by phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 107, 3888-3893
14. Anderson, M. P., Berger, H. A., Rich, D. P., Gregory, R. J., Smith, A. E., and Welsh, M. J. (1991) Nucleoside triphosphates are required to open the CFTR chloride channel. Cell 67, 775-784 (Pubitemid 121001490)
15. Gunderson, K. L., and Kopito, R. R. (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
16. Auerbach A (2012) Thinking in cycles. MWC is a good model for acetycholine receptor channels. J. Physiol. 590, 93-98
17. Monod, J., Wyman, J., and Changeux, J.-P. (1965) On the nature of allosteric transitions. A plausible model. J. Mol. Biol. 12, 88-118
18. Changeux, J.-P, and Edelstein, S. J. (2005) Allosteric mechanisms of signal transduction. Science 308, 1424-1428 (Pubitemid 40791288)
19. Chang, Y., and Weiss, D. S. (1999) Allosteric activation mechanism of the α1β2γ2 γ-aminobutyric acid type A receptor revealed by mutation of the conserved M2 leucine. Biophys. J. 77, 2542-2551 (Pubitemid 29519500)
20. Colquhoun, D. (1998) Binding, gating, affinity, and efficacy. The interpretation of structure-activity relationships for agonists and the effects of mutating receptors. Br. J. Pharmacol. 125, 924-947
21. Grosman, C., and Auerbach, A. (2000) Kinetic, mechanistic, and structural aspects of unliganded gating of acetylcholine receptor channels. A single channel study of second transmembrane segment 12′ mutants. J. Gen. Physiol. 115, 621-635 (Pubitemid 30249977)
22. Galzi, J. L., Edelstein, S. J., and Changeux, J. (1996) The multiple phenotypes of allosteric receptor mutants. Proc. Natl. Acad. Sci. U.S.A. 93, 1853-1858 (Pubitemid 26079843)
23. Cui, L., Aleksandrov, L., Chang, X. B., Hou, Y. X., He, L., Hegedus, T., Gentzsch, M., Aleksandrov, A., Balch, W. E., and Riordan, J. R. (2007) Domain interdependence in the biosynthetic assembly of CFTR. J. Mol. Biol. 365, 981-994 (Pubitemid 46014191)
24. Wang, W., Bernard, K., Li, G., and Kirk, K. L. (2007) Curcumin opens cystic fibrosis transmembrane conductance regulator channels by a novel mechanism that requires neither ATP binding nor dimerization of the nucleotide binding domains. J. Biol. Chem. 282, 4533-4544 (Pubitemid 47100973)
25. Szollosi, A., Vergani, P., and Csanády, L. (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
26. Bai, Y., Li, M., and 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
27. Wang, W., Oliva, C., Li, G., Holmgren, A., Lillig, C. H., and Kirk, K. L. (2005) Reversible silencing of CFTR chloride channels by glutathionylation. J. Gen. Physiol. 125, 127-141 (Pubitemid 40224113)
28. Mornon, J. P., Lehn, P., and Callebaut, I. (2009) Molecular models of the open and closed states of the whole human CFTR protein. Cell. Mol. Life Sci. 66, 3469-3486
29. Ward, A., Reyes, C. L., Yu, J., Roth, C. B., and Chang, G. (2007) Flexibility in the ABC transporter MsbA. Alternating access with a twist. Proc. Natl. Acad. Sci. U.S.A. 104, 19005-19010
30. Wang, W., Li, G., Clancy, J. P., and Kirk, K. L. (2005) Activating cystic fibrosis transmembrane conductance regulator channels with pore blocker analogs. J. Biol. Chem. 280, 23622-23630 (Pubitemid 40884842)
31. Purohit, P., and Auerbach, A. (2009) Unliganded gating of acetylcholine receptor channels. Proc. Natl. Acad. Sci. U.S.A. 106, 115-120
32. Zhou, M., Engel, A. G., and Auerbach, A. (1999) Serum choline activates mutant acetylcholine receptors that cause slow channel congenital myasthenic syndromes. Proc. Natl. Acad. Sci. U.S.A. 96, 10466-10471 (Pubitemid 29422582)
33. Moody, J. E., Millen, L., Binns, D., Hunt, J. F., and Thomas, P. J. (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 (Pubitemid 34952244)
34. Gulick, A. M., Bauer, C. B., Thoden, J. B., and Rayment, I. (1997) X-ray structures of the MgADP, MgATPγS, and MgAMPPNP complexes of the Dictyostelium discoideum myosin motor domain. Biochemistry 36, 11619-11628 (Pubitemid 27424086)
35. Sauna, Z. E., Kim, I. W., Nandigama, K., Kopp, S., Chiba, P., and Ambudkar, S. V. (2007) Catalytic cycle of ATP hydrolysis by P-glycoprotein. Evidence for formation of the E.S reaction intermediate with ATP-γ-S, a nonhydrolyzable analogue of ATP. Biochemistry 46, 13787-13799 (Pubitemid 350223906)
36. Siarheyeva, A., Liu, R., and Sharom, F. J. (2010) Characterization of an asymmetric occluded state of P-glycoprotein with two bound nucleotides. Implications for catalysis. J. Biol. Chem. 285, 7575-7586
37. Lewis, H. A., Buchanan, S. G., Burley, S. K., Conners, K., Dickey, M., Dorwart, M., Fowler, R., Gao, X., Guggino, W. B., Hendrickson, W. A., Hunt, J. F., Kearins, M. C., Lorimer, D., Maloney, P. C., Post, K. W., Rajashankar, K. R., Rutter, M. E., Sauder, J. M., Shriver, S., Thibodeau, P. H., Thomas, P. J., Zhang, M., Zhao, X., Emtage, S. (2004) Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J. 23, 282-293 (Pubitemid 38294493)
38. Csanády, L., Nairn, A. C., and Gadsby, D. C. (2006) Thermodynamics of CFTR channel gating. A spreading conformational change initiates an irreversible gating cycle. J. Gen. Physiol. 128, 523-533 (Pubitemid 44664630)
39. Szentpétery, Z., Kern, A., Liliom, K., Sarkadi, B., Váradi, A., and Bakos, E. (2004) The role of the conserved glycines of ATP-binding cassette signature motifs of MRP1 in the communication between the substrate-binding site and the catalytic centers. J. Biol. Chem. 279, 41670-41678 (Pubitemid 39313612)
40. Payen, L., Gao, M., Westlake, C., Theis, A., Cole, S. P., and Deeley, R. G. (2005) Functional interactions between nucleotide binding domains and leukotriene C4 binding sites of multidrug resistance protein 1 (ABCC1). Mol. Pharmacol. 67, 1944-1953 (Pubitemid 41007776)
41. Aleksandrov, A. A., Aleksandrov, L. A., and Riordan, J. R. (2007) CFTR (ABCC7) is a hydrolysable-ligand-gated channel. Pflugers Arch. 453, 693-702
42. Aleksandrov, A. A., and Riordan, J. R. (1998) Regulation of CFTR ion channel gating by MgATP. FEBS Lett. 431, 97-101 (Pubitemid 28330860)
43. Ramjeesingh, M., Li, C., Garami, E., Huan, L. J., Galley, K., Wang, Y., and Bear, C. E. (1999) Walker mutations reveal loose relationship between catalytic and channel-gating activities of purified CFTR (cystic fibrosis transmembrane conductance regulator). Biochemistry 38, 1463-1468
44. Eckford, P. D., Li, C., Ramjeesingh, M., and Bear, C. E. (2012) Cystic fibrosis transmembrane conductance regulator (CFTR) potentiator VX-770 (ivacaftor) opens the defective channel gate of mutant CFTR in a phosphorylation-dependent but ATP-independent manner. J. Biol. Chem. 287, 36639-36649