The intact CFTR protein mediates ATPase rather than adenylate kinase activity

Biochemical Journal

Volumn 412, Issue 2, 2008, Pages 315-321

  Ramjeesingh, Mohabir ^a   Ugwu, Francisca ^a   Stratford, Fiona L L ^a   Huan, Ling Jun ^a   Li, Canhui ^a   Bear, Christine E ^a  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

Adenylate kinase; ATP binding cassette (ABC) superfamily; ATPase; Chloride electrodiffusion; Nucleotide binding domain (NBD); Protein kinase A (PKA)

Indexed keywords

BINDING SITES; BIOLOGICAL MEMBRANES; HYDROLYSIS; MUTAGENESIS; NUCLEOTIDES; PROTEINS;

ADENYLATE KINASE; ATP BINDING CASSETTE (ABC) SUPERFAMILY; ATPASE; CHLORIDE ELECTRODIFFUSION; CYSTIC FIBROSIS; NUCLEOTIDE BINDING DOMAIN (NBD); PROTEIN KINASE A (PKA);

ENZYME ACTIVITY;

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; ADENYLATE KINASE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ARTICLE; CATALYSIS; ENZYME ACTIVITY; HUMAN; HYDROLYSIS; MUTANT; MUTATION; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; ANIMALS; CELL LINE; CHLORIDES; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DINUCLEOSIDE PHOSPHATES; HUMANS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

PROKARYOTA;

EID: 44449169949     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20071719     Document Type: Article

References (50)

1. Riordan, J. R., Rommens, J. M., Kerem, B., Alon, N., Rozmahel, R., Grzelczak, Z., Zielenski, J., Lok, S., Plavsic, N., Chou, J. L. et al. (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245, 1066-1073
2. Higgins, C. F. (2001) ABC transporters: physiology, structure and mechanism - an overview. Res. Microbiol. 152, 205-210
3. Higgins, C. F. and Linton, K. J. (2001) Structural biology. The xyz of ABC transporters. Science 293, 1782-1784
4. Li, C., Ramjeesingh, M., Wang, W., Garami, E., Hewryk, M., Lee, D., Rommens, J. M., Galley, K. and Bear, C. E. (1996) ATPase activity of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 271, 28463-28468
5. 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
6. Vergani, P., Basso, C., Mense, M., Nairn, A. C. and Gadsby, D. C. (2005) Control of the CFTR channel's gates. Biochem. Soc. Trans. 33, 1003-1007
7. Gadsby, D. C., Vergani, P. and Csanady, L. (2006) The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440, 477-483
8. Vergani, P., Lockless, S. W., Nairn, A. C. and Gadsby, D. C. (2005) CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains. Nature 433, 876-880
9. 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
10. 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
11. Bear, C. E., Li, C., Galley, K., Wang, Y., Garami, E. and Ramjeesingh, M. (1997) Coupling of ATP hydrolysis with channel gating by purified, reconstituted CFTR. J. Bioenerg. Biomembr. 29, 465-473
12. Kogan, I., Ramjeesingh, M., Li, C., Kidd, J. F., Wang, Y., Leslie, E. M., Cole, S. P. and Bear, C. E. (2003) CFTR directly mediates nucleotide-regulated glutathione flux. EMBO J. 22, 1981-1989
13. Zaitseva, J., Jenewein, S., Jumpertz, T., Holland, I. B. and Schmitt, L. (2005) H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J. 24, 1901-1910
14. Yuan, Y. R., Blecker, S., Martsinkevich, O., Milien, L., Thomas, P. J. and Hunt, J. F. (2001) The crystal structure of the MJ0796 ATP-binding cassette. Implications for the structural consequences of ATP hydrolysis in the active site of an ABC transporter. J. Biol. Chem. 276, 32313-32321
15. Wang, C., Karpowich, N., Hunt, J. F., Ranee, M. and Palmer, A. G. (2004) Dynamics of ATP-binding cassette contribute to allosteric control, nucleotide binding and energy transduction in ABC transporters. J. Mol. Biol. 342, 525-537
16. Zaitseva, J., Oswald, C., Jumpertz, T., Jenewein, S., Wiedenmann, A., Holland, I. B. and Schmitt, L. (2006) A structural analysis of asymmetry required for catalytic activity of an ABC-ATPase domain dimer. EMBO J. 25, 3432-3443
17. Pinkett, H. W., Lee, A. T., Lum, P., Locher, K. P. and Rees, D. C. (2007) An inward-facing conformation of a putative metal-chelate-type ABC transporter. Science 315, 373-377
18. Oldham, M. L., Khare, D., Quiocho, F. A., Davidson, A. L. and Chen, J. (2007) Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450, 515-521
19. Locher, K. P., Lee, A. T. and Rees, D. C. (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296, 1091-1098
20. Karpowich, N., Martsinkevich, C., Milien, L., Yuan, Y. R., Dai, P. L., MacVey, K., Thomas, P. J. and Hunt, J. F. (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
21. Hopfner, K. P., Karcher, A., Shin, D. S., Craig, L., Arthur, L. M., Carney, J. P. and Tainer, J. A. (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
22. Hollenstein, K., Frei, D. C. and Locher, K. P. (2007) Structure of an ABC transporter in complex with its binding protein. Nature 446, 213-216
23. Aleksandrov, L., Mengos, A., Chang, X., Aleksandrov, A. and Riordan, J. R. (2001) Differential interactions of nucleotides at the two nucleotide binding domains of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 276, 12918-12923
24. Smith, P. C., Karpowich, N., Millen, L., Moody, J. E., Rosen, J., Thomas, P. J. and Hunt, J. F. (2002) ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell 10, 139-149
25. Randak, C. O. and Welsh, M. J. (2005) Adenylate kinase activity in ABC transporters. J. Biol. Chem. 280, 34385-34388
26. Randak, C. and Welsh, M. J. (2003) An intrinsic adenylate kinase activity regulates gating of the ABC transporter CFTR. Cell 115, 837-850
27. Gross, C. H., Abdul-Manan, N., Fulghum, J., Lippke, J., Liu, X., Prabhakar, P., Brennan, D., Willis, M. S., Faerman, C., Connelly, P. et al. (2006) Nucleotide-binding domains of cystic fibrosis transmembrane conductance regulator, an ABC transporter, catalyze adenylate kinase activity but not ATP hydrolysis. J. Biol. Chem. 281, 4058-4068
28. Kidd, J. F., Ramjeesingh, M., Stratford, F., Huan, L. J. and Bear, C. E. (2004) A heteromeric complex of the two nucleotide binding domains of cystic fibrosis transmembrane conductance regulator (CFTR) mediates ATPase activity. J. Biol. Chem. 279, 41664-41669
29. 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
30. Ramjeesingh, M., Li, C., Kogan, I., Wang, Y., Huan, L. J. and Bear, C. E. (2001) A monomer is the minimum functional unit required for channel and ATPase activity of the cystic fibrosis transmembrane conductance regulator. Biochemistry 40, 10700-10706
31. Stratford, F. L., Ramjeesingh, M., Cheung, J. C., Huan, L. J. and Bear, C. E. (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
32. 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. et al. (2004) Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J. 23, 282-293
33. Travis, S. M., Carson, M. R., Ries, D. R. and Welsh, M. J. (1993) Interaction of nucleotides with membrane-associated cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 268, 15336-15339
34. Rosenberg, M. F., Kamis, A. B., Aleksandrov, L. A., Ford, R. C. and Riordan, J. R. (2004) Purification and crystallization of the cystic fibrosis transmembrane conductance regulator (CFTR). J. Biol. Chem. 279, 39051-39057
35. Callebaut, I., Eudes, R., Mornon, J. P. and Lehn, P. (2004) Nucleotide-binding domains of human cystic fibrosis transmembrane conductance regulator: detailed sequence analysis and three-dimensional modeling of the heterodimer. Cell. Mol. Life Sci. 61, 230-242
36. Eudes, R., Lehn, P., Ferec, C., Mornon, J. P. and Callebaut, I. (2005) Nucleotide binding domains of human CFTR: a structural classification of critical residues and disease-causing mutations. Cell. Mol. Life Sci. 62, 2112-2123
37. Goldberg, A. F. and Miller, C. (1991) Solubilization and functional reconstitution of a chloride channel from Torpedo californica electroplax. J. Membr. Biol. 124, 199-206
38. Garty, H., Rudy, B. and Karlish, S. J. (1983) A simple and sensitive procedure for measuring isotope fluxes through ion-specific channels in heterogenous populations of membrane vesicles. J. Biol. Chem. 258, 13094-13099
39. 2+ ATPase activity. J. Mol. Med. 75, 674-677
40. Aleksandrov, A. A., Aleksandrov, L. A. and Riordan, J. R. (2007) CFTR (ABCC7) is a hydrolyzable-ligand-gated channel. Pflugers Arch. 453, 693-702
41. Davidson, A. L. and Chen, J. (2004) ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem. 73, 241-268
42. Bhaskara, V., Dupre, A., Lengsfeld, B., Hopkins, B. B., Chan, A., Lee, J. H., Zhang, X., Gautier, J., Zakian, V. and Pauli, T. T. (2007) Rad50 adenylate kinase activity regulates DNA tethering by Mre11/Rad50 complexes. MoL. Cell 25, 647-661
43. Hyde, S. C., Emsley, P., Hartshorn, M. J., Mimmack, M. M., Gileadi, U., Pearce, S. R., Gallagher, M. P., Gill, D. R., Hubbard, R. E. and Higgins, C. F. (1990) Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature 346, 362-365
44. Criswell, A. R., Bae, E., Stec, B., Konisky, J. and Phillips, Jr., G. N. (2003) Structures of thermophilic and mesophilic adenylate kinases from the genus Methanococcus. J. Mol. Biol. 330, 1087-1099
45. Zhang, H. J., Sheng, X. R., Pan, X. M. and Zhou, J. M. (1997) Activation of adenylate kinase by denaturants is due to the increasing conformational flexibility at its active sites. Biochem. Biophys. Res. Commun. 238, 382-386
46. Hung, L. W., Wang, I. X., Nikaido, K., Liu, P. Q., Ames, G. F. and Kim, S. H. (1998) Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396, 703-707
47. Zaitseva, J., Jenewein, S., Wiedenmann, A., Benabdelhak, H., Holland, I. B. and Schmitt, L. (2005) Functional characterization and ATP-induced dimerization of the isolated ABC-domain of the haemolysin B transporter. Biochemistry 44, 9680-9690
48. 2+-bound dimer of GlcV, an ABC-ATPase from Sulfolobus solfataricus. J. Mol. Biol. 334, 255-267
49. Urbatsch, I. L., Julien, M., Carrier, I., Rousseau, M. E., Cayrol, R. and Gros, P. (2000) Mutational analysis of conserved carboxylate residues in the nucleotide binding sites of P-glycoprotein. Biochemistry 39, 14138-14149
50. Imagawa, T., Kaya, S. and Taniguchi, K. (2003) The amino acid sequence 442GDASE446 in Na/K-ATPase is an important motif in forming the high and low affinity ATP binding pockets. J. Biol. Chem. 278, 50283-50292