ATP and AMP mutually influence their interaction with the ATP-binding cassette (ABC) adenylate kinase cystic fibrosis transmembrane conductance regulator (CFTR) at separate binding sites

Journal of Biological Chemistry

Volumn 288, Issue 38, 2013, Pages 27692-27701

  Randak, Christoph O ^a   Dong, Qian ^a   Ver Heul, Amanda R ^a   Elcock, Adrian H ^a   Welsh, Michael J ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; NUCLEOTIDES; PROTEINS; SEPARATION;

8-AZIDOADENOSINE; ADENYLATE KINASE; ATP-BINDING CASSETTE; ATP-BINDING CASSETTE TRANSPORTERS; CHROMOSOME PROTEIN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATORS; NUCLEOTIDE TRIPHOSPHATES; STRUCTURAL MAINTENANCE;

ENZYMES;

8 AZIDOADENOSINE PHOSPHATE; 8 AZIDOADENOSINE TRIPHOSPHATE; ABC TRANSPORTER; ADENOSINE DERIVATIVE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG; CFTR PROTEIN, HUMAN;

ARTICLE; BINDING SITE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MECHANISM; HELA CELL; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; PATCH CLAMP; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; ANALOGS AND DERIVATIVES; CHEMISTRY; GENETICS; HELA CELL LINE; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ADENOSINE MONOPHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; BINDING SITES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HELA CELLS; HUMANS; PROTEIN STRUCTURE, TERTIARY;

EID: 84884562449     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.479675     Document Type: Article

References (62)

1. Hanrahan, J. W., Gentzsch, M., and Riordan, J. R. (2003) The cystic fibrosis transmembrane conductance regulator (ABCC7). in ABC Proteins from Bacteria to Man (Holland, I. B., Cole, S. P. C., Kuchler, K., and Higgins, C. F., eds) pp. 589-618, Academic Press, Amsterdam
2. Hwang, T. C., and Kirk, K. L. (2013) The CFTR ion channel. Gating, regulation, and anion permeation. Cold Spring Harb. Perspect. Med. 3, a009498
3. Davidson, A. L., Dassa, E., Orelle, C., and Chen, J. (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317-364
4. Walker, J. E., Saraste, M., Runswick, M. J., and Gay, N. J. (1982) Distantly related sequences in the α-and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1, 945-951
5. Shyamala, V., Baichwal, V., Beall, E., and Ames, G. F. (1991) Structurefunction analysis of the histidine permease and comparison with cystic fibrosis mutations. J. Biol. Chem. 266, 18714-18719
6. Ames, G. F., Mimura, C. S., Holbrook, S. R., and Shyamala, V. (1992) Traffic ATPases. Asuperfamily of transport proteins operating from Escherichia coli to humans. Adv. Enzymol. Relat. Areas Mol. Biol. 65, 1-47
7. Bianchet, M. A., Ko, Y. H., Amzel, L. M., and Pedersen, P. L. (1997) Modeling of nucleotide binding domains of ABC transporter proteins based on a F1-ATPase/recA topology. Structural model of the nucleotide binding domains of the cystic fibrosis transmembrane conductance regulator (CFTR). J. Bioenerg. Biomembr. 29, 503-524
8. 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
9. 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
10. 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
11. Gadsby, D. C., Vergani, P., and Csanády, L. (2006) TheABCprotein turned chloride channel whose failure causes cystic fibrosis. Nature 440, 477-483
12. Aleksandrov, A. A., Aleksandrov, L. A., and Riordan, J. R. (2007) CFTR (ABCC7) is a hydrolyzable-ligand-gated channel. Pflugers Arch. 453, 693-702
13. Cheung, J. C., Kim Chiaw, P., Pasyk, S., and Bear, C. E. (2008) Molecular basis for the ATPase activity of CFTR. Arch. Biochem. Biophys. 476, 95-100
14. - channel by ATP-driven nucleotide-binding domain dimerisation. J. Physiol. 587, 2151-2161
15. 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
16. 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
17. Szabó, K., Szakács, G., Hegeds, T., and Sarkadi, B. (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
18. - channels. J. Gen. Physiol. 121, 17-36
19. Randak, C., and Welsh, M. J. (2003) An intrinsic adenylate kinase activity regulates gating of the ABC transporter CFTR. Cell 115, 837-850
20. Randak, C. O., and Welsh, M. J. (2005) ADP inhibits function of the ABC transporter cystic fibrosis transmembrane conductance regulator via its adenylate kinase activity. Proc. Natl. Acad. Sci. U. S. A. 102, 2216-2220
21. Gross, C. H., Abdul-Manan, N., Fulghum, J., Lippke, J., Liu, X., Prabhakar, P., Brennan, D., Willis, M. S., Faerman, C., Connelly, P., Raybuck, S., and Moore, J. (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
22. Randak, C. O., Ver Heul, A. R., and Welsh, M. J. (2012) Demonstration of phosphoryl group transfer indicates that the ATP-binding cassette (ABC) transporter cystic fibrosis transmembrane conductance regulator (CFTR) exhibits adenylate kinase activity. J. Biol. Chem. 287, 36105-36110
23. Bhaskara, V., Dupré, A., Lengsfeld, B., Hopkins, B. B., Chan, A., Lee, J. H., Zhang, X., Gautier, J., Zakian, V., and Paull, T. T. (2007) Rad50 adenylate kinase activity regulates DNA tethering by Mre11/Rad50 complexes. Mol. Cell 25, 647-661
24. Lammens, A., and Hopfner, K. P. (2010) Structural basis for adenylate kinase activity in ABC ATPases. J. Mol. Biol. 401, 265-273
25. Schulz, G. E. (1992) Induced-fit movements in adenylate kinases. Faraday Discuss. 93, 858-893
26. Berry, M. B., Meador, B., Bilderback, T., Liang, P., Glaser, M., and Phillips, G. N., Jr. (1994) The closed conformation of a highly flexible protein. The structure of E. coli adenylate kinase with bound AMP and AMPPNP. Proteins 19, 183-198
27. Yan, H., and Tsai, M. D. (1999) Nucleoside monophosphate kinases. Structure, mechanism, and substrate specificity. Adv. Enzymol. Relat. Areas Mol. Biol. 73, 103-134
28. 5-di (adenosine-5') pentaphosphate, a potent multisubstrate inhibitor of adenylate kinase. J. Biol. Chem. 248, 1121-1123
29. 5A refined at 1.9 Å resolution. A model for a catalytic transition state. J. Mol. Biol. 224, 159-177
30. Tomasselli, A. G., and Noda, L. H. (1979) Mitochondrial GTP-AMP phosphotransferase. 2. Kinetic and equilibrium dialysis studies. Eur. J. Biochem. 93, 263-267
31. Tomasselli, A. G., and Noda, L. H. (1980) Mitochondrial ATP: AMP phosphotransferase from beef heart. Purification and properties. Eur. J. Biochem. 103, 481-491
32. Tomasselli, A. G., and Noda, L. H. (1983) Baker's yeast adenylate kinase. Evidence of conformational change from intrinsic fluorescence and difference spectra. Determination of the structure of enzyme-bound metalnucleotide by use of phosphorothioate analogues of ATP. Eur. J. Biochem. 132, 109-115
33. Ito, Y., Tomasselli, A. G., and Noda, L. H. (1980) ATP: AMP phosphotransferase from baker's yeast. Eur. J. Biochem. 105, 85-92
34. Bilderback, T., Fulmer, T., Mantulin, W. W., and Glaser, M. (1996) Substrate binding causes movement in the ATP binding domain of Escherichia coli adenylate kinase. Biochemistry 35, 6100-6106
35. Chuan, H., Lin, J., and Wang, J. H. (1989) 8-Azido-2α-O-dansyl-ATP. A fluorescent photoaffinity reagent for ATP-binding proteins and its application to adenylate kinase. J. Biol. Chem. 264, 7981-7988
36. Berry, M. B., Bae, E., Bilderback, T. R., Glaser, M., and Phillips, G. N., Jr. (2006) Crystal structure of ADP/AMP complex of Escherichia coli adenylate kinase. Proteins 62, 555-556
37. Criswell, A. R., Bae, E., Stec, B., Konisky, J., and Phillips, G. N., Jr. (2003) Structures of thermophilic and mesophilic adenylate kinases from the genus Methanococcus. J. Mol. Biol. 330, 1087-1099
38. Potter, R. L., and Haley, B. E. (1983) Photoaffinity labeling of nucleotide binding sites with 8-azidopurine analogs. Techniques and applications. Methods Enzymol. 91, 613-633
39. Polshakov, D., Rai, S., Wilson, R. M., Mack, E. T., Vogel, M., Krause, J. A., Burdzinski, G., and Platz, M. S. (2005) Photoaffinity labeling with 8-azidoadenosine and its derivatives. Chemistry of closed and opened adenosine diazaquinodimethanes. Biochemistry 44, 11241-11253
40. Gregory, R. J., Cheng, S. H., Rich, D. P., Marshall, J., Paul, S., Hehir, K., Ostedgaard, L., Klinger, K. W., Welsh, M. J., and Smith, A. E. (1990) Expression and characterization of the cystic fibrosis transmembrane conductance regulator. Nature 347, 382-386
41. Kartner, N., Augustinas, O., Jensen, T. J., Naismith, A. L., and Riordan, J. R. (1992) Mislocalization of ΔF508 CFTR in cystic fibrosis sweat gland. Nat. Genet. 1, 321-327
42. 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
43. Ostedgaard, L. S., and Welsh, M. J. (1992) Partial purification of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 267, 26142-26149
44. Schägger, H., and Von Jagow, G. (1987) Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379
45. Dong, Q., Randak, C. O., and Welsh, M. J. (2008) A mutation in CFTR modifies the effects of the adenylate kinase inhibitor Ap5A on channel gating. Biophys. J. 95, 5178-5185
46. 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., and Emtage, S. (2004) Structure of nucleotidebinding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J. 23, 282-293
47. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISSMODEL workspace. A web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201
48. Brandt, B. W., Heringa, J., and Leunissen, J. A. (2008) SEQATOMS. AWeb tool for identifying missing regions in PDB in sequence context. Nucleic Acids Res. 36, W255-W259
49. Xiang, Z., Soto, C. S., and Honig, B. (2002) Evaluating conformational free energies. The colony energy and its application to the problem of loop prediction. Proc. Natl. Acad. Sci. U. S. A. 99, 7432-7437
50. Callebaut, I., Eudes, R., Mornon, J. P., and Lehn, P. (2004) Nucleotidebinding 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
51. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb-Viewer. An environment for comparative protein modeling. Electrophoresis 18, 2714-2723
52. Cheng, S. H., Gregory, R. J., Marshall, J., Paul, S., Souza, D. W., White, G. A., O'Riordan, C. R., and Smith, A. E. (1990) Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63, 827-834
53. 2-terminal nucleotide binding domain and its role in channel gating. J. Gen. Physiol. 122, 333-348
54. 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
55. Gabriel, S. E., Brigman, K. N., Koller, B. H., Boucher, R. C., and Stutts, M. J. (1994) Cystic fibrosis heterozygote resistance to cholera toxin in the cystic fibrosis mouse model. Science 266, 107-109
56. Salvucci, M. E., Chavan, A. J., and Haley, B. E. (1992) Identification of peptides from the adenine binding domains of ATP and AMPin adenylate kinase. Isolation of photoaffinity-labeled peptides by metal chelate chromatography. Biochemistry 31, 4479-4487
57. Ramjeesingh, M., Ugwu, F., Stratford, F. L., Huan, L. J., Li, C., and Bear, C. E. (2008) The intact CFTR protein mediates ATPase rather than adenylate kinase activity. Biochem. J. 412, 315-321
58. Yazawa, M., and Noda, L. H. (1976) Studies on tyrosine residues in porcine muscle adenylate kinase. Circular dichroism spectra and chemical modification with tetranitromethane. J. Biol. Chem. 251, 3021-3026
59. 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
60. 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
61. 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
62. Karpowich, N., Martsinkevich, O., Millen, 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