Dynamics of ATP-binding cassette contribute to allosteric control, nucleotide binding and energy transduction in ABC transporters

Journal of Molecular Biology

Volumn 342, Issue 2, 2004, Pages 525-537

  Wang, Chunyu ^a   Karpowich, Nathan ^a   Hunt, John F ^a   Rance, Mark ^b   Palmer, Arthur G ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

ABC; allosteric regulation; ATP binding cassette; dynamics; NMR

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE MAGNESIUM; BACTERIAL PROTEIN; NITROGEN 15; NUCLEOTIDE; PROTEIN MJ1267; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; CONFORMATIONAL TRANSITION; CORRELATION ANALYSIS; ENERGY TRANSFER; HYDROLYSIS; MECHANOTRANSDUCTION; METHANOCOCCUS JANNASCHII; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

METHANOCALDOCOCCUS JANNASCHII; METHANOCOCCUS;

EID: 4344592803     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.07.001     Document Type: Article

References (58)

1. J. Monod, J. Wyman, and J.P. Changeux On the nature of allosteric transitions: a plausible model J. Mol. Biol. 12 1965 88 118
2. L.N. Johnson Control by protein phosphorylation Nature Struct. Biol. 1 1994 657 659
3. C.F. Higgins ABC transporters: from microorganisms to man Annu. Rev. Cell Biol. 8 1992 67 113
4. S.V. Ambudkar, S. Dey, C.A. Hrycyna, M. Ramachandra, I. Pastan, and M.M. Gottesman Biochemical, cellular, and pharmacological aspects of the multidrug transporter Annu. Rev. Pharmacol. Toxicol. 39 1999 361 398
5. J.R. Riordan, J.M. Rommens, B. Kerem, N. Alon, R. Rozmahel, and Z. Grzelczak Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA Science 245 1989 1066 1073
6. A. Brooks-Wilson, M. Marcil, S.M. Clee, L.H. Zhang, K. Roomp, and M. van Dam Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency Nature Genet. 22 1999 336 345
7. S. Rust, M. Rosier, H. Funke, J. Real, Z. Amoura, and J.C. Piette Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1 Nature Genet. 22 1999 352 355
8. M. Bodzioch, E. Orso, J. Klucken, T. Langmann, A. Bottcher, and W. Diederich The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease Nature Genet. 22 1999 347 351
9. M. van Eck, I.S. Bos, W.E. Kaminski, E. Orso, G. Rothe, and J. Twisk Leukocyte ABCA1 controls susceptibility to atherosclerosis and macrophage recruitment into tissues Proc. Natl Acad. Sci. USA 99 2002 6298 6303
10. J. Mosser, A.M. Douar, C.O. Sarde, P. Kiochis, R. Feil, and H. Moser Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters Nature 361 1993 726 730
11. C.F. Higgins The ABC of channel regulation Cell 82 1995 693 696
12. C.F. Higgins, I.D. Hiles, G.P. Salmond, D.R. Gill, J.A. Downie, and J.J. Evans A family of related ATP-binding subunits coupled to many distinct biological processes in bacteria Nature 323 1986 448 450
13. W. Saurin, M. Hofnung, and E. Dassa Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters J. Mol. Evol. 48 1999 22 41
14. L.W. Hung, I.X. Wang, K. Nikaido, P.Q. Liu, G.F. Ames, and S.H. Kim Crystal structure of the ATP-binding subunit of an ABC transporter Nature 396 1998 703 707
15. K. Diederichs, J. Diez, G. Grellar, C. Muller, J. Breed, and C. Schnell Crystal structure of MalK, the ATPase subunit of the trehalose/maltose ABC transporter of the archaeon Thermococcus litoralis Embo J. 19 2000 5951 5961
16. N. Karpowich, O. Martsinkevich, L. Millen, Y.R. Yuan, P.L. Dai, and K. MacVey Crystal structures of the MJ1267 ATP binding cassette reveal an induced-fit effect at the ATPase active site of an ABC transporter Structure 9 2001 571 586
17. Y.R. Yuan, S. Blecker, O. Martsinkevich, L. Millen, P.J. Thomas, and J.F. Hunt 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 2001 32313 32321
18. L. Schmitt, H. Benabdelhak, M.A. Blight, I.B. Holland, and M.T. Stubbs Crystal structure of the nucleotide-binding domain of the ABC-transporter haemolysin B: identification of a variable region within ABC helical domains J. Mol. Biol. 330 2003 333 342
19. G. Verdon, S.V. Albers, B.W. Dijkstra, A.J. Driessen, and A.M. Thunnissen Crystal structures of the ATPase subunit of the glucose ABC transporter from Sulfolobus solfataricus: nucleotide-free and nucleotide-bound conformations J. Mol. Biol. 330 2003 343 358
20. P.C. Smith, N. Karpowich, L. Millen, J.E. Moody, J. Rosen, P.J. Thomas, and J.F. Hunt ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer Mol. Cell 10 2002 139 149
21. J. Chen, G. Lu, J. Lin, A.L. Davidson, and F.A. Quiocho A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle Mol. Cell 12 2003 651 661
22. K.P. Hopfner Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily Cell 101 2000 789 800
23. K.P. Hopfner, and J.A. Tainer Rad50/SMC proteins and ABC transporters: unifying concepts from high-resolution structures Curr. Opin. Struct. Biol. 13 2003 249 255
24. G. Chang, and C.B. Roth Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters Science 293 2001 1793 1800
25. G. Chang Structure of MsbA from Vibrio cholera: a multidrug resistance ABC transporter homolog in a closed conformation J. Mol. Biol. 330 2003 419 430
26. K.P. Locher, A.T. Lee, and D.C. Rees The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism Science 296 2002 1091 1098
27. E. Schneider, and S. Hunke ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains FEMS Microbiol. Rev. 22 1998 1 20
28. M.F. Rosenberg, G. Verlarde, R.C. Ford, C. Martin, G. Berridge, and I.D. Kerr Repacking of the transmembrane domains of P-glycoprotein during the transport ATPase cycle EMBO J. 20 2001 5615 5625
29. P.J. Thomas, and J.F. Hunt A snapshot of Nature's favorite pump Nature Struct. Biol. 8 2001 920 923
30. B. Sarkadi, E.M. Price, R.C. Boucher, U.A. Germann, and G.A. Scarborough Expression of the human multidrug resistance cDNA in insect cells generates a high activity drug-stimulated membrane ATPase J. Biol. Chem. 267 1992 4854 4858
31. Q. Mao, E.M. Leslie, R.G. Deeley, and S.P. Cole ATPase activity of purified and reconstituted multidrug resistance protein MRP1 from drug-selected H69AR cells Biochim. Biophys. Acta 1461 1999 69 82
32. J. Chen, S. Sharma, F.A. Quiocho, and A.L. Davidson Trapping the transition state of an ATP-binding cassette transporter: evidence for a concerted mechanism of maltose transport Proc. Natl Acad. Sci. USA 98 2001 1525 1530
33. C.E. Liu, P.Q. Liu, and G.F. Ames Characterization of the adenosine triphosphatase activity of the periplasmic histidine permease, a traffic ATPase (ABC transporter) J. Biol. Chem. 272 1997 21883 21891
34. 15N relaxation data exclusively J. Biomol. NMR 6 1995 153 162
35. C. Wang, M. Rance, and A.G. Palmer Mapping chemical exchange in proteins with MW >50 kDa J. Am. Chem. Soc. 125 2003 8968 8969
36. A.G. Palmer, C.D. Kroenke, and J.P. Loria Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules Methods Enzymol. 339 2001 204 238
37. 13C backbone assignment of MJ1267, an ATP-binding cassette J. Biomol. NMR 24 2002 167 168
38. C. Wang, and A.G. Palmer Solution NMR methods for quantitative identification of chemical exchange in 15N-labeled proteins Magn. Reson. Chem. 41 2003 866 876
39. 15N NMR relaxation Biochemistry 33 1994 5984 6003
40. 2 free-precession relaxation in the presence of n-site chemical exchange. J. Magn. Reson. In the Press.
41. D. Kern, and E.R. Zuiderweg The role of dynamics in allosteric regulation Curr. Opin. Struct. Biol. 13 2003 748 757
42. D.E. Koshland Jr, G. Nemethy, and D. Filmer Comparison of experimental binding data and theoretical models in proteins containing subunits Biochemistry 5 1966 365 385
43. V.A. Feher, and J. Cavanagh Millisecond-timescale motions contribute to the function of the bacterial response regulator protein Spo0F Nature 400 1999 289 293
44. L.C. James, and D.S. Tawfik Conformational diversity and protein evolution: a 60-year-old hypothesis revisited Trends Biochem. Sci. 28 2003 361 368
45. D.E. Koshland Application of a theory of enzyme specificity to protein synthesis Proc. Natl Acad. Sci. USA 44 1958 98 104
46. 3--activated Spo0F reveals the conformational switch in a phosphorelay system J. Mol. Biol. 331 2003 245 254
47. B.F. Volkman, D. Lipson, D.E. Wemmer, and D. Kern Two-state allosteric behavior in a single-domain signaling protein Science 291 2001 2429 2433
48. B. Ma, M. Shatsky, H.J. Wolfson, and R. Nussinov Multiple diverse ligands binding at a single protein site: a matter of pre-existing populations Protein Sci. 11 2002 184 197
49. I.D. Kerr Structure and association of ATP-binding cassette transporter nucleotide-binding domains Biochim. Biophys. Acta 1561 2002 47 64
50. C. Wang, N.H. Pawley, and L.K. Nicholson The role of backbone motions in ligand binding to the c-Src SH3 domain J. Mol. Biol. 313 2001 873 887
51. J. Evenas, A. Malmendal, and M. Akke Dynamics of the transition between open and closed conformations in a calmodulin C-terminal domain mutant Structure 9 2001 185 195
52. L.C. James, P. Roversi, and D.S. Tawfik Antibody multispecificity mediated by conformational diversity Science 299 2003 1362 1367
53. J.A. Lukin, G. Kontaxis, V. Simplaceanu, Y. Yuan, A. Bax, and C. Ho Quaternary structure of hemoglobin in solution Proc. Natl Acad. Sci. USA 100 2003 517 520
54. H. Yang, G. Luo, P. Karnchanaphanurach, T.M. Louie, I. Rech, and S. Cova Protein conformational dynamics probed by single-molecule electron transfer Science 302 2003 262 266
55. A.M. van Oijen, P.C. Blainey, D.J. Crampton, C.C. Richardson, T. Ellenberger, and X.S. Xie Single-molecule kinetics of λ exonuclease reveal base dependence and dynamic disorder Science 301 2003 1235 1238
56. A.L. Lee, S.A. Kinnear, and A.J. Wand Redistribution and loss of side chain entropy upon formation of a calmodulin-peptide complex Nature Struct. Biol. 7 2000 72 77
57. C. Bracken, P.A. Carr, J. Cavanagh, and A.G. Palmer Temperature dependence of intramolecular dynamics of the basic leucine zipper of GCN4: implications for the entropy of association with DNA J. Mol. Biol. 285 1999 2133 2146
58. G.J. Kroon, H. Mo, M.A. Martinez-Yamout, H.J. Dyson, and P.E. Wright Changes in structure and dynamics of the Fv fragment of a catalytic antibody upon binding of inhibitor Protein Sci. 12 2003 1386 1394