Distinct Structural and Functional Properties of the ATPase Sites in an Asymmetric ABC Transporter

Molecular Cell

Volumn 24, Issue 1, 2006, Pages 51-62

  Procko, Erik ^a   Ferrin O'Connell, Ian ^a   Ng, Sze Ling ^a   Gaudet, Rachelle ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

PROTEINS

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE;

ANTIGEN PRESENTATION; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOCHEMISTRY; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTALLOGRAPHY; CYTOSOL; DIMERIZATION; HYDROLYSIS; MAMMAL; MUTAGENESIS; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; TRANSPORT KINETICS;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID MOTIFS; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BINDING SITES; CONSENSUS SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HYDROLYSIS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; RATS;

MAMMALIA;

EID: 33749076230     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.07.034     Document Type: Article

References (48)

1. Admiraal S.J., and Herschlag D. Mapping the transition state for ATP hydrolysis: implications for enzymatic catalysis. Chem. Biol. 2 (1995) 729-739
2. Alberts P., Daumke O., Deverson E.V., Howard J.C., and Knittler M.R. Distinct functional properties of the TAP subunits coordinate the nucleotide-dependent transport cycle. Curr. Biol. 11 (2001) 242-251
3. Androlewicz M.J., and Cresswell P. Human transporters associated with antigen processing possess a promiscuous peptide-binding site. Immunity 1 (1994) 7-14
4. Campbell J.D., and Sansom M.S. Nucleotide binding to the homodimeric MJ0796 protein: a computational study of a prokaryotic ABC transporter NBD dimer. FEBS Lett. 579 (2005) 4193-4199
5. Chen J., Lu G., Lin J., Davidson A.L., and Quiocho F.A. A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol. Cell 12 (2003) 651-661
6. Chen M., Abele R., and Tampe R. Peptides induce ATP hydrolysis at both subunits of the transporter associated with antigen processing. J. Biol. Chem. 278 (2003) 29686-29692
7. Chen M., Abele R., and Tampe R. Functional non-equivalence of ATP-binding cassette signature motifs in the transporter associated with antigen processing (TAP). J. Biol. Chem. 279 (2004) 46073-46081
8. DeLano W.L. The PyMOL Molecular Graphics System (2002). http://www.pymol.org
9. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
10. Gao M., Cui H.R., Loe D.W., Grant C.E., Almquist K.C., Cole S.P., and Deeley R.G. Comparison of the functional characteristics of the nucleotide binding domains of multidrug resistance protein 1. J. Biol. Chem. 275 (2000) 13098-13108
11. Gaudet R., and Wiley D.C. Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J. 20 (2001) 4964-4972
12. Hewitt E.W., and Lehner P.J. The ABC-transporter signature motif is required for peptide translocation but not peptide binding by TAP. Eur. J. Immunol. 33 (2003) 422-427
13. Higgins C.F., and Linton K.J. The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 11 (2004) 918-926
14. Hopfner K.P., Karcher A., Shin D.S., Craig L., Arthur L.M., Carney J.P., and Tainer J.A. 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
15. Hung L.W., Wang I.X., Nikaido K., Liu P.Q., Ames G.F., and Kim S.H. Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396 (1998) 703-707
16. Jin X., Touhey J., and Gaudet R. Structure of the N-terminal ankyrin repeat domain of the TRPV2 ion channel. J. Biol. Chem. 281 (2006) 25006-25010
17. Jones P.M., and George A.M. Subunit interactions in ABC transporters: towards a functional architecture. FEMS Microbiol. Lett. 179 (1999) 187-202
18. Jones P.M., and George A.M. The ABC transporter structure and mechanism: perspectives on recent research. Cell. Mol. Life Sci. 61 (2004) 682-699
19. Karpowich N., Martsinkevich O., Millen L., Yuan Y.R., Dai P.L., MacVey K., Thomas P.J., and Hunt J.F. 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
20. Karttunen J.T., Lehner P.J., Gupta S.S., Hewitt E.W., and Cresswell P. Distinct functions and cooperative interaction of the subunits of the transporter associated with antigen processing (TAP). Proc. Natl. Acad. Sci. USA 98 (2001) 7431-7436
21. Kelly A., Powis S.H., Kerr L.A., Mockridge I., Elliott T., Bastin J., Uchanska-Ziegler B., Ziegler A., Trowsdale J., and Townsend A. Assembly and function of the two ABC transporter proteins encoded in the human major histocompatibility complex. Nature 355 (1992) 641-644
22. Koch J., Guntrum R., Heintke S., Kyritsis C., and Tampe R. Functional dissection of the transmembrane domains of the transporter associated with antigen processing (TAP). J. Biol. Chem. 279 (2004) 10142-10147
23. Lamzin V.S., and Wilson K.S. Automated refinement of protein models. Acta Crystallogr. D Biol. Crystallogr. 49 (1993) 129-147
24. Lapinski P.E., Neubig R.R., and Raghavan M. Walker A lysine mutations of TAP1 and TAP2 interfere with peptide translocation but not peptide binding. J. Biol. Chem. 276 (2001) 7526-7533
25. Lapinski P.E., Raghuraman G., and Raghavan M. Nucleotide interactions with membrane-bound transporter associated with antigen processing proteins. J. Biol. Chem. 278 (2003) 8229-8237
26. Lauvau G., Gubler B., Cohen H., Daniel S., Caillat-Zucman S., and van Endert P.M. Tapasin enhances assembly of transporters associated with antigen processing-dependent and -independent peptides with HLA-A2 and HLA-B27 expressed in insect cells. J. Biol. Chem. 274 (1999) 31349-31358
27. Locher K.P., Lee A.T., and Rees D.C. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296 (2002) 1091-1098
28. Maegley K.A., Admiraal S.J., and Herschlag D. Ras-catalyzed hydrolysis of GTP: a new perspective from model studies. Proc. Natl. Acad. Sci. USA 93 (1996) 8160-8166
29. Moody J.E., Millen L., Binns D., Hunt J.F., and Thomas P.J. Cooperative, ATP-dependent association of the nucleotide binding cassettes during the catalytic cycle of ATP-binding cassette transporters. J. Biol. Chem. 277 (2002) 21111-21114
30. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53 (1997) 240-255
31. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
32. Payen L.F., Gao M., Westlake C.J., Cole S.P., and Deeley R.G. Role of carboxylate residues adjacent to the conserved core Walker B motifs in the catalytic cycle of multidrug resistance protein 1 (ABCC1). J. Biol. Chem. 278 (2003) 38537-38547
33. Potter T.A., Rajan T.V., Dick II R.F., and Bluestone J.A. Substitution at residue 227 of H-2 class I molecules abrogates recognition by CD8-dependent, but not CD8-independent, cytotoxic T lymphocytes. Nature 337 (1989) 73-75
34. Powis S.J., Townsend A.R., Deverson E.V., Bastin J., Butcher G.W., and Howard J.C. Restoration of antigen presentation to the mutant cell line RMA-S by an MHC-linked transporter. Nature 354 (1991) 528-531
35. Procko E., Raghuraman G., Wiley D.C., Raghavan M., and Gaudet R. Identification of domain boundaries within the N-termini of TAP1 and TAP2 and their importance in tapasin binding and tapasin-mediated increase in peptide loading of MHC class I. Immunol. Cell Biol. 83 (2005) 475-482
36. Reyes C.L., and Chang G. Structure of the ABC transporter MsbA in complex with ADP.vanadate and lipopolysaccharide. Science 308 (2005) 1028-1031
37. Sadasivan B., Lehner P.J., Ortmann B., Spies T., and Cresswell P. Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 5 (1996) 103-114
38. Salter R.D., Norment A.M., Chen B.P., Clayberger C., Krensky A.M., Littman D.R., and Parham P. Polymorphism in the alpha 3 domain of HLA-A molecules affects binding to CD8. Nature 338 (1989) 345-347
39. Senior A.E., al-Shawi M.K., and Urbatsch I.L. The catalytic cycle of P-glycoprotein. FEBS Lett. 377 (1995) 285-289
40. Smith P.C., Karpowich N., Millen L., Moody J.E., Rosen J., Thomas P.J., and Hunt J.F. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell 10 (2002) 139-149
41. Spies T., and DeMars R. Restored expression of major histocompatibility class I molecules by gene transfer of a putative peptide transporter. Nature 351 (1991) 323-324
42. Stam N.J., Vroom T.M., Peters P.J., Pastoors E.B., and Ploegh H.L. HLA-A- and HLA-B-specific monoclonal antibodies reactive with free heavy chains in western blots, in formalin-fixed, paraffin-embedded tissue sections and in cryo-immuno-electron microscopy. Int. Immunol. 2 (1990) 113-125
43. Vagin A., and Teplyakov A. An approach to multi-copy search in molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 56 (2000) 1622-1624
44. van Endert P.M., Saveanu L., Hewitt E.W., and Lehner P. Powering the peptide pump: TAP crosstalk with energetic nucleotides. Trends Biochem. Sci. 27 (2002) 454-461
45. van Endert P.M., Tampe R., Meyer T.H., Tisch R., Bach J.F., and McDevitt H.O. A sequential model for peptide binding and transport by the transporters associated with antigen processing. Immunity 1 (1994) 491-500
46. Verdon G., Albers S.V., van Oosterwijk N., Dijkstra B.W., Driessen A.J., and Thunnissen A.M. Formation of the productive ATP-Mg2+-bound dimer of GlcV, an ABC-ATPase from Sulfolobus solfataricus. J. Mol. Biol. 334 (2003) 255-267
47. Wyatt P.J. Light scattering and the absolute characterization of macromolecules. Anal. Chim. Acta 272 (1993) 1-40
48. Zaitseva J., Jenewein S., Jumpertz T., Holland I.B., and Schmitt L. H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J. 24 (2005) 1901-1910