The mechanism of ABC transporters: General lessons from structural and functional studies of an antigenic peptide transporter

FASEB Journal

Volumn 23, Issue 5, 2009, Pages 1287-1302

  Procko, Erik ^a   O'Mara, Megan L ^b   Drew Bennett, W F ^b   Peter Tieleman, D ^b   Gaudet, Rachelle ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Accessory domains; Asymmetry; ATP hydrolysis; ATPase; Homology model; Membrane protein structure

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; CARRIER PROTEINS AND BINDING PROTEINS; NUCLEOTIDE BINDING PROTEIN; PEPTIDE TRANSPORTER 1; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING; UNCLASSIFIED DRUG;

ANTIGENICITY; CRYSTAL STRUCTURE; DIMERIZATION; HUMAN; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN TRANSPORT; REVIEW; STRUCTURE ANALYSIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; DIMERIZATION; HUMANS; MODELS, MOLECULAR; PEPTIDES; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS);

EID: 70349333637     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-121855     Document Type: Review

References (108)

1. Biemans-Oldehinkel, E., Doeven, M. K., and Poolman, B. (2006) ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett. 580, 1023-1035 (Pubitemid 43186038)
2. Dawson, R. J., and Locher, K. P. (2006) Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185
3. 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 (Pubitemid 34517120)
4. 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 (Pubitemid 350190241)
5. 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
6. 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 (Pubitemid 46175517)
7. 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 (Pubitemid 46398672)
8. Hvorup, R. N., Goetz, B. A., Niederer, M., Hollenstein, K., Perozo, E., and Locher, K. P. (2007) Asymmetry in the structure of the ABC transporter-binding protein complex BtuCD-BtuF. Science 317, 1387-1390 (Pubitemid 47417478)
9. Gerber, S., Comellas-Bigler, M., Goetz, B. A., and Locher, K. P. (2008) Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science 321, 246-250 (Pubitemid 351989095)
10. Kadaba, N. S., Kaiser, J. T., Johnson, E., Lee, A., and Rees, D. C. (2008) The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science 321, 250-253 (Pubitemid 351989096)
11. Jardetzky, O. (1966) Simple allosteric model for membrane pumps. Nature 211, 969-970
12. Davidson, A. L., and Maloney, P. C. (2007) ABC transporters: how small machines do a big job. Trends Microbiol. 15, 448-455
13. Hollenstein, K., Dawson, R. J., and Locher, K. P. (2007) Structure and mechanism of ABC transporter proteins. Curr. Opin. Struct. Biol. 17, 412-418 (Pubitemid 47451766)
14. Sonne, J., Kandt, C., Peters, G. H., Hansen, F. Y., Jensen, M. O., and Tieleman, D. P. (2007) Simulation of the coupling between nucleotide binding and transmembrane domains in the ATP binding cassette transporter BtuCD. Biophys. J. 92, 2727-2734 (Pubitemid 46557848)
15. Procko, E., Ferrin-O'Connell, I., Ng, S. L., and Gaudet, R. (2006) Distinct structural and functional properties of the ATPase sites in an asymmetric ABC transporter. Mol. Cell 24, 51-62 (Pubitemid 44466678)
16. Bahram, S., Arnold, D., Bresnahan, M., Strominger, J. L., and Spies, T. (1991) Two putative subunits of a peptide pump encoded in the human major histocompatibility complex class II region. Proc. Natl. Acad. Sci. U. S. A. 88, 10094-10098 (Pubitemid 21915781)
17. Kleijmeer, M. J., Kelly, A., Geuze, H. J., Slot, J. W., Townsend, A., and Trowsdale, J. (1992) Location of MHC-encoded transporters in the endoplasmic reticulum and cis-Golgi. Nature 357, 342-344
18. Powis, S. J., Townsend, A. R., Deverson, E. V., Bastin, J., Butcher, G. W., and Howard, J. C. (1991) Restoration of antigen presentation to the mutant cell line RMA-S by an MHC-linked transporter. Nature 354, 528-531 (Pubitemid 21896833)
19. Spies, T., and DeMars, R. (1991) Restored expression of major histocompatibility class I molecules by gene transfer of a putative peptide transporter. Nature 351, 323-324 (Pubitemid 21896591)
20. Kelly, A., Powis, S. H., Kerr, L. A., Mockridge, I., Elliott, T., Bastin, J., Uchanska-Ziegler, B., Ziegler, A., Trowsdale, J., and Townsend, A. (1992) Assembly and function of the two ABC transporter proteins encoded in the human major histocompatibility complex. Nature 355, 641-644
21. Spies, T., Cerundolo, V., Colonna, M., Cresswell, P., Townsend, A., and DeMars, R. (1992) Presentation of viral antigen by MHC class I molecules is dependent on a putative peptide transporter heterodimer. Nature 355, 644-646
22. Ortmann, B., Copeman, J., Lehner, P. J., Sadasivan, B., Herberg, J. A., Grandea, A. G., Riddell, S. R., Tampe, R., Spies, T., Trowsdale, J., and Cresswell, P. (1997) A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science 277, 1306-1309 (Pubitemid 27449083)
23. Rufer, E., Leonhardt, R. M., and Knittler, M. R. (2007) Molecular architecture of the TAP-associated MHC class I peptide-loading complex. J. Immunol. 179, 5717-5727
24. Bangia, N., Lehner, P. J., Hughes, E. A., Surman, M., and Cresswell, P. (1999) The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur. J. Immunol. 29, 1858-1870 (Pubitemid 29265541)
25. Lehner, P. J., Surman, M. J., and Cresswell, P. (1998) Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line. 220. Immunity 8, 221-231
26. Yang, T., Lapinski, P. E., Zhao, H., Zhou, Q., Zhang, H., Raghavan, M., Liu, Y., and Zheng, P. (2005) A rare transporter associated with antigen processing polymorphism overpresented in HLAlow colon cancer reveals the functional significance of the signature domain in antigen processing. Clin. Cancer Res. 11, 3614-3623 (Pubitemid 40685576)
27. Seliger, B., Ritz, U., Abele, R., Bock, M., Tampe, R., Sutter, G., Drexler, I., Huber, C., and Ferrone, S. (2001) Immune escape of melanoma: first evidence of structural alterations in two distinct components of the MHC class I antigen processing pathway. Cancer Res. 61, 8647-8650 (Pubitemid 34013870)
28. Tomazin, R., Hill, A. B., Jugovic, P., York, I., van Endert, P., Ploegh, H. L., Andrews, D. W., and Johnson, D. C. (1996) Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. EMBO J. 15, 3256-3266 (Pubitemid 26231931)
29. Ahn, K., Meyer, T. H., Uebel, S., Sempe, P., Djaballah, H., Yang, Y., Peterson, P. A., Fruh, K., and Tampe, R. (1996) Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J. 15, 3247-3255 (Pubitemid 26231930)
30. Kyritsis, C., Gorbulev, S., Hutschenreiter, S., Pawlitschko, K., Abele, R., and Tampe, R. (2001) Molecular mechanism and structural aspects of transporter associated with antigen processing inhibition by the cytomegalovirus protein US6. J. Biol. Chem. 276, 48031-48039 (Pubitemid 37370704)
31. Hewitt, E. W., Gupta, S. S., and Lehner, P. J. (2001) The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J. 20, 387-396
32. Kage, K., Tsukahara, S., Sugiyama, T., Asada, S., Ishikawa, E., Tsuruo, T., and Sugimoto, Y. (2002) Dominant-negative inhibition of breast cancer resistance protein as drug efflux pump through the inhibition of S-S dependent homodimerization. Int. J. Cancer 97, 626-630 (Pubitemid 34087801)
33. Bhatia, A., Schafer, H. J., and Hrycyna, C. A. (2005) Oligomerization of the human ABC transporter ABCG2: evaluation of the native protein and chimeric dimers. Biochemistry 44, 10893-10904 (Pubitemid 41153650)
34. Decottignies, A., and Goffeau, A. (1997) Complete inventory of the yeast ABC proteins. Nat. Genet. 15, 137-145 (Pubitemid 27061632)
35. Lubelski, J., van Merkerk, R., Konings, W. N., and Driessen, A. J. (2006) Nucleotide-binding sites of the heterodimeric LmrCD ABC-multidrug transporter of Lactococcus lactis are asymmetric. Biochemistry 45, 648-656 (Pubitemid 43100429)
36. Bohm, A., Diez, J., Diederichs, K., Welte, W., and Boos, W. (2002) Structural model of MalK, the ABC subunit of the maltose transporter of Escherichia coli: implications for mal gene regulation, inducer exclusion, and subunit assembly. J. Biol. Chem. 277, 3708-3717 (Pubitemid 34953245)
37. Chen, J., Lu, G., Lin, J., Davidson, A. L., and Quiocho, F. A. (2003) A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol. Cell 12, 651-661 (Pubitemid 37222486)
38. 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 (Pubitemid 40314897)
39. 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)
40. Koch, J., Guntrum, R., Heintke, S., Kyritsis, C., and Tampe, R. (2004) Functional dissection of the transmembrane domains of the transporter associated with antigen processing (TAP). J. Biol. Chem. 279, 10142-10147 (Pubitemid 38372619)
41. Procko, E., Raghuraman, G., Wiley, D. C., Raghavan, M., and Gaudet, R. (2005) 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, 475-482 (Pubitemid 41805748)
42. Tan, P., Kropshofer, H., Mandelboim, O., Bulbuc, N., Hammerling, G. J., and Momburg, F. (2002) Recruitment of MHC class I molecules by tapasin into the transporter associated with antigen processing-associated complex is essential for optimal peptide loading. J. Immunol. 168, 1950-1960 (Pubitemid 34135798)
43. Sadasivan, B., Lehner, P. J., Ortmann, B., Spies, T., and Cresswell, P. (1996) Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 5, 103-114 (Pubitemid 26301087)
44. Bryan, J., Vila-Carriles, W. H., Zhao, G., Babenko, A. P., and Aguilar-Bryan, L. (2004) Toward linking structure with function in ATP-sensitive K+ channels. Diabetes 53(Suppl. 3), S104-S112 (Pubitemid 39564531)
45. Babenko, A. P., and Bryan, J. (2003) Sur domains that associate with and gate KATP pores define a novel gatekeeper. J. Biol. Chem. 278, 41577-41580
46. Chan, K. W., Zhang, H., and Logothetis, D. E. (2003) N-terminal transmembrane domain of the SUR controls trafficking and gating of Kir6 channel subunits. EMBO J. 22, 3833-3843 (Pubitemid 36975711)
47. Moody, J. E., and Thomas, P. J. (2005) Nucleotide binding domain interactions during the mechanochemical reaction cycle of ATP-binding cassette transporters. J. Bioenerg. Biomembr. 37, 475-479
48. Oswald, C., Holland, I. B., and Schmitt, L. (2006) The motor domains of ABC-transporters. What can structures tell us? Naunyn Schmiedebergs Arch. Pharmacol. 372, 385-399
49. 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 (Pubitemid 29003952)
50. 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 (Pubitemid 34876568)
51. 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
52. Walker, J. E., Saraste, M., Runswick, M. J., and Gay, N. J. (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1, 945-951
53. Jones, P. M., and George, A. M. (1999) Subunit interactions in ABC transporters: towards a functional architecture. FEMS Microbiol. Lett. 179, 187-202
54. Procko, E., and Gaudet, R. (2008) Functionally important interactions between the nucleotide-binding domains of an antigenic peptide transporter. Biochemistry 47, 5699-5708 (Pubitemid 351747048)
55. Ye, J., Osborne, A. R., Groll, M., and Rapoport, T. A. (2004) RecA-like motor ATPases-lessons from structures. Biochim. Biophys. Acta 1659, 1-18
56. Perria, C. L., Rajamanickam, V., Lapinski, P. E., and Raghavan, M. (2006) Catalytic site modifications of TAP1 and TAP2 and their functional consequences. J. Biol. Chem. 281, 39839-39851 (Pubitemid 46041787)
57. Alberts, P., Daumke, O., Deverson, E. V., Howard, J. C., and Knittler, M. R. (2001) Distinct functional properties of the TAP subunits coordinate the nucleotide-dependent transport cycle. Curr. Biol. 11, 242-251 (Pubitemid 32185326)
58. Lapinski, P. E., Neubig, R. R., and Raghavan, M. (2001) Walker A lysine mutations of TAP1 and TAP2 interfere with peptide translocation but not peptide binding. J. Biol. Chem. 276, 7526-7533 (Pubitemid 37392065)
59. Karttunen, J. T., Lehner, P. J., Gupta, S. S., Hewitt, E. W., and Cresswell, P. (2001) Distinct functions and cooperative interaction of the subunits of the transporter associated with antigen processing (TAP). Proc. Natl. Acad. Sci. U. S. A. 98, 7431-7436
60. Park, S., Lim, B. B., Perez-Terzic, C., Mer, G., and Terzic, A. (2008) Interaction of asymmetric ABCC9-encoded nucleotide binding domains determines KATP channel SUR2A catalytic activity. J. Proteome Res. 7, 1721-1728
61. Jha, S., Dabas, N., Karnani, N., Saini, P., and Prasad, R. (2004) ABC multidrug transporter Cdr1p of Candida albicans has divergent nucleotide-binding domains which display functional asymmetry. FEMS Yeast Res. 5, 63-72 (Pubitemid 39307049)
62. Zhang, D. W., Graf, G. A., Gerard, R. D., Cohen, J. C., and Hobbs, H. H. (2006) Functional asymmetry of nucleotide-binding domains in ABCG5 and ABCG8. J. Biol. Chem. 281, 4507-4516
63. Basso, C., Vergani, P., Nairn, A. C., and Gadsby, D. C. (2003) Prolonged nonhydrolytic interaction of nucleotide with CFTR's NH2-terminal nucleotide binding domain and its role in channel gating. J. Gen. Physiol. 122, 333-348 (Pubitemid 37163281)
64. Ernst, R., Kueppers, P., Klein, C. M., Schwarzmueller, T., Kuchler, K., and Schmitt, L. (2008) A mutation of the H-loop selectively affects rhodamine transport by the yeast multidrug ABC transporter Pdr5. Proc. Natl. Acad. Sci. U. S. A. 105, 5069-5074 (Pubitemid 351738511)
65. Gao, M., Cui, H. R., Loe, D. W., Grant, C. E., Almquist, K. C., Cole, S. P., and Deeley, R. G. (2000) Comparison of the functional characteristics of the nucleotide binding domains of multidrug resistance protein 1. J. Biol. Chem. 275, 13098-13108 (Pubitemid 30241472)
66. Vergani, P., Nairn, A. C., and Gadsby, D. C. (2003) On the mechanism of MgATP-dependent gating of CFTR Cl- channels. J. Gen. Physiol. 121, 17-36 (Pubitemid 36133934)
67. Hou, Y., Cui, L., Riordan, J. R., and Chang, X. (2000) Allosteric interactions between the two non-equivalent nucleotide binding domains of multidrug resistance protein MRP1. J. Biol. Chem. 275, 20280-20287 (Pubitemid 30457601)
68. Dietrich, D., Schmuths, H., De Marcos Lousa, C., Baldwin, J. M., Baldwin, S. A., Baker, A., Theodoulou, F. L., and Holdsworth, M. J. (2008) Mutations in the arabidopsis peroxisomal ABC transporter COMATOSE allow differentiation between multiple functions in planta: insights from an allelic series. [E-pub ahead of print] Mol. Biol. Cell 10.1091/mbc.E08-07-0745
69. Linder, J. U. (2006) Class III adenylyl cyclases: molecular mechanisms of catalysis and regulation. Cell. Mol. Life Sci. 63, 1736-1751 (Pubitemid 44223083)
70. Sinha, S. C., and Sprang, S. R. (2006) Structures, mechanism, regulation and evolution of class III nucleotidyl cyclases. Rev. Physiol. Biochem. Pharmacol. 157, 105-140 (Pubitemid 44816532)
71. Liu, Y., Ruoho, A. E., Rao, V. D., and Hurley, J. H. (1997) Catalytic mechanism of the adenylyl and guanylyl cyclases: modeling and mutational analysis. Proc. Natl. Acad. Sci. U. S. A. 94, 13414-13419 (Pubitemid 28009596)
72. Pakotiprapha, D., Inuzuka, Y., Bowman, B. R., Moolenaar, G. F., Goosen, N., Jeruzalmi, D., and Verdine, G. L. (2008) Crystal structure of Bacillus stearothermophilus UvrA provides insight into ATP-modulated dimerization, UvrB interaction, and DNA binding. Mol. Cell 29, 122-133
73. Karcher, A., Buttner, K., Martens, B., Jansen, R. P., and Hopfner, K. P. (2005) X-ray structure of RLI, an essential twin cassette ABC ATPase involved in ribosome biogenesis and HIV capsid assembly. Structure 13, 649-659 (Pubitemid 40503328)
74. 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 (Pubitemid 44141799)
75. Kreimer, D. I., Chai, K. P., and Ferro-Luzzi Ames, G. (2000) Nonequivalence of the nucleotide-binding subunits of an ABC transporter, the histidine permease, and conformational changes in the membrane complex. Biochemistry 39, 14183-14195
76. Campbell, J. D., and Sansom, M. S. (2005) Nucleotide binding to the homodimeric MJ0796 protein: a computational study of a prokaryotic ABC transporter NBD dimer. FEBS Lett. 579, 4193-4199
77. Higgins, C. F., and Linton, K. J. (2004) The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 11, 918-926
78. Janas, E., Hofacker, M., Chen, M., Gompf, S., van der Does, C., and Tampe, R. (2003) The ATP hydrolysis cycle of the nucleotide-binding domain of the mitochondrial ATP-binding cassette transporter Mdl1p. J. Biol. Chem. 278, 26862-26869 (Pubitemid 36876837)
79. Oloo, E. O., Fung, E. Y., and Tieleman, D. P. (2006) The dynamics of the MgATP-driven closure of MalK, the energy-transducing subunit of the maltose ABC transporter. J. Biol. Chem. 281, 28397-28407
80. Oloo, E. O., and Tieleman, D. P. (2004) Conformational transitions induced by the binding of MgATP to the vitamin B12 ATP-binding cassette (ABC) transporter BtuCD. J. Biol. Chem. 279, 45013-45019
81. Jones, P. M., and George, A. M. (2008) Opening of the ADP-bound active site in the ABC transporter ATPase dimer: evidence for a constant contact, alternating sites model for the catalytic cycle. [E-pub ahead of print] Proteins doi:10.1002/prot.22250
82. Herget, M., Oancea, G., Schrodt, S., Karas, M., Tampe, R., and Abele, R. (2007) Mechanism of substrate sensing and signal transmission within an ABC transporter: use of a Trojan horse strategy. J. Biol. Chem. 282, 3871-3880 (Pubitemid 47084466)
83. Chen, M., Abele, R., and Tampe, R. (2003) Peptides induce ATP hydrolysis at both subunits of the transporter associated with antigen processing. J. Biol. Chem. 278, 29686-29692 (Pubitemid 36962354)
84. Gadsby, D. C., Vergani, P., and Csanady, L. (2006) The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440, 477-483
85. Hou, Y. X., Riordan, J. R., and Chang, X. B. (2003) ATP binding, not hydrolysis, at the first nucleotide-binding domain of multidrug resistance-associated protein MRP1 enhances ADP. Vi trapping at the second domain. J. Biol. Chem. 278, 3599-3605
86. Benabdelhak, H., Schmitt, L., Horn, C., Jumel, K., Blight, M. A., and Holland, I. B. (2005) Positive co-operative activity and dimerization of the isolated ABC ATPase domain of HlyB from Escherichia coli. Biochem. J. 386, 489-495 (Pubitemid 40445873)
87. Liu, C. E., Liu, P. Q., and Ames, G. F. (1997) Characterization of the adenosine triphosphatase activity of the periplasmic histidine permease, a traffic ATPase (ABC transporter). J. Biol. Chem. 272, 21883-21891
88. Davidson, A. L., Laghaeian, S. S., and Mannering, D. E. (1996) The maltose transport system of Escherichia coli displays positive cooperativity in ATP hydrolysis. J. Biol. Chem. 271, 4858-4863
89. 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)
90. Bouabe, H., and Knittler, M. R. (2003) The distinct nucleotide binding states of the transporter associated with antigen processing (TAP) are regulated by the nonhomologous C-terminal tails of TAP1 and TAP2. Eur. J. Biochem. 270, 4531-4546 (Pubitemid 37452530)
91. Lapinski, P. E., Raghuraman, G., and Raghavan, M. (2003) Nucleotide interactions with membrane-bound transporter associated with antigen processing proteins. J. Biol. Chem. 278, 8229-8237 (Pubitemid 36800567)
92. Ahn, J., Beharry, S., Molday, L. L., and Molday, R. S. (2003) Functional interaction between the two halves of the photoreceptor-specific ATP binding cassette protein ABCR (ABCA4). Evidence for a non-exchangeable ADP in the first nucleotide binding domain. J. Biol. Chem. 278, 39600-39608 (Pubitemid 37248519)
93. Matsuo, M., Tanabe, K., Kioka, N., Amachi, T., and Ueda, K. (2000) Different binding properties and affinities for ATP and ADP among sulfonylurea receptor subtypes, SUR1, SUR2A, and SUR2B. J. Biol. Chem. 275, 28757-28763 (Pubitemid 30704211)
94. Matsuoka, T., Matsushita, K., Katayama, Y., Fujita, A., Inageda, K., Tanemoto, M., Inanobe, A., Yamashita, S., Matsuzawa, Y., and Kurachi, Y. (2000) C-terminal tails of sulfonylurea receptors control ADP-induced activation and diazoxide modulation of ATP-sensitive K(+) channels. Circ. Res. 87, 873-880 (Pubitemid 30943824)
95. Deverson, E. V., Leong, L., Seelig, A., Coadwell, W. J., Tredgett, E. M., Butcher, G. W., and Howard, J. C. (1998) Functional analysis by site-directed mutagenesis of the complex polymorphism in rat transporter associated with antigen processing. J. Immunol. 160, 2767-2779 (Pubitemid 28136730)
96. Momburg, F., Armandola, E. A., Post, M., and Hammerling, G. J. (1996) Residues in TAP2 peptide transporters controlling substrate specificity. J. Immunol. 156, 1756-1763 (Pubitemid 26069307)
97. Senior, A. E., al-Shawi, M. K., and Urbatsch, I. L. (1995) The catalytic cycle of P-glycoprotein. FEBS Lett. 377, 285-289
98. Al-Shawi, M. K., and Omote, H. (2005) The remarkable transport mechanism of P-glycoprotein: a multidrug transporter. J. Bioenerg. Biomembr. 37, 489-496 (Pubitemid 43725181)
99. Grote, M., Bordignon, E., Polyhach, Y., Jeschke, G., Steinhoff, H. J., and Schneider, E. (2008) A comparative EPR study of the nucleotide-binding domains' catalytic cycle in the assembled maltose ABC-importer. Biophys. J. 95, 2924-2938
100. Orelle, C., Ayvaz, T., Everly, R. M., Klug, C. S., and Davidson, A. L. (2008) Both maltose-binding protein and ATP are required for nucleotide-binding domain closure in the intact maltose ABC transporter. Proc. Natl. Acad. Sci. U. S. A. 105, 12837-12842
101. Weng, J., Ma, J., Fan, K., and Wang, W. (2008) The conformational coupling and translocation mechanism of vitamin B12 ATP-binding cassette transporter BtuCD. Biophys. J. 94, 612-621
102. Schrodt, S., Koch, J., and Tampe, R. (2006) Membrane topology of the transporter associated with antigen processing (TAP1) within an assembled functional peptide-loading complex. J. Biol. Chem. 281, 6455-6462 (Pubitemid 43847578)
103. Bakos, E., Evers, R., Szakacs, G., Tusnady, G. E., Welker, E., Szabo, K., de Haas, M., van Deemter, L., Borst, P., Varadi, A., and Sarkadi, B. (1998) Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J. Biol. Chem. 273, 32167-32175 (Pubitemid 29177162)
104. Peelman, F., Labeur, C., Vanloo, B., Roosbeek, S., Devaud, C., Duverger, N., Denefle, P., Rosier, M., Vandekerckhove, J., and Rosseneu, M. (2003) Characterization of the ABCA transporter subfamily: identification of prokaryotic and eukaryotic members, phylogeny and topology. J. Mol. Biol. 325, 259-274 (Pubitemid 36062687)
105. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (Pubitemid 24007801)
106. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723 (Pubitemid 28059943)
107. Van der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and Berendsen, H. J. (2005) GROMACS: fast, flexible, and free. J. Comput. Chem. 26, 1701-1718
108. DeLano, W. L. (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, U. S. A. http://www.pymol.org