Multidrug resistance ABC transporter structure predictions by homology modeling approaches

Current Drug Metabolism

Volumn 12, Issue 3, 2011, Pages 268-277

  Honorat, Mylène ^a,b   Falson, Pierre ^c   Terreux, Raphael ^c   Di Pietro, Attilio ^c   Dumontet, Charles ^a,b   Payen, Léa ^a,b,d,e  

^a UNIVERSITÉ LYON 1   (France)

^b CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^c INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^d HOSPICES CIVILS DE LYON   (France)

^e INSERM   (France)

Author keywords

3D Structure; ABC transporter; Docking; Drug Disposition; Homology; Human; Modeling; Multidrug resistance

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER C1; ABC TRANSPORTER C4; ABC TRANSPORTER C5; BREAST CANCER RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; UNCLASSIFIED DRUG;

ARTICLE; BIOCHEMISTRY; CATALYSIS; CRYSTAL STRUCTURE; DRUG DESIGN; DRUG IDENTIFICATION; DRUG STRUCTURE; GENOME; GENOME ANALYSIS; HUMAN; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MULTIDRUG RESISTANCE; NONHUMAN; PROTEIN TRANSPORT;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BINDING SITES; DRUG DESIGN; DRUG RESISTANCE, MULTIPLE; HUMANS; PHARMACOKINETICS; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 79953649285     PISSN: 13892002     EISSN: None     Source Type: Journal    
DOI: 10.2174/138920011795101804     Document Type: Article

References (60)

1. Scherrmann, J.M. Expression and function of multidrug resistance transporters at the blood-brain barriers. Expert Opin. Drug Metab. Toxicol., 2005, 1, 233-246.
2. Klaassen, C.D.; Aleksunes, L.M. Xenobiotic, bile acid, and cholesterol transporters: function and regulation. Pharmacol. Rev., 62, 1-96.
3. Oostendorp, R.L.; Beijnen, J.H.; Schellens, J.H. The biological and clinical role of drug transporters at the intestinal barrier. Cancer Treat Rev., 2009, 35, 137-147.
4. Benderra, Z.; Faussat, A.M.; Sayada, L.; Perrot, J.Y.; Tang, R.; Chaoui, D.; Morjani, H.; Marzac, C.; Marie, J.P.; Legrand, O. MRP3, BCRP, and P-glycoprotein activities are prognostic factors in adult acute myeloid leukemia. Clin. Cancer Res., 2005, 11, 7764-7772. (Pubitemid 41611620)
5. Benderra, Z.; Faussat, A.M.; Sayada, L.; Perrot, J.Y.; Chaoui, D.; Marie, J.P.; Legrand, O. Breast cancer resistance protein and Pglycoprotein in 149 adult acute myeloid leukemias. Clin. Cancer Res., 2004, 10, 7896-7902. (Pubitemid 39587528)
6. Honorat, M.; Guitton, J.; Dumontet, C.; Payen, L. Expression level and hormonal regulation of ABC transporters in breast cancer. Current cancer therapy review, 2010, in press.
7. Larbcharoensub, N.; Leopairat, J.; Sirachainan, E.; Narkwong, L.; Bhongmakapat, T.; Rasmeepaisarn, K.; Janvilisri, T. Association between multidrug resistance-associated protein 1 and poor prognosis in patients with nasopharyngeal carcinoma treated with radiotherapy and concurrent chemotherapy. Hum. Pathol., 2008, 39, 837-845.
8. Noguchi, K.; Katayama, K.; Mitsuhashi, J.; Sugimoto, Y. Functions of the breast cancer resistance protein (BCRP/ABCG2) in chemotherapy. Adv. Drug Deliv. Rev., 2009, 61, 26-33.
9. Dean, M.; Rzhetsky, A.; Allikmets, R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res, 2001, 11, 1156-1166. (Pubitemid 32677289)
10. Bhatia, A.; Schafer, H.J.; Hrycyna, C.A. Oligomerization of the human ABC transporter ABCG2: evaluation of the native protein and chimeric dimers. Biochemistry, 2005, 44, 10893-10904. (Pubitemid 41153650)
11. Graf, G.A.; Li, W.P.; Gerard, R.D.; Gelissen, I.; White, A.; Cohen, J.C.; Hobbs, H.H. Coexpression of ATP-binding cassette proteins ABCG5 and ABCG8 permits their transport to the apical surface. J. Clin. Invest., 2002, 110, 659-669. (Pubitemid 34988790)
12. Aller, S.G.; Yu, J.; Ward, A.; Weng, Y.; Chittaboina, S.; Zhuo, R.; Harrell, P.M.; Trinh, Y.T.; Zhang, Q.; Urbatsch, I.L.; Chang, G. Structure of P-glycoprotein reveals a molecular basis for polyspecific drug binding. Science, 2009, 323, 1718-1722.
13. Dawson, R.J.; Locher, K.P. Structure of a bacterial multidrug ABC transporter. Nature, 2006, 443, 180-5. (Pubitemid 44387602)
14. Ward, A.; Reyes, C.L.; Yu, J.; Roth, C.B.; Chang, G. Flexibility in the ABC transporter MsbA: Alternating access with a twist. Proc. Natl. Acad. Sci. U S A, 2007, 104, 19005-19010.
15. Locher, K.P.; Lee, A.T.; Rees, D.C. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science, 2002, 296, 1091-1098. (Pubitemid 34517120)
16. Gerber, S.; Comellas-Bigler, M.; Goetz, B.A.; Locher, K.P. Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science, 2008, 321, 246-250. (Pubitemid 351989095)
17. Pinkett, H.W.; Lee, A.T.; Lum, P.; Locher, K.P.; Rees, D.C. An inward-facing conformation of a putative metal-chelate-type ABC transporter. Science, 2007, 315, 373-377. (Pubitemid 46175517)
18. Oldham, M.L.; Khare, D.; Quiocho, F.A.; Davidson, A.L.; Chen, J. Crystal structure of a catalytic intermediate of the maltose transporter. Nature, 2007, 450, 515-521. (Pubitemid 350190241)
19. Kadaba, N.S.; Kaiser, J.T.; Johnson, E.; Lee, A.; Rees, D.C. The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science, 2008, 321, 250-253. (Pubitemid 351989096)
20. Kerr, I.D. Structure and association of ATP-binding cassette transporter nucleotide-binding domains. Biochim.Biophys. Acta, 2002, 1561, 47-64. (Pubitemid 34442244)
21. Seeger, M.A.; van Veen, H.W. Molecular basis of multidrug transport by ABC transporters. Biochim. Biophys. Acta, 2009, 1794, 725-737.
22. Jones, P.M.; George, A.M. Nucleotide-dependent allostery within the ABC transporter ATP-binding cassette: a computational study of the MJ0796 dimer. J. Biol. Chem., 2007, 282, 22793-22803. (Pubitemid 47267351)
23. Smith, C.A.; Rayment, I. X-ray structure of the magnesium( II).ADP.vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 A resolution. Biochemistry, 1996, 35, 5404-5417.
24. Smith, P.C.; Karpowich, N.; Millen, L.; Moody, J.E.; Rosen, J.; Thomas, P.J.; Hunt, J.F. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell, 2002, 10, 139-149. (Pubitemid 34876568)
25. Jones, P.M.; George, A.M. 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. Proteins, 2009, 75, 387-396.
26. Wen, P.C.; Tajkhorshid, E. Dimer opening of the nucleotide binding domains of ABC transporters after ATP hydrolysis. Biophys. J., 2008, 95, 5100-5110.
27. Oliveira, A.S.; Baptista, A.M.; Soares, C.M. Insights into the molecular mechanism of an ABC transporter: conformational changes in the NBD dimer of MJ0796. J. Phys. Chem. B., 114, 5486-5496.
28. Dawson, R.J.; Locher, K.P. Structure of the multidrug ABC transporterSav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett., 2007, 581, 935-938. (Pubitemid 46282725)
29. Ward, A.; Mulligan, S.; Carragher, B.; Chang, G.; Milligan, R.A. Nucleotide dependent packing differences in helical crystals of the ABC transporter MsbA. J. Struct. Biol., 2009, 165, 169-175.
30. Rosenberg, M.F.; Kamis, A.B.; Callaghan, R.; Higgins, C.F.; Ford, R.C. Three-dimensional structures of the mammalian multidrug resistance P-glycoprotein demonstrate major conformational changes in the transmembrane domains upon nucleotide binding. J. Biol. Chem., 2003, 278, 8294-8299. (Pubitemid 36800576)
31. Lee, J.Y.; Urbatsch, I.L.; Senior, A.E.; Wilkens, S. Nucleotideinduced structural changes in P-glycoprotein observed by electron microscopy. J. Biol. Chem., 2008, 283, 5769-79.
32. Urbatsch, I.L.; Beaudet, L.; Carrier, I.; Gros, P. Mutations in either nucleotide-binding site of P-glycoprotein (Mdr3) prevent vanadate trapping of nucleotide at both sites. Biochemistry, 1998, 37, 4592-602. (Pubitemid 28217177)
33. Lerner-Marmarosh, N.; Gimi, K.; Urbatsch, I.L.; Gros, P.; Senior, A.E. Large scale purification of detergent-soluble P-glycoprotein from Pichia pastoris cells and characterization of nucleotide binding properties of wild-type, Walker A, and Walker B mutant proteins. J. Biol. Chem., 1999, 274, 34711-8. (Pubitemid 129509511)
34. Urbatsch, I.L.; Wilke-Mounts, S.; Gimi, K.; Senior, A.E. Purification and characterization of N-glycosylation mutant mouse and human P-glycoproteins expressed in Pichia pastoris cells. Arch. Biochem. Biophys., 2001, 388, 171-7. (Pubitemid 32911576)
35. Ramaen, O.; Sizun, C.; Pamlard, O.; Jacquet, E.; Lallemand, J.Y. Attempts to characterize the NBD heterodimer of MRP1: transient complex formation involves Gly771 of the ABC signature sequence but does not enhance the intrinsic ATPase activity. Biochem. J., 2005, 391, 481-90. (Pubitemid 41634774)
36. Ramaen, O.; Leulliot, N.; Sizun, C.; Ulryck, N.; Pamlard, O.; Lallemand, J.Y.; Tilbeurgh, H.; Jacquet, E. Structure of the human multidrug resistance protein 1 nucleotide binding domain 1 bound to Mg2+/ATP reveals a non-productive catalytic site. J. Mol. Biol., 2006, 359, 940-9. (Pubitemid 43831921)
37. Payen, L.F.; Gao, M.; Westlake, C.J.; Cole, S.P.; 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, 2003, 278, 38537-47. (Pubitemid 37221749)
38. Thompson, J.D.; Higgins, D.G.; Gibson, T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 1994, 22, 4673-80. (Pubitemid 24354800)
39. Cserzo, M.; Wallin, E.; Simon, I.; von Heijne, G.; Elofsson, A. Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng., 1997, 10, 673-6. (Pubitemid 27332074)
40. Tusnady, G.E.; Simon, I. The HMMTOP transmembrane topology prediction server. Bioinformatics, 2001, 17, 849-50. (Pubitemid 32970487)
41. Rost, B.; Yachdav, G.; Liu, J. The PredictProtein server. Nucleic Acids Res, 2004, 32, W321-326. (Pubitemid 39004075)
42. Gouet, P.; Courcelle, E.; Stuart, D.I.; Metoz, F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics, 1999, 15, 305-308. (Pubitemid 29213756)
43. Sali, A.; Blundell, T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol., 1993, 234, 779-815. (Pubitemid 24007801)
44. Arnold, K.; Bordoli, L.; Kopp, J.; Schwede, T. The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics, 2006, 22, 195-201. (Pubitemid 43205406)
45. Van Der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A.E.; Berendsen, H.J. GROMACS: fast, flexible, and free. J. Comput. Chem., 2005, 26, 1701-1718.
46. Sippl, M.J. Recognition of errors in three-dimensional structures of proteins. Proteins, 1993, 17, 355-362. (Pubitemid 23358545)
47. Wallner, B.; Elofsson, A. Can correct protein models be identified? Protein Sci., 2003, 12, 1073-1086.
48. Hooft, R.W.; Vriend, G.; Sander, C.; Abola, E.E. Errors in protein structures. Nature, 1996, 381, 272.
49. Becker, J.P.; Depret, G.; Van Bambeke, F.; Tulkens, P.M.; Prevost, M. Molecular models of human P-glycoprotein in two different catalytic states. BMC. Struct. Biol., 2009, 9, 3.
50. Ravna, A.W.; Sylte, I.; Sager, G. Molecular model of the outward facing state of the human P-glycoprotein (ABCB1), and comparison to a model of the human MRP5 (ABCC5). Theor. Biol. Med. Model, 2007, 4, 33.
51. Stockner, T.; de Vries, S.J.; Bonvin, A.M.; Ecker, G.F.; Chiba, P. Data-driven homology modelling of P-glycoprotein in the ATPbound state indicates flexibility of the transmembrane domains. Febs J., 2009, 276, 964-972.
52. Ravna, A.W.; Sylte, I.; Sager, G. Binding site of ABC transporter homology models confirmed by ABCB1 crystal structure. Theor. Biol. Med. Model., 2009, 6, 20.
53. Mares-Samano, S.; Badhan, R.; Penny, J. Identification of putative steroid-binding sites in human ABCB1 and ABCG2. Eur. J .Med. Chem., 2009, 44, 3601-3611.
54. Pajeva, I.K.; Globisch, C.; Wiese, M. Comparison of the inwardand outward-open homology models and ligand binding of human P-glycoprotein. Febs J., 2009, 276, 7016-7026.
55. Rosenberg, M.F.; Mao, Q.; Holzenburg, A.; Ford, R.C.; Deeley, R.G.; Cole, S.P. The structure of the multidrug resistance protein 1 (MRP1/ABCC1). crystallization and single-particle analysis. J. Biol. Chem., 2001, 276, 16076-16082.
56. Ravna, A.W.; Sager, G. Molecular model of the outward facing state of the human multidrug resistance protein 4 (MRP4/ABCC4). Bioorg. Med. Chem. Lett., 2008, 18, 3481-3483. (Pubitemid 351787578)
57. Ravna, A.W.; Sylte, I.; Sager, G. A molecular model of a putative substrate releasing conformation of multidrug resistance protein 5 (MRP5). Eur. J. Med. Chem., 2008, 43, 2557-2567.
58. Li, Y.F.; Polgar, O.; Okada, M.; Esser, L.; Bates, S.E.; Xia, D. Towards understanding the mechanism of action of the multidrug resistance-linked half-ABC transporter ABCG2: a molecular modeling study. J. Mol. Graph Model, 2007, 25, 837-851. (Pubitemid 46216119)
59. Hazai, E.; Bikadi, Z. Homology modeling of breast cancer resistance protein (ABCG2). J. Struct. Biol., 2008, 162, 63-74.
60. DeGorter, M.K.; Conseil, G.; Deeley, R.G.; Campbell, R.L.; Cole, S.P. Molecular modeling of the human multidrug resistance protein 1 (MRP1/ABCC1). Biochem. Biophys. Res. Commun., 2008, 365, 29-34. (Pubitemid 350102450)