Mutations of the central tyrosines of putative cholesterol recognition amino acid consensus (CRAC) sequences modify folding, activity, and sterol-sensing of the human ABCG2 multidrug transporter

Biochimica et Biophysica Acta - Biomembranes

Volumn 1848, Issue 2, 2015, Pages 477-487

  Gál, Zita ^a   Hegedüs, Csilla ^a   Szakács, Gergely ^a   Váradi, András ^a   Sarkadi, Balázs ^a   Özvegy Laczka, Csilla ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

ABCG2; Bile acids; Cholesterol; Cholesterol recognition amino acid consensus; Multidrug resistance

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BILE ACID; BREAST CANCER RESISTANCE PROTEIN; CHOLESTEROL; TYROSINE DERIVATIVE; ABC TRANSPORTER; ABCG2 PROTEIN, HUMAN; PHENYLALANINE; RECOMBINANT PROTEIN; SERINE; TUMOR PROTEIN; TYROSINE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CHOLESTEROL RECOGNITION AMINO ACID CONSENSUS; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INSECT CELL; MAMMAL CELL; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN TRANSPORT; REGULATORY MECHANISM; STEROL SENSING; ANIMAL; CHEMISTRY; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN FOLDING; SF9 CELL LINE; SPODOPTERA;

AMINO ACID MOTIFS; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BILE ACIDS AND SALTS; CHOLESTEROL; CONSERVED SEQUENCE; GENE EXPRESSION; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NEOPLASM PROTEINS; PHENYLALANINE; PROTEIN FOLDING; RECOMBINANT PROTEINS; SERINE; SF9 CELLS; SPODOPTERA; TYROSINE;

EID: 84912083461     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.11.006     Document Type: Article

References (43)

1. B. Sarkadi, C. Ozvegy-Laczka, K. Nemet, and A. Varadi ABCG2 - a transporter for all seasons FEBS Lett. 567 2004 116 120
2. U. Henriksen, J.U. Fog, T. Litman, and U. Gether Identification of intra- and intermolecular disulfide bridges in the multidrug resistance transporter ABCG2 J. Biol. Chem. 280 2005 36926 36934
3. K. Noguchi, K. Katayama, and Y. Sugimoto Human ABC transporter ABCG2/BCRP expression in chemoresistance: basic and clinical perspectives for molecular cancer therapeutics Pharmgenomics Pers. Med. 7 2014 53 64
4. I.D. Kerr, A.J. Haider, and I.C. Gelissen The ABCG family of membrane-associated transporters: you don't have to be big to be mighty Br. J. Pharmacol. 164 2011 1767 1779
5. G. Szakacs, A. Varadi, C. Ozvegy-Laczka, and B. Sarkadi The role of ABC transporters in drug absorption, distribution, metabolism, excretion and toxicity (ADME-Tox) Drug Discov. Today 13 2008 379 393
6. P. Godoy, N.J. Hewitt, U. Albrecht, M.E. Andersen, N. Ansari, S. Bhattacharya, J.G. Bode, J. Bolleyn, C. Borner, J. Bottger, A. Braeuning, R.A. Budinsky, B. Burkhardt, N.R. Cameron, G. Camussi, C.S. Cho, Y.J. Choi, J. Craig Rowlands, U. Dahmen, G. Damm, O. Dirsch, M.T. Donato, J. Dong, S. Dooley, D. Drasdo, R. Eakins, K.S. Ferreira, V. Fonsato, J. Fraczek, R. Gebhardt, A. Gibson, M. Glanemann, C.E. Goldring, M.J. Gomez-Lechon, G.M. Groothuis, L. Gustavsson, C. Guyot, D. Hallifax, S. Hammad, A. Hayward, D. Haussinger, C. Hellerbrand, P. Hewitt, S. Hoehme, H.G. Holzhutter, J.B. Houston, J. Hrach, K. Ito, H. Jaeschke, V. Keitel, J.M. Kelm, B. Kevin Park, C. Kordes, G.A. Kullak-Ublick, E.L. LeCluyse, P. Lu, J. Luebke-Wheeler, A. Lutz, D.J. Maltman, M. Matz-Soja, P. McMullen, I. Merfort, S. Messner, C. Meyer, J. Mwinyi, D.J. Naisbitt, A.K. Nussler, P. Olinga, F. Pampaloni, J. Pi, L. Pluta, S.A. Przyborski, A. Ramachandran, V. Rogiers, C. Rowe, C. Schelcher, K. Schmich, M. Schwarz, B. Singh, E.H. Stelzer, B. Stieger, R. Stober, Y. Sugiyama, C. Tetta, W.E. Thasler, T. Vanhaecke, M. Vinken, T.S. Weiss, A. Widera, C.G. Woods, J.J. Xu, K.M. Yarborough, and J.G. Hengstler Recent advances in 2D and 3D in vitro systems using primary hepatocytes, alternative hepatocyte sources and non-parenchymal liver cells and their use in investigating mechanisms of hepatotoxicity, cell signaling and ADME Arch. Toxicol. 87 2013 1315 1530
7. O.M. Woodward, A. Kottgen, J. Coresh, E. Boerwinkle, W.B. Guggino, and M. Kottgen Identification of a urate transporter, ABCG2, with a common functional polymorphism causing gout Proc. Natl. Acad. Sci. U. S. A. 106 2009 10338 10342
8. A. Nakayama, H. Matsuo, T. Takada, K. Ichida, T. Nakamura, Y. Ikebuchi, K. Ito, T. Hosoya, Y. Kanai, H. Suzuki, and N. Shinomiya ABCG2 is a high-capacity urate transporter and its genetic impairment increases serum uric acid levels in humans Nucleosides Nucleotides Nucleic Acids 30 2011 1091 1097
9. A. Dehghan, A. Kottgen, Q. Yang, S.J. Hwang, W.L. Kao, F. Rivadeneira, E. Boerwinkle, D. Levy, A. Hofman, B.C. Astor, E.J. Benjamin, C.M. van Duijn, J.C. Witteman, J. Coresh, and C.S. Fox Association of three genetic loci with uric acid concentration and risk of gout: a genome-wide association study Lancet 372 2008 1953 1961
10. P. Krishnamurthy, and J.D. Schuetz The ABC transporter Abcg2/Bcrp: role in hypoxia mediated survival Biometals 18 2005 349 358
11. D. Turk, and G. Szakacs Relevance of multidrug resistance in the age of targeted therapy Curr. Opin. Drug Discov. Devel. 12 2009 246 252
12. R.W. Robey, P.R. Massey, L. Amiri-Kordestani, and S.E. Bates ABC transporters: unvalidated therapeutic targets in cancer and the CNS Anticancer Agents Med. Chem. 10 2010 625 633
13. K. Natarajan, Y. Xie, M.R. Baer, and D.D. Ross Role of breast cancer resistance protein (BCRP/ABCG2) in cancer drug resistance Biochem. Pharmacol. 83 2012 1084 1103
14. A. Pal, D. Mehn, E. Molnar, S. Gedey, P. Meszaros, T. Nagy, H. Glavinas, T. Janaky, O. von Richter, G. Bathori, L. Szente, and P. Krajcsi Cholesterol potentiates ABCG2 activity in a heterologous expression system: improved in vitro model to study function of human ABCG2 J. Pharmacol. Exp. Ther. 321 2007 1085 1094
15. A. Telbisz, C. Hegedus, A. Varadi, B. Sarkadi, and C. Ozvegy-Laczka Regulation of the Function of the Human ABCG2 Multidrug Transporter by Cholesterol and Bile Acids: Effects of Mutations in Potential Substrate and Steroid Binding Sites Drug Metab. Dispos. 42 2007 575 585
16. A. Telbisz, C. Ozvegy-Laczka, T. Hegedus, A. Varadi, and B. Sarkadi Effects of the lipid environment, cholesterol and bile acids on the function of the purified and reconstituted human ABCG2 protein Biochem. J. 450 2013 387 395
17. G.A. Graf, L. Yu, W.P. Li, R. Gerard, P.L. Tuma, J.C. Cohen, and H.H. Hobbs ABCG5 and ABCG8 are obligate heterodimers for protein trafficking and biliary cholesterol excretion J. Biol. Chem. 278 2003 48275 48282
18. N. Wang, L. Yvan-Charvet, D. Lutjohann, M. Mulder, T. Vanmierlo, T.W. Kim, and A.R. Tall ATP-binding cassette transporters G1 and G4 mediate cholesterol and desmosterol efflux to HDL and regulate sterol accumulation in the brain FASEB J. 22 2008 1073 1082
19. A. Telbisz, C. Hegedus, A. Varadi, B. Sarkadi, and C. Ozvegy-Laczka Regulation of the function of the human ABCG2 multidrug transporter by cholesterol and bile acids: effects of mutations in potential substrate and steroid binding sites Drug Metab. Dispos. 42 2014 575 585
20. S. Velamakanni, T. Janvilisri, S. Shahi, and H.W. van Veen A functional steroid-binding element in an ATP-binding cassette multidrug transporter Mol. Pharmacol. 73 2008 12 17
21. J.J. Lacapere, and V. Papadopoulos Peripheral-type benzodiazepine receptor: structure and function of a cholesterol-binding protein in steroid and bile acid biosynthesis Steroids 68 2003 569 585
22. R.M. Epand Proteins and cholesterol-rich domains Biochim. Biophys. Acta 1778 2008 1576 1582
23. R.M. Epand, B.G. Sayer, and R.F. Epand Caveolin scaffolding region and cholesterol-rich domains in membranes J. Mol. Biol. 345 2005 339 350
24. A. Midzak, G. Rammouz, and V. Papadopoulos Structure-activity relationship (SAR) analysis of a family of steroids acutely controlling steroidogenesis Steroids 77 2012 1327 1334
25. A.K. Singh, J. McMillan, A.N. Bukiya, B. Burton, A.L. Parrill, and A.M. Dopico Multiple cholesterol recognition/interaction amino acid consensus (CRAC) motifs in cytosolic C tail of Slo1 subunit determine cholesterol sensitivity of Ca2 + - and voltage-gated K + (BK) channels J. Biol. Chem. 287 2012 20509 20521
26. C. Ozvegy, A. Varadi, and B. Sarkadi Characterization of drug transport, ATP hydrolysis, and nucleotide trapping by the human ABCG2 multidrug transporter. Modulation of substrate specificity by a point mutation J. Biol. Chem. 277 2002 47980 47990
27. C. Ozvegy, T. Litman, G. Szakacs, Z. Nagy, S. Bates, A. Varadi, and B. Sarkadi Functional characterization of the human multidrug transporter, ABCG2, expressed in insect cells Biochem. Biophys. Res. Commun. 285 2001 111 117
28. H. Saranko, H. Tordai, A. Telbisz, C. Ozvegy-Laczka, G. Erdos, B. Sarkadi, and T. Hegedus Effects of the gout-causing Q141K polymorphism and a CFTR DeltaF508 mimicking mutation on the processing and stability of the ABCG2 protein Biochem. Biophys. Res. Commun. 437 2013 140 145
29. O. Kolacsek, V. Krizsik, A. Schamberger, Z. Erdei, A. Apati, G. Varady, L. Mates, Z. Izsvak, Z. Ivics, B. Sarkadi, and T.I. Orban Reliable transgene-independent method for determining Sleeping Beauty transposon copy numbers Mob. DNA 2 2011 5
30. E. Bakos, I. Klein, E. Welker, K. Szabo, M. Muller, B. Sarkadi, and A. Varadi Characterization of the human multidrug resistance protein containing mutations in the ATP-binding cassette signature region Biochem. J. 323 Pt 3 1997 777 783
31. M.F. Khan, T.L. Unruh, and J.P. Deans Implementation of a Flow Cytometry Strategy to Isolate and Assess Heterogeneous Membrane Raft Domains Flow Cytometry - Recent Perspectives 2012
32. C. Ozvegy-Laczka, G. Koblos, B. Sarkadi, and A. Varadi Single amino acid (482) variants of the ABCG2 multidrug transporter: major differences in transport capacity and substrate recognition Biochim. Biophys. Acta 1668 2005 53 63
33. C.H. Storch, R. Ehehalt, W.E. Haefeli, and J. Weiss Localization of the human breast cancer resistance protein (BCRP/ABCG2) in lipid rafts/caveolae and modulation of its activity by cholesterol in vitro J. Pharmacol. Exp. Ther. 323 2007 257 264
34. H. Li, and V. Papadopoulos Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern Endocrinology 139 1998 4991 4997
35. R.F. Epand, B.G. Sayer, and R.M. Epand The tryptophan-rich region of HIV gp41 and the promotion of cholesterol-rich domains Biochemistry 44 2005 5525 5531
36. S. Oddi, E. Dainese, F. Fezza, M. Lanuti, D. Barcaroli, V. De Laurenzi, D. Centonze, and M. Maccarrone Functional characterization of putative cholesterol binding sequence (CRAC) in human type-1 cannabinoid receptor J. Neurochem. 116 2011 858 865
37. G.M. Denning, M.P. Anderson, J.F. Amara, J. Marshall, A.E. Smith, and M.J. Welsh Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive Nature 358 1992 761 764
38. I. Zoernig, C. Ziegelmeier, B. Lahrmann, N. Grabe, D. Jager, and N. Halama Sequence mutations of the substrate binding pocket of stem cell factor and multidrug resistance protein ABCG2 in renal cell cancer: a possible link to treatment resistance Oncol. Rep. 29 2013 1697 1700
39. Z. Ni, Z. Bikadi, X. Cai, M.F. Rosenberg, and Q. Mao Transmembrane helices 1 and 6 of the human breast cancer resistance protein (BCRP/ABCG2): identification of polar residues important for drug transport Am. J. Physiol. Cell Physiol. 299 2010 C1100 C1109
40. B. Sarkadi, L. Homolya, G. Szakacs, and A. Varadi Human multidrug resistance ABCB and ABCG transporters: participation in a chemoimmunity defense system Physiol. Rev. 86 2006 1179 1236
41. E.J. Tarling, and P.A. Edwards ATP binding cassette transporter G1 (ABCG1) is an intracellular sterol transporter Proc. Natl. Acad. Sci. U. S. A. 108 2011 19719 19724
42. G.E. Tusnady, and I. Simon The HMMTOP transmembrane topology prediction server Bioinformatics 17 2001 849 850
43. L. Dobson, I. Reményi, and G.E. Tusnády The Human Transmembrane Proteome submitted to PLoS One 2014