Putative transmembrane domain 6 of the human organic anion transporting polypeptide 1A2 (OATP1A2) influences transporter substrate binding, protein trafficking, and quality control

Molecular Pharmaceutics

Volumn 12, Issue 1, 2015, Pages 111-119

  Chan, Ting ^a   Zheng, Jian ^a,b   Zhu, Ling ^c   Grewal, Thomas ^a   Murray, Michael ^a   Zhou, Fanfan ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NORTHEAST FORESTRY UNIVERSITY   (China)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

membrane trafficking; organic anion transporting polypeptide 1A2; protein quality control; transporter substrate binding

Indexed keywords

ALANINE; ESTRONE SULFATE; MEMBRANE PROTEIN; METHOTREXATE; ORGANIC ANION TRANSPORTER; ORGANIC ANION TRANSPORTING POLYPEPTIDE 1A2; TRANSMEMBRANE DOMAIN 6; UNCLASSIFIED DRUG; ESTRONE; PROTEIN BINDING; SLCO1A2 PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; ARTICLE; BIOTINYLATION; CELL MEMBRANE; CONTROLLED STUDY; GENE OVEREXPRESSION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN QUALITY; QUALITY CONTROL; SITE DIRECTED MUTAGENESIS; UPTAKE ASSAY; ANALOGS AND DERIVATIVES; CELL LINE; CHEMISTRY; GENETICS; KINETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHARMACOGENETICS; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

BASE SEQUENCE; BIOTINYLATION; CELL LINE; ESTRONE; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; KINETICS; METHOTREXATE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; ORGANIC ANION TRANSPORTERS; PHARMACOGENETICS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

EID: 84920372546     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp500459b     Document Type: Article

References (39)

1. Roth, M.; Obaidat, A.; Hagenbuch, B. OATPs, OATs and OCTs: the organic anion and cation transporters of the SLCO and SLC22A gene superfamilies Br. J. Pharmacol. 2012, 165 (5) 1260-87
2. Gong, I. Y.; Kim, R. B. Impact of genetic variation in OATP transporters to drug disposition and response Drug Metab. Pharmacokinet. 2013, 28 (1) 4-18
3. Konig, J.; Muller, F.; Fromm, M. F. Transporters and drug-drug interactions: important determinants of drug disposition and effects Pharmacol. Rev. 2013, 65 (3) 944-66
4. Shitara, Y.; Maeda, K.; Ikejiri, K.; Yoshida, K.; Horie, T.; Sugiyama, Y. Clinical significance of organic anion transporting polypeptides (OATPs) in drug disposition: their roles in hepatic clearance and intestinal absorption Biopharm. Drug Dispos. 2013, 34 (1) 45-78
5. Lee, W.; Glaeser, H.; Smith, L. H.; Roberts, R. L.; Moeckel, G. W.; Gervasini, G.; Leake, B. F.; Kim, R. B. Polymorphisms in human organic anion-transporting polypeptide 1A2 (OATP1A2): implications for altered drug disposition and central nervous system drug entry J. Biol. Chem. 2005, 280 (10) 9610-7
6. Gao, B.; Hagenbuch, B.; Kullak-Ublick, G. A.; Benke, D.; Aguzzi, A.; Meier, P. J. Organic anion-transporting polypeptides mediate transport of opioid peptides across blood-brain barrier J. Pharmacol. Exp. Ther. 2000, 294 (1) 73-9
7. Glaeser, H.; Bailey, D. G.; Dresser, G. K.; Gregor, J. C.; Schwarz, U. I.; McGrath, J. S.; Jolicoeur, E.; Lee, W.; Leake, B. F.; Tirona, R. G.; Kim, R. B. Intestinal drug transporter expression and the impact of grapefruit juice in humans Clin. Pharmacol. Ther. 2007, 81 (3) 362-70
8. Groer, C.; Bruck, S.; Lai, Y.; Paulick, A.; Busemann, A.; Heidecke, C. D.; Siegmund, W.; Oswald, S. LC-MS/MS-based quantification of clinically relevant intestinal uptake and efflux transporter proteins J. Pharm. Biomed. Anal. 2013, 85, 253-61
9. Drozdzik, M.; Groer, C.; Penski, J.; Lapczuk, J.; Ostrowski, M.; Lai, Y.; Prasad, B.; Unadkat, J. D.; Siegmund, W.; Oswald, S. Protein abundance of clinically relevant multidrug transporters along the entire length of the human intestine Mol. Pharmaceutics 2014, 11 (10) 3547-55
10. Kalliokoski, A.; Niemi, M. Impact of OATP transporters on pharmacokinetics Br. J. Pharmacol. 2009, 158 (3) 693-705
11. Eechoute, K.; Franke, R. M.; Loos, W. J.; Scherkenbach, L. A.; Boere, I.; Verweij, J.; Gurney, H.; Kim, R. B.; Tirona, R. G.; Mathijssen, R. H.; Sparreboom, A. Environmental and genetic factors affecting transport of imatinib by OATP1A2 Clin. Pharmacol. Ther. 2011, 89 (6) 816-20
12. Badagnani, I.; Castro, R. A.; Taylor, T. R.; Brett, C. M.; Huang, C. C.; Stryke, D.; Kawamoto, M.; Johns, S. J.; Ferrin, T. E.; Carlson, E. J.; Burchard, E. G.; Giacomini, K. M. Interaction of methotrexate with organic-anion transporting polypeptide 1A2 and its genetic variants J. Pharmacol. Exp. Ther. 2006, 318 (2) 521-9
13. Hartkoorn, R. C.; Kwan, W. S.; Shallcross, V.; Chaikan, A.; Liptrott, N.; Egan, D.; Sora, E. S.; James, C. E.; Gibbons, S.; Bray, P. G.; Back, D. J.; Khoo, S. H.; Owen, A. HIV protease inhibitors are substrates for OATP1A2, OATP1B1 and OATP1B3 and lopinavir plasma concentrations are influenced by SLCO1B1 polymorphisms Pharmacogenet. Genomics 2010, 20 (2) 112-20
14. Shirasaka, Y.; Suzuki, K.; Shichiri, M.; Nakanishi, T.; Tamai, I. Intestinal absorption of HMG-CoA reductase inhibitor pitavastatin mediated by organic anion transporting polypeptide and P-glycoprotein/multidrug resistance 1 Drug Metab. Pharmacokinet. 2011, 26 (2) 171-9
15. Konig, J.; Seithel, A.; Gradhand, U.; Fromm, M. F. Pharmacogenomics of human OATP transporters Naunyn Schmiedebergs Arch Pharmacol 2006, 372 (6) 432-43
16. Hagenbuch, B.; Meier, P. J. Organic anion transporting polypeptides of the OATP/ SLC21 family: phylogenetic classification as OATP/ SLCO superfamily, new nomenclature and molecular/functional properties Pflugers Arch. 2004, 447 (5) 653-65
17. Zhou, F.; Zheng, J.; Zhu, L.; Jodal, A.; Cui, P. H.; Wong, M.; Gurney, H.; Church, W. B.; Murray, M. Functional analysis of novel polymorphisms in the human SLCO1A2 gene that encodes the transporter OATP1A2 AAPS J. 2013, 15 (4) 1099-108
18. Huang, J.; Li, N.; Hong, W.; Zhan, K.; Yu, X.; Huang, H.; Hong, M. Conserved tryptophan residues within putative transmembrane domain 6 affect transport function of organic anion transporting polypeptide 1B1 Mol. Pharmacol. 2013, 84 (4) 521-7
19. Taylor-Wells, J.; Meredith, D. The signature sequence region of the human drug transporter organic anion transporting polypeptide 1B1 is important for protein surface expression J. Drug Delivery 2014, 2014, 129849
20. Zhou, F.; Lee, A. C.; Krafczyk, K.; Zhu, L.; Murray, M. Protein kinase C regulates the internalization and function of the human organic anion transporting polypeptide 1A2 Br. J. Pharmacol. 2011, 162 (6) 1380-8
21. Zhou, F.; Zhu, L.; Cui, P. H.; Church, W. B.; Murray, M. Functional characterization of nonsynonymous single nucleotide polymorphisms in the human organic anion transporter 4 (hOAT4) Br. J. Pharmacol. 2010, 159 (2) 419-27
22. Zheng, J.; Chan, T.; Cheung, F. S.; Zhu, L.; Murray, M.; Zhou, F. PDZK1 and NHERF1 regulate the function of human organic anion transporting polypeptide 1A2 (OATP1A2) by modulating its subcellular trafficking and stability PLoS One 2014, 9 (4) e94712
23. Hong, M.; Li, S.; Zhou, F.; Thomas, P. E.; You, G. Putative transmembrane domain 12 of the human organic anion transporter hOAT1 determines transporter stability and maturation efficiency J. Pharmacol. Exp. Ther. 2010, 332 (2) 650-8
24. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-54
25. Zhou, F.; Tanaka, K.; Pan, Z.; Ma, J.; You, G. The role of glycine residues in the function of human organic anion transporter 4 Mol. Pharmacol. 2004, 65 (5) 1141-7
26. Hong, M.; Zhou, F.; You, G. Critical amino acid residues in transmembrane domain 1 of the human organic anion transporter hOAT1 J. Biol. Chem. 2004, 279 (30) 31478-82
27. Zhou, F.; Pan, Z.; Ma, J.; You, G. Mutational analysis of histidine residues in human organic anion transporter 4 (hOAT4) Biochem. J. 2004, 384 (Pt 1) 87-92
28. Kaur, J.; Bachhawat, A. K. Gln-222 in transmembrane domain 4 and Gln-526 in transmembrane domain 9 are critical for substrate recognition in the yeast high affinity glutathione transporter, Hgt1p J. Biol. Chem. 2009, 284 (35) 23872-84
29. Landgraf, K. E.; Pilling, C.; Falke, J. J. Molecular mechanism of an oncogenic mutation that alters membrane targeting: Glu17Lys modifies the PIP lipid specificity of the AKT1 PH domain Biochemistry 2008, 47 (47) 12260-9
30. Lecker, S. H.; Goldberg, A. L.; Mitch, W. E. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states J. Am. Soc. Nephrol. 2006, 17 (7) 1807-19
31. Hong, M.; Zhou, F.; Lee, K.; You, G. The putative transmembrane segment 7 of human organic anion transporter hOAT1 dictates transporter substrate binding and stability J. Pharmacol. Exp. Ther. 2007, 320 (3) 1209-15
32. Hideshima, T.; Bradner, J. E.; Chauhan, D.; Anderson, K. C. Intracellular protein degradation and its therapeutic implications Clin. Cancer Res. 2005, 11 (24 Pt 1) 8530-3
33. Jensen, T. J.; Loo, M. A.; Pind, S.; Williams, D. B.; Goldberg, A. L.; Riordan, J. R. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing Cell 1995, 83 (1) 129-35
34. Kock, K.; Koenen, A.; Giese, B.; Fraunholz, M.; May, K.; Siegmund, W.; Hammer, E.; Volker, U.; Jedlitschky, G.; Kroemer, H. K.; Grube, M. Rapid modulation of the organic anion transporting polypeptide 2B1 (OATP2B1, SLCO2B1) function by protein kinase C-mediated internalization J. Biol. Chem. 2010, 285 (15) 11336-47
35. Kostova, Z.; Wolf, D. H. For whom the bell tolls: protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection EMBO J. 2003, 22 (10) 2309-17
36. Ohnishi, S.; Hays, A.; Hagenbuch, B. Cysteine scanning mutagenesis of transmembrane domain 10 in organic anion transporting polypeptide 1B1 Biochemistry 2014, 53 (14) 2261-70
37. Li, N.; Hong, W.; Huang, H.; Lu, H.; Lin, G.; Hong, M. Identification of amino acids essential for estrone-3-sulfate transport within transmembrane domain 2 of organic anion transporting polypeptide 1B1 PLoS One 2012, 7 (5) e36647
38. Nilsson, I.; Saaf, A.; Whitley, P.; Gafvelin, G.; Waller, C.; von Heijne, G. Proline-induced disruption of a transmembrane alpha-helix in its natural environment J. Mol. Biol. 1998, 284 (4) 1165-75
39. Gui, C.; Hagenbuch, B. Amino acid residues in transmembrane domain 10 of organic anion transporting polypeptide 1B3 are critical for cholecystokinin octapeptide transport Biochemistry 2008, 47 (35) 9090-7