Evolutionary analysis and classification of OATs, OCTs, OCTNs, and other SLC22 transporters: Structure-function implications and analysis of sequence motifs

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Zhu, Christopher ^a   Nigam, Kabir B ^a   Date, Rishabh C ^a   Bush, Kevin T ^a   Springer, Stevan A ^a   Saier, Milton H ^a   Wu, Wei ^a   Nigam, Sanjay K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARNITINE TRANSPORTER 1; CARNITINE TRANSPORTER 2; FLY LIKE TRANSPORTER 1; FLY LIKE TRANSPORTER 2; MEMBRANE PROTEIN; ORGANIC ANION TRANSPORTER; ORGANIC ANION TRANSPORTER 1; ORGANIC ANION TRANSPORTER 10; ORGANIC ANION TRANSPORTER 2; ORGANIC ANION TRANSPORTER 3; ORGANIC ANION TRANSPORTER 4; ORGANIC ANION TRANSPORTER 5; ORGANIC ANION TRANSPORTER 6; ORGANIC ANION TRANSPORTER 7; ORGANIC CARNITINE TRANSPORTER; ORGANIC CATION TRANSPORTER; ORGANIC CATION TRANSPORTER 1; ORGANIC CATION TRANSPORTER 2; ORGANIC CATION TRANSPORTER 3; SLC22A17 PROTEIN; SLC22A18 PROTEIN; SLC22A23 PROTEIN; SLC22A31 PROTEIN; UNCLASSIFIED DRUG; URATE TRANSPORTER; ZWITTERION TRANSPORTER; AMINO ACID TRANSPORTER; CARNITINE;

AMINO ACID SEQUENCE; ARTICLE; CLADISTICS; CONTROLLED STUDY; EVOLUTION; GENE LOCATION; HUMAN; INVERTEBRATE; MOUSE; MUTAGENESIS; NONHUMAN; PHYLOGENY; PROTEIN MOTIF; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; STRUCTURE ACTIVITY RELATION; VERTEBRATE; ANIMAL; GENETICS; METABOLISM; MULTIGENE FAMILY; PROTEIN TERTIARY STRUCTURE; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACID TRANSPORT SYSTEMS, NEUTRAL; ANIMALS; BIOLOGICAL EVOLUTION; BIOLOGICAL TRANSPORT; CARNITINE; HUMANS; MICE; MULTIGENE FAMILY; ORGANIC ANION TRANSPORTERS; ORGANIC CATION TRANSPORT PROTEINS; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN STRUCTURE, TERTIARY;

EID: 84951128933     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0140569     Document Type: Article

References (56)

1. Nigam SK (2015) What do drug transporters really do? Nat Rev Drug Discov 14: 29-44. doi: 10.1038/nrd4461 PMID: 25475361
2. Lopez-Nieto CE, You G, Barros EJG, Beier DR, Nigam SK (1996) Molecular cloning and characterization of a novel transporter protein with very high expression in the kidney. J Am Soc Nephrol 7: 1301.
3. Lopez-Nieto CE, You G, Bush KT, Barros EJ, Beier DR, Nigam SK (1997) Molecular cloning and characterization of NKT, a gene product related to the organic cation transporter family that is almost exclusively expressed in the kidney. J Biol Chem 272: 6471-6478. PMID: 9045672
4. Grundemann D, Gorboulev V, Gambaryan S, Veyhl M, Koepsell H (1994) Drug excretion mediated by a new prototype of polyspecific transporter. Nature 372: 549-552. PMID: 7990927
5. Simonson GD, Vincent AC, Roberg KJ, Huang Y, Iwanij V (1994) Molecular cloning and characterization of a novel liver-specific transport protein. J Cell Sci 107 (Pt 4): 1065-1072. PMID: 8056831
6. Cesar-Razquin A, Snijder B, Frappier-Brinton T, Isserlin R, Gyimesi G, Bai X, et al. (2015) A Call for Systematic Research on Solute Carriers. Cell 162: 478-487. doi: 10.1016/j.cell.2015.07.022 PMID: 26232220
7. Eraly SA, Monte JC, Nigam SK (2004) Novel slc22 transporter homologs in fly, worm, and human clarify the phylogeny of organic anion and cation transporters. Physiol Genomics 18: 12-24. PMID: 15054140
8. Koepsell H (2013) The SLC22 family with transporters of organic cations, anions and zwitterions. Mol Aspects Med 34: 413-435. doi: 10.1016/j.mam.2012.10.010 PMID: 23506881
9. Nies AT, Koepsell H, Damme K, Schwab M (2011) Organic cation transporters (OCTs, MATEs), in vitro and in vivo evidence for the importance in drug therapy. Handb Exp Pharmacol 105-167.
10. Nigam SK, Bush KT, Martovetsky G, Ahn SY, Liu HC, Richard E, et al. (2015) The Organic Anion Transporter (OAT) Family: A Systems Biology Perspective. Physiol Rev 95: 83-123. doi: 10.1152/physrev. 00025.2013 PMID: 25540139
11. Srimaroeng C, Perry JL, Pritchard JB (2008) Physiology, structure, and regulation of the cloned organic anion transporters. Xenobiotica 38: 889-935. doi: 10.1080/00498250801927435 PMID: 18668434
12. Emami Riedmaier A, Nies AT, Schaeffeler E, Schwab M (2012) Organic anion transporters and their implications in pharmacotherapy. Pharmacol Rev 64: 421-449. doi: 10.1124/pr.111.004614 PMID: 22457399
13. Saier MH Jr, Reddy VS, Tamang DG, Vastermark A (2014) The transporter classification database. Nucleic Acids Res 42: D251-258. doi: 10.1093/nar/gkt1097 PMID: 24225317
14. Ahn SY, Eraly SA, Tsigelny I, Nigam SK (2009) Interaction of organic cations with organic anion transporters. J Biol Chem 284: 31422-31430. doi: 10.1074/jbc.M109.024489 PMID: 19737926
15. Bleasby K, Hall LA, Perry JL, Mohrenweiser HW, Pritchard JB (2005) Functional consequences of single nucleotide polymorphisms in the human organic anion transporter hOAT1 (SLC22A6). J Pharmacol Exp Ther 314: 923-931. PMID: 15914676
16. Keller T, Egenberger B, Gorboulev V, Bernhard F, Uzelac Z, Gorbunov D, et al. (2011) The large extracellular loop of organic cation transporter 1 influences substrate affinity and is pivotal for oligomerization. J Biol Chem 286: 37874-37886. doi: 10.1074/jbc.M111.289330 PMID: 21896487
17. Tsigelny IF, Kovalskyy D, Kouznetsova VL, Balinskyi O, Sharikov Y, Bhatnagar V, et al. (2011) Conformational changes of the multispecific transporter organic anion transporter 1 (OAT1/SLC22A6) suggests a molecular mechanism for initial stages of drug and metabolite transport. Cell Biochem Biophys 61: 251-259. doi: 10.1007/s12013-011-9191-7 PMID: 21499753
18. Perry JL, Dembla-Rajpal N, Hall LA, Pritchard JB (2006) A three-dimensional model of human organic anion transporter 1: aromatic amino acids required for substrate transport. J Biol Chem 281: 38071-38079. PMID: 17038320
19. Jacobsson JA, Haitina T, Lindblom J, Fredriksson R (2007) Identification of six putative human transporters with structural similarity to the drug transporter SLC22 family. Genomics 90: 595-609. PMID: 17714910
20. Wu W, Baker ME, Eraly SA, Bush KT, Nigam SK (2009) Analysis of a large cluster of SLC22 transporter genes, including novel USTs, reveals species-specific amplification of subsets of family members. Physiol Genomics 38: 116-124. doi: 10.1152/physiolgenomics.90309.2008 PMID: 19417012
21. Blair JE, Hedges SB (2005) Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22: 2275-2284. PMID: 16049193
22. Ahn SY, Nigam SK (2009) Toward a systems level understanding of organic anion and other multispecific drug transporters: a remote sensing and signaling hypothesis. Mol Pharmacol 76: 481-490. doi: 10.1124/mol.109.056564 PMID: 19515966
23. Kaler G, Truong DM, Khandelwal A, Nagle M, Eraly SA, Swaan PW, et al. (2007) Structural variation governs substrate specificity for organic anion transporter (OAT) homologs. Potential remote sensing by OAT family members. J Biol Chem 282: 23841-23853. PMID: 17553798
24. Wu W, Dnyanmote AV, Nigam SK (2011) Remote Communication through Slc and Abc Drug Transporter Pathways: An Update on the Remote Sensing and Signaling Hypothesis. Mol Pharmacol 79: 795-805. doi: 10.1124/mol.110.070607 PMID: 21325265
25. Boratyn GM, Camacho C, Cooper PS, Coulouris G, Fong A, Ma N, et al. (2013) BLAST: a more efficient report with usability improvements. Nucleic Acids Res 41: W29-33. doi: 10.1093/nar/gkt282 PMID: 23609542
26. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. (2007) ClustalW and Clustal X version 2.0. Bioinformatics 23: 2947-2948. PMID: 17846036
27. Li W, Cowley A, Uludag M, Gur T, McWilliam H, Squizzato S, et al. (2015) The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Res 43: W580-584. doi: 10.1093/nar/gkv279 PMID: 25845596
28. Bailey TL, Baker ME, Elkan CP (1997) An artificial intelligence approach to motif discovery in protein sequences: application to steriod dehydrogenases. J Steroid Biochem Mol Biol 62: 29-44. PMID: 9366496
29. Canestro C, Bassham S, Postlethwait JH (2003) Seeing chordate evolution through the Ciona genome sequence. Genome Biol 4: 208. PMID: 12620098
30. Fang G, Bhardwaj N, Robilotto R, Gerstein MB (2010) Getting started in gene orthology and functional analysis. PLoS Comput Biol 6: e1000703. doi: 10.1371/journal.pcbi.1000703 PMID: 20361041
31. Eraly SA, Vallon V, Vaughn DA, Gangoiti JA, Richter K, Nagle M, et al. (2006) Decreased renal organic anion secretion and plasma accumulation of endogenous organic anions in OAT1 knock-out mice. J Biol Chem 281: 5072-5083. PMID: 16354673
32. Sweet DH, Miller DS, Pritchard JB, Fujiwara Y, Beier DR, Nigam SK (2002) Impaired organic anion transport in kidney and choroid plexus of organic anion transporter 3 (Oat3 (Slc22a8)) knockout mice. J Biol Chem 277: 26934-26943. PMID: 12011098
33. Vallon V, Eraly SA, Rao SR, Gerasimova M, Rose M, Nagle M, et al. (2012) A role for the organic anion transporter OAT3 in renal creatinine secretion in mice. Am J Physiol Renal Physiol 302: F1293-1299. doi: 10.1152/ajprenal.00013.2012 PMID: 22338083
34. Bennett KM, Liu J, Hoelting C, Stoll J (2011) Expression and analysis of two novel rat organic cation transporter homologs, SLC22A17 and SLC22A23. Mol Cell Biochem 352: 143-154. doi: 10.1007/s11010-011-0748-y PMID: 21359964
35. Nagle MA, Wu W, Eraly SA, Nigam SK (2013) Organic anion transport pathways in antiviral handling in choroid plexus in Oat1 (Slc22a6) and Oat3 (Slc22a8) deficient tissue. Neurosci Lett 534: 133-138. doi: 10.1016/j.neulet.2012.11.027 PMID: 23196129
36. Eraly SA, Nigam SK (2002) Novel human cDNAs homologous to Drosophila Orct and mammalian carnitine transporters. Biochem Biophys Res Commun 297: 1159-1166. PMID: 12372408
37. Kaler G, Truong DM, Sweeney DE, Logan DW, Nagle M, Wu W, et al. (2006) Olfactory mucosaexpressed organic anion transporter, Oat6, manifests high affinity interactions with odorant organic anions. Biochem Biophys Res Commun 351: 872-876. PMID: 17094945
38. Monte JC, Nagle MA, Eraly SA, Nigam SK (2004) Identification of a novel murine organic anion transporter family member, OAT6, expressed in olfactory mucosa. Biochem Biophys Res Commun 323: 429-436. PMID: 15369770
39. Schnabolk GW, Youngblood GL, Sweet DH (2006) Transport of estrone sulfate by the novel organic anion transporter Oat6 (Slc22a20). Am J Physiol Renal Physiol 291: F314-321. PMID: 16478971
40. Bahn A, Hagos Y, Reuter S, Balen D, Brzica H, Krick W, et al. (2008) Identification of a new urate and high affinity nicotinate transporter, hOAT10 (SLC22A13). J Biol Chem 283: 16332-16341. doi: 10.1074/jbc.M800737200 PMID: 18411268
41. Gess RW, Coates MI, Rubidge BS (2006) A lamprey from the Devonian period of South Africa. Nature 443: 981-984. PMID: 17066033
42. Tamai I, Ohashi R, Nezu J, Yabuuchi H, Oku A, Shimane M, et al. (1998) Molecular and functional identification of sodium ion-dependent, high affinity human carnitine transporter OCTN2. J Biol Chem 273: 20378-20382. PMID: 9685390
43. Tamai I, Yabuuchi H, Nezu J, Sai Y, Oku A, Shimane M, et al. (1997) Cloning and characterization of a novel human pH-dependent organic cation transporter, OCTN1. FEBS letters 419: 107-111. PMID: 9426230
44. Markov GV, Tavares R, Dauphin-Villemant C, Demeneix BA, Baker ME, Laudet V (2009) Independent elaboration of steroid hormone signaling pathways in metazoans. Proc Natl Acad Sci U S A 106: 11913-11918. doi: 10.1073/pnas.0812138106 PMID: 19571007
45. Baker ME (2005) Xenobiotics and the evolution of multicellular animals: emergence and diversification of ligand-activated transcription factors. Integr Comp Biol 45: 172-178. doi: 10.1093/icb/45.1.172 PMID: 21676759
46. Enomoto A, Wempe MF, Tsuchida H, Shin HJ, Cha SH, Anzai N, et al. (2002) Molecular identification of a novel carnitine transporter specific to human testis. Insights into the mechanism of carnitine recognition. J Biol Chem 277: 36262-36271. PMID: 12089149
47. Eraly SA, Hamilton BA, Nigam SK (2003) Organic anion and cation transporters occur in pairs of similar and similarly expressed genes. Biochem Biophys Res Commun 300: 333-342. PMID: 12504088
48. Chu SH, Zhou ZM, Karri S, Li ZQ, Zhao JM (2014) In vitro and in vivo radiosensitization of human glioma U251 cells induced by upregulated expression of SLC22A18. Cancer Gene Ther 21: 103-109. doi: 10.1038/cgt.2014.4 PMID: 24481489
49. Brunet FG, Roest Crollius H, Paris M, Aury JM, Gibert P, Jaillon O, et al. (2006) Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol Biol Evol 23: 1808-1816. PMID: 16809621
50. Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27: 937-945. PMID: 16108068
51. Burckhardt G (2012) Drug transport by Organic Anion Transporters (OATs). Pharmacol Ther 136: 106-130. doi: 10.1016/j.pharmthera.2012.07.010 PMID: 22841915
52. Van Wert AL, Gionfriddo MR, Sweet DH (2010) Organic anion transporters: discovery, pharmacology, regulation and roles in pathophysiology. Biopharm Drug Dispos 31: 1-71. doi: 10.1002/bdd.693 PMID: 19953504
53. Xu G, Bhatnagar V, Wen G, Hamilton BA, Eraly SA, Nigam SK (2005) Analyses of coding region polymorphisms in apical and basolateral human organic anion transporter (OAT) genes [OAT1 (NKT), OAT2, OAT3, OAT4, URAT (RST)]. Kidney Int 68: 1491-1499. PMID: 16164626
54. Astorga B, Wunz TM, Morales M, Wright SH, Pelis RM (2011) Differences in the substrate binding regions of renal organic anion transporters 1 (OAT1) and 3 (OAT3). Am J Physiol Renal Physiol 301: F378-386. doi: 10.1152/ajprenal.00735.2010 PMID: 21543413
55. Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23: 127-128. PMID: 17050570
56. Wu W, Bush KT, Liu HC, Zhu C, Abagyan R, Nigam SK (2015) Shared Ligands between Organic Anion Transporters (Oat1 and Oat6) and Odorant Receptors. Drug Metab Dispos. 43: 1-9.