Multiple organic anion transporters contribute to net renal excretion of uric acid

Physiological Genomics

Volumn 33, Issue 2, 2008, Pages 180-192

  Eraly, Satish A ^a   Vallon, Volker ^a,b,c   Rieg, Timo ^a,c   Gangoiti, Jon A ^d   Wikoff, William R ^e   Siuzdak, Gary ^e   Barshop, Bruce A ^d   Nigam, Sanjay K ^a,d,f,g  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b San Diego   (United States)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Metabolomics; Organic anion transport; Renal reabsorption; Renal secretion; Urate

Indexed keywords

ELECTROLYTE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 4; ORGANIC ANION TRANSPORTER; ORGANIC ANION TRANSPORTER 1; ORGANIC ANION TRANSPORTER 3; URATE TRANSPORTER 1; URIC ACID;

ABSORPTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; BLOOD LEVEL; CONTROLLED STUDY; ELECTROLYTE EXCRETION; GENE EXPRESSION; GLOMERULUS FILTRATION RATE; KIDNEY FUNCTION; KNOCKOUT MOUSE; MALE; MASS SPECTROMETRY; METABOLOMICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIORITY JOURNAL; TRANSPORT KINETICS; URIC ACID URINE LEVEL; URINALYSIS; URINARY EXCRETION;

ANIMALS; BETA-GALACTOSIDASE; BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION; GENE TARGETING; KIDNEY; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; ORGANIC ANION TRANSPORTERS; PHENOTYPE; RNA, MESSENGER; URIC ACID;

MURINAE; MUS;

EID: 43049121374     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00207.2007     Document Type: Article

References (71)

1. Ames BN, Cathcart R, Schwiers E, Hochstein P. Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: a hypothesis. Proc Natl Acad Sci USA 78: 6858-6862, 1981.
2. Anzai N, Miyazaki H, Noshiro R, Khamdang S, Chairoungdua A, Shin HJ, Enomoto A, Sakamoto S, Hirata T, Tomita K, Kanai Y, Endou H. The multivalent PDZ domain-containing protein PDZK1 regulates transport activity of renal urate-anion exchanger URAT1 via its C terminus. J Biol Chem 279: 45942-45950, 2004.
3. Babu E, Takeda M, Narikawa S, Kobayashi Y, Enomoto A, Tojo A, Cha SH, Sekine T, Sakthisekaran D, Endou H. Role of human organic anion transporter 4 in the transport of ochratoxin A. Biochim Biophys Acta 1590: 64-75, 2002.
4. Bakhiya A, Bahn A, Burckhardt G, Wolff N. Human organic anion transporter 3 (hOAT3) can operate as an exchanger and mediate secretory urate flux. Cell Physiol Biochem 13: 249-256, 2003.
5. Brady KP, Dushkin H, Fornzler D, Koike T, Magner F, Her H, Gullans S, Segre GV, Green RM, Beier DR. A novel putative transporter maps to the osteosclerosis (oc) mutation and is not expressed in the oc mutant mouse. Genomics 56: 254-261, 1999.
6. Buist SC, Cherrington NJ, Klaassen CD. Endocrine regulation of rat organic anion transporters. Drug Metab Dispos 31: 559-564, 2003.
7. Buist SCN, Cherrington NJ, Choudhuri S, Hartley DP, Klaassen CD. Gender-specific and developmental influences on the expression of rat organic anion transporters. J Pharmacol Exp Ther 301: 145-151, 2002.
8. Buist SCN, Klaassen CD. Rat and mouse differences in gender-predominant expression of organic anion transporter (OAT1-3; SLC22A6-8) mRNA levels. Drug Metab Dispos 32: 620-625, 2004.
9. Burckhardt BC, Burckhardt G. Transport of organic anions across the basolateral membrane of proximal tubule cells. Rev Physiol Biochem Pharmacol 146: 95-158, 2003.
10. Cunningham R, Brazie M, Kanumuru S, E X, Biswas R, Wang F, Steplock D, Wade JB, Anzai N, Endou H, Shenolikar S, Weinman EJ. Sodium-hydrogen exchanger regulatory factor-1 interacts with mouse urate transporter 1 to regulate renal proximal tubule uric acid transport. J Am Soc Nephrol 18: 1419-1425, 2007.
11. Dudas PL, Pelis RM, Braun EJ, Renfro JL. Transepithelial urate transport by avian renal proximal tubule epithelium in primary culture. J Exp Biol 208: 4305-4315, 2005.
12. Ekaratanawong S, Anzai N, Jutabha P, Miyazaki H, Noshiro R, Takeda M, Kanai Y, Sophasan S, Endou H. Human organic anion transporter 4 is a renal apical organic anion/dicarboxylate exchanger in the proximal tubules. J Pharmacol Sci 94: 297-304, 2004.
13. Enomoto A, Kimura H, Chairoungdua A, Shigeta Y, Jutabha P, Cha SH, Hosoyamada M, Takeda M, Sekine T, Igarashi T, Matsuo H, Kikuchi Y, Oda T, Ichida K, Hosoya T, Shimokata K, Niwa T, Kanai Y, Endou H. Molecular identification of a renal urate anion exchanger that regulates blood urate levels. Nature 417: 447-452, 2002.
14. Eraly SA, Bush KT, Sampogna RV, Bhatnagar V, Nigam SK. The molecular pharmacology of organic anion transporters: from DNA to FDA? Mol Pharmacol 65: 479-487, 2004.
15. Eraly SA, Hamilton BA, Nigam SK. Organic anion and cation transporters occur in pairs of similar and similarly expressed genes. Biochem Biophys Res Commun 300: 333-342, 2003.
16. Eraly SA, Monte JC, Nigam SK. Novel slc22 transporter homologs in fly, worm, and human clarify the phylogeny of organic anion and cation transporters. Physiol Genomics 18: 12-24, 2004.
17. Eraly SA, Vallon V, Vaughn DA, Gangoiti JA, Richter K, Nagle M, Monte JC, Rieg T, Truong DM, Long JM, Barshop BA, Kaler G, Nigam SK. Decreased renal organic anion secretion and plasma accumulation of endogenous organic anions in OAT1 knockout mice. J Biol Chem 281: 5072-5083, 2006.
18. Feig DI, Mazzali M, Kang DH, Nakagawa T, Price K, Kannelis J, Johnson RJ. Serum uric acid: a risk factor and a target for treatment? J Am Soc Nephrol 17: S69-73, 2006.
19. Gorman GS, Tamura T, Baggott JE. Mass spectrometric method for detecting carbon 13 enrichment introduced by folate coenzymes in uric acid. Anal Biochem 321: 188-191, 2003.
20. Hagos Y, Stein D, Ugele B, Burckhardt G, Bahn A. Human renal organic anion transporter 4 operates as an asymmetric urate transporter. J Am Soc Nephrol 18: 430-439, 2007.
21. Hediger MA. Kidney function: gateway to a long life? Nature 417: 393, 395, 2002.
22. Hediger MA, Johnson RJ, Miyazaki H, Endou H. Molecular physiology of urate transport. Physiology (Bethesda) 20: 125-133, 2005.
23. Hoffmann G, Aramaki S, Blum-Hoffmann E, Nyhan WL, Sweetman L. Quantitative analysis for organic acids in biological samples: batch isolation followed by gas chromatographic-mass spectrometric analysis. Clin Chem 35: 587-595, 1989.
24. Hosoyamada M, Ichida K, Enomoto A, Hosoya T, Endou H. Function and localization of urate transporter 1 in mouse kidney. J Am Soc Nephrol 15: 261-268, 2004.
25. Hosoyamada M, Sekine T, Kanai Y, Endou H. Molecular cloning and functional expression of a multispecific organic anion transporter from human kidney. Am J Physiol Renal Physiol 276: F122-F128, 1999.
26. Hsiao A, Ideker T, Olefsky JM, Subramaniam S. VAMPIRE microarray suite: a web-based platform for the interpretation of gene expression data. Nucleic Acids Res 33: W627-W32, 2005.
27. Hsiao A, Worrall DS, Olefsky JM, Subramaniam S. Variance-modeled posterior inference of microarray data: detecting gene-expression changes in 3T3-L1 adipocytes. Bioinformatics 20: 3108-3127, 2004.
28. Ichida K, Hosoyamada M, Hisatome I, Enomoto A, Hikita M, Endou H, Hosoya T. Clinical and molecular analysis of patients with renal hypouricemia in Japan: influence of URAT1 gene on urinary urate excretion. J Am Soc Nephrol 15: 164-173, 2004.
29. Ichida K, Hosoyamada M, Kimura H, Takeda M, Utsunomiya Y, Hosoya T, Endou H. Urate transport via human PAH transporter hOAT1 and its gene structure. Kidney Int 63: 143-155, 2003.
30. Imaoka T, Kusuhara H, Adachi-Akahane S, Hasegawa M, Morita N, Endou H, Sugiyama Y. The renal-specific transporter mediates facilitative transport of organic anions at the brush border membrane of mouse renal tubules. J Am Soc Nephrol 15: 2012-2022, 2004.
31. Kojima R, Sekine T, Kawachi M, Cha SH, Suzuki Y, Endou H. Immunolocalization of multispecific organic anion transporters, OAT1, OAT2, and OAT3, in rat kidney. J Am Soc Nephrol 13: 848-857, 2002.
32. Komatsuda A, Iwamoto K, Wakui H, Sawada K, Yamaguchi A. Analysis of mutations in the urate transporter 1 (URAT1) gene of Japanese patients with hypouricemia in northern Japan and review of the literature. Ren Fail 28: 223-227, 2006.
33. Lipkowitz MS, Leal-Pinto E, Cohen BE, Abramson RG. Galectin 9 is the sugar-regulated urate transporter/channel UAT. Glycoconj J 19: 491-498, 2004.
34. Lise MF, El-Husseini A. The neuroligin and neurexin families: from structure to function at the synapse. Cell Mol Life Sci 63: 1833-1849, 2006.
35. Ljubojevic M, Herak-Kramberger CM, Hagos Y, Bahn A, Endou H, Burckhardt G, Sabolic I. Rat renal cortical OAT1 and OAT3 exhibit gender differences determined by both androgen stimulation and estrogen inhibition. Am J Physiol Renal Physiol 287: F124-F138, 2004.
36. Lopez-Nieto CE. NKT cDNA sequence, GenBank Accession Number MMU52842. Submitted March 27, 1996.
37. Lopez-Nieto CE, Nigam SK. Selective amplification of protein-coding regions of large sets of genes using statistically designed primer sets. Nat Biotechnol 14: 857-861, 1996.
38. Lopez-Nieto CE, You G, Barros EJG, Beier DR, Nigam SK. Molecular cloning and characterization of a novel transport protein with very high expression in the kidney (Abstract). J Am Soc Nephrol 7: 1301, 1996.
39. Lopez-Nieto CE, You G, Bush KT, Barros EJG, Beier DR, Nigam SK. 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, 1997.
40. Mori K, Ogawa Y, Ebihara K, Aoki T, Tamura N, Sugawara A, Kuwahara T, Ozaki S, Mukoyama M, Tashiro K. Kidney-specific expression of a novel mouse organic cation transporter-like protein. FEBS Lett 417: 371-374, 1997.
41. Moriwaki Y, Yamamoto T, Higashino K. Enzymes involved in purine metabolism - a review of histochemical localization and functional implications. Histol Histopathol 14: 1321-1340, 1999.
42. Motohashi H, Sakurai Y, Saito H, Masuda S, Urakami Y, Goto M, Fukatsu A, Ogawa O, Inui K. Gene expression levels and immunolocalization of organic ion transporters in the human kidney. J Am Soc Nephrol 13: 866-874, 2002.
43. Mount DB. Molecular physiology and the four-component model of renal urate transport. Curr Opin Nephrol Hypertens 14: 460-463, 2005.
44. Mutch DM, O'Maille G, Wikoff WR, Wiedmer T, Sims PJ, Siuzdak G. Mobilization of pro-inflammatory lipids in obese Plscr3-deficient mice. Genome Biol 8: R38, 2007.
45. Nakagawa T, Kang DH, Feig D, Sanchez-Lozada LG, Srinivas TR, Sautin Y, Ejaz AA, Segal M, Johnson RJ. Unearthing uric acid: an ancient factor with recently found significance in renal and cardiovascular disease. Kidney Int 69: 1722-1725, 2006.
46. Rafey MA, Lipkowitz MS, Leal-Pinto E, Abramson RG. Uric acid transport. Curr Opin Nephrol Hypertens 12: 511-516, 2003.
47. Sekine T, Watanabe N, Hosoyamada M, Kanai Y, Endou H. Expression cloning and characterization of a novel multispecific organic anion transporter. J Biol Chem 272: 18526-18529, 1997.
48. Smith CA, O'Maille G, Want EJ, Qin C, Trauger SA, Brandon TR, Custodio DE, Abagyan R, Siuzdak G. METLIN: a metabolite mass spectral database. Ther Drug Monit 27: 747-751, 2005.
49. Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 78: 779-787, 2006.
50. Stuart RO, Bush KT, Nigam SK. Changes in gene expression patterns in the ureteric bud and metanephric mesenchyme in models of kidney development. Kidney Int 64: 1997-2008, 2003.
51. Stuart RO, Bush KT, Nigam SK. Changes in global gene expression patterns during development and maturation of the rat kidney. Proc Natl Acad Sci USA 98: 5649-5654, 2001.
52. + gradient. Am J Physiol Renal Physiol 284: F763-F769, 2003.
53. Sweet DH, Eraly SA, Vaughn DA, Bush KT, Nigam SK. Organic anion and cation transporter expression and function during embryonic kidney development and in organ culture model systems. Kidney Int 69: 837-845, 2006.
54. Sweet DH, Miller DS, Pritchard JB, Fujiwara Y, Beier DR, Nigam SK. Impaired organic anion transport in kidney and choroid plexus of organic anion transporter 3 (Oat3 [Slc22a8]) knockout mice. J Biol Chem 277: 26934-26943, 2002.
55. Sweet DH, Wolff NA, Pritchard JB. Expression cloning and characterization of ROAT1. The basolateral organic anion transporter in rat kidney. J Biol Chem 272: 30088-30095, 1997.
56. Tanaka M, Itoh K, Matsushita K, Matsushita K, Wakita N, Adachi M, Nonoguchi H, Kitamura K, Hosoyamada M, Endou H, Tomita K. Two male siblings with hereditary renal hypouricemia and exercise-induced ARF. Am J Kidney Dis 42: 1287-1292, 2003.
57. Terkeltaub R, Bushinsky DA, Becker MA. Recent developments in our understanding of the renal basis of hyperuricemia and the development of novel antihyperuricemic therapeutics. Arthritis Res Ther 8, Suppl 1: S4, 2006.
58. Terkeltaub RA. Clinical practice. Gout. N Engl J Med 349: 1647-1655, 2003.
59. Thangaraju M, Ananth S, Martin PM, Roon P, Smith SB, Sterneck E, Prasad PD, Ganapathy V. c/ebpδ Null mouse as a model for the double knock-out of slc5a8 and slc5a12 in kidney. J Biol Chem 281: 26769-26773, 2006.
60. Tojo A, Sekine T, Nakajima N, Hosoyamada M, Kanai Y, Kimura K, Endou H. Immunohistochemical localization of multispecific renal organic anion transporter 1 in rat kidney. J Am Soc Nephrol 10: 464-471, 1999.
61. Tzovaras V, Chatzikyriakidou A, Bairaktari E, Liberopoulos EN, Georgiou I, Elisaf M. Absence of SLC22A12 gene mutations in Greek Caucasian patients with primary renal hypouricaemia. Scand J Clin Lab Invest 67: 589-595, 2007.
62. Vallon V, Rieg T, Ahn S-Y, Wu W, Eraly SA, Nigam SK. Overlapping in vitro and in vivo specificities of the organic anion transporters OAT1 and OAT3 for loop and thiazide diuretics. Am J Physiol Renal Physiol January 23, 2008; doi:10.1152/ajprenal.00528.2007.
63. Van Aubel RAMH, Smeets PHE, van den Heuvel JJMW, Russel FGM. Human organic anion transporter MRP4 (ABCC4) is an efflux pump for the purine end metabolite urate with multiple allosteric substrate binding sites. Am J Physiol Renal Physiol 288: F327-F333, 2005.
64. VanWert AL, Bailey RM, Sweet DH. Organic anion transporter 3 (Oat3/Slc22a8) knockout mice exhibit altered clearance and distribution of penicillin G. Am J Physiol Renal Physiol 293: F1332-F1341, 2007.
65. Vazquez-Mellado J, Alvarado-Romano V, Burgos-Vargas R, Jimenez-Vaca AL, Pozo-Molina G, Cuevas-Covarrubias SA. Homozygous frameshift mutation in the SLC22A12 gene in a patient with primary gout and high levels of serum uric acid. J Clin Pathol 60: 947-948, 2007.
66. Want EJ, Cravatt BF, Siuzdak G. The expanding role of mass spectrometry in metabolite profiling and characterization. Chembiochem 6: 1941-1951, 2005.
67. Watanabe S, Kang DH, Feng L, Nakagawa T, Kanellis J, Lan H, Mazzali M, Johnson RJ. Uric acid, hominoid evolution, and the pathogenesis of salt-sensitivity. Hypertension 40: 355-360, 2002.
68. Wikoff WR, Gangoiti JA, Barshop BA, Siuzdak G. Metabolomics identifies perturbations in human disorders of propionate metabolism. Clin Chem 53: 2169-2176, 2007.
69. Wright SH, Dantzler WH. Molecular and cellular physiology of renal organic cation and anion transport. Physiol Rev 84: 987-1049, 2004.
70. Wu X, Lee CC, Muzny DM, Caskey CT. Urate oxidase: primary structure and evolutionary implications. Proc Natl Acad Sci USA 86: 9412-9416, 1989.
71. Wu X, Wakamiya M, Vaishnav S, Geske R, Montgomery C Jr, Jones P, Bradley A, Caskey C. Hyperuricemia and urate nephropathy in urate oxidase-deficient mice. Proc Natl Acad Sci USA 91: 742-746, 1994.