Analysis of ABCG2 and other urate transporters in uric acid homeostasis in chronic kidney disease: Potential role of remote sensing and signaling

Clinical Kidney Journal

Volumn 9, Issue 3, 2016, Pages 444-453

  Bhatnagar, Vibha ^a   Richard, Erin L ^a   Wu, Wei ^b,c,d   Nievergelt, Caroline M ^e   Lipkowitz, Michael S ^f   Jeff, Janina ^g   Maihofer, X ^e   Nigam, Sanjay K ^b,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^g MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

ABCG2; CKD; Gastrointestinal transport; Sex interaction; SLC2A9

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; MEMBRANE PROTEIN; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 4; ORGANIC ANION TRANSPORTER 1; ORGANIC ANION TRANSPORTER 10; ORGANIC ANION TRANSPORTER 3; ORGANIC ANION TRANSPORTER 4; PROTEIN SLC17A3; PROTEIN SLC22A10; PROTEIN SLC22A9; SODIUM PHOSPHATE COTRANSPORTER 1; SODIUM PHOSPHATE COTRANSPORTER 2; UNCLASSIFIED DRUG; URATE TRANSPORTER; URIC ACID;

ADULT; ARTICLE; CHRONIC KIDNEY DISEASE; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; GENETIC ASSOCIATION; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMAN; KIDNEY FUNCTION; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PRIORITY JOURNAL; REMOTE SENSING; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; URIC ACID BLOOD LEVEL;

EID: 84978966834     PISSN: 20488505     EISSN: 20488513     Source Type: Journal    
DOI: 10.1093/ckj/sfw010     Document Type: Article

References (43)

1. Eraly SA, Vallon V, Rieg T et al. Multiple organic anion transporters contribute to net renal excretion of uric acid. Physiol Genomics 2008; 33: 180-192
2. Mount DB. The kidney in hyperuricemia and gout. Curr Opin Nephrol Hypertens 2013; 22: 216-223
3. Nigam SK. What do drug transporters really do? Nature reviews Drug discovery 2015; 14: 29-44
4. Lipkowitz MS. Regulation of uric acid excretion by the kidney. Curr Rheumatol Rep 2012; 14: 179-188
5. Yano H, Tamura Y, Kobayashi K et al. Uric acid transporter ABCG2 is increased in the intestine of the 5/6 nephrectomy rat model of chronic kidney disease. Clin Exp Nephrol 2014; 18: 50-55
6. Köttgen A, Albrecht E, Teumer A et al. Genome-wide association analyses identify 18 new loci associated with serum urate concentrations. Nat Genet 2013; 45: 145-154
7. Kolz M, Johnson T, Sanna S et al. Meta-analysis of 28,141 individuals identifies common variants within five new loci that influence uric acid concentrations. PLoS Genet 2009; 5: e1000504
8. Tin A, Woodward OM, Kao WHL et al. Genome-wide association study for serum urate concentrations and gout among African Americans identifies genomic risk loci and a novel URAT1 loss-of-function allele. Hum Mol Genet 2011; 20: 4056-4068
9. Vitart V, Rudan I, Hayward C et al. SLC2A9 is a newly identified urate transporter influencing serum urate concentration, urate excretion and gout. Nat Genet 2008; 40: 437-442
10. Preitner F, Bonny O, Laverriere A et al. Glut9 is a major regulator of urate homeostasis and its genetic inactivation induces hyperuricosuria and urate nephropathy. Proc Natl Acad Sci USA 2009; 106: 15501-15506
11. Döring A, Gieger C, Mehta D et al. SLC2A9 influences uric acid concentrations with pronounced sex-specific effects. Nat Genet 2008; 40: 430-436
12. Anzai N, Ichida K, Jutabha P et al. Plasma urate level is directly regulated by a voltage-driven urate efflux transporter URATv1 (SLC2A9) in humans. J Biol Chem2008; 283: 26834-26838
13. Nakayama A, Matsuo H, Shimizu T et al. Common missense variant of monocarboxylate transporter 9 (MCT9/SLC16A9) gene is associated with renal overload gout, but not with all gout susceptibility. Hum Cell 2013; 26: 133-136
14. Hosomi A, Nakanishi T, Fujita T et al. Extra-renal elimination of uric acid via intestinal efflux transporter BCRP/ABCG2. PLoS One 2012; 7: e30456
15. Matsuo H, Yamamoto K, Nakaoka H et al. Genome-wide association study of clinically defined gout identifies multiple risk loci and its association with clinical subtypes. Ann Rheum Dis 2015; 0: 1-8. doi:10. 1136/annrheumdis-2014-206191
16. Matsuo H, Takada T, Ichida K et al. Common defects of ABCG2, a high-capacity urate exporter, cause gout: a function-based genetic analysis in a Japanese population. Sci Transl Med 2009; 1: 5ra11
17. Matsuo H, Takada T, Nakayama A et al. ABCG2 dysfunction increases the risk of renal overload hyperuricemia. Nucleosides Nucleotides Nucleic Acids 2014; 33: 266-274
18. Kratzer JT, Lanaspa MA, Murphy MN et al. Evolutionary history and metabolic insights of ancient mammalian uricases. Proc Natl Acad Sci USA 2014; 111: 3763-3768
19. Feldman HI, Appel LJ, ChertowGMet al. The Chronic Renal Insufficiency Cohort (CRIC) Study: design and methods. J Am Soc Nephrol 2003; 14 (7 Suppl 2): S148-S153
20. Cockburn M, Hamilton A, Zadnick J et al. The occurrence of chronic disease and other conditions in a large populationbased cohort of native Californian twins. Twin Res 2002; 5: 460-467
21. Zhang L, Rao F,Wessel J et al. Functional allelic heterogeneity and pleiotropy of a repeat polymorphism in tyrosine hydroxylase: prediction of catecholamines and response to stress in twins. Physiol Genomics 2004; 19: 277-291
22. Wright JT Jr, Bakris G, Greene T et al. Effect of blood pressure lowering and antihypertensive drug class on progression of hypertensive kidney disease: results from the AASK trial. JAMA 2002; 288: 2421-2431
23. Lash JP, Go AS, Appel LJ et al. Chronic renal insufficiency cohort (CRIC) study: baseline characteristics and associations with kidney function. Clin J Am Soc Nephrol 2009; 4: 1302-1311
24. Pruim RJ, Welch RP, Sanna S et al. LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 2010; 26: 2336-2337
25. Purcell S, Neale B, Todd-Brown K et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007; 81: 559-575
26. Brandstatter A, Kiechl S, Kollerits B et al. Sex-specific association of the putative fructose transporter SLC2A9 variants with uric acid levels is modified by BMI. Diabetes Care 2008; 31: 1662-1667
27. Sabolic? I, Asif AR, Budach WE et al. Gender differences in kidney function. Pflugers Arch 2007; 455: 397-429
28. Hu M, Tomlinson B. Gender-dependent associations of uric acid levels with a polymorphism in SLC2A9 in Han Chinese patients. Scand J Rheumatol 2012; 41: 161-163
29. Woodward OM, Kottgen A, Coresh J et al. Identification of a urate transporter, ABCG2, with a common functional polymorphism causing gout. Proc Natl Acad Sci USA 2009; 106: 10338-10342
30. NakayamaA,Matsuo H, Takada Tet al. ABCG2 is a high-capacity urate transporter and its genetic impairment increases serum uric acid levels in humans. Nucleosides Nucleotides Nucleic Acids 2011; 30: 1091-1097
31. Nakayama A, Matsuo H, Nakaoka H et al. Common dysfunctional variants of ABCG2 have stronger impact on hyperuricemia progression than typical environmental risk factors. Sci Rep 2014; 4: 5227
32. Matsuo H, Chiba T, Nagamori S et al. Mutations in glucose transporter 9 gene SLC2A9 cause renal hypouricemia. Am J Hum Genet 2008; 83: 744-751
33. Tabara Y, Kohara K, Kawamoto R et al. Association of four genetic loci with uric acid levels and reduced renal function: the J-SHIPP Suita study. Am J Nephrol 2010; 32: 279-286
34. Martovetsky G, Tee JB, Nigam SK. Hepatocyte nuclear factors 4alpha and 1alpha regulate kidney developmental expression of drug-metabolizing enzymes and drug transporters. Mol Pharmacol 2013; 84: 808-823
35. Ahn S-Y, Nigam SK. Toward a systems level understanding of organic anion and other multispecific drug transporters: a remote sensing and signaling hypothesis. Mol Pharmacol 2009; 76: 481-490
36. Kaler G, Truong DM, Khandelwal A et al. Structural variation governs substrate specificity for organic anion transporters (OAT) homologs: potential remote sensing by oat family members. J Biol Chem 2007; 282: doi:10. 1074/jbc. M703467200
37. Nigam SK, Bush KT, Martovetsky G et al. The organic anion transporter (OAT) family: a systems biology perspective. Physiol Rev 2015; 95: 83-123
38. Wu W, Dnyanmote AV, Nigam SK. Remote communication through solute carriers and ATP binding cassette drug transporter pathways: an update on the remote sensing and signaling hypothesis. Mol Pharmacol 2011; 79: 795-805
39. NigamSK, Bush KT, Bhatnagar V. Drug and toxicant handling by the OAT organic anion transporters in the kidney and other tissues. Nat Clin Pract Nephrol 2007; 3: 443-448
40. Eraly SA, Hamilton BA, Nigam SK. Organic anion and cation transporters occur in pairs of similar and similarly expressed genes. Biochem Biophys Res Commun 2003; 300: 333-342
41. Xu G, Bhatnagar V, Wen G et al. Analyses of coding region polymorphisms in apical and basolateral human organic anion transporter (OAT) genes [OAT1 (NKT), OAT2, OAT3, OAT4, URAT (RST)]: Rapid communication. Kidney Int 2005; 68: 1491-1499
42. Jeroncic I, Mulic R, Klismanic Z et al. Interactions between genetic variants in glucose transporter type 9 (SLC2A9) and dietary habits in serum uric acid regulation. Croat Med J 2010; 51: 40-47
43. Zhu C, Nigam KB, Date RC et al. Evolutionary analysis and classification of OATs, OCTs, OCTNs and other SLC22 transporters: structure-function implications and analysis of sequence motifs. PLoS One 2015; 10: e0140569