Oxalate: From the Environment to Kidney Stones

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Oxalate urolithiasis (nephrolithiasis) is the most frequent type of kidney stone disease. Epidemiological research has shown that urolithiasis is approximately twice as common in men as in women, but the underlying mechanism of this sex-related prevalence is unclear. Oxalate in the organism partially originate from food (exogenous oxalate) and largely as a metabolic end-product from numerous precursors generated mainly in the liver (endogenous oxalate). Oxalate concentrations in plasma and urine can be modified by various foodstuffs, which can interact in positively or negatively by affecting oxalate absorption, excretion, and/or its metabolic pathways. Oxalate is mostly removed from blood by kidneys and partially via bile and intestinal excretion. In the kidneys, after reaching certain conditions, such as high tubular concentration and damaged integrity of the tubule epithelium, oxalate can precipitate and initiate the formation of stones. Recent studies have indicated the importance of the SoLute Carrier 26 (SLC26) family of membrane transporters for handling oxalate. Two members of this family [Sulfate Anion Transporter 1 (SAT-1; SLC26A1) and Chloride/Formate EXchanger (CFEX; SLC26A6)] may contribute to oxalate transport in the intestine, liver, and kidneys. Malfunction or absence of SAT-1 or CFEX has been associated with hyperoxaluria and urolithiasis. However, numerous questions regarding their roles in oxalate transport in the respective organs and male-prevalent urolithiasis, as well as the role of sex hormones in the expression of these transporters at the level of mRNA and protein, still remain to be answered.

1. Bushinsky DA, Coe FL, Moe OW. Nephrolithiasis. In: Brenner BM, editor. The kidney. 8th ed. Vol 2. Philadelphia (PA): Saunders; 2008. p. 1299-1375.

2. Watts RWE. Idiopathic urinary stone disease: possible polygenic aetiological factors. Q J Med 2005;98:241-6. doi: 10.1093/qjmed/hci041

3. Sakhaee K. Nephrolithiasis as a systemic disorder. Curr Opin Nephrol Hypertens 2008;17:304-9. doi: 10.1097/ MNH.0b013e3282f8b34d

4. Coe FL, Parks JH. New insights into pathophysiology and treatment of nephrolithiasis: new research venues. J Bone M i n e r R e s 1 9 9 7 ; 1 2 : 5 2 2 - 3 3 . d o i : 1 0 . 1 3 5 9 / jbmr.1997.12.4.522

5. Coe FL, Parks JH. Pathogenesis and treatment of urolithiasis.

In: Seldin DW, Giebisch G, editors. The kidney. 3rd. ed. Vol II. Philadelphia (PA): Lippincott Williams & Wilkins; 2000. p. 1841-67.

6. Daudon M, Donsimoni R, Hennequin C, Fellahi S, Le Moel G, Paris M, Troupel S, Lacour B. Sex- and age-related composition of 10617 calculi analyzed by infrared spectroscopy. Urol Res 1995;23:319-26. doi: 10.1007/ BF00300021

7. Yoshida O, Okada Y. Epidemiology of urolithiasis in Japan: a chronological and geographical study. Urol Int 1990;45:104-11. doi: 10.1159/000281680

8. Robertson WG, Peacock M. The cause of idiopathic calcium stone disease: hypercalciuria or hyperoxaluria? Nephron 1980;26:105-10. doi: 10.1159/000181963

9. Pak CYC, Adams-Huet B, Poindexter JR, Pearle MS, Peterson RD, Moe OW. Relative effect of urinary calcium and oxalate on saturation of calcium oxalate. Kidney Int 2004;66:2032-7. doi: doi:10.1111/j.1523-1755.2004.00975.x

10. Coe FL, Evan A, Worcester E. Kidney stone disease. J Clin Invest 2005;115:2598-608. PMID: 16200192

11. Williams AW, Wilson DM. Dietary intake, absorption, metabolism and excretion of oxalate. Semin Nephrol 1990;10:2-8. PMID: 2404326

12. Hautman RE. The stomach: a new and powerful oxalate absorption site in man. J Urol 1993;149:1401-4. PMID: 8501776

13. Chen Z, Ye Z, Zeng L, Yang W. Clinical investigation on gastric oxalate absorption. Chin Med J 2003;116:1749-51.


14. Hagler L, Herman RH. Oxalate metabolism. Am J Clin Nutr 1973;26:758-65. PMID: 4576881

15. Singh PP, Kothari LK, Sharma DC, Saxena SN. Nutritional value of foods in relation to their oxalic acid conetent. Am J Clin Nutr 1972;25:1147-52. PMID: 5086037

16. Brinkley L, McGuire J, Gregory J, Pak CY. Bioavailability of oxalate in foods. Urology 1981;17:534-8. PMID: 7245443

17. Caliskan M. The metabolism of oxalic acid. Turk J Zoo 2000;24:103-6.

18. Tang M, Larson-Meyer E, Liebman M. Effect of cinnamon and turmeric on urinary oxalate excretion, plasma lipids, and plasma glucose in healthy subjects. Am J Clin Nutr 2008;87:1262-7. PMID: 18469248

19. Trinchieri A, Mandressi A, Luongo P, Longo G, Pisani E.

The infl uence of diet on urinary risk factors for stones in healthy subjects and idiopathic renal calcium stone formers.

Br J Urol 1991;67:230-6. PMID: 2021806

20. Prenen JAC, Boer P, Dorhout-Mess EJ. Absorption kinetics of oxalate from oxalate-rich food in man. Am J Clin Nutr 1984;40:1007-10. PMID: 6496379

21. Holmes RP, Goodman HO, Assimos DG. Dietary oxalate and its intestinal absorption. Scanning Microsc 1995;9:1109-20.

PMID: 8819892

22. Holmes RP, Assimos DG. The impact of dietary oxalate on kidney stone formation. Urol Res 2004;32:311-6. PMID: 15221245

23. Holmes RP, Goodman HO, Assimos DG. Contribution of dietary oxalate to urinary oxalate excretion. Kidney Int 2001;59:270-6. doi: 10.1046/j.1523-1755.2001.00488.x

24. Holmes RP, Kennedy M. Estimation of the oxalate content of foods and daily oxalate intake. Kidney Int 2000;57:1662-7. doi:10.1046/j.1523-1755.2000.00010.x

25. Siener R, Ebert D, Nicolay C, Hesse A. Dietary risk factors for hyperoxaluria in calcium oxalate stone formers. Kidney Int 2003;63:1037-43. doi: 10.1046/j.1523-1755.2003.00807. x

26. Tiselius HG, Ahistrand C, Lundstrom B, Nilsson MA. [14C]Oxalate Absorption by normal persons, calcium oxalate stone formers, and patients with surgically disturbed intestinal function. Clin Chem 1981;27:1682-5. PMID: 7285319

27. Dawson KA, Allison MJ, Hartman PA. Isolation and some characteristics of anaerobic oxalate-degrading bacteria from the rumen. Appl Environ Microbiol 1980;40:833-9. PMID: 7425628

28. Allison MJ, Cook HM, Milne DB, Gallagher S, Clayman RV. Oxalate degradation by gastrointestinal bacteria from humans. J Nutr 1986;116:455-60. PMID: 3950772

29. Argenzio RA, Liacos JA, Allison MJ. Intestinal oxalatedegrading bacteria reduce oxalate absorption and toxicity in guinea pigs. J Nutr 1988;118:787-92. PMID: 3373343

30. Kaufman DW, Kelly JP, Curhan GC, Anderson TE, Dretler SP, Preminger GM, Cave DR. Oxalobacter formigenes may reduce the risk of calcium oxalate kidney stones. J Am Soc N e p h r o l 2 0 0 8 ; 1 9 : 11 9 7 - 2 0 3 . d o i : 1 0 . 1 6 8 1 / ASN.2007101058

31. Zarembski PM, Hodgkinson A. Some factors infl uencing the urinary excretion of oxalic acid in man. Clin Chim Acta 1969;25:1-10. PMID: 4978800

32. Unruh GEV, Voss S, Sauerbruch T, Hesse A. Dependence of oxalate absorption on the daily calcium intake. J Am Soc Nephrol 2004;15:1567-73. PMID: 15153567

33. Hanes DA, Weaver CM, Heany RP, Wastney M. Absorption of calcium oxalate does not require dissociation in rats. J Nutr 1999;129:170-3. PMID: 9915895

34. Liebman M, Chai W. Effect of dietary calcium on urinary oxalate excretion after oxalate loads. Am J Clin Nutr 1997;65:1453-9. doi: 10.1016/0002-8223(93)91530

35. Liebman M, Costa G. Effects of calcium and magnesium on urinary oxalate excretion after oxalate loads. J Urol 2000;163:1565-9. doi: PMID: 10751889

36. Saunders DR, Sillery J, McDonald GB. Regional differences in oxalate absorption by rat intestine: evidence for excessive absorption by the colon in steatorrhoea. Gut 1975;16:543-8.

PMID: 1158192

37. Caspary WF, Tonissen J, Lankisch PG. “Enteral” hyperoxaluria. Effect of cholesyramine, calcium, neomycin, and bile acids on intestinal oxalate absorption in man. Acta Hepatogastroenterol 1977;24:193-200. PMID: 883468

38. Saso L, Grippa E, Gatto MT, Silvestrini B. Inhibition of calcium oxalate precipitation by bile salts. Int J Urol 2001;8:124-7. PMID: 11260337

39. Taylor EN, Curhan GC. Oxalate intake and the risk for nephrolithiasis. J Am Soc Nephrol 2007;18:2198-204. doi: 10.1681/ASN.2007020219

40. Poore RE, Hurst CH, Assimos DG, Holmes RP. Pathways of hepatic oxalate synthesis and their regulation. Am J Physiol Cell Physiol 1997;272:C289-94. PMID: 9038835

41. Yanagawa M, Maeda-Nakai E, Yamakawa K, Yamamoto I, Kawamura J, Tada S, Ichiyama A. The formation of oxalate from glycolate in rat and human liver. Biochim Biophys Acta 1990;1036:24-33. PMID: 2223823

42. Miller H, Barceloux DG, Krenzelok EP, Olson K, Watson W. American academy of clinical toxicology practice guidelines on the treatment of ethylene glycol poisoning.

Clin Toxicol 1999;37:537-60. PMID: 10497633

43. Langman CB. The molecular basis of kidney stones. Curr Opin Pediatr 2004;16:188-93. PMID: 15021200

44. Richardson KE, Tolbert NE. Oxidation of glyoxylic acid to oxalic acid by glycolic acid oxidase. J Biol Chem 1961;236:1280-4. PMID: 13741299

45. Haimovici J, Beck JS, Molla-Hosseini C, Vallerand D, Haddad P. Different modulation of hepatocellular Na+/H+ exchange activity by insulin and EGF. Am J Physiol Gastrointest Liver Physiol 1994;267:G364-70. PMID: 7943232

46. Selvam R. Calcium oxalate stone disease: role of lipid peroxidation and antioxidants. Urol Res 2002;30:35-47.

PMID: 11942324

47. Finlayson B. Physicochemical aspects of urolithiasis. Kidney Int 1978;13:344-60. doi: 10.1038/ki.1978.53

48. Verkoelen CF, Van Der Boom BG, Houtsmuller AB, Schroder FH, Romijn JC. Increased calcium oxalate monohydrate crystal binding to injured renal tubular epithelial cells in culture. Am J Physiol Renal Physiol 1998;274:F958-65.

PMID: 9612335

49. Phulwinder KG, Thurgood LA, Ryall RL. Effect of urine fractionation on attachment of calcium crystals to renal epithelial cells: implications for studying renal calculogenesis.

Am J Physiol Renal Physiol 2007;292:F1396-403. doi: 10.1152/ajprenal.00456.2006

50. Gambaro G, Valente ML, Zanetti E, Barbera MD, Del Prete D, D’Angelo A, Trevisan A. Mild tubular damage induces calcium oxalate crystalluria in a model of subtle hyperoxaluria: evidence that a second hit is necessary for renal lithogenesis.

J Am Soc Nephrol 2006;17:2213-9. PMID: 16790510

51. Hackett RL, Shevock PN, Khan SR. Madin-Darby canine kidney cells are injured by exposure to oxalate and to calcium oxalate crystals. Urol Res 1994;22:197-203. PMID: 7871629

52. Scheid C, Koul H, Hill WA, Luber-Narod J, Kennington L, Honeyman T, Jonassen J, Menon M. Oxalate toxicity in LLC-PK1 cells: role of free radicals. Kidney Int 1996;49:413-9. doi: 10.1038/ki.1996.60

53. Thamilselvan S, Byer KJ, Hackett RL, Khan SR. Free radical scavengers, catalase and superoxide dismutase provide protection from oxalate-associated injury to LLC-PK1 and MDCK sells. J Urol 2000;164:224-9. PMID: 10840464

54. Grases F, Garcia-Ferragut L, Costa-Bauza A. Development of calcium oxalate crystals on urothelium: effect of free r a d i c a l s . N e p h r o n 1 9 9 8 ; 7 8 : 2 9 6 - 3 0 1 . d o i : 10.1159/000044939

55. Thamilselvan S, Hackett RL, Khan SR. Lipid peroxidation in ethylene glycol induced hyperoxaluria and calcium oxalate nephrolithiasis. J Urol 1997;157:1059-63. PMID: 9072543

56. Huang HS, Chen CF, Chien CT, Chen J. Possible biphasic changes of free radicals in ethylene glycol-induced nephrolithiasis in rats. BJU Int 2000;85:1143-9. PMID: 10848711

57. Huang HS, Ma MC, Chen J, Chen CF. Changes in oxidantantioxidant balance in the kidney of rats with nephrolithiasis induced by ethylene glycol. J Urol 2002;167:2584-93. doi: 10.1016/S0022-5347(05)65042-2

58. Huang HS, Ma MC, Chen J, Chen CF. Changes in renal hemodynamycs and urodynamics in rats with chronic hyperoxaluria and after acute oxalate infusion: role of free radicals. Neurourol Urodynam 2003;22:176-82. PMID: 12579636

59. Umekawa T, Chegini N, Khan SR. Oxalate ions and calcium oxalate crystals stimulate MCP-1 expression by renal epithelial cells. Kidney Int 2002;61:105-12. doi: 10.1046/ j.1523-1755.2002.00106.x

60. Umekawa T, Chegini N, Khan SR. Increased expression of monocyte chemoattractant protein-1 (MCP-1) by renal epithelial cells in culture on exposure to calcium oxalate, phosphate, and uric acid crystals. Nephrol Dial Transplant 2003;18:664-9. doi: 10.1093/ndt/gfg140

61. Umekawa T, Byer K, Uemura H, Khan SR. Diphenyleneiodium (DPI) reduces oxalate ion- and calcium oxalate monohydrate and brushite crystal-induced upregulation of MCP-1 in NRK52E cells. Nephrol Dial Transplant 2005;20:870-8. doi: 10.1093/ndt/gfh750

62. Lieske JC, Leonard R, Toback FG. Adhesion of calcium oxalate monohydrate crystals to renal epithelial cells is inhibited by specific anions. Am J Physiol Renal Fluid Electrolyte Physiol 1995;268:F604-12. PMID: 8769839

63. Kumar V, Yu S, Farell G, Toback FG, Lieske JC. Renal epithelial cells constitutively produce a protein that blocks adhesion of crystals to their surface. Am J Physiol Renal P h y s i o l 2 0 0 4 ; 2 8 7 : F 3 7 2 - 8 3 . d o i : 1 0 . 11 5 2 / ajprenal.00418.2003

64. Wesson JA, Worcester EM, Wiessner JH, Mandel NS, Kleinman JG. Control of calcium oxalate crystal structure and cell adherence by urinary macromolecules. Kidney Int 1998;53:952-7. doi: 10.1111/j.1523-1755.1998.00839.x

65. Yagisawa T, Chandhoke PS, Fan J, Lucia S. Renal osteopontin expression in experimental urolithiasis. J Endourol 1998;12:171-6. PMID: 9607445

66. Khan SR, Johnson JM, Peck AB, Cornelius JG, Glenton PA.

Expression of osteopontin in rat kidneys: induction during ethylene glycol induced calcium oxalate nephrolithiasis. J U r o l 2 0 0 2 ; 1 6 8 : 11 7 3 - 8 1 . d o i : 1 0 . 1 0 9 7 / 0 1 . ju.0000024398.45396.6c

67. Sokalingum NP, Asplin JR, Coe FL. Evidence that calgranulin is produced by kidney cells and is inhibitor of calcium oxalate crystallization. Am J Physiol Renal Physiol 1998;275:F255-61. PMID: 9691016

68. Hess B, Jordi S, Zipperle LJ, Ettinger E, Giovanoli R. Citrate determines calcium oxalate crystallization kinetics and crystal morphology - studies in the presence of Tamm- Horsfall protein of a healthy subject and severely recurrent calcium stone former. Nephrol Dial Transplant 2000;15:366-74. doi: 10.1093/ndt/15.3.366

69. Grover PK, Thurgood LA, Fleming DE, van Bronswijk W, Wang T, Ryall RL. Intracrystalline urinary proteins facilitate degradation and dissolution of calcium oxalate crystals in cultured renal cells. Am J Physiol Renal Physiol 2008;294: F355-61. doi: 10.1152/ajprenal.00529.2007

70. Atmani F, Khan SR. Characterization of uronic acid-rich inhibitor of calcium crystallization isolated from rat urine.

Urol Res 1995;3:95-101. doi: 10.1007/BF00307939

71. Iida S, Peck AB, Johnosn-Tardieu J, Moriyama M, Glenton PA, Byer KJ, Khan Sr. Temporal changes in mRNA expression for Bikunin in the kidneys of rats during calcium oxalate nephrolithiasis. J Am Soc Nephrol 1999;10:986-96.

PMID: 10232684

72. Selvam R, Adhirai M. Vitamin E pretreatment prevents cyclosporine A-induced crystal deposition in hyperoxaluric rats. Nephron 1997;75:77-81. doi: 10.1159/000189503

73. Reckelhoff JF, Kanji V, Racusen LC, Schmidt AM, Yan SD, Morrow J, Roberts LJ, Salahudeen AK. Vitamin E ameliorates enhanced renal lipid peroxidation and accumulation of F2- isoprostanes in aging kidneys. Am J Physiol Regul Integr Comp Physiol 1998;274:R767-74. PMID: 9530244

74. Huang HS, Chen J, Chen CF, Ma MC. Vitamin E attenuates crystal formation in rat kidneys: role of renal tubular cell death and crystallization inhibitors. Kidney Int 2006;70:699-710. doi: 10.1038/sj.ki.5001651

75. Huang HS, Ma MC, Chen J. Low vitamin E diet exacerbates calcium oxalate crystal formation via enhanced oxidative stress in rat hyperoxaluric kidney. Am J Physiol Renal Physiol 2009;296:F34-45. doi: 10.1152/ajprenal.90309.2008

76. Gershoff SN, Faragalla FF. Endogenous oxalate synthesis and glycine, serine, deoxypyridoxine interrelationships in vitamin B6-deficient rats. J Biol Chem 1959;234:2391-3.

PMID: 13827605

77. Gershof SN, Prien EP, Faragalla FF, Shen GSH, Kearny MM.

Excretion of urinary metabolites in calcium oxalate urolithiasis. Effect of tryptophan and vitamin B6 administration. Am J Clin Nutr 1960;8:812-6. PMID: 13704750

78. Runyan TJ, Gershoff SN. The effect of vitamin B6 defi ciency in rats on the metabolism of oxalic acid precursors. J Biol Chem 1965;240:1889-92. PMID: 14299606

79. Ravichandran V, Selvam R. Increased lipid peroxidation in kidney of vitamin B-6 defi cient rats. Biochem Int 1990;21:599-605. PMID: 2241985

80. Curhan GC, Willet WC, Speizer FE, Stamper MJ. Inatke of vitamin B6 and C and the risk of kidney stones in women. J Am Soc Nephrol 1999;10:840-5. PMID: 10203369

81. Ribaya JD, Gershoff SN. Effects of hydroxyproline and vitamin B-6 on oxalate synthesis in rats. J Nutr 1981;111:1231-9. PMID: 6788912

82. Sakly R, Achour A, Zouaghi H. Etude sur l’action antilithogene et litholytique de la vitamine A vis-a-vis de la lithiase experimentale chez le rat [Antilithogenic and litholytic action of vitamin A vis-a-vis experimental calculi in rats, in French]. Ann Urol (Paris) 1994;28:128-31.

83. Urivetzky M, Kessaris D, Smith AD. Ascorbic acid overdosing: a risk factor for calcium oxalate. J Urol 1992;147:1215-8. PMID: 1569652

84. Massey LK, Liebman M, Kynast-Gales SA. Ascorbate increases human oxaluria and kidney stone risk. J Nutr 2005;135:1673-7. PMID: 15987848

85. Ribaya-Mercado JD, Gershoff SN. Effects of sugars and vitamin B-6 defi ciency on oxalate synthesis in rats. J Nutr 1984;114:1447-53. PMID: 6747727

86. Welshman SG, McGeown MG. Urinary citrate excretion in stone-formers and normal controls. Br J Urol 1976;48:7-11. doi: 10.1111/j.1464-410X.1976.tb02731.x

87. Osther PJ. [Citrate and kidney stones, in Danish]. Ugeskr Laeger 1993;155:3835-9. PMID: 8256384

88. Rudman D, Kutner MH, Redd SC, Waters WC, Gerron GG, Bleier J. Hypocitraturia in calcium nephrolithiasis. J Clin Endocrinol Metab 1982;55:1052-7. PMID: 7130336

89. Cowley DM, McWhinney BC, Brown JM, Chaimers AH.

Effect of citrate on the urinary excretion of calcium and oxalate: relevance to calcium oxalate nephrolithiasis. Clin Chem 1989;35:23-8. PMID: 2910576

90. Goldberg H, Grass L, Vogl R, Rapaport A, Oreopoulos DG.

Urine citrate and renal stone disease. Can Med Assoc J 1989;141:217-21. PMCID: PMC1269410

91. Tiselius HG, Berg C, Fornander AM, Nilsson MA. Effects of citrate on the different phases of calcium oxalate crystallization. Scanning Microsc 1993;7:381-90. PMID: 8316807

92. Mount DB, Romero MF. The SLC26 gene family of multifunctional anion exchangers. Pfl ugers Arch - Eur J Physiol 2004;447:710-21. doi: 10.1007/s00424-003-1090-3

93. Hatch M, Freel RW. Intestinal transport of an obdurate anion: oxalate. Urol Res 2005;33:1-16. PMID: 15565438

94. Sindic A, Chang MH, Mount DB, Romero MF. Renal physiology of SLC26 anion exchangers. Curr Opin Nephrol Hypertens 2007;16:484-90. PMID: 17693766

95. Dorwart MR, Shcheynikov N, Yang D, Muallem S. The solute carrier 26 family of proteins in epithelial ion transport.

P h y s i o l o g y 2 0 0 8 ; 2 3 : 1 0 4 - 1 4 . d o i : 1 0 . 11 5 2 / physiol.00037.2007

96. Quandamatteo F, Krick W, Schubert K, Brzica H, Balen D, Sabolic I, Burckhardt G, Burckhardt BC. Localization of sat-1 (slc26a6) along the gastrointestinal tract. Acta Physiol 2007;189 (Suppl 653):56.

97. Wang Z, Petrovic S, Mann E, Soleimani M. Identifi cation of an apical Cl-/HCO3 - exchanger in the small intestine. Am J Physiol Gastrointest Liver Physiol 2002;282:G573-9. doi: 10.1152/ajpgi.00338.2001

98. Xie Q, Welch R, Mercado A, Romero MF, Mount DB.

Molecular characterization of the murine Slc26a6 anion exchanger: functional comparison with Slc26a1. Am J Physiol Renal Physiol 2002;283:F826-38. doi: 10.1152/ ajprenal.00079.2002

99. Petrovic S, Wang Z, Ma L, Seidler U, Forte JG, Shull GE, Soleimani M. Colocalization of the apical Cl-/HCO3 - exchanger PAT1 and gastric H-K-ATPase in stomach parietal cells. Am J Physiol Gastrointest Liver Physiol 2002;283: G1207-16. PMID: 12381535

100. Petrovic S, Ju X, Barone S, Siedler U, Alper SL, Lohi H, Kere J, Soleimani M. Identifi cation of a basolateral Cl-/HCO exchanger specifi c to gastric parietal cells. Am J Physiol Gastrointest Liver Physiol 2003;284:G1093-103. doi: 10.1152/ajpgi.00454.2002

101. Hofmann AF, Laker MF, Dharmsathaphorn K, Sherr HP, Lorenzo D. Complex pathogenesis of hyperoxaluria after jejunoileal bypass surgery. Oxalogenic substances in diet contribute to urinary oxalate. Gastroenterology 1983;84:293-300. PMID: 6848409

102. Hatch M, Freel RW, Goldner AM, Earnest DL. Oxalate and chloride absorption by the rabbit colon: sensitivity to metabolic and anion transport inhibitors. Gut 1984;25:232-7. doi: 10.1136/gut.25.3.232

103. Knickelbein RG, Aronson PS, Dobbins JW. Oxalate transport by anion exchange across rabbit ileal brush border. J Clin Invest 1986;77:170-5. doi: 10.1172/JCI112272

104. Hatch M, Freel RW, Vaziri ND. Characteristics of the transport of oxalate and other ions across rabbit proximal colon. Pfl ugers Arch - Eur J Physiol 1993;423:206-12. doi: 10.1007/BF00374396

105. Hatch M, Freel RW, Vaziri ND. Mechanisms of oxalate absorption and secretion across the rabbit distal colon.

Pflugers Arch - Eur J Physiol 1994;426:101-9. PMID: 8146012

106. Wang Z, Wang T, Petrovic S, Tuo B, Riederer B, Barone S, Lorenz JN, Seidler U, Aronson PS, Soleimani M. Renal and intestinal transport defects in Slc26a6-null mice. Am J Physiol Cell Physiol 2005;288:C957-65. doi: 10.1152/ ajpcell.00505.2004

107. Freel RW, Hatch M, Green M, Soleimani M. Ileal oxalate absorption and urinary oxalate excretion are enhanced in Slc26a6 null mice. Am J Physiol Gastrointest Liver Physiol 2006;290:G719-28. doi: 10.1152/ajpgi.00481.2005

108. Jiang Z, Asplin JR, Evan AP, Rajendran VM, Velazquez H, Nottoli TP, Binder HJ, Aronson PS. Calcium oxalate urolithiasis in mice lacking anion transporter Slc26a6. Nat Genet 2006;38:474-8. PMID: 16532010

109. Soleimani M. The role of SLC26A6-mediated chloride/ oxalate exchange in causing susceptibility to nephrolithiasis.

J P h y s i o l 2 0 0 8 ; 5 8 6 : 1 2 0 5 - 6 . d o i : 1 0 . 1113 / jphysiol.2007.150565

110. Hatch M, Freel RW, Vaziri ND. Intestinal excretion of oxalate in chronic renal failure. J Am Soc Nephrol 1994;5:1339-43.

PMID: 7893999

111. Freel RW, Hatch M, Vaziri ND. Conductive pathways for chloride and oxalate in rabbit ileal brush-border membrane vesicles. Am J Physiol Cell Physiol 1998;275:C748-57.

PMID: 9730958

112. Lee A, Beck L, Markovich D. The mouse sulfate anion transporter gene sat1 (Slc26a6): cloning, tissue distribution, gene structure, functional characterization, and transcriptional regulation by thyroid hormone. DNA Cell Biol 2003;22:19-31. doi: 10.1089/104454903321112460

113. Regeer RR, Lee A, Markovich D. Characteriaztion of the human sulfate anion transporter (hsat-1) protein and gene.

DNA Cell Biol 2003;22:107-17. PMID: 12713736

114. Hatch M, Freel RW. The roles and mechanisms of intestinal oxalate transport in oxalate homeostasis. Semin Nephrol 2008;28:143-51. doi: 10.1016/j.semnephrol.2008.01.007

115. Robijn S, Hoppe B, Vervaet BA, D’Haese PC, Verhulst A.

Hyperoxaluria: a gut-kidney axis? Kidney Int 2011;80:1146-58. doi: 10.1038/ki.2011.287

116. Quondamatteo F, Krick W, Hagos Y, Kruger MH, Neubauer- Saile K, Herken R, Ramadori G, Burckhardt G, Burckhardt BC. Localization of sulfate/anion exchanger in the rat liver.

Am J Physiol Gastrointest Liver Physiol 2006;290:G1075-81. doi: 10.1152/ajpgi.00492.2005

117. Brzica H, Breljak D, Krick W, Lovric M, Burckhardt G, Burckhardt BC, Sabolic I. The liver and kidney expression of sulfate anion transporter sat-1 in rats exhibits maledominant gender differences. Pfl ugers Arch Eur J Physiol 2009;457:1381-92. doi: 10.1007/s00424-008-0611-5

118. Karniski LP, Lotscher M, Fucentese M, Hilfi ker H, Biber J, Murer H. Immunolocalization of sat-1 sulfate/oxalate/ bicarbonate anion exchanger in the rat kidney. Am J Physiol Renal Physiol 1998;275:F79-87. PMID: 9689008

119. Brzica H, Balen D, Breljak D, Ljubojevic M, Zlender V, Burckhardt BC, Burckhardt G, Sabolic I. Immunolocalization of Na+-independent sulfate transporter Sat-1 (Slc26a1) in rat kidney and gastrointestinal tract. Period Biol 2007;109(Suppl 2):148.

120. Ko N, Knauf F, Jiang Z, Markovich D, Aronson PS. Sat1 is dispensable for active oxalate secretion in mouse duodenum.

Am J Physiol Cell Physiol 2012;303:C52-7. doi: 10.1152/ ajpcell.00385.2011

121. Silberg DG, Wang W, Moseley H, Traber PG. The down regulated in adenoma (dra) gene encodes intestine-specifi c membrane sulfate transporter protein. J Biol Chem 1995;270:11897-902. doi: 10.1074/jbc.270.20.11897

122. Byeon MK, Frankel A, Papas TS, Henderson KW, Schweinfest CW. Human DRA functions as a sulfate transporter in Sf9 insect cells. Protein Expr Purif 1998;12:67-74. PMID: 9473459

123. Jacob P, Rosmann H, Lamprecht G, Kretz A, Neff C, Lin-Wu E, Gregor M, Groneberg DA, Kere J, Sedler U. Downregulated in adenoma mediates apical Cl-/HCO3- exchange in rabbit, rat, and human duodenum. Gastroenterology 2002;122:709-24. doi: 10.1053/gast.2002.31875

124. Schweinfest CW, Spyropoulos DD, Henderson KW, Kim JH, Chapman JM, Barone S, Worell RT, Wang Z, Soleimani M. slc26a3 (dra)-defi cient mice display chloride-losing diarrhea, enhanced colonic proliferation and distinct up-regulation of ion transporters in the colon. J Biol Chem 2006;281:37962-71. doi: 10.1074/jbc.M607527200

125. Hoglund P, Halia S, Socha J, Tomaszewski I, Saarialho-Kere U, Karjalainen-Lindsberg ML, Airola K, Holmerg C, de la Chapelle A, Kere J. Mutations of the down-regulated in adenoms (DRA) gene cause congenital chloride diarrhoea.

Nat Genet 1996;14:316-9. doi: 10.1038/ng1196-316

126. Haila S, Saarialho-Kere U, Karjalainen-Lindsberg ML, Lohi H, Airola K, Holmberg C, Hastbacka J, Kere J, Hoglund P.

The congenital chloride diarrhea gene is expressed in seminal vesicle, sweat gland, infl ammatory colon epithelium, and in some dysplastic colon cells. Histochem Cell Biol 2000;113:279-86. PMID: 10857479

127. Freel RW, Morozumi M, Hatch M. Parsing apical oxalate exchange in Caco-2BBe1 monolayers: siRNA knockdown of SLC26A6 reveals the roles and properties of PAT-1. Am J Physiol Gastrointest Liver Physiol 2009;297:G918-G929.

128. Heneghan JF, Akhvaein A, Salas M, Shmukler BE, Karniski LP, Vandorpe DH, Alper SL. Regulated transport of sulfate and oxalate by SLC26A2/DTDST. Am J Physiol Cell Physiol 2010;298:C1363-75. doi: 10.1152/ajpcell.00004.2010

129. Hugentobler G, Meier PJ. Multispecifi c anion exchange in basolateral (sinusoidal) rat liver plasma membrane vesicles.

Am J Physiol Gastrointest Liver Physiol 1986;251:G656-64.

PMID: 3777171

130. Bissig M, Hagenbuch B, Stieger B, Koller T, Meier PJ.

Functional expression cloning of the canalicular sulfate transport system of rat hepatocytes. J Biol Chem 1994;269:3022-6. PMID: 8300633

131. Krick W, Schnedler N, Burckhardt G, Burckhardt BC. Ability of sat-1 to transport sulfate, bicarbonate, or oxalate under physiological conditions. Am J Physiol Renal Physiol 2009;297:145-54. doi: 10.1152/ajprenal.90401.2008

132. Cattell WR, Spencer AG, Taylor GW, Watts RWE. The mechanism of the renal oxalate excretion in the dog. Clin Sci 1962;22:43-52. PMID: 13877395

133. Williams HE, Johnson GA, Smith LH. The renal clearance of oxalate in normal subjects and patients with primary hyperoxaluria. Clin Sci 1971;41:213-8. PMID: 5571501

134. McIntosh GH, Belling GB. An isotopic study of oxalate excretion in sheep. Aust J Exp Biol Med Sci 1975;53:479-87.

PMID: 1230144

135. Greger R, Lang F, Oberleithner H, Deetjen P. Handling of oxalate by the rat kidney. Pfl ugers Arch 1978;374:243-8. doi: 10.1007/BF00585601

136. Weinman EJ, Frankfurt SJ, Ince A, Sansom S. Renal tubular transport of organic acids. J Clin Invest 1978;61:801-6. doi: 10.1172/JCI108994

137. Knight TF, Senekjian HO, Weinman EJ. Effect of paraaminohippurate on renal transport of oxalate. Kidney Int 1979;15:38-42. doi: 10.1038/ki.1979.5

138. Knight TF, Sansom SC, Senekjian HO, Weinman EJ. Oxalate secretion in the rat proximal tubule. Am J Physiol Renal Fluid Electrolyte Physiol 1981;240:F295-8. PMID: 7223887

139. Senekjian HO, Weinman EJ. Oxalate transport by proximal tubule of the rabbit kidney. Am J Physiol Renal Fluid Electrolyte Physiol 1982;243:F271-5. PMID: 7114257

140. Low I, Friedrich T, Burckhardt G. Properties of an anion exchanger in rat renal basolateral membrane vesicles. Am J Physiol Renal Fluid Electrolyte Physiol 1984;246:F334-42.

PMID: 6703066

141. Hagenbuch B, Stange G, Murer H. Transport of sulphate in rat jejuna and rat proximal tubular basolateral membrane vesicles. Pflugers Arch 1985;405:202-8. doi: 10.1007/ BF00582561

142. Kuo SM, Aronson PS. Oxalate transport via the sulfate/HCO3 exchanger in rabbit renal basolateral membrane vesicles. J Biol Chem 1988;263:9710-7. PMID: 3384817

143. Markovich D, Bissig M, Sorribas V, Hagenbuch B, Meier PJ, Murer H. Expression of rat renal sulfate transport systems in Xenopus Laevis oocytes. J Biol Chem 1994;269:3022-6.

PMID: 8300634

144. Brandle E, Bernt U, Hautmann RE. In situ characterization of oxalate transport across the basolateral membrane of the proximal tubule. Pfl ugers Arch 1998;435:840-9. 10.1007/ s004240050592

145. Karniski LP, Aronson PS. Chloride/formate exchange with formic acid recycling: a mechanism of active chloride transport across epithelial membranes. Proc Natl Acad Sci USA 1985;82:6362-5. PMCID: PMC391054

146. Karniski LP, Aronson PS. Anion exchange pathways for Cltransport in rabbit renal microvillus membranes. Am J Physiol Renal Fluid Electrolyte Physiol 1987;253:F513-21. PMID: 3631282

147. Koul H, Ebisuno S, Renzulli L, Yanagawa, Menon M, Scheid C. Polarized distribution of oxalate transport systems in LLC-PK1 cells, a line of renal epithelial cells. Am J Physiol Renal Fluid Electrolyte Physiol 1994;266:F266-74. PMID: 8141327

148. Kuo SM, Aronson PS. Pathways for oxalate transport in rabbit renal microvillus membrane vesicles. J Biol Chem 1996;271:15491-7. PMID: 8663096

149. Knauff F, Yang CL, Thomson RB, Mentone SA, Giebisch G, Aronson PS. Identifi cation of a chloride-formate exchanger expressed on the brush border membrane of renal proximal tubule cells. Proc Natl Acad Sci USA 2001;98:9425-30. doi: 10.1073/pnas.141241098

150. Jiang Z, Grichtchenko II, Boron WF, Aronson PS. Specifi ty of anion exchange mediated by mouse Slc26a6. J Biol Chem 2002;277:33963-7. PMID: 12119287

151. Wang T, Egbert AL, Abbiati T, Aronson PS, Giebisch G.

Mechanisms of stimulation of proximal tubule chloride transport by formate and oxalate. Am J Physiol Renal Fluid Electrolyte Physiol 1996;271:F446-50. PMID: 8770178

152. Aronson PS. Essential roles of CFEX-mediated Cl--oxalate exchange in proximal tubule NaCl transport and prevention of urolithiasis. Kidney Int 2006;70:1207-13. doi: 10.1038/ sj.ki.5001741

153. Markovich D. Slc13a1 and Slc26a1 KO models reveal physiological roles of anion transporters. Physiology 2012;27:7-14. doi: 10.1152/physiol.00041.2011

154. Laski ME, Kurtzman NA, Sabatini S. Chronic renal failure.

In: Seldin DW, Giebisch G, editors. The Kidney, 3rd ed. Vol II. Philadelphia (PA): Lippincott Williams & Wilkins; 2000. p. 2375-409.

155. Costello J, Smith M, Stolarski C, Sadovnic MJ. Extrarenal clearance of oxalate increases with progression of renal failure in the rat. J Am Soc Nephrol 1992;3:1098-104. PMID: 1482750

156. Fernandes I, Laouari D, Tutt P, Hampson G, Friedlander G, Silve C. Sulfate homeostasis, NaSi-1 cotransporter, and SAT-1 exchanger in chronic renal failure in rats. Kidney Int 2001;59:210-21. doi: 10.1046/j.1523-1755.2001.00481.x

157. Khan SR, Glenton PA. Calcium oxalate crystal deposition in kidneys of hypercalciuric mice with disrupted type IIa sodium-phosphate cotransporter. Am J Physiol Renal Physiol 2008;294:F1109-15. doi: 10.1152/ajprenal.00620.2007

158. Koutsoukos PG, Sheehan ME, Nancollas GH. Epitaxial considerations in urinary stone formation II. The oxalatephosphate system. Invest Urol 1981;18:358-63. PMID: 7203960

159. Evan AP, Lingeman JE, Coe FL, Parks JH, Bledsoe SB, Shao Y, Sommer AJ, Paterson RF, Kuo RL, Grynpas M. Randall’s plaque of patients with nephrolithiasis begins in basement membranes of thin loops of Henle. J Clin Invest 2003;111:607-16. doi: 10.1172/JCI200317038

160. He Y, Chen X, Yu Z, Wu D, Lv Y, Shi S, Zhu H. Sodium dicarboxylate cotransporter-1 expression in renal tissues and its role in rat experimental nephrolithiasis. J Nephrol 2004;17:34-42. PMID: 15151257

161. Kohri K, Ishikawa Y, Katoh Y, Kataoka K, Iguchi M, Yachiku S, Kurita T. Epidemiology of urolithiasis in the elderly. Int Urol Nephrol 1991;23:413-21. PMID: 1938239

162. Dall’era J, Kim F, Chandhoke PS. Gender differences among Hispanics and Caucasians in symptomatic presentation of kidney and ureteral stones. J Endourol 2005;159:283-6.

PMID: 15865513

163. Costa-Bauza A, Ramis M, Montesinos V, Conte A, Piza P, Pieras P, Grases F. Type of renal calculi: variation with age and sex. World J Urol 2007;25:415-21. doi. 10.1007/s00345-007-0177-4

164. Lemann J, Pleuss JA, Worcester EM, Hornick L, Schrab D, Hoffman RG. Urinary oxalate excretion increases with body size and decreases with increasing dietary calcium intake among healthy adults. Kidney Int 1996;49:200-8. PMID: 8770968

165. Daudon M, Lacour B, Jungers P. Infl uence of body size on urinary stone composition in men and women. Urol Res 2006;34:193-9. PMID: 16474948

166. Lee YH, Huang WC, Huang JK, Chang LS. Testosterone enhances whereas estrogen inhibits calcium oxalate stone formation in ethylene glycol treated rats. J Urol 1996;156:502-5. doi: 10.1097/00005392-199608000-00071

167. Yoshihara H, Yamaguchi S, Yachiku S. Effect of sex hormones on oxalate-synthesizing enzymes in male and female rat livers. J Urol 1999;161:668-73. doi: 10.1097/00005392-199902000-00097

168. Dembic Z, Sabolic I. Alcohol dehydrogense activity in rat kidney cortex stimulated by oestradiol. Biochim Biophys Acta 1982;714:331-6. doi: 10.1016/0304-4165(82)90341-5

169. Qulali M, Ross RA, Crabb DW. Estradiol induces class I alcohol dehydrogenase activity and mRNA in kidney of female rats. Arch Biochem Biophys1991;288:406-13. PMID: 1716872

170. Harada S, Tachiyashiki K, Imaizumi K. Effect of sex hormones on rat liver cytosolic alcohol dehydrogenase activity. J Nutr Sci Vitaminol 1998;44:625-39. PMID: 9919483

171. Rachamin G, Israel Y. Sex differences in hepatic alcohol dehydrogenase activity in animal species. Biochem Pharmacol 1985;34:2385-6. PMID: 3160354

172. Simon FR, Fortune J, Iwahashi M, Sutherland E. Sexual dimorphic expression of ADH in rat liver: importance of the hypothalamic-pituitary-liver axis. Am J Physiol Gastrointest Liver Physiol 2002;283:G646-55. PMID: 12181179

173. Yoshioka I, Tsujihata M, Momohara C, Wongsawat A, Nonomura N, Okuyama A. Effect of sex-hormones on crystal formation in a stone-forming rat model. Urology 2010;75:907-13. doi: 10.1016/j.urology.2009.09.094

174. Wegner W, Burckhardt BC, Burckhardt G, Henjakovic M.

Male-dominant activation of rat renal organic anion transporter 1 (Oat1) and 3 (Oat3) expression by transcription factor BCL6. PLoS ONE 2012;7:e35556. doi: 10.1371/ journal.pone.0035556

175. Iguchi M, Takamura C, Umekawa T, Kurita T, Kohri K.

Inhibitory effects of female sex hormones on urinary stone formation in rats. Kidney Int 1999;56:479-85. PMID: 10432386

176. Sabolic I, Asif AR, Budach WE, Wanke C, Bahn A, Burckhardt G. Gender differences in kidney function.

Pfl ugers Arch - Eur J Physiol 2007;455:397-29. doi: 10.1007/ s00424-007-0308-1

177. Jennings ML, Al-Rhaiyel S. Modifi cation of a carboxyl group that appears to cross the permeability barrier in the red blood cell anion transporter. J Gen Physiol 1988;92:161-78. PMID: 3171537

178. Jennings ML, Adame MF. Characterization of oxalate transport by the human erythrocyte band 3 protein. J Gen Physiol 1996;107:145-59. doi: 10.1085/jgp.107.1.145

179. Gambaro G, Marchini F, Piccoli A, Nassuato MA, Bilora F, Baggio B. The abnormal red-cell oxalate transport is a risk factor for idiopathic calcium nephrolithiasis: a prospective study. J Am Soc Nephrol 1996;7:608-12. PMID: 8724895

180. Hatch M, Freel RW, Vaziri ND. Local upregulation of colonic angiotensin II receptors enhances potassium excretion in chronic renal failure. Am J Physiol Renal Physiol 1998;274: F275-82. PMID: 9486222

181. Hatch M, Freel RW, Shahnifar S, Vaziri ND. Effects of specifi c angiotensin II receptor antagonist losartan on urate homeostasis and intestinal urate transport. J Pharmacol Exp Ther 1996;276:187-93. PMID: 8558429

182. Hatch M, Freel RW, Vaziri ND. AT1 receptor up-regulation in intestine in chronic renal failure is segment specifi c.

Pflugers Arch - Eur J Physiol 1999;437:881-7. PMID: 10370066

183. Hatch M, Freel RW. Angiotensin II involvement in adaptive enteric oxalate excretion in rats with chronic renal failure induced by hyperoxaluria. Urol Res 2003;31:426-32. PMID: 14574528

184. Gershoff SN. Production of urinary calculi in vitamin B6 defi cient male, female and castrated male rats. J Nutrition 1969;100:117-22. PMID: 5412125

185. Markovich D, James KM. Heavy metals mercury, cadmium, and chromium inhibit the activity of the mammalian liver and kidney sulfate transporter sat-1. Toxicol Appl Pharmacol 1999;154:181-7. PMID: 9925802

186. Chernova MN, Jiang L, Friedman DJ, Darman RB, Lohi H, Kere J, Vandorpe DH, Alper SL. Functional comparison of mouse slc26a6 anion exchanger with human SLC26A6 polypeptide variants. J Biol Chem 2005;280:8564-80. PMID: 15548529

187. Clark JS, Vandorpe DH, Chernove MN, Heneghan JF, Stewart AK, Alper SL. Species differences in Cl- affi nity and in electrogenicity of SLC26A6-mediated oxalate/Cl- exchange correlate with the distinct human and mouse susceptibilities to nephrolithiasis. J Physiol 2008;586:1291-306. doi: 10.1113/jphysiol.2007.143222

188. Schnedler N, Burckhardt G, Burckhardt BC. Glyoxylate is a substrate of the sulfate-oxalate exchanger, sat-1, and increases its expression in HepG2 cells. J Hepatol 2011;54:513-20. doi: 10.1016/j.jhep.2010.07.036

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