Skip to main content
Top
Published in: Urolithiasis 3/2019

01-06-2019 | Original Paper

Oxalate transport by the mouse intestine in vitro is not affected by chronic challenges to systemic acid–base homeostasis

Authors: Jonathan M. Whittamore, Marguerite Hatch

Published in: Urolithiasis | Issue 3/2019

Login to get access

Abstract

In rats, we recently showed how a chronic metabolic acidosis simultaneously reduced urinary oxalate excretion and promoted oxalate secretion by the distal colon leading to the proposition that acid–base disturbances may trigger changes to renal and intestinal oxalate handling. The present study sought to reproduce and extend these observations using the mouse model, where the availability of targeted gene knockouts (KOs) would offer future opportunities to reveal some of the underlying transporters and mechanisms involved. Mice were provided with a sustained load of acid (NH4Cl), base (NaHCO3) or the carbonic anhydrase inhibitor acetazolamide (ATZ) for 7 days after which time the impacts on urinary oxalate excretion and its transport by the intestine were evaluated. Mice consuming NH4Cl developed a metabolic acidosis but urinary oxalate was only reduced 46% and not statistically different from the control group, while provision of NaHCO3 provoked a significant 2.6-fold increase in oxalate excretion. For mice receiving ATZ, the rate of urinary oxalate excretion did not change significantly. Critically, none of these treatments altered the fluxes of oxalate (or chloride) across the distal ileum, cecum or distal colon. Hence, we were unable to produce the same effects of a metabolic acidosis in mice that we had previously found in rats, failing to find any evidence of the ‘gut-kidney axis’ influencing oxalate handling in response to various acid–base challenges. Despite the potential advantages offered by KO mice, this model species is not suitable for exploring how acid–base status regulates oxalate handling between the kidney and intestine.
Literature
4.
go back to reference Costello JF, Smith M, Stolarski C, Sadovnic MJ (1992) Extrarenal clearance of oxalate increases with progression of renal-failure in the rat. J Am Soc Nephrol 3(5):1098–1104PubMed Costello JF, Smith M, Stolarski C, Sadovnic MJ (1992) Extrarenal clearance of oxalate increases with progression of renal-failure in the rat. J Am Soc Nephrol 3(5):1098–1104PubMed
5.
go back to reference Hatch M, Freel RW, Vaziri ND (1994) Intestinal excretion of oxalate in chronic-renal-failure. J Am Soc Nephrol 5(6):1339–1343PubMed Hatch M, Freel RW, Vaziri ND (1994) Intestinal excretion of oxalate in chronic-renal-failure. J Am Soc Nephrol 5(6):1339–1343PubMed
11.
go back to reference Charney AN, Goldfarb DS, Dagher PC (1995) Metabolic disorders associated with gastrointestinal disease. In: Arieff AI, DeFronzo RA (eds) Fluid, electrolyte, and acid–base disorders, 2nd edn. Churchill Livingstone, New York, pp 813–836 Charney AN, Goldfarb DS, Dagher PC (1995) Metabolic disorders associated with gastrointestinal disease. In: Arieff AI, DeFronzo RA (eds) Fluid, electrolyte, and acid–base disorders, 2nd edn. Churchill Livingstone, New York, pp 813–836
13.
go back to reference Charney AN, Feldman GM (1984) Systemic acid–base-disorders and intestinal electrolyte transport. Am J Physiol Gastrointest Liver Physiol 247(1):G1–G12CrossRef Charney AN, Feldman GM (1984) Systemic acid–base-disorders and intestinal electrolyte transport. Am J Physiol Gastrointest Liver Physiol 247(1):G1–G12CrossRef
22.
go back to reference Alesutan I, Daryadel A, Mohebbi N, Pelzl L, Leibrock C, Voelkl J, Bourgeois S, Dossena S, Nofziger C, Paulmichl M, Wagner CA, Lang F (2011) Impact of bicarbonate, ammonium chloride, and acetazolamide on hepatic and renal SLC26A4 expression. Cell Physiol Biochem 28(3):553–558. https://doi.org/10.1159/000335114 CrossRefPubMed Alesutan I, Daryadel A, Mohebbi N, Pelzl L, Leibrock C, Voelkl J, Bourgeois S, Dossena S, Nofziger C, Paulmichl M, Wagner CA, Lang F (2011) Impact of bicarbonate, ammonium chloride, and acetazolamide on hepatic and renal SLC26A4 expression. Cell Physiol Biochem 28(3):553–558. https://​doi.​org/​10.​1159/​000335114 CrossRefPubMed
26.
go back to reference Ribayamercado JD, Gershoff SN (1984) Effects of sugars and vitamin-b-6 deficiency on oxalate synthesis in rats. J Nutr 114(8):1447–1453CrossRef Ribayamercado JD, Gershoff SN (1984) Effects of sugars and vitamin-b-6 deficiency on oxalate synthesis in rats. J Nutr 114(8):1447–1453CrossRef
29.
go back to reference Freel RW, Hatch M, Earnest DL, Goldner AM (1980) Oxalate transport across the isolated rat colon. A re-examination. Biochem Biophys Acta 600(3):838–843CrossRefPubMed Freel RW, Hatch M, Earnest DL, Goldner AM (1980) Oxalate transport across the isolated rat colon. A re-examination. Biochem Biophys Acta 600(3):838–843CrossRefPubMed
32.
go back to reference Wagner JD, Kurtin P, Charney AN (1985) Effect of systemic acid–base-disorders on colonic intracellular ph and ion-transport. Am J Physiol Gastrointest Liver Physiol 249(1):G39–G47CrossRef Wagner JD, Kurtin P, Charney AN (1985) Effect of systemic acid–base-disorders on colonic intracellular ph and ion-transport. Am J Physiol Gastrointest Liver Physiol 249(1):G39–G47CrossRef
33.
go back to reference Feldman GM (1989) Effect of chronic metabolic-acidosis on net electrolyte transport in rat colon. Am J Physiol Gastrointest Liver Physiol 256(6):G1036–G1040CrossRef Feldman GM (1989) Effect of chronic metabolic-acidosis on net electrolyte transport in rat colon. Am J Physiol Gastrointest Liver Physiol 256(6):G1036–G1040CrossRef
34.
go back to reference Goldfarb DS, Sly WS, Waheed A, Charney AN (2000) Acid–base effects on electrolyte transport in CA II-deficient mouse colon. Am J Physiol Gastrointest Liver Physiol 278(3):G409–G415CrossRefPubMed Goldfarb DS, Sly WS, Waheed A, Charney AN (2000) Acid–base effects on electrolyte transport in CA II-deficient mouse colon. Am J Physiol Gastrointest Liver Physiol 278(3):G409–G415CrossRefPubMed
36.
go back to reference Brion LP, Cammer W, Satlin LM, Suarez C, Zavilowitz BJ, Schuster VL (1997) Expression of carbonic anhydrase IV in carbonic anhydrase II-deficient mice. Am J Physiol Renal Physiol 273(2):F234–F245CrossRef Brion LP, Cammer W, Satlin LM, Suarez C, Zavilowitz BJ, Schuster VL (1997) Expression of carbonic anhydrase IV in carbonic anhydrase II-deficient mice. Am J Physiol Renal Physiol 273(2):F234–F245CrossRef
37.
go back to reference Lien YHH, Lai LW (1998) Respiratory acidosis in carbonic anhydrase II-deficient mice. Am J Physiol Lung Cell Mol Physiol 274(2):L301–L304CrossRef Lien YHH, Lai LW (1998) Respiratory acidosis in carbonic anhydrase II-deficient mice. Am J Physiol Lung Cell Mol Physiol 274(2):L301–L304CrossRef
38.
go back to reference Packer RK, Curry CA, Brown KM (1995) Urinary organic anion excretion in response to dietary acid and base loading. J Am Soc Nephrol 5(8):1624–1629PubMed Packer RK, Curry CA, Brown KM (1995) Urinary organic anion excretion in response to dietary acid and base loading. J Am Soc Nephrol 5(8):1624–1629PubMed
41.
go back to reference Lemann J, Hornick LJ, Pleuss JA, Gray RW (1989) Oxalate is overestimated in alkaline urines collected during administration of bicarbonate with no specimen pH adjustment. Clin Chem 35(10):2107–2110PubMed Lemann J, Hornick LJ, Pleuss JA, Gray RW (1989) Oxalate is overestimated in alkaline urines collected during administration of bicarbonate with no specimen pH adjustment. Clin Chem 35(10):2107–2110PubMed
42.
go back to reference Mazzachi BC, Teubner JK, Ryall RL (1984) Factors affecting measurement of urinary oxalate. Clin Chem 30(8):1339–1343PubMed Mazzachi BC, Teubner JK, Ryall RL (1984) Factors affecting measurement of urinary oxalate. Clin Chem 30(8):1339–1343PubMed
43.
go back to reference Chalmers AH, Cowley DM, McWhinney BC (1985) Stability of ascorbate in urine—relevance to analyses for ascorbate and oxalate. Clin Chem 31(10):1703–1705PubMed Chalmers AH, Cowley DM, McWhinney BC (1985) Stability of ascorbate in urine—relevance to analyses for ascorbate and oxalate. Clin Chem 31(10):1703–1705PubMed
45.
go back to reference Miki K, Sudo A (1998) Effect of urine pH, storage time, and temperature on stability of catecholamines, cortisol, and creatinine. Clin Chem 44(8):1759–1762PubMed Miki K, Sudo A (1998) Effect of urine pH, storage time, and temperature on stability of catecholamines, cortisol, and creatinine. Clin Chem 44(8):1759–1762PubMed
46.
go back to reference Wyss M, Kaddurah-Daouk R (2000) Creatine and creatinine metabolism. Physiol Rev 80(3):1107–1213CrossRef Wyss M, Kaddurah-Daouk R (2000) Creatine and creatinine metabolism. Physiol Rev 80(3):1107–1213CrossRef
47.
go back to reference Perrone RD, Madias NE, Levey AS (1992) Serum creatinine as an index of renal-function - new insights into old concepts. Clin Chem 38(10):1933–1953PubMed Perrone RD, Madias NE, Levey AS (1992) Serum creatinine as an index of renal-function - new insights into old concepts. Clin Chem 38(10):1933–1953PubMed
48.
go back to reference Hamm LL, Simon EE (1987) Roles and mechanisms of urinary buffer excretion. Am J Physiol Renal Physiol 253(4):F595–F605CrossRef Hamm LL, Simon EE (1987) Roles and mechanisms of urinary buffer excretion. Am J Physiol Renal Physiol 253(4):F595–F605CrossRef
49.
go back to reference Wamberg S, Hansen AC, Engel K, Kildeberg P (1978) Balance of net base in rat. 3. Effects of oral sodium-bicarbonate and sodium citrate loading. Biol Neonate 34(1–2):24–31CrossRefPubMed Wamberg S, Hansen AC, Engel K, Kildeberg P (1978) Balance of net base in rat. 3. Effects of oral sodium-bicarbonate and sodium citrate loading. Biol Neonate 34(1–2):24–31CrossRefPubMed
50.
go back to reference Oster JR, Stemmer CL, Perez GO, Vaamonde CA (1988) Comparison of the effects of sodium-bicarbonate versus sodium-citrate on renal acid excretion. Miner Electrol Metab 14(2–3):97–102 Oster JR, Stemmer CL, Perez GO, Vaamonde CA (1988) Comparison of the effects of sodium-bicarbonate versus sodium-citrate on renal acid excretion. Miner Electrol Metab 14(2–3):97–102
51.
go back to reference Brown JC, Packer RK, Knepper MA (1989) Role of organic-anions in renal response to dietary acid and base loads. Am J Physiol Renal Physiol 257(2):F170–F176CrossRef Brown JC, Packer RK, Knepper MA (1989) Role of organic-anions in renal response to dietary acid and base loads. Am J Physiol Renal Physiol 257(2):F170–F176CrossRef
54.
go back to reference Hood VL (1985) pH regulation of endogenous acid production in subjects with chronic ketoacidosis. Am J Physiol Renal Physiol 249(2):F220–F226CrossRef Hood VL (1985) pH regulation of endogenous acid production in subjects with chronic ketoacidosis. Am J Physiol Renal Physiol 249(2):F220–F226CrossRef
55.
go back to reference Lindinger MI, Franklin TW, Lands LC, Pedersen PK, Welsh DG, Heigenhauser GJF (2000) NaHCO3 and KHCO3 ingestion rapidly increases renal electrolyte excretion in humans. J Appl Physiol 88(2):540–550CrossRefPubMed Lindinger MI, Franklin TW, Lands LC, Pedersen PK, Welsh DG, Heigenhauser GJF (2000) NaHCO3 and KHCO3 ingestion rapidly increases renal electrolyte excretion in humans. J Appl Physiol 88(2):540–550CrossRefPubMed
56.
go back to reference Khanna A, Kurtzman NA (2006) Metabolic alkalosis. J Nephrol 19:S86–S96PubMed Khanna A, Kurtzman NA (2006) Metabolic alkalosis. J Nephrol 19:S86–S96PubMed
57.
go back to reference Maren TH (1967) Carbonic anhydrase—chemistry physiology and inhibition. Physiol Rev 47(4):595–781CrossRefPubMed Maren TH (1967) Carbonic anhydrase—chemistry physiology and inhibition. Physiol Rev 47(4):595–781CrossRefPubMed
62.
go back to reference Ohana E, Shcheynikov N, Moe OW, Muallem S (2013) SLC26A6 and NaDC-1 transporters interact to regulate oxalate and citrate homeostasis. J Am Soc Nephrol 24(10):1617–1626CrossRefPubMedPubMedCentral Ohana E, Shcheynikov N, Moe OW, Muallem S (2013) SLC26A6 and NaDC-1 transporters interact to regulate oxalate and citrate homeostasis. J Am Soc Nephrol 24(10):1617–1626CrossRefPubMedPubMedCentral
63.
go back to reference Maren TH (1977) Use of inhibitors in physiological studies of carbonic-anhydrase. Am J Physiol Renal Physiol 232(4):F291–F297CrossRef Maren TH (1977) Use of inhibitors in physiological studies of carbonic-anhydrase. Am J Physiol Renal Physiol 232(4):F291–F297CrossRef
67.
go back to reference Higashihara E, Nutahara K, Takeuchi T, Shoji N, Araie M, Aso Y (1991) Calcium-metabolism in acidotic patients induced by carbonic-anhydrase inhibitors—responses to citrate. J Urol 145(5):942–948CrossRefPubMed Higashihara E, Nutahara K, Takeuchi T, Shoji N, Araie M, Aso Y (1991) Calcium-metabolism in acidotic patients induced by carbonic-anhydrase inhibitors—responses to citrate. J Urol 145(5):942–948CrossRefPubMed
Metadata
Title
Oxalate transport by the mouse intestine in vitro is not affected by chronic challenges to systemic acid–base homeostasis
Authors
Jonathan M. Whittamore
Marguerite Hatch
Publication date
01-06-2019
Publisher
Springer Berlin Heidelberg
Published in
Urolithiasis / Issue 3/2019
Print ISSN: 2194-7228
Electronic ISSN: 2194-7236
DOI
https://doi.org/10.1007/s00240-018-1067-5

Other articles of this Issue 3/2019

Urolithiasis 3/2019 Go to the issue

Letter to the Editor

Gene therapy for cystinuria