Effect of renal tubule-specific knockdown of the Na+/H+exchanger NHE3 in Akita diabetic mice
Open accessAbstract
Na+/H+exchanger isoform 3 (NHE3) contributes to Na+/bicarbonate reabsorption and ammonium secretion in early proximal tubules. To determine its role in the diabetic kidney, type 1 diabetic Akita mice with tubular NHE3 knockdown [Pax8-Cre; NHE3-knockout (KO) mice] were generated. NHE3-KO mice had higher urine pH, more bicarbonaturia, and compensating increases in renal mRNA expression for genes associated with generation of ammonium, bicarbonate, and glucose (phosphoenolpyruvate carboxykinase) in proximal tubules and H+and ammonia secretion and glycolysis in distal tubules. This left blood pH and bicarbonate unaffected in nondiabetic and diabetic NHE3-KO versus wild-type mice but was associated with renal upregulation of proinflammatory markers. Higher renal phosphoenolpyruvate carboxykinase expression in NHE3-KO mice was associated with lower Na+-glucose cotransporter (SGLT)2 and higher SGLT1 expression, indicating a downward tubular shift in Na+and glucose reabsorption. NHE3-KO was associated with lesser kidney weight and glomerular filtration rate (GFR) independent of diabetes and prevented diabetes-associated albuminuria. NHE3-KO, however, did not attenuate hyperglycemia or prevent diabetes from increasing kidney weight and GFR. Higher renal gluconeogenesis may explain similar hyperglycemia despite lower SGLT2 expression and higher glucosuria in diabetic NHE3-KO versus wild-type mice; stronger SGLT1 engagement could have affected kidney weight and GFR responses. Chronic kidney disease in humans is associated with reduced urinary excretion of metabolites of branched-chain amino acids and the tricarboxylic acid cycle, a pattern mimicked in diabetic wild-type mice. This pattern was reversed in nondiabetic NHE3-KO mice, possibly reflecting branched-chain amino acids use for ammoniagenesis and tricarboxylic acid cycle upregulation to support formation of ammonia, bicarbonate, and glucose in proximal tubule. NHE3-KO, however, did not prevent the diabetes-induced urinary downregulation in these metabolites.
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Mouse studies show a functional relationship between SGLT2 and NHE3.
“Studies in mice have shown a functional relationship between SGLT2 and NHE3 (Onishi et al., 2019).”
From A kidney perspective on the mechanism of action of sodium glucose co-transporter 2 inhibitors (2021) · cites this paper as Onishi et al., 2019
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- Authors
- Onishi, A., Fu, Y., Darshi, M., Crespo-Masip, M., Huang, W., Song, P., Patel, R., Kim, Y. C., Nespoux, J., Freeman, B., Soleimani, M., Thomson, S., Sharma, K., & Vallon, V.
- Affiliations
- Department of Medicine, University of California San Diego and Veterans Affairs San Diego Healthcare System, San Diego, California
- University of California San Diego (US)
- The University of Texas at San Antonio Health Science Center (US)
- University of Cincinnati (US)
- Corresponding author
- Vallon, Volker
- ORCID
- Venue
- American Journal of Physiology-Renal Physiology
- Publisher
- American Physiological Society
- Published
- 2019-08-01
- Volume
- 317
- Issue
- 2
- Pages
- F419-F434
- ISSN
- 1522-1466 (ISSN-L)
- 1931-857X
- PMC
- PMC6732454
- OpenAlex
- W2948205308
- Cited by
- 71
- References
- 70
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 14 · 2023: 6 · 2022: 10 · 2021: 15 · 2020: 13 · 2019: 3
- FWCI
- 3.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- American Journal of Physiology-Renal Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK) (R01DK112042, R01DK106102, P30DK079337)
- U.S. Department of Veterans Affairs (VA)
- Boehringer Ingelheim (Boehringer Ingelheim Pharmaceuticals)
- HHS | NIH | National Heart, Lung, and Blood Institute (NHBLI) (R01HL142814)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
- Health Sciences › Medicine › Nephrology › Chronic Kidney Disease and Diabetes
- Health Sciences › Medicine › Nephrology › Acute Kidney Injury Research
- Keywords
- NHE3, type 1 diabetes, diabetic kidney, proximal tubule, bicarbonate reabsorption, ammoniagenesis, renal gluconeogenesis, phosphoenolpyruvate carboxykinase, SGLT2, SGLT1, glucose reabsorption, glycosuria, albuminuria, glomerular filtration rate, chronic kidney disease, branched-chain amino acids, TCA cycle, pro-inflammatory markers, Akita mice
- MeSH terms
- Sodium-Hydrogen Exchanger 3, Acid-Base Equilibrium, Amino Acids, Branched-Chain, Ammonia, Animals, Bicarbonates, Blood Glucose, Diabetes Mellitus, Type 1, Diabetic Nephropathies, Disease Models, Animal, Energy Metabolism, Gene Expression Regulation, Hydrogen-Ion Concentration, Kidney Tubules, Male, Mice, Inbred C57BL, Sodium, Biomarkers, Mice, Knockout, Sodium-Glucose Transporter 1, Sodium-Glucose Transporter 2, Metabolomics, Gene Knockdown Techniques, Renal Reabsorption
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