Osmotic diuresis by SGLT2 inhibition stimulates vasopressin-induced water reabsorption to maintain body fluid volume

Physiological Reports

Volumn 8, Issue 2, 2020, Pages

  Masuda, Takahiro ^a   Muto, Shigeaki ^a   Fukuda, Keiko ^a   Watanabe, Minami ^a   Ohara, Ken ^a   Koepsell, Hermann ^b   Vallon, Volker ^c   Nagata, Daisuke ^a  

^a JICHI MEDICAL UNIVERSITY   (Japan)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

bioimpedance analysis; glucosuria; SGLT2 inhibition; vasopressin; water reabsorption

Indexed keywords

AQUAPORIN 2; CREATININE; GLUCOSE; GLUCOSE TRANSPORTER 2; INSULIN; IPRAGLIFLOZIN; SERINE 269; SODIUM GLUCOSE COTRANSPORTER 2 INHIBITOR; UNCLASSIFIED DRUG; VASOPRESSIN; GLUCOSIDE; OSMOTIC DIURETIC AGENT; THIOPHENE DERIVATIVE; VASOPRESSIN DERIVATIVE; WATER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; BODY FLUID; BODY WEIGHT; CONTROLLED STUDY; CREATININE CLEARANCE; EXPERIMENTAL DIABETES MELLITUS; FLUID BALANCE; FLUID INTAKE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; GLUCOSE URINE LEVEL; GLUCOSURIA; HEART RATE; HEMATOCRIT; HOSPITALIZATION; IMPEDANCE SPECTROSCOPY; NONHUMAN; OSMOLALITY; OSMOTIC DIURESIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION; UREA NITROGEN BLOOD LEVEL; URINALYSIS; URINE FLOW RATE; URINE OSMOLALITY; URINE VOLUME; WATER ABSORPTION; WESTERN BLOTTING; ANIMAL; BODY FLUID COMPARTMENT; DIURESIS; DRUG EFFECT; KIDNEY TUBULE ABSORPTION; METABOLISM; OSMOSIS; PHARMACOLOGY; PHYSIOLOGY; RAT; URINE;

ANIMALS; BODY FLUID COMPARTMENTS; BODY FLUIDS; DIURESIS; DIURETICS, OSMOTIC; GLUCOSIDES; OSMOSIS; RATS; RENAL REABSORPTION; SODIUM-GLUCOSE TRANSPORTER 2 INHIBITORS; THIOPHENES; VASOPRESSINS; WATER;

EID: 85078688212     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.14360     Document Type: Article

References (60)

1. Abdeen, A., Sonoda, H., El-Shawarby, R., Takahashi, S., & Ikeda, M. (2014). Urinary excretion pattern of exosomal aquaporin-2 in rats that received gentamicin. American Journal of Physiology-Renal Physiology, 307, F1227–F1237. https://doi.org/10.1152/ajprenal.00140.2014
2. Ando, F., Mori, S., Yui, N., Morimoto, T., Nomura, N., Sohara, E., … Uchida, S. (2018). AKAPs-PKA disruptors increase AQP2 activity independently of vasopressin in a model of nephrogenic diabetes insipidus. Nature Communications, 9, 1411. https://doi.org/10.1038/s41467-018-03771-2
3. Ansary, T. M., Nakano, D., & Nishiyama, A. (2019). Diuretic Effects of sodium glucose cotransporter 2 inhibitors and their influence on the renin-angiotensin system. International Journal of Molecular Sciences, 20(3), 629. https://doi.org/10.3390/ijms20030629
4. Balen, D., Ljubojevic, M., Breljak, D., Brzica, H., Zlender, V., Koepsell, H., & Sabolic, I. (2008). Revised immunolocalization of the Na+-D-glucose cotransporter SGLT1 in rat organs with an improved antibody. The American Journal of Physiology-Cell Physiology, 295, C475–C489.
5. Blaustein, M. P., Zhang, J., Chen, L., & Hamilton, B. P. (2006). How does salt retention raise blood pressure? American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 290, R514–R523. https://doi.org/10.1152/ajpregu.00819.2005
6. Chapman, M. E., Hu, L., Plato, C. F., & Kohan, D. E. (2010). Bioimpedance spectroscopy for the estimation of body fluid volumes in mice. The American Journal of Physiology-Renal Physiology, 299, F280–F283. https://doi.org/10.1152/ajprenal.00113.2010
7. Chen, L., LaRocque, L. M., Efe, O., Wang, J., Sands, J. M., & Klein, J. D. (2016). Effect of dapagliflozin treatment on fluid and electrolyte balance in diabetic rats. The American Journal of the Medical Sciences, 352, 517–523. https://doi.org/10.1016/j.amjms.2016.08.015
8. Chung, S., Kim, S., Son, M., Kim, M., Koh, E. S., Shin, S. J., … Kim, H. S. (2019). Empagliflozin contributes to polyuria via regulation of sodium transporters and water channels in diabetic rat kidneys. Frontiers in Physiology, 10, 271. https://doi.org/10.3389/fphys.2019.00271
9. Dolgor, B., Kitano, S., Yoshida, T., Bandoh, T., Ninomiya, K., & Matsumoto, T. (1998). Vasopressin antagonist improves renal function in a rat model of pneumoperitoneum. Journal of Surgical Research, 79, 109–114. https://doi.org/10.1006/jsre.1998.5409
10. Donnan, J. R., Grandy, C. A., Chibrikov, E., Marra, C. A., Aubrey-Bassler, K., Johnston, K., … Gamble, J. M. (2019). Comparative safety of the sodium glucose co-transporter 2 (SGLT2) inhibitors: A systematic review and meta-analysis. British Medical Journal Open, 9, e022577.
11. Ettema, E. M., Zittema, D., Kuipers, J., Gansevoort, R. T., Vart, P., de Jong, P. E., … Franssen, C. F. (2014). Dialysis hypotension: A role for inadequate increase in arginine vasopressin levels? A systematic literature review and meta-analysis. The American Journal of Nephrology, 39, 100–109.
12. Gilbert, R. E., & Thorpe, K. E. (2019). Acute kidney injury with sodium-glucose co-transporter-2 inhibitors: A meta-analysis of cardiovascular outcome trials. Diabetes, Obesity and Metabolism, 21(8), 1996–2000. https://doi.org/10.1111/dom.13754
13. Hew-Butler, T., Noakes, T. D., Soldin, S. J., & Verbalis, J. G. (2010). Acute changes in arginine vasopressin, sweat, urine and serum sodium concentrations in exercising humans: Does a coordinated homeostatic relationship exist? British Journal of Sports Medicine, 44, 710–715. https://doi.org/10.1136/bjsm.2008.051771
14. Hu, L., Maslanik, T., Zerebeckyj, M., & Plato, C. F. (2012). Evaluation of bioimpedance spectroscopy for the measurement of body fluid compartment volumes in rats. Journal of Pharmacological and Toxicological Methods, 65, 75–82. https://doi.org/10.1016/j.vascn.2012.02.001
15. Huang, D. Y., Pfaff, I., Serradeil-Le Gal, C., & Vallon, V. (2000). Acute renal response to the non-peptide vasopressin V2-receptor antagonist SR 121463B in anesthetized rats. Naunyn-Schmiedeberg's Archives of Pharmacology, 362, 201–207. https://doi.org/10.1007/s002100000282
16. Ishikawa, S. E., & Schrier, R. W. (2003). Pathophysiological roles of arginine vasopressin and aquaporin-2 in impaired water excretion. Clinical Endocrinology, 58, 1–17. https://doi.org/10.1046/j.1365-2265.2003.01647.x
17. Iuchi, H., Sakamoto, M., Matsutani, D., Suzuki, H., Kayama, Y., Takeda, N., … Utsunomiya, K. (2017). Time-dependent effects of ipragliflozin on behaviour and energy homeostasis in normal and type 2 diabetic rats: Continuous glucose telemetry analysis. Science Reports, 7, 11906.
18. Iwasaki, Y., Kondo, K., Murase, T., Hasegawa, H., & Oiso, Y. (1996). Osmoregulation of plasma vasopressin in diabetes mellitus with sustained hyperglycemia. Journal of Neuroendocrinology, 8, 755–760. https://doi.org/10.1046/j.1365-2826.1996.05124.x
19. Kanai, Y., Lee, W. S., You, G., Brown, D., & Hediger, M. A. (1994). The human kidney low affinity Na+/glucose cotransporter SGLT2. Delineation of the major renal reabsorptive mechanism for D-glucose. Journal of Clinical Investigation, 93, 397–404. https://doi.org/10.1172/JCI116972
20. Khan, Y. H., Sarriff, A., Adnan, A. S., Khan, A. H., & Mallhi, T. H. (2017). Outcomes of diuretic use in pre-dialysis CKD patients with moderate renal deterioration attending tertiary care referral center. Clinical and Experimental Nephrology, 21, 1011–1023. https://doi.org/10.1007/s10157-017-1397-6
21. Knepper, M. A., Kwon, T. H., & Nielsen, S. (2015). Molecular physiology of water balance. New England Journal of Medicine, 372, 1349–1358. https://doi.org/10.1056/NEJMra1404726
22. Lambers Heerspink, H. J., de Zeeuw, D., Wie, L., Leslie, B., & List, J. (2013). Dapagliflozin a glucose-regulating drug with diuretic properties in subjects with type 2 diabetes. Diabetes, Obesity and Metabolism, 15, 853–862. https://doi.org/10.1111/dom.12127
23. Layton, A. T., Vallon, V., & Edwards, A. (2016). Predicted consequences of diabetes and SGLT inhibition on transport and oxygen consumption along a rat nephron. American Journal of Physiology-Renal Physiology, 310, F1269–F1283. https://doi.org/10.1152/ajprenal.00543.2015
24. Maric-Bilkan, C., Flynn, E. R., & Chade, A. R. (2012). Microvascular disease precedes the decline in renal function in the streptozotocin-induced diabetic rat. American Journal of Physiology-Renal Physiology, 302, F308–F315. https://doi.org/10.1152/ajprenal.00421.2011
25. Masuda, T., Fu, Y., Eguchi, A., Czogalla, J., Rose, M. A., Kuczkowski, A., … Vallon, V. (2014). Dipeptidyl peptidase IV inhibitor lowers PPARgamma agonist-induced body weight gain by affecting food intake, fat mass, and beige/brown fat but not fluid retention. The American Journal of Physiology-Endocrinology and Metabolism, 306, E388–E398.
26. Masuda, T., Muto, S., Fujisawa, G., Iwazu, Y., Kimura, M., Kobayashi, T., … Kusano, E. (2012). Heart angiotensin II-induced cardiomyocyte hypertrophy suppresses coronary angiogenesis and progresses diabetic cardiomyopathy. American Journal of Physiology-Heart and Circulatory Physiology, 302, H1871–H1883. https://doi.org/10.1152/ajpheart.00663.2011
27. Masuda, T., Ohara, K., Murakami, T., Imai, T., Nakagawa, S., Okada, M., … Nagata, D. (2017). Sodium-glucose cotransporter 2 inhibition with dapagliflozin ameliorates extracellular volume expansion in diabetic kidney disease patients. POJ Diabetes & Obesity, 1, 1–8.
28. Masuda, T., Watanabe, Y., Fukuda, K., Watanabe, M., Onishi, A., Ohara, K., … Nagata, D. (2018). Unmasking a sustained negative effect of SGLT2 inhibition on body fluid volume in the rat. American Journal of Physiology-Renal Physiology, 315, F653–F664. https://doi.org/10.1152/ajprenal.00143.2018
29. Matsui, K., Share, L., Wang, B. C., Crofton, J. T., & Brooks, D. P. (1983). Effects of changes in steady state plasma vasopressin levels on renal and urinary vasopressin clearances in the dog. Endocrinology, 112, 2107–2113. https://doi.org/10.1210/endo-112-6-2107
30. Montiel, V., Leon Gomez, E., Bouzin, C., Esfahani, H., Romero Perez, M., Lobysheva, I., … Balligand, J. L. (2014). Genetic deletion of aquaporin-1 results in microcardia and low blood pressure in mouse with intact nitric oxide-dependent relaxation, but enhanced prostanoids-dependent relaxation. Pflügers Archiv - European Journal of Physiology, 466, 237–251. https://doi.org/10.1007/s00424-013-1325-x
31. Mullens, W., Damman, K., Harjola, V. P., Mebazaa, A., Brunner-La Rocca, H. P., Martens, P., … Coats, A. J. (2019). The use of diuretics in heart failure with congestion – A position statement from the Heart Failure Association of the European Society of Cardiology. European Journal of Heart Failure, 21, 137–155. https://doi.org/10.1002/ejhf.1369
32. Nadkarni, G. N., Ferrandino, R., Chang, A., Surapaneni, A., Chauhan, K., Poojary, P., … Coca, S. G. (2017). Acute kidney injury in patients on SGLT2 inhibitors: A propensity-matched analysis. Diabetes Care, 40, 1479–1485.
33. Neal, B., Perkovic, V., Mahaffey, K. W., de Zeeuw, D., Fulcher, G., Erondu, N., … Matthews, D. R. (2017). Canagliflozin and cardiovascular and renal events in type 2 diabetes. New England Journal of Medicine, 377(7), 644–657. https://doi.org/10.1056/NEJMoa1611925
34. Nguyen, M. K., & Kurtz, I. (2005). Derivation of a new formula for calculating urinary electrolyte-free water clearance based on the Edelman equation. American Journal of Physiology-Renal Physiology, 288, F1–F7. https://doi.org/10.1152/ajprenal.00259.2004
35. Ohara, K., Masuda, T., Murakami, T., Imai, T., Yoshizawa, H., Nakagawa, S., … Nagata, D. (2019). Effects of the sodium-glucose cotransporter 2 inhibitor dapagliflozin on fluid distribution: A comparison study with furosemide and tolvaptan. Nephrology (Carlton), 24, 904–911.
36. Onishi, A., Fu, Y., Darshi, M., Crespo-Masip, M., Huang, W., Song, P., … Vallon, V. (2019). Effect of renal tubule-specific knockdown of the Na(+)/H(+) exchanger NHE3 in Akita diabetic mice. The American Journal of Physiology-Renal Physiology, 317, F419–F434.
37. Perkovic, V., Jardine, M. J., Neal, B., Bompoint, S., Heerspink, H. J. L., Charytan, D. M., … Mahaffey, K. W.; Investigators CT. (2019). Canagliflozin and renal outcomes in type 2 diabetes and nephropathy. New England Journal of Medicine, 380(24), 2295–2306. https://doi.org/10.1056/NEJMoa1811744
38. Sabolic, I., Vrhovac, I., Eror, D. B., Gerasimova, M., Rose, M., Breljak, D., … Koepsell, H. (2012). Expression of Na+-D-glucose cotransporter SGLT2 in rodents is kidney-specific and exhibits sex and species differences. The American Journal of Physiology-Renal Physiology, 302, C1174–C1188.
39. Sansoe, G., Aragno, M., Smedile, A., Rizzetto, M., & Rosina, F. (2009). Solute-free water retention in preascitic cirrhotic rats following intravenous water loading. Journal of Physiology, 60, 111–117.
40. Schork, A., Saynisch, J., Vosseler, A., Jaghutriz, B. A., Heyne, N., Peter, A., … Artunc, F. (2019). Effect of SGLT2 inhibitors on body composition, fluid status and renin-angiotensin-aldosterone system in type 2 diabetes: A prospective study using bioimpedance spectroscopy. Cardiovascular Diabetology, 18, 46.
41. Sladek, C. D., & Knigge, K. M. (1977). Osmotic control of vasopressin release by rat hypothalamo-neurohypophyseal explants in organ culture. Endocrinology, 101, 1834–1838. https://doi.org/10.1210/endo-101-6-1834
42. Tahara, A., Kurosaki, E., Yokono, M., Yamajuku, D., Kihara, R., Hayashizaki, Y., … Shibasaki, M. (2012a). Antidiabetic effects of SGLT2-selective inhibitor ipragliflozin in streptozotocin-nicotinamide-induced mildly diabetic mice. Journal of Pharmacology Science, 120, 36–44.
43. Tahara, A., Kurosaki, E., Yokono, M., Yamajuku, D., Kihara, R., Hayashizaki, Y., … Shibasaki, M. (2012b). Pharmacological profile of ipragliflozin (ASP1941), a novel selective SGLT2 inhibitor, in vitro and in vivo. Naunyn-Schmiedeberg's Archives of Pharmacology, 385, 423–436. https://doi.org/10.1007/s00210-011-0713-z
44. Tanaka, H., Takano, K., Iijima, H., Kubo, H., Maruyama, N., Hashimoto, T., … Kaku, K. (2017). Factors affecting canagliflozin-induced transient urine volume increase in patients with type 2 diabetes mellitus. Advances in Therapy, 34, 436–451. https://doi.org/10.1007/s12325-016-0457-8
45. Thrasher, T. N., Brown, C. J., Keil, L. C., & Ramsay, D. J. (1980). Thirst and vasopressin release in the dog: An osmoreceptor or sodium receptor mechanism? American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 238, R333–R339. https://doi.org/10.1152/ajpregu.1980.238.5.R333
46. Vallon, V., Gerasimova, M., Rose, M. A., Masuda, T., Satriano, J., Mayoux, E., … Rieg, T. (2014). SGLT2 inhibitor empagliflozin reduces renal growth and albuminuria in proportion to hyperglycemia and prevents glomerular hyperfiltration in diabetic Akita mice. American Journal of Physiology-Renal Physiology, 306, F194–F204. https://doi.org/10.1152/ajprenal.00520.2013
47. Vallon, V., Platt, K. A., Cunard, R., Schroth, J., Whaley, J., Thomson, S. C., … Rieg, T. (2011). SGLT2 mediates glucose reabsorption in the early proximal tubule. Journal of the American Society of Nephrology, 22, 104–112. https://doi.org/10.1681/ASN.2010030246
48. Vallon, V., & Thomson, S. C. (2017). Targeting renal glucose reabsorption to treat hyperglycaemia: The pleiotropic effects of SGLT2 inhibition. Diabetologia, 60, 215–225.
49. Vallon, V., Verkman, A., & Schnermann, J. (2000). Luminal hypotonicity in proximal tubules of aquaporin-1-knockout mice. American Journal of Physiology-Renal Physiology, 278, F1030–F1033. https://doi.org/10.1152/ajprenal.2000.278.6.F1030
50. Vokes, T. P., Aycinena, P. R., & Robertson, G. L. (1987). Effect of insulin on osmoregulation of vasopressin. American Journal of Physiology-Endocrinology and Metabolism, 252, E538–E548. https://doi.org/10.1152/ajpendo.1987.252.4.E538
51. Wanner, C., Inzucchi, S. E., Lachin, J. M., Fitchett, D., von Eynatten, M., Mattheus, M., … Zinman, B.; Investigators E-RO. (2016). Empagliflozin and progression of kidney disease in type 2 diabetes. New England Journal of Medicine, 375, 323–334. https://doi.org/10.1056/NEJMoa1515920
52. Wiviott, S. D., Raz, I., Bonaca, M. P., Mosenzon, O., Kato, E. T., Cahn, A., … Sabatine, M. S.; Investigators D-T. (2019). Dapagliflozin and cardiovascular outcomes in type 2 diabetes. New England Journal of Medicine, 380, 347–357. https://doi.org/10.1056/NEJMoa1812389
53. Xie, L., Hoffert, J. D., Chou, C. L., Yu, M. J., Pisitkun, T., Knepper, M. A., & Fenton, R. A. (2010). Quantitative analysis of aquaporin-2 phosphorylation. American Journal of Physiology-Renal Physiology, 298, F1018–F1023. https://doi.org/10.1152/ajprenal.00580.2009
54. Yasui, A., Lee, G., Hirase, T., Kaneko, T., Kaspers, S., von Eynatten, M., & Okamura, T. (2018). Empagliflozin induces transient diuresis without changing long-term overall fluid balance in japanese patients with type 2 diabetes. Diabetes Therapy, 9, 863–871. https://doi.org/10.1007/s13300-018-0385-5
55. Yasuoka, Y., Kobayashi, M., Sato, Y., Zhou, M., Abe, H., Okamoto, H., … Kawahara, K. (2013). The intercalated cells of the mouse kidney OMCD(is) are the target of the vasopressin V1a receptor axis for urinary acidification. Clinical and Experimental Nephrology, 17, 783–792. https://doi.org/10.1007/s10157-013-0783-y
56. Yui, N., Sasaki, S., & Uchida, S. (2017). Aquaporin-2 Ser-261 phosphorylation is regulated in combination with Ser-256 and Ser-269 phosphorylation. Biochemical and Biophysical Research Communications, 482, 524–529. https://doi.org/10.1016/j.bbrc.2016.11.118
57. Zelniker, T. A., Wiviott, S. D., Raz, I., Im, K., Goodrich, E. L., Bonaca, M. P., … Sabatine, M. S. (2019). SGLT2 inhibitors for primary and secondary prevention of cardiovascular and renal outcomes in type 2 diabetes: A systematic review and meta-analysis of cardiovascular outcome trials. Lancet, 393, 31–39.
58. Zerbe, R. L., & Robertson, G. L. (1983). Osmoregulation of thirst and vasopressin secretion in human subjects: Effect of various solutes. The American Journal of Physiology, 244, E607–E614.
59. Zerbe, R. L., Vinicor, F., & Robertson, G. L. (1979). Plasma vasopressin in uncontrolled diabetes mellitus. Diabetes, 28, 503–508. https://doi.org/10.2337/diabetes.28.5.503
60. Zinman, B., Wanner, C., Lachin, J. M., Fitchett, D., Bluhmki, E., Hantel, S., … Inzucchi, S. E.; Investigators E-RO. (2015). Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. New England Journal of Medicine, 373, 2117–2128. https://doi.org/10.1056/NEJMoa1504720