Sodium-glucose linked cotransporter-2 inhibition does not attenuate disease progression in the rat remnant kidney model of chronic kidney disease

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Zhang, Yanling ^a   Thai, Kerri ^a   Kepecs, David M ^a   Gilbert, Richard E ^a  

^a ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CANAGLIFLOZIN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; DAPAGLIFLOZIN; SODIUM GLUCOSE COTRANSPORTER 2; TRANSFORMING GROWTH FACTOR BETA1; 2-(3-(4-ETHOXYBENZYL)-4-CHLOROPHENYL)-6-HYDROXYMETHYLTETRAHYDRO-2H-PYRAN-3,4,5-TRIOL; ANTIDIABETIC AGENT; BENZHYDRYL DERIVATIVE; GLUCOSIDE; MESSENGER RNA; SGLT2 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC KIDNEY DISEASE; CLINICAL TRIAL (TOPIC); CONTROLLED STUDY; DIABETIC NEPHROPATHY; DISEASE COURSE; DRUG EFFECT; DRUG MECHANISM; GENE EXPRESSION REGULATION; GLOMERULOSCLEROSIS; GLOMERULUS FILTRATION RATE; GLUCOSURIA; HISTOPATHOLOGY; KIDNEY FIBROSIS; KIDNEY FUNCTION; MALE; MORTALITY; MULTICENTER STUDY (TOPIC); NONHUMAN; PARTIAL NEPHRECTOMY; RAT; UPREGULATION; URINE VOLUME; ADVERSE EFFECTS; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; DRUG EFFECTS; FIBROSIS; GENE EXPRESSION; GENETICS; GLYCOSURIA; HUMAN; HYPERTENSION, RENAL; KIDNEY; METABOLISM; NEPHRECTOMY; PATHOLOGY; PROTEINURIA; RENAL INSUFFICIENCY, CHRONIC; SPRAGUE DAWLEY RAT; TREATMENT FAILURE;

ANIMALS; BENZHYDRYL COMPOUNDS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FIBROSIS; GENE EXPRESSION; GLOMERULAR FILTRATION RATE; GLUCOSIDES; GLYCOSURIA; HUMANS; HYPERTENSION, RENAL; HYPOGLYCEMIC AGENTS; KIDNEY; MALE; NEPHRECTOMY; PROTEINURIA; RATS; RATS, SPRAGUE-DAWLEY; RENAL INSUFFICIENCY, CHRONIC; RNA, MESSENGER; SODIUM-GLUCOSE TRANSPORTER 2; TRANSFORMING GROWTH FACTOR BETA1; TREATMENT FAILURE;

EID: 84954104372     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0144640     Document Type: Article

References (53)

1. Brenner BM, Meyer TW, Hostetter TH. Dietary protein intake and the progressive nature of kidney disease: the role of hemodynamically mediated glomerular injury in the pathogenesis of progressive glomerular sclerosis in aging, renal ablation, and intrinsic renal disease. N Engl J Med. 1982;307(11):652-9. PMID: 7050706.
2. Toke A, Meyer TW. Hemodynamic effects of angiotensin II in the kidney. Contrib Nephrol. 2001; (135:): 34-46. PMID: 11705290.
3. Wiseman MJ, Saunders AJ, Keen H, Viberti G. Effect of blood glucose control on increased glomerular filtration rate and kidney size in insulin-dependent diabetes. N Engl J Med. 1985;312:617-21. PMID: 3883162
4. Hayashi K, Epstein M, Loutzenhiser R, Forster H. Impaired myogenic responsiveness of the afferent arteriole in streptozotocin-induced diabetic rats: role of eicosanoid derangements. J Am Soc Nephrol. 1992;2(11):1578-86. PMID: 1610978.
5. Davalos M, Frega NS, Saker B, Leaf A. Effect of exogenous and endogenous angiotensin II in the isolated perfused rat kidney. Am J Physiol. 1978;235(6):F605-10. PMID: 736144.
6. Munger KA, Kost CK, Brenner BM, Maddox DA. The Renal Circulations and Glomerular Ultrafiltration. In: Taal MW, editor. Brenner and Rector's The Kidney. 1.9th ed. Philadelphia: Elsevier; 2012. p. 94-137.
7. Cherney DZ, Perkins BA, Soleymanlou N, Maione M, Lai V, Lee A, et al. Renal hemodynamic effect of sodium-glucose cotransporter 2 inhibition in patients with type 1 diabetes mellitus. Circulation. 2014;129(5):587-97. doi: 10.1161/CIRCULATIONAHA.113.005081 PMID: 24334175.
8. Thomson SC, Rieg T, Miracle C, Mansoury H, Whaley J, Vallon V, et al. Acute and chronic effects of SGLT2 blockade on glomerular and tubular function in the early diabetic rat. Am J Physiol Regul Integr Comp Physiol. 2012;302(1):R75-83. doi: 10.1152/ajpregu.00357.2011 PMID: 21940401; PubMed Central PMCID: PMC3349378.
9. Cherney DZ, Perkins BA. Sodium-glucose cotransporter 2 inhibition in type 1 diabetes: simultaneous glucose lowering and renal protection? Can J Diabetes. 2014;38(5):356-63. doi: 10.1016/j.jcjd.2014. 05.006 PMID: 25192954.
10. De Nicola L, Gabbai FB, Liberti ME, Sagliocca A, Conte G, Minutolo R. Sodium/glucose cotransporter 2 inhibitors and prevention of diabetic nephropathy: targeting the renal tubule in diabetes. Am J Kidney Dis. 2014;64(1):16-24. doi: 10.1053/j.ajkd.2014.02.010 PMID: 24673844.
11. Gilbert RE. Sodium-glucose linked transporter-2 inhibitors: potential for renoprotection beyond blood glucose lowering? Kidney Int. 2014;86(4):693-700. doi: 10.1038/ki.2013.451 PMID: 24257692.
12. Komoroski B, Vachharajani N, Boulton D, Kornhauser D, Geraldes M, Li L, et al. Dapagliflozin, a novel SGLT2 inhibitor, induces dose-dependent glucosuria in healthy subjects. Clin Pharmacol Ther. 2009;85(5):520-6. doi: 10.1038/clpt.2008.251 PMID: 19129748.
13. Sha S, Devineni D, Ghosh A, Polidori D, Chien S, Wexler D, et al. Canagliflozin, a novel inhibitor of sodium glucose co-transporter 2, dose dependently reduces calculated renal threshold for glucose excretion and increases urinary glucose excretion in healthy subjects. Diabetes Obes Metab. 2011;13(7):669-72. doi: 10.1111/j.1463-1326.2011.01406.x PMID: 21457428.
14. List JF, Whaley JM. Glucose dynamics and mechanistic implications of SGLT2 inhibitors in animals and humans. Kidney Int Suppl. 2011; (120:): S20-7. doi: 10.1038/ki.2010.512 PMID: 21358698.
15. Kasichayanula S, Liu X, Lacreta F, Griffen SC, Boulton DW. Clinical pharmacokinetics and pharmacodynamics of dapagliflozin, a selective inhibitor of sodium-glucose co-transporter type 2. Clinical pharmacokinetics. 2014;53(1):17-27. doi: 10.1007/s40262-013-0104-3 PMID: 24105299.
16. Fujimori Y, Katsuno K, Ojima K, Nakashima I, Nakano S, Ishikawa-Takemura Y, et al. Sergliflozin etabonate, a selective SGLT2 inhibitor, improves glycemic control in streptozotocin-induced diabetic rats and Zucker fatty rats. Eur J Pharmacol. 2009;609(1-3):148-54. doi: 10.1016/j.ejphar.2009.03.007 PMID: 19281809.
17. Anderson S, Rennke HG, Brenner BM. Therapeutic advantage of converting enzyme inhibitors in arresting progressive renal disease associated with systemic hypertension in the rat. J Clin Invest. 1986;77(6):1993-2000. doi: 10.1172/JCI112528 PMID: 3011863; PubMed Central PMCID: PMC370560.
18. Zatz R, Dunn BR, Meyer TW, Anderson S, Rennke HG, Brenner BM. Prevention of diabetic glomerulopathy by pharmacological amelioration of glomerular capillary hypertension. J Clin Invest. 1986;77(6):1925-30. doi: 10.1172/JCI112521 PMID: 3011862; PubMed Central PMCID: PMC370553.
19. Wu L, Cox A, Roe C, Dziadek M, Cooper ME, Gilbert RE. Transforming growth factor β1 and renal injury following subtotal nephrectomy in the rat: Role of the renin-angiotensin system. Kidney Int. 1997;51:1553-67. PMID: 9150473
20. Advani A, Kelly DJ, Advani SL, Cox AJ, Thai K, Zhang Y, et al. Role of VEGF in maintaining renal structure and function under normotensive and hypertensive conditions. Proc Natl Acad Sci U S A. 2007;104(36):14448-53. PMID: 17726104.
21. Yuen DA, Connelly KA, Zhang Y, Advani SL, Thai K, Kabir G, et al. Early outgrowth cells release soluble endocrine antifibrotic factors that reduce progressive organ fibrosis. Stem Cells. 2013;31(11):2408-19. doi: 10.1002/stem.1502 PMID: 23922321.
22. Gilbert RE, Wu LL, Kelly DJ, Cox A, Wilkinson-Berka JL, Johnston CI, et al. Pathological expression of renin and angiotensin II in the renal tubule after subtotal nephrectomy-Implications for the pathogenesis of tubulointerstitial fibrosis. American Journal of Pathology. 1999;155(2):429-40. PMID: 10433936
23. Gilbert RE, Zhang Y, Williams SJ, Zammit SC, Stapleton DI, Cox AJ, et al. A purpose-synthesised antifibrotic agent attenuates experimental kidney diseases in the rat. PLoS One. 2012;7(10):e47160. doi: 10.1371/journal.pone.0047160 PMID: 23071743; PubMed Central PMCID: PMC3468513.
24. Lehr HA, Mankoff DA, Corwin D, Santeusanio G, Gown AM. Application of photoshop-based image analysis to quantification of hormone receptor expression in breast cancer. J Histochem Cytochem. 1997;45(11):1559-65. PMID: 9358857
25. Lehr HA, van der Loos CM, Teeling P, Gown AM. Complete chromogen separation and analysis in double immunohistochemical stains using photoshop-based image analysis. J Histochem Cytochem. 1999;47(1):119-26. PMID: 9857219
26. Kelly DJ, Zhang Y, Gow R, Gilbert RE. Tranilast attenuates structural and functional aspects of renal injury in the remnant kidney model. J Am Soc Nephrol. 2004;15(10):2619-29. PMID: 15466266.
27. Kelly DJ, Zhang Y, Cox AJ, Gilbert RE. Combination therapy with tranilast and angiotensin-converting enzyme inhibition provides additional renoprotection in the remnant kidney model. Kidney Int. 2006;69(11):1954-60. PMID: 16557218.
28. Kelly DJ, Chanty A, Gow RM, Zhang Y, Gilbert RE. Protein kinase Cbeta inhibition attenuates osteopontin expression, macrophage recruitment, and tubulointerstitial injury in advanced experimental diabetic nephropathy. J Am Soc Nephrol. 2005;16(6):1654-60. PMID: 15843473.
29. Connelly KA, Kelly DJ, Zhang Y, Prior DL, Advani A, Cox AJ, et al. Inhibition of protein kinase C-beta by ruboxistaurin preserves cardiac function and reduces extracellular matrix production in diabetic cardiomyopathy. Circ Heart Fail. 2009;2(2):129-37. PMID: 19808328. doi: 10.1161/CIRCHEARTFAILURE. 108.765750
30. The GISEN Group (Gruppo Italiano di Studi Epidemiologici in Nefrologia). Randomised placebo-controlled trial of effect of ramipril on decline in glomerular filtration rate and risk of terminal renal failure in proteinuric, non-diabetic nephropathy. Lancet. 1997;349:1857-63. PMID: 9217756
31. Lewis EJ, Hunsicker LG, Bain RP, Rohde RD, for the Collaborative Study Group. The effect of angiotensinconverting-enzyme inhibition on diabetic nephropathy. N Engl J Med. 1993;329:1456-62. PMID: 8413456
32. DeFronzo RA, Hompesch M, Kasichayanula S, Liu X, Hong Y, Pfister M, et al. Characterization of renal glucose reabsorption in response to dapagliflozin in healthy subjects and subjects with type 2 diabetes. Diabetes Care. 2013;36(10):3169-76. doi: 10.2337/dc13-0387 PMID: 23735727; PubMed Central PMCID: PMC3781504.
33. Shannon JA, Smith HW. The Excretion of Inulin, Xylose and Urea by Normal and Phlorizinized Man. J Clin Invest. 1935;14(4):393-401. doi: 10.1172/JCI100690 PMID: 16694313; PubMed Central PMCID: PMC424694.
34. Brenner BM. Hemodynamically mediated glomerular injury and the progressive nature of kidney disease. Kidney Int. 1983;23(4):647-55. PMID: 6336299.
35. Benigni A, Zoja C, Noris M, Corna D, Benedetti G, Bruzzi I, et al. Renoprotection by nitric oxide donor and lisinopril in the remnant kidney model. Am J Kidney Dis. 1999;33(4):746-53. PMID: 10196019.
36. Tesch GH, Allen TJ. Rodent models of streptozotocin-induced diabetic nephropathy. Nephrology (Carlton). 2007;12(3):261-6. doi: 10.1111/j.1440-1797.2007.00796.x PMID: 17498121.
37. Allen TJ, Cooper ME, Lan HY. Use of genetic mouse models in the study of diabetic nephropathy. Curr Diab Rep. 2004;4(6):435-40. PMID: 15539008.
38. Terami N, Ogawa D, Tachibana H, Hatanaka T, Wada J, Nakatsuka A, et al. Long-term treatment with the sodium glucose cotransporter 2 inhibitor, dapagliflozin, ameliorates glucose homeostasis and diabetic nephropathy in db/db mice. PLoS One. 2014;9(6):e100777. doi: 10.1371/journal.pone.0100777 PMID: 24960177; PubMed Central PMCID: PMC4069074.
39. Gembardt F, Bartaun C, Jarzebska N, Mayoux E, Todorov VT, Hohenstein B, et al. The SGLT2 inhibitor empagliflozin ameliorates early features of diabetic nephropathy in BTBR ob/ob type 2 diabetic mice with and without hypertension. Am J Physiol Renal Physiol. 2014;307(3):F317-25. doi: 10.1152/ajprenal.00145.2014 PMID: 24944269.
40. Vallon V, Gerasimova M, Rose MA, Masuda T, Satriano J, Mayoux E, et al. SGLT2 inhibitor empagliflozin reduces renal growth and albuminuria in proportion to hyperglycemia and prevents glomerular hyperfiltration in diabetic Akita mice. Am J Physiol Renal Physiol. 2014;306(2):F194-204. doi: 10. 1152/ajprenal.00520.2013 PMID: 24226524; PubMed Central PMCID: PMC3920018.
41. Nagata T, Fukuzawa T, Takeda M, Fukazawa M, Mori T, Nihei T, et al. Tofogliflozin, a novel sodiumglucose co-transporter 2 inhibitor, improves renal and pancreatic function in db/db mice. Br J Pharmacol. 2013;170(3):519-31. doi: 10.1111/bph.12269 PMID: 23751087; PubMed Central PMCID: PMC3791991.
42. Cordonnier DJ, Pinel N, Barro C, Maynard C, Zaoui P, Halimi S, et al. Expansion of cortical interstitium is limited by converting enzyme inhibition in type 2 diabetic patients with glomerulosclerosis. Journal of the American Society of Nephrology. 1999;10(6):1253-63. PMID: 10361863
43. Ruster C, Wolf G. Angiotensin II as a morphogenic cytokine stimulating renal fibrogenesis. J Am Soc Nephrol. 2011;22(7):1189-99. doi: 10.1681/ASN.2010040384 PMID: 21719784.
44. Kagami S, Border WA, Miller DE, Noble NA. Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-beta expression in rat glomerular mesangial cells. J Clin Invest. 1994;93(6):2431-7. PMID: 8200978
45. Wolf G, Mueller E, Stahl RAK, Ziyadeh FN. Angiotensin II-induced hypertrophy of cultured murine proximal tubular cells is mediated by endogenous transforming growth factor-β. J Clin Invest. 1993;92:1366-72. PMID: 7690779
46. Gilbert RE, Cox A, Wu LL, Allen TJ, Hulthen L, Jerums G, et al. Expression of transforming growth factor-β1 and type IV collagen in the renal tubulointerstitium in experimental diabetes: effects of angiotensin converting enzyme inhibition. Diabetes. 1998;47:414-22. PMID: 9519748
47. Langham RG, Kelly DJ, Gow RM, Zhang Y, Cordonnier DJ, Pinel N, et al. Transforming growth factorbeta in human diabetic nephropathy: effects of ACE inhibition. Diabetes Care. 2006;29(12):2670-5. PMID: 17130203.
48. Houlihan CA, Akdeniz A, Tsalamandris C, Cooper ME, Jerums G, Gilbert RE. Urinary transforming growth factor-beta excretion in patients with hypertension, type 2 diabetes, and elevated albumin excretion rate: effects of angiotensin receptor blockade and sodium restriction. Diabetes Care. 2002;25(6):1072-7. PMID: 12032117.
49. Komoroski B, Vachharajani N, Feng Y, Li L, Kornhauser D, Pfister M. Dapagliflozin, a novel, selective SGLT2 inhibitor, improved glycemic control over 2 weeks in patients with type 2 diabetes mellitus. Clin Pharmacol Ther. 2009;85(5):513-9. doi: 10.1038/clpt.2008.250 PMID: 19129749.
50. Gilbert RE. SGLT-2 inhibition in patients with kidney disease. Diabetes Metab. 2014;40(6 Suppl 1):S23-7. doi: 10.1016/S1262-3636 (14) 72692-8 PMID: 25554068.
51. Lambers Heerspink HJ, de Zeeuw D, Wie L, Leslie B, List J. Dapagliflozin a glucose-regulating drug with diuretic properties in subjects with type 2 diabetes. Diabetes Obes Metab. 2013;15(9):853-62. doi: 10.1111/dom.12127 PMID: 23668478; PubMed Central PMCID: PMC3906841.
52. Seyer-Hansen K. Renal hypertrophy in experimental diabetes. Kidney Int. 1983;23:643-6. PMID: 6571419
53. Gangadharan Komala M, Gross S, Mudaliar H, Huang C, Pegg K, Mather A, et al. Inhibition of kidney proximal tubular glucose reabsorption does not prevent against diabetic nephropathy in type 1 diabetic eNOS knockout mice. PLoS One. 2014;9(11):e108994. doi: 10.1371/journal.pone.0108994 PMID: 25369239; PubMed Central PMCID: PMC4219667.