open access

Vol 74, No 4 (2023)
Review paper
Submitted: 2023-02-22
Accepted: 2023-03-13
Published online: 2023-06-30
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The influence of SGLT2 inhibitors on oxidative stress in heart failure and chronic kidney disease in patients with type 2 diabetes

Diana Nabrdalik-Leśniak1, Katarzyna Nabrdalik23, Krzysztof Irlik4, Oliwia Janota1, Hanna Kwiendacz2, Paulina Szromek-Białek2, Mirosław Maziarz2, Tomasz Stompór5, Janusz Gumprecht2, Gregory Y. H. Lip36
·
Pubmed: 37431873
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Endokrynol Pol 2023;74(4):349-362.
Affiliations
  1. Doctoral School, Department of Internal Medicine, Diabetology, and Nephrology, Faculty of Medical Sciences in Zabrze, Medical University of Silesia, Katowice, Poland
  2. Department of Internal Medicine, Diabetology and Nephrology, Faculty of Medical Sciences in Zabrze, Medical University of Silesia, Katowice, Poland
  3. Liverpool Centre for Cardiovascular Science at University of Liverpool, Liverpool John Moores University and Liverpool Heart & Chest Hospital, Liverpool, United Kingdom
  4. Students’ Scientific Association by the Department of Internal Medicine, Diabetology and Nephrology, Faculty of Medical Sciences in Zabrze, Medical University of Silesia, Katowice, Poland
  5. Department of Nephrology, Hypertensiology, and Internal Diseases, University of Warmia and Mazury, Olsztyn, Poland
  6. Department of Clinical Medicine, Aalborg University, Aalborg, Denmark

open access

Vol 74, No 4 (2023)
Review Article
Submitted: 2023-02-22
Accepted: 2023-03-13
Published online: 2023-06-30

Abstract

There is increasing interest in sodium-glucose cotransporter 2 inhibitors (SGLT2i) as not only a new oral glucose-lowering drug class but also one with cardio- and nephroprotective potential. Understanding the underlying mechanisms is therefore of great interest, and postulated benefits have included increased natriuresis, lower blood pressure, increased haematocrit, enhanced cardiac fatty acid utilization, reduced low-grade inflammation, and decreased oxidative stress. In particular, redox homeostasis seems to be crucial in the pathogenesis of heart and kidney disease in diabetes, and there is accumulating evidence that SGLT2i have beneficial effects in this perspective.

In this review, we aimed to summarize the potential mechanisms of the influence of SGLT2i on oxidative stress parameters in animal and human studies, with a special focus on heart failure and chronic kidney disease in diabetes mellitus.

Abstract

There is increasing interest in sodium-glucose cotransporter 2 inhibitors (SGLT2i) as not only a new oral glucose-lowering drug class but also one with cardio- and nephroprotective potential. Understanding the underlying mechanisms is therefore of great interest, and postulated benefits have included increased natriuresis, lower blood pressure, increased haematocrit, enhanced cardiac fatty acid utilization, reduced low-grade inflammation, and decreased oxidative stress. In particular, redox homeostasis seems to be crucial in the pathogenesis of heart and kidney disease in diabetes, and there is accumulating evidence that SGLT2i have beneficial effects in this perspective.

In this review, we aimed to summarize the potential mechanisms of the influence of SGLT2i on oxidative stress parameters in animal and human studies, with a special focus on heart failure and chronic kidney disease in diabetes mellitus.

Get Citation

Keywords

sodium-glucose cotransporter 2 inhibitors; oxidative stress; diabetes mellitus; chronic kidney disease; heart failure

About this article
Title

The influence of SGLT2 inhibitors on oxidative stress in heart failure and chronic kidney disease in patients with type 2 diabetes

Journal

Endokrynologia Polska

Issue

Vol 74, No 4 (2023)

Article type

Review paper

Pages

349-362

Published online

2023-06-30

Page views

1207

Article views/downloads

537

DOI

10.5603/EP.a2023.0039

Pubmed

37431873

Bibliographic record

Endokrynol Pol 2023;74(4):349-362.

Keywords

sodium-glucose cotransporter 2 inhibitors
oxidative stress
diabetes mellitus
chronic kidney disease
heart failure

Authors

Diana Nabrdalik-Leśniak
Katarzyna Nabrdalik
Krzysztof Irlik
Oliwia Janota
Hanna Kwiendacz
Paulina Szromek-Białek
Mirosław Maziarz
Tomasz Stompór
Janusz Gumprecht
Gregory Y. H. Lip

References (102)
  1. Ling X, Kuo KL. Oxidative stress in chronic kidney disease. Renal Replace Ther. 2018; 4(1).
  2. Marrocco I, Altieri F, Peluso I. Measurement and Clinical Significance of Biomarkers of Oxidative Stress in Humans. Oxid Med Cell Longev. 2017; 2017: 6501046.
  3. IDF Diabetes Atlas. https://diabetesatlas.org..
  4. Einarson TR, Acs A, Ludwig C, et al. Prevalence of cardiovascular disease in type 2 diabetes: a systematic literature review of scientific evidence from across the world in 2007-2017. Cardiovasc Diabetol. 2018; 17(1): 83.
  5. World Health Organization. Cardiovascular diseases (CVDs). https://www who int/news-room/fact-sheets/detail/cardiovascular-diseases-(cvds).
  6. Lovre D, Shah S, Sihota A, et al. Managing Diabetes and Cardiovascular Risk in Chronic Kidney Disease Patients. Endocrinol Metab Clin North Am. 2018; 47(1): 237–257.
  7. Zinman B, Wanner C, Lachin JM, et al. EMPA-REG OUTCOME Investigators. Empagliflozin, Cardiovascular Outcomes, and Mortality in Type 2 Diabetes. N Engl J Med. 2015; 373(22): 2117–2128.
  8. Neal B, Perkovic V, Mahaffey KW, et al. CANVAS Program Collaborative Group. Canagliflozin and Cardiovascular and Renal Events in Type 2 Diabetes. N Engl J Med. 2017; 377(7): 644–657.
  9. Akinci B. Dapagliflozin and Cardiovascular Outcomes in Type 2 Diabetes. N Engl J Med. 2019; 380(19): 1880–1882.
  10. Anker S, Butler J, Filippatos G, et al. Empagliflozin in Heart Failure with a Preserved Ejection Fraction. N Engl J Med. 2021; 385(16): 1451–1461.
  11. Packer M, Anker SD, Butler J, et al. EMPEROR-Reduced Trial Committees and Investigators. Empagliflozin in Patients With Heart Failure, Reduced Ejection Fraction, and Volume Overload: EMPEROR-Reduced Trial. J Am Coll Cardiol. 2021; 77(11): 1381–1392.
  12. Herrington WG, Staplin N, Wanner C, et al. The EMPA-KIDNEY Collaborative Group. Empagliflozin in Patients with Chronic Kidney Disease. N Engl J Med. 2023; 388(2): 117–127.
  13. McMurray JJV, Solomon SD, Inzucchi SE, et al. DAPA-HF Trial Committees and Investigators. Dapagliflozin in Patients with Heart Failure and Reduced Ejection Fraction. N Engl J Med. 2019; 381(21): 1995–2008.
  14. Solomon SD, McMurray JJV, Claggett B, et al. DELIVER Trial Committees and Investigators. Dapagliflozin in Heart Failure with Mildly Reduced or Preserved Ejection Fraction. N Engl J Med. 2022; 387(12): 1089–1098.
  15. Heerspink HJL, Stefánsson BV, Correa-Rotter R, et al. DAPA-CKD Trial Committees and Investigators. Dapagliflozin in Patients with Chronic Kidney Disease. N Engl J Med. 2020; 383(15): 1436–1446.
  16. Wróbel M, Rokicka D, Strojek K. Flozins - in the light of the latest recommendations. Endokrynol Pol. 2021; 72(6): 589–591.
  17. Griffin M, Rao VS, Ivey-Miranda J, et al. Empagliflozin in Heart Failure: Diuretic and Cardiorenal Effects. Circulation. 2020; 142(11): 1028–1039.
  18. Baker WL, Smyth LR, Riche DM, et al. Effects of sodium-glucose co-transporter 2 inhibitors on blood pressure: a systematic review and meta-analysis. J Am Soc Hypertens. 2014; 8(4): 262–75.e9.
  19. Fitchett D, Inzucchi SE, Zinman B, et al. Mediators of the improvement in heart failure outcomes with empagliflozin in the EMPA-REG OUTCOME trial. ESC Heart Fail. 2021; 8(6): 4517–4527.
  20. Kim SoRa, Lee SG, Kim SH, et al. SGLT2 inhibition modulates NLRP3 inflammasome activity via ketones and insulin in diabetes with cardiovascular disease. Nat Commun. 2020; 11(1): 2127.
  21. Verma S, Rawat S, Ho KL, et al. Empagliflozin Increases Cardiac Energy Production in Diabetes: Novel Translational Insights Into the Heart Failure Benefits of SGLT2 Inhibitors. JACC Basic Transl Sci. 2018; 3(5): 575–587.
  22. Ferrannini E, Baldi S, Frascerra S, et al. Shift to Fatty Substrate Utilization in Response to Sodium-Glucose Cotransporter 2 Inhibition in Subjects Without Diabetes and Patients With Type 2 Diabetes. Diabetes. 2016; 65(5): 1190–1195.
  23. Shigiyama F, Kumashiro N, Miyagi M, et al. Effectiveness of dapagliflozin on vascular endothelial function and glycemic control in patients with early-stage type 2 diabetes mellitus: DEFENCE study. Cardiovasc Diabetol. 2017; 16(1): 84.
  24. Kolijn D, Pabel S, Tian Y, et al. Empagliflozin improves endothelial and cardiomyocyte function in human heart failure with preserved ejection fraction via reduced pro-inflammatory-oxidative pathways and protein kinase Gα oxidation. Cardiovasc Res. 2021; 117(2): 495–507.
  25. Nabrdalik-Leśniak D, Nabrdalik K, Sedlaczek K, et al. Influence of SGLT2 Inhibitor Treatment on Urine Antioxidant Status in Type 2 Diabetic Patients: A Pilot Study. Oxid Med Cell Longev. 2021; 2021: 5593589.
  26. Winiarska A, Knysak M, Nabrdalik K, et al. Inflammation and Oxidative Stress in Diabetic Kidney Disease: The Targets for SGLT2 Inhibitors and GLP-1 Receptor Agonists. Int J Mol Sci. 2021; 22(19).
  27. He J, Ogden LG, Bazzano LA, et al. Risk factors for congestive heart failure in US men and women: NHANES I epidemiologic follow-up study. Arch Intern Med. 2001; 161(7): 996–1002.
  28. Guglin M, Lynch K, Krischer J. Heart failure as a risk factor for diabetes mellitus. Cardiology. 2014; 129(2): 84–92.
  29. Lommi J, Kupari M, Yki-Järvinen H. Free fatty acid kinetics and oxidation in congestive heart failure. Am J Cardiol. 1998; 81(1): 45–50.
  30. Suskin N, McKelvie RS, Burns RJ, et al. Glucose and insulin abnormalities relate to functional capacity in patients with congestive heart failure. Eur Heart J. 2000; 21(16): 1368–1375.
  31. Maack C, Lehrke M, Backs J, et al. Heart failure and diabetes: metabolic alterations and therapeutic interventions: a state-of-the-art review from the Translational Research Committee of the Heart Failure Association-European Society of Cardiology. Eur Heart J. 2018; 39(48): 4243–4254.
  32. Kayama Y, Raaz U, Jagger A, et al. Diabetic Cardiovascular Disease Induced by Oxidative Stress. Int J Mol Sci. 2015; 16(10): 25234–25263.
  33. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005; 54(6): 1615–1625.
  34. Wold LE, Ceylan-Isik AF, Ren J. Oxidative stress and stress signaling: menace of diabetic cardiomyopathy. Acta Pharmacol Sin. 2005; 26(8): 908–917.
  35. Alvarez MC, Caldiz C, Fantinelli JC, et al. Is cardiac hypertrophy in spontaneously hypertensive rats the cause or the consequence of oxidative stress? Hypertens Res. 2008; 31(7): 1465–1476.
  36. Aragno M, Mastrocola R, Alloatti G, et al. Oxidative stress triggers cardiac fibrosis in the heart of diabetic rats. Endocrinology. 2008; 149(1): 380–388.
  37. Fu YC, Chi CS, Yin SC, et al. Norepinephrine induces apoptosis in neonatal rat cardiomyocytes through a reactive oxygen species-TNF alpha-caspase signaling pathway. Cardiovasc Res. 2004; 62(3): 558–567.
  38. Che R, Yuan Y, Huang S, et al. Mitochondrial dysfunction in the pathophysiology of renal diseases. Am J Physiol Renal Physiol. 2014; 306(4): F367–F378.
  39. Sedeek M, Callera G, Montezano A, et al. Critical role of Nox4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: implications in type 2 diabetic nephropathy. Am J Physiol Renal Physiol. 2010; 299(6): F1348–F1358.
  40. Kashihara N, Haruna Y, Kondeti VK, et al. Oxidative stress in diabetic nephropathy. Curr Med Chem. 2010; 17(34): 4256–4269.
  41. Srinivasan S, Hatley ME, Bolick DT, et al. Hyperglycaemia-induced superoxide production decreases eNOS expression via AP-1 activation in aortic endothelial cells. Diabetologia. 2004; 47(10): 1727–1734.
  42. Yu M, Kim YJ, Kang DH. Indoxyl Sulfate–Induced Endothelial Dysfunction in Patients with Chronic Kidney Disease via an Induction of Oxidative Stress. Clin J Am Soc Nephrol. 2011; 6(1): 30–39.
  43. Dou L, Jourde-Chiche N, Faure V, et al. The uremic solute indoxyl sulfate induces oxidative stress in endothelial cells. J Thromb Haemost. 2007; 5(6): 1302–1308.
  44. Tbahriti HF, Kaddous A, Bouchenak M, et al. Effect of different stages of chronic kidney disease and renal replacement therapies on oxidant-antioxidant balance in uremic patients. Biochem Res Int. 2013; 2013: 358985.
  45. Zachara BA. Selenium and selenium-dependent antioxidants in chronic kidney disease. Adv Clin Chem. 2015; 68: 131–151.
  46. Ceballos-Picot I, Witko-Sarsat V, Merad-Boudia M, et al. Glutathione antioxidant system as a marker of oxidative stress in chronic renal failure. Free Radic Biol Med. 1996; 21(6): 845–853.
  47. Hasdan G, Benchetrit S, Rashid G, et al. Endothelial dysfunction and hypertension in 5/6 nephrectomized rats are mediated by vascular superoxide. Kidney Int. 2002; 61(2): 586–590.
  48. Ceballos-Picot I, Witko-Sarsat V, Merad-Boudia M, et al. Glutathione antioxidant system as a marker of oxidative stress in chronic renal failure. Free Radic Biol Med. 1996; 21(6): 845–853.
  49. Ha H, Lee HB. Reactive oxygen species as glucose signaling molecules in mesangial cells cultured under high glucose. Kidney Int Suppl. 2000; 77: S19–S25.
  50. Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes. 1991; 40(4): 405–412.
  51. Salahudeen AK, Kanji V, Reckelhoff JF, et al. Pathogenesis of diabetic nephropathy: a radical approach. Nephrol Dial Transplant. 1997; 12(4): 664–668.
  52. Satoh M, Fujimoto S, Haruna Y, et al. NAD(P)H oxidase and uncoupled nitric oxide synthase are major sources of glomerular superoxide in rats with experimental diabetic nephropathy. Am J Physiol Renal Physiol. 2005; 288(6): F1144–F1152.
  53. Gorin Y, Block K, Hernandez J, et al. Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J Biol Chem. 2005; 280(47): 39616–39626.
  54. Zhang L, Liu J, Zhou F, et al. PGC-1α ameliorates kidney fibrosis in mice with diabetic kidney disease through an antioxidative mechanism. Mol Med Rep. 2018; 17(3): 4490–4498.
  55. Li Li, Zhang L, Chen D, et al. PEDF relieves kidney injury in type 2 diabetic nephropathy mice by reducing macrophage infiltration. Endokrynol Pol. 2021; 72(6): 643–651.
  56. Bondor CI, Potra AR, Moldovan D, et al. Relationship of adiponectin to markers of oxidative stress in type 2 diabetic patients: influence of incipient diabetes-associated kidney disease. Int Urol Nephrol. 2015; 47(7): 1173–1180.
  57. Apakkan Aksun S, Ozmen B, Ozmen D, et al. Serum and urinary nitric oxide in Type 2 diabetes with or without microalbuminuria: relation to glomerular hyperfiltration. J Diabetes Complications. 2003; 17(6): 343–348.
  58. Roumeliotis A, Roumeliotis S, Tsetsos F, et al. Oxidative Stress Genes in Diabetes Mellitus Type 2: Association with Diabetic Kidney Disease. Oxid Med Cell Longev. 2021; 2021: 2531062.
  59. DeFronzo RA, Hompesch M, Kasichayanula S, 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): 3169–3176.
  60. Zelniker TA, Braunwald E. Mechanisms of Cardiorenal Effects of Sodium-Glucose Cotransporter 2 Inhibitors: JACC State-of-the-Art Review. J Am Coll Cardiol. 2020; 75(4): 422–434.
  61. Vallon V, Rose M, Gerasimova M, et al. Knockout of Na-glucose transporter SGLT2 attenuates hyperglycemia and glomerular hyperfiltration but not kidney growth or injury in diabetes mellitus. Am J Physiol Renal Physiol. 2013; 304(2): F156–F167.
  62. Ni L, Yuan C, Chen G, et al. SGLT2i: beyond the glucose-lowering effect. Cardiovasc Diabetol. 2020; 19(1): 98.
  63. Aragón-Herrera A, Feijóo-Bandín S, Otero Santiago M, et al. Empagliflozin reduces the levels of CD36 and cardiotoxic lipids while improving autophagy in the hearts of Zucker diabetic fatty rats. Biochem Pharmacol. 2019; 170: 113677.
  64. Salt I, Hardie D. AMP-Activated Protein Kinase. Circul Res. 2017; 120(11): 1825–1841.
  65. Zhou H, Wang S, Zhu P, et al. Empagliflozin rescues diabetic myocardial microvascular injury via AMPK-mediated inhibition of mitochondrial fission. Redox Biol. 2018; 15: 335–346.
  66. Chen R, Dioum EM, Hogg RT, et al. Hypoxia increases sirtuin 1 expression in a hypoxia-inducible factor-dependent manner. J Biol Chem. 2011; 286(16): 13869–13878.
  67. Lee WC, Chau YY, Ng HY, et al. Empagliflozin Protects HK-2 Cells from High Glucose-Mediated Injuries via a Mitochondrial Mechanism. Cells. 2019; 8(9).
  68. Liu X, Xu C, Xu L, et al. Empagliflozin improves diabetic renal tubular injury by alleviating mitochondrial fission via AMPK/SP1/PGAM5 pathway. Metabolism. 2020; 111: 154334.
  69. Lee YH, Kim SH, Kang JM, et al. Empagliflozin attenuates diabetic tubulopathy by improving mitochondrial fragmentation and autophagy. Am J Physiol Renal Physiol. 2019; 317(4): F767–F780.
  70. Vallon V, Gerasimova M, Rose MA, 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–F204.
  71. Ojima A, Matsui T, Nishino Y, et al. Empagliflozin, an Inhibitor of Sodium-Glucose Cotransporter 2 Exerts Anti-Inflammatory and Antifibrotic Effects on Experimental Diabetic Nephropathy Partly by Suppressing AGEs-Receptor Axis. Horm Metab Res. 2015; 47(9): 686–692.
  72. Hudkins KL, Li X, Holland AL, et al. Regression of diabetic nephropathy by treatment with empagliflozin in BTBR ob/ob mice. Nephrol Dial Transplant. 2022; 37(5): 847–859.
  73. Tang Li, Wu Y, Tian Mi, et al. Dapagliflozin slows the progression of the renal and liver fibrosis associated with type 2 diabetes. Am J Physiol Endocrinol Metab. 2017; 313(5): E563–E576.
  74. Tanaka S, Sugiura Y, Saito H, et al. Sodium-glucose cotransporter 2 inhibition normalizes glucose metabolism and suppresses oxidative stress in the kidneys of diabetic mice. Kidney Int. 2018; 94(5): 912–925.
  75. Abdel-Wahab AF, Bamagous GA, Al-Harizy RM, et al. Renal protective effect of SGLT2 inhibitor dapagliflozin alone and in combination with irbesartan in a rat model of diabetic nephropathy. Biomed Pharmacother. 2018; 103: 59–66.
  76. Wu X, Li He, Wan Z, et al. The combination of ursolic acid and empagliflozin relieves diabetic nephropathy by reducing inflammation, oxidative stress and renal fibrosis. Biomed Pharmacother. 2021; 144: 112267.
  77. Food and Drug Administration. Drug Approval Package. Invokana (canagliflozin) Tablets. https://www accessdata fda gov/drugsatfda_docs/nda/2013/204042Orig1s000TOC cfm.
  78. Anderson EJ, Kypson AP, Rodriguez E, et al. Substrate-specific derangements in mitochondrial metabolism and redox balance in the atrium of the type 2 diabetic human heart. J Am Coll Cardiol. 2009; 54(20): 1891–1898.
  79. Montaigne D, Marechal X, Coisne A, et al. Myocardial contractile dysfunction is associated with impaired mitochondrial function and dynamics in type 2 diabetic but not in obese patients. Circulation. 2014; 130(7): 554–564.
  80. Connelly K, Advani A, Advani S, et al. Impaired cardiac anti-oxidant activity in diabetes: human and correlative experimental studies. Acta Diabetol. 2014; 51(5): 771–782.
  81. Wang B, Raedschelders K, Shravah J, et al. Differences in myocardial PTEN expression and Akt signalling in type 2 diabetic and nondiabetic patients undergoing coronary bypass surgery. Clin Endocrinol (Oxf). 2011; 74(6): 705–713.
  82. Polidori MC, Praticó D, Savino K, et al. Increased F2 isoprostane plasma levels in patients with congestive heart failure are correlated with antioxidant status and disease severity. J Card Fail. 2004; 10(4): 334–338.
  83. Gupte RS, Vijay V, Marks B, et al. Upregulation of glucose-6-phosphate dehydrogenase and NAD(P)H oxidase activity increases oxidative stress in failing human heart. J Card Fail. 2007; 13(6): 497–506.
  84. Li C, Zhang J, Xue M, et al. SGLT2 inhibition with empagliflozin attenuates myocardial oxidative stress and fibrosis in diabetic mice heart. Cardiovasc Diabetol. 2019; 18(1): 15.
  85. Steven S, Oelze M, Hanf A, et al. The SGLT2 inhibitor empagliflozin improves the primary diabetic complications in ZDF rats. Redox Biol. 2017; 13: 370–385.
  86. Habibi J, Aroor AR, Sowers JR, et al. Sodium glucose transporter 2 (SGLT2) inhibition with empagliflozin improves cardiac diastolic function in a female rodent model of diabetes. Cardiovasc Diabetol. 2017; 16(1): 9.
  87. Oelze M, Kröller-Schön S, Welschof P, et al. The sodium-glucose co-transporter 2 inhibitor empagliflozin improves diabetes-induced vascular dysfunction in the streptozotocin diabetes rat model by interfering with oxidative stress and glucotoxicity. PLoS One. 2014; 9(11): e112394.
  88. Lin B, Koibuchi N, Hasegawa Yu, et al. Glycemic control with empagliflozin, a novel selective SGLT2 inhibitor, ameliorates cardiovascular injury and cognitive dysfunction in obese and type 2 diabetic mice. Cardiovasc Diabetol. 2014; 13: 148.
  89. Xing YJ, Liu BH, Wan SJ, et al. A SGLT2 Inhibitor Dapagliflozin Alleviates Diabetic Cardiomyopathy by Suppressing High Glucose-Induced Oxidative Stress and . Front Pharmacol. 2021; 12: 708177.
  90. Tian J, Zhang M, Suo M, et al. Dapagliflozin alleviates cardiac fibrosis through suppressing EndMT and fibroblast activation via AMPKα/TGF-β/Smad signalling in type 2 diabetic rats. J Cell Mol Med. 2021; 25(16): 7642–7659.
  91. Kondo H, Akoumianakis I, Badi I, et al. Effects of canagliflozin on human myocardial redox signalling: clinical implications. Eur Heart J. 2021; 42(48): 4947–4960.
  92. Terami N, Ogawa D, Tachibana H, 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.
  93. Shin SJ, Chung S, Kim SJ, et al. Effect of Sodium-Glucose Co-Transporter 2 Inhibitor, Dapagliflozin, on Renal Renin-Angiotensin System in an Animal Model of Type 2 Diabetes. PLoS One. 2016; 11(11): e0165703.
  94. Kamezaki M, Kusaba T, Komaki K, et al. Comprehensive renoprotective effects of ipragliflozin on early diabetic nephropathy in mice. Sci Rep. 2018; 8(1): 4029.
  95. Cooper Woods T, Satou R, Miyata K, et al. Canagliflozin Prevents Intrarenal Angiotensinogen Augmentation and Mitigates Kidney Injury and Hypertension in Mouse Model of Type 2 Diabetes Mellitus. Am J Nephrol. 2019; 49(4): 331–342.
  96. Ali BH, Al Salam S, Al Suleimani Y, et al. Effects of the SGLT-2 Inhibitor Canagliflozin on Adenine-Induced Chronic Kidney Disease in Rats. Cell Physiol Biochem. 2019; 52(1): 27–39.
  97. Hasan R, Lasker S, Hasan A, et al. Canagliflozin ameliorates renal oxidative stress and inflammation by stimulating AMPK-Akt-eNOS pathway in the isoprenaline-induced oxidative stress model. Sci Rep. 2020; 10(1): 14659.
  98. Kim MN, Moon JH, Cho YM. Sodium-glucose cotransporter-2 inhibition reduces cellular senescence in the diabetic kidney by promoting ketone body-induced NRF2 activation. Diabetes Obes Metab. 2021; 23(11): 2561–2571.
  99. Ahmed AS, Mona MM, Abdel-Kareem MA, et al. SGLT2 inhibitor empagliflozin monotherapy alleviates renal oxidative stress in albino Wistar diabetic rats after myocardial infarction induction. Biomed Pharmacother. 2021; 139: 111624.
  100. Chi PJ, Lee CJ, Hsieh YJ, et al. Dapagliflozin Ameliorates Lipopolysaccharide Related Acute Kidney Injury in Mice with Streptozotocin-induced Diabetes Mellitus. Int J Med Sci. 2022; 19(4): 729–739.
  101. Osonoi T, Gouda M, Kubo M, et al. Effect of Canagliflozin on Urinary Albumin Excretion in Japanese Patients with Type 2 Diabetes Mellitus and Microalbuminuria: A Pilot Study. Diabetes Technol Ther. 2018; 20(10): 681–688.
  102. Liu H, Sridhar VS, Lovblom LE, et al. Markers of Kidney Injury, Inflammation, and Fibrosis Associated With Ertugliflozin in Patients With CKD and Diabetes. Kidney Int Rep. 2021; 6(8): 2095–2104.

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