Dapagliflozin rescues endoplasmic reticulum stress-mediated cell death

Scientific Reports

Volumn 9, Issue 1, 2019, Pages

  Shibusawa, Ryo ^a   Yamada, Eijiro ^a   Okada, Shuichi ^a   Nakajima, Yasuyo ^a   Bastie, Claire C ^b   Maeshima, Akito ^c   Kaira, Kyoichi ^a   Yamada, Masanobu ^a  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2-(3-(4-ETHOXYBENZYL)-4-CHLOROPHENYL)-6-HYDROXYMETHYLTETRAHYDRO-2H-PYRAN-3,4,5-TRIOL; BENZHYDRYL DERIVATIVE; GLUCOSE; GLUCOSIDE;

ANIMAL; APOPTOSIS; CELL DEATH; CELL LINE; DIABETIC NEPHROPATHY; DRUG EFFECT; ENDOPLASMIC RETICULUM STRESS; EPITHELIUM CELL; HUMAN; KIDNEY; MALE; METABOLISM; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS;

ANIMALS; APOPTOSIS; BENZHYDRYL COMPOUNDS; CELL DEATH; CELL LINE; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; ENDOPLASMIC RETICULUM STRESS; EPITHELIAL CELLS; GLUCOSE; GLUCOSIDES; HUMANS; KIDNEY; MALE; MICE; SODIUM-GLUCOSE TRANSPORTER 2 INHIBITORS;

EID: 85068775267     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-019-46402-6     Document Type: Article

References (56)

1. Tuomilehto, J. et al. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N. Engl. J. Med. 344(18), 1343–1350 (2001).
2. Orozco, L. J. et al. Exercise or exercise and diet for preventing type 2 diabetes mellitus. Cochrane Database Syst. Rev. 3, CD003054 (2008).
3. Baik, J., Nguyen, D., Nguyen, V., Hu, Z. & Abbott, G. W. Kcne2 deletion impairs insulin secretion and causes type 2 diabetes mellitus. FASEB J. 31(6), 2674–2685 (2017).
4. Costantino, L., Rastelli, G., Vianello, P., Cignarella, G. & Barlocco, D. Diabetes complications and their potential prevention: aldose reductase inhibition and other approaches. Med. Res. Rev. 19(1), 3–23 (1999).
5. Fan, Y., Lee, K., Wang, N. & He, J. C. The role of endoplasmic reticulum stress in diabetic nephropathy. Curr. Diab. Rep. 17, 17 (2017).
6. Cunard, R. Endoplasmic reticulum stress in the diabetic kidney, the good, the bad and the ugly. J. Clin. Med. 4, 715–740 (2015).
7. Cao, S. S. & Kaufman, R. J. Unfolded protein response. Curr. Biol. 22(16), R622–R626 (2012).
8. Ellgaard, L., Molinari, M. & Helenius, A. Setting the standards: quality control in the secretory pathway. Science 286(5446), 1882–1888 (1999).
9. Harding, H. P., Zhang, Y., Bertolotti, A., Zeng, H. & Ron, D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell. 5(5), 897–904 (2000).
10. Huber, A. L. et al. p58(IPK)-mediated attenuation of the proapoptotic PERK-CHOP pathway allows malignant progression upon low glucose. Mol. Cell. 49(6), 1049–1059 (2013).
11. Chen, X., Shen, J. & Prywes, R. The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. J. Biol. Chem. 277(15), 13045–13052 (2010).
12. Urano, F. et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287(5453), 664–666 (2000).
13. Liu, G. et al. Apoptosis induced by endoplasmic reticulum stress involved in diabetic kidney disease. Biochem. Biophys. Res. Commun. 370(4), 651–656 (2008).
14. Basha, B., Samuel, S. M., Triggle, C. R. & Ding, H. Endothelial dysfunction in diabetes mellitus: possible involvement of endoplasmic reticulum stress? Exp. Diabetes Res. 2012, 481840 (2012).
15. Zhong, Y. et al. Activation of endoplasmic reticulum stress by hyperglycemia is essential for Müller cell-derived inflammatory cytokine production in diabetes. Diabetes 61(2), 492–504 (2012).
16. Ponnusamy, S. et al. Sphingolipids and cancer: ceramide and sphingosine-1-phosphate in the regulation of cell death and drug resistance. Future Oncol. 6(10), 1603–1624 (2010).
17. Movsesyan, V. A., Yakovlev, A. G., Dabaghyan, E. A., Stoica, B. A. & Faden, A. I. Ceramide induces neuronal apoptosis through the caspase-9/caspase-3 pathway. Biochem. Biophys. Res. Commun. 299(2), 201–207 (2002).
18. Haus, J. M. et al. Plasma ceramides are elevated in obese subjects with type 2 diabetes and correlate with the severity of insulin resistance. Diabetes 58(2), 337–343 (2009).
19. Yaribeygi, H, Bo, S, Ruscica, M & Sahebkar, A. Ceramides and diabetes mellitus: an update on the potential molecular relationships. Diabet Med. Feb 25 (2019).
20. Galadari, S et al. Role of ceramide in diabetes mellitus: evidence and mechanisms. Lipids in Health and Disease 12 (98) (2013).
21. Srivastava, S. P. et al. Lipid mediators in diabetic nephronpathy. Fibrogenesis Tissue Repair. 7–12 (2014).
22. Choi, S. R. et al. Adiponectin receptor agonist AdipoRon decreased ceramide, and lipotoxicity, and ameliorated diabetic nephronpathy. Metabolism. 85, 348–360 (2018).
23. Bonventre, J. V. Can we target tubular damage to prevent renal function decline in diabetes? Semin. Nephrol. 32(5), 452–462 (2012).
24. Mosley, J. F. II, Smith, L., Everton, E. & Fellner, C. Sodium-glucose linked transporter 2 (SGLT2) inhibitors in the management of type-2. diabetes: a drug class overview. P T. 40(7), 451–462 (2015).
25. Gnudi, L., Coward, R. J. & Long, D. A. Diabetic nephropathy: perspective on novel molecular mechanisms. Trends Endocrinol. Metab. 27(11), 820–830 (2016).
26. Zhang, J., Fan, Y., Zeng, C., He, L. & Wang, N. Tauroursodeoxycholic acid attenuates renal tubular injury in a mouse model of type 2 diabetes. Nutrients 8 (10) (2016).
27. Cao, A. L. et al. Ursodeoxycholic acid and 4-phenylbutyrate prevent endoplasmic reticulum stress-induced podocyte apoptosis in diabetic nephropathy. Lab. Invest. 96(6), 610–622 (2016).
28. Fan, Y. et al. Rtn1a-Mediated Endoplasmic Reticulum Stress in Podocyte Injury and Diabetic Nephropathy. Sci Rep. 7(1), 323 (2017).
29. Chen, J. et al. stress triggers MCP-1 expression through SET7/9-induced histone methylation in the kidneys of db/db mice. Am J Physiol Renal Physiol. 306(8), F916–925 (2014).
30. Jia, Y. et al. Dapagliflozin Aggravates Renal Injury via Promoting Gluconeogenesis in db/db Mice. Cellular Physiology and Biochemistry 45, 1747–1758 (2018).
31. Terami, N. 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 9 (6) (2014).
32. Bakris, G. L., Fonseca, V. A., Sharma, K. & Wright, E. M. Renal sodium-glucose transport: role in diabetes mellitus and potential clinical implications. Kidney Int. 75(12), 1272–1277 (2009).
33. Komoroski, B. et al. Dapagliflozin, a Novel SGLT2 Inhibitor, Induces Dose‐Dependent Glucosuria in Healthy Subjects. Clinical Pharmacology & Therapeutics (2009)
34. Kasichayanula, S. et al. Clinical Pharmacokinetics and Pharmacodynamics of Dapagliflozin, a Selective Inhibitor of Sodium-Glucose Co-transporter Type 2. Clinical Pharmacokinetics 53(1), 17–27 (2014).
35. Lim, J. C. et al. Cannabinoid receptor 1 mediates high glucose-induced apoptosis via endoplasmic reticulum stress in primary cultured rat mesangial cells. American Journal of Physiology-Renal Physiology 301 (1) (2011).
36. Chang, Y. K. et al. Dapagliflozin, SGLT2 Inhibitor, Attenuates Renal Ischemia-Reperfusion Injury. PLoS One. 8, 11(7) (2016).
37. Lu, Y. T. et al. A Fluorescent Glucose Transport Assay for Screening SGLT2 Inhibitors in Endogenous SGLT2-Expressing HK-2 Cells. Nat Prod Bioprospect. 9(1), 13–21 (2019).
38. Kothinti, R. K., Blodgett, A. B., North, P. E., Roman, R. J. & Tabatabai, N. M. A novel SGLT is expressed in the human kidney. Eur J Pharmacol. 5;690(1–3), 77–83 (2012).
39. Karunakaran, U. et al. Myricetin Protects Against High Glucose-Induced β-Cell Apoptosis by Attenuating Endoplasmic Reticulum Stress via Inactivation of Cyclin-Dependent Kinase 5. Diabetes Metab J. 43(2), 192–205 (2019).
40. Ma, L. et al. Low glucose and metformin-induced apoptosis of human ovarian cancer cells is connected to ASK1 via mitochondrial and endoplasmic reticulum stress-associated pathways. J Exp Clin Cancer Res 38(1), 77 (2019).
41. Chang, J. W. et al. Up-Regulation of SIRT1 Reduces Endoplasmic Reticulum Stress and Renal Fibrosis. Nephron. 133(2), 116–128 (2016).
42. Jiang, X. et al. Overexpression of augmenter of liver regeneration (ALR) mitigates the effect of H(2)O(2)-induced endoplasmic reticulum stress in renal tubule epithelial cells. Apoptosis. 24(3-4), 278–289 (2019).
43. Lin, M. et al. Baicalin ameliorates H2O2 induced cytotoxicity in HK-2 cells through the inhibition of ER stress and the activation of Nrf2 signaling. Int J Mol Sci. 15;15(7), 12507–12522 (2014).
44. Zhou, X. et al. Propofol decreases endoplasmic reticulum stress-mediated apoptosis in retinal pigment epithelial cells. PLoS One 11(6), e0157590 (2016).
45. Ozcan, L. & Tabas, I. Role of endoplasmic reticulum stress in metabolic disease and other disorders. Annu. Rev. Med. 63, 317–328 (2012).
46. Zhang, K. & Kaufman, R. J. From endoplasmic-reticulum stress to the inflammatory response. Nature 454(7203), 455–462 (2008).
47. Wu, X., He, Y., Jing, Y., Li, K. & Zhang, J. Albumin overload induces apoptosis in renal tubular epithelial cells through a CHOP-dependent pathway. OMICS 14(1), 61–73 (2010).
48. Wang, M. & Kaufman, R. J. The impact of the endoplasmic reticulum protein-folding environment on cancer development. Nat. Rev. Cancer 14(9), 581–597 (2014).
49. Ogretmen, B. & Hannun, Y. A. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat. Rev. Cancer 4(8), 604–616 (2004).
50. Ueda, N., Kaushal, G. P., Hong, X. & Shah, S. V. Role of enhanced ceramide generation in DNA damage and cell death in chemical hypoxic injury to LLC-PK1 cells. Kidney Int. 54(2), 399–406 (1998).
51. Basnakian, A. G. et al. Ceramide synthase is essential for endonuclease-mediated death of renal tubular epithelial cells induced by hypoxia-reoxygenation. Am. J. Physiol. Renal Physiol. 288(2), F308–F314 (2005).
52. Komoroski, B. et al. Dapagliflozin, a novel, selective SGLT2 inhibitor, improved glycemic control over 2 weeks in patients with type 2 diabetes mellitus. Clin. Pharmacol. Ther. 85(5), 513–519 (2009).
53. Wanner, C. et al. EMPA-REG OUTCOME Investigators. Empagliflozin and Progression of Kidney Disease in Type 2 Diabetes. N Engl J Med. Jul 28;375(4), 323–34 (2016).
54. Neal, B. et al. CANVAS Program Collaborative Group. Canagliflozin and Cardiovascular and Renal Events in Type 2 Diabetes. N Engl J Med. Aug 17;377(7), 644–657(2017).
55. Zinman, B. et al. Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. N. Engl. J. Med. 373(22), 2117–2128 (2015).
56. Yamada, E. et al. Fyn phosphorylates AMPK to inhibit AMPK activity and AMP-dependent activation of autophagy. Oncotarget 7(46), 74612–74629 (2016).