QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS

Emine Sözüer; Yeter Topçu

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QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS

Year 2021, Volume: 22 Issue: 2, 131 - 138, 15.10.2021

Emine Sözüer Yeter Topçu

Abstract

Diabetes mellitus is an important health problem worldwide due to its frequency and complications. In this study, the protective effect of quercetin on the apoptotic changes of rat kidney in the early stages of diabetes induced by streptozotocin (STZ) was evaluated.
Rats are divided into 3 groups as control, diabetic and diabetic+quercetin groups. STZ was applied as a single dose of 50 mg/kg intraperitoneal (i.p.) to diabetic and diabetic+quercetin groups. Quercetin was given at 30 mg/kg i.p. once a day for 15 days, 48 hours after induction of diabetes. At the end of quercetin treatment, all animals were sacrificed and kidneys were harvested and weighed. The terminal deoxynucleotidyl transferase-mediated dUTP nick end-labeling assay (TUNEL) for apoptosis was performed and evaluated renal histopathology.
The induction of diabetes via STZ caused a significant increase in blood glucose levels, the index of glomerulosclerosis, the histopathologic score, the number of TUNEL positive tubular and glomerular cells. Quercetin treatment lowered blood glucose levels, prevented renal cell apoptotic changes and histopathological alterations in diabetic rat kidney.
The findings of the study suggested that quercetin may be useful in preventing diabetic nephropathy by regulating renal apoptotic changes that occur in the early stages of diabetes.

Keywords

streptozotocin, quercetin, nephropathy, apoptosis, Diabetes mellitus, rat

Supporting Institution

The study was supported by the Trakya University Scientific Research Committee.

Project Number

2017/15

References

1. Al-Rasheed, N.M., Fadda, L.M., Attia, H.A., Ali, H.M. & Al-Rasheed, N.M. 2017. Quercetin inhibits sodium nitrite-induced inflammation and apoptosis in different rats organs by suppressing Bax, HIF1-α, TGF-β, Smad-2, and AKT pathways. Journal of Biochemical and Molecular Toxicology, 31(5): e21883.
2. Ali, M.A.M., Heeba, G.H. & El-Sheikh, A.A.K. 2017. Modulation of heme oxygenase-1 expression and activity affects streptozotocin-induced diabetic nephropathy in rats. Fundamental & Clinical Pharmacology, 31(5): 546-557.
3. Allen, D.A., Harwood, S., Varagunam, M., Raftery, M.J. & Yaqoob, M.M. 2003. High glucose-induced oxidative stress causes apoptosis in proximal tubular epithelial cells and is mediated by multiple caspases. Federation of American Societies for Experimental Biolog, 17(8): 908-910.
4. American Diabetes Association: Diagnosis and classification of diabetes mellitus. Diabetes Care. http://care.diabetesjournals.org/content/33/Supplement_1/S62. (2010, accessed 15 May 2019)
5. Andallu, B. & Varadacharyulu, N.C. 2003. Antioxidant role of mulberry (Morus indica L. cv. Anantha) leaves in streptozotocin-diabetic rats. Clinica Chimica Acta, 338: 3-10.
6. Anjaneyulu, M. & Chopra, K. 2004. Quercetin, an antioxidan bioflavonoid, attenuates diabetic nephropathy in rats. Clinical and Experimental Pharmacology and Physiology, 31(4): 244-248.
7. Armagan, A., Uz, E., Yilmaz, H.R., Soyupek, S., Oksay, T. & Ozcelik, N. 2006. Effects of melatonin on lipid peroxidation and antioxidant enzymes in streptozotocin-induced diabetic rat testis. Asian Journal of Andrology, 8(5): 595-600.
8. Bamri-Ezzine, S., Ao, Z.J., Londono, I. Gingras, D. & Bendayan, M. 2003. Apoptosis of tubular epithelial cells in glycogen nephrosis during diabetes. Laboratory Investigation, 83: 1069-1080.
9. Bhathena, S.J. & Velasquez, M.T. 2002. Beneficial role of dietary phytoestrogens in obesity and diabetes. American Journal of Clinical Nutrition, 76(6): 1191-1201.
10. Bleyer, A.J., Fumo, P., Snipes, E.R., Goldfarb, S., Simmons, D.A. & Ziyadeh, F.N. 1994. Polyol pathway mediates high glucose-induced collagen synthesis in proximal tubule. Kidney International, 45(3): 659-666.
11. Cheisson, G., Jacqueminet, S., Cosson, E., Ichai, C., Leguerrier, A.M., Nicolescu-Catargi, B., Quattara, A., Valensi, P. & Benhamou, D. 2018. Review of hyperglycaemia: definitions and pathophysiology. Anaesthesia, Critical Care & Pain, 37: S5-S8.
12. Chen, S., Hong, S.W., Iglesias-dela Cruz, M.C., Isono, M., Casaretto, A. & Ziyadeh, F.N. 2001. The key role of the transforming growth factor-beta system in the pathogenesis of diabetic nephropathy. Renal Failure, 3(3&4): 471-481.
13. Chuang, P.Y., Yu, Q., Fang, W., Uribarri, J. & He, J.C. 2007. Advanced glycation endproducts induce podocyte apoptosis by activation of the FOXO4 transcription factor. Kidney International, 72: 965-976.
14. Coldiron, A.D., Sanders, R.A. & Watkins, J.B. 2002. Effects of combined quercetin and coenzyme Q10 treatment on oxidative stress in normal and diabetic rats. Journal of Biochemical and Molecular Toxicology, 16: 197-202.
15. Elbe, H., Vardi, N., Esrefoglu, M., Ates, B., Yologlu, S. & Taskapan, C. 2015. Amelioration of streptozotocin-induced diabetic nephropathy by melatonin, quercetin, and resveratrol in rats. Human and Experimental Toxicology. 34(1): 100-113.
16. Geoffroy, K., Troncy, L., Wiernsperger, N., Lagarde, M. & Bawab, S.E 2005. Glomerular proliferation during early stages of diabetic nephropathy is associated with local increase of sphingosine-1-phosphate levels. Federation of European Biochemical Societies, 579: 1249-1254.
17. Gilbert, R.E. & Cooper, M.E. 1999. The tubulointerstitium in progressive diabetic kidney disease: more than an aftermath of glomerular injury? Kidney International, 56: 1627-1637.
18. Giribabu, N., Karim, K., Kilari, E.K. & Salleh, N. 2017. Phyllanthus niruri leaves aqueous extract improves kidney functions, ameliorates kidney oxidative stress, inflammation, fibrosis and apoptosis and enhances kidney cell proliferation in adult male rats with diabetes mellitus. Journal of Ethnopharmacol, 205: 123-137.
19. Gomes, I.B., Porto, M.L., Santos, M.C., Campagnaro, B.P., Pereira T.MC., Meyrelles S.S. & Vasquez, E.C. 2014. Renoprotective, anti-oxidative and anti-apoptotic effects of oral low-dose quercetin in the C57BL/6J model of diabetic nephropathy. Lipids in Health and Disease, 13: 184.
20. Harwood, M., Danielewska-Nikiel, B., Borzelleca, J.F., Flaam, G.W., Williams, G.M. & Lines, T.C. 2007. A critical review of the data related to the safety of quercetin and lack of evidence of in vivo toxicity, including lack of genotoxic/carcinogenic properties. Food Chemical Toxicology, 45(11): 2179-2205.
21. Ichinose, K., Kawasaki, E. & Eguchi, K. 2007. Recent advancement of understanding pathogenesis of type 1 diabetes and potential relevance to diabetic nephropathy. American Journal of Nephrology, 27: 554-564.
22. Ji, L., Wang, Q., Huang, F., An, T., Guo, F., Zhao, Y., Liu, Y., He, Y., Song,Yi. & Qin, G. 2019. FOXO1 Overexpression attenuates tubulointerstitial fibrosis and apoptosis in diabetic kidneys by ameliorating oxidative injury via TXNIP-TRX. Hindawi Oxidative Medicine and Cellular Longevit,. https://doi.org/10.1155/219/3286928
23. Kaur, N., Kishore, L. & Singh, R. 2017. Dillenia indica L. attenuates diabetic nephropathy via inhibition of advanced glycation end products accumulation in STZ-nicotinamide induced diabetic rats. Journal of Traditional and Complementary Medicine, 8(1): 226-38.
24. Kelly, D.J., Cox, A.J., Tolcos, M., Cooper, M.E., Wilkinson-Berka, J.L. & Gilbert, R.E. 2002. Attenuation of tubular apoptosis by blockade of the renin-angiotensin system in diabetic Ren-2 rats. Kidney International, 61(1): 31-39.
25. Kolset, S.O., Reinholt, F.P. & Jenssen T. 2012. Diabetic nephropathy and extracellular matrix. Journal of Histochemistry and Cytochemistry, 60(12): 976-986.
26. Kushwaha, S. & Jena, G.B. 2012. Enalapril reduces germ cell toxicity in streptozotocin-induced diabetic rat: investigation on possible mechanisms. Naunyn-Schmiedeberg's Archives of Pharmacology, 385: 111-124.
27. Li, J.H., Huang, X.R., Zhu, H., Johnson, R. & Lan, H.Y. 2003. Role of TGF B signaling in extracellular matrix production under high glucose conditions. Kidney International, 63(6): 2010-2019.
28. Li, X., Zheng, T., Sang, S. & Lv, L. 2014. Quercetin ınhibits advanced glycation end product formation by trapping methylglyoxal and glyoxal. Journal of Agricultural and Food Chemistry, 62(50): 12152-12158.
29. Lin, C.F., Kuo, Y.T., Chen, T.Y. & Chien, C.T. 2016. Quercetin-Rich Guava (Psidium guajava) juice in combination with trehalose reduces autophagy, apoptosis and pyroptosis formation in the kidney and pancreas of type ıı diabetic rats. Molecule, 21(3): 334.
30. Liu, B.C., Chen, Q., Luo, D.D. 2003. Mechanisms of irbesartan in prevention of renal lesion in streptozotocin-induced diabetic rats. Acta Pharmacologica Sinica, 24(1): 67-73.
31. Mori, J., Patel, V.B., Ramprasath, T., Alrob, O.A., DesAulniers, J., Scholey, J.W., Lopaschuk, G.D. & Qudit, G.Y. 2014. Angiotensin 1-7 mediates renoprotection against diabetic nephropathy by reducing oxidative stress, inflammation, and lipotoxicity. American Journal of Physiology-Renal Physiology, 306(8): F812-F821.
32. Nessar, A. 2005. Advanced glycation endproducts-role in pathology of diabetic complications. Diabetes Research and Clinical Practice, 67(1): 3-21.
33. New, J.P., Canavan, J.P., Flyvbjerg, A., Hamon, G. Bilous, R.W. & Marshall, S.M. 1996. Renal enlargement and insulin-like growth factor-1 accumulation in the wistar rat model of experimental diabetes is not prevented by angiotensin converting enzyme inhibition. Diabetologia, 39(2): 166-171.
34. Offor, U., Naidu, E.C., Ogedengbe, O.O., Jegede, A.I., Peter, A.I. & Azu, O.O. 2019. Renal histopathological and biochemical changes following adjuvant intervention of Momordica charantia and antiretroviral therapy in diabetic rats. Iranian Journal of Basic Medical Science, 22(11): 1359-1367.
35. Ortiz, A., Ziyadeh, F.N. & Neilson, E.G. 1997. Expression of apoptosisregulatory genes in renal proximal tubular epithelial cells exposed to high ambient glucose and in diabetic kidneys. Journal of Investigative Medicine, 45(2): 50-56.
36. Roslan, J., Giribabu, N., Karim, K. & Salleh, N. 2017. Quercetin ameliorates oxidative stress, inflammation and apoptosis in the heart of streptozotocin-nicotinamide-induced adult male diabetic rats. Biomed Pharmacother, 86: 570-582.
37. Saito, T., Sumithran, E., Glasgow, E.F. & Atkins, R.C. 1987. The enhancement of aminonucleoside nephrosis by the co-administration of protamine. Kidney International, 32(5): 691-699.
38. Sanai, T., Sobka, T., Johnson, T., El-Essawy, M., Muchaneta-Kubara, E.C., Gharbia, O.B., Oldroyd, S. & El Nahas, A.M. 2000. Expression of cytoskeletal proteins during the course of experimental diabetic nephropathy. Diabetologia, 43(1): 91-100.
39. Senyigit, A., Durmus, S., Mirzatas, E.B., Ozsobacı, N.P., Gelisgen, R., Tuncdemir, M., Ozcelik, D., Simsek, G. & Uzun, H. 2019. Effects of quercetin on lipid and protein damage in the liver of streptozotocin-induced experimental diabetic rats. Journal of Medicinal Food, 22(1): 52-56.
40. Susztak, K., Raff, A.C., Schiffer, M. & Böttinger, E.P. 2006. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes, 55(1): 225-233.
41. Tan, A.L., Forbes, J.M. & Cooper, M.E. 2007. AGE, RAGE, and ROS in diabetic nephropathy. Seminars in Nephrology, 27(2): 130-143.
42. Tucker, B.J., Collins, R.C., Ziegler, M.G. & Blantz, R.C. 1991. Disassociation between glomerular hyperfiltration and extracellular volume in diabetic rats. Kidney International. 39: 1176-1183.
43. Tunçdemir, M., Mirzataş, E.B. & Uzun, H. 2018. Renoprotective potential of quercetin in experimental diabetic nephropathy: assesing antiapoptotic and antioxidant effects. Archives of Clinical and Experimental Medicine, 3(3): 179-185.
44. Tunçdemir, M. & Ozturk, M. 2008. The effects of ACE inhibitor and angiotensin receptor blocker on clusterin and apoptosis in the kidney tissue of streptozotocin-diabetic rats. Journal of Molecular Histology, 39(6): 605-616.
45. Vessal, M., Hemmati, M. & Vasei, M. 2003. Antidiabetic effects of quercetin in streptozocin-induced diabetic rats. Comparative Biochemistry and Physiology, 135C(3): 357-364.
46. Vincent, A.M., Russell, J.W., Low, P. Feldman, E.L. 2004. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocrine Reviews, 25(4): 612-628.
47. Vural, H., Sabuncu, T., Arslan, S.O. & Aksoy, N. 2001. Melatonin inhibits lipid peroxidation and stimulates the antioxidant status of diabetic rats. Journal of Pineal Research, 31(3): 193-198.
48. Wang, R.M., Wang, Z.B., Wang, Y., Liu, W.Y., Li, Y. & Tong, L.C. 2018. Swiprosin-1 promotes mitochondria-dependent apoptosis of glomerular podocytes via P38 MAPK pathway in early-stage diabetic nephropathy. Cellular Physiology and Biochemistry, 45(3): 899-916.
49. Yang, D.K. & Kang, H.S. 2018. Anti-diabetic effect of cotreatment with quercetin and resveratrol in streptozotocin-ınduced diabetic rats. Biomolecules & Therapeutics (Seoul), 26(2): 130-138.
50. Yasuda, Y., Nakamura, J., Hamada, Y., Nakayama, M., Naruse, K., Nakashima, E., Kato, K., Kamiya, H. & Hotta, N. 2001. Role of PKC and TGF-beta receptor in glucose-induced proliferation of smooth muscle cells. Biochemical and Biophysical Research Communications, 281: 71-77.
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52. Ziyadeh, F.N. & Goldfarb, S. 1991. The renal tubulointerstitium in diabetes mellitus. Kidney Internationa, 39: 464-475.

Year 2021, Volume: 22 Issue: 2, 131 - 138, 15.10.2021

Emine Sözüer Yeter Topçu

Abstract

Diabetes mellitus, sıklığı ve komplikasyonları nedeniyle dünya çapında önemli bir sağlık sorunudur. Bu çalışmada, streptozotosin (STZ) ile oluşturulan diyabetin erken evrelerinde böbrek dokusunda meydana gelen apoptotik değişiklikler üzerine quercetinin koruyucu etkileri değerlendirildi.
Deneklerden kontrol, diyabetik ve diyabetik + quercetin grupları olarak 3 grup oluşturuldu. Diyabetik ve diyabetik+quercetin gruplarına tek doz 50 mg/kg STZ intraperitoneal (i.p.) olarak uygulandı. Quercetin, diyabet indüksiyonundan 48 saat sonra 15 gün boyunca günde bir kez 30 mg/kg i.p. olarak verildi.
Quercetin tedavisinin sonunda tüm hayvanlar sakrifiye edildi ve böbrekler çıkartılarak, tartıldı. Böbrek dokularında TUNEL (Terminal deoxynucleotidyl transferase-mediated dUTP nick end-labeling) yöntemi ile hücre apoptozu ve ayrıca histopatolojik değişiklikler değerlendirildi.
STZ yoluyla diyabet indüksiyonu, kan glukoz seviyelerinde, glomerüloskleroz indeksinde, histopatolojik skorda, TUNEL pozitif tübüler ve glomerüler hücre sayısında önemli bir artışa neden oldu. Quercetin tedavisi kan glukoz seviyelerini düşürdü, renal hücre apoptozunu ve histopatolojik değişiklikleri azalttı.
Bu çalışmanın bulguları, quercetinin, diyabetin erken evrelerinde meydana gelen böbrekteki apoptotik değişiklikleri düzenleyerek diyabetik nefropati gelişimini önlemede faydalı olabileceğini göstermektedir.

Project Number

2017/15

References

1. Al-Rasheed, N.M., Fadda, L.M., Attia, H.A., Ali, H.M. & Al-Rasheed, N.M. 2017. Quercetin inhibits sodium nitrite-induced inflammation and apoptosis in different rats organs by suppressing Bax, HIF1-α, TGF-β, Smad-2, and AKT pathways. Journal of Biochemical and Molecular Toxicology, 31(5): e21883.
2. Ali, M.A.M., Heeba, G.H. & El-Sheikh, A.A.K. 2017. Modulation of heme oxygenase-1 expression and activity affects streptozotocin-induced diabetic nephropathy in rats. Fundamental & Clinical Pharmacology, 31(5): 546-557.
3. Allen, D.A., Harwood, S., Varagunam, M., Raftery, M.J. & Yaqoob, M.M. 2003. High glucose-induced oxidative stress causes apoptosis in proximal tubular epithelial cells and is mediated by multiple caspases. Federation of American Societies for Experimental Biolog, 17(8): 908-910.
4. American Diabetes Association: Diagnosis and classification of diabetes mellitus. Diabetes Care. http://care.diabetesjournals.org/content/33/Supplement_1/S62. (2010, accessed 15 May 2019)
5. Andallu, B. & Varadacharyulu, N.C. 2003. Antioxidant role of mulberry (Morus indica L. cv. Anantha) leaves in streptozotocin-diabetic rats. Clinica Chimica Acta, 338: 3-10.
6. Anjaneyulu, M. & Chopra, K. 2004. Quercetin, an antioxidan bioflavonoid, attenuates diabetic nephropathy in rats. Clinical and Experimental Pharmacology and Physiology, 31(4): 244-248.
7. Armagan, A., Uz, E., Yilmaz, H.R., Soyupek, S., Oksay, T. & Ozcelik, N. 2006. Effects of melatonin on lipid peroxidation and antioxidant enzymes in streptozotocin-induced diabetic rat testis. Asian Journal of Andrology, 8(5): 595-600.
8. Bamri-Ezzine, S., Ao, Z.J., Londono, I. Gingras, D. & Bendayan, M. 2003. Apoptosis of tubular epithelial cells in glycogen nephrosis during diabetes. Laboratory Investigation, 83: 1069-1080.
9. Bhathena, S.J. & Velasquez, M.T. 2002. Beneficial role of dietary phytoestrogens in obesity and diabetes. American Journal of Clinical Nutrition, 76(6): 1191-1201.
10. Bleyer, A.J., Fumo, P., Snipes, E.R., Goldfarb, S., Simmons, D.A. & Ziyadeh, F.N. 1994. Polyol pathway mediates high glucose-induced collagen synthesis in proximal tubule. Kidney International, 45(3): 659-666.
11. Cheisson, G., Jacqueminet, S., Cosson, E., Ichai, C., Leguerrier, A.M., Nicolescu-Catargi, B., Quattara, A., Valensi, P. & Benhamou, D. 2018. Review of hyperglycaemia: definitions and pathophysiology. Anaesthesia, Critical Care & Pain, 37: S5-S8.
12. Chen, S., Hong, S.W., Iglesias-dela Cruz, M.C., Isono, M., Casaretto, A. & Ziyadeh, F.N. 2001. The key role of the transforming growth factor-beta system in the pathogenesis of diabetic nephropathy. Renal Failure, 3(3&4): 471-481.
13. Chuang, P.Y., Yu, Q., Fang, W., Uribarri, J. & He, J.C. 2007. Advanced glycation endproducts induce podocyte apoptosis by activation of the FOXO4 transcription factor. Kidney International, 72: 965-976.
14. Coldiron, A.D., Sanders, R.A. & Watkins, J.B. 2002. Effects of combined quercetin and coenzyme Q10 treatment on oxidative stress in normal and diabetic rats. Journal of Biochemical and Molecular Toxicology, 16: 197-202.
15. Elbe, H., Vardi, N., Esrefoglu, M., Ates, B., Yologlu, S. & Taskapan, C. 2015. Amelioration of streptozotocin-induced diabetic nephropathy by melatonin, quercetin, and resveratrol in rats. Human and Experimental Toxicology. 34(1): 100-113.
16. Geoffroy, K., Troncy, L., Wiernsperger, N., Lagarde, M. & Bawab, S.E 2005. Glomerular proliferation during early stages of diabetic nephropathy is associated with local increase of sphingosine-1-phosphate levels. Federation of European Biochemical Societies, 579: 1249-1254.
17. Gilbert, R.E. & Cooper, M.E. 1999. The tubulointerstitium in progressive diabetic kidney disease: more than an aftermath of glomerular injury? Kidney International, 56: 1627-1637.
18. Giribabu, N., Karim, K., Kilari, E.K. & Salleh, N. 2017. Phyllanthus niruri leaves aqueous extract improves kidney functions, ameliorates kidney oxidative stress, inflammation, fibrosis and apoptosis and enhances kidney cell proliferation in adult male rats with diabetes mellitus. Journal of Ethnopharmacol, 205: 123-137.
19. Gomes, I.B., Porto, M.L., Santos, M.C., Campagnaro, B.P., Pereira T.MC., Meyrelles S.S. & Vasquez, E.C. 2014. Renoprotective, anti-oxidative and anti-apoptotic effects of oral low-dose quercetin in the C57BL/6J model of diabetic nephropathy. Lipids in Health and Disease, 13: 184.
20. Harwood, M., Danielewska-Nikiel, B., Borzelleca, J.F., Flaam, G.W., Williams, G.M. & Lines, T.C. 2007. A critical review of the data related to the safety of quercetin and lack of evidence of in vivo toxicity, including lack of genotoxic/carcinogenic properties. Food Chemical Toxicology, 45(11): 2179-2205.
21. Ichinose, K., Kawasaki, E. & Eguchi, K. 2007. Recent advancement of understanding pathogenesis of type 1 diabetes and potential relevance to diabetic nephropathy. American Journal of Nephrology, 27: 554-564.
22. Ji, L., Wang, Q., Huang, F., An, T., Guo, F., Zhao, Y., Liu, Y., He, Y., Song,Yi. & Qin, G. 2019. FOXO1 Overexpression attenuates tubulointerstitial fibrosis and apoptosis in diabetic kidneys by ameliorating oxidative injury via TXNIP-TRX. Hindawi Oxidative Medicine and Cellular Longevit,. https://doi.org/10.1155/219/3286928
23. Kaur, N., Kishore, L. & Singh, R. 2017. Dillenia indica L. attenuates diabetic nephropathy via inhibition of advanced glycation end products accumulation in STZ-nicotinamide induced diabetic rats. Journal of Traditional and Complementary Medicine, 8(1): 226-38.
24. Kelly, D.J., Cox, A.J., Tolcos, M., Cooper, M.E., Wilkinson-Berka, J.L. & Gilbert, R.E. 2002. Attenuation of tubular apoptosis by blockade of the renin-angiotensin system in diabetic Ren-2 rats. Kidney International, 61(1): 31-39.
25. Kolset, S.O., Reinholt, F.P. & Jenssen T. 2012. Diabetic nephropathy and extracellular matrix. Journal of Histochemistry and Cytochemistry, 60(12): 976-986.
26. Kushwaha, S. & Jena, G.B. 2012. Enalapril reduces germ cell toxicity in streptozotocin-induced diabetic rat: investigation on possible mechanisms. Naunyn-Schmiedeberg's Archives of Pharmacology, 385: 111-124.
27. Li, J.H., Huang, X.R., Zhu, H., Johnson, R. & Lan, H.Y. 2003. Role of TGF B signaling in extracellular matrix production under high glucose conditions. Kidney International, 63(6): 2010-2019.
28. Li, X., Zheng, T., Sang, S. & Lv, L. 2014. Quercetin ınhibits advanced glycation end product formation by trapping methylglyoxal and glyoxal. Journal of Agricultural and Food Chemistry, 62(50): 12152-12158.
29. Lin, C.F., Kuo, Y.T., Chen, T.Y. & Chien, C.T. 2016. Quercetin-Rich Guava (Psidium guajava) juice in combination with trehalose reduces autophagy, apoptosis and pyroptosis formation in the kidney and pancreas of type ıı diabetic rats. Molecule, 21(3): 334.
30. Liu, B.C., Chen, Q., Luo, D.D. 2003. Mechanisms of irbesartan in prevention of renal lesion in streptozotocin-induced diabetic rats. Acta Pharmacologica Sinica, 24(1): 67-73.
31. Mori, J., Patel, V.B., Ramprasath, T., Alrob, O.A., DesAulniers, J., Scholey, J.W., Lopaschuk, G.D. & Qudit, G.Y. 2014. Angiotensin 1-7 mediates renoprotection against diabetic nephropathy by reducing oxidative stress, inflammation, and lipotoxicity. American Journal of Physiology-Renal Physiology, 306(8): F812-F821.
32. Nessar, A. 2005. Advanced glycation endproducts-role in pathology of diabetic complications. Diabetes Research and Clinical Practice, 67(1): 3-21.
33. New, J.P., Canavan, J.P., Flyvbjerg, A., Hamon, G. Bilous, R.W. & Marshall, S.M. 1996. Renal enlargement and insulin-like growth factor-1 accumulation in the wistar rat model of experimental diabetes is not prevented by angiotensin converting enzyme inhibition. Diabetologia, 39(2): 166-171.
34. Offor, U., Naidu, E.C., Ogedengbe, O.O., Jegede, A.I., Peter, A.I. & Azu, O.O. 2019. Renal histopathological and biochemical changes following adjuvant intervention of Momordica charantia and antiretroviral therapy in diabetic rats. Iranian Journal of Basic Medical Science, 22(11): 1359-1367.
35. Ortiz, A., Ziyadeh, F.N. & Neilson, E.G. 1997. Expression of apoptosisregulatory genes in renal proximal tubular epithelial cells exposed to high ambient glucose and in diabetic kidneys. Journal of Investigative Medicine, 45(2): 50-56.
36. Roslan, J., Giribabu, N., Karim, K. & Salleh, N. 2017. Quercetin ameliorates oxidative stress, inflammation and apoptosis in the heart of streptozotocin-nicotinamide-induced adult male diabetic rats. Biomed Pharmacother, 86: 570-582.
37. Saito, T., Sumithran, E., Glasgow, E.F. & Atkins, R.C. 1987. The enhancement of aminonucleoside nephrosis by the co-administration of protamine. Kidney International, 32(5): 691-699.
38. Sanai, T., Sobka, T., Johnson, T., El-Essawy, M., Muchaneta-Kubara, E.C., Gharbia, O.B., Oldroyd, S. & El Nahas, A.M. 2000. Expression of cytoskeletal proteins during the course of experimental diabetic nephropathy. Diabetologia, 43(1): 91-100.
39. Senyigit, A., Durmus, S., Mirzatas, E.B., Ozsobacı, N.P., Gelisgen, R., Tuncdemir, M., Ozcelik, D., Simsek, G. & Uzun, H. 2019. Effects of quercetin on lipid and protein damage in the liver of streptozotocin-induced experimental diabetic rats. Journal of Medicinal Food, 22(1): 52-56.
40. Susztak, K., Raff, A.C., Schiffer, M. & Böttinger, E.P. 2006. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes, 55(1): 225-233.
41. Tan, A.L., Forbes, J.M. & Cooper, M.E. 2007. AGE, RAGE, and ROS in diabetic nephropathy. Seminars in Nephrology, 27(2): 130-143.
42. Tucker, B.J., Collins, R.C., Ziegler, M.G. & Blantz, R.C. 1991. Disassociation between glomerular hyperfiltration and extracellular volume in diabetic rats. Kidney International. 39: 1176-1183.
43. Tunçdemir, M., Mirzataş, E.B. & Uzun, H. 2018. Renoprotective potential of quercetin in experimental diabetic nephropathy: assesing antiapoptotic and antioxidant effects. Archives of Clinical and Experimental Medicine, 3(3): 179-185.
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There are 52 citations in total.

Details

Primary Language	English
Subjects	Structural Biology
Journal Section	Research Article/Araştırma Makalesi
Authors	Emine Sözüer This is me 0000-0003-0352-7361 Yeter Topçu 0000-0002-1851-7839
Project Number	2017/15
Publication Date	October 15, 2021
Submission Date	February 12, 2021
Acceptance Date	May 11, 2021
Published in Issue	Year 2021 Volume: 22 Issue: 2

Cite

APA	Sözüer, E., & Topçu, Y. (2021). QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS. Trakya University Journal of Natural Sciences, 22(2), 131-138.
AMA	Sözüer E, Topçu Y. QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS. Trakya Univ J Nat Sci. October 2021;22(2):131-138.
Chicago	Sözüer, Emine, and Yeter Topçu. “QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS”. Trakya University Journal of Natural Sciences 22, no. 2 (October 2021): 131-38.
EndNote	Sözüer E, Topçu Y (October 1, 2021) QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS. Trakya University Journal of Natural Sciences 22 2 131–138.
IEEE	E. Sözüer and Y. Topçu, “QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS”, Trakya Univ J Nat Sci, vol. 22, no. 2, pp. 131–138, 2021.
ISNAD	Sözüer, Emine - Topçu, Yeter. “QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS”. Trakya University Journal of Natural Sciences 22/2 (October 2021), 131-138.
JAMA	Sözüer E, Topçu Y. QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS. Trakya Univ J Nat Sci. 2021;22:131–138.
MLA	Sözüer, Emine and Yeter Topçu. “QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS”. Trakya University Journal of Natural Sciences, vol. 22, no. 2, 2021, pp. 131-8.
Vancouver	Sözüer E, Topçu Y. QUERCETIN AMELIORATES THE STREPTOZOTOCIN-INDUCED DIABETIC RENAL INJURY BY INHIBITING APOPTOSIS. Trakya Univ J Nat Sci. 2021;22(2):131-8.

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