Effects of Apocynin against Monosodium Glutamate-Induced Oxidative Damage in Rat Kidney
Year 2022,
Volume: 81 Issue: 2, 231 - 239, 29.12.2022
Merve Açıkel Elmas
,
Gökçen Özgün
,
Özlem Bingöl Özakpınar
,
Zozan Güleken
,
Serap Arbak
Abstract
Objective: Monosodium glutamate causes oxidative stress that affects a variety of organ systems, along with the kidney. The aim of this study was to evaluate the protective role of apocynin in kidney degeneration caused by monosodium glutamate using biochemical and histological methods. Materials and Methods: Sprague-Dawley rats (n=32) were used for this study. Four experimental groups were randomly formed: the Control (Cont), Apocynin (APO), Monosodium Glutamate (MSG), and MSG+APO groups. The MSG group received oral administration of MSG (120 mg/kg) for 28 days. The MSG+APO and APO groups received apocynin (25 mg/kg) during the last 5 days of the experiment. Kidney tissue was processed for biochemical and microscopic analyses. Biochemical methods were used to examine the levels of malondialdehyde (MDA) and glutathione (GSH) in the tissue and the activities of myeloperoxidase (MPO) and superoxide dismutase (SOD). Light and electron microscopy were also used to examine for histological changes in kidney tissue. Results: The MSG group was compared with the Cont and APO groups; it was found that MDA and MPO levels were elevated, whereas GSH and SOD activity were decreased. In contrast to the Cont and APO groups, the MSG+APO group showed higher GSH levels, lower MPO activities and increased MDA levels. While apocynin treatment improved renal tissue histology, MSGinduction led to deterioration of renal morphology. Conclusion: The study revealed that MSG increased oxidative damage and renal tissue degeneration. Moreover, apocynin reduced renal damage by modulating the ratio of antioxidants to oxidants.
Thanks
The authors would like to thank Dr. Selcuk Birdogan for his assistance with electron microscopic imaging.
References
- 1. Diniz YS, Fernandes AA, Campos KE, Mani F, Ribas BO, Novelli EL. Toxicity of hypercaloric diet and monosodium glutamate: oxidative stress and metabolic shifting in hepatic tissue. Food Chem Tox 2004; 42(2): 313-19. google scholar
- 2. Farombi EO, Onyema OO. Monosodium glutamate-induced oxidative damage and genotoxicity in the rat: modulatory role of vitamin C, vitamin E and quercetin. Hum Exp Toxicol
2006; 25(5): 251-9. google scholar
- 3. Sharma A, Prasongwattana V, Cha’on U, Selmi C, Hipkaeo W, Boon-nate P, Pethlert S, Titipungul T, Intarawichian P, Waraasawapati S, Puapiroj A, Sitprija V, Reungjui S. Monosodium
glutamate (MSG) consumption is associated with urolithiasis and urinary tract obstruction in rats. PloS One 2013; 8(9): e75546. google scholar
- 4. Sharma A, Wongkham C, Prasongwattana V, Boonnate P, Thanan R, Reungjui S, Cha’on U. Proteomic analysis of kidney in rats chronically exposed to monosodium glutamate. PloS
One 2014; 9(12): e116233. google scholar
- 5. Bashan N, Kovsan J, Kachko I, Ovadia H, Rudich A. Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol Rev 2009; 89(1): 27-71.
google scholar
- 6. Stankiewicz A, Skrzydlewska E, Makiela M. Effects of amifostine on liver oxidative stress caused by cyclophosphamide administration to rats. Drug Metabol Drug Interact 2002;
19(2): 67-82. google scholar
- 7. Simons JM, Hart BA, Ip Vai Ching TR, Van Dijk H, Labadie RP. Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils. Free
Radic Biol & Med 1990; 8(3): 251-8. google scholar
- 8. Liu PG, He SQ, Zhang YH, Wu J. Protective effects of apocynin and allopurinol on ischemia/reperfusion-induced liver injury in mice. World J Gastroenterol 2008; 14(18): 2832-7.
google scholar
- 9. Tan YC, Abdul Sattar M, Ahmeda AF, Abdul Karim Khan N, Murugai-yah V, Ahmad A, Hassan Z, Kaur G. Apocynin and catalase prevent hypertension and kidney injury in
Cyclosporine A-induced nephrotoxicity in rats. PloS One 2020; 15(4): e0231472. google scholar
- 10. Bao Q, Hughes RC. Galectin-3 expression and effects on cyst enlargement and tubulogenesis in kidney epithelial MDCK cells cultured in three-dimensional matrices in vitro. J Cell
Sci 1995; 108 (Pt 8): 2791-800. google scholar
- 11. Chen SC, Kuo PL. The Role of Galectin-3 in the Kidneys. Int J Mol Sci 2016; 17(4): 565. google scholar
- 12. Nishiyama J, Kobayashi S, Ishida A, Nakabayashi I, Tajima O, Miura S, Katayama M, Nogami H. Up-regulation of galectin-3 in acute renal failure of the rat. Am J Pathol 2000; 157(3):
815-23. google scholar
- 13. Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med 1963;61:882-8. google scholar
- 14. Abd-Elkareem M, Soliman M, Abd El-Rahman MAM, Abou Khalil NS. Effect of Nigella sativa L. Seed on the Kidney of Monosodium Glutamate Challenged Rats. Front Pharmacol
2022; 13: 789988. google scholar
- 15. Omurtag GZ, Güranlioglu FD, Sehirli O, Arbak S, Uslu B, Gedik N, Sener G. Protective effect of aqueous garlic extract against naphthalene-induced oxidative stress in mice. Journal
Pharm Pharmacol 2005; 57(5): 623-30. google scholar
- 16. Besler C, Lang D, Urban D, Rommel KP, von Roeder M, Fengler K, Blazek S, Kandolf R, Klingel K, Thiele H, Linke A, Schuler G, Adams V, Lurz P. Plasma and Cardiac Galectin-3 in Patients
With Heart Failure Reflects Both Inflammation and Fibrosis: Implications for Its Use as a Biomarker. Circ Heart Fail 2017; 10(3). google scholar
- 17. Acikel Elmas M, Cakici SE, Dur IR, Kozluca I, Arinc M, Binbuga B, Bingol Ozakpinar O, Kolgazi M, Sener G, Ercan F. Protective effects of exercise on heart and aorta in high-fat diet-
induced obese rats. Tissue Cell 2019; 57: 57-65. google scholar
- 18. Van der Veen BS, de Winther MP, Heeringa P. Myeloperoxidase: molecular mechanisms of action and their relevance to human health and disease. Antioxidants & Redox Signaling 2009; 11(11): 2899937. google scholar
- 19. Kisic B, Miric D, Dragojevic I, Rasic J, Popovic L. Role of Myeloperoxidase in Patients with Chronic Kidney Disease. Oxidative Medicine and Cellular Longevity 2016; 1069743. google
scholar
- 20. Stefanska J, Pawliczak R. Apocynin: molecular aptitudes. Mediators Inflamm 2008; 106507. google scholar
- 21. Ortiz GG, Bitzer-Quintero OK, Zárate CB, Rodríguez-Reynoso S, Lari-os-Arceo F, Velázquez-Brizuela IE, Pacheco-Moisés F, Rosales-Corral SA. Monosodium glutamate-induced
damage in liver and kidney: a morphological and biochemical approach. Biomed Pharmacoth-er 2006; 60(2): 86-91. google scholar
- 22. Pfaller W, Gstraunthaler G, Willinger CC. Morphology of renal tubular damage from nephrotoxins. Toxicol Lett 1990; 53(1-2): 39-43. google scholar
- 23. Paul MV, Abhilash M, Varghese MV, Alex M, Nair RH. Protective effects ofa-tocopherol against oxidative stress related to nephrotoxicity by monosodium glutamate in rats.
Toxicology Mech Methods 2012; 22(8): 625-30. google scholar
- 24. Ozaki M, Yamada Y, Matoba K, Otani H, Mune M, Yukawa S, Sakamoto W. Phospholipase A2 activity in ox-LDL-stimulated mesangial cells and modulation by alpha-tocopherol.
Kidney Int Suppl 1999; 71: S171-3. google scholar
- 25. Bowie AG, O’Neill LA. Vitamin C inhibits NF-kappa B activation by TNF via the activation of p38 mitogen-activated protein kinase. J Immunol 2000; 165(12): 7180-8. google scholar
- 26. Sharma A. Monosodium glutamate-induced oxidative kidney damage and possible mechanisms: a mini-review. J Biomed Sci 2015; 22(1): 93. google scholar
- 27. Afeefy A, Mahmoud M, Arafa M. Effect of Honey on Monosodium Glutamate Induced Nephrotoxicity (Histological and Electron Microscopic Studies). J Am Sci 2012; 8: 146-56.
google scholar
- 28. El-Mawla AMAA, Osman HEH. HPLC analysis and role of the Saudi Arabian propolis in improving the pathological changes of kidney treated with monosodium glutamate. Spatula
DD 2011; 1: 119-27. google scholar
- 29. Sinha N, Dabla PK. Oxidative stress and antioxidants in hyperten-sion-a current review. Curr Hypertens Rev 2015; 11(2): 132-42. google scholar
30. Deng W, Abliz A, Xu S, Sun R, Guo W, Shi Q, Yu J, Wang W. Severity of pancreatitis-associated intestinal mucosal barrier injury is reduced following treatment with the NADPH
oxidase inhibitor apocynin. Molecular Med Rep 2016; 14(4): 3525-34. google scholar
- 31. Impellizzeri D, Esposito E, Mazzon E, Paterniti I, Di Paola R, Bramanti P, Cuzzocrea S. Effect of apocynin, a NADPH oxidase inhibitor, on acute lung inflammation. Biochem Pharmacol
2011; 81(5): 636-48. google scholar
- 32. Ciarcia R, Damiano S, Florio A, Spagnuolo M, Zacchia E, Squillacioti C, Mirabella N, Florio S, Pagnini U, Garofano T, Polito MS, Capasso G, Giordano A. The Protective Effect of
Apocynin on Cyclosporine A-Induced Hypertension and Nephrotoxicity in Rats. J Cell Bio-chem 2015; 116(9): 1848-56. google scholar
- 33. Iacobini C, Menini S, Oddi G, Ricci C, Amadio L, Pricci F, Olivieri A, Sorcini M, Di Mario U, Pesce C, Pugliese G. Galectin-3/AGE-receptor 3 knockout mice show accelerated AGE-
induced glomerular injury: evidence for a protective role of galectin-3 as an AGE receptor. FASEB J 2004; 18(14): 1773-5. google scholar
- 34. Henderson NC, Mackinnon AC, Farnworth SL, Kipari T, Haslett C, Iredale JP, Liu FT, Hughes J, Sethi T. Galectin-3 expression and secretion links macrophages to the promotion of
renal fibrosis. Am J Pathol 2008; 172(2): 288-98. google scholar
Year 2022,
Volume: 81 Issue: 2, 231 - 239, 29.12.2022
Merve Açıkel Elmas
,
Gökçen Özgün
,
Özlem Bingöl Özakpınar
,
Zozan Güleken
,
Serap Arbak
References
- 1. Diniz YS, Fernandes AA, Campos KE, Mani F, Ribas BO, Novelli EL. Toxicity of hypercaloric diet and monosodium glutamate: oxidative stress and metabolic shifting in hepatic tissue. Food Chem Tox 2004; 42(2): 313-19. google scholar
- 2. Farombi EO, Onyema OO. Monosodium glutamate-induced oxidative damage and genotoxicity in the rat: modulatory role of vitamin C, vitamin E and quercetin. Hum Exp Toxicol
2006; 25(5): 251-9. google scholar
- 3. Sharma A, Prasongwattana V, Cha’on U, Selmi C, Hipkaeo W, Boon-nate P, Pethlert S, Titipungul T, Intarawichian P, Waraasawapati S, Puapiroj A, Sitprija V, Reungjui S. Monosodium
glutamate (MSG) consumption is associated with urolithiasis and urinary tract obstruction in rats. PloS One 2013; 8(9): e75546. google scholar
- 4. Sharma A, Wongkham C, Prasongwattana V, Boonnate P, Thanan R, Reungjui S, Cha’on U. Proteomic analysis of kidney in rats chronically exposed to monosodium glutamate. PloS
One 2014; 9(12): e116233. google scholar
- 5. Bashan N, Kovsan J, Kachko I, Ovadia H, Rudich A. Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol Rev 2009; 89(1): 27-71.
google scholar
- 6. Stankiewicz A, Skrzydlewska E, Makiela M. Effects of amifostine on liver oxidative stress caused by cyclophosphamide administration to rats. Drug Metabol Drug Interact 2002;
19(2): 67-82. google scholar
- 7. Simons JM, Hart BA, Ip Vai Ching TR, Van Dijk H, Labadie RP. Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils. Free
Radic Biol & Med 1990; 8(3): 251-8. google scholar
- 8. Liu PG, He SQ, Zhang YH, Wu J. Protective effects of apocynin and allopurinol on ischemia/reperfusion-induced liver injury in mice. World J Gastroenterol 2008; 14(18): 2832-7.
google scholar
- 9. Tan YC, Abdul Sattar M, Ahmeda AF, Abdul Karim Khan N, Murugai-yah V, Ahmad A, Hassan Z, Kaur G. Apocynin and catalase prevent hypertension and kidney injury in
Cyclosporine A-induced nephrotoxicity in rats. PloS One 2020; 15(4): e0231472. google scholar
- 10. Bao Q, Hughes RC. Galectin-3 expression and effects on cyst enlargement and tubulogenesis in kidney epithelial MDCK cells cultured in three-dimensional matrices in vitro. J Cell
Sci 1995; 108 (Pt 8): 2791-800. google scholar
- 11. Chen SC, Kuo PL. The Role of Galectin-3 in the Kidneys. Int J Mol Sci 2016; 17(4): 565. google scholar
- 12. Nishiyama J, Kobayashi S, Ishida A, Nakabayashi I, Tajima O, Miura S, Katayama M, Nogami H. Up-regulation of galectin-3 in acute renal failure of the rat. Am J Pathol 2000; 157(3):
815-23. google scholar
- 13. Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med 1963;61:882-8. google scholar
- 14. Abd-Elkareem M, Soliman M, Abd El-Rahman MAM, Abou Khalil NS. Effect of Nigella sativa L. Seed on the Kidney of Monosodium Glutamate Challenged Rats. Front Pharmacol
2022; 13: 789988. google scholar
- 15. Omurtag GZ, Güranlioglu FD, Sehirli O, Arbak S, Uslu B, Gedik N, Sener G. Protective effect of aqueous garlic extract against naphthalene-induced oxidative stress in mice. Journal
Pharm Pharmacol 2005; 57(5): 623-30. google scholar
- 16. Besler C, Lang D, Urban D, Rommel KP, von Roeder M, Fengler K, Blazek S, Kandolf R, Klingel K, Thiele H, Linke A, Schuler G, Adams V, Lurz P. Plasma and Cardiac Galectin-3 in Patients
With Heart Failure Reflects Both Inflammation and Fibrosis: Implications for Its Use as a Biomarker. Circ Heart Fail 2017; 10(3). google scholar
- 17. Acikel Elmas M, Cakici SE, Dur IR, Kozluca I, Arinc M, Binbuga B, Bingol Ozakpinar O, Kolgazi M, Sener G, Ercan F. Protective effects of exercise on heart and aorta in high-fat diet-
induced obese rats. Tissue Cell 2019; 57: 57-65. google scholar
- 18. Van der Veen BS, de Winther MP, Heeringa P. Myeloperoxidase: molecular mechanisms of action and their relevance to human health and disease. Antioxidants & Redox Signaling 2009; 11(11): 2899937. google scholar
- 19. Kisic B, Miric D, Dragojevic I, Rasic J, Popovic L. Role of Myeloperoxidase in Patients with Chronic Kidney Disease. Oxidative Medicine and Cellular Longevity 2016; 1069743. google
scholar
- 20. Stefanska J, Pawliczak R. Apocynin: molecular aptitudes. Mediators Inflamm 2008; 106507. google scholar
- 21. Ortiz GG, Bitzer-Quintero OK, Zárate CB, Rodríguez-Reynoso S, Lari-os-Arceo F, Velázquez-Brizuela IE, Pacheco-Moisés F, Rosales-Corral SA. Monosodium glutamate-induced
damage in liver and kidney: a morphological and biochemical approach. Biomed Pharmacoth-er 2006; 60(2): 86-91. google scholar
- 22. Pfaller W, Gstraunthaler G, Willinger CC. Morphology of renal tubular damage from nephrotoxins. Toxicol Lett 1990; 53(1-2): 39-43. google scholar
- 23. Paul MV, Abhilash M, Varghese MV, Alex M, Nair RH. Protective effects ofa-tocopherol against oxidative stress related to nephrotoxicity by monosodium glutamate in rats.
Toxicology Mech Methods 2012; 22(8): 625-30. google scholar
- 24. Ozaki M, Yamada Y, Matoba K, Otani H, Mune M, Yukawa S, Sakamoto W. Phospholipase A2 activity in ox-LDL-stimulated mesangial cells and modulation by alpha-tocopherol.
Kidney Int Suppl 1999; 71: S171-3. google scholar
- 25. Bowie AG, O’Neill LA. Vitamin C inhibits NF-kappa B activation by TNF via the activation of p38 mitogen-activated protein kinase. J Immunol 2000; 165(12): 7180-8. google scholar
- 26. Sharma A. Monosodium glutamate-induced oxidative kidney damage and possible mechanisms: a mini-review. J Biomed Sci 2015; 22(1): 93. google scholar
- 27. Afeefy A, Mahmoud M, Arafa M. Effect of Honey on Monosodium Glutamate Induced Nephrotoxicity (Histological and Electron Microscopic Studies). J Am Sci 2012; 8: 146-56.
google scholar
- 28. El-Mawla AMAA, Osman HEH. HPLC analysis and role of the Saudi Arabian propolis in improving the pathological changes of kidney treated with monosodium glutamate. Spatula
DD 2011; 1: 119-27. google scholar
- 29. Sinha N, Dabla PK. Oxidative stress and antioxidants in hyperten-sion-a current review. Curr Hypertens Rev 2015; 11(2): 132-42. google scholar
30. Deng W, Abliz A, Xu S, Sun R, Guo W, Shi Q, Yu J, Wang W. Severity of pancreatitis-associated intestinal mucosal barrier injury is reduced following treatment with the NADPH
oxidase inhibitor apocynin. Molecular Med Rep 2016; 14(4): 3525-34. google scholar
- 31. Impellizzeri D, Esposito E, Mazzon E, Paterniti I, Di Paola R, Bramanti P, Cuzzocrea S. Effect of apocynin, a NADPH oxidase inhibitor, on acute lung inflammation. Biochem Pharmacol
2011; 81(5): 636-48. google scholar
- 32. Ciarcia R, Damiano S, Florio A, Spagnuolo M, Zacchia E, Squillacioti C, Mirabella N, Florio S, Pagnini U, Garofano T, Polito MS, Capasso G, Giordano A. The Protective Effect of
Apocynin on Cyclosporine A-Induced Hypertension and Nephrotoxicity in Rats. J Cell Bio-chem 2015; 116(9): 1848-56. google scholar
- 33. Iacobini C, Menini S, Oddi G, Ricci C, Amadio L, Pricci F, Olivieri A, Sorcini M, Di Mario U, Pesce C, Pugliese G. Galectin-3/AGE-receptor 3 knockout mice show accelerated AGE-
induced glomerular injury: evidence for a protective role of galectin-3 as an AGE receptor. FASEB J 2004; 18(14): 1773-5. google scholar
- 34. Henderson NC, Mackinnon AC, Farnworth SL, Kipari T, Haslett C, Iredale JP, Liu FT, Hughes J, Sethi T. Galectin-3 expression and secretion links macrophages to the promotion of
renal fibrosis. Am J Pathol 2008; 172(2): 288-98. google scholar