Online first
Original article
Published online: 2024-06-03
Multifaceted Impacts of Monosodium Glutamate on Testicular Health: Insights into Pyroptosis and Therapeutic Potential of Resveratrol
DOI: 10.5603/fm.99434
Pubmed: 38842078
Abstract
Background: Monosodium glutamate was considered one of the food additive and flavor enhancer in processed meat and soup that affects testicular tissues, the aim of this research to investigates the impact of monosodium glutamate (MSG) on testicular structure in rats and explores the potential protective effects of resveratrol. Material and Methods: Four experimental groups involved in our study 10 rats of each.: the first group as control group; the second group (Resveratrol group: control rats received 20 mg/kg of resveratrol, via oral gavage); the third group (MSG group: rats received monosodium glutamate (MSG) with a dose 60 mg/kg body weight daily, via gastric tube, and the fourth group (MSG+ Resveratrol group). Serum level of testosterone, FSH, LH, were measured. Testicular tissues were prepared for measurement of oxidative stress markers, and gene expression of NLRP3, Caspase 3, and GSK-3β. Moreover, paraffin blocks contained testicular tissue used for histological and immunohistochemical examination. Additionally, seminal smear from epididymis were examined. Results: MSG administration adversely affected testosterone production, hormonal levels, and sperm parameters, Histological examination revealed marked testicular degeneration, and oxidative stress assessments indicated elevated level of MDA a lipid peroxidation marker and decrease in SOD, CAT antioxidant enzymes. Moreover, MSG-induced apoptotic and pyroptotic markers and its gene expressions. Importantly. Administration of resveratrol reversed the detrimental effects of MSG, demonstrating its corrective influence on the hypothalamic–pituitary–gonadal axis disruption, improvement of sperm parameters, attenuation of oxidative stress, anti-apoptotic activity, and anti-pyroptotic effects. The expression of Ki-67 as a cell proliferation marker further supported the positive response to spermatogenesis dysfunction upon resveratrol treatment. Conclusions: This comprehensive exploration sheds light on the protective effect of resveratrol against MSG-induced testicular with exploration of its mechanistic role.
Keywords: Testicular damageMonosodium GlutamateResveratrolPyroptosisOxidative stressApoptosis.
References
- Abdul-Hamid M, Galaly S, Ahmed R, et al. Histopathological and biochemical effect of quercetin on monosodium glutamate supplementation-induced testicular toxicity. Beni-Suef Univ J Basic Appl Sci. 2021; 10(1).
- Acikel-Elmas M, Algilani SA, Sahin B, et al. Apocynin ameliorates monosodium glutamate induced testis damage by impaired blood-testis barrier and oxidative stress parameters. Life (Basel). 2023; 13(3).
- Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Oxid Med Cell Longev. 2008; 1(1): 15–24.
- Alalwani A. Monosodium glutamate induced testicular lesions in rats (histological study). Middle East Fertil Soc J. 2014; 19(4): 274–280.
- Alderman T, Carpenter C, McGirr R. Animal research biosafety. Appl Biosaf. 2018; 23(3): 130–142.
- Alshehri FS. Resveratrol ameliorates vancomycin-induced testicular dysfunction in male rats. Medicina (Kaunas). 2023; 59(3).
- Aly HAA. Mitochondria-mediated apoptosis induced testicular dysfunction in diabetic rats: ameliorative effect of resveratrol. Endocrinology. 2021; 162(4).
- Baazm M, Babaei R, Fathi AN, et al. Resveratrol ameliorates spermatogenesis by increasing protamine 1, 2 and HSPA2 expression in experimental varicocele rat model. Rev Int Androl. 2023; 21(4): 100370.
- Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov. 2006; 5(6): 493–506.
- Bordbar H, Yahyavi SS, Noorafshan A, et al. Resveratrol ameliorates bisphenol A-induced testicular toxicity in adult male rats: a stereological and functional study. Basic Clin Androl. 2023; 33(1): 1.
- Bradamante S, Barenghi L, Villa A. Cardiovascular protective effects of resveratrol. Cardiovasc Drug Rev. 2004; 22(3): 169–188.
- Carter LG, D'Orazio JA, Pearson KJ. Resveratrol and cancer: focus on in vivo evidence. Endocr Relat Cancer. 2014; 21(3): R209–R225.
- Hageman JP. Handling, storage, treatment, and disposal of mixed wastes at medical facilities and academic institutions. Health Phys. 2002; 82(5 Suppl): S66–S76.
- Darbandi M, Darbandi S, Agarwal A, et al. Reactive oxygen species and male reproductive hormones. Reprod Biol Endocrinol. 2018; 16(1): 87.
- Darbandi S, Darbandi M. Lifestyle modifications on further reproductive problems. Cresco J Reprod Sci. 2016; 1(1): 1–2.
- de Oliveira FA, Costa WS, B Sampaio FJ, et al. Resveratrol attenuates metabolic, sperm, and testicular changes in adult Wistar rats fed a diet rich in lipids and simple carbohydrates. Asian J Androl. 2019; 21(2): 201–207.
- Doitsh G, Galloway NLK, Geng X, et al. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature. 2014; 505(7484): 509–514.
- Dominic S, Padmaja AV. Protective effect of an herbal extract in amlodipine induced testicular dysfunction in rats. Hygeia Infertility. 2017; 9(1): 22–42.
- Dyck GJB, Raj P, Zieroth S, et al. The effects of resveratrol in patients with cardiovascular disease and heart failure: a narrative review. Int J Mol Sci. 2019; 20(4).
- Sperm head abnormality and mutagenic effects of aspirin, paracetamol and caffeine containing analgesics in rats. Internet J Toxicol. 2009; 7(1).
- El-Gamal R, Abdelrahim M, El-Sherbiny M, et al. Gasdermin D: A potential mediator and prognostic marker of bladder cancer. Front Mol Biosci. 2022; 9: 972087.
- Fernandes GSa, Arena AC, Campos KE, et al. Glutamate-induced obesity leads to decreased sperm reserves and acceleration of transit time in the epididymis of adult male rats. Reprod Biol Endocrinol. 2012; 10: 105.
- Flores J, Noël A, Foveau B, et al. Caspase-1 inhibition alleviates cognitive impairment and neuropathology in an Alzheimer's disease mouse model. Nat Commun. 2018; 9(1): 3916.
- França LR, Suescun MO, Miranda JR, et al. Testis structure and function in a nongenetic hyperadipose rat model at prepubertal and adult ages. Endocrinology. 2006; 147(3): 1556–1563.
- Gülçin İ. Antioxidant properties of resveratrol: A structure–activity insight. Innov Food Sci Emerg Technol. 2010; 11(1): 210–218.
- Hamza RZ, Al-Harbi MS. Monosodium glutamate induced testicular toxicity and the possible ameliorative role of vitamin E or selenium in male rats. Toxicol Rep. 2014; 1: 1037–1045.
- Iamsaard S, Sukhorum W, Samrid R, et al. The sensitivity of male rat reproductive organs to monosodium glutamate. Acta Med Acad. 2014; 43(1): 3–9.
- Igwebuike UM, Ochiogu IS, Ihedinihu BC, et al. The effects of oral administration of monosodium glutamate (MSG) on the testicular morphology and cauda epididymal sperm reserves of young and adult male rats. Veterinarski Arhiv. 2011; 81(4): 525–534.
- Jang M, Cai L, Udeani GO, et al. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science. 1997; 275(5297): 218–220.
- Jeyaraman MM, Al-Yousif NSH, Singh Mann A, et al. Resveratrol for adults with type 2 diabetes mellitus. Cochrane Database Syst Rev. 2020; 1(1): CD011919.
- Juan ME, González-Pons E, Munuera T, et al. trans-Resveratrol, a natural antioxidant from grapes, increases sperm output in healthy rats. J Nutr. 2005; 135(4): 757–760.
- Jubaidi FF, Mathialagan RD, Noor MM, et al. Monosodium glutamate daily oral supplementation: study of its effects on male reproductive system on rat model. Syst Biol Reprod Med. 2019; 65(3): 194–204.
- Kalender Y, Yel M, Kalender S. Doxorubicin hepatotoxicity and hepatic free radical metabolism in rats. The effects of vitamin E and catechin. Toxicology. 2005; 209(1): 39–45.
- Kayode OT, Rotimi DE, Kayode AAA, et al. Monosodium glutamate (MSG)-induced male reproductive dysfunction: a mini review. Toxics. 2020; 8(1).
- Kianifard D, Shoar SM, Karkan MF, et al. Effects of monosodium glutamate on testicular structural and functional alterations induced by quinine therapy in rat: An experimental study. Int J Reprod Biomed. 2021; 19(2): 167–180.
- Konyalioglu S, Armagan G, Yalcin A, et al. Effects of resveratrol on hydrogen peroxide-induced oxidative stress in embryonic neural stem cells. Neural Regen Res. 2013; 8(6): 485–495.
- Marques FZ, Markus MA, Morris BJ. Resveratrol: cellular actions of a potent natural chemical that confers a diversity of health benefits. Int J Biochem Cell Biol. 2009; 41(11): 2125–2128.
- McCormick-Ell J, Connell N. Laboratory safety, biosecurity, and responsible animal use. ILAR J. 2019; 60(1): 24–33.
- Means JC, Gerdes BC, Koulen P. Distinct mechanisms underlying resveratrol-mediated protection from types of cellular stress in C6 glioma cells. Int J Mol Sci. 2017; 18(7).
- Najafi M, Cheki M, Amini P, et al. Evaluating the protective effect of resveratrol, Q10, and alpha-lipoic acid on radiation-induced mice spermatogenesis injury: A histopathological study. Int J Reprod Biomed. 2019; 17(12): 907–914.
- Ourique GM, Finamor IA, Saccol EMH, et al. Resveratrol improves sperm motility, prevents lipid peroxidation and enhances antioxidant defences in the testes of hyperthyroid rats. Reprod Toxicol. 2013; 37: 31–39.
- Pan S, Li S, Hu Y, et al. Resveratrol post-treatment protects against neonatal brain injury after hypoxia-ischemia. Oncotarget. 2016; 7(48): 79247–79261.
- Papuc C, Goran GV, Predescu CN, et al. Plant polyphenols as antioxidant and antibacterial agents for shelf-life extension of meat and meat products: classification, structures, sources, and action mechanisms. Compr Rev Food Sci Food Saf. 2017; 16(6): 1243–1268.
- Park E, Yu KH, Kim DoK, et al. Protective effects of N-acetylcysteine against monosodium glutamate-induced astrocytic cell death. Food Chem Toxicol. 2014; 67: 1–9.
- Peña-Blanco A, García-Sáez AJ. Bax, Bak and beyond - mitochondrial performance in apoptosis. FEBS J. 2018; 285(3): 416–431.
- Quiles JL, Huertas JR, Battino M, et al. Antioxidant nutrients and adriamycin toxicity. Toxicology. 2002; 180(1): 79–95.
- Rahimi Anbarkeh F, Baradaran R, Ghandy N, et al. Effects of monosodium glutamate on apoptosis of germ cells in testicular tissue of adult rat: An experimental study. Int J Reprod Biomed. 2019; 17(4): 261–270.
- Ren CP, Zhang YN, Wu YL, et al. [Effects of resveratrol on inhibiting pyroptosis of intestinal cancer cells]. Zhongguo Ying Yong Sheng Li Xue Za Zhi. 2022; 38(4): 326–331.
- Shaha C, Tripathi R, Mishra DP. Male germ cell apoptosis: regulation and biology. Philos Trans R Soc Lond B Biol Sci. 2010; 365(1546): 1501–1515.
- Sinha K, Chaudhary G, Gupta YK. Protective effect of resveratrol against oxidative stress in middle cerebral artery occlusion model of stroke in rats. Life Sci. 2002; 71(6): 655–665.
- Szekanecz Z, Szamosi S, Kovács GE, et al. The NLRP3 inflammasome — interleukin 1 pathway as a therapeutic target in gout. Arch Biochem Biophys. 2019; 670: 82–93.
- Tufekci KU, Eltutan BI, Isci KB, et al. Resveratrol inhibits NLRP3 inflammasome-induced pyroptosis and miR-155 expression in microglia through sirt1/ampk pathway. Neurotox Res. 2021; 39(6): 1812–1829.
- Wu C, Lu W, Zhang Y, et al. Inflammasome activation triggers blood clotting and host death through pyroptosis. Immunity. 2019; 50(6): 1401–1411.e4.
- Xia N, Daiber A, Förstermann U, et al. Antioxidant effects of resveratrol in the cardiovascular system. Br J Pharmacol. 2017; 174(12): 1633–1646.
- Yang F, Zhu W, Cai X, et al. Minocycline alleviates NLRP3 inflammasome-dependent pyroptosis in monosodium glutamate-induced depressive rats. Biochem Biophys Res Commun. 2020; 526(3): 553–559.
- Yuluğ E, Türedi S, Alver A, et al. Effects of resveratrol on methotrexate-induced testicular damage in rats. ScientificWorldJournal. 2013; 2013: 489659.
- Zhao WP, Wang HW, Liu J, et al. Positive PCNA and Ki-67 expression in the testis correlates with spermatogenesis dysfunction in fluoride-treated rats. Biol Trace Elem Res. 2018; 186(2): 489–497.
- Zhao Y, Song W, Wang Z, et al. Resveratrol attenuates testicular apoptosis in type 1 diabetic mice: role of Akt-mediated Nrf2 activation and p62-dependent Keap1 degradation. Redox Biol. 2018; 14: 609–617.
- Zheng X, Guo C, Lv Z, et al. From animal to cell model: pyroptosis targeted-fibrosis is a novel mechanism of lead-induced testicular toxicity. Food Chem Toxicol. 2023; 178: 113886.
- Zhou J, Zeng L, Zhang Y, et al. Cadmium exposure induces pyroptosis in testicular tissue by increasing oxidative stress and activating the AIM2 inflammasome pathway. Sci Total Environ. 2022; 847: 157500.
