Luteolin Co-treatment abates Polystyrene Microplastics (PS-MPs) Induced Spermatotoxicity and Dysgonadogenesis in Rats Via up-regulation of Gonadotropin, Enhanced Spermatogenesis, Downregulation of Caspases, and Oxido-inflammation
محورهای موضوعی :
Oyovwi Mega Obukohwo
1
,
Ohwin Peggy Ejiro
2
1 - Department of Physiology, Adeleke University, Ede, Osun State, Nigeria
2 - Department of Physiology, Faculty of Basic Medical Sciences, Delta State University, Abraka, Nigeria
کلید واژه: Luteolin, Polystyrene microplastics, Oxido-inflammation, Apoptosis, Spermtotoxicity, Dysgonadogenesis,
چکیده مقاله :
Polystyrene microplastics (PS-MPs) pose a significant scientific concern due to their chemical makeup. Luteolin (LUT), a phytochemical-biological substance with anti-oxidative and anti-inflammatory properties, was tested against polystyrene microplastics (PS-MPs)-induced reproductive toxicity in male Wistar rats. The rats were randomly assigned to 4 groups and treated as follows: Group I received 0.01 mL kg-1 of DMSO alone, Group II received 100 mg kg-1 of LUT dissolved in DMSO, Group III received 0.01 mg kg-1 of PS-MPs, and Group IV received 0.01 mg kg-1 of PS-MPs and 100 mg kg-1 of LUT. PS-MPs alone dramatically increased sperm morphological defects, xanthine oxidase, and lipid peroxidation while decreasing testicular enzymes, luteinizing hormone (LH), follicle-stimulating hormone (FSH), testosterone, antioxidants, and interleukin-10 (IL-10). The study demonstrates that PS-MPs can alter male rat testicular function and androgenicity. However, as a result of LUT co-treatment, sperm count, motility, and viability were increased whereas MDA and XO, IL-1β and TNF-α, and caspase-3 activities in the testis were reduced. Supplementing with LUT might act as a cytoprotective agent to lessen the spermatotoxicity and dysgonadogenesis brought on by PS-MPs.
Polystyrene microplastics (PS-MPs) pose a significant scientific concern due to their chemical makeup. Luteolin (LUT), a phytochemical-biological substance with anti-oxidative and anti-inflammatory properties, was tested against polystyrene microplastics (PS-MPs)-induced reproductive toxicity in male Wistar rats. The rats were randomly assigned to 4 groups and treated as follows: Group I received 0.01 mL kg-1 of DMSO alone, Group II received 100 mg kg-1 of LUT dissolved in DMSO, Group III received 0.01 mg kg-1 of PS-MPs, and Group IV received 0.01 mg kg-1 of PS-MPs and 100 mg kg-1 of LUT. PS-MPs alone dramatically increased sperm morphological defects, xanthine oxidase, and lipid peroxidation while decreasing testicular enzymes, luteinizing hormone (LH), follicle-stimulating hormone (FSH), testosterone, antioxidants, and interleukin-10 (IL-10). The study demonstrates that PS-MPs can alter male rat testicular function and androgenicity. However, as a result of LUT co-treatment, sperm count, motility, and viability were increased whereas MDA and XO, IL-1β and TNF-α, and caspase-3 activities in the testis were reduced. Supplementing with LUT might act as a cytoprotective agent to lessen the spermatotoxicity and dysgonadogenesis brought on by PS-MPs.
1. Zhang Q., He Y., Cheng R., Li Q., Qian Z., Lin X., 2022. Recent advances in toxicological research and potential health impact of microplastics and nanoplastics in vivo. Environmental Science and Pollution Research. 29(27), 40415-40448.
2. Yuan Z., Nag R., Cummins E., 2022. Human health concerns regarding microplastics in the aquatic environment-From marine to food systems. Science of the Total Environment. 823, 153730.
3. Vitali C., Peters R., Janssen H.G., Nielen M.W., Ruggeri F.S., 2022. Microplastics and nanoplastics in food, water, and beverages, part ii. Methods. TrAC Trends in Analytical Chemistry. 116819.
4. Ziani K., Ioniță-Mîndrican C.B., Mititelu M., Neacșu S.M., Negrei C., Moroșan E., Drăgănescu D., Preda O.T., 2023. Microplastics: a real global threat for environment and food safety: a state of the art review. Nutrients. 15(3), 617.
5. Dong X., Liu X., Hou Q., Wang Z., 2023. From natural environment to animal tissues: A review of microplastics (nanoplastics) translocation and hazards studies. Science of the Total Environment. 855, 158686.
6. Wei Z., Wang Y., Wang S., Xie J., Han Q., Chen M., 2022. Comparing the effects of polystyrene microplastics exposure on reproduction and fertility in male and female mice. Toxicology. 465, 153059.
7. Xie X., Deng T., Duan J., Xie J., Yuan J., Chen M., 2020. Exposure to polystyrene microplastics causes reproductive toxicity through oxidative stress and activation of the p38 MAPK signaling pathway. Ecotoxicology and Environmental Safety. 190, 110133.
8. Ferrante M.C., Monnolo A., Del Piano F., Mattace Raso G., Meli R., 2022. The pressing issue of micro-and nanoplastic contamination: profiling the reproductive alterations mediated by oxidative stress. Antioxidants. 11(2), 193.
9. Ramesh P., Jagadeesan R., Sekaran S., Dhanasekaran A., Vimalraj S., 2021. Flavonoids: classification, function, and molecular mechanisms involved in bone remodelling. Frontiers in Endocrinology. 12, 779638.
10. Aghakhani A., Hezave M.B., Rasouli A., Rounkian M.S., Soleimanlou F., Alhani A., Eqlidi N.S., Pirani M., Mehrtabar S., Zerangian N., Pormehr-Yabandeh A., 2023. Endoplasmic Reticulum as a Therapeutic Target in Cancer: Is there a Role for Flavonoids? Current Molecular Medicine. doi: 10.2174/1566524023666230320103429.
11. Oyovwi M.O., Oghenetega O.B., Victor E., Faith F.Y., Uchechukwu J.G., 2023. Quercetin protects against levetiracetam induced gonadotoxicity in rats. Toxicology. 491, 153518.
12. Oyovwi M.O., Ben-Azu B., Edesiri T.P., Victor E., Rotu, R.A., Ozegbe Q.E., Nwangwa E.K., Atuadu V. and Adebayo O.G., 2021. Kolaviron abates busulfan-induced episodic memory deficit and testicular dysfunction in rats: The implications for neuroendopathobiological changes during chemotherapy. Biomedicine & Pharmacotherapy. 142, 112022.
13. Oyovwi M.O., Ben-Azu B., Edesiri T.P. ., Arientare R.R., Emojevwe V., Nwangwa K.E., Edje K.E., Adebayo O.G., 2022. Lutein Attenuates Cyclosporin-induced Testicular Impairment in Male Rats through Modulation of Androgenic Hormones and Enzymes. Pharmacology and Toxicology of Natural Medicines. 2(1), 12-24. https://doi.org/10.52406/ptnm.v2i1.17
14. Asiwe J.N., Ekene E.N., Agbugba L.C., Moke E.G., Akintade A.V., Ben-Azu B., Eruotor H., Daubry T.M.E., Anachuna K.K., Oyovwi M.O., 2023. Ginkgo biloba supplement abates lead-induced endothelial and testicular dysfunction in Wistar rats via up-regulation of Bcl-2 protein expression, pituitary-testicular hormones and down-regulation of oxido-inflammatory reactions. Journal of Trace Elements in Medicine and Biology. 79, 127216.
15. Chijiokwu E. A., Nwangwa E. K., Oyovwi M. O., Naiho A. O., Emojevwe V., Ohwin E. P., Ogheneyoma O.O., 2022. Intermittent fasting and exercise therapy abates STZ‐induced diabetotoxicity in rats through modulation of adipocytokines hormone, oxidative glucose metabolic and glycolytic pathway. Physiological Reports. 10(20), e15279.
16. Tesi E.P., Ben‐Azu B., Mega O.O., Mordi J., Knowledge O.O., Awele E.D., Rotu R.A., Emojevwe V., Adebayo O.G., Eneni O.A.E., 2022. Kolaviron, a flavonoid‐rich extract ameliorates busulfan‐induced chemo‐brain and testicular damage in male rats through inhibition of oxidative stress, inflammatory, and apoptotic pathways. Journal of Food Biochemistry. 46(4), e14071.
17. Oyovwi M.O., Edesiri T.P., Victor E., Kingsley N.E., Rume R.A., Faith F.Y., Agbonifo‐Chijiokwu E., 2022. D‐ribose‐L‐cysteine abrogates testicular maladaptive responses induced by polychlorinated bisphenol intoxication in rats via activation of the mTOR signaling pathway mediating inhibition of apoptosis, inflammation, and oxidonitrergic flux. Journal of Biochemical and Molecular Toxicology. 36(10), e23161.
18. Emojevwe V., Nwangwa E.K., Naiho A.O., Oyovwi M.O., Igiehon O., Ogunwole E., Makinde‐Taylor M.S., Ayotomide O.A., Akinola A.O., Edesiri P.T. and Oghenetega B.O., 2022. Therapeutic efficacy of N‐acetylcysteine and zinc sulphate against di‐(2‐ethylhexyl) phthalate‐induced testicular oxido‐nitrergic stress in male Wistar rat. Andrologia. 54(9), p.e14508.
19. Agbonifo-Chijiokwu E., Nwangwa K.E., Oyovwi M.O., Ben-Azu B., Naiho A.O., Emojevwe V., Ohwin E.P., Ehiwarior A.P., Ojugbeli E.T., Nwabuoku S.U., Moke E.G., 2023. Underlying biochemical effects of intermittent fasting, exercise and honey on streptozotocin-induced liver damage in rats. Journal of Diabetes & Metabolic Disorders. 22(1), 515-527.
20. Fatima T., Bashir O., Naseer B., Hussain S.Z., 2018. Dandelion: Phytochemistry and clinical potential. J Med Plants Stud. 6(2), 198-202.
21. Xu H., Yu W., Sun S., Li C., Zhang Y., Ren J., 2020. Luteolin attenuates doxorubicin-induced cardiotoxicity through promoting mitochondrial autophagy. Frontiers in Physiology. 11, 113.
22. Owumi S.E., Nwozo S.O., Arunsi U.O., Oyelere A.K. and Odunola O.A., 2021. Co-administration of Luteolin mitigated toxicity in rats' lungs associated with doxorubicin treatment. Toxicology and Applied Pharmacology. 411, 115380.
23. Jin H., Yan M., Pan C., Liu Z., Sha X., Jiang C., Li L., Pan M., Li D., Han X., Ding J., 2022. Chronic exposure to polystyrene microplastics induced male reproductive toxicity and decreased testosterone levels via the LH-mediated LHR/cAMP/PKA/StAR pathway. Particle and Fibre Toxicology. 19(1), 13.
24. Sadik N.A., 2008. Effects of diallyl sulfide and zinc on testicular steroidogenesis in cadmium‐treated male rats. Journal of Biochemical and Molecular Toxicology. 22(5), 345-353.
25. Adedara I.A., Omole O., Okpara E.S., Fasina O.B., Ayeni M.F., Ajayi O.M., Busari E.O., Farombi E.O., 2018. Impact of prepubertal exposure to dietary protocatechuic acid on the hypothalamic-pituitary-testicular axis in rats. Chemico-Biological Interactions. 290, 99-109.
26. Owumi S.E., Umez A.O., Arunsi U. and Irozuru C.E., 2023. Dietary aflatoxin B1 and antimalarial—a lumefantrine/artesunate—therapy perturbs male rat reproductive function via pro-inflammatory and oxidative mechanisms. Scientific Reports. 13(1), 12172.
27. Zhang X., Peng Z., Zheng H., Zhang C., Lin H., Qin X., 2021. The potential protective effect and possible mechanism of peptides from oyster (Crassostrea hongkongensis) hydrolysate on triptolide-induced testis injury in male mice. Marine Drugs. 19(10), 566.
28. Koju N., Qin Z.H., Sheng R., 2022. Reduced nicotinamide adenine dinucleotide phosphate in redox balance and diseases: a friend or foe? Acta Pharmacologica Sinica. 43(8), 1889-1904.
29. Olaniyi K.S., Amusa O.A., Oniyide A.A., Ajadi I.O., Akinnagbe N.T. and Babatunde S.S., 2020. Protective role of glutamine against cadmium-induced testicular dysfunction in Wistar rats: involvement of G6PD activity. Life sciences. 242, 117250.
30. D’Angelo S., Meccariello R., 2021. Microplastics: a threat for male fertility. International Journal of Environmental Research and Public Health. 18(5), 2392.
31. Saraceni A., Cottone E., Mognetti B., Schiavo V., Palermo S., Geddo F., Querio G., Antoniotti S., Gallo M.P., Merlo G., Dal Bello F., 2023. Evalution of the exposure to microplastics andassociated contaminants in in vitro and in vivo moldes. European Journal of Histochemistry. 67(s3), 3-3.
32. Wen S., Zhao Y., Liu S., Yuan H., You T., Xu H., 2022. Microplastics-perturbed gut microbiota triggered the testicular disorder in male mice: Via fecal microbiota transplantation. Environmental Pollution. 309, 119789.
33. Aitken R.J., Roman S.D., 2008. Antioxidant systems and oxidative stress in the testes. Molecular Mechanisms in Spermatogenesis. 154-171.
34. Adedara I.A., Alake S.E., Adeyemo M.O., Olajide L.O., Ajibade T.O., Farombi E.O., 2018. Taurine enhances spermatogenic function and antioxidant defense mechanisms in testes and epididymis of L-NAME-induced hypertensive rats. Biomedicine & Pharmacotherapy. 97, 181-189.
35. Kelley E.E., Khoo N.K., Hundley N.J., Malik U.Z., Freeman B.A., Tarpey M.M., 2010. Hydrogen peroxide is the major oxidant product of xanthine oxidase. Free Radical Biology and Medicine. 48(4), 493-498.
36. Hedger M.P., 2011. Toll-like receptors and signalling in spermatogenesis and testicular responses to inflammation—a perspective. Journal of Reproductive Immunology. 88(2), 130-141.
37. Meroni S.B., Galardo M.N., Rindone G., Gorga A., Rier M.F., Cigorraga S.B., 2019. Molecular mechanisms and signaling pathways involved in sertoli cell proliferation. Frontiers in Endocrinology. 10, p.224.
38. Ni F.D., Hao S.L., Yang W.X., 2019. Multiple signaling pathways in Sertoli cells: recent findings in spermatogenesis. Cell death & Disease. 10(8), 541.
39. Hou B., Wang F., Liu T. and Wang Z., 2021. Reproductive toxicity of polystyrene microplastics: In vivo experimental study on testicular toxicity in mice. Journal of Hazardous Materials. 405, 124028.
40. Ijaz M.U., Shahzadi S., Samad A., Ehsan N., Ahmed H., Tahir A., Rehman H., Anwar H., 2021. Dose-dependent effect of polystyrene microplastics on the testicular tissues of the male Sprague Dawley rats. Dose-Response. 19(2), p.15593258211019882.
41. Ijaz M.U., Najam S., Hamza A., Azmat R., Ashraf, A. Unuofin J.O., Lebelo S.L., Simal-Gandara J., 2023. Pinostrobin alleviates testicular and spermatological damage induced by polystyrene microplastics in adult albino rats. Biomedicine & Pharmacotherapy. 162, p.114686.
42. Magura J., Moodley R., Mackraj I., 2022. The effect of hesperidin and luteolin isolated from Eriocephalus africanus on apoptosis, cell cycle and miRNA expression in MCF-7. Journal of Biomolecular Structure and Dynamics. 40(4), 1791-1800.
