Exogenous taurine administration abates reproductive dysfunction in male rats exposed to silver nanoparticles.
Caspase-3
oxido-inflammatory stress
reproductive dysfunction
silver nanoparticles
taurine
Journal
Environmental toxicology
ISSN: 1522-7278
Titre abrégé: Environ Toxicol
Pays: United States
ID NLM: 100885357
Informations de publication
Date de publication:
28 Aug 2023
28 Aug 2023
Historique:
revised:
18
07
2023
received:
16
05
2023
accepted:
13
08
2023
medline:
28
8
2023
pubmed:
28
8
2023
entrez:
28
8
2023
Statut:
aheadofprint
Résumé
The broad contemporary applications of silver nanoparticles (AgNPs) have been associated with various toxicities including reproductive toxicity. Taurine is well acknowledged for its potent pharmacological role in numerous disease models and chemically-mediated toxicity. We investigated the effect of taurine on AgNPs-induced reproductive toxicity in male rats. The animals were intraperitoneally injected with AgNPs (200 μg/kg) alone or co-administered with taurine at 50 and 100 mg/kg for 21 successive days. Exogenous taurine administration significantly abated AgNPs-induced oxidative injury by decreasing the levels of oxidative stress indices while boosting antioxidant enzymes activities and glutathione level in the hypothalamus, testes and epididymis of exposed animals. Taurine administration alleviated AgNPs-induced inflammatory response and caspase-3 activity, an apoptotic biomarker. Moreover, taurine significantly improved spermiogram, reproductive hormones and the marker enzymes of testicular function in AgNPs-treated animals. The ameliorative effect of taurine on pathological lesions induced by AgNPs in the exposed animals was substantiated by histopathological data. This study provides the first mechanistic evidence that taurine supplementation affords therapeutic effect against reproductive dysfunction associated with AgNPs exposure in male rats.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Dos Santos CA, Seckler MM, Ingle AP, et al. Silver nanoparticles: therapeutical uses, toxicity, and safety issues. J Pharm Sci. 2014;103:1931-1944.
Nie P, Zhao Y, Xu H. Synthesis, applications, toxicity and toxicity mechanisms of silver nanoparticles: a review. Ecotoxicol Environ Saf. 2023;253:114636. doi:10.1016/j.ecoenv.2023.114636
Sharma A, Kontodimas K, Bosmann M. Nanomedicine: a diagnostic and therapeutic approach to COVID-19. Front Med (Lausanne). 2021;8:648005. doi:10.3389/fmed.2021.648005
Salleh A, Naomi R, Utami ND, et al. The potential of silver nanoparticles for antiviral and antibacterial applications: a mechanism of action. Nanomaterials (Basel). 2020;10:1566. doi:10.3390/nano10081566
Choudhury H, Pandey M, Lim YQ, et al. Silver nanoparticles: advanced and promising technology in diabetic wound therapy. Mater Sci Eng C. 2020;112:110925. doi:10.1016/j.msec.2020.110925
Almanza-Reyes H, Moreno S, Plascencia-López I, et al. Evaluation of silver nanoparticles for the prevention of SARS-CoV-2 infection in health workers: in vitro and in vivo. PloS One. 2021;16:e0256401. doi:10.1371/journal.pone.0256401
Basit F, Asghar S, Ahmed T, et al. Facile synthesis of nanomaterials as nanofertilizers: a novel way for sustainable crop production. Environ Sci Pollut Res Int. 2022;29:51281-51297.
Guleria G, Thakur S, Shandilya M, Sharma S, Thakur S, Kalia S. Nanotechnology for sustainable agro-food systems: the need and role of nanoparticles in protecting plants and improving crop productivity. Plant Physiol Biochem. 2023;194:533-549.
Jeremiah SS, Miyakawa K, Morita T, Yamaoka Y, Ryo A. Potent antiviral effect of silver nanoparticles on SARS-CoV-2. Biochem Biophys Res Commun. 2020;533:195-200.
Banu AN, Kudesia N, Raut AM, Pakrudheen I, Wahengbam J. Toxicity, bioaccumulation, and transformation of silver nanoparticles in aqua biota: a review environ. Chem Lett. 2021;19:4275-4296.
Bi Y, Marcus AK, Robert H, et al. The complex puzzle of dietary silver nanoparticles, mucus and microbiota in the gut. J Toxicol Environ Health B Crit Rev. 2020;23:69-89.
Karuppaiah A, Selvaraj D, Sellappan M, et al. A perspective on therapeutic applications and strategies to mitigate toxicity of metallic nanoparticles. Curr Pharm Des. 2023;29:239-245.
Skvortsov AN, Ilyechova EY, Puchkova LV. Chemical background of silver nanoparticles interfering with mammalian copper metabolism. J Hazard Mater. 2023;451:131093. doi:10.1016/j.jhazmat.2023.131093
Asare N, Instanes C, Sandberg WJ, et al. Cytotoxic and genotoxic effects of silver nanoparticles in testicular cells. Toxicology. 2012;291(1-3):65-72.
Habas K, Brinkworth MH, Anderson D. Silver nanoparticle-mediated cellular responses in isolated primary sertoli cells in vitro. Food Chem Toxicol. 2018;116:182-188.
Wang E, Huang Y, Du Q, Sun Y. Silver nanoparticle induced toxicity to human sperm by increasing ROS (reactive oxygen species) production and DNA damage. Environ Toxicol Pharmacol. 2017;52:193-199.
Ma YB, Lu CJ, Junaid M, et al. Potential adverse outcome pathway (AOP) of silver nanoparticles mediated reproductive toxicity in zebrafish. Chemosphere. 2018;207:320-328.
Gromadzka-Ostrowska J, Dziendzikowska K, Lankoff A, et al. Silver nanoparticles effects on epididymal sperm in rats. Toxicol Lett. 2012;214:251-258.
Rezazadeh-Reyhani Z, Razi M, Malekinejad H, Sadrkhanlou R. Cytotoxic effect of nanosilver particles on testicular tissue: evidence for biochemical stress and Hsp70-2 protein expression. Environ Toxicol Pharmacol. 2015;40:626-638.
Ansar S, Abudawood M, Hamed SS, Aleem MM. Sodium selenite protects against silver nanoparticle-induced testicular toxicity and inflammation. Biol Trace Elem Res. 2017;175:161-168.
Elsharkawy EE, Abd El-Nasser M, Kamaly HF. Silver nanoparticles testicular toxicity in rat. Environ Toxicol Pharmacol. 2019;70:103194. doi:10.1016/j.etap.2019.103194
Ray A, Nath D. Dose dependent intra-testicular accumulation of silver nanoparticles triggers morphometric changes in seminiferous tubules and Leydig cells and changes the structural integrity of spermatozoa chromatin. Theriogenology. 2022;192:122-131.
Assar DH, Mokhbatly AA, ELazab MFA, et al. Silver nanoparticles induced testicular damage targeting NQO1 and APE1 dysregulation, apoptosis via Bax/Bcl-2 pathway, fibrosis via TGF-β/α-SMA upregulation in rats. Environ Sci Pollut Res Int. 2023;30:26308-26326.
Jurkowska H, Stipanuk MH, Hirschberger LL, Roman HB. Propargylglycine inhibits hypotaurine/taurine synthesis and elevates cystathionine and homocysteine concentrations in primary mouse hepatocytes. Amino Acids. 2015;47:1215-1223.
Franconi F, Loizzo A, Ghirlanda G, Seghieri G. Taurine supplementation and diabetes mellitus. Curr Opin Clin Nutr Metab Care. 2006;9:32-36.
Abud GF, de Carvalho FG, Batitucci G, et al. Taurine as a possible antiaging therapy: a controlled clinical trial on taurine antioxidant activity in women ages 55 to 70. Nutrition. 2022;101:111706. doi:10.1016/j.nut.2022.111706
Shao A, Hathcock JN. Risk assessment for the amino acids taurine, L-glutamine and L-arginine. Regul Toxicol Pharmacol. 2008;50:376-399.
Waldron M, Patterson SD, Tallent J, Jeffries O. The effects of an oral taurine dose and supplementation period on endurance exercise performance in humans: a meta-analysis. Sports Med. 2018;48:1247-1253.
Lobo MV, Alonso FJ, del Río RM. Immunohistochemical localization of taurine in the male reproductive organs of the rat. J Histochem Cytochem. 2000;48:313-320.
Wu H, Zhang X, Yang J, et al. Taurine and its transporter TAUT positively affect male reproduction and early embryo development. Hum Reprod. 2022;37:1229-1243.
Ma J, Yang Z, Jia S, Yang R. A systematic review of preclinical studies on the taurine role during diabetic nephropathy: focused on anti-oxidative, anti-inflammation, and anti-apoptotic effects. Toxicol Mech Methods. 2022;32:420-430.
Li Y, Peng Q, Shang J, et al. The role of taurine in male reproduction: physiology, pathology and toxicology. Front Endocrinol (Lausanne). 2023;14:1017886. doi:10.3389/fendo.2023.1017886
Khalaf HA, Elsamanoudy AZ, Abo-Elkhair SM, Hassan FE, Mohie PM, Ghoneim FM. Endoplasmic reticulum stress and mitochondrial injury are critical molecular drivers of AlCl3-induced testicular and epididymal distortion and dysfunction: protective role of taurine. Histochem Cell Biol. 2022;158:97-121.
Ommati MM, Sabouri S, Retana-Marquez S, et al. Taurine improves sperm mitochondrial indices, blunts oxidative stress parameters, and enhances steroidogenesis and kinematics of sperm in lead-exposed mice. Reprod Sci. 2022;30:1891-1910. doi:10.1007/s43032-022-01140-5
Adedara IA, Alake SE, Adeyemo MO, Olajide LO, Ajibade TO, Farombi EO. Taurine enhances spermatogenic function and antioxidant defense mechanisms in testes and epididymis of L-NAME-induced hypertensive rats. Biomed Pharmacother. 2018;97:181-189.
ElBanna AH, Osman AS, Hossny A, ElBanna H, Abo El-Ela FI. Dose-dependent effects of taurine against testicular damage in a streptozotocin-induced type 1 diabetes mellitus rat model. Int J Immunopathol Pharmacol. 2023;37:3946320231172745. doi:10.1177/03946320231172745
Agnihotri S, Soumyo Mukherji S, Mukherji S. Size-controlled silver nanoparticles synthesized over the range 5-100 nm using the same protocol and their antibacterial efficacy. RSC Adv. 2014;4:3974-3983.
Njoku CA, Ileola-Gold AV, Adelaja UA, et al. Amelioration of neurobehavioral, biochemical, and morphological alterations associated with silver nanoparticles exposure by taurine in rats. J Biochem Mol Toxicol. 2023;12:e23457. doi:10.1002/jbt.23457
Ghaderi S, Tabatabaei SR, Varzi HN, Rashno M. Induced adverse effects of prenatal exposure to silver nanoparticles on neurobehavioral development of offspring of mice. J Toxicol Sci. 2015;40:263-275.
Cooke PS, Zhao YD, Hansen LG. Neonatal polychlorinated biphenyl treatment increases adult testis size and sperm production in the rat. Toxicol Appl Pharmacol. 1996;136:112-117.
Chandra AK, Chatterjee A, Ghosh R, Sarkar M. Vitamin E-supplementation protect chromium (VI)-induced spermatogenic and steroidogenic disorders intesticular tissues of rats, food chem. Toxicology. 2010;48:972-979.
Rogers KR, Navratilova J, Stefaniak A, et al. Characterization of engineered nanoparticles in commercially available spray disinfectant products advertised to contain colloidal silver. Sci Total Environ. 2018;619−620:1375-1384.
Park EJ, Bae E, Yi J, et al. Repeated-dose toxicity and inflammatory responses in mice by oral administration of silver nanoparticles. Environ Toxicol Pharmacol. 2010;30:162-168.
Dziendzikowska K, Gromadzka-Ostrowska J, Lankoff A, et al. Time-dependent biodistribution and excretion of silver nanoparticles in male Wistar rats. J Appl Toxicol. 2012;32:920-928.
Grün AL, Emmerling C. Long-term effects of environmentally relevant concentrations of silver nanoparticles on major soil bacterial phyla of a loamy soil. Environ Sci Eur. 2018;30:31. doi:10.1186/s12302-018-0160-2
Wang P, Menzies NW, Chen H, et al. Risk of silver transfer from soil to the food chain is low after long-term (20 years) field applications of sewage sludge. Environ Sci Technol. 2018;52:4901-4909.
Gray DB, Gagnon V, Button M, et al. Silver nanomaterials released from commercial textiles have minimal impacts on soil microbial communities at environmentally relevant concentrations. Sci Total Environ. 2022;806:151248. doi:10.1016/j.scitotenv.2021.151248
Adedara IA, Okpara ES, Busari EO, Omole O, Owumi SE, Farombi EO. Dietary protocatechuic acid abrogates male reproductive dysfunction in streptozotocin-induced diabetic rats via suppression of oxidative damage, inflammation and caspase-3 activity. Eur J Pharmacol. 2019;849:30-42.
Zemjanis R. Collection and evaluation of semen. In: Zemjanis R, ed. Diagnostic and Therapeutic Technique in Animal Reproduction. 2nd ed. William and Wilkins Company, Waverly Press, Inc; 1970:139-153.
World Health Organization. Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction. Vol 76, 1999. 4th ed. Cambridge University Press; 1999:4-33.
Farombi EO, Abarikwu SO, Adedara IA, Oyeyemi MO. Curcumin and kolaviron ameliorate di-n-butylphthalate-induced testicular damage in rats. Basic Clin Pharmacol Toxicol. 2007;100:43-48.
Blazak WF, Trienen KA, Juniewicz PE. Application of testicular sperm head counts in the assessment of male reproductive toxicity. In: Chapin RE, Heindel J, eds. Methods in Toxiciology. Male Reproductive Toxicology. Vol 3A. Academic Press; 1993:86-94.
Bradford MM. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254.
Clairborne A. Catalase activity. In: Greewald AR, ed. Handbook of Methods for Oxygen Radical Research. CRC Press; 1995:237-242.
Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG. Selenium: biochemical role as a component of glutathione peroxidase. Science. 1973;179:588-590.
Misra HP, Fridovich I. The role of superoxide anion in the autooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247:3170-3175.
Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferase. The first enzymatic step in mercapturic acid formation. J Biol Chem. 1974;249:7130-7139.
Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR. Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology. 1974;11:151-169.
Wolff SP. Ferrous ion oxidation in the presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. Methods Enzymol. 1994;233:182-189.
Adedara IA, Abolaji AO, Rocha JB, Farombi EO. Diphenyl diselenide protects against mortality, locomotor deficits and oxidative stress in drosophila melanogaster model of manganese-induced neurotoxicity. Neurochem Res. 2016;41:1430-1438.
Farombi EO, Tahnteng JG, Agboola AO, Nwankwo JO, Emerole GO. Chemoprevention of 2-acetylaminofluorene-induced hepatotoxicity and lipid peroxidation in rats by kolaviron-a Garcinia kola seed extract, food chem. Toxicology. 2000;38:535-541.
Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem. 1982;126:131-138.
Granell S, Gironella M, Bulbena O, et al. Heparin mobilizes xanthine oxidase and induces lung inflammation in acute pancreatitis. Crit Care Med. 2003;31:525-530.
Bancroft JD, Gamble M. Theory and Practice of Histology Techniques. 6th ed. Churchill Livingstone Elsevier; 2008:83-134.
Adedara IA, Awogbindin IO, Mohammed KA, Da-Silva OF, Farombi EO. Abatement of the dysfunctional hypothalamic-pituitary-gonadal axis due to ciprofloxacin administration by selenium in male rats. J Biochem Mol Toxicol. 2021;35:e22741.
Adedara IA, Ebokaiwe AP, Mathur PP, Farombi EO. Nigerian bonny light crude oil induces endocrine disruption in male rats. Drug Chem Toxicol. 2014;37:198-203.
Zirkin BR, Papadopoulos V. Leydig cells: formation, function, and regulation. Biol Reprod. 2018;99:101-111.
Muerköster AP, Frederiksen H, Juul A, et al. Maternal phthalate exposure associated with decreased testosterone/LH ratio in male offspring during mini-puberty. Odense Child Cohort Environ Int. 2020;144:106025. doi:10.1016/j.envint.2020.106025
Zhang Z, Cheng Q, Liu Y, et al. Zinc-enriched yeast may improve spermatogenesis by regulating steroid production and antioxidant levels in mice. Biol Trace Elem Res. 2022;200:3712-3722.
Salihu M, Ajayi BO, Adedara IA, Farombi EO. 6-gingerol-rich fraction prevents disruption of histomorphometry and marker enzymes of testicular function in carbendazim-treated rats. Andrologia. 2017;49:e12782. doi:10.1111/and.12782
Kempinas WG, Lamano-Carvalho TL. A method for estimating the concentration of spermatozoa in the rat cauda epididymidis. Lab Anim. 1988;22:154-156.
Turner TT. Necessity's potion: inorganic ions and small organic molecules in the epididymal lumen. The Epididymis: From Molecules to Clinical Practice. Springer; 2002:131-150.
Murdoch RN, Armstrong VL, Clulow J, Jones RC. Relationship between motility and oxygen consumption of sperm from the cauda epididymides of the rat. Reprod Fertil Dev. 1999;11:87-94.
Si W, Men H, Benson JD, Critser JK. Osmotic characteristics and fertility of murine spermatozoa collected in different solutions. Reproduction. 2009;137:215-223.
Aitken RJ, Jones KT, Robertson SA. Reactive oxygen species and sperm function - in sickness and in health. J Androl. 2012;33:1096-1106.
Khanna P, Ong C, Bay BH, Baeg GH. Nanotoxicity: an interplay of oxidative stress, inflammation and cell death. Nanomaterials (Basel). 2015;5:1163-1180.
Rana T. Influence and implications of the molecular paradigm of nitric oxide underlying inflammatory reactions of the gastrointestinal tract of dog: a major Hallmark of inflammatory bowel disease. Inflamm Bowel Dis. 2022;28:1280-1288.
Kargapolova Y, Geißen S, Zheng R, Baldus S, Winkels H, Adam M. The enzymatic and non-enzymatic function of myeloperoxidase (MPO) in inflammatory communication. Antioxidants. 2021;10:562. doi:10.3390/antiox10040562