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Research Articles

Cadmium exposure induces testicular oxidative damage and histopathological changes in the freshwater leech Limnatis nilotica (Savigny, 1822): the protective role of salicylic acid

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Pages 189-198 | Received 16 May 2022, Accepted 04 Apr 2023, Published online: 12 Jun 2023

References

  • Aebi H. 1984. Catalase in vitro. Methods in Enzymology 105: 121–126. https://doi.org/10.1016/S0076-6879(84)05016-3.
  • Alharthi WA, Hamza RZ, Elmahdi MM, Abuelzahab HS, Saleh H. 2020. Selenium and L-carnitine ameliorate reproductive toxicity induced by cadmium in male mice. Biological Trace Element Research 197: 619–627. https://doi.org/10.1007/s12011-019-02016-7.
  • Ansar S, Abudawood M, Alaraj AS, Hamed SS. 2018. Hesperidin alleviates zinc oxide nanoparticle induced hepatotoxicity and oxidative stress. BMC Pharmacology and Toxicology 19: article 65. https://doi.org/10.1186/s40360-018-0256-8.
  • Beyer WF Jr, Fridovich I. 1987. Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical Biochemistry 161: 559–566. https://doi.org/10.1016/0003-2697(87)90489-1.
  • Bhardwaj JK, Panchal H, Saraf P. 2021. Cadmium as a testicular toxicant: a review. Journal of Applied Toxicology 41: 105–117. https://doi.org/10.1002/jat.4055.
  • Buege JA, Aust SD. 1978. Microsomal lipid peroxidation. Methods in Enzymology 52: 302–310. https://doi.org/10.1016/s0076-6879(78)52032-6.
  • Chatterjee I. 1973. Evolution and the biosynthesis of ascorbic acid. Science 182: 1271–1272. https://doi.org/10.1126/science.182.4118.1271.
  • Cupertino MC, Novaes RD, Santos EC, Bastos DSS, Marques dos Santos DC, do Carmo Queiroz Fialho M, Matta SLP. 2017. Cadmium-induced testicular damage is associated with mineral imbalance, increased antioxidant enzymes activity and protein oxidation in rats. Life Sciences 175: 23–30. https://doi.org/10.1016/j.lfs.2017.03.007.
  • da Silva J, Goncalves RV, de Melo FCSA, Sarandy MM, da Matta SLP. 2021. Cadmium exposure and testis susceptibility: a systematic review in murine models. Biological Trace Element Research 199: 2663–2676. https://doi.org/10.1007/s12011-020-02389-0.
  • Davies RW, Singhal R, Wicklum D. 1995. Changes in reproductive potential of the leech Nephelopsis obscura (Erpobdellidae) as biomarkers for cadmium stress. Canadian Journal of Zoology 73: 2192–2196. https://doi.org/10.1139/z95-259.
  • Dinis-Oliveira RJ, Sousa C, Remião F, Duarte JA, Ferreira R, Sánchez Navarro A, Bastos ML, Carvalho F. 2007 Sodium salicylate prevents paraquat-induced apoptosis in the rat lung. Free Radical Biology and Medicine 43: 48–61. https://doi.org/10.1016/j.freeradbiomed.2007.03.014.
  • Drew JE, Arthur JR, Farquharson AJ, Russell WR, Morrice PC, Duthie GG. 2005. Salicylic acid modulates oxidative stress and glutathione peroxidase activity in the rat colon. Biochemical Pharmacology 70: 888–893. https://doi.org/10.1016/j.bcp.2005.06.011.
  • El-Demerdash FM, Yousef MI, Kedwany FS, Baghdadi HH. 2004. Cadmium-induced changes in lipid peroxidation, blood hematology, biochemical parameters and semen quality of male rats: protective role of vitamin E and β-carotene. Food and Chemical Toxicology 42: 1563–1571. https://doi.org/10.1016/j.fct.2004.05.001.
  • El-Esawi MA, Elansary HO, El-Shanhorey NA, Abdel-Hamid AM, Ali HM, Elshikh MS. 2017. Salicylic acid-regulated antioxidant mechanisms and gene expression enhance rosemary performance under saline conditions. Frontiers in Physiology 8: article 716. https://doi.org/10.3389/fphys.2017.00716.
  • Ellman GL. 1959. Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 82: 70–77. https://doi.org/10.1016/0003-9861(59)90090-6.
  • Ensibi C, Yahia MND. 2017. Toxicity assessment of cadmium chloride on planktonic copepods Centropages ponticus using biochemical markers. Toxicology Reports 4: 83–88. https://doi.org/10.1016/j.toxrep.2017.01.005.
  • Flohé L, Günzler WA. 1984. Assays of glutathione peroxidase. Methods in Enzymology 105: 114–120. https://doi.org/10.1016/S0076-6879(84)05015-1.
  • Gao Y, Hong J, Guo Y, Chen M, Chang AK, Xie L, Ying X. 2021. Assessment spermatogenic cell apoptosis and the transcript levels of metallothionein and p53 in Meretrix meretrix induced by cadmium. Ecotoxicology and Environmental Safety 217: article 112230. https://doi.org/10.1016/j.ecoenv.2021.112230.
  • Glasby CJ, Erséus C, Martin P. 2021. Annelids in extreme aquatic environments: diversity, adaptations and evolution. Diversity (Basel) 13: article 98. https://doi.org/10.3390/d13020098.
  • Gómez-Velázquez HD, Aparicio-Fernández X, Reynoso-Camacho R. 2021. Chia sprouts elicitation with salicylic acid and hydrogen peroxide to improve their phenolic content, antioxidant capacities in vitro and the antioxidant status in obese rats. Plant Foods for Human Nutrition 76: 363–370. https://doi.org/10.1007/s11130-021-00912-9.
  • Goretti E, Pallottini M, Ricciarini M, Selvaggi R, Cappelletti D. 2016. Heavy metals bioaccumulation in selected tissues of red swamp crayfish: an easy tool for monitoring environmental contamination levels. Science of the Total Environment 559: 339–346. https://doi.org/10.1016/j.scitotenv.2016.03.169.
  • Gueboudji Z, Addad D, Kadi K, Nagaz K, Secrafi M, Yahya LB, Lachehib B, Abdelmalek A. 2022. Biological activities and phenolic compounds of olive oil mill wastewater from Abani, endemic Algerian variety. Scientific Reports 12: article 6042. https://doi.org/10.1038/s41598-022-10052-y.
  • Guerrero A, González-Correa JA, Arrebola MM, Muñoz-Marín J, Sánchez De La Cuesta F, De La Cruz JP. 2004. Antioxidant effects of a single dose of acetylsalicylic acid and salicylic acid in rat brain slices subjected to oxygen-glucose deprivation in relation with its antiplatelet effect. Neuroscience Letters 358: 153–156. https://doi.org/10.1016/j.neulet.2004.01.036.
  • Halliwell B, Gutteridge JM. 2015. Free Radicals in Biology and Medicine. Oxford: Oxford University Press. https://doi.org/10.1093/acprof:oso/9780198717478.001.0001.
  • Hayati A, Pratiwi H, Khoiriyah I, Winarni D, Sugiharto. 2017. Histopathological assessment of cadmium effect on testicles and kidney of Oreochromis niloticus in different salinity. AIP Conference Proceedings 1854: article 020014. https://doi.org/10.1063/1.4985405.
  • Hissin PJ, Hilf R. 1976. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Analytical Biochemistry 74: 214–226. https://doi.org/10.1016/0003-2697(76)90326-2.
  • Ighodaro O, Akinloye O. 2018. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alexandria Journal of Medicine 54: 287–293. https://doi.org/10.1016/j.ajme.2017.09.001.
  • John J, Rugmini SD, Nair BS. 2017. Kinetic analysis of thermal and hydrolytic decomposition of spiroborate ester of curcumin with salicylic acid. Oriental Journal of Chemistry 33: 849–858. https://doi.org/10.13005/ojc/330234.
  • Jollow D, Mitchell J, Zampaglione N, Gillette J. 1974. Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11: 151–169. https://doi.org/10.1159/000136485.
  • Joseph L, Jun B-M, Flora JR, Park CM, Yoon Y. 2019. Removal of heavy metals from water sources in the developing world using low-cost materials: a review. Chemosphere 229: 142–159. https://doi.org/10.1016/j.chemosphere.2019.04.198.
  • Jovanovic Z. 2021. The electrophysiological effects of cadmium on Retzius nerve cells of the leech Haemopis sanguisuga. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 247: article 109062. https://doi.org/10.1016/j.cbpc.2021.109062.
  • Khaled I, Ferjani H, Ben Ahmed R, Harrath AH. 2016. Effects of oil-related environmental pollutants on gonads of the freshwater leech Limnatis nilotica (Annelida, Hirudinea). Invertebrate Reproduction & Development 60: 263–270. https://doi.org/10.1080/07924259.2016.1208118.
  • Khaled I, Ahmed RB, Saidi I, Abbassi R, Abdelkader MO, Harrath AH. 2022a. Salicyclic acid against the disruptive effects of cadmium induces oxidative stress and biochemical and histopathological changes in the ovary of the freshwater leech Limnatis nilotica (Savigny, 1822). Environmental Pollutants and Bioavailability 34: 321–330. https://doi.org/10.1080/26395940.2022.2105749.
  • Khaled I, Saidi I, Ferjani H, Ahmed RB, Alrezaki A, Guesmi F, Bouzenna H, Harrath AH. 2022b. BTEX induces histopathological alterations, oxidative stress response and DNA damage in the testis of the freshwater leech Erpobdella johanssoni (Johansson, 1927). Journal of King Saud University – Science 34: article 102196. https://doi.org/10.1016/j.jksus.2022.102196.
  • Kumar S, Sharma A. 2019. Cadmium toxicity: effects on human reproduction and fertility. Reviews on Environmental Health 34: 327–338. https://doi.org/10.1515/reveh-2019-0016.
  • Li Q, Wang G, Wang Y, Yang D, Guan C, Ji J. 2019. Foliar application of salicylic acid alleviate the cadmium toxicity by modulation the reactive oxygen species in potato. Ecotoxicology and Environmental Safety 172: 317–325. https://doi.org/10.1016/j.ecoenv.2019.01.078.
  • Lu K, Qiao R, An H, Zhang Y. 2018. Influence of microplastics on the accumulation and chronic toxic effects of cadmium in zebrafish (Danio rerio). Chemosphere 202: 514–520. https://doi.org/10.1016/j.chemosphere.2018.03.145.
  • Luevano J, Damodaran C. 2014. A review of molecular events of cadmium-induced carcinogenesis. Journal of Environmental Pathology, Toxicology and Oncology 33: 183–194. https://doi.org/10.1615/jenvironpatholtoxicoloncol.2014011075.
  • Mihaljević Z, Ternjej I, Stanković I, Kerovec M, Kopjar N. 2009. Application of the comet assay and detection of DNA damage in haemocytes of medicinal leech affected by aluminium pollution: a case study. Environmental Pollution 157: 1565–1572. https://doi.org/10.1016/j.envpol.2009.01.002.
  • Moustafa-Farag M, Mohamed HI, Mahmoud A, Elkelish A, Misra AN, Guy KM, Kamran M, Ai S, Zhang M. 2020. Salicylic acid stimulates antioxidant defense and osmolyte metabolism to alleviate oxidative stress in watermelons under excess boron. Plants 9: article 724. https://doi.org/10.3390/plants9060724.
  • Mukherjee S, Choudhuri M. 1983. Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiologia Plantarum 58: 166–170. https://doi.org/10.1111/j.1399-3054.1983.tb04162.x.
  • Nna VU, Usman UZ, Ofutet EO, Owu DU. 2017. Quercetin exerts preventive, ameliorative and prophylactic effects on cadmium chloride-induced oxidative stress in the uterus and ovaries of female Wistar rats. Food and Chemical Toxicology 102: 143–155. https://doi.org/10.1016/j.fct.2017.02.010.
  • Ognjanović BI, Marković SD, Ðorđević NZ, Trbojević IS, Štajn AŠ, Saičić ZS. 2010. Cadmium-induced lipid peroxidation and changes in antioxidant defense system in the rat testes: protective role of coenzyme Q10 and Vitamin E. Reproductive Toxicology 29: 191–197. https://doi.org/10.1016/j.reprotox.2009.11.009.
  • Ojekunle OO, Sodipe A. 2020. Antioxidative effect of selenium in cadmium-exposed tardigrade (H. exemplaris). Water, Air, & Soil Pollution 231: article 577. https://doi.org/10.1007/s11270-020-04938-8.
  • Othman AI, Abdel-Hamid M. 2017. Curcumin mitigates fenthioninduced testicular toxicity in rats: histopathological and immunohistochemical study. African Zoology 52: 209–215. https://doi.org/10.1080/15627020.2017.1396194.
  • Park K, Kwak I-S. 2020. Cadmium-induced developmental alteration and upregulation of serine-type endopeptidase transcripts in wild freshwater populations of Chironomus plumosus. Ecotoxicology and Environmental Safety 192: article 110240. https://doi.org/10.1016/j.ecoenv.2020.110240.
  • Patananan AN, Budenholzer LM, Pedraza ME, Torres ER, Adler LN, Clarke SG. 2015. The invertebrate Caenorhabditis elegans biosynthesizes ascorbate. Archives of Biochemistry and Biophysics 569: 32–44. https://doi.org/10.1016/j.abb.2015.02.002.
  • Randjelović P, Veljković S, Stojiljković N, Janković-Velicković L, Sokolović D, Stojiljković M, Ilić I. 2012. Salicylic acid attenuates gentamicin-induced nephrotoxicity in rats. The Scientific World Journal 2012: article 390613. https://doi.org/10.1100/2012/390613.
  • Randjelović P, Veljković S, Stojiljković N, Sokolović D, Ilić I, Laketić D, Randjelović D, Randjelović N. 2015. The beneficial biological properties of salicylic acid. Acta Facultatis Medicae Naissensis 32: 259–265. https://doi.org/10.1515/afmnai-2015-0026.
  • Ray PD, Huang B-W, Tsuji Y. 2012. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cellular Signalling 24: 981–990. https://doi.org/10.1016/j.cellsig.2012.01.008.
  • Ren Y, Shao W, Zuo L, Zhao W, Qin H, Hua Y, Lu D, Mi C, Zeng S, Zu L. 2019. Mechanism of cadmium poisoning on testicular injury in mice. Oncology Letters 18: 1035–1042. https://doi.org/10.3892/ol.2019.10418.
  • Saidi I, Guesmi F, Kharbech O, Hfaiedh N, Djebali W. 2021. Gallic acid improves the antioxidant ability against cadmium toxicity: impact on leaf lipid composition of sunflower (Helianthus annuus) seedlings. Ecotoxicology and Environmental Safety 210: article 111906. https://doi.org/10.1016/j.ecoenv.2021.111906.
  • Saidi I, Yousfi N, Borgi MA. 2017. Salicylic acid improves the antioxidant ability against arsenic-induced oxidative stress in sunflower (Helianthus annuus) seedling. Journal of Plant Nutrition 40: 2326–2335. https://doi.org/10.1080/01904167.2017.1310888.
  • Sedlak J, Lindsay RH. 1968. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Analytical Biochemistry 25: 192–205. https://doi.org/10.1016/0003-2697(68)90092-4.
  • Sierra-Marquez L, Espinosa-Araujo J, Atencio-Garcia V, Olivero-Verbel J. 2019. Effects of cadmium exposure on sperm and larvae of the neotropical fish Prochilodus magdalenae. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 225: article 108577. https://doi.org/10.1016/j.cbpc.2019.108577.
  • Tang YE, Wang J, Li N, He Y, Zeng Z, Peng Y, Lv B, Zhang X, Sun H, Wang Z, et al. 2022. Comparative analysis unveils the cadmium-induced reproductive toxicity on the testes of Pardosa pseudoannulata. Science Sci of The Total Environment 828: article 154328. https://doi.org/10.1016/j.scitotenv.2022.154328.
  • Unsal V, Dalkıran T, Çiçek M, Kölükçü E. 2020. The role of natural antioxidants against reactive oxygen species produced by cadmium toxicity: a review. Advanced Pharmaceutical Bulletin 10: 184–202. https://doi.org/10.34172/apb.2020.023.
  • Venditti M, Ben Rhouma M, Romano MZ, Messaoudi I, Reiter RJ, Minucci S. 2021. Altered expression of DAAM1 and PREP induced by cadmium toxicity is counteracted by melatonin in the rat testis. Genes (Basel) 12: article 1016. https://doi.org/10.3390/genes12071016.
  • Wan L, Zhang H. 2012. Cadmium toxicity: effects on cytoskeleton, vesicular trafficking and cell wall construction. Plant Signaling & Behavior 7: 345–348. https://doi.org/10.4161/psb.18992.
  • Wang J, Zhu H, Wang K, Yang Z, Liu Z. 2020. Protective effect of quercetin on rat testes against cadmium toxicity by alleviating oxidative stress and autophagy. Environmental Science and Pollution Research 27: 25278–25286. https://doi.org/10.1007/s11356-020-08947-2.
  • Westcott FM. 1997. The effects of low-level chronic cadmium exposure on a freshwater leech. Unpublished MSc, University of Calgary, Canada.
  • Wicklum D, Davies RW. 1996. The effects of chronic cadmium stress on energy acquisition and allocation in a freshwater benthic invertebrate predator. Aquatic Toxicology 35: 237–252. https://doi.org/10.1016/0166-445X(96)00795-3.
  • Wicklum D, Smith D, Davies RW. 1997. Mortality, preference, avoidance, and activity of a predatory leech exposed to cadmium. Archives of Environmental Contamination and Toxicology 32: 178–183. https://doi.org/10.1007/s002449900172.
  • Wong SZ, Ching B, Chng YR, Wong WP, Chew SF, Ip YK. 2013. Ascorbic acid biosynthesis and brackish water acclimation in the euryhaline freshwater white-rimmed stingray, Himantura signifer. PLoS ONE 8: e66691. https://doi.org/10.1371/journal.pone.0066691.
  • Wu D, Xu J, Song E, Tang S, Zhang X, Kemper N, Hartung J, Bao E. 2015. Acetyl salicylic acid protected against heat stress damage in chicken myocardial cells and may associate with induced Hsp27 expression. Cell Stress and Chaperones 20: 687–696. https://doi.org/10.1007/s12192-015-0596-x.
  • Xu J, Tang S, Yin B, Sun J, Song E, Bao E. 2017. Co-enzyme Q10 and acetyl salicylic acid enhance Hsp70 expression in primary chicken myocardial cells to protect the cells during heat stress. Molecular and Cellular Biochemistry 435: 73–86. https://doi.org/10.1007/s11010-017-3058-1.
  • Yabuta Y, Nagata R, Aoki Y, Kariya A, Wada K, Yanagimoto A, Hara H, Bito T, Okamoto N, Yoshida S, et al. 2020. L-ascorbate biosynthesis involves carbon skeleton rearrangement in the nematode Caenorhabditis elegans. Metabolites 10: article 334. https://doi.org/10.3390/metabo10080334.
  • Yang SH, He JB, Yu LH, Li L, Long M, Liu MD, Li P. 2019. Protective role of curcumin in cadmium-induced testicular injury in mice by attenuating oxidative stress via Nrf2/ARE pathway. Environmental Science and Pollution Research 26: 34575–34583. https://doi.org/10.1007/s11356-019-06587-9.
  • Zaidi SNF, Usman SM. 2021. Salicylic acid attenuates gentamicin-induced nephrotoxicity in rabbits. Pakistan Journal of Pharmaceutical Sciences 34: 165–170.
  • Zhang Y, Li Y, Feng Q, Shao M, Yuan F, Liu F. 2020. Polydatin attenuates cadmium-induced oxidative stress via stimulating SOD activity and regulating mitochondrial function in Musca domestica larvae. Chemosphere 248: article 126009. https://doi.org/10.1016/j.chemosphere.2020.126009.
  • Zhang Y, Li Z, Kholodkevich S, Sharov A, Feng Y, Ren N, Sun K. 2019. Cadmium-induced oxidative stress, histopathology, and transcriptome changes in the hepatopancreas of freshwater crayfish (Procambarus clarkii). Science of the Total Environment 666: 944–955. https://doi.org/10.1016/j.scitotenv.2019.02.159.
  • Zhao H, Xu X, Na J, Hao L, Huang L, Li G, Xu Q. 2008. Protective effects of salicylic acid and vitamin C on sulfur dioxide-induced lipid peroxidation in mice. Inhalation Toxicology 20: 865–871. https://doi.org/10.1080/08958370701861512.
  • Zhu Q, Li X, Ge R-S. 2020. Toxicological effects of cadmium on mammalian testis. Frontiers in Genetics 11: article 527. https://doi.org/10.3389/fgene.2020.00527.

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