Evaluation of Respiratory Toxicity Potential of Acrylamide in Zebrafish: Oxidative Stress Parameters, mRNAs Expression, and Histomorphological Changes in Gills

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Authors

  • Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Kamdhenu University, Junagadh - 362001, Gujarat ,IN
  • Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Kamdhenu University, Junagadh - 362001, Gujarat ,IN
  • Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Kamdhenu University, Junagadh - 362001, Gujarat ,IN
  • Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Kamdhenu University, Junagadh - 362001, Gujarat ,IN
  • Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Kamdhenu University, Junagadh - 362001, Gujarat ,IN
  • Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Kamdhenu University, Junagadh - 362001, Gujarat ,IN
  • Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Kamdhenu University, Junagadh - 362001, Gujarat ,IN

DOI:

https://doi.org/10.18311/ti/2024/v31i3/43008

Keywords:

Acrylamide, Gills, Histopathological Changes, mRNA Expression, Oxidative Stress Parameters, Zebrafish

Abstract

Anthropogenic contamination of surface water by chemicals is a worldwide concern, which affects human health and aquatic organisms including fish. Acrylamide (ACR), a Neo-Formed Contaminants (NFC) leads to serious toxic effects on the respiratory system of marine inhabitants. The mechanisms underlying ACR-induced oxidative stress and altered mRNA expressions in zebrafish are unclear. The present investigation aimed to evaluate the effects of ACR exposure for 28 days on the activity or level of antioxidant response elements (ARE), mRNA expressions of antioxidant genes and histomorphological changes in the gills of adult zebrafish. The 270 adult zebrafish were randomly allocated into 03 experimental groups viz. control group, T1 group (ACR: 8.5 mg/L) and T2 group (ACR: 17 mg/L). After 28 days of ACR exposure, Superoxide Dismutase (SOD) activity was significantly (p<0.01) decreased in the gills of zebrafish of the T2 group; and no change in Catalase (CAT) activity was observed in both the treatment groups. The levels of reduced Glutathione (GSH) were significantly (p<0.001) decreased and Malondialdehyde (MDA) were significantly (p<0.001) increased in a concentration-dependent manner. The sod and nuclear factor erythroid 2-related factor 2 (nrf2) mRNA expressions were significantly (p<0.001) downregulated in the gills of zebrafish of both treatment groups. Noticeable histomorphological alterations were recorded in the gills of zebrafish of the T2 group. Alterations in ARE activity, mRNA expressions of antioxidant genes and histopathological findings suggest ACR exposure has been shown to produce oxidative stress-mediated damage in the gills of adult zebrafish.

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Published

2024-08-05

How to Cite

Patel, H. R., Patel, H. B., Paida, B. V., Patel, P. M., Ramchandani, D. M., Patel, U. D., & Modi, C. M. (2024). Evaluation of Respiratory Toxicity Potential of Acrylamide in Zebrafish: Oxidative Stress Parameters, mRNAs Expression, and Histomorphological Changes in Gills. Toxicology International, 31(3), 477–487. https://doi.org/10.18311/ti/2024/v31i3/43008
Received 2024-03-22
Accepted 2024-06-11
Published 2024-08-05

 

References

Zamani E, Shokrzadeh M, Fallah M, Shaki F. A review of acrylamide toxicity and its mechanism. Pharm Biomed Res. 2017; 3(1):1-7. http://pbr.mazums.ac.ir/article-1-146-en.html DOI: https://doi.org/10.18869/acadpub.pbr.3.1.1

Friedman M. Chemistry, biochemistry, and safety of acrylamide: A review. J Agric Food Chem. 2003; 51(16):4504-26. https://doi.org/10.1021/jf030204 DOI: https://doi.org/10.1021/jf030204+

Duan X, Wang QC, Chen KL, Zhu CC, Liu J, Sun SC. Acrylamide toxic effects on mouse oocyte quality and fertility in vivo. Sci Rep. 2015; 5(1):1-11. https://doi.org/10.1038/srep11562 DOI: https://doi.org/10.1038/srep11562

Weston DP, Lentz RD, Cahn MD, Ogle RS, Rothert AK, Lydy MJ. Toxicity of anionic polyacrylamide formulations when used for erosion control in agriculture. J Environ Qual. 2009; 38(1):238-47. https://doi.org/10.2134/jeq2008.0109 DOI: https://doi.org/10.2134/jeq2008.0109

Brown L, Rhead M. Liquid chromatographic determination of acrylamide monomer in natural and polluted aqueous environments. Analyst. 1979; 104(1238):391-99. https://doi.org/10.1039/AN9790400391 DOI: https://doi.org/10.1039/an9790400391

Mucci LA, Wilson KM. Acrylamide intake through diet and human cancer risk. J Agric Food Chem. 2008; 56(15):6013-19. https://doi.org/10.1021/jf703747b DOI: https://doi.org/10.1021/jf703747b

Shamla L, Nisha P. Acrylamide in deep-fried snacks of India. Food Addit Contam. 2014; 7(3):220-25. https://doi.org/10.1080/19393210.2014.894141 DOI: https://doi.org/10.1080/19393210.2014.894141

Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 2013; 496(7446):498-503. DOI: https://doi.org/10.1038/nature12111

Evans DH, Piermarini PM, Choe KP. The multifunctional fish gill: Dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev. 2005; 85:97-177. https://doi.org/10.1152/physrev.00050.2003 DOI: https://doi.org/10.1152/physrev.00050.2003

Wendelaar-Bonga SE. The stress response in fish. Physiol Rev. 1997; 77:591-625. https://doi.org/10.1152/physrev.1997.77.3.591 DOI: https://doi.org/10.1152/physrev.1997.77.3.591

Dybing E, Farmer PB, Andersen M, Fennell TR, Lalljie SPD, Müller DJG, et al. Human exposure and internal dose assessments of acrylamide in food. Food Chem Toxicol. 2005; 43(3):365-410. https://doi.org/10.1016/j.fct.2004.11.004 DOI: https://doi.org/10.1016/j.fct.2004.11.004

Chen W, Shen Y, Su H, Zheng X. Hispidin derived from Phellinuslinteus affords protection against acrylamide-induced oxidative stress in Caco-2 cells. Chem-Biol Interact. 2014; 219:83-9. https://doi.org/10.1016/j.cbi.2014.05.010 DOI: https://doi.org/10.1016/j.cbi.2014.05.010

Hellou J, Ross NW, Moon TW. Glutathione, glutathione S-transferase, and glutathione conjugates, complementary markers of oxidative stress in aquatic biota. Environ Sci Pollut Res. 2012; 19:2007-23. https://doi.org/10.1007/s11356-012-0909-x DOI: https://doi.org/10.1007/s11356-012-0909-x

Ighodaro OM, Akinloye OA. First line defense antioxidants-Superoxide Dismutase (SOD), Catalase (CAT), and Glutathione Peroxidase (GPX): Their fundamental role in the entire antioxidant defense grid. Alex J Med. 2018; 54:287-93. https://doi.org/10.1016/j.ajme.2017.09.001 DOI: https://doi.org/10.1016/j.ajme.2017.09.001

Park JS, Samanta P, Lee S, Lee J, Cho JW, Chun HS, et al. Developmental and neurotoxicity of acrylamide to zebrafish. Int J Mol Sci. 2021; 22(7):3518. https://doi.org/10.3390/ijms22073518 DOI: https://doi.org/10.3390/ijms22073518

Xiuming C, Fei L, Yu F. Toxic effects of acrylamide on zebrafish organs and DNA damage of germ cell. Asian J Chem. 2016; 10(1):382-88.

Sharma C, Kang SC. Garcinol pacifies acrylamide induced cognitive impairments, neuroinflammation and neuronal apoptosis by modulating GSK signaling and activation of pCREB by regulating cathepsin B in the brain of zebrafish larvae. Food Chem Toxicol. 2020; 138:111246. https://doi.org/10.1016/j.fct.2020.111246 DOI: https://doi.org/10.1016/j.fct.2020.111246

Kachot RL, Patel UD, Patel HB, Modi CM, Chauhan R, Kariya MH, et al. Neurotoxicity of acrylamide in adult zebrafish following short-term and long-term exposure: Evaluation of behavior alterations, oxidative stress markers, expression of antioxidant genes, and histological examination of the brain and eyes. Environ Sci Pollut Res. 2023; 30(14):40116-31. https://doi.org/10.1007/s11356-022-25112-z DOI: https://doi.org/10.1007/s11356-022-25112-z

Faria M, Ziv T, Gomez-Canela C, Ben-Lulu S, Prats E, Novoa-Luna KA, et al. Acrylamide acute neurotoxicity in adult zebrafish. Scient Rep. 2018; 8(1):1-14. https://doi.org/10.1038/s41598-018-26343-2 DOI: https://doi.org/10.1038/s41598-018-26343-2

Wilson JM, Bunte RM, Carty AJ. Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). J Am Assoc Lab Anim Sci. 2009; 48(6):785-89.

Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 1974; 47(3):469-74. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x DOI: https://doi.org/10.1111/j.1432-1033.1974.tb03714.x

Sinha AK. Colorimetric assay of catalase. Anal Biochem. 1972; 47(2):389-94. https://doi.org/10.1016/0003-2697(72)90132-7 DOI: https://doi.org/10.1016/0003-2697(72)90132-7

Ellman G. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959; 82(1):70-7. https://doi.org/10.1016/0003-9861(59)90090-6 DOI: https://doi.org/10.1016/0003-9861(59)90090-6

Lykkesfeldt J. Determination of malondialdehyde as dithiobarbituric acid adduct in biological samples by HPLC with fluorescence detection: comparison with ultraviolet-visible spectrophotometry. Clin Chem. 2001; 47(9):1725-27. https://doi.org/10.1093/clinchem/47.9.1725 DOI: https://doi.org/10.1093/clinchem/47.9.1725

Sambrook L, Russell RW. Molecular cloning: A laboratory, 3rd ed. Cold Spring Laboratory Press. Cold spring harbor, New York; 2001.

Sarkar S, Mukherjee S, Chattopadhyay A, Bhattacharya S. Low dose of arsenic trioxide triggers oxidative stress in zebrafish brain: Expression of antioxidant genes. Ecotoxicol Environ Saf. 2014; 107:1-8. https://doi.org/10.1016/j.ecoenv.2014.05.012 DOI: https://doi.org/10.1016/j.ecoenv.2014.05.012

Jaramillo ML, Pereira AG, Davico CE, Nezzi L, Ammar D, Müller YMR, et al. Evaluation of reference genes for reverse transcription-quantitative PCR assays in organs of zebrafish exposed to glyphosate-based herbicide, Roundup. Animal. 2018; 12(7):1424-34. https://doi.org/10.1017/S1751731117003111 DOI: https://doi.org/10.1017/S1751731117003111

Velasques RR, Sandrini JZ, da Rosa CE. Roundup® in zebrafish: Effects on oxidative status and gene expression. Zebrafish. 2016; 13(5):432-41. https://doi.org/10.1089/zeb.2016.1259 DOI: https://doi.org/10.1089/zeb.2016.1259

Bautista FEA, Junior ASV, Corcini CD, Acosta IB, Caldas SS, Primel EG, et al. The herbicide atrazine affects sperm quality and the expression of antioxidant and spermatogenesis genes in zebrafish testes. Comp Biochem Physiol C Toxicol Pharmacol. 2018; 206:17-22. https://doi.org/10.1016/j.cbpc.2018.02.003 DOI: https://doi.org/10.1016/j.cbpc.2018.02.003

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative pcr and the 2-δδct method. Methods. 2001; 25(4):402-8. https://doi.org/10.1006/meth.2001.1262 DOI: https://doi.org/10.1006/meth.2001.1262

Luna LG. Routine staining procedures: Hematoxylin and eosin stains. Manual of histologic staining methods of the armed forces institute of pathology, 3rd ed. McGraw-Hill, New York; 1968. p. 32-9.

Bhattacharya S, Bhattacharya A, Roy S. Arsenic induced responses in fresh water teleosts. Fish Physiol Biochem. 2007; 33(4):463-73. https://doi.org/10.1007/s10695-007-9173-2 DOI: https://doi.org/10.1007/s10695-007-9173-2

Cao C, Leng Y, Liu X, Yi YP, Li P, Kufe D. Catalase is regulated by ubiquitination and proteosomal degradation. Role of the c-Abl and Arg tyrosine kinases. Biochem. 2003; 42(35):10348-53. https://doi.org/10.1021/bi035023f DOI: https://doi.org/10.1021/bi035023f

Liu Y, Wang J, Wei Y, Zhang H, Xu M, Dai J. Induction of time-dependent oxidative stress and related transcriptional effects of perfluorododecanoic acid in zebrafish liver. Aquat Toxicol. 2008; 89(4):242-50. https://doi.org/10.1016/j.aquatox.2008.07.009 DOI: https://doi.org/10.1016/j.aquatox.2008.07.009

Di Giulio R, Meyer J. Reactive oxygen species and oxidative stress. The Toxicology of Fishes; 2008. p. 273-324. DOI: https://doi.org/10.1201/9780203647295.ch6

Cong B, Liu C, Wang L, Chai Y. The impact on antioxidant enzyme activity and related gene expression following adult zebrafish (Danio rerio) exposure to dimethyl phthalate. Animals. 2020; 10(717):1-12. https://doi.org/10.3390/ani10040717 DOI: https://doi.org/10.3390/ani10040717

Bhattacharya A, Bhattacharya S. Induction of oxidative stress by arsenic in Clarias batrachus: Involvement of peroxisomes. Ecotoxicol Environ Saf. 2007; 66(2):178-87. https://doi.org/10.1016/j.ecoenv.2005.11.002 DOI: https://doi.org/10.1016/j.ecoenv.2005.11.002

Saez GT, Bannister WH, Bannister JV. Free radicals and thiol compounds. The role of glutathione against free radical toxicity. In: Vina J, editors, Glutathione: Metabolism and physiological functions. CRC Press, Boca Raton, Fl, USA; 1990. p. 237-54.

Larguinho M, Cordeiro A, Diniz MS, Costa PM, Baptista PV. Metabolic and histopathological alterations in the marine bivalve Mytilus galloprovincialis induced by chronic exposure to acrylamide. Environ Res. 2014; 135:55-62. https://doi.org/10.1016/j.envres.2014.09.004 DOI: https://doi.org/10.1016/j.envres.2014.09.004

Radwan MA, El-Gendy KS, Gad AF, Khamis AE, Eshra ESH. Ecotoxicological biomarkers as investigating tools to evaluate the impact of acrylamide on Thebapisana snails. Environ Sci Pollut Res. 2019; 26(14):14184-93. https://doi.org/10.1007/s11356-019-04784-0 DOI: https://doi.org/10.1007/s11356-019-04784-0

Albalawi A, Alhasani RHA, Biswas L, Reilly J, Akhtar S, Shu X. Carnosic acid attenuates ACR-induced retinal toxicity in zebrafish embryos. Exp Eye Res. 2018; 175:103-14. https://doi.org/10.1016/j.exer.2018.06.018 DOI: https://doi.org/10.1016/j.exer.2018.06.018

Trabelsi W, Chetoui I, Fouzai C, Bejaoui S, Rabeh I, Telahigue K, et al. Redox status and fatty acid composition of Mactracorallina digestive gland following exposure to acrylamide. Environ Sci Pollut Res. 2019; 26(22):22197-208. https://doi.org/10.1007/s11356-019-05492-5 DOI: https://doi.org/10.1007/s11356-019-05492-5

Acaroz U, Ince S, Arslan-Acaroz D, Gurler Z, Kucukkurt I, Demirel HH, et al. The ameliorative effects of boron against acrylamide-induced oxidative stress, inflammatory response, and metabolic changes in rats. Food Chem Toxicol. 2018; 118:745-52. https://doi.org/10.1016/j.fct.2018.06.029 DOI: https://doi.org/10.1016/j.fct.2018.06.029

Santhrani T, Vineela S, Devi CM. Neuroprotective effect of naringin on acrylamide induced cytotoxicity in U87MG cells and Wistar rats: An in-vitro and in-vivo study. Toxicol Int. 2021; 28(1):49-56. DOI: https://doi.org/10.18311/ti/2021/v28i1/26267

Morrow JD, Frei B, Longmire AW, Gaziano JM, Lynch SM, Shyr Y, et al. Increase in circulating products of lipid peroxidation (F2-isoprostanes) in smokers-smoking as a cause of oxidative damage. New Engl J Med. 1995; 332(18):1198-203. https://www.nejm.org/doi/full/10.1056/ NEJM199505043321804 DOI: https://doi.org/10.1056/NEJM199505043321804

Banerjee BD, Seth V, Bhattacharya A, Pasha ST, Chakraborty AK. Biochemical effects of some pesticides on lipid peroxidation and free-radical scavengers. Toxicol Lett. 1999; 107(1-3):33-47. https://doi.org/10.1016/S0378-4274 (99)00029-6 DOI: https://doi.org/10.1016/S0378-4274(99)00029-6

Abd-Elkareem M, Khalil NSA, Sayed AH. Hepatotoxic responses of 4-nonylphenol on African catfish (Clarias gariepinus): Antioxidant and histochemical biomarkers. Fish Physiol Biochem 2018; 44(3):969-81. https://doi.org/10.1007/s10695-018-0485-1 DOI: https://doi.org/10.1007/s10695-018-0485-1

Aydogan M, Korkmaz A, Barlas N, Kolankaya D. The effect of Vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats. Toxicology. 2008; 249(1):35-9. https://doi.org/10.1016/j.tox.2008.04.002 DOI: https://doi.org/10.1016/j.tox.2008.04.002

Mohamed WA, El-Houseiny W, Ibrahim RE, Abd-Elhakim YM. Palliative effects of zinc sulfate against the immunosuppressive, hepato-and nephrotoxic impacts of nonylphenol in Nile tilapia (Oreochromis niloticus). Aquaculture. 2019; 504:227-38. https://doi.org/10.1016/j.aquaculture.2019.02.004 DOI: https://doi.org/10.1016/j.aquaculture.2019.02.004

Wu M, Xu H, Shen Y, Qiu W, Yang M. Oxidative stress in zebrafish embryos induced by short-term exposure to bisphenol A, nonylphenol, and their mixture. Environ Toxicol Chem. 2011; 30(10):2335-41. https://doi.org/10.1002/etc.634 DOI: https://doi.org/10.1002/etc.634

Osburn WO, Kensler TW. nrf2 signaling: An adaptive response pathway for protection against environmental toxic insults. Mutat Res-Rev Mutat Res. 2008; 659(1-2):31-9. https://doi.org/10.1016/j.mrrev.2007.11.006 DOI: https://doi.org/10.1016/j.mrrev.2007.11.006

Sporn MB, Liby KT. nrf2 and cancer: The good, the bad and the importance of context. Nat Rev Cancer. 2012; 12(8):564-71. https://doi.org/10.1038/nrc3278 DOI: https://doi.org/10.1038/nrc3278

Dai G, Vaughn S, Zhang Y, Wang ET, Garcia-Cardena G, Gimbrone Jr MA. Biomechanical forces in atherosclerosis-resistant vascular regions regulate endothelial redox balance via phosphoinositol 3-kinase/Akt-dependent activation of Nrf2. Circ Res. 2007; 101(7):723-33. https://doi.org/10.1161/CIRCRESAHA.107.152942 DOI: https://doi.org/10.1161/CIRCRESAHA.107.152942

Kobayashi S, Ishimaru M, Hiraoka K, Honda C. Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta. 2002; 215(6):924-33. https://doi.org/10.1007/s00425-002-0830-5 DOI: https://doi.org/10.1007/s00425-002-0830-5

Kobayashi M, Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal. 2005; 7(3-4):385-94. https://doi.org/10.1089/ars.2005.7.385 DOI: https://doi.org/10.1089/ars.2005.7.385

Petersen DW, Cooper KR, Friedman MA, Lech JJ. Behavioral and histological effects of acrylamide in rainbow trout. Toxicol Appl Pharmacol. 1987; 87(1):177-84. https://doi.org/10.1016/0041-008X(87)90095-0 DOI: https://doi.org/10.1016/0041-008X(87)90095-0

Kilicle PA, Evren KOÇ, Dogan A, Süleyman GUL, Doğan ANC, Ersan Y. Investigation of the effect of acrylamide on Capoeta Capoeta (Guldensttead 1773) by histopathological, electrophoretic and biochemical methods. Caucasian J Sci. 2020; 7(2):153-66. https://doi.org/10.48138/cjo.836674 DOI: https://doi.org/10.48138/cjo.836674