Acute exposure of glyphosate-based herbicide induced damages on common carp organs via heat shock proteins-related immune response and oxidative stress

References

• Amar, E.C., Kiron, V., and Satoh, S., 2004. Enhancement of innate immunity in rainbow trout (Oncorhynchus mykiss Walbaum) associated with dietary intake of carotenoids from natural products. Fish shellfish immunity, 16 (4), 527–537.
   PubMed Web of Science ®Google Scholar
• Awad, E., Mitchell, W.J., and Austin, B., 2011. Effect of dietary supplements on cytokine gene expression in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of fish diseases, 34 (8), 629–634.
   PubMed Web of Science ®Google Scholar
• Basu, N., et al., 2002. Heat shock protein genes and their functional significance in fish. Gene, 295 (2), 173–183.
   PubMed Web of Science ®Google Scholar
• Bhargav, D., et al., 2008. Toxic potential of municipal solid waste leachates in transgenic Drosophila melanogaster (hsp70-lacZ): hsp70 as a marker of cellular damage. Ecotoxicology and environmental saftey, 69 (2), 233–245.
   PubMed Web of Science ®Google Scholar
• Biswas, G., et al., 2012. Cytokine responses in the common carp, Cyprinus carpio L. treated with baker's yeast extract. Aquaculture, 356–357, 169–175.
   Web of Science ®Google Scholar
• Black, P.H., 2002. Stress and the inflammatory response: a review of neurogenic inflammation. Journal of brain behaviour and immunity, 116, 622–653.
   Google Scholar
• Botta, F., et al., 2009. Transfer of glyphosate and its degradate AMPA to surface waters through urban sewerage systems. Chemosphere, 77 (1), 133–139.
   PubMed Web of Science ®Google Scholar
• Brewster, D.W., Warren, J.A., and Hopkins, I.I.W., 1991. Metabolism of glyphosate in Sprague–Dawley rats: tissue distribution, identification, and quantitation of glyphosate-derived materials following a single oral dose. Fundamental and applied toxicology, 17 (1), 43–51.
   PubMedGoogle Scholar
• Bustin, S.A., et al., 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical chemistry, 55 (4), 611–622.
   PubMed Web of Science ®Google Scholar
• Campisi, J., Leem, T.H., and Fleshner, M., 2003. Stress-induced extracellular Hsp72 is a functionally significant danger signal to the immune system. Cell stress and chaperones, 8 (3), 272–286.
   PubMed Web of Science ®Google Scholar
• Cao, H., et al., 2016. Alterations in trace element levels and mRNA expression of Hsps and inflammatory cytokines in livers of duck exposed to molybdenum or/and cadmium. Ecotoxicology and environmental safety, 125, 93–101.
   PubMed Web of Science ®Google Scholar
• Çavaş, T., and Könen, S., 2007. Detection of cytogenetic and DNA damage in peripheral erythrocytes of goldfish (Carassius auratus) exposed to a glyphosate formulation using the micronucleus test and the comet assay. Mutagenesis, 22 (4), 263–268.
   PubMed Web of Science ®Google Scholar
• Chen, C.C., and Manning, A.M., 1996. TGF-β1, IL-10 and IL-4 differentially modulate the cytokine-induced expression of IL-6 and IL-8 in human endothelial cells. Cytokine, 8 (1), 58–65.
   PubMed Web of Science ®Google Scholar
• de Moura, F.R., et al., 2017. Oxidative stress in the hybrid fish jundiara (Leiarius marmoratus × Pseudoplatystoma reticulatum) exposed to Roundup Original®. Chemosphere, 185, 445–451.
   PubMed Web of Science ®Google Scholar
• Draper, H.H., and Hadley, M., 1990. Malondialdehyde determination as index of lipid peroxidation. Methods in enzymology, 186, 421–431.
   PubMed Web of Science ®Google Scholar
• Eder, K.J., et al., 2009. Effects of neurotoxic insecticides on heat-shock proteins and cytokine transcription in Chinook salmon (Oncorhynchus tshawytscha). Ecotoxicology and environmental safety, 72 (1), 182–190.
   PubMed Web of Science ®Google Scholar
• Giesy, J.P., Dobson, S., and Solomon, K.R., 2000. Ecotoxicological risk assessment for roundup herbicide. Reviews of environmental contamination and toxicology, 167, 35–120.
   Web of Science ®Google Scholar
• Guilherme, S., et al., 2012. Differential genotoxicity of Roundup(®) formulation and its constituents in blood cells of fish (Anguilla anguilla): considerations on chemical interactions and DNA damaging mechanisms. Ecotoxicology (London, England), 21 (5), 1381–1390.
   PubMed Web of Science ®Google Scholar
• Heikkila, J.J., 2010. Heat shock protein gene expression and function in amphibian model systems. Comparative biochemistry and physiology. part a, molecular and integrative physiology, 156 (1), 19–33.
   PubMed Web of Science ®Google Scholar
• Hemalatha, D., et al., 2016. Sublethal toxicity of quinalphos on oxidative stress and antioxidant responses in a freshwater fish Cyprinus carpio. Environmental toxicology, 31 (11), 1399–1406.
   PubMed Web of Science ®Google Scholar
• Huang, C.F., et al., 2008. The immunopharmaceutical effects and mechanisms of herb medicine. Cellular and molecular immunology, 5 (1), 23–31.
   PubMed Web of Science ®Google Scholar
• Jiang, J., et al., 2015. In vitro and in vivo protective effect of arginine against lipopolysaccharide induced inflammatory response in the intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Fish and shellfish immunology, 42 (2), 457–464.
   PubMed Web of Science ®Google Scholar
• Jing, J., et al., 2013. Acute effect of copper and cadmium exposure on the expression of heat shock protein 70 in the Cyprinidae fish Tanichthys albonubes. Chemosphere, 91 (8), 1113–1122.
   PubMed Web of Science ®Google Scholar
• Kakkar, V., et al., 2014. Barcoding heat shock proteins to human diseases: looking beyond the heat shock response. Disease models and mechanisms, 7 (4), 421–434.
   PubMed Web of Science ®Google Scholar
• Kärber, G., 1931. Beitrag zur kollektiven behandlung pharmakologischer reihenversuche. Naunyn-Schmiedebergs archiv für experimentelle pathologie und pharmakologie, 162 (4), 480–483.
   Google Scholar
• Koller, V.J., et al., 2012. Cytotoxic and DNA-damaging properties of glyphosate and Roundup in human-derived buccal epithelial cells. Archives of toxicology, 86 (5), 805–813.
   PubMed Web of Science ®Google Scholar
• Kondera, E., et al., 2018. Effect of glyphosate-based herbicide on hematological and hemopoietic parameters in common carp (Cyprinus carpio L). Fish physiology and biochemistry, 44 (3), 1011–1018.
   PubMed Web of Science ®Google Scholar
• Kreutz, L.C., et al., 2011. Altered hematological and immunological parameters in silver catfish (Rhamdia quelen) following short term exposure to sublethal concentration of glyphosate. Fish shellfish immunity, 30 (1), 51–57.
   PubMed Web of Science ®Google Scholar
• Kreutz, L.C., et al., 2010. Exposure to sublethal concentration of glyphosate or atrazine-based herbicides alters the phagocytic function and increases the susceptibility of silver catfish fingerlings (Rhamdia quelen) to Aeromonas hydrophila challenge. Fish and shellfish immunology, 29 (4), 694–697.
   PubMed Web of Science ®Google Scholar
• Li, X.Y., et al., 2012. Acute toxicity and responses of antioxidant systems to 1-methyl-3-octylimidazolium bromide at different developmental stages of goldfish. Ecotoxicology (London, England), 21 (1), 253–259.
   PubMed Web of Science ®Google Scholar
• Livak, K.J., and Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 −△△Ct method. Methods (San Diego, California), 25 (4), 402–408.
   PubMed Web of Science ®Google Scholar
• Lindquist, S., and Craig, E.A., 1988. The heat-shock proteins. Annual review of genetics, 22, 631–677.
   PubMed Web of Science ®Google Scholar
• Lowry, O.H., et al., 1951. Protein measurement with the Folin phenol reagent. Journal of biological chemistry, 193, 265–275.
   PubMed Web of Science ®Google Scholar
• Ma, J., et al., 2014. Biochemical responses to the toxicity of the biocide abamectin on the freshwater snail Physa acuta. Ecotoxicology and environmental saftey, 101, 31–35.
   PubMed Web of Science ®Google Scholar
• Ma, J., and Li, X., 2015. Alteration in the cytokine levels and histopathological damage in common carp induced by glyphosate. Chemosphere, 128, 293–298.
   PubMed Web of Science ®Google Scholar
• Ma, J., et al., 2015. Effects of chlorpyrifos on the transcription of CYP3A cDNA, activity of acetylcholinesterase, and oxidative stress response of goldfish (Carassius auratus). Environmental toxicology, 30 (4), 422–429.
   PubMed Web of Science ®Google Scholar
• Ma, J., et al., 2017. Altered cellular metabolism of HepG2 cells caused by microcystin-LR. Environmental pollution (Barking, Essex: 1987), 225, 610–619.
   PubMed Web of Science ®Google Scholar
• Ma, J., et al., 2018a. Hepatotoxicity of paraquat on common carp (Cyprinus carpio L.). Science and total environment, 616, 889–898.
   PubMed Web of Science ®Google Scholar
• Ma, J., et al., 2018b. Serum immune responses in common carp (Cyprinus carpio L.) to paraquat exposure: the traditional parameters and circulating microRNAs. Fish shellfish immunity, 76, 133–142.
   PubMed Web of Science ®Google Scholar
• Martin, J.E., et al., 1991. Expression of heat shock protein epitopes in tubular aggregates. Muscle and nerve, 14 (3), 219–225.
   PubMed Web of Science ®Google Scholar
• Ming, J.H., et al., 2010. Molecular cloning and expression of two HSP70 genes in the Wuchang bream (Megalobrama amblycephala Yih). Fish shellfish immunity, 28 (3), 407–418.
   PubMed Web of Science ®Google Scholar
• Modesto, K.A., and Martinez, C.B., 2010. Roundup® causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus. Chemosphere, 78 (3), 294–299.
   PubMed Web of Science ®Google Scholar
• Modesto, K.A., and Martinez, C.B., 2010. Effects of roundup transorb on fish: hematology, antioxidant defenses and acetylcholinesterase activity. Chemosphere, 81 (6), 781–787.
   PubMed Web of Science ®Google Scholar
• Montgomery, J.H., 1993. Agrochemical desk reference: environmental data. Chelsea, MI: Lewis, 625.
   Google Scholar
• Mottier, A., et al., 2013. Effects of glyphosate-based herbicides on embryo-larval development and metamorphosis in the Pacific oyster, Crassostrea gigas. Aquatic toxicology, 128–129, 67–78.
   PubMed Web of Science ®Google Scholar
• Mrdaković, M., et al., 2016. Acetylcholinesterase (AChE) and heat shock proteins (Hsp70) of gypsy moth (Lymantria dispar L.) larvae in response to long-term fluoranthene exposure. Chemosphere, 159, 565–569.
   PubMed Web of Science ®Google Scholar
• Nazir, A., Saxena, D., and Kar, C.D., 2003. Induction of hsp70 in transgenic Drosophila: biomarker of exposure against phthalimide group of chemicals. Journal of biochimica et biophysica acta, 1621 (2), 218–225.
   PubMed Web of Science ®Google Scholar
• Nootash, S., et al., 2013. Green tea (Camellia sinensis) administration induces expression of immune relevant genes and biochemical parameters in rainbow trout (Oncorhynchus mykiss). Fish shellfish immunity, 35 (6), 1916–1923.
   PubMed Web of Science ®Google Scholar
• Nwani, C.D., et al., 2013. DNA damage and oxidative stress modulatory effects of glyphosate-based herbicide in freshwater fish, Channa punctatus. Environmental toxicology and pharmacology, 36 (2), 539–547.
   PubMed Web of Science ®Google Scholar
• OECD, 1984. Guideline for testing of chemicals no. 204. Fish, prolonged toxicity test: 14-day study. Paris: Organization for Economic Co-operation and Development.
   Google Scholar
• Paganelli, A., et al., 2010. Glyphosate-based herbicides produce teratogenic effects on vertebrates by impairing retinoic acid signaling. Chemical research in toxicology, 23 (10), 1586–1595.
   PubMed Web of Science ®Google Scholar
• Papadakis, K.A., and Targan, S.R., 2000. Role of cytokines in the pathogenesis of inflammatory bowel disease. Annual review of medicine, 51, 289–298.
   PubMed Web of Science ®Google Scholar
• Peng, J., Jones, G.L., and Watson, K., 2000. Stress proteins as biomarkers of oxidative stress: effects of antioxidant supplements. Free radical biology and medicine, 28 (11), 1598–1606.
   PubMed Web of Science ®Google Scholar
• Puértolas, L., et al., 2010. Evaluation of side-effects of glyphosate mediated control of giant reed (Arundo donax) on the structure and function of a nearby Mediterranean river ecosystem. Environmental research, 110 (6), 556–564.
   PubMed Web of Science ®Google Scholar
• Sambrook, J., and Russel, D.V., 2001. Molecular cloning: a laboratory manual. Vol. 1, 3rd ed. New York: Cold Spring Harbor Laboratory, 13–17.
   Google Scholar
• Savan, R., and Sakai, M., 2004. Presence of multiple isoforms of TNF alpha in carp (Cyprinus carpio L.): genomic and expression analysis. Fish shellfish immunity, 17 (1), 87–94.
   PubMed Web of Science ®Google Scholar
• Sørensen, J.G., Kristensen, T.N., and Loeschcke, V., 2003. The evolutionary and ecological role of heat shock proteins. Ecology letters, 6 (11), 1025–1037.
   Web of Science ®Google Scholar
• Snyder, M.J., Girvetz, E., and Mulder, E.P., 2001. Induction of marine mollusc stress proteins by chemical or physical stress. Archives of environmental contamination and toxicology, 41 (1), 22–29.
   PubMed Web of Science ®Google Scholar
• Srivastava, P., 2002. Roles of heat-shock proteins in innate and adaptive immunity. Nature reviews: immunology, 2 (3), 185–194.
   PubMed Web of Science ®Google Scholar
• Vereecken, H., 2005. Mobility and leaching of glyphosate: a review. Pest management science, 61 (12), 1139–1151.
   PubMed Web of Science ®Google Scholar
• Williams, G.M., Kroes, R., and Munro, I.C., 2000. Safety evaluation and risk assessment of the herbicide Roundup and its active ingredient, glyphosate, for humans. Regulatory toxicology and pharmacology, 31 (2), 117–165.
   PubMed Web of Science ®Google Scholar
• Xing, H.J., et al., 2013. Effects of atrazine and chlorpyrifos on the mRNA levels of HSP70 and HSC70 in the liver, brain, kidney and gill of common carp (Cyprinus carpio L.). Chemosphere, 90 (3), 910–916.
   PubMed Web of Science ®Google Scholar
• Yuan, C.T., et al., 2008. Effects of Astragalus polysaccharides (APS) on the expression of immune response genes in head kidney, gill and spleen of the common carp, Cyprinus carpio L. International Immunopharmacology, 8 (1), 51–58.
   PubMed Web of Science ®Google Scholar
• Zou, J., and Secombes, C.J., 2011. Teleost fish interferons and their role in immunity. Developmental and comparative immunology, 35 (12), 1376–1387.
   PubMed Web of Science ®Google Scholar