[en] Glyphosate-based herbicides (GBH), including Roundup®, are the most used herbicides in agricultural and nonagricultural areas, which can reach aquatic environments through drift during application or surface runoff. Some studies, mostly in fish, demonstrated that GBH caused oxidative stress in non-target animals. However, only few information is available on the GBH effects in the antioxidant and stress proteins of many other organisms, such as freshwater crustaceans. Thus, we aimed to investigate the effects of environmentally relevant GBH concentrations on the relative transcript expression (RTE) of the superoxide dismutase (sod1), catalase (cat), selenium-dependent glutathione peroxidase (gpx), glutathione-S-transferase (gst), thioredoxin (txn), heat shock protein (hsp70 and hsp90) in the hepatopancreas of the ecologically important freshwater prawn Macrobrachium potiuna. Moreover, this study aimed to assess the gender-differences responses to GBH exposure. Male and female prawns were exposed to three Roundup WG® concentrations (0.0065, 0.065 and 0.28 mg of glyphosate/L) and a control group (0.0 mg/L) for 7 and 14 days. In general, males had an under-expression of the studied genes, indicating an oxidative stress and possible accumulation of ROS in the hepatopancreas. In the opposite, females had an overexpression of the same genes, indicating a more robust antioxidant system, in order to cope with the possible ROS increase after Roundup WG® exposure. Therefore, results confirmed that gender could be a confounding factor in ecotoxicological assessment of GBH effects. Additionally, this work highlights that sod1, cat, gpx, gst, txn, hsp70 and hsp90 gene expressions seem to be useful biomarkers to investigate the oxidative stress caused by Roundup WG® in Macrobrachium sp.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Disciplines :
Environmental sciences & ecology
Author, co-author :
de Melo, Madson
Nazari, Evelise Maria
Muller, Yara Maria Rauh
Gismondi, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie animale et écotoxicologie
Language :
English
Title :
Modulation of antioxidant gene expressions by Roundup® exposure in the decapod Macrobrachium potiuna
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Addinsoft, XLSTAT Statistical and Data Analysis Solution. 2019, France, Paris https://www.xlstat.com.
Aguirre, J., Ríos-Momberg, M., Hewitt, D., Hansberg, W., Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol. 13 (2005), 111–118, 10.1016/j.tim.2005.01.007.
Annett, R., Habibi, H.R., Hontela, A., Impact of glyphosate and glyphosate-based herbicides on the freshwater environment. J. Appl. Toxicol. 34 (2014), 458–479, 10.1002/jat.2997.
Arnér, E.S.J., Holmgren, A., Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267 (2000), 6102–6109, 10.1046/j.1432-1327.2000.01701.x.
Arun, S., Subramanian, P., Antioxidant enzymes in freshwater prawn Macrobrachium malcolmsonii during embryonic and larval development. Comp. Biochem. Physiol., B 121 (1998), 273–277, 10.1016/S0305-0491(98)10100-1.
Avigliano, E., Schenone, N.F., Human health risk assessment and environmental distribution of trace elements, glyphosate, fecal coliform and total coliform in Atlantic Rainforest mountain rivers (South America). Microchem. J. 122 (2015), 149–158, 10.1016/j.microc.2015.05.004.
Baler, R., Dahl, G., Voellmy, R., Activation of human heat shock genes is accompanied by oligomerization, modification, and rapid translocation of heat shock transcription factor HSF1. Mol. Cell. Biol. 13 (1993), 2486–2496, 10.1128/mcb.13.4.2486.
Barata, C., Varo, I., Navarro, J.C., Arun, S., Porte, C., Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp. Biochem. Physiol., C 140 (2005), 175–186, 10.1016/j.cca.2005.01.013.
Benbrook, C.M., Trends in glyphosate herbicide use in the United States and globally. Environ. Sci. Eur., 28, 2016, 15, 10.1186/s12302-016-0070-0.
Benbrook, C.M., How did the US EPA and IARC reach diametrically opposed conclusions on the genotoxicity of glyphosate-based herbicides?. Environ. Sci. Eur. 31 (2019), 1–16, 10.1186/s12302-018-0184-7.
Bhavan, P.S., Geraldine, P., Biochemical stress responses in tissues of the prawn Macrobrachium malcolmsonii on exposure to endosulfan. Pestic. Biochem. Physiol. 70 (2001), 27–41, 10.1006/pest.2001.2531.
Boorstein, W.R., Ziegelhoffer, T., Craig, E.A., Molecular evolution of the HSP70 multigene family. J. Mol. Evol. 38 (1994), 1–17, 10.1007/BF00175490.
Brot, N., Weissbach, H., The biochemistry of methionine sulfoxide residues in proteins. Trends Biochem. Sci. 7 (1982), 137–139, 10.1016/0968-0004(82)90204-3.
Bukau, B., Weissman, J., Horwich, A., Molecular chaperones and protein quality Control. Cell 125 (2006), 443–451, 10.1016/j.cell.2006.04.014.
Chae, H.Z., Kang, S.W., Kirn, H.J., Kirn, K., Baines, I.C., Rhee, S.G., Characterization of three isoforms of mammalian peroxiredoxin that reduce peroxides in the presence of thioredoxin. Diabetes Res. Clin. Pract. 45 (1999), 101–112.
Csshang, C.C., Lee, P.P., Chun, H.L., Cheng, W., Trichlorfon, an organophosphorus insecticide, depresses the immune responses and resistance to Lactococcus garvieae of the giant freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immunol. 20 (2006), 574–585, 10.1016/j.fsi.2005.06.012.
Chaurasia, M.K., Nizam, F., Ravichandran, G., Arasu, M.V., Al-dhabi, N.A., Arshad, A., Elumalai, P., Arockiaraj, J., Molecular importance of prawn large heat shock proteins 60, 70 and 90. Fish Shellfish Immunol. 48 (2016), 228–238, 10.1016/j.fsi.2015.11.034.
Chen, Y.N., Tseng, D.Y., Ho, P.Y., Kuo, C.M., Site of vitellogenin synthesis determined from a cDNA encoding a vitellogenin fragment in the freshwater giant prawn, Macrobrachium rosenbergii. Mol. Reprod. Dev. 54 (1999), 215–222.
CONAMA, Conselho nacional do Meio Ambiente. Resolução número 357, 03/04/2018. Available in: http://www.mma.gov.br/port/conama/legiabre.cfm?codlegi-459, 2005.
Conrad, A., Schröter-Kermani, C., Hoppe, H.W., Rüther, M., Pieper, S., Kolossa-Gehring, M., Glyphosate in German adults – time trend (2001 to 2015) of human exposure to a widely used herbicide. Int. J. Hyg Environ. Health 220 (2017), 8–16, 10.1016/j.ijheh.2016.09.016.
CoreTeam, R Development, R: A Language and Environment for Statistical Computing. 2011, R foun- dation for Statistical Computing, Vienna, Austria available online at: http://www.R-project.org/.
de Melo, Silveira, Madson, Nazari, E.M., Joaquim-Justo, C., Muller, Y.M.R., Gismondi, E., Effects of low glyphosate-based herbicide concentrations on endocrine-related gene expression in the decapoda Macrobrachium potiuna. Environ. Sci. Pollut. Res. 26 (2019), 21535–21545, 10.1007/s11356-019-05496-1.
de Melo, M.S., dos Santos, T.P.G., Jaramillo, M., Nezzi, L., Rauh Muller, Y.M., Nazari, E.M., Histopathological and ultrastructural indices for the assessment of glyphosate-based herbicide cytotoxicity in decapod crustacean hepatopancreas. Aquat. Toxicol. 210 (2019), 207–214, 10.1016/j.aquatox.2019.03.007.
Dupont-Prinet, A., Pillet, M., Chabot, D., Hansen, T., Tremblay, R., Audet, C., Northern shrimp (Pandalus borealis) oxygen consumption and metabolic enzyme activities are severely constrained by hypoxia in the Estuary and Gulf of St. Lawrence. J. Exp. Mar. Biol. Ecol. 448 (2013), 298–307, 10.1016/j.jembe.2013.07.019.
Freire, R., Schneider, R.M., Freitas, F.H. De, Bonifácio, C.M., Tavares, C.R.G., Monitoring of toxic chemical in the basin of Maringá stream. Acta Sci. Technol. 34 (2012), 295–302, 10.4025/actascitechnol.v34i3.10302.
Fridovich, I., Superoxide radical and superoxide dismutase. Annu. Rev. Biochem. 64 (1995), 97–112, 10.1021/ar50058a001.
Frova, C., Glutathione transferases in the genomics era: new insights and perspectives. Biomol. Eng. 23 (2006), 149–169, 10.1016/j.bioeng.2006.05.020.
Gasnier, C., Dumont, C., Benachour, N., Clair, E., Chagnon, M., Séralini, G., Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines. Toxicology 262 (2009), 184–191, 10.1016/j.tox.2009.06.006.
Gismondi, E., Cossu-Leguille, C., Beisel, J., Do male and female gammarids defend themselves differently during chemical stress?. Aquat. Toxicol. 140–141 (2013), 432–438, 10.1016/j.aquatox.2013.07.006.
Gismondi, E., Mazzucchelli, G., De Pauw, E., Joaquim-Justo, C., Thomé, J.P., Gender differences in responses in Gammarus pulex exposed to BDE-47: a gel-free proteomic approach. Ecotoxicol. Environ. Saf. 122 (2015), 205–213.
Gunarathna, S., Gunawardana, B., Jayaweera, M., Zoysa, K., Glyphosate and AMPA of agricultural soil, surface water, groundwater and sediments in areas prevalent with chronic kidney disease of unknown etiology, Sri Lanka. J. Environ. Sci. Heal. Part B, 2018, 1–9, 10.1080/03601234.2018.1480157 0.
Halliwell, B., Free radicals, antioxidants, and human disease: curiosity, cause, or consequence?. Lancet 344 (1994), 721–724.
Halliwell, B., Gutteridge, J.M.C., Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem. J. 219 (1984), 1–14, 10.1042/bj2190001.
Hansen, B.H., Altin, D., Vang, S.H., Nordtug, T., Olsen, A.J., Effects of naphthalene on gene transcription in Calanus finmarchicus (Crustacea: copepoda). Aquat. Toxicol. 86 (2008), 157–165, 10.1016/j.aquatox.2007.10.009.
Hartl, F.U., Molecular chaperones in cellular protein folding. Nature 13 (1996), 571–580.
Hassouni, M. El, Chambost, J.P., Expert, D., Gijsegem, F. Van, Barras, F., The minimal gene set member msrA, encoding peptide methionine sulfoxide reductase, ia s virulence determinant of the plant pathogen Erwinia chrysanthemi. Proc. Natl. Acad. Sci. 96 (1999), 887–892.
Hightower, L.E., Cultured animal cells exposed to amino acid analogues or puromycin rapidly synthesize several polypeptides. J. Cell. Physiol. 102 (1980), 407–427, 10.1002/jcp.1041020315.
Holmgren, A., Enzymatic reduction-oxidation of protein disulfides. Methods Enzymol. 107 (1984), 295–300.
Holmgren, A., Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264 (1989), 13963–13966.
Hong, Y., Yang, X., Huang, Y., Yan, G., Cheng, Y., Assessment of the oxidative and genotoxic effects of the glyphosate-based herbicide roundup on the freshwater shrimp, Macrobrachium nipponensis. Chemosphere 210 (2018), 896–906, 10.1016/j.chemosphere.2018.07.069.
Hong, Y., Huang, Y., Yan, G., Pan, C., Zhang, J., Antioxidative status, immunological responses, and heat shock protein expression in hepatopancreas of Chinese mitten crab, Eriocheir sinensis under the exposure of glyphosate. Fish Shellfish Immunol. 86 (2019), 840–845, 10.1016/j.fsi.2018.12.020.
Horion, S., Thomé, J.P., Gismondi, E., Changes in antitoxic defense systems of the freshwater amphipod Gammarus pulex exposed to BDE-47 and BDE-99. Ecotoxicology 24 (2015), 959–966, 10.1007/s10646-015-1438-4.
Kang, S.W., Chae, H.Z., Seo, M.S., Kim, K., Baines, I.C., Rhee, S.G., Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generatedin response to growth factors and tumor necrosis factor-α. J. Biol. Chem. 273 (1998), 6297–6302, 10.1074/jbc.273.11.6297.
Kasuba, V., Milie, M., Rozgaj, R., Kopjar, N., Mladini, M., Zunec, S., Vrdoljalk, A.L., Pavicie, I., Cermak, A.M.M., Pizent, A., Tariba, B., Davor, Ž., Effects of low doses of glyphosate on DNA damage, cell proliferation and oxidative stress in the HepG2 cell line. Environ. Sci. Pollut. Res., 2017, 1–15, 10.1007/s11356-017-9438-y.
Katagiri, K., Matsuzawa, A., Ichijo, H., Regulation of apoptosis signal-regulating kinase 1 in redox signaling. Methods Enzymol. 474 (2010), 277–288, 10.1016/S0076-6879(10)74016-7.
Ketterer, B., Coles, B., Meyer, D.J., The role of glutathione in detoxication. Environ. Health Perspect. 49 (1983), 59–69.
Kurutas, E.B., The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current State. Nutr. J. 15 (2016), 1–22, 10.1186/s12937-016-0186-5.
Kurutas, E.B., Ciragil, P., Gul, M., Kilinc, M., The effects of oxidative stress in urinary tract infection. Mediat. Inflamm. 4 (2005), 242–244, 10.1155/MI.2005.309.
Lavarias, S., Garcia, C., Crespo, R., Pedrini, N., Heras, H., Study of biochemical biomarkers in freshwater prawn Macrobrachium borellii (Crustacea: palaemonidae) exposed to organophosphate fenitrothion. Ecotoxicol. Environ. Saf. 96 (2013), 10–16, 10.1016/j.ecoenv.2013.05.040.
Li, Y., Ding, W., Li, X., Acute exposure of glyphosate-based herbicide induced damages on common carp organs via heat shock proteins-related immune response and oxidative stress. Toxin Rev., 2019, 1–13, 10.1080/15569543.2019.1621903.
Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real- time quantitative PCR and the 2 -ΔΔCT Method. Methods 25 (2001), 402–408, 10.1006/meth.2001.1262.
Livingstone, D.R., The fate of organic xenobiotics in aquatic ecosystems: quantitative and qualitative differences in biotransformation by invertebrates and fish. Comp. Biochem. Physiol., A 120 (1998), 43–49, 10.1016/S1095-6433(98)10008-9.
Livingstone, D.R., Lips, F., Martinez, P.G., Pipe, R.K., Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Mar. Biol. 112 (1992), 265–276, 10.1007/BF00702471.
Loizzi, R.F., Interpretation of crayfish hepatopancreatic function based on fine structural analysis of epithelial cell lines and muscle network. Z. für Zellforsch. Mikrosk. Anat. 113 (1971), 420–440, 10.1007/BF00968548.
Malik, Z., Jones, C.J.P., Connock, M.J., Assay and subcellular localization of H2O2 generating mannitol oxidase in the terrestrial slug Arion ater. J. Exp. Zool. 242 (1987), 9–15, 10.1002/jez.1402420103.
Modesto, K.A., Martinez, C.B.R., Roundup causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus. Chemosphere 78 (2010), 294–299, 10.1016/j.chemosphere.2009.10.047.
Molavian, H., Madani Tonekaboni, A., Kohandel, M., Sivaloganathan, S., The Synergetic coupling among the cellular antioxidants glutathione peroxidase/peroxiredoxin and other antioxidants and its effect on the concentration of H2O2. Sci. Rep. 5 (2015), 1–8, 10.1038/srep13620.
Moorhouse, K.G., Casida, J.E., Pesticides as activators of mouse liver microsomal glutathione S-transferase. Pestic. Biochem. Physiol. 44 (1992), 83–90, 10.1016/0048-3575(92)90105-9.
Nakamura, K., Rokutan, K., Marui, N., Aoike, A., Kawai, K., Induction of heat shock proteins and their implication in protection against ethanol-induced damage in cultured Guinea pig gastric mucosal cells. Gastroenterology 101 (1991), 161–166, 10.1016/0016-5085(91)90473-X.
Okada, E., Pérez, D., Gerónimo, E., De Aparicio, V., Massone, H., Costa, J.L., Non-point source pollution of glyphosate and AMPA in a rural basin from the southeast Pampas, Argentina. Environ. Sci. Pollut. Res. 25 (2018), 15120–15132.
Orbea, A., Dariush Fahimi, H., Cajaraville, M.P., Immunolocalization of four antioxidant enzymes in digestive glands of mollusks and crustaceans and fish liver. Histochem. Cell Biol. 114 (2000), 393–404, 10.1007/s004180000207.
Osten, J.R.-V., Dzul-Caamal, R., Glyphosate residues in groundwater, drinking water and urine of subsistence farmers from intensive agriculture localities: a survey in Hopelchén, Campeche, Mexico. Int. J. Environ. Res. Public Health 14 (2017), 1–13, 10.3390/ijerph14060595.
Pereira, P., de Pablo, H., Dulce Subida, M., Vale, C., Pacheco, M., Biochemical responses of the shore crab (Carcinus maenas) in a eutrophic and metal-contaminated coastal system (Óbidos lagoon, Portugal). Ecotoxicol. Environ. Saf. 72 (2009), 1471–1480, 10.1016/j.ecoenv.2008.12.012.
Peruzzo, P.J., Porta, A.A., Ronco, A.E., Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environ. Pollut. 156 (2008), 61–66, 10.1016/j.envpol.2008.01.015.
Pratt, W.B., Toft, D.O., Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol. Med. 228 (2003), 111–133.
Richmond, M.E., Glyphosate: a review of its global use, environmental impact, and potential health effects on humans and other species. J. Environ. Soc. Sci., 50, 2018, 19.
Ryan, M.T., Pfanner, N., Hsp70 proteins in protein translocation. Adv. Protein Chem. 59 (2002), 223–242, 10.1016/S0065-3233(01)59007-5.
Saibil, H., Chaperone machines for protein folding, unfolding and disaggregation. Nat. Rev. Mol. Cell Biol. 14 (2013), 630–642, 10.1038/nrm3658.
Saitoh, M., Nishitoh, H., Fujii, M., Takeda, K., Tobiume, K., Sawada, Y., Kawabata, M., Miyazono, K., Ichijo, H., Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17 (1998), 2596–2606, 10.1039/DT9890001143.
Sanchez, W., Burgeot, T., Porcher, J.M., A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environ. Sci. Pollut. Res. 20 (2013), 2721–2725, 10.1007/s11356-012-1359-1.
Scandalios, J.G., Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz. J. Med. Biol. Res. 38 (2005), 995–1014.
Schvezov, N., Lovrich, G.A., Romero, M.C., Oxidative stress during re-immersion of the king crab Lithodes santolla (Molina, 1782) (Decapoda: anomura: Lithodidae) after air exposure. J. Crustac Biol. 37 (2017), 195–203, 10.1093/jcbiol/rux004.
Simmons, T.W., Jamall, I.S., Significance of alterations in hepatic antioxidant enzymes. Primacy of glutathione peroxidase. Biochem. J. 251 (1988), 913–917, 10.1042/bj2510913.
Sinhorin, V.D.G., Sinhorin, A.P., Teixeira, J.M., dos, S., Miléski, K.M.L., Hansen, P.C., Moreira, P.S.A., Kawashita, N.H., Baviera, A.M., Loro, V.L., Effects of the acute exposition to glyphosate-based herbicide on oxidative stress parameters and antioxidant responses in a hybrid Amazon fish surubim (Pseudoplatystoma sp). Ecotoxicol. Environ. Saf. 106 (2014), 181–187, 10.1016/j.ecoenv.2014.04.040.
Sobjak, T.M., Romão, S., do Nascimento, C.Z., dos Santos, A.F.P., Vogel, L., Guimarães, A.T.B., Assessment of the oxidative and neurotoxic effects of glyphosate pesticide on the larvae of Rhamdia quelen fish. Chemosphere 182 (2017), 267–275, 10.1016/j.chemosphere.2017.05.031.
Srivastava, P., Roles of heat-shock proteins in innate and adaptive immunity. Nat. Rev. Immunol. 2 (2002), 185–194, 10.1038/nri749.
Tremblay, N., Gómez-Gutiérrez, J., Zenteno-Savín, T., Robinson, C.J., Sánchez-Velasco, L., Role of oxidative stress in seasonal and daily vertical migration of three krill species in the Gulf of California. Limnol. Oceanogr. 55 (2010), 2570–2584, 10.4319/lo.2010.55.6.2570.
Trott, A., West, J.D., Klaic, L., Westerheide, S.D., Silverman, R.B., Morimoto, R.I., Morano, K.A., Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of thiol-targeted molecule. Mol. Biol. Cell 19 (2008), 1104–1112, 10.1091/mbc.E07.
USEPA. United States Environmental Protection Agency, National Primary Drinking Water Regulation. 2009 EPA 816-F-09- 0042009.
Valko, M., Rhodes, C.J., Moncol, J., Izakovic, M., Mazur, M., Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Interact. 160:160 (2006), 1–40, 10.1016/j.cbi.2005.12.009.
Valko, M., Leibfritz, D., Moncol, J., Cronin, M.T.D., Mazur, M., Telser, J., Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39 (2007), 44–84, 10.1016/j.biocel.2006.07.001.
Vogt, G., Functional cytology of the hepatopancreas of decapod crustaceans. J. Morphol., 2019, 1–40, 10.1002/jmor.21040.
Wang, M., Dhingra, K., Hittelman, W.N., Liehr, J.G., de Andrade, M., Li, D., Lipid peroxidation-induced putative malondialdehyde-DNA adducts in human breast tissue. Cancer Epidemiol. Biomark. Prev. 5 (1996), 705–710.
Wang, W.N., Zhou, J., Wang, P., Tian, T.T., Zheng, Y., Liu, Y., Mai, W., Wang, A.L., Oxidative stress, DNA damage and antioxidant enzyme gene expression in the Pacific white shrimp, Litopenaeus vannamei when exposed to acute pH stress. Comp. Biochem. Physiol., C 150 (2009), 428–435, 10.1016/j.cbpc.2009.06.010.
Wu, H.Y., Xu, H.X., Hong, Y.B., Zhang, J.F., Wu, J.C., The use of biomarkers in the antioxidant responses of Daphnia magna to the acute and chronic exposure to no. 20 diesel oil and 2,4-dichlorophenol. Chem. Speciat. Bioavailab. 23 (2011), 80–87, 10.3184/095422911X13027015402949.
Wu, C.W., Biggar, K.K., Zhang, J., Tessier, S.N., Pifferi, F., Perret, M., Storey, K.B., Induction of antioxidant and heat shock protein responses during torpor in the gray mouse Lemur, Microcebus murinus. Genom. Proteom. Bioinform. 13 (2015), 119–126, 10.1016/j.gpb.2015.03.004.
Xing, H., Li, S., Wang, Xu, Gao, X., Xu, S., Wang, Xiaolong, 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 (2013), 910–916, 10.1016/j.chemosphere.2012.06.028.
Zhang, P., Liu, B., Kang, S.W., Seo, M.S., Rhee, S.G., Obeid, L.M., Thioredoxin peroxidase is a novel inhibitor of apoptosis with a mechanism distinct from that of Bcl-2. J. Biol. Chem. 272 (1997), 30615–30618, 10.1074/jbc.272.49.30615.
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.