Effects of T-2 Toxin on Pacific White Shrimp Litopenaeus vannamei: Growth, and Antioxidant Defenses and Capacity and Histopathology in the Hepatopancreas

REFERENCES

• Ahmad, I., T. Hamid, M. Fatima, H. S. Chand, S. K. Jain, M. Athar, and S. Raisuddin. 2000. Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochimica et Biophysica Acta 1523:37–48.
   PubMed Web of Science ®Google Scholar
• Al-Mohanna, S. Y., and J. A. Nott. 1986. B-cells and digestion in the hepatopancreas of Penaeus semisulcatus (Crustacea: Decapoda). Journal of the Marine Biological Association of the UK 66:403–414.
   Web of Science ®Google Scholar
• Anukul, N., T. Maneeboon, C. Roopkham, C. Chuaysrinule, and W. Mahakarnchanakul. 2014. Fumonisin and T-2 toxin production of Fusarium spp. isolated from complete feed and individual agricultural commodities used in shrimp farming. Mycotoxin Research 30:9–16.
   Google Scholar
• Bautista, M. N., C. R. Lavilla-Pitogo, and P. F. Subosa. 1994. Aflatoxin B1 contamination of shrimp feeds and its effect on growth and hepatopancreas of pre-adult Penaeus monodon. Journal of the Science of Food and Agriculture 65:5–11.
   Web of Science ®Google Scholar
• Beers, R. F., and I. W. Sizer. 1952. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. Journal of Biological Chemistry 195:133–140.
   PubMed Web of Science ®Google Scholar
• Berthiller, F., C. Crew, C. Dall’Asta, S. De Saeger, G. Haesaert, P. Karlovsky, I. P. Oswald, W. Seefelder, G. Speijers, and J. Stroka. 2013. Masked mycotoxins: a review. Molecular Nutrition and Food Research 57:65–189.
   Web of Science ®Google Scholar
• Berthiller, F., R. Krska, K. J. Domig, W. Kneifel, N. Juge, R. Schuhmacher, and G. Adam. 2011. Hydrolytic fate of deoxynivalenol-3-glucoside during digestion. Toxicology Letters 206:264–267.
   PubMed Web of Science ®Google Scholar
• Beyer, M., I. Ferse, D. Mulac, E. U. Würthwein, and H. U. Humpf. 2009. Structural elucidation of T-2 toxin thermal degradation products and investigations toward their occurrence in retail food. Journal of Agricultural and Food Chemistry 57:1867–1875.
   PubMed Web of Science ®Google Scholar
• Blajet-Kosicka, A., M. Twaruźek, R. Kosicki, E. Sibiorowska, and J. Grajewski. 2013. Co-occurrence and evaluation of mycotoxins in organic and conventional rye grain and products. Food Control 38:61–66.
   Web of Science ®Google Scholar
• Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of micro-gram quantities of protein using the principle of protein–dye binding. Analytical Biochemistry 72:248–254.
   PubMed Web of Science ®Google Scholar
• Burgos-Hernández, A., S. I. Farias, W. Torres-Arreola, and J. M. Ezquerra-Brauer. 2005. In vitro studies of the effects of aflatoxin B1 and fumonisin B1 on trypsin-like and collagenase-like activity from the hepatopancreas of white shrimp (Litopenaeus vannamei). Aquaculture 250:399–410.
   Web of Science ®Google Scholar
• Capcarova, M., P. Petruska, K. Zbynovska, A. Kolesarova, and A. V. Sirotkin. 2015. Changes in antioxidant status of porcine ovarian granulosa cells after quercetin and T-2 toxin treatment. Journal of Environmental Science and Health B 50:201–206.
   PubMed Web of Science ®Google Scholar
• Chaudhari, M., R. Jayaraj, S. R. Santhosh, and R. P. Lakshmana. 2009. Oxidative damage and gene expression profile of antioxidant enzymes after T-2 toxin exposure in mice. Journal of Biochemical and Molecular Toxicology 23:212–221.
   PubMed Web of Science ®Google Scholar
• Chen, H., H. Yoshioka, G. S. Kim, J. E. Jung, N. Okami, H. Sakata, C. M. Maier, P. Narasimhan, C. E. Goeders, and P. H. Chan. 2011. Oxidative stress in ischemic brain damage: mechanisms of cell death and potential molecular targets for neuroprotection. Antioxidants and Redox Signaling 14:1505–1517.
   PubMed Web of Science ®Google Scholar
• Chen, J. H., S. H. Xue, S. Y. Li, Z. L. Wang, H. J. Yang, W. Wang, D. Q. Song, X. R. Zhou, and C. Chen. 2012. Oxidant damage in Kashin-Beck disease and a rat Kashin-Beck disease model by employing T-2 toxin treatment under selenium deficient conditions. Journal of Orthopaedic Research 30:1229–1237.
   PubMed Web of Science ®Google Scholar
• Clear, R. M., S. K. Patrick, D. Gaba, M. Roscoe, T. Demeke, S. Pouleur, L. Couture, T. J. Ward, K. O’Donnell, and T. K. Turkington. 2006. Trichothecene and zearalenone production, in culture, by isolates of Fusarium pseudograminearum from western Canada. Canadian Journal of Plant Pathology 28:131–136.
   Google Scholar
• Cuervo, A. M., and J. F. Dice. 2000. Unique properties of lamp2a compared to other lamp2 isoforms. Journal of Cell Science 113:4441–4450.
   PubMed Web of Science ®Google Scholar
• Dai, Z., Y. L. Wang, L. J. Sun, Q. Shi, D. F. Xu, J. J. Chen, and F. H. Nie. 2013. Preparation and assessment of T-2 toxic feed of shrimp by microcapsule technology. Guangdong Agriculture Science 11:94–103. ( In Chinese.)
   Google Scholar
• Danion, M., S. Le Floch, F. Lamour, and C. Quentel. 2014. Effects of in vivo chronic exposure to pendimethalin on EROD activity and antioxidant defenses in Rainbow Trout (Oncorhynchus mykiss). Ecotoxicology and Environmental Safety 99:21–27.
   PubMed Web of Science ®Google Scholar
• Duan, Y. F., J. S. Zhang, H. B. Dong, Y. Wang, Q. S. Liu, and H. Li. 2015. Oxidative stress response of the black tiger shrimp Penaeus monodon to Vibrio parahaemolyticus challenge. Fish and Shellfish Immunology 46:354–365.
   PubMed Web of Science ®Google Scholar
• Gopinath, R., R. P. Raj, K. C. George, and N. K. Sanil. 2012. Ultrastructural changes in the hepatopancreas of Penaeus monodon Fabricius 1798 given aflatoxin a B1 diets. Aquaculture Research 43:32–43.
   Web of Science ®Google Scholar
• Grabley, S., M. Gareis, W. Bockers, and J. Thiem. 1991. Glycosylation of mycotoxins. Synthesis-Stuttgart 11:1078–1080.
   Google Scholar
• Gu, J., G. S. Liu, J. Guo, and J. Zhang. 2008. Effects of vitamin E on the activities of protective enzymes and membrane lipid peroxidation in Leymus chinensis under drought stress. Chemical Research in Chinese Universities 24:80–83.
   Web of Science ®Google Scholar
• Gurr, E. 1962. Staining animal tissues. Practical and theoretical. Leonard Hill, London.
   Google Scholar
• He, C. H., Y. H. Fan, Y. Wang, C. Y. Huang, X. C. Wang, and H. B. Zhang. 2010. The individual and combined effects of deoxyivalenol and aflatoxin B1 on primary hepatocytes of Cyprinus carpio. International Journal of Molecular Sciences 11:3760–3768.
   PubMed Web of Science ®Google Scholar
• Hernández-Gea, V., M. Hilscher, R. Rozenfeld, M. P. Lim, N. Nieto, S. Werner, L. A. Devi, and S. L. Friedman. 2013. Endoplasmic reticulum stress induces fibrogenic activity in hepatic stellate cells through autophagy. Hepatology 59:98–104.
   PubMed Web of Science ®Google Scholar
• Jagadeesan, V., C. Rukmini, M. Vijayaraghavana, and P. G. Tulpulea. 1982. Immune studies with T-2 toxin: effect of feeding and withdrawal in monkeys. Food and Cosmetics Toxicology 20:83–87.
   Google Scholar
• Kang, S. W., S. G. Rhee, T. S. Chang, W. Jeong, and M. H. Choi. 2005. 2-Cys peroxiredoxin function in intracellular signal transduction, therapeutic implications. Trends in Molecular Medicine 11:571–578.
   PubMed Web of Science ®Google Scholar
• Khoa, L. V., K. Hatai, and T. Aoki. 2004. Fusarium incarnatum isolated from black tiger shrimp, Penaeus monodon Fabricius, with black gill disease cultured in Vietnam. Journal of Fish Diseases 27:507–515.
   PubMed Web of Science ®Google Scholar
• Koike, M., M. Shibata, M. Tadakoshi, K. Gotoh, M. Komatsu, S. Waguri, N. Kawahara, K. Kuida, S. Nagata, and E. Kominami. 2008. Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. American Journal of Pathology 172:454–469.
   PubMed Web of Science ®Google Scholar
• Liang, J. P., J. Li, J. T. Li, P. Liu, Z. Q. Chang, and G. X. Nie. 2014. Accumulation and elimination of enrofloxacin and its metabolite ciprofloxacin in the ridgetail white prawn Exopalaemon carinicauda following medicated feed and bath administration. Journal of Veterinary Pharmacology and Therapeutics 37:508–514.
   PubMed Web of Science ®Google Scholar
• Lightner, D. V., R. M. Redman, R. L. Price, and M. O. Wiseman. 1982. Histopathology of aflatoxicosis in the marine shrimp Penaeus stylirostris and P. vannamei. Journal of Invertebrate Pathology 40:279–291.
   PubMed Web of Science ®Google Scholar
• Liu, Y., F. Walker, B. Hoeglinger, and H. Buchenauer. 2005. Solvolysis procedures for the determination of bound residues of the mycotoxin deoxynivalenol in fusarium species infected grain of two winter wheat cultivars preinfected with barley yellow dwarf virus. Journal of Agricultural and Food Chemistry 53:6864–6869.
   PubMed Web of Science ®Google Scholar
• Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin Phenol reagent. Journal of Biological Chemistry 193:265–275.
   PubMed Web of Science ®Google Scholar
• Lu, P., C. Wu, Q. Shi, Y. Wang, L. Sun, J. Liao, S. Zhong, D. Xu, J. Chen, Y. Liu, J. Li, and R. Gooneratne. 2016. A sensitive and validated method for determination of T-2 and HT-2 toxin residues in shrimp tissues by LC-MS/MS. Food Analytical Methods 9:1580–1594.
   Web of Science ®Google Scholar
• Lykkesfeldt, J. 2007. Malondialdehyde as biomarker of oxidative damage to lipids caused by smoking. Clinica Chimica Acta 380:50–58.
   PubMed Web of Science ®Google Scholar
• Marklund, S., and G. Marklund. 1974. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. European Journal of Biochemistry 47:469–474.
   PubMedGoogle Scholar
• Matés, J. M., C. Pérez-Gómez, and I. Núnez De Castro. 1999. Antioxidant enzymes and human diseases. Clinical Biochemistry 32:595–603.
   PubMed Web of Science ®Google Scholar
• Moore, M. N., A. Viarengo, P. Donkin, and A. J. S. Hawkins. 2007. Autophagic and lysosomal reactions to stress in the hepatopancreas of blue mussels. Aquatic Toxicology 84:80–91.
   PubMed Web of Science ®Google Scholar
• Nagl, V., B. Wöchtl, H. E. Schwartz-Zimmermann, I. Hennig-Pauka, W. D. Moll, G. Adam, and F. Berthiller. 2014. Metabolism of the masked mycotoxin deoxynivalenol-3-glucoside in pigs. Toxicology Letters 229:190–197.
   PubMed Web of Science ®Google Scholar
• Oliveira, M., M. Pacheco, and M. A. Santos. 2008. Organ specific antioxidant responses in Golden Grey Mullet (Liza aurata) following a short-term exposure to phenanthrene. Science of the Total Environment 396:70–78.
   PubMed Web of Science ®Google Scholar
• Osselaere, A., S. J. Li, L. De Bock, M. Devreese, J. Goossens, V. Vandenbroucke, J. Van Bocxlaer, K. Boussery, F. Pasmans, A. Martel, P. De Backer, and S. Croubels. 2013. Toxic effects of dietary exposure to T-2 toxin on intestinal and hepatic biotransformation enzymes and drug transporter systems in broiler chickens. Food and Chemical Toxicology 55:150–155.
   PubMed Web of Science ®Google Scholar
• Pandey, S., S. Parvez, R. Ansari, F. Hayat, F. Ahmad, and S. Raisuddin. 2008. Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish, Channa punctata Bloch. Chemico-Biological Interactions 174:183–192.
   PubMed Web of Science ®Google Scholar
• Paul, S., R. Jakhar, M. Bhardwaj, and S. C. Kang. 2015. Glutathione-S-transferase omega 1 (GSTO1-1) acts as mediator of signaling pathways involved in aflatoxin B1-induced apoptosis-autophagy crosstalk in macrophages. Free Radical Biology and Medicine 89:1218–1230.
   PubMed Web of Science ®Google Scholar
• Petruška, P., A. Latacz, A. Kolesárová, and M. Capcarová. 2012. Effect of quercetin and T-2 toxin on antoxidant parameters of porcine blood in vitro. Journal of Clinical Microbiology 2:510–516.
   Google Scholar
• Poston, H. A., J. L. Coffin, and G. F. Combs. 1982. Biological effects of dietary T-2 toxin on Rainbow Trout, Salmo gairdneri. Aquatic Toxicology 2:79–88.
   Web of Science ®Google Scholar
• Reyes-Gonzales, M. C., L. Fuentes-Broto, E. Martínez-Ballarín, F. J. Miana-Mena, C. Berzosa, F. A. García-Gil, M. Aranda, and J. J. García. 2009. Effects of tryptophan and 5-Hydroxytryptophan on the hepatic cell membrane rigidity due to oxidative stress. Journal of Membrane Biology 2–3:93–99.
   PubMed Web of Science ®Google Scholar
• Rotter, B. A., D. B. Prelusky, and J. J. Pestka. 1996. Toxicology of deoxynivalenol (vomitoxin). Journal of Toxicology Environmental Health A 48:1–34.
   PubMed Web of Science ®Google Scholar
• Saera-Vila, A., L. Benedito-Palos, A. Sitjà-Bobadilla, R. Serrano, S. Kaushik, and J. Pérez-Sánchez. 2009. Assessment of the health and antioxidant trade-off in Gilthead Sea Bream (Sparus aurata L.) fed alternative diets with low levels of contaminant. Aquaculture 296:87–95.
   Web of Science ®Google Scholar
• Scherz-Shouval, R., and Z. Elazar. 2011. Regulation of autophagy by ROS: physiology and pathology. Trends in Biochemical Sciences 36:30–38.
   PubMed Web of Science ®Google Scholar
• Sehata, S., N. Kiyosawa, F. Atsumi, K. Ito, T. Yamoto, M. Teranishi, K. Uetsuka, H. Nakayama, and K. Doi. 2005. Microarray analysis of T-2 toxin-induced liver, placenta and fetal liver lesions in pregnant rats. Experimental and Toxicologic Pathology 57:15–28.
   PubMed Web of Science ®Google Scholar
• Sousa, G., and A. Petriella. 2000. Histology of the hepatopancreas of the freshwater prawn Palaemonetes argentinus (Crustacea, Caridea). Biocell 24:189–195.
   PubMed Web of Science ®Google Scholar
• Stroomberg, G. J., F. Ariese, C. A. M. Gestel, B. Hattum, N. H. Velthorst, and N. M. Straalen. 2004. Pyrene biotransformation and kinetics in the hepatopancreas of the isopod Porcellio scaber. Archives of Environmental Contamination and Toxicology 47:324–331.
   PubMed Web of Science ®Google Scholar
• Tapia-Salazar, M., O. D. Garcia-Perez, R. A. Velasquez-Soto, M. G. Nieto-Lopez, D. Villarreal-Cavazos, D. Ricque-Marie, and L. E. Cruz-Suarez. 2012. Growth, feed intake, survival, and histological response of white shrimp Litopenaeus vannamei fed diets containing grains naturally contaminated with aflatoxin. Ciencias Marinas 38:491–504.
   Web of Science ®Google Scholar
• Tran, S. T., and T. K. Smith. 2011. Determination of optimal conditions for hydrolysis of conjugated deoxynivalenol in corn and wheat with trifluoromethanesulfonic acid. Animal Feed Science and Technology 163:84–92.
   Web of Science ®Google Scholar
• Ueno, Y., M. Nakauima, K. Sakai, K. Ishii, N. Sato, and N. Schimada. 1973. Comparative toxicology of tricothecene mycotoxins: inhibition of protein synthesis in animal cells. Biochemical Journal 74:285–296.
   Google Scholar
• Vandeputte, C., I. Guizon, I. Genestie-Denis, B. Vannier, and G. Lorenzon. 1994. A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell Biology and Toxicology 10:415–421.
   PubMed Web of Science ®Google Scholar
• Wang, X. C., X. D. Liu, J. C. Liu, G. Wang, and K. Y. Wan. 2012. Contamination level of T-2 and HT-2 toxin in cereal crops from Aba Area in Sichuan Province, China. Bulletin of Environmental Contamination and Toxicology 88:396–400.
   PubMed Web of Science ®Google Scholar
• Wang, Y. L., Z. Dai, L. J. Sun, P. L. Lu, D. F. Xu, Y. Liu, R. Y. Ye, and F. H. Nie. 2015. Acute oral toxicity of T-2 toxin on Litopenaeus vannamei. Modern Food Science Technology 31:221–226. ( In Chinese.)
   Google Scholar
• Warth, B., P. Fruhmann, G. Wiesenberger, B. Kluger, B. Sarkanj, M. Lemmens, C. Hametner, J. Fröhlich, G. Adam, R. Krska, and R. Schuhmacher. 2015. Deoxynivalenol-sulfates: identification and quantification of novel conjugated (masked) mycotoxins in wheat. Analytical and Bioanalytical Chemistry 407:1033–1039.
   PubMed Web of Science ®Google Scholar
• Weber, M., K. Balogh, J. Fodor, M. Erdlyi, Z. Ancsin, and M. Mzes. 2010. Effect of T-2 and HT-2 toxin during the growing period on body weight, lipid peroxide and glutathione redox status of broiler chickens. Acta Veterinaria Brno 79:29–31.
   Web of Science ®Google Scholar
• Wu, C. J. 2014. The common representation and hazard identification of masked T-2 toxin in Litopenaeus vannamei. Master’s thesis. Guandong Ocean University, Zhanjiang, China. ( In Chinese.)
   Google Scholar
• Wu, F. J., Y. Xue, X. F. Liu, C. H. Xue, J. F. Wang, L. Du, K. Takahashi, and Y. M. Wang. 2013a. The protective effect of eicosapentaenoic acid-enriched phospholipids from sea cucumber Cucumaria frondosa on oxidative stress in PC12 cells and SAMP8 mice. Neurochemistry International 64:9–17.
   PubMed Web of Science ®Google Scholar
• Wu, J., D. Tu, L. Y. Yuan, H. Yuan, and L. X. Wen. 2013b. T-2 toxin exposure induces apoptosis in rat ovarian granulosa cells through oxidative stress. Environmental Toxicology and Pharmacology 36:493–500.
   PubMed Web of Science ®Google Scholar
• Wyatt, R. D., J. A. Doerr, P. B. Hamilton, and H. R. Burmeister. 1975. Egg production, shell thickness and other physiological parameters of laying hens affected by T-2 toxin. Applied and Environmental Microbiology 29:641–647.
   Google Scholar
• Xia, Y. M., and L. Z. Zhu. 1987. Detection method of glutathione peroxidase in blood and tissue. Journal of Hygiene Research 16:29–32.
   Google Scholar
• Yang, B., X. L. Song, J. Huang, C. Y. Shi, Q. H. Liu, and L. Liu. 2006. A single-step multiplex PCR for simultaneous detection of white spot syndrome virus and infectious hypodermal and haematopoietic necrosis virus in penaeid shrimp. Journal of Fish Diseases 29:301–305.
   PubMed Web of Science ®Google Scholar
• Ye, J., Y. Zhang, S. W. Chen, C. N. Liu, Y. Q. Zhu, and W. P. Liu. 2014. Enantioselective changes in oxidative stress and toxin release in Microcystis aeruginosa exposed to chiral herbicide diclofop acid. Aquatic Toxicology 146:12–19.
   PubMed Web of Science ®Google Scholar
• Yoshizawa, T., T. Sakamoto, Y. Ayano, and C. J. Mirocha. 1982. 3ʹ-hydroxy T-2 and 3ʹ-OH-HT-2 toxins: new metabolites of T-2 toxin, a trichothecene mycotoxin, in animals. Agricultural and Biological Chemistry 46:2613–2615.
   Web of Science ®Google Scholar
• Zeng, T., C. L. Zhang, Z. P. Zhu, L. H. Yu, X. L. Zhao, and K. Q. Xie. 2008. Dially trisulfide (DATS) effectively attenuated oxidative stress-mediated liver injury and hepatic mitochondrial dysfunction in acute ethanol-exposed mice. Toxicology 252:86–91.
   PubMed Web of Science ®Google Scholar
• Zhang, Q. L., F. H. Li, X. J. Zhang, B. Dong, J. Q. Zhang, Y. S. Xie, and J. H. Xiang. 2008. cDNA cloning, characterization and expression analysis of the antioxidant enzyme gene, catalase, of Chinese shrimp Fenneropenaeus chinensis. Fish and Shellfish Immunology 24:584–591.
   PubMed Web of Science ®Google Scholar
• Zhou, B., Y. Li, J. Gillespie, G. Q. He, R. Horsley, and P. Schwarz. 2007. Doehlert matrix design for optimization of the determination of bound deoxynivalenol in barley grain with trifluoroacetic acid (TFA). Journal of Agricultural and Food Chemistry 55:10141–10149.
   PubMed Web of Science ®Google Scholar