Effect of the mycotoxin deoxynivalenol on the immune responses of rainbow trout (Oncorhynchus mykiss)
I. Matejova, M. Vicenova, L. Vojtek, H. Kudlackova, K. Nedbalcova, M. Faldyna, E. Sisperova, H. Modra, Z. Svobodovahttps://doi.org/10.17221/8443-VETMEDCitation:Matejova I., Vicenova M., Vojtek L., Kudlackova H., Nedbalcova K., Faldyna M., Sisperova E., Modra H., Svobodova Z. (2015): Effect of the mycotoxin deoxynivalenol on the immune responses of rainbow trout (Oncorhynchus mykiss). Veterinarni Medicina, 60: 515-521.
The trichothecene mycotoxin deoxynivalenol (DON) is commonly found as a natural contaminant in cereals such as wheat, barley, and corn, and exhibits various toxicological effects when present in animal feeds. The effects of DON at a nominal 2 mg/kg feed on immune responses of rainbow trout were investigated, including relative gene expression of important cytokines (TNF-α, IL-8, IL-1β, IL-10), lysozyme concentration in skin mucus, and level of antigen-specific IgM in blood plasma after vaccination with the commercial vaccine AquaVac ERM containing Yersinia ruckeri type 1 (Hagerman strain). Twenty one-year-old rainbow trout Oncorhynchus mykiss were randomly divided into two groups. The control received a commercial feed with a naturally occurring low level of DON (225 μg/kg feed), while an experimental group was fed the same formulation with DON added to 1964 μg/kg feed. The trial continued for 23 days. Consumption of feed with added DON showed a significant effect on the immune system, as indicated by a higher level of pro-inflammatory cytokine TNF-α (P < 0.05) and of IL-8 (non-significant) in head kidney. Expression of the pro-inflammatory gene IL-1β and the expression of a gene encoding anti-inflammatory cytokine (IL-10) were not influenced by DON treatment. Effects on the concentration of skin mucus lysozyme and specific IgM antibody levels were not observed during this experiment. These results suggest that prolonged ingestion of low doses of DON may influence the immune responses of rainbow trout.Keywords:fish; feedstuffs; mycotoxin; immune systemReferences:
Balfry SK, Iwama GK (2014): Observations on the inherent variability of measuring lysozyme activity in coho salmon (Oncorhynchus kisutch). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 138, 207–211.Bracarense Ana-Paula F. L., Lucioli Joelma, Grenier Bertrand, Drociunas Pacheco Graziela, Moll Wulf-Dieter, Schatzmayr Gerd, Oswald Isabelle P. (2012): Chronic ingestion of deoxynivalenol and fumonisin, alone or in interaction, induces morphological and immunological changes in the intestine of piglets. British Journal of Nutrition, 107, 1776-1786 https://doi.org/10.1017/S0007114511004946Chung Yong-Joo, Zhou Hui-Ren, Pestka James J (2003): Transcriptional and posttranscriptional roles for p38 mitogen-activated protein kinase in upregulation of TNF-α expression by deoxynivalenol (vomitoxin). Toxicology and Applied Pharmacology, 193, 188-201 https://doi.org/10.1016/S0041-008X(03)00299-0Esteban MA (2012): An Overview of the immunological defences in fish skin. ISRN Immunology, doi: 10.5402/ 2012/853470.Fink-Gremmels Johanna (2008): Mycotoxins in cattle feeds and carry-over to dairy milk: A review. Food Additives & Contaminants: Part A, 25, 172-180 https://doi.org/10.1080/02652030701823142Guan Shu, He Jianwei, Young J. Christopher, Zhu Honghui, Li Xiu-Zhen, Ji Cheng, Zhou Ting (2009): Transformation of trichothecene mycotoxins by microorganisms from fish digesta. Aquaculture, 290, 290-295 https://doi.org/10.1016/j.aquaculture.2009.02.037Hooft Jamie M., Elmor Abd El Hakeem Ibraheem, Encarnação Pedro, Bureau Dominique P. (2011): Rainbow trout (Oncorhynchus mykiss) is extremely sensitive to the feed-borne Fusarium mycotoxin deoxynivalenol (DON). Aquaculture, 311, 224-232 https://doi.org/10.1016/j.aquaculture.2010.11.049Jung Tae Sung, del Castillo Carmelo S., Javaregowda Palaksha K., Dalvi Rishikesh S., Nho Seong Won, Park Seong Bin, Jang Ho Bin, Cha In Seok, Sung Haan Woo, Hikima Jun-ichi, Aoki Takashi (2012): Seasonal variation and comparative analysis of non-specific humoral immune substances in the skin mucus of olive flounder (Paralichthys olivaceus). Developmental & Comparative Immunology, 38, 295-301 https://doi.org/10.1016/j.dci.2012.06.005Manning Bruce B., Abbas Hamed K. (2012): The effect of Fusarium mycotoxins deoxynivalenol, fumonisin, and moniliformin from contaminated moldy grains on aquaculture fish. Toxin Reviews, 31, 11-15 https://doi.org/10.3109/15569543.2011.651519Matejova Iveta, Modra Helena, Blahova Jana, Franc Ales, Fictum Petr, Sevcikova Marie, Svobodova Zdenka (2014): The Effect of Mycotoxin Deoxynivalenol on Haematological and Biochemical Indicators and Histopathological Changes in Rainbow Trout (Oncorhynchus mykiss). BioMed Research International, 2014, 1-5 https://doi.org/10.1155/2014/310680Ondračková Markéta, Valová Zdenka, Kortan Jiří, Vojtek Libor, Adámek Zdeněk (2012): Consequent effects of the great cormorant (Phalacrocorax carbo sinensis) predation on parasite infection and body condition of common carp (Cyprinus carpio). Parasitology Research, 110, 1487-1493 https://doi.org/10.1007/s00436-011-2652-5Pérez-Sánchez Tania, Balcázar José Luis, Merrifield Daniel L., Carnevali Oliana, Gioacchini Giorgia, de Blas Ignacio, Ruiz-Zarzuela Imanol (2011): Expression of immune-related genes in rainbow trout (Oncorhynchus mykiss) induced by probiotic bacteria during Lactococcus garvieae infection. Fish & Shellfish Immunology, 31, 196-201 https://doi.org/10.1016/j.fsi.2011.05.005Pestka James J. (2010): Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Archives of Toxicology, 84, 663-679 https://doi.org/10.1007/s00204-010-0579-8Pestka James J., Zhou Hui-Ren, Moon Y., Chung Y.J. (2004): Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: unraveling a paradox. Toxicology Letters, 153, 61-73 https://doi.org/10.1016/j.toxlet.2004.04.023Pietsch Constanze, Kersten Susanne, Burkhardt-Holm Patricia, Valenta Hana, Dänicke Sven (2013): Occurrence of Deoxynivalenol and Zearalenone in Commercial Fish Feed: An Initial Study. Toxins, 5, 184-192 https://doi.org/10.3390/toxins5010184Pietsch Constanze, Michel Christian, Kersten Susanne, Valenta Hana, Dänicke Sven, Schulz Carsten, Kloas Werner, Burkhardt-Holm Patricia (2014): In vivo effects of deoxynivalenol (DON) on innate immune responses of carp (Cyprinus carpio L.). Food and Chemical Toxicology, 68, 44-52 https://doi.org/10.1016/j.fct.2014.03.012Pinton P., Tsybulskyy D., Lucioli J., Laffitte J., Callu P., Lyazhri F., Grosjean F., Bracarense A. P., Kolf-Clauw M., Oswald I. P. (): Toxicity of Deoxynivalenol and Its Acetylated Derivatives on the Intestine: Differential Effects on Morphology, Barrier Function, Tight Junction Proteins, and Mitogen-Activated Protein Kinases. Toxicological Sciences, 130, 180-190 https://doi.org/10.1093/toxsci/kfs239Poisot T., Å imkovÃ¡ A., HyrÅ¡l P., Morand S. (2009): Interactions between immunocompetence, somatic condition and parasitism in the chub Leuciscus cephalus in early spring. Journal of Fish Biology, 75, 1667-1682 https://doi.org/10.1111/j.1095-8649.2009.02400.xPress C.McL., Evensen Ø. (1999): The morphology of the immune system in teleost fishes. Fish & Shellfish Immunology, 9, 309-318 https://doi.org/10.1006/fsim.1998.0181Sanden Monica, Jørgensen Susanne, Hemre Gro-Ingunn, Ørnsrud Robin, Sissener Nini H. (2012): Zebrafish (Danio rerio) as a model for investigating dietary toxic effects of deoxynivalenol contamination in aquaculture feeds. Food and Chemical Toxicology, 50, 4441-4448 https://doi.org/10.1016/j.fct.2012.08.042Secombes C (2008): Will advances in fish immunology change vaccination strategies? Fish and Shellfish Immunology 25, 409–416.Streit Elisabeth, Schatzmayr Gerd, Tassis Panagiotis, Tzika Eleni, Marin Daniela, Taranu Ionelia, Tabuc Cristina, Nicolau Anca, Aprodu Iuliana, Puel Olivier, Oswald Isabelle P. (2012): Current Situation of Mycotoxin Contamination and Co-occurrence in Animal Feed—Focus on Europe. Toxins, 4, 788-809 https://doi.org/10.3390/toxins4100788SUGITA-KONISHI Yoshiko, PARK Bong Joo, KOBAYASHI-HATTORI Kazuo, TANAKA Toshitugu, CHONAN Takao, YOSHIKAWA Kunie, KUMAGAI Susumu (): Effect of Cooking Process on the Deoxynivalenol Content and Its Subsequent Cytotoxicity in Wheat Products. Bioscience, Biotechnology and Biochemistry, 70, 1764-1768 https://doi.org/10.1271/bbb.50571Vandenbroucke Virginie, Croubels Siska, Martel An, Verbrugghe Elin, Goossens Joline, Van Deun Kim, Boyen Filip, Thompson Arthur, Shearer Neil, De Backer Patrick, Haesebrouck Freddy, Pasmans Frank, Sestak Karol (2011): The Mycotoxin Deoxynivalenol Potentiates Intestinal Inflammation by Salmonella Typhimurium in Porcine Ileal Loops. PLoS ONE, 6, e23871- https://doi.org/10.1371/journal.pone.0023871Waché Yann J., Valat Charlotte, Postollec Gilbert, Bougeard Stephanie, Burel Christine, Oswald Isabelle P., Fravalo Philippe (2009): Impact of Deoxynivalenol on the Intestinal Microflora of Pigs. International Journal of Molecular Sciences, 10, 1-17 https://doi.org/10.3390/ijms10010001Wegulo Stephen (2012): Factors Influencing Deoxynivalenol Accumulation in Small Grain Cereals. Toxins, 4, 1157-1180 https://doi.org/10.3390/toxins4111157Woodward Bill, Young L.G., Lun A.K. (1983): Vomitoxin in diets for rainbow trout (Salmo gairdneri). Aquaculture, 35, 93-101 https://doi.org/10.1016/0044-8486(83)90077-7Zelnickova Petra, Matiasovic Jan, Pavlova Barbora, Kudlackova Hana, Kovaru Frantisek, Faldyna Martin (2008): Quantitative nitric oxide production by rat, bovine and porcine macrophages. Nitric Oxide, 19, 36-41 https://doi.org/10.1016/j.niox.2008.04.001