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Zearalenone Affects Immune-Related Parameters in Lymphoid Organs and Serum of Rats Vaccinated with Porcine Parvovirus Vaccine

  • Choi, Byung-Kook (Toxicology & Residue Chemistry Division, Animal, Plant and Fisheries Quarantine and Inspection Agency) ;
  • Cho, Joon-Hyung (Toxicology & Residue Chemistry Division, Animal, Plant and Fisheries Quarantine and Inspection Agency) ;
  • Jeong, Sang-Hee (GLP Research Center, College of Natural Science, Hoseo University) ;
  • Shin, Hyo-Sook (Toxicology & Residue Chemistry Division, Animal, Plant and Fisheries Quarantine and Inspection Agency) ;
  • Son, Seong-Wan (Toxicology & Residue Chemistry Division, Animal, Plant and Fisheries Quarantine and Inspection Agency) ;
  • Yeo, Young-Keun (Lipid Chemistry Laboratory, Kyungpook University) ;
  • Kang, Hwan-Goo (Toxicology & Residue Chemistry Division, Animal, Plant and Fisheries Quarantine and Inspection Agency)
  • Received : 2012.10.08
  • Accepted : 2012.12.16
  • Published : 2012.12.31

Abstract

Rats were administered zearalenone (ZEA) via gavage at dosages of 0, 1, 5, and 30 mg/kg for 36 days. On treatment day 8, inactivated porcine parvovirus vaccine (Vac) was injected intraperitoneally. Antibody production against porcine parvovirus was then measured as a function of ZEA treatment. Compared to the vaccine alone, ZEA treatment, with or without Vac, decreased the serum level of IgG. The level of IgM decreased in all ZEA groups at day 22, but the decrease was sustained only in the medium-dose ZEA group at day 36. The level of IgA was unchanged in the Vac only and ZEA groups at day 22, but was decreased in the 5 mg/kg ZEA plus Vac group compared to the Vac only group at day 36. The level of IgE was decreased by all doses of ZEA at day 22, but was unaffected in ZEA plus Vac groups compared to the Vac only group. The levels of IL-1 in the thymus and spleen; INF-${\gamma}$ in serum; IL-2, IL-6, and IL-10 in the thymus; and IL-10 and IFN-${\gamma}$ in the spleen decreased after ZEA administration. Furthermore, the levels of IL-$1{\beta}$ in the spleen and mesenteric lymph node, IL-$1{\beta}$ in the thymus, IL-2 in the thymus and spleen, IL-6 in the thymus, IL-10 and IFN-${\gamma}$ in the spleen, and GM-CSF and TNF-${\alpha}$ in the thymus decreased after vaccination in rats exposed to ZEA. In conclusion, these results suggest that ZEA exposure via drinking water can cause an immunosuppressive effect by decreasing immunoglobulins in serum and cytokines in lymphoid organs.

Keywords

References

  1. Abbes, S., Ouanes, Z., ben Salah-Abbès, J., Houas, Z., Oueslati, R., Bacha, H. and Othman, O. (2006). The protective effect of hydrated sodium calcium aluminosilicate against haematological, biochemical and pathological changes induced by Zearalenone in mice. Toxicon., 47, 567-574. https://doi.org/10.1016/j.toxicon.2006.01.016
  2. Abbes, S., Salah-Abbes, J.B., Ouanes, Z., Houas, Z., Othman, O., Bacha, H., Abdel-Wahhab, M.A. and Oueslati, R. (2006). Preventive role of phyllosilicate clay on the Immunological and Biochemical toxicity of zearalenone in Balb/c mice. Int. Immunopharmacol., 6, 1251-1258. https://doi.org/10.1016/j.intimp.2006.03.012
  3. Ahmed, T., Wuest, D. and Ciavarella, D. (1992). Peripheral blood stem cell mobilization by cytokines. J. Clin. Apher., 7, 129-131. https://doi.org/10.1002/jca.2920070306
  4. Atkinson, H.A. and Miller, K. (1984). Inhibitory effect of deoxynivalenol, 3-acetyldeoxynivalenol and zearalenone on induction of rat and human lymphocyte proliferation. Toxicol. Lett., 23, 215-221. https://doi.org/10.1016/0378-4274(84)90129-2
  5. Ben Salah-Abbes, J., Abbes, S., Houas, Z., Abdel-Wahhab, M.A. and Oueslati, R. (2008). Zearalenone induces immunotoxicity in mice: possible protective effects of radish extract (Raphanus sativus). J. Pharm. Pharmacol., 60, 761-770. https://doi.org/10.1211/jpp.60.6.0012
  6. Bende, R.J., Jochems, G.J., Frame, T.H., Klein, M.R., van Eijk, R.V., van Lier, R.A. and Zeijlemaker, W.P. (1992). Effects of IL-4, IL-5, and IL-6 on growth and immunoglobulin production of Epstein-Barr virus-infected human B cells. Cell. Immunol., 143, 310-323. https://doi.org/10.1016/0008-8749(92)90028-N
  7. Bennett, G.A., Nelsen, T.C. and Miller, B.M. (1994). Enzymelinked immunosorbent assay for detection of zearalenone in corn, wheat, and pig feed: collaborative study. J. AOAC. Int., 77, 1500-1509.
  8. Bodine, A.B., Alberty, C.F., Buck, C.S., Richardson, M.E. and Wright, R.E. (1981). Possible "immuno-protection" of the bovine parvovirus in the uterus: Preliminary communication. Theriogenology, 16, 201-206. https://doi.org/10.1016/0093-691X(81)90102-3
  9. Bondy, G.S. and Pestka, J.J. (2000). Immunomodulation by fungal toxins. J. Toxicol. Environ. Health B, 3, 109-143. https://doi.org/10.1080/109374000281113
  10. Brown, K.E. and Young, N.S. (1995). Parvovirus B19 infection and hematopoiesis. Blood Rev., 9, 176-182. https://doi.org/10.1016/0268-960X(95)90023-3
  11. Bryce, P.J., Miller, M.L., Miyajima, I., Tsai, M., Galli, S.J. and Oettgen, H.C. (2005). Immune sensitization in the skin is enhanced by antigen-independent effects of IgE on mast cells. Novartis Found. Symp., 271, 15-24. https://doi.org/10.1002/9780470033449.ch3
  12. Chapes, S.K. and Ganta, R.R. (2008). Defining the immune response to Ehrlichia species using murine models. Vet Parasitol., 158, 344-359. https://doi.org/10.1016/j.vetpar.2008.09.028
  13. Chisaka, H., Morita, E., Yaegashi, N. and Sugamura, K. (2003). Parvovirus B19 and the pathogenesis of anaemia. Rev. Med. Virol., 13, 347-359. https://doi.org/10.1002/rmv.395
  14. Dusetti, N.J., Ortiz, E.M., Mallo, G.V., Dagorn, J.C. and Iovanna, J.L. (1995). Pancreatitis-associated protein I (PAP I), an acute phase protein induced by cytokines. Identification of two functional interleukin-6 response elements in the rat PAP I promoter region. J. Biol. Chem., 270, 22417-22421. https://doi.org/10.1074/jbc.270.38.22417
  15. Elenkov, I.J. and Chrousos, G.P. (2002). Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann. N. Y. Acad. Sci., 966, 290-303. https://doi.org/10.1111/j.1749-6632.2002.tb04229.x
  16. Finkelman, F.D., Holmes, J., Katona, I.M., Urban, J.F. Jr., Beckmann, M.P., Park, L.S., Schooley, K.A., Coffman, R.L., Mosmann, T.R. and Paul, W.E. (1990). Lymphokine control of in vivo immunoglobulin isotype selection. Annu. Rev. Immunol., 8, 303-333. https://doi.org/10.1146/annurev.iy.08.040190.001511
  17. Forsell, J.H. and Pestka, J.J. (1985). Relation of 8-ketotrichothecene and zearalenone analog structure to inhibition of mitogen- induced human lymphocyte blastogenesis. Appl. Environ. Microbiol., 50, 1304-1307.
  18. Ganapathi, M.K., Schultz, D., Mackiewicz, A., Samols, D., Hu, S.I., Brabenec, A., Macintyre, S.S. and Kushner, I. (1988). Heterogeneous nature of the acute phase response. Differential regulation of human serum amyloid A, C-reactive protein, and other acute phase proteins by cytokines in Hep 3B cells. J. Immunol., 141, 564-569.
  19. Heyes, M.P., Saito, K., Chen, C.Y., Proescholdt, M.G., Nowak, T.S. Jr., Li, J., Beagles, K.E., Proescholdt, M.A., Zito, M.A., Kawai, K. and Markey, S.P. (1997). Species heterogeneity between gerbils and rats: quinolinate production by microglia and astrocytes and accumulations in response to ischemic brain injury and systemic immune activation. J. Neurochem., 69, 1519-1529.
  20. Innes, E.A. (1997). Toxoplasmosis: comparative species susceptibility and host immune response. Comp. Immunol. Microbiol. Infect. Dis., 20, 131-138. https://doi.org/10.1016/S0147-9571(96)00038-0
  21. Kuiper-Goodman, T., Scott, P.M. and Watanabe, H. (1987). Risk assessment of the mycotoxin zearalenone. Regul. Toxicol. Pharmacol., 7, 253-306. https://doi.org/10.1016/0273-2300(87)90037-7
  22. Li, M., Cuff, C.F. and Pestka, J. (2005). Modulation of murine host response to enteric reovirus infection by the trichothecene deoxynivalenol. Toxicol. Sci., 87, 134-145. https://doi.org/10.1093/toxsci/kfi225
  23. Marin, D.E., Taranu, I., Burlacu, R., Manda, G., Motiu, M., Neagoe, I., Dragomir, C., Stancu, M. and Calin, L. (2011). Effects of zearalenone and its derivatives on porcine immune response. Toxicol. In Vitro, 25, 1981-1988. https://doi.org/10.1016/j.tiv.2011.06.022
  24. Marin, D.E., Taranu, I., Burlacu, R. and Tudor, D.S. (2010). Effects of zearalenone and its derivatives on the innate immune response of swine. Toxicon., 56, 956-963. https://doi.org/10.1016/j.toxicon.2010.06.020
  25. Marin, M.L., Murtha, J., Dong, W. and Pestka, J.J. (1996). Effects of mycotoxins on cytokine production and proliferation in EL-4 thymoma cells. J. Toxicol. Environ. Health, 48, 379-396. https://doi.org/10.1080/009841096161267
  26. O'Shea, J.J., Ma, A. and Lipsky, P. (2002). Cytokines and autoimmunity. Nat. Rev. Immunol., 2, 37-45. https://doi.org/10.1038/nri702
  27. Pestka, J.J. and Smolinski, A.T. (2005). Deoxynivalenol: toxicology and potential effects on humans. J. Toxicol. Environ. Health B, 8, 39-69. https://doi.org/10.1080/10937400590889458
  28. Pestka, J.J., Tai, J.H., Witt, M.F., Dixon, D.E. and Forsell, J.H. (1987). Suppression of immune response in the B6C3F1 mouse after dietary exposure to the Fusarium mycotoxins deoxynivalenol (vomitoxin) and zearalenone. Food Chem. Toxicol., 25, 297-304. https://doi.org/10.1016/0278-6915(87)90126-8
  29. Pestka, J.J., Zhou, H.R., Moon, Y. and Chung, Y.J. (2004). Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: unraveling a paradox. Toxicol. Lett., 153, 61-73. https://doi.org/10.1016/j.toxlet.2004.04.023
  30. Pinton, P., Accensi, F., Beauchamp, E., Cossalter, A.M., Callu, P., Grosjean, F. and Oswald, I.P. (2008). Ingestion of deoxynivalenol (DON) contaminated feed alters the pig vaccinal immune responses. Toxicol. Lett., 177, 215-222. https://doi.org/10.1016/j.toxlet.2008.01.015
  31. Prelusky, D.B., Scott, P.M., Trenholm, H.L. and Lawrence, G.A. (1990). Minimal transmission of zearalenone to milk of dairy cows. J. Environ. Sci. Health B, 25, 87-103. https://doi.org/10.1080/03601239009372678
  32. Shiao, R.T., McLeskey, S.B., Khera, S.Y., Wolfson, A. and Freter, C.E. (1996). Mechanisms of inhibition of IL-6-mediated immunoglobulin secretion by dexamethasone and suramin in human lymphoid and myeloma cell lines. Leuk. Lymphoma, 21, 293-303. https://doi.org/10.3109/10428199209067610
  33. Swamy, H.V., Smith, T.K. and MacDonald, E.J. (2004). Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on brain regional neurochemistry of starter pigs and broiler chickens. J. Anim. Sci., 82, 2131-2139. https://doi.org/10.2527/2004.8272131x
  34. Urraca, J.L., Benito- Pena, E., Perez-Conde, C., Moreno-Bondi, M.C. and Pestka, J.J. (2005). Analysis of zearalenone in cereal and Swine feed samples using an automated flow-through immunosensor. J. Agric. Food Chem., 53, 3338-3344. https://doi.org/10.1021/jf048092p
  35. Waldmann, T.A. (2006). The biology of interleukin-2 and interleukin- 15: implications for cancer therapy and vaccine design. Nat. Rev. Immunol., 6, 595-601. https://doi.org/10.1038/nri1901
  36. Zinedine, A., Soriano, J.M., Moltó, J.C. and Mañes, J. (2007). Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food Chem. Toxicol., 45, 1-18. https://doi.org/10.1016/j.fct.2006.07.030

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