Immunotoxicity of aflatoxin B1: Impairment of the cell-mediated response to vaccine antigen and modulation of cytokine expression

Toxicology and Applied Pharmacology

Volumn 231, Issue 2, 2008, Pages 142-149

  Meissonnier, Guylaine M ^a,b   Pinton, Philippe ^a   Laffitte, Joëlle ^a   Cossalter, Anne Marie ^a   Gong, Yun Yun ^c   Wild, Christopher P ^c   Bertin, Gérard ^b   Galtier, Pierre ^a   Oswald, Isabelle P ^a  

^a CEMAGREF   (France)

^b ALLTECH INC   (United States)

^c Leeds Institute of Genetics   (United Kingdom)

Author keywords

Aflatoxin B1; Cytokines; Lymphocytes; Real time PCR; Spleen; Swine; Vaccination

Indexed keywords

AFLATOXIN B1; ANTIGEN; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; OVALBUMIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOMODULATION; IMMUNOTOXICITY; LYMPHOCYTE; LYMPHOCYTE PROLIFERATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; SPLEEN; SWINE; UPREGULATION; VACCINATION;

AFLATOXIN B1; ANIMALS; ANTIBODY FORMATION; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; IMMUNITY, CELLULAR; IMMUNOGLOBULIN ISOTYPES; IMMUNOTOXINS; LYMPHOCYTES; MALE; MITOGENS; OVALBUMIN; POLYMERASE CHAIN REACTION; SPLEEN; SWINE; VACCINES;

ASPERGILLUS FLAVUS; SUIDAE;

EID: 49749088725     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2008.04.004     Document Type: Article

References (62)

1. Accensi F., Pinton P., Callu P., Abella-Bourges N., Guelfi J.F., Grosjean F., and Oswald I.P. Ingestion of low doses of deoxynivalenol does not affect hematological, biochemical, or immune responses of piglets. J. Anim. Sci. 84 (2006) 1935-1942
2. Almond G.W. Research applications using pigs. Vet. Clin. North Am. Food Anim. Pract. 12 (1996) 707-716
3. Atkuri K.R., Herzenberg L.A., Niemi A.K., and Cowan T. Importance of culturing primary lymphocytes at physiological oxygen levels. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 4547-4552
4. Batra P., Pruthi A.K., and Sadana J.R. Effect of aflatoxin B1 on the efficacy of turkey herpesvirus vaccine against Marek's disease. Res. Vet. Sci. 51 (1991) 115-119
5. Bimczok D., Rau H., Wundrack N., Naumann M., Rothkötter H.J., McCullough K., and Summerfield A. Cholera toxin promotes the generation of semi-mature porcine monocytes-derived dendritic cells that are unable to stimulate T cells. Vet. Res. 38 (2007) 597-612
6. Bondy G.S., and Pestka J.J. Immunomodulation by fungal toxins. J. Toxicol. Environ. Health. B Crit. Rev. 3 (2000) 109-143
7. Caldwell C.C., Kojima H., Lukashev D., Armstrong J., Farber M., Apasov S.G., and Sitkovsky M.V. Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J. Immunol. 167 (2001) 6140-6149
8. CAST. Mycotoxins: risks in plants, animals and human systems. Council for Agricultural Science and Technology (2003), Ames, Iowa
9. Chapot B., and Wild C.P. ELISA for quantification of aflatoxin-albumin adducts and their application to human exposure assessment. In: Warhol M., van Velzen D., and Bullock G.R. (Eds). Techniques in Diagnostic Pathology vol. 2 (1991), Academic Press, San Diego CA 135-155
10. Cysewski S.J., Wood R.L., Pier A.C., and Baetz A.L. Effects of aflatoxin on the development of acquired immunity to swine erysipelas. Am. J. Vet. Res. 39 (1978) 445-448
11. Dimitri R.A., and Gabal M.A. Immunosuppressant activity of aflatoxin ingestion in rabbits measured by response to Mycobacterium bovis antigen I. Cell mediated immune response measured by skin test reaction. Vet. Hum. Toxicol. 38 (1996) 333-336
12. Dugyala R.R., and Sharma R.P. The effect of aflatoxin B1 on cytokine mRNA and corresponding protein levels in peritoneal macrophages and splenic lymphocytes. Int. J. Immunopharmacol. 18 (1996) 599-608
13. Ellinger-Ziegelbauer H., Stuart B., Wahle B., Bomann W., and Ahr H.J. Characteristic expression profiles induced by genotoxic carcinogens in rat liver. Toxicol. Sci. 77 (2004) 19-34
14. Fournout S., Dozois C.M., Yerle M., Pinton P., Fairbrother J.M., Oswald E., and Oswald I.P. Cloning, chromosomal location, and tissue expression of the gene for pig interleukin-18. Immunogenetics 51 (2000) 358-365
15. Ghosh R.C., Chauhan H.V., and Jha G.J. Suppression of cell-mediated immunity by purified aflatoxin B1 in broiler chicks. Vet. Immunol. Immunopathol. 28 (1991) 165-172
16. Giambrone J.J., Diener U.L., Davis N.D., Panangala V.S., and Hoerr F.J. Effects of purified aflatoxin on broiler chickens. Poult. Sci. 64 (1985) 852-858
17. Gong Y., Hounsa A., Egal S., Turner P.C., Sutcliffe A.E., Hall A.J., Cardwell K., and Wild C.P. Postweaning exposure to aflatoxin results in impaired child growth: a longitudinal study in Benin, West Africa. Environ. Health Perspect. 112 (2004) 1334-1338
18. Gong Y.Y., Egal S., Hounsa A., Turner P.C., Hall A.J., Cardwell K.F., and Wild C.P. Determinants of aflatoxin exposure in young children from Benin and Togo, West Africa: the critical role of weaning. Int. J. Epidemiol. 32 (2003) 556-562
19. Groopman J.D., and Kensler T.W. Role of metabolism and viruses in aflatoxin-induced liver cancer. Toxicol. Appl. Pharmacol. 206 (2005) 131-137
20. Harizi H., and Gualde N. Pivotal role of PGE2 and IL-10 in the cross-regulation of dendritic cell-derived inflammatory mediators. Cell. Mol. Immunol. 3 (2006) 271-277
21. Harvey R.B., Edrington T.S., Kubena L.F., Elissalde M.H., and Rottinghaus G.E. Influence of aflatoxin and fumonisin B1-containing culture material on growing barrows. Am. J. Vet. Res. 56 (1995) 1668-1672
22. Harvey R.B., Huff W.E., Kubena L.F., Corrier D.E., and Phillips T.D. Progression of aflatoxicosis in growing barrows. Am. J. Vet. Res. 49 (1988) 482-487
23. Hinton D.M., Myers M.J., Raybourne R.A., Francke-Carroll S., Sotomayor R.E., Shaddock J., Warbritton A., and Chou M.W. Immunotoxicity of aflatoxin B1 in rats: effects on lymphocytes and the inflammatory response in a chronic intermittent dosing study. Toxicol. Sci. 73 (2003) 362-377
24. IARC. Aflatoxins. IARC Monographs 82 (2002) 171
25. Jakab G.J., Hmieleski R.R., Zarba A., Hemenway D.R., and Groopman J.D. Respiratory aflatoxicosis: suppression of pulmonary and systemic host defenses in rats and mice. Toxicol. Appl. Pharmacol. 125 (1994) 198-205
26. Jamin A., Gorin S., Le Potier M.F., and Kuntz-Simon G. Characterization of conventional and plasmacytoid dendritic cells in swine secondary lymphoid organs and blood. Vet. Immunol. Immunopathol. 114 (2006) 224-237
27. Jiang Y., Jolly P.E., Ellis W.O., Wang J.S., Phillips T.D., and Williams J.H. Aflatoxin B1 albumin adduct levels and cellular immune status in Ghanaians. Int. Immunol. 17 (2005) 807-814
28. Joens L.A., Pier A.C., and Cutlip R.C. Effects of aflatoxin consumption on the clinical course of swine dysentery. Am. J. Vet. Res. 42 (1981) 1170-1172
29. Kurlander R.J., Tawab A., Fan Y., Carter C.S., and Read E.J. A functional comparison of mature human dendritic cells prepared in fluorinated ethylene-propylene bags or polystyrene flasks. Transfusion 46 (2006) 1494-1504
30. Lewis L., Onsongo M., Njapau H., Schurz-Rogers H., Luber G., Kieszak S., Nyamongo J., Backer L., Dahiye A.M., Misore A., DeCock K., and Rubin C. Aflatoxin contamination of commercial maize products during an outbreak of acute aflatoxicosis in eastern and central Kenya. Environ. Health Perspect. 113 (2005) 1763-1767
31. Liu B.H., Yu F.Y., Chan M.H., and Yang Y.L. The effects of mycotoxins, fumonisin B1 and aflatoxin B1, on primary swine alveolar macrophages. Toxicol. Appl. Pharmacol. 180 (2002) 197-204
32. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(- Delta Delta C(T)) Method. Methods 25 (2001) 402-408
33. Marin D.E., Taranu I., Bunaciu R.P., Pascale F., Tudor D.S., Avram N., Sarca M., Cureu I., Criste R.D., Suta V., and Oswald I.P. Changes in performance, blood parameters, humoral and cellular immune responses in weanling piglets exposed to low doses of aflatoxin. J. Anim. Sci. 80 (2002) 1250-1257
34. Marin D.E., Taranu I., Pascale F., Lionide A., Burlacu R., Bailly J.D., and Oswald I.P. Sex-related differences in the immune response of weanling piglets exposed to low doses of fumonisin extract. Br. J. Nutr. 95 (2006) 1185-1192
35. Meissonnier G.M., Marin D.E., Galtier P., Bertin G., and Oswald I.P. Modulation of the immune response by a group of fungal food contaminant, the aflatoxins. In: Mengheri E., Roselli M., Britti M.S., and Finamore A. (Eds). Nutrition and Immunity (2006), Research Signpost, Kerala 147-166
36. Meissonnier G.M., Laffitte J., Loiseau N., Benoit E., Raymond I., Pinton P., Cossalter A.M., Bertin G., Oswald I.P., and Galtier P. Selective impairment of drug-metabolizing enzymes in pig liver during subchronic dietary exposure to aflatoxin B1. Food Chem. Toxicol. 45 (2007) 2145-2154
37. Meissonnier G.M., Laffitte J., Raymond I., Benoit E., Cossalter A.-M., Pinton P., Bertin G., Oswald I.P., and Galtier P. Subclinical doses of T-2 toxin impair acquired immune response and liver cytochrome P450 in pigs. Toxicology 247 (2008) 46-54
38. Miller D.M., Stuart B.P., and Crowell W.A. Experimental aflatoxicosis in swine: morphological and clinical pathological results. Can. J. Comp. Med. 45 (1981) 343-351
39. Moon E.Y., Rhee D.K., and Pyo S. Inhibition of various functions in murine peritoneal macrophages by aflatoxin B1 exposure in vivo. Int. J. Immunopharmacol. 21 (1999) 47-58
40. Mosmann T.R. Interleukin-10. In: Thomson A.W. (Ed). The Cytokine Handbook (1994), Academic Press Limited, London, UK
41. Oswald I.P., and Comera C. Immunotoxicity of mycotoxins. Rev. Med. Vet. 149 (1998) 585-590
42. Oswald I.P., Desautels C., Laffitte J., Fournout S., Peres S.Y., Odin M., Le Bars P., Le Bars J., and Fairbrother J.M. Mycotoxin fumonisin B1 increases intestinal colonization by pathogenic Escherichia coli in pigs. Appl. Environ. Microbiol. 69 (2003) 5870-5874
43. Oswald I.P., Dozois C.M., Barlagne R., Fournout S., Johansen M.V., and Bogh H.O. Cytokine mRNA expression in pigs infected with Schistosoma japonicum. Parasitology 122 (2001) 299-307
44. Panangala V.S., Giambrone J.J., Diener U.L., Davis N.D., Hoerr F.J., Mitra A., Schultz R.D., and Wilt G.R. Effects of aflatoxin on the growth performance and immune responses of weanling swine. Am. J. Vet. Res. 47 (1986) 2062-2067
45. Park S.J., Nakagawa T., Kitamura H., Atsumi T., Kamon H., Sawa S., Kamimura D., Ueda N., Iwakura Y., Ishihara K., Murakami M., and Hirano T. IL-6 regulates in vivo dendritic cell differentiation through STAT3 activation. J. Immunol. 173 (2004) 3844-3854
46. Pestka S., Krause C.D., Sarkar D., Walter M.R., Shi Y., and Fisher P.B. Interleukin-10 and related cytokines and receptors. Annu. Rev. Immunol. 22 (2004) 929-979
47. Pinton P., Accensi F., Beauchamps E., Cossalter A.-M., Callu P., Grosjean F., and Oswald I.P. Ingestion of deoxynivalenol (DON) contaminated feed alters the pig vaccinal immune responses. Tox. Letters 177 (2008) 215-222
48. Raisuddin S., Singh K.P., Zaidi S.I., Paul B.N., and Ray P.K. Immunosuppressive effects of aflatoxin in growing rats. Mycopathologia 124 (1993) 189-194
49. Rossano F., Ortega De Luna L., Buommino E., Cusumano V., Losi E., and Catania M.R. Secondary metabolites of Aspergillus exert immunobiological effects on human monocytes. Res. Microbiol. 150 (1999) 13-19
50. Rothkotter H.J., Sowa E., and Pabst R. The pig as a model of developmental immunology. Hum. Exp. Toxicol. 21 (2002) 533-536
51. Royaee A.R., Husmann R.J., Dawson H.D., Calzada-Nova G., Schnitzlein W.M., Zuckermann F.A., and Lunney J.K. Deciphering the involvement of innate immune factors in the development of the host response to PRRSV vaccination. Vet. Immunol. Immunopathol. 102 (2004) 199-216
52. Sandhu B.S., Singh H., and Singh B. Pathological studies in broiler chicks fed aflatoxin or ochratoxin and inoculated with inclusion body hepatitis virus singly and in concurrence. Vet. Res. Commun. 19 (1995) 27-37
53. Takahashi M., and Kobayashi Y. Cytokine production in association with phagocytosis of apoptotic cells by immature dendritic cells. Cell. Immunol. 226 (2003) 105-115
54. Taranu I., Marin D.E., Bouhet S., Pascale F., Bailly J.D., Miller J.D., Pinton P., and Oswald I.P. Mycotoxin fumonisin B1 alters the cytokine profile and decreases the vaccinal antibody titer in pigs. Toxicol. Sci. 84 (2005) 301-307
55. Turner P.C., Moore S.E., Hall A.J., Prentice A.M., and Wild C.P. Modification of immune function through exposure to dietary aflatoxin in Gambian children. Environ. Health Perspect. 111 (2003) 217-220
56. van Heugten E., Spears J.W., Coffey M.T., Kegley E.B., and Qureshi M.A. The effect of methionine and aflatoxin on immune function in weanling pigs. J. Anim. Sci. 72 (1994) 658-664
57. Venturini M.C., Perfumo C.J., Risso M.A., Gomez C.M., Piscopo M.V., Sala de Miguel M., and Godoy H. Effect of aflatoxin B1 on resistance induced by Bordetella bronchiseptica vaccine in rabbits. Vet. Microbiol. 25 (1990) 209-216
58. Venturini M.C., Quiroga M.A., Risso M.A., Lorenzo C.D., Omata Y., Venturini L., and Godoy H. Mycotoxin T-2 and aflatoxin B1 as immunosuppressors in mice chronically infected with Toxoplasma gondii. J. Comp. Pathol. 115 (1996) 229-237
59. von der Hardt K., Kandler M.A., Popp K., Schoof E., Chada M., Rascher W., and Dotsch J. Aerosolized adrenomedullin suppresses pulmonary transforming growth factor-beta1 and interleukin-1 beta gene expression in vivo. Eur. J. Pharmacol. 457 (2002) 71-76
60. von der Hardt K., Kandler M.A., Fink L., Schoof E., Dotsch J., Brandenstein O., Bohle R.M., and Rascher W. High frequency oscillatory ventilation suppresses inflammatory response in lung tissue and microdissected alveolar macrophages in surfactant depleted piglets. Pediatr. Res. 55 (2004) 339-346
61. Watzl B., Neudecker C., Hansch G.M., Rechkemmer G., and Pool-Zobel B.L. Short-term moderate aflatoxin B1 exposure has only minor effects on the gut-associated lymphoid tissue of Brown Norway rats. Toxicology 138 (1999) 93-102
62. Wild C.P., Yin F., Turner P.C., Chemin I., Chapot B., Mendy M., Whittle H., Kirk G.D., and Hall A.J. Environmental and genetic determinants of aflatoxin-albumin adducts in the Gambia. Int. J. Cancer 86 (2000) 1-7