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Sex-related differences in the immune response of weanling piglets exposed to low doses of fumonisin extract

Published online by Cambridge University Press:  08 March 2007

Daniela E. Marin ,
Ionelia Taranu ,
Florentina Pascale ,
Alexandru Lionide ,
Radu Burlacu ,
Jean-Denis Bailly  and
Isabelle P. Oswald
Daniela E. Marin
Affiliation:
Laboratoire de Pharmacologie-ToxicologieUR 66Institut National de la Recherche AgronomiqueToulouseFrance IBNAInstitute of Biology and Animal NutritionBalotestiRomania
Ionelia Taranu
Affiliation:
Laboratoire de Pharmacologie-ToxicologieUR 66Institut National de la Recherche AgronomiqueToulouseFrance IBNAInstitute of Biology and Animal NutritionBalotestiRomania
Florentina Pascale
Affiliation:
Pasteur InstituteBucharestRomania
Alexandru Lionide
Affiliation:
IBNAInstitute of Biology and Animal NutritionBalotestiRomania
Radu Burlacu
Affiliation:
Institute of the Bovine Research DevelopmentBalotestiRomania
Jean-Denis Bailly
Affiliation:
Ecole Nationale VétérinaireToulouseFrance
Isabelle P. Oswald*
Affiliation:
Laboratoire de Pharmacologie-ToxicologieUR 66Institut National de la Recherche AgronomiqueToulouseFrance
*
*Corresponding author: Dr Isabelle P. Oswald, fax +33 5 61 28 53 10, email ioswald@toulouse.inra.fr
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Abstract

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Fumonisin B1 (FB1) is a mycotoxin produced by Fusarium verticillioides, a fungus that commonly contaminates maize. Sex-related effects of FB1 have been observed with respect to carcinogenicity in rodents, to performances in pigs and immunosuppression in mice. In the present study the sex-related effect of FB1 on the pig immune response was determined. Female and castrated male piglets received for 28d either control feed or feed contaminated with 8mg FB1/kgfeed in the form of F. verticillioidesculture material. At day 7 and day 21, animals were immunised subcutaneously with a Mycoplasma agalactiae vaccine. Ingestion of FB1-contaminated feed significantly decreased weight gain in males but had no effect in females. No sex-related difference was observed in biochemical parameters, but a higher level of creatinine was noted in toxin-treated animals. FB1 also altered the pig immune response in a sex-specific manner. In males, ingestion of FB1-contaminated feed significantly decreased specific antibody levels after vaccination as well as the mRNA expression level of IL-10. In females, the toxin has no effect on specific antibodies or on cytokine mRNA levels. The results of the present study indicatethat FB1 is immunosuppressive in pigs. The magnitude of this FB1-induced immunosuppression is highly dependent on sex, with males being more susceptible than females.

Keywords

FumonisinMycotoxinsImmunosuppressionFood contaminationPigGender-related effects
Type
Research Article
Information
British Journal of Nutrition , Volume 95 , Issue 6 , June 2006 , pp. 1185 - 1192
Copyright
Copyright © The Nutrition Society 2006

References

Abbas, AK, Murphy, KM & Sher, AFunctional diversity of helper T lymphocytes. Nature 1996 383, 787–793.Google Scholar
Bhandari, N, Brown, CC & Sharma, RPFumonisin B1-induced localized activation of cytokine network in mouse liver. Food Chem Toxicol 2002 40, 1483–1490.CrossRefGoogle ScholarPubMed
Bhandari, N, He, Q & Sharma, RPGender-related differences in subacute fumonisin B1 hepatotoxicity in BALB/c mice. Toxicology 2001 165, 195–204.CrossRefGoogle ScholarPubMed
Bolger, M, Coker, RD, Dinovi, M, Gaylor, D, Gelderblom, MO, Paster, N, Riley, RT, Shephard, G & Speijers, JAFumonisins. In Safety Evaluation of Certain Mycotoxins in Food, Food and Agriculture Organization of the United Nations, paper no. 74. World Health Organization Food Additives, series 47, 103–279Geneva: WHO FOOD Additives. 2001Google Scholar
Bondy, G, Suzuki, C, Barker, M, Armstrong, C, Fernie, S, Hierlihy, L, Rowsell, P & Mueller, RToxicity of fumonisin B1 administered intraperitoneally to male Sprague–Dawley rats. Food Chem Toxicol 1995 33, 653–665.Google Scholar
Bouhet, S, Hourcade, E, Loiseau, N, Fikri, A, Martinez, S, Roselli, M, Galtier, P, Mengheri, E & Oswald, IPThe mycotoxin, fumonisin B1 alters the proliferation and the barrier function of porcine intestinal epithelial cells. Toxicol Sci 2004 77, 165–171.CrossRefGoogle ScholarPubMed
Bouhet, S & Oswald, IPEffects of mycotoxins, fungal food contaminants, on the intestinal epithelial cell derived innate immune response. Vet Immunol Immunopathol Bouhet 2005 108, 199–209.Google Scholar
Darwich, L, Pie, S, Rovira, A, Segales, J, Domingo, M, Oswald, IP & Mateu, ECytokine mRNA expression profiles in lymphoid tissues of pigs naturally affected by postweaning multisystemic wasting syndrome. J Gen Virol 2003 84, 2117–2125.Google Scholar
Desai, Fumonisins and fumonisin analogs as inhibitors of ceramide synthase and inducers of apoptosis. Biochim Biophys Acta 2002 1585, 188–192CrossRefGoogle ScholarPubMed
Diehl, S & Rincon, MThe two faces of IL-6 on Th1/Th2 differentiation. Mol Immunol 2002 39, 531–536.CrossRefGoogle ScholarPubMed
Dozois, CM, Oswald, E, Gautier, N, Serthelon, JP, Fairbrother, JM & Oswald, IPA reverse transcription-polymerase chain reaction method to analyse porcine cytokine gene expression. Vet Immunol Immunopathol 1997 58, 287–300.CrossRefGoogle ScholarPubMed
Fink-Gremmels, JMycotoxins: their implications for human and animal health. Vet Q 1999 21, 115–120.Google Scholar
Foey, & Brennan, Conventional protein kinase C and atypical protein kinase Czeta differentially regulate macrophage production of tumour necrosis factor-alpha and interleukin-10. Immunology 2002 112, 44–53.CrossRefGoogle Scholar
Fournout, S, Dozois, CM, Odin, MLack of a role of cytotoxic necrotizing factor 1 toxin from Escherichia coli in bacterial pathogenicity and host cytokine response in infected germfree piglets. Infect Immun 2000 68, 839–847.Google Scholar
Gopee, NV & Sharma, RPSphingoid bases and their phosphates: transient activation and delayed repression of protein kinase C isoforms and their possible involvement in fumonisin B1 cytotoxicity. Toxicology 2003 187, 239–250.Google Scholar
Halloy, DJ, Gustin, PG, Bouhet, S & Oswald, IPOral exposure to culture material extract containing fumonisins predisposes swine to the development of pneumonitis caused by Pasteurella multocida. Toxicology 2005 213, 34–44.Google Scholar
Haschek, WM, Gumprecht, LA, Smith, G, Tumbleson, ME & Constable, PDFumonisin toxicosis in swine: an overview of porcine pulmonary edema and current perspectives. Environ Health Perspect, 2001 109, 251–257.Google Scholar
He, Q, Bhandari, N & Sharma, RPFumonisin B1 alters sphingolipid metabolism and tumor necrosis factor alpha expression in heart and lung of mice. Life Sci 2002 71, 2015–2023.CrossRefGoogle ScholarPubMed
Howard, PC, Eppley, RM, Stack, ME, Warbritton, A, Voss, KA, Lorentzen, RJ, Kovach, RM & Bucci, TJFumonisin B1 carcinogenity in a two-year feeding study using F344 rats and B6C3F1 mice. Environ Health Perspect 2001 2, 277–282.Google Scholar
International Agency for Research on Cancer Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. In IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 275–366, Lyon, France: IARC Press, 2002.Google Scholar
International Programme on Chemical Safety Fumonisin B1. In Environmental Health Criteria, no. 219, Geneva: WHO. 2000 43–50Google Scholar
Johnson, VJ & Sharma, RPGender-dependent immunosuppression following subacute exposure to fumonisin B1. Int Immunopharmacol 2001 11, 2023–2034.Google Scholar
Kanda, NGangliosides GD1a and GM3 induce interleukin-10 production by human T cells. Biochem Biophys Res Commun 1999 256, 41–44.CrossRefGoogle ScholarPubMed
Kanda, N & Watanabe, SGanglioside GD1a enhances immunoglobulin production by human blood mononuclear cells. Exp Hematol 2000 28, 672–679.CrossRefGoogle Scholar
Kanda, N & Watanabe, SGangliosides GD1b, GT1b, and GQ1b enhance IL-2 and IFN-gamma production and suppress IL-4 and IL-5 production in phytohemagglutinin-stimulated human T cells. J Immunol 2001 166, 72–80.CrossRefGoogle ScholarPubMed
Li, YC, Ledoux, DR, Bermudez, AJ,Fritsche, KL & Rottinghaus, GEThe individual and combined effects of fumonisin B1 and moniliformin on performance and selected immune parameters in turkey poults. Poult Sci 2000 79, 871–878.Google Scholar
Marin, DE, Taranu, I, Bunaciu, RP, Pascale, F, Tudor, DS, Avram, N, Sarca, M, Cureu, I, Criste, RD, Suta, V & Oswald, IPChanges in performance, blood parameters, humoral and cellular immune responses in weanling piglets exposed to low doses of aflatoxin. J Anim Sci, 2002 80, 1250–1257.Google Scholar
Martinova, EA & Merrill, AH Jr Fumonisin B1 alters sphingolipid metabolism and immune function in BALB/c mice: immunological responses to fumonisin B1. Mycopathologia 1995 130, 163–170.Google Scholar
Merrill, AH Jr, Sullards, MC, Wang, E, Voss, KA & Riley, RTSphingolipid metabolism: roles in signal transduction and disruption by fumonisins. Environ Health Perspect 2001 109, 283–289.Google Scholar
Mocellin, S, Panelli, MC, Wang, E, Nagorsen, D & Marincola, FMThe dual role of IL-10. Trends Immunol 2003 24, 36–43.CrossRefGoogle ScholarPubMed
Murphy, PA, Hendrich, S, Hopmans, EC, Hauck, CC, Lu, Z, Buseman, G & Munkvold, GEffect of processing on fumonisin content of corn. Adv Exp Med Biol 1996 392, 323–334.Google Scholar
Murphy, PA, Rice, LG & Ross, PFFumonisin B1, B2 and B3 content of Iowa, Wisconsin and Illinois corn and corn screening. J Agric Food Chem 1993 41, 263–266.Google Scholar
Nelms, K, Ryan, J, Keegan, A, Huang, H & Paul, WEInterleukin- 4 receptor signalling mechanisms and their biological signifi- cance. Adv Exp Med Biol 1998 452, 37–43.Google Scholar
Oswald, IP, Desautels, C, Laffitte, J, Fournout, S, Peres, SY, Odin, M, LeBars, P, Le Bars, J & Fairbrother, JMMycotoxin fumonisin B1 increases intestinal colonization by pathogenic Escherichia coli in pigs. Appl Environ Microbiol 2003 69, 5870–5874.CrossRefGoogle ScholarPubMed
Oswald, IP, Marin, DE, Bouhet, S, Pinton, P, Taranu, I & Accensi, FImmunotoxicological risk of mycotoxins for domestic animals. Food Addit Contam 2005 22, 354–360.CrossRefGoogle ScholarPubMed
Pié, S, Lalles, JP, Blazy, F, Laffitte, J, Sève, B & Oswald, IPWeaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J Nutr 2004 134, 641–647.Google ScholarPubMed
Qureshi, MA, Garlich, JD, Hagler, WM Jr & Weinstock, DFusarium proliferatum culture material alters several production and immune performance parameters in White Leghorn chickens. Immunopharmacol Immunotoxicol 1995 17, 791–804.CrossRefGoogle ScholarPubMed
Riley, RT, Voss, KA,Norred, WP,Sharma, RP, Wang, E & Merrill, AHFumonisins: mechanism of mycotoxicity. Rev Med Vet 1998 149, 617–626.Google Scholar
Rotter, BA, Thompson, BK,Prelusky, DB, Trenholm, HL, Stewart, B, Miller, JD & Savard, MEResponse of growing swine to dietary exposure to pure fumonisin B1 during an eight-week period: growth and clinical parameters. Nat Toxins 1996 4, 42–50.Google Scholar
Scudamore, KA, Nawaz, S & Hetmanski, MTMycotoxins ingredients of animal feeding stuffs: II. Determination of mycotoxins in maize and maize products. Food Addit Contam 1990 15, 30–55.Google Scholar
Taranu, I, Marin, DE, Bouhet, S, Pascale, F, Bailly, JD, Miller, JD, Pinton, P & Oswald, IPMycotoxin fumonisin B1 alters the cytokine profile and decreases vaccinal antibody titer in pigs. Toxicol Sci 2005 84, 301–307.CrossRefGoogle ScholarPubMed
Tokura, Y, Wakita, H, Yagi, H, Nishimura, K, Furukawa, F & Takigawa, MTh2 suppressor cells are more susceptible to sphingosine than Th1 cells in murine contact photosensitivity. J Invest Dermatol 1996 107, 34–40.Google Scholar
Tornyos, G, Kovacs, M, Rusvai, M, Horn, P, Fodor, J & Kovacs, FEffect of dietary fumonisin B1 on certain immune parameters of weaned pigs. Acta Vet Hung 2003 51, 171–179.CrossRefGoogle ScholarPubMed
Tran, ST, Bailly, JD,Tardieu, D, Durand, S, Benard, G & Guerre, PSphinganine to sphingosine ratio and predictive biochemical markers of fumonisin B1 exposure in ducks. Chem Biol Interact 2003 146, 61–72.Google Scholar
Tryphonas, H, Bondy, G, Miller, JD, Lacroix, F, Hodgen, M, Mcguire, P, Fernie, S, Miller, D & Hayward, SEffects of fumonisin B1 on the immune system of Sprague–Dawley rats following a 14-day oral (gavage) exposure. Fundam Appl Toxicol 1997 39, 53–59.CrossRefGoogle ScholarPubMed
Zomborszky, MK, Vetesi, F, Repa, I, Kovacs, F, Bata, A, Horn, P, Toth, A & Romvari, RExperiment to determine limits of tolerance for fumonisin B11 in weaned piglets. J Vet Med 2000 47, 277–286.CrossRefGoogle Scholar
Zomborszky-Kovacs, M, Vetesi, F, Horn, P, Repa, I & Kovacs, FEffects of prolonged exposure to low-dose fumonisin B1in pigs. J Vet Med 2002 49, 197–201.Google Scholar