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The influence of apple- and red-wine pomace rich diet on mRNA expression of inflammatory and apoptotic markers in different piglet organs

Published online by Cambridge University Press:  13 March 2007

J. Sehm
Affiliation:
Lehrstuhl für Physiologie, Wissenschaftszentrum Weihenstephan (WZW), Zentralinstitut für Ernährung- und Lebensmittelforschung (ZIEL), Technische Universität München (TUM), D-85354, Freising, Germany
H. Lindermayer
Affiliation:
Institut für Tierernährung und Futterwirtschaft, Bayerische Landesanstalt für Landwirtschaft (LfL), D-85586 Poing-Grub, Germany
H. H. D. Meyer
Affiliation:
Lehrstuhl für Physiologie, Wissenschaftszentrum Weihenstephan (WZW), Zentralinstitut für Ernährung- und Lebensmittelforschung (ZIEL), Technische Universität München (TUM), D-85354, Freising, Germany
M. W. Pfaffl*
Affiliation:
Lehrstuhl für Physiologie, Wissenschaftszentrum Weihenstephan (WZW), Zentralinstitut für Ernährung- und Lebensmittelforschung (ZIEL), Technische Universität München (TUM), D-85354, Freising, Germany
*
E-mail: [email protected]
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Abstract

Flavan-3-ols are a class of flavonoids that are widely distributed in fruits and beverages including red wine and apples. Consumption of flavanoid-rich food has been shown to exhibit anti-microbial, anti-oxidative, anti-inflammatory, and immune-modulating effects. To test the nutritional effects of flavanols on mRNA gene-expression of inflammatory and apoptotic marker genes, piglets were given two flavanoids-rich feeding regimens: a low flavanoid standard diet (SD) was compared with diets enriched with 3·5% apple pomace (APD) or 3·5% red-wine pomace (RWPD). The influence on mRNA expression levels was investigated in different immunological active tissues and in the gastro-intestinal tract (GIT). The investigation took place from 1 week prior weaning to 19 days post weaning in 78 piglets. The expression of expressed marker genes was determinate by one-step quantitative real-time (qRT-PCR): TNFα, NFκB as pro-inflammatory; IL10, as anti-inflammatory; caspase 3 as apoptosis; cyclin D1 as cell cycle marker; and nucleosome component histon H3 as reference gene.

The feeding regimens result in tissue individual regulation of mRNA gene expression in all investigated organs. It was discovered that there were significant differences between the applied diets and significant changes during feeding time curse. Both pomace treatments caused a significant up-regulation of all investigated genes in liver. The effect on mesenterial lymph nodes and spleen was not prominent. In the GIT, the treatment groups showed a inhibitory effects on gene expression mainly in stomach and jejunum (NFκB, cyclin D1 and caspase 3). In colon the trend of caspase 3 was positive with the greatest change in the RWPD group.

In jejunum and stomach the cell cycle turn over was reduced, whereas in liver the cell turn over was highly accelerate. The influence on inflammatory marker gene expression is mainly relevant in stomach. It is presume that both flavanoid rich feeding regimens have the potential to modulate the mRNA expressions of inflammatory, proliferation and apoptotic marker genes in the GIT and piglet organs.

Type
Research Article
Copyright
Copyright © British Society of Animal Science 2006

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References

Aarestrup, F.M. (1999) Association between the consumption of antimicrobial agents in animal husbandry and the occurrence of resistant bacteria among food animals International Journal of Antimicrobial Agents 12: 279285CrossRefGoogle ScholarPubMed
Adaim, A.Zhang, J.Lauren, D.R.Stanley, R.Skinner, M.A. (2005) Polyphenols and health using cell-based assays to aid in the development of new functional foods Asia Pacific Journal of Clinical Nutrition 14: 106.Google Scholar
Agarwal, R. (2000) Cell signaling and regulators of cell cycle as molecular targets for prostate cancer prevention by dietary agents Biochemical Pharmacology 60: 10511059CrossRefGoogle ScholarPubMed
Albanese, C.D'Amico, M.Reutens, A.T.Fu, M.Watanabe, G.Lee, R.J.Kitsis, R.N.Henglein, B.Avantaggiati, M.Somasundaram, K.Thimmapaya, B.Pestell, R.G. (1999) Activation of the cyclin D1 gene by the E1A-associated protein p300 through AP-1 inhibits cellular apoptosis Journal of Biological Chemistry 274: 3418634195CrossRefGoogle ScholarPubMed
Bach, Knudsen K.E. (2001) Development of antibiotic resistance and options to replace antimicrobials in animals diets Proceedings of the Nutrition Society 60: 291299Google Scholar
Baldwin, A.S. Jr (1996) The NFκB and IκB protein new discoveries and insights Annual Review of Immunology 14: 649683CrossRefGoogle Scholar
Barnes, P.J.Karin, M. (1997) Nuclear factor-kappa B: a pivotal transcription factoring chronic inflammatory diseases New England Journal of Medicine 336: 10661071CrossRefGoogle Scholar
Baud, V.Karin, M. (2001) Signal transduction by tumor necrosis factor and its relatives Trends in Cell Biology 11: 372377CrossRefGoogle ScholarPubMed
Beg, A.A.Baltimore, D. (1996) An essential role for NFκB in preventing TNFα-induced cell death Science 274: 782784CrossRefGoogle Scholar
Boudry, G.Peron, V. Le Huerou-Luron, I.Lalles, J.P.Seve, B. (2004) Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine Journal of Nutrition 9: 22562262CrossRefGoogle Scholar
Boyer, J.Liu, R.H. (2004) Apple phytochemicals and their health benefits Journal of Nutrition 12: 35Google Scholar
Carbonneau, M.A.Leger, C.L.Monnier, L.Bonnet, C.Michael, F.Fouret, G.Dedieu, F.Descomps, B. (1997) Supplementation with wine phenolic compounds increases the antioxidant capacity of plasma and vitamin E of low-density lipoprotein without changing the lipoprotein Cu(2+)-oxidizability: possible explanation by phenolic location European Journal of Clinical Nutrition 51: 982990CrossRefGoogle ScholarPubMed
Chang, H.Y.Yang, X. (2000) Proteases for cell suicidefunctions and regulation of caspases Microbiology and Molecular Biology Reviews 64: 821846CrossRefGoogle ScholarPubMed
Chen, M.S.Chen, D.Dou, Q.P. (2004) Inhibition of proteasome activity by various fruits and vegetables is associated with cancer cell death In Vivo 18: 7380Google ScholarPubMed
Collins, K.Jacks, T.Pavletich, N.P. (1997) The cell cycle and cancer Proceedings of the National Academy of Sciences of the United States of America 94: 27762778CrossRefGoogle ScholarPubMed
Damianaki, A.Bakogeorgou, E.Kampa, M.Notas, G.Hatzoglou, A.Panagiotou, S.Gemetzi, C.Kouroumalis, E.Martin, P.-M.Castanas, E. (2000) Potent inhibitory action of red wine polyphenols on human breast cancer cells Journal of Cellular Biochemistry 78: 4294413.0.CO;2-M>CrossRefGoogle ScholarPubMed
Eberhardt, M.Lee, C.Liu, R.H. (2000) Antioxidant activity of fresh apples Nature 405: 903904CrossRefGoogle ScholarPubMed
Enari, M.Sakahira, H.Yokoyama, H.Okawa, K.Iwamatsu, A.Nagata, S. (1998) A caspase-activated DNAs that degredes DNA during apoptosis, and its inhibitor ICAD Nature 391: 4350CrossRefGoogle Scholar
Fujiki, H.Suganuma, M.Okabe, S.Sueoka, E.Sueoka, N.Fujimoto, N.Goto, Y.Matsuyama, S.Imai, K.Nakachi, K. (2001) Cancer prevention with green tea and monitoring by a new biomarker, hnRNP B1 Mutation Research 480: 299304CrossRefGoogle ScholarPubMed
Fossum, C. (1998) Cytokines as markers for infections and their effect on growth performance and well-being in the pig Domestic Animal Endocrinology 15: 439444CrossRefGoogle ScholarPubMed
Ghosh, S.Karin, M. (2002) Missing pieces in the NF-kappaB puzzle Cell 109: 8196CrossRefGoogle ScholarPubMed
Guttridge, D.C.Albanese, C.Reuther, J.Y.Pestell, R.G.Baldwin, A.S. Jr, (1999) NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1 Molecular and Cellular Biology 19: 57855799CrossRefGoogle ScholarPubMed
Guyot, S.Marnet, N.Sanoner, P.Drilleau, J.F. (2003) Variability of the polyphenolic composition of cider apple (Malus domestica) fruits and juices Journal of Agricultural and Food Chemistry 51: 62406247CrossRefGoogle ScholarPubMed
Hammerstone, J.Lazarus, S.A.Mitchell, A.E.Rucker, R.Schmitz, H.H. (1999) Identification of procyanidins in cocoa ( Theobroma cacao ) and chocolate using high-performance liquid chromatography mass spectrometry Journal of Agricultural and Food Chemistry 47: 490496CrossRefGoogle ScholarPubMed
Hedemann, M.S.Kristiansen, E.Brunsgaard, G. (2002) Morphology of the large intestine of the pig: haustra versus taenia Annals of anatomy=Anatomischer Anzeiger: official organ of the Anatomische Gesellschaft 184: 401403CrossRefGoogle ScholarPubMed
Heczko, U.Carthy, C.M.O'Brien, B.A.Finlay, B.B. (2001) Decreased apoptosis in the ileum and ileal Peyer's patches: a feature after infection with rabbit enteropathogenic Escherichia coli O103 Infection and Immunity 69: 45804589CrossRefGoogle ScholarPubMed
Hinz, M.Krappmann, D.Eichten, A.Heder, A.Scheidereit, C.Strauss, M. (1999) NF-kappaB function in growth controlregulation of cyclin D1 expression and G0/G1-to-S-phase transition Molecular and Cellular Biology 19: 26902698CrossRefGoogle Scholar
Horstmann, S.Ferrari, S.Klempnauer, K.H. (2000) Regulation of B-Myb activity by cyclin D1 Oncogene 19: 298306CrossRefGoogle ScholarPubMed
Inoue, K.Sherr, C.J. (1998) Gene expression and cell cycle arrest mediated by transcription factor DMP1 is antagonized by D-type cyclins through a cyclin-dependent-kinase-independent mechanism Molecular and Cellular Biology 18: 15901600CrossRefGoogle ScholarPubMed
Jacks, T.Weinberg, R.A. (1996) Cell-cycle control and its watchman Nature 381: 643644CrossRefGoogle ScholarPubMed
Jung, H.C.Eckmann, L.Yang, S.K.Panja, A.Fierer, J. Morzycka-Wroblewska, E.Kagnoff, M.F. (1995) A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion Journal of Clinical Investigation 95: 5565CrossRefGoogle ScholarPubMed
Kotunia, A.Wolinski, J.Laubitz, D.Jurkowska, M.Rome, V.Guilloteau, P.Zabielski, R. (2004) Effect of sodium butyrate on the small intestine development in neonatal piglets feed by artificial sow Journal of Physiology and Pharmacology. Official Journal of the Polish Physiological Society 55: 5968Google ScholarPubMed
Lambert, J. Yang Ch. (2003) Mechanisms of cancer prevention by tea constituents Journal of Nutrition 133: 32623267CrossRefGoogle ScholarPubMed
Lawrence, T.Gilroy, D.W. Colville-Nash, P.R.Willoughby, D.A. (2002) Anti-inflammatory lipid mediators and insights into the resolution of inflammation Nature Reviews. Immunology 2: 787795CrossRefGoogle ScholarPubMed
Leitzmann, C. (2003) Nutrition ecology: the contribution of vegetarian diets The American Journal of Clinical Nutrition 78: 657659CrossRefGoogle ScholarPubMed
Livak, K.J.Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method Methods 25: 402408CrossRefGoogle Scholar
Liu, X.Zou, H.Slaighter, C.Wang, X. (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis Cell 89: 175184CrossRefGoogle ScholarPubMed
Macleod, K.F.Sherry, N.Hannon, G.Beach, D.Tokino, T.Kinzler, K.Vogelstein, B.Jacks, T. (1995) p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage Genes and Development 9: 935944CrossRefGoogle ScholarPubMed
Murtaugh, M.P.Baarsch, M.J.Zhou, Y.Scamurra, R.W.Lin, G. (1996) Inflammatory cytokines in animal health and disease Veterinary Immunology and Immunopathology 54: 4555CrossRefGoogle ScholarPubMed
Philpott, M.Ferguson, L.R. (2004) Immunonutrition and cancer Mutation Research 551: 2942 ReviewCrossRefGoogle ScholarPubMed
Pie, S.Lalles, J.P.Blazy, F.Laffitte, J.Sebe, B.Oswald, I.P. (2004) Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets Journal of Nutrition 134: 641647Google ScholarPubMed
Schmittgen, T.D. (2001) Real time quantitative PCR Methods 25: 383385CrossRefGoogle ScholarPubMed
Sigma Stat (1995) User's manual, version 5.0 Chicago, IL Jandel Scientific SoftwareGoogle Scholar
Santos-Buelga, C.Scalbert, A. (2000) Proanthocyanidins and tannin-like compounds: nature, occurrence, dietary intake and effects on nutrition and health Journal of the science of food and agriculture 80: 109411173.0.CO;2-1>CrossRefGoogle Scholar
Shaulian, E.Karin, M. (2001) AP-1 in cell proliferation and survival Oncogene 20: 23902400CrossRefGoogle ScholarPubMed
Scalbert, A.Williamson, J.R. (2000) Dietary intake and biovailabity of polyphenols Journal of Nutrition 130: 20732085CrossRefGoogle ScholarPubMed
Sehm, J.Polster, J.Pfaffl, M.W. (2005) Effects of varied EGCG and (+)-catechin concentrations on proinflammatory cytokines mRna expression in ConA-stimulated primary white blood cell cultures Journal of Agricultural and Food Chemistry 53: 69076911CrossRefGoogle ScholarPubMed
Sherr, C.J. (1994) G1 phase progression cycling on cue Cell 79: 551555CrossRefGoogle Scholar
Sherr, C.J.Roberts, J.M. (1999) CDK inhibitorspositive and negative regulators of G1-phase progression Genes and Development 13: 15011512CrossRefGoogle Scholar
Sherr, C.J.Roberts, J.M. (1995) Inhibitors of mammalian G1 cyclin-dependent kinases Genes and Development 9: 11491163CrossRefGoogle ScholarPubMed
Shrikhande, A.J. (2000) Wine by-products with heath benefits Food Research International 33: 469474CrossRefGoogle Scholar
Stadnyk, A.W. (1994) Cytokine production by epithelial cells The FASEB Journal: official publication of the Federation of American Societies for Experimental Biology 8: 10411047CrossRefGoogle ScholarPubMed
Stoll, D.A. (1997) Der Apfel Zürich Verlag NegiriGoogle Scholar
Treutter, D. (1989) chemical reaction detection of catechins and proanthocyanidins with 4-dimethylaminocinnamaldehyde Journal of Chromatography 467: 185193CrossRefGoogle Scholar
Van Antwerp, D.J.Martin, S.J.Kafri, T.Green, D.R.Verma, I.M. (1996) Suppression of TNF-alpha-induced apoptosis by NFκB Science 274: 787789CrossRefGoogle ScholarPubMed
Wang, C.Li, Z.Fu, M.Bouras, T.Pestell, R.G. (2004) Signal transduction mediated by cyclin D1from mitogens to cell proliferation: a molecular target with therapeutic potential Cancer Treatment and Research 119: 217237CrossRefGoogle Scholar
Waterhouse, A.L.Shirley, J.R.Donovan, J.L. (1996) Antioxidants in chocolate Lancet 348: 834CrossRefGoogle ScholarPubMed
Wolfe, K.Wu, X.Liu, R.H. (2003) Antioxidant activity of fresh peels Journal of Agricultural and Food Chemistry 51: 253256CrossRefGoogle ScholarPubMed
Yang, F.Oz, H.S.Barve, S. de Villiers, W.J.McClain, C.J.Varile, G.W. (2001) The green tea polyphenol (?)-epigallocatechin-3-gallate blocks nuclear factor-kappa B activation by inhibiting I kappa B kinase activity in the intestinal epithelial cell line IEC-6 Molecular Pharmacology 60: 528533Google ScholarPubMed
Zhang, J.M.Wie, Q.Zhao, X.Paterson, B.M. (1999) Coupling of the cell cycle and myogenesis through the cyclin D1-dependent interaction of myoD with cdk4 The EMBO Journal 18: 926933CrossRefGoogle ScholarPubMed