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Effect of feed supplementation with live yeast on the intestinal transcriptome profile of weaning pigs orally challenged with Escherichia coli F4

Published online by Cambridge University Press:  30 June 2016

P. Trevisi ,
R. Latorre ,
D. Priori ,
D. Luise ,
I. Archetti ,
M. Mazzoni ,
R. D’Inca  and
P. Bosi
P. Trevisi*
Affiliation:
Department of Agricultural and Food Science, University of Bologna, v. Fanin 46, 40127 Bologna, Italy
R. Latorre
Affiliation:
Veterinary Medical Sciences, University of Bologna, v. Tolara di Sopra 50, 40064 Ozzano dell’Emilia, Italy
D. Priori
Affiliation:
Department of Agricultural and Food Science, University of Bologna, v. Fanin 46, 40127 Bologna, Italy
D. Luise
Affiliation:
Department of Agricultural and Food Science, University of Bologna, v. Fanin 46, 40127 Bologna, Italy
I. Archetti
Affiliation:
Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna Bruno Ubertini, V. Bianchi 9, 25124 Brescia, Italy
M. Mazzoni
Affiliation:
Veterinary Medical Sciences, University of Bologna, v. Tolara di Sopra 50, 40064 Ozzano dell’Emilia, Italy
R. D’Inca
Affiliation:
Société Industrielle Lesaffre, Phileo–Lesaffre Animal Care, 137 rue Gabriel Péri, 59700 Marcq-en-Baroeul, France
P. Bosi
Affiliation:
Department of Agricultural and Food Science, University of Bologna, v. Fanin 46, 40127 Bologna, Italy
*
†E-mail: paolo.trevisi@unibo.it
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Abstract

The ability of live yeasts to modulate pig intestinal cell signals in response to infection with Escherichia coli F4ac (ETEC) has not been studied in-depth. The aim of this trial was to evaluate the effect of Saccharomyces cerevisiae CNCM I-4407 (Sc), supplied at different times, on the transcriptome profile of the jejunal mucosa of pigs 24 h after infection with ETEC. In total, 20 piglets selected to be ETEC-susceptible were weaned at 24 days of age (day 0) and allotted by litter to one of following groups: control (CO), CO+colistin (AB), CO+5×1010 colony-forming unit (CFU) Sc/kg feed, from day 0 (PR) and CO+5×1010 CFU Sc/kg feed from day 7 (CM). On day 7, the pigs were orally challenged with ETEC and were slaughtered 24 h later after blood sampling for haptoglobin (Hp) and C-reactive protein (CRP) determination. The jejunal mucosa was sampled (1) for morphometry; (2) for quantification of proliferation, apoptosis and zonula occludens (ZO-1); (3) to carry out the microarray analysis. A functional analysis was carried out using Gene Set Enrichment Analysis. The normalized enrichment score (NES) was calculated for each gene set, and statistical significance was defined when the False Discovery Rate % was <25 and P-values of NES were <0.05. The blood concentration of CRP and Hp, and the score for ZO-1 integrity on the jejunal villi did not differ between groups. The intestinal crypts were deeper in the AB (P=0.05) and the yeast groups (P<0.05) than in the CO group. Antibiotic treatment increased the number of mitotic cells in intestinal villi as compared with the control group (P<0.05). The PR group tended to increase the mitotic cells in villi and crypts and tended to reduce the cells in apoptosis as compared with the CM group. The transcriptome profiles of the AB and PR groups were similar. In both groups, the gene sets involved in mitosis and in mitochondria development ranked the highest, whereas in the CO group, the gene sets related to cell junction and anion channels were affected. In the CM group, the gene sets linked to the metabolic process, and transcription ranked the highest; a gene set linked with a negative effect on growth was also affected. In conclusion, the constant supplementation in the feed with the strain of yeast tested was effective in counteracting the detrimental effect of ETEC infection in susceptible pigs limits the early activation of the gene sets related to the impairment of the jejunal mucosa.

Keywords

healthdisease preventionprobioticpig
Type
Research Article
Information
animal , Volume 11 , Issue 1 , January 2017 , pp. 33 - 44
Copyright
© The Animal Consortium 2016 

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References

Badia, R, Lizardo, R, Martinez, P, Badiola, I and Brufau, J 2012. The influence of dietary locust bean gum and live yeast on some digestive immunological parameters of piglets experimentally challenged with Escherichia coli . Journal of Animal Science 90, 260–262.CrossRefGoogle ScholarPubMed
Baregamian, N, Song, J, Jeschke, MG, Evers, BM and Chung, DH 2006. IGF-1 protects intestinal epithelial cells from oxidative stress-induced apoptosis. Journal of Surgery Research 136, 31–37.CrossRefGoogle ScholarPubMed
Bontempo, V, Di Giancamillo, A, Savoini, G, Dell’Orto, V and Domeneghini, C 2006. Live yeast dietary supplementation acts upon intestinal morpho-functional aspects and growth in weanling piglets. Animal Feed Science and Technology 129, 224–236.CrossRefGoogle Scholar
Brousseau, J, Talbot, G, Beaudoin, F, Lauzon, K, Roy, D and Lessard, M 2015. Effects of probiotics Pediococcus acidilactici strain MA18/5M and Saccharomyces cerevisiae subsp. boulardii strain SB-CNCM I-1079 on fecal and intestinal microbiota of nursing and weanling piglets. Journal of Animal Science 93, 5313–5326.Google Scholar
Daudelin, JF, Lessard, M, Beaudoin, F, Nadeau, É, Bissonnette, N, Boutin, Y, Brousseau, JP, Lauzon, K and Fairbrother, JM 2011. Administration of probiotics influences F4 (K88)-positive enterotoxigenic Escherichia coli attachment and intestinal cytokine expression in weaned pigs. Veterinary Research 42, 69.CrossRefGoogle ScholarPubMed
Jensen, GM, Frydendahl, K, Svendsen, O, Jørgensen, CB, Cirera, S, Fredholm, M, Nielsen, JP and Møller, K 2006. Experimental infection with Escherichia coli O149:F4ac in weaned piglets. Veterinary Microbiology 115, 243–249.CrossRefGoogle ScholarPubMed
Justino, PF, Melo, LF, Nogueira, AF, Costa, JV, Silva, L, Santos, CM, Mendes, WO, Costa, MR, Franco, AX, Lima, AA, Ribeiro, RA, Souza, MH and Soares, PM 2014. Treatment with Saccharomyces boulardii reduces the inflammation and dysfunction of the gastrointestinal tract in 5-fluorouracil-induced intestinal mucositis in mice. British Journal of Nutrition 111, 1611–1621.CrossRefGoogle ScholarPubMed
Kisielinski, K, Willis, S, Prescher, A, Klosterhalfen, B and Schumpelick, V 2002. A simple new method to calculate small intestine absorptive surface in the rat. Clinical and Experimental Medicine 2, 131–135.Google Scholar
Klunker, LR, Kahlert, S, Panther, P, Diesing, AK, Reinhardt, N, Brosig, B, Kersten, S, Dänicke, S, Rothkötter, HJ and Kluess, JW 2013. Deoxynivalenol and lipopolysaccharide alter epithelial proliferation and spatial distribution of apical junction proteins along the small intestinal axis. Journal of Animal Science 91, 276–285.Google Scholar
Le Bon, M, Davies, HE, Glynn, C, Thompson, C, Madden, M, Wiseman, J, Dodda, CER, Hurdidgec, L, Paynec, G, Le Treutd, Y, Craigona, J, Tötemeyerb, S and Craigon, J 2010. Influence of probiotics on gut health in the weaned pig. Livestock Science 133, 179–181.CrossRefGoogle Scholar
Li, J, Li, D, Gong, L, Ma, Y, He, Y and Zhai, H 2006. Effects of live yeast on the performance, nutrient digestibility, gastrointestinal microbiota and concentration of volatile fatty acids in weanling pigs. Archives of Animal Nutrition 60, 277–288.CrossRefGoogle ScholarPubMed
Li, RW, Li, C, Elsasser, TH, Liua, G, Garrett, WM and Gasbarre, LC 2009. Mucin biosynthesis in the bovine goblet cell induced by Cooperia oncophora infection. Veterinary Parasitology 165, 281–289.CrossRefGoogle ScholarPubMed
Ma, C, Wickham, ME, Guttman, JA, Deng, W, Walker, J, Madsen, KL, Jacobson, K, Vogl, WA, Finley, BB and Vallance, BA 2006. Citrobacter rodentium infection causes both mitochondrial dysfunction and intestinal epithelial barrier disruption in vivo: role of mitochondrial associated protein (Map). Cellular Microbiology 8, 1669–1686.CrossRefGoogle ScholarPubMed
McFarland, LV 2010. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World Journal of Gastroenterology 16, 2202–2222.CrossRefGoogle ScholarPubMed
Mulder, IE, Schmidt, B, Stokes, CR, Lewis, M, Bailey, M, Aminov, RI, Prosser, JI, Gill, BP, Pluske, JR, Mayer, C-D, Musk, CC and Kelly, D 2009. Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biology 7, 79.Google Scholar
Niewold, TA, van der Meulena, J, Kerstens, HDD, Smits, M and Hulst, MH 2010. Transcriptomics of enterotoxigenic Escherichia coli infection. Individual variation in intestinal gene expression correlates with intestinal function. Veterinary Microbiology 141, 110–114.CrossRefGoogle ScholarPubMed
Ortuño Sahagún, D, Márquez-Aguirre, AL, Quintero-Fabián, S, López-Roa, RI and Rojas-Mayorquín, AE 2012. Modulation of PPAR-γ by nutraceutics as complementary treatment for obesity-related disorders and inflammatory diseases. PPAR Research. Article ID 318613.Google Scholar
Priori, D, Colombo, M, Koopmans, SJ, Jansman, AJM, van der Meulen, J, Trevisi, P and Bosi, P 2016. The A0 blood group genotype modifies the jejunal glycomic binding pattern profile of piglets early associated with a simple or complex microbiota. Journal of Animal Science 94, 592–601.Google Scholar
Rieger, J, Janczyk, P, Hünigen, H, Neumann, K and Plendl, J 2015. Intraepithelial lymphocyte numbers and histomorphological parameters in the porcine gut after Enterococcus faecium NCIMB 10415 feeding in a Salmonella Typhimurium challenge. Veterinary Immunology and Immunopathology 164, 40–50.Google Scholar
Ruemmele, FM, Beaulieu, JF, Dionne, S, Levy, E, Seidman, EG, Cerf-Bensussan, N and Lentze, MJ 2002. Lipopolysaccharide modulation of normal enterocyte turnover by toll-like receptors is mediated by endogenously produced tumour necrosis factor α. Gut 51, 842–848.CrossRefGoogle ScholarPubMed
Saran, S, Tran, DD, Klebba-Färber, S, Moran-Losada, P, Wiehlmann, L, Koch, A, Chopra, H, Pabst, O, Hoffmann, A, Klopfleisch, R and Tamura, T 2013. THOC5, a member of the mRNA export complex, contributes to processing of a subset of wingless/integrated (Wnt) target mRNAs and integrity of the gut epithelial barrier. BMC Cell Biology 14, 51.CrossRefGoogle ScholarPubMed
Scaldaferri, F, Vetrano, S, Sans, M, Arena, V, Straface, G, Stigliano, E, Repici, A, Sturm, A, Malesci, A, Panes, J, Yla–Herttuala, S, Fiocchi, C and Danese, S 2009. VEGF-A links angiogenesis and inflammation in inflammatory bowel disease pathogenesis. Gastroenterology 136, 585–595.Google Scholar
Sibartie, S, O’Hara, AM, Ryan, J, Fanning, Á, O’Mahony, J, O’Neill, S, Sheil, B, O’Mahony, L and Shanahan, F 2009. Modulation of pathogen-induced CCL20 secretion from HT-29 human intestinal epithelial cells by commensal bacteria. BMC Immunology 10, 54.CrossRefGoogle ScholarPubMed
Sougioultzis, S, Simeonidis, S, Bhaskar, KR, Chen, X, Anton, PM, Keates, S, Pothoulakis, C and Kelly, CP 2006. Saccharomyces boulardii produces a soluble anti-inflammatory factor that inhibits NF-kappaB-mediated IL-8 gene expression. Biochemical and Biophysical Research Communications 343, 69–76.Google Scholar
Taupin, D, Pedersen, J, Familari, M, Cook, G, Yeomans, N and Giraud, AS 2001. Augmented Intestinal Trefoil Factor (TFF3) and loss of pS2 (TFF1) expression precedes metaplastic differentiation of gastric epithelium. Laboratory Investigation 81, 397–408.Google Scholar
Trevisi, P, Colombo, M, Priori, D, Fontanesi, L, Galimberti, G, Calò, G, Motta, V, Latorre, R, Fanelli, F, Mezzullo, M, Pagotto, U, Gherpelli, Y, D’Inca, R and Bosi, P 2015a. Comparison of three patterns of feed supplementation with live Saccharomyces cerevisiae yeast on post-weaning diarrhea, health status and blood metabolic profile of susceptible weaning pigs orally challenged with Escherichia coli F4ac. Journal of Animal Science 93, 2225–2233.Google Scholar
Trevisi, P, Corrent, E, Mazzoni, M, Messori, S, Priori, D, Gherpelli, Y, Simongiovanni, A and Bosi, P 2015b. Effect of added dietary threonine on growth performance, health, immunity and gastrointestinal function of weaning pigs with differing genetic susceptibility to Escherichia coli infection and challenged with E. coli K88ac. Journal of Animal Physiology Animal Nutrition 99, 511–520.CrossRefGoogle ScholarPubMed
Van den Broeck, W, Cox, E and Goddeeris, BM 1999. Receptor-dependent immune responses in pigs after oral immunization with F4 fimbriae. Infection and Immunity 67, 520–526.CrossRefGoogle ScholarPubMed
Wullaert, A, Bonnet, MC and Pasparakis, M 2011. NFκB in the regulation of epithelial homeostasis and inflammation. Cell Research 21, 146–158.Google Scholar
Zanello, G, Berri, M, Dupont, J, Sizaret, PY, D’Inca, R, Salmon, H and Meurens, F 2011. Saccharomyces cerevisiae modulates immune gene expressions and inhibits ETEC mediated ERK1/2 and p38 signaling pathways in intestinal epithelial cells. PLoS ONE 6, e18573.Google Scholar
Zhou, C, Liu, Z, Jiang, J, Yu, Y and Zhang, Q 2012. Differential gene expression profiling of porcine epithelial cells infected with three enterotoxigenic Escherichia coli strains. BMC Genomics 13, 330.Google Scholar
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