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Intestinal gene expression profiles of piglets benefit from maternal supplementation with a yeast mannan-rich fraction during gestation and lactation

Published online by Cambridge University Press:  08 December 2014

D. E. Graugnard ,
R. S. Samuel ,
R. Xiao ,
L. F. Spangler  and
K. M. Brennan
D. E. Graugnard
Affiliation:
Center for Animal Nutrigenomics and Applied Animal Nutrition, Alltech Inc., Nicholasville, KY 40356, USA
R. S. Samuel
Affiliation:
Center for Animal Nutrigenomics and Applied Animal Nutrition, Alltech Inc., Nicholasville, KY 40356, USA
R. Xiao
Affiliation:
Center for Animal Nutrigenomics and Applied Animal Nutrition, Alltech Inc., Nicholasville, KY 40356, USA
L. F. Spangler
Affiliation:
Center for Animal Nutrigenomics and Applied Animal Nutrition, Alltech Inc., Nicholasville, KY 40356, USA
K. M. Brennan*
Affiliation:
Center for Animal Nutrigenomics and Applied Animal Nutrition, Alltech Inc., Nicholasville, KY 40356, USA
*
†E-mail: kbrennan@alltech.com
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Abstract

The objective was to study the effect of maternal supplementation with a yeast cell wall-based product containing a mannan-rich fraction (MRF) during gestation and lactation on piglet intestinal gene expression. First parity sows were fed experimental gestation and lactation diets with or without MRF (900 mg/kg). After farrowing, piglets were fostered within treatment, as necessary. Sow and litter production performance data were collected until weaning. On day 10 post farrowing, jejunum samples from piglets were collected for gene expression analysis using the Affymetrix Porcine GeneChip array. Most performance parameters did not differ between the treatments. However, protein (P<0.01), total solids less fat (P<0.03) and the concentration of immunoglobulin G (IgG) in milk were greater (P<0.05) in the MRF-supplemented group. Gene expression results using hierarchical clustering revealed an overall dietary effect. Further analysis elucidated activation of pathways involved in tissue development, functioning and immunity, as well as greater cell proliferation and less migration of cells in the jejunum tissue. In conclusion, feeding the sow MRF during pregnancy and lactation was an effective nutritional strategy to bolster colostrum and milk IgG that are essential for development of piglet immune system and gut. In addition, the gene expression patterns affected by the passive immunity transfer showed indicators that could benefit animal performance long term.

Keywords

yeast cell wallpigmicroarrayimmunityintestine
Type
Research Article
Information
animal , Volume 9 , Issue 4 , April 2015 , pp. 622 - 628
Copyright
© The Animal Consortium 2014 

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References

Beaulieu, JF 1997. Extracellular matrix components and integrins in relationship to human intestinal epithelial cell differentiation. Progress in Histochemistry and Cytochemistry 31, 1–78.CrossRefGoogle ScholarPubMed
Bleul, CC, Farzan, M, Choe, H, Parolin, C, Clark-Lewis, I, Sodroski, J and Springer, TA 1996. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382, 829–833.CrossRefGoogle ScholarPubMed
Blum, JW 2006. Nutritional physiology of neonatal calves. Journal of Animal Physiology and Animal Nutrition 90, 1–11.Google Scholar
Bragado, MJ, Groblewski, GE and Williams, JA 1998. Regulation of protein synthesis by cholecystokinin in rat pancreatic acini involves PHAS-I and the p70 S6 kinase pathway. Gastroenterology 115, 733–742.CrossRefGoogle ScholarPubMed
Buckner, CM, Moir, S, Kardava, L, Ho, J, Santich, BH, Kim, LJ, Funk, EK, Nelson, AK, Winckler, B, Chairez, CL, Theobald-Whiting, NL, Anaya-O'Brien, S, Alimchandani, M, Quezado, MM, Yao, MD, Kovacs, JA, Chun, TW, Fauci, AS, Malech, HL and De Ravin, SS 2013. CXCR4/IgG-expressing plasma cells are associated with human gastrointestinal tissue inflammation. Journal of Allergy and Clinical Immunology 133, 1676–1685.Google Scholar
Che, TM, Johnson, RW, Kelley, KW, Dawson, KA, Moran, CA and Pettigrew, JE 2012. Effects of mannan oligosaccharide on cytokine secretions by porcine alveolar macrophages and serum cytokine concentrations in nursery pigs. Journal of Animal Science 90, 657–668.Google Scholar
Che, TM, Johnson, RW, Kelley, KW, Van Alstine, WG, Dawson, KA, Moran, CA and Pettigrew, JE 2011. Mannan oligosaccharide improves immune responses and growth efficiency of nursery pigs experimentally infected with porcine reproductive and respiratory syndrome virus. Journal of Animal Science 89, 2592–2602.Google Scholar
Cheng, ZJ, Zhao, J, Sun, Y, Hu, W, Wu, YL, Cen, B, Wu, GX and Pei, G 2000. Beta-arrestin differentially regulates the chemokine receptor CXCR4-mediated signaling and receptor internalization, and this implicates multiple interaction sites between beta-arrestin and CXCR4. Journal of Biological Chemistry 275, 2479–2485.CrossRefGoogle ScholarPubMed
Clarke, RM and Hardy, RN 1971. Histological changes in the small intestine of the young pig and their relation to macromolecular uptake. Journal of Anatomy 108, 63–77.Google Scholar
Crosby, TF, O’Donnell, A, O’Doherty, JV, Quinn, PJ and Evans, AC 2005. Effects of exogenous progesterone on gestation length, foetal survival and colostrum yield in ewes. Theriogenology 64, 1121–1129.CrossRefGoogle ScholarPubMed
Crowley, SD and Coffman, TM 2012. Recent advances involving the renin–angiotensin system. Experimental Cell Research 318, 1049–1056.CrossRefGoogle ScholarPubMed
Czech, A, Grela, ER, Mokrzycka, A and Pejsak, Z 2010. Efficacy of mannanoligosaccharides additive to sows diets on colostrum, blood immunoglobulin content and production parameters of piglets. Polish Journal of Veterinary Science 13, 525–531.Google Scholar
Fandriks, L 2011. The renin–angiotensin system and the gastrointestinal mucosa. Acta Physiologica 201, 157–167.CrossRefGoogle ScholarPubMed
Frank, JW, Escobar, J, Suryawan, A, Kimball, SR, Nguyen, HV, Jefferson, LS and Davis, TA 2005. Protein synthesis and translation initiation factor activation in neonatal pigs fed increasing levels of dietary protein. Journal of Nutrition 135, 1374–1381.Google Scholar
Hanson, L, Silfverdal, SA, Stromback, L, Erling, V, Zaman, S, Olcen, P and Telemo, E 2001. The immunological role of breast feeding. Pediatric Allergy and Immunology 12 (suppl. 14), 15–19.Google Scholar
Hardy, RN 1969. The absorption of polyvinyl pyrrolidone by the new-born pig intestine. Journal of Physiology 204, 633–651.CrossRefGoogle ScholarPubMed
Heath, JK 2010. Transcriptional networks and signaling pathways that govern vertebrate intestinal development. Current Topics in Developmental Biology 90, 159–192.Google Scholar
Heath, JP 1996. Epithelial cell migration in the intestine. Cell Biology International 20, 139–146.CrossRefGoogle ScholarPubMed
Houde, M, Laprise, P, Jean, D, Blais, M, Asselin, C and Rivard, N 2001. Intestinal epithelial cell differentiation involves activation of p38 mitogen-activated protein kinase that regulates the homeobox transcription factor CDX2. Journal of Biological Chemistry 276, 21885–21894.Google Scholar
Hurley, WL and Theil, PK 2011. Perspectives on immunoglobulins in colostrum and milk. Nutrients 3, 442–474.Google Scholar
Hynes, RO 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110, 673–687.Google Scholar
Ishizuya-Oka, A and Shimozawa, A 1992. Connective tissue is involved in adult epithelial development of the small intestine during anuran metamorphosis in vitro. Roux’s Archives of Developmental Biology 201, 322–329.Google Scholar
Jain, RN and Samuelson, LC 2006. Differentiation of the gastric mucosa. II. Role of gastrin in gastric epithelial cell proliferation and maturation. American Journal of Physiology. Gastrointestinal and Liver Physiology 291, G762–G765.CrossRefGoogle ScholarPubMed
Jahan-Mihan, A, Luhovyy, BL, El Khoury, D and Anderson, GH 2011. Dietary proteins as determinants of metabolic and physiologic functions of the gastrointestinal tract. Nutrients 3, 574–603.CrossRefGoogle ScholarPubMed
Jurgens, MH, Rikabi, RA and Zimmerman, DR 1997. The effect of dietary active dry yeast supplement on performance of sows during gestation-lactation and their pigs. Journal of Animal Science 75, 593–597.CrossRefGoogle ScholarPubMed
Lebenthal, A and Lebenthal, E 1999. The ontogeny of the small intestinal epithelium. Journal of Parenteral and Enteral Nutrition 23, S3–S6.Google Scholar
Lecce, JG and Broughton, CW 1973. Cessation of uptake of macromolecules by neonatal guinea pig, hamster and rabbit intestinal epithelium (closure) and transport into blood. Journal of Nutrition 103, 744–750.Google Scholar
Lecce, JG, Matrone, G and Morgan, DO 1961. The effect of diet on the maturation of the neonatal piglet’s serum protein profile and resistance to disease. Annals of the New York Academy of Sciences 94, 250–264.CrossRefGoogle ScholarPubMed
Leece, JG 1973. Effect of dietary regimen on cessation of uptake of macromolecules by piglet intestinal epithelium (closure) and transport to the blood. Journal of Nutrition 103, 751–756.CrossRefGoogle ScholarPubMed
Meyer, AM, Neville, TL, Reed, JJ, Taylor, JB, Reynolds, LP, Redmer, DA, Hammer, CJ, Vonnahme, KA and Caton, JS 2013. Maternal nutritional plane and selenium supply during gestation impact visceral organ mass and intestinal growth and vascularity of neonatal lamb offspring. Journal of Animal Science 91, 2628–2639.Google Scholar
National Research Council 1998. Nutrient requirements of swine (10th edition). National Academy Press, Washington, D.C. Google Scholar
Newburg, DS and Walker, WA 2007. Protection of the neonate by the innate immune system of developing gut and of human milk. Pediatric Research 61, 2–8.Google Scholar
Nie, Y, Waite, J, Brewer, F, Sunshine, MJ, Littman, DR and Zou, YR 2004. The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. The Journal of Experimental Medicine 200, 1145–1156.Google Scholar
Nochta, I, Tuboly, T, Halas, V and Babinszky, L 2009. Effect of different levels of mannan-oligosaccharide supplementation on some immunological variables in weaned piglets. Journal of Animal Physiology and Animal Nutrition 93, 496–504.CrossRefGoogle ScholarPubMed
Salmon, H, Berri, M, Gerdts, V and Meurens, F 2009. Humoral and cellular factors of maternal immunity in swine. Developmental and Comparative Immunology 33, 384–393.CrossRefGoogle ScholarPubMed
Schwartz, PH, Nethercott, H, Kirov, II, Ziaeian, B, Young, MJ and Klassen, H 2005. Expression of neurodevelopmental markers by cultured porcine neural precursor cells. Stem Cells 23, 1286–1294.Google Scholar
Shalekoff, S, Gray, GE and Tiemessen, CT 2004. Age-related changes in expression of CXCR4 and CCR5 on peripheral blood leukocytes from uninfected infants born to human immunodeficiency virus type 1-infected mothers. Clinical and Diagnostic Laboratory Immunology 11, 229–234.Google ScholarPubMed
Shen, YB, Carroll, JA, Yoon, I, Mateo, RD and Kim, SW 2011. Effects of supplementing Saccharomyces cerevisiae fermentation product in sow diets on performance of sows and nursing piglets. Journal of Animal Science 89, 2462–2471.CrossRefGoogle ScholarPubMed
Simmen, FA, Cera, KR and Mahan, DC 1990. Stimulation by colostrum or mature milk of gastrointestinal tissue development in newborn pigs. Journal of Animal Science 68, 3596–3603.Google Scholar
Smith, MW and Jarvis, LG 1978. Growth and cell replacement in the new-born pig intestine. Proceedings of Biological Sciences/The Royal Society 203, 69–89.Google ScholarPubMed
Suryawan, A and Davis, TA 2005. Developmental regulation of protein kinase B activation is isoform specific in skeletal muscle of neonatal pigs. Pediatric Research 58, 719–724.Google Scholar
Thomas, RP, Hellmich, MR, Townsend, CM Jr. and Evers, BM 2003. Role of gastrointestinal hormones in the proliferation of normal and neoplastic tissues. Endocrine Reviews 24, 571–599.Google Scholar
Uo, M, Hisamatsu, T, Miyoshi, J, Kaito, D, Yoneno, K, Kitazume, MT, Mori, M, Sugita, A, Koganei, K, Matsuoka, K, Kanai, T and Hibi, T 2013. Mucosal CXCR4+IgG plasma cells contribute to the pathogenesis of human ulcerative colitis through FcgammaR-mediated CD14 macrophage activation. Gut 62, 1734–1744.CrossRefGoogle Scholar
van der Peet-Schwering, CM, Jansman, AJ, Smidt, H and Yoon, I 2007. Effects of yeast culture on performance, gut integrity, and blood cell composition of weanling pigs. Journal of Animal Science 85, 3099–3109.Google Scholar
Waskiewicz, AJ and Cooper, JA 1995. Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Current Opinion in Cell Biology 7, 798–805.Google Scholar
Williams, JA 2001. Intracellular signaling mechanisms activated by cholecystokinin-regulating synthesis and secretion of digestive enzymes in pancreatic acinar cells. Annual Review of Physiology 63, 77–97.Google Scholar
Xu, RJ and Cranwell, PD 1991. Gastrin in fetal and neonatal pigs. Comparative Biochemistry and Physiology 98, 615–621.Google Scholar
Yang, J, Gu, P, Menges, S and Klassen, H 2012. Quantitative changes in gene transcription during induction of differentiation in porcine neural progenitor cells. Molecular Vision 18, 1484–1504.Google Scholar
Ye, L, Tuo, W, Liu, X, Simister, NE and Zhu, X 2008. Identification and characterization of an alternatively spliced variant of the MHC class I-related porcine neonatal Fc receptor for IgG. Developmental and Comparative Immunology 32, 966–979.Google Scholar
Zanello, G, Meurens, F, Serreau, D, Chevaleyre, C, Melo, S, Berri, M, D'Inca, R, Auclair, E and Salmon, H 2013. Effects of dietary yeast strains on immunoglobulin in colostrum and milk of sows. Veterinary Immunology and Immunopathology 152, 20–27.Google Scholar
Zhao, PY, Jung, JH and Kim, IH 2012. Effect of mannan oligosaccharides and fructan on growth performance, nutrient digestibility, blood profile, and diarrhea score in weanling pigs. Journal of Animal Science 90, 833–839.Google Scholar