Maternal short-chain fructooligosaccharide supplementation influences intestinal immune system maturation in piglets

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Bourgot, Cindy Le ^a   Ferret Bernard, Stéphanie ^a   Normand, Laurence Le ^a   Savary, Gérard ^a   Menendez Aparicio, Enrique ^a   Blat, Sophie ^a   Appert Bossard, Emmanuelle ^b   Respondek, Frédérique ^b   Le Huërou Luron, Isabelle ^a  

^a CEMAGREF   (France)

^b Tereos Syral   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID; CD4 ANTIGEN; FRUCTOSE OLIGOSACCHARIDE; GAMMA INTERFERON; IMMUNOGLOBULIN; IMMUNOGLOBULIN A; INTERLEUKIN 2 RECEPTOR ALPHA; PROPIONIC ACID; SHORT CHAIN FATTY ACID; SHORT CHAIN FRUCTOOLIGOSACCHARIDE; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VALERIC ACID; OLIGOSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST MILK; COLOSTRUM; CONTROLLED STUDY; CYTOKINE RELEASE; DIET SUPPLEMENTATION; FEMALE; HELPER CELL; IMMUNE SYSTEM; IMMUNOGLOBULIN PRODUCTION; INTESTINE; LACTATION; MATERNAL NUTRITION; MESENTERY LYMPH NODE; MUCOSAL IMMUNITY; NONHUMAN; PERINATAL PERIOD; PEYER PATCH; PIGLET; POSTNATAL DEVELOPMENT; PUERPERIUM; SUCKLING ANIMAL; T LYMPHOCYTE; WEANING; ANIMAL; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; PIG; PREGNANCY;

ANIMALS; COLOSTRUM; DIETARY SUPPLEMENTS; FEMALE; INTESTINES; OLIGOSACCHARIDES; PREGNANCY; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; SWINE;

EID: 84907192022     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107508     Document Type: Article

References (56)

1. Inman CF, Jones P, Harris C, Haverson K, Miller B, et al. (2005) The mucosal immune system of the neonatal piglet. Pig Journal 55: 211-222.
2. Kelly D, Coutts AG (2000) Early nutrition and the development of immune function in the neonate. The Proceedings of the Nutrition Society 59: 177-185.
3. Salmon H, Berri M, Gerdts V, Meurens F (2009) Humoral and cellular factors of maternal immunity in swine. Developmental and Comparative Immunology 33: 384-393.
4. Harris NL, Spoerri I, Schopfer JF, Nembrini C, Merky P, et al. (2006) Mechanisms of neonatal mucosal antibody protection. Journal of Immunology 177: 6256-6262.
5. Brandtzaeg P, Farstad IN, Haraldsen G, Jahnsen FL (1998) Cellular and molecular mechanisms for induction of mucosal immunity. Developments in Biological Standardization 92: 93-108.
6. Perez PF, Dore J, Leclerc M, Levenez F, Benyacoub J, et al. (2007) Bacterial imprinting of the neonatal immune system: Lessons from maternal cells? Pediatrics 119: E724-E732.
7. Verhasselt V, Milcent V, Cazareth J, Kanda A, Fleury S, et al. (2008) Breast milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma. Nature Medicine 14: 170-175.
8. Gibson GR, Probert HM, Van Loo J, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutrition Research Reviews 17: 259-275.
9. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, et al. (2010) Prebiotic effects: metabolic and health benefits. The British journal of nutrition 104 Suppl 2: S1-63.
10. Howard MD, Gordon DT, Garleb KA, Kerley MS (1995) Dietary fructooli-gosaccharide, xylooligosaccharide and gum-arabic have variable effects on cecal and colonic microbiota and epithelial-cell proliferation in mice and rats. Journal of Nutrition 125: 2604-2609.
11. Berg EL, Fu CJ, Porter JH, Kerley MS (2005) Fructooligosaccharide supplementation in the yearling horse: Effects on fecal pH, microbial content, and volatile fatty acid concentrations. Journal of Animal Science 83: 1549-1553.
12. Pan X-d, Chen F-q, Wu T-x, Tang H-g, Zhao Z-y (2009) Prebiotic oligosaccharides change the concentrations of short-chain fatty acids and the microbial population of mouse bowel. Journal of Zhejiang University-Science B 10: 258-263.
13. Tsukahara T, Iwasaki Y, Nakayama K, Ushida K (2003) Stimulation of butyrate production in the large intestine of weaning piglets by dietary fructooligosac-charides and its influence on the histological variables of the large intestinal mucosa. Journal of Nutritional Science and Vitaminology 49: 414-421.
14. Respondek F, Gerard P, Bossis M, Boschat L, Bruneau A, et al. (2013) Short-chain fructo-oligosaccharides modulate intestinal microbiota and metabolic parameters of humanized gnotobiotic diet induced obesity mice. PloS One 8: e71026.
15. Cecchini DA, Laville E, Laguerre S, Robe P, Leclerc M, et al. (2013) Functional metagenomics reveals novel pathways of prebiotic breakdown by human gut bacteria. PloS One 8: e72766.
16. De Vuyst L, Moens F, Selak M, Riviere A, Leroy F (2013) Summer Meeting 2013: growth and physiology of bifidobacteria. Journal of Applied Microbiology.
17. Manhart N, Spittler A, Bergmeister H, Mittlbock M, Roth E (2003) Influence of fructooligosaccharides on Peyer's patch lymphocyte numbers in healthy and endotoxemic mice. Nutrition 19: 657-660.
18. Hosono A, Ozawa A, Kato R, Ohnishi Y, Nakanishi Y, et al. (2003) Dietary fructooligosaccharides induce immunoregulation of intestinal IgA secretion by murine Peyer's patch cells. Bioscience Biotechnology and Biochemistry 67: 758-764.
19. Swanson KS, Grieshop CM, Flickinger EA, Bauer LL, Healy HP, et al. (2002) Supplemental fructooligosaccharides and mannanoligosaccharides influence immune function, ileal and total tract nutrient digestibilities, microbial populations and concentrations of protein catabolites in the large bowel of dogs. Journal of Nutrition 132: 980-989.
20. Bakker-Zierikzee AM, Alles MS, Knol J, Kok FJ, Tolboom JJM, et al. (2005) Effects of infant formula containing a mixture of galacto-and fructo-oligosaccharides or viable Bifidobacterium animalis on the intestinal microflora during the first 4 months of life. British Journal of Nutrition 94: 783-790.
21. Scholtens PAMJ, Alliet P, Raes M, Alles MS, Kroes H, et al. (2008) Fecal secretory immunoglobulin A is increased in healthy infants who receive a formula with short-chain galacto-oligosaccharides and long-chain fructo-oligosaccharides. Journal of Nutrition 138: 1141-1147.
22. Shadid R, Haarman M, Knol J, Theis W, Beermann C, et al. (2007) Effects of galactooligosaccharide and long-chain fructooligosaccharide supplementation during pregnancy on maternal and neonatal microbiota and immunity-a randomized, double-blind, placebo-controlled study. American Journal of Clinical Nutrition 86: 1426-1437.
23. Fujiwara R, Takemura N, Watanabe J, Sonoyama K (2010) Maternal consumption of fructo-oligosaccharide diminishes the severity of skin inflammation in offspring of NC/Nga mice. British Journal of Nutrition 103: 530-538.
24. Fujiwara R, Watanabe J, Sonoyama K (2008) Assessing changes in composition of intestinal microbiota in neonatal BALB/c mice through cluster analysis of molecular markers. British Journal of Nutrition 99: 1174-1177.
25. Adlerberth I, Wold AE (2009) Establishment of the gut microbiota in Western infants. Acta Paediatrica 98: 229-238.
26. Adogony V, Respondek F, Biourge V, Rudeaux F, Delaval J, et al. (2007) Effects of dietary scFOS on immunoglobulins in colostrums and milk of bitches. Journal of Animal Physiology and Animal Nutrition 91: 169-174.
27. Czech A, Grela ER, Mokrzycka A, Pejsak Z (2010) Efficacy of mannanoligo-saccharides additive to sows diets on colostrum, blood immunoglobulin content and production parameters of piglets. Polish Journal of Veterinary Sciences 13: 525-531.
28. Gourbeyre P, Desbuards N, Gremy G, Le Gall S, Champ M, et al. (2012) Exposure to a galactooligosaccharides/inulin prebiotic mix at different developmental time points differentially modulates immune responses in mice. Journal of Agricultural and Food Chemistry 60: 11942-11951.
29. Peroni DG, Piacentini GL, Bodini A, Pigozzi R, Boner AL (2009) Transforming growth factor-beta(1) is elevated in unpasteurized cow's milk. Pediatric Allergy and Immunology 20: 42-44.
30. Tourais-Esteves I, Bernardet N, Lacroix-Lamande S, Ferret-Bernard S, Laurent F (2008) Neonatal goats display a stronger TH1-type cytokine response to TLR ligands than adults. Developmental and Comparative Immunology 32: 1231-1241.
31. Haverson K, Corfield G, Jones PH, Kenny M, Fowler J, et al. (2009) Effect of oral antigen and antibody exposure at birth on subsequent immune status. International Archives of Allergy and Immunology 150: 192-204.
32. Nakamura Y, Nosaka S, Suzuki M, Nagafuchi S, Takahashi T, et al. (2004) Dietary fructooligosaccharides up-regulate immunoglobulin A response and polymeric immunoglobulin receptor expression in intestines of infant mice. Clinical and Experimental Immunology 137: 52-58.
33. Jouany JP, Zainab B, Senaud J, Groliere CA, Grain J, et al. (1981) Role of the rumen ciliate protozoa polyplastron-multivesiculatum, entodinium sp and isotricha-prostoma in the digestion of a mixed diet in sheep. Reproduction Nutrition Development 21: 871-884.
34. Desbuards N, Gourbeyre P, Haure-Mirande V, Darmaun D, Champ M, et al. (2012) Impact of perinatal prebiotic consumption on gestating mice and their offspring: a preliminary report. British Journal of Nutrition 107: 1245-1248.
35. Delmee E, Cani PD, Gual G, Knauf C, Burcelin R, et al. (2006) Relation between colonic proglucagon expression and metabolic response to oligofructose in high fat diet-fed mice. Life sciences 79: 1007-1013.
36. Respondek F, Swanson KS, Belsiro KR, Vester BN, Wagner A, et al. (2008) Short-chain fructooligosaccharides influence insulin sensitivity and gene expression of fat tissue in obese dogs. Journal of Nutrition 138: 1712-1718.
37. Pere MC, Etienne M (2007) Insulin sensitivity during pregnancy, lactation, and postweaning in primiparous gilts. Journal of Animal Science 85: 101-110.
38. Dourmad JY, Etienne M, Noblet J (1996) Reconstitution of body reserves in multiparous sows during pregnancy: effect of energy intake during pregnancy and mobilization during the previous lactation. Journal of Animal Science 74: 2211-2219.
39. Salmon H (1999) The mammary gland and neonate mucosal immunity. Veterinary Immunology and Immunopathology 72: 143-155.
40. Brandtzaeg P (2003) Role of secretory antibodies in the defence against infections. International Journal of Medical Microbiology 293: 3-15.
41. Nguyen TV, Yuan L, Azevedo MS, Jeong KI, Gonzalez AM, et al. (2007) Transfer of maternal cytokines to suckling piglets: in vivo and in vitro models with implications for immunomodulation of neonatal immunity. Veterinary Immunology and Immunopathology 117: 236-248.
42. Donnet-Hughes A, Duc N, Serrant P, Vidal K, Schiffrin EJ (2000) Bioactive molecules in milk and their role in health and disease: the role of transforming growth factor-beta. Immunology and Cell Biology 78: 74-79.
43. Ando T, Hatsushika K, Wako M, Ohba T, Koyama K, et al. (2007) Orally administered TGF-beta is biologically active in the intestinal mucosa and enhances oral tolerance. The Journal of Allergy and Clinical Immunology 120: 916-923.
44. Konkel JE, Chen W (2011) Balancing acts: the role of TGF-beta in the mucosal immune system. Trends in Molecular Medicine 17: 668-676.
45. Iijima H, Takahashi I, Kiyono H (2001) Mucosal immune network in the gut for the control of infectious diseases. Reviews in Medical Virology 11: 117-133.
46. Adkins B, Leclerc C, Marshall-Clarke S (2004) Neonatal adaptive immunity comes of age. Nature Reviews Immunology 4: 553-564.
47. Marodi L (2001) IL-12 and IFN-gamma deficiencies in human neonates. Pediatric Research 49: 316.
48. Lewis DB, Larsen A, Wilson CB (1986) Reduced interferon-gamma mRNA levels in human neonates. Evidence for an intrinsic T cell deficiency independent of other genes involved in T cell activation. The Journal of Experimental Medicine 163: 1018-1023.
49. Wilson CB, Westall J, Johnston L, Lewis DB, Dower SK, et al. (1986) Decreased production of interferon-gamma by human neonatal cells. Intrinsic and regulatory deficiencies. The Journal of Clinical Investigation 77: 860-867.
50. Arredouani M, Matthijs P, Van Hoeyveld E, Kasran A, Baumann H, et al. (2003) Haptoglobin directly affects T cells and suppresses T helper cell type 2 cytokine release. Immunology 108: 144-151.
51. Makino H, Kushiro A, Ishikawa E, Kubota H, Gawad A, et al. (2013) Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant's microbiota. PloS One 8: e78331.
52. Hedemann MS, Theil PK, Bach Knudsen KE (2009) The thickness of the intestinal mucous layer in the colon of rats fed various sources of non-digestible carbohydrates is positively correlated with the pool of SCFA but negatively correlated with the proportion of butyric acid in digesta. The British Journal of Nutrition 102: 117-125.
53. Kapsenberg ML (2003) Dendritic-cell control of pathogen-driven T-cell polarization. Nature Reviews Immunology 3: 984-993.
54. Nakanishi Y, Hosono A, Hiramatsu Y, Kimura T, Nakamura R, et al. (2005) Characteristic immune response in Peyer's patch cells induced by oral administration of Bifidobacterium components. Cytotechnology 47: 69-77.
55. Niers LE, Hoekstra MO, Timmerman HM, van Uden NO, de Graaf PM, et al. (2007) Selection of probiotic bacteria for prevention of allergic diseases: immunomodulation of neonatal dendritic cells. Clinical and Experimental Immunology 149: 344-352.
56. Ibnou-Zekri N, Blum S, Schiffrin EJ, von der Weid T (2003) Divergent patterns of colonization and immune response elicited from two intestinal Lactobacillus strains that display similar properties in vitro. Infection and Immunity 71: 428-436.