Transcriptional response of HT-29 intestinal epithelial cells to human and bovine milk oligosaccharides

British Journal of Nutrition

Volumn 110, Issue 12, 2013, Pages 2127-2137

  Lane, Jonathan A ^a,b   O'Callaghan, John ^a   Carrington, Stephen D ^b   Hickey, Rita M ^a  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Bovine milk; HT 29 cells; Human milk; Immune response; Oligosaccharides; Transcriptional response

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; FRACTALKINE; GAMMA INTERFERON RECEPTOR 1; GLYCAN; GLYCOCONJUGATE; GRANULOCYTE CHEMOTACTIC PROTEIN 2; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERCELLULAR ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 2; INTERLEUKIN 10 RECEPTOR ALPHA; INTERLEUKIN 12P40; INTERLEUKIN 17F; INTERLEUKIN 1BETA; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; OLIGOSACCHARIDE; RANTES; THROMBOCYTE FACTOR 4;

ARTICLE; CCL20 GENE; CCL5 GENE; CD74 GENE; CLEC4E GENE; COLON MUCOSA; COLOSTRUM; CONTROLLED STUDY; CSF2 GENE; CX3CL1 GENE; CXCL1 GENE; CXCL2 GENE; CXCL3 GENE; CXCL6 GENE; EPITHELIUM CELL; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLYCOGENE; HUMAN; HUMAN CELL; ICAM 1 GENE; ICAM 2 GENE; IFNGR1 GENE; IL10RA GENE; IL2RG GENE; IL4R GENE; IMMUNE SYSTEM; INTERLEUKIN 12B GENE; INTERLEUKIN 17C GENE; INTERLEUKIN 17F GENE; INTERLEUKIN 1BETA GENE; INTERLEUKIN 8 GENE; LOCOMOTION; MILK; NONHUMAN; PF4 GENE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VALIDATION STUDY;

ANIMALS; CATTLE; CHEMOKINES; COLON; COLOSTRUM; CYTOKINES; EPITHELIAL CELLS; FEMALE; HT29 CELLS; HUMANS; IMMUNITY; INTESTINAL MUCOSA; MILK; MILK, HUMAN; OLIGOSACCHARIDES; PREGNANCY; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84889262580     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114513001591     Document Type: Article

References (45)

1. Kunz C, Rodriguez-Palmero M, Koletzko B, et al. (1999) Nutritional and biochemical properties of human milk, part I: General aspects, proteins, and carbohydrates. Clin Perinatol 26, 307-333.
2. Kuntz S, Rudloff S & Kunz C (2008) Oligosaccharides from human milk influence growth-related characteristics of intestinally transformed and non-Transformed intestinal cells. Br J Nutr 99, 462-471.
3. Newburg DS, Ruiz-Palacios GM & Morrow AL (2005) Human milk glycans protect infants against enteric pathogens. Annu Rev Nutr 25, 37-58.
4. Bode L (2006) Recent advances on structure, metabolism, and function of human milk oligosaccharides. J Nutr 136, 2127-2130.
5. Hickey RM (2009) Harnessing milk oligosaccharides for nutraceutical applications. In Dairy-derived Ingredients: Food and Nutraceutical Uses, pp. 308-343 [M Corredig, editor]. Guelph, ON: University of Guelph.
6. Field AC, Caccavelli L, Fillion J, et al. (2001) Neonatal induction and maintenance of tolerance to Th2-induced immune manifestations in rats. Transplant Proc 33, 2275-2276.
7. Schack-Nielsen L & Michaelsen KF (2007) Advances in our understanding of the biology of human milk and its effects on the offspring. J Nutr 137, 503S-510S.
8. Romagnani S (2004) The increased prevalence of allergy and the hygiene hypothesis: Missing immune deviation, reduced immune suppression, or both? Immunology 112, 352-363.
9. Niers LEM, Hoekstra MO, Timmerman HM, et al. (2007) Selection of probiotic bacteria for prevention of allergic diseases: Immunomodulation of neonatal dendritic cells. Clin Experimen Immunol 149, 344-352.
10. Velupillai P & Harn DA (1994) Oligosaccharide-specific induction of interleukin 10 production by B220+ cells from schistosome-infected mice: A mechanism for regulation of CD4+ T-cell subsets. Proc Natl Acad Sci U S A 91, 18-22.
11. Eiwegger T, Stahl B, Schmitt J, et al. (2004) Human milkderived oligosaccharides and plant-derived oligosaccharides stimulate cytokine production of cord blood T-cells in vitro. Pediatr Res 56, 536-540.
12. Vos AP, Haarman M, van Ginkel JW, et al. (2007) Dietary supplementation of neutral and acidic oligosaccharides enhances Th1-dependent vaccination responses in mice. Pediatr Aller Immunol 18, 304-312.
13. Tao N, DePeters EJ, Freeman S, et al. (2008) Bovine milk glycome. J Dairy Sci 91, 3768-3778.
14. Tao N, DePeters EJ, German JB, et al. (2009) Variations in bovine milk oligosaccharides during early and middle lactation stages analyzed by high-performance liquid chromatography- chip/mass spectrometry. J Dairy Sci 92, 2991-3001.
15. Barile D, Marotta M, Chu C, et al. (2010) Neutral and acidic oligosaccharides in Holstein-Friesian colostrum during the first 3 days of lactation measured by high performance liquid chromatography on a microfluidic chip and time-offlight mass spectrometry. J Dairy Sci 93, 3940-3949.
16. Marino K, Lane JA, Abrahams JL, et al. (2011) Method for milk oligosaccharide profiling by 2-Aminobenzamide labeling and hydrophilic interaction chromatography. Glycobiology 21, 1317-1330.
17. Mysore JV, Wigginton T, Simon PM, et al. (1999) Treatment of Helicobacter pylori infection in rhesus monkeys using a novel antiadhesion compound. Gastroenterology 117, 1316-1325.
18. Hakkarainen J, Toivanen M, Leinonen A, et al. (2005) Human and bovine milk oligosaccharides inhibit Neisseria meningitidis pili attachment in vitro. J Nutr 135, 2445-2448.
19. Matrosovich MN, Gambaryan AS, Tuzikov AB, et al. (1993) Probing of the receptor-binding sites of the H1 and H3 influenza A and influenza B virus hemagglutinins by synthetic and natural sialosides. Virology 196, 111-121.
20. Lane JA, Marino K, Naughton J, et al. (2012) Anti-infective bovine colostrum oligosaccharides: Campylobacter jejuni as a case study. Int J Food Microbiol 157, 182-188.
21. Otani H & Monnai M (1993) Inhibition of proliferative responses of mouse spleen lymphocytes by bovine milk k-casein digests. Food Agric Immunol 5, 219-229.
22. Kobata A & Ginsburg V (1972) Oligosaccharides of human milk. IV. Isolation and characterization of a new hexasaccharide, lacto-N-neohexaose. Arch Biochem Biophys 150, 273-281.
23. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
24. Maere S, Heymans K & Kuiper M (2005) BiNGO: A Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21, 3448-3449.
25. Dydensborg AB, Herring E, Auclair J, et al. (2006) Normalizing genes for quantitative RT-PCR in differentiating human intestinal epithelial cells and adenocarcinomas of the colon. Am J Physiol Gastrointest Liver Physiol 290, G1067-G1074.
26. Kuntz S, Kunz C & Rudloff S (2009) Oligosaccharides from human milk induce growth arrest via G2/M by influencing growth-related cell cycle genes in intestinal epithelial cells. Br J Nutr 101, 1306-1315.
27. Ninonuevo MR, Park Y, Yin HF, et al. (2006) A strategy for annotating the human milk glycome. J Agric Food Chem 54, 7471-7480.
28. Urashima T, Kitaoka M, Terabayashi T, et al. (2011) Milk Oligosaccharides. New York: Nova Science Publishers.
29. Bruntz R, Dabrowski U, Dabrowski J, et al. (1988) Fucosecontaining oligosaccharides from human milk from a donor of blood group 0 Le(a) nonsecretor. Biol Chem Hoppe Seyler 369, 257-273.
30. Haeuw-Fievre S, Wieruszeski JM, Plancke Y, et al. (1993) Primary structure of human milk octa-, dodeca- And tridecasaccharides determined by a combination of 1H-NMR spectroscopy and fast-Atom-bombardment mass spectrometry. Evidence for a new core structure, the paralacto- N-octaose. Eur J Biochem 215, 361-371.
31. Boehm G & Stahl B (2007) Oligosaccharides from milk. J Nutr 137, 847s-849s.
32. Pappu R, Ramirez-Carrozzi V & Sambandam A (2011) The interleukin-17 cytokine family: Critical players in host defence and inflammatory diseases. Immunology 134, 8-16.
33. Lee JW, Wang P, Kattah MG, et al. (2008) Differential regulation of chemokines by IL-17 in colonic epithelial cells. J Immunol 181, 6536-6545.
34. Yang D, Chen Q, Hoover DM, et al. (2003) Many chemokines including CCL20/MIP-3 alpha display antimicrobial activity. J Leukoc Biol 74, 448-455.
35. Ryan KA, O'Hara AM, van Pijkeren JP, et al. (2009) Lactobacillus salivarius modulates cytokine induction and virulence factor gene expression in Helicobacter pylori. J Med Microbiol 58, 996-1005.
36. Sibartie S, O'Hara AM, Ryan J, et al. (2009) Modulation of pathogen-induced CCL20 secretion from HT-29 human intestinal epithelial cells by commensal bacteria. BMC Immunol 10, 54.
37. O'Callaghan J, Butto LF, Macsharry J, et al. (2012) Influence of adhesion and bacteriocin production by Lactobacillus salivarius on the intestinal epithelial cell transcriptional response. Appl Environ Microbiol 78, 5196-5203.
38. O'Flaherty S & Klaenhammer TR (2012) Influence of exposure time on gene expression by human intestinal epithelial cells exposed to Lactobacillus acidophilus. Appl Environ Microbiol 78, 5028-5032.
39. van Baarlen P, Troost F, van der Meer C, et al. (2011) Human mucosal in vivo transcriptome responses to three lactobacilli indicate how probiotics may modulate human cellular pathways. Proc Natl Acad Sci U S A 108, 4562-4569.
40. van Baarlen P, Troost FJ, van Hemert S, et al. (2009) Differential NF-kappa B pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc Natl Acad Sci U S A 106, 2371-2376.
41. Spehlmann ME & Eckmann L (2009) Nuclear factor-kappa B in intestinal protection and destruction. Curr Opin Gastroenterol 25, 92-99.
42. Claud EC, Savidge T & Walker WA (2003) Modulation of human intestinal epithelial cell IL-8 secretion by human milk factors. Pediatr Res 53, 419-425.
43. Daddaoua A, Puerta V, Requena P, et al. (2006) Goat milk oligosaccharides are anti-inflammatory in rats with hapteninduced colitis. J Nutr 136, 672-676.
44. Matsushita K, Takeuchi O, Standley DM, et al. (2009) Zc3h12a is an RNase essential for controlling immune responses by regulating mRNA decay. Nature 458, 1185-1190.
45. Field CJ (2005) The immunological components of human milk and their effect of immune development in infants. J Nutr 135, 1-4.