Wild-type and IL10-null mice have differential colonic epithelial gene expression responses to dietary supplementation with synbiotic Bifidobacterium animalis subspecies lactis and inulin

Journal of Nutrition

Volumn 144, Issue 3, 2014, Pages 245-251

  Kuo, Shiu Ming ^a,b   Chan, Wan Chun ^a   Hu, Zihua ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BIFIDOBACTERIUM; COLON; DIET; EPITHELIUM; GENE EXPRESSION; GENOTYPE; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-10; INULIN; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; PREBIOTICS; PROBIOTICS; RNA, RIBOSOMAL, 18S; SYNBIOTICS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84894254680     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.113.185249     Document Type: Article

References (61)

1. Maslowski KM, Mackay C. Diet, gut microbiota and immune responses. Nat Immunol. 2011;12:5-9.
2. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions. Science. 2012;336:1262-7.
3. Shanahan F. The colonic microbiota in health and disease. Curr Opin Gastroenterol. 2013;29:49-54.
4. Gibson GR, Roberfroid M. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125: 1401-12.
5. Roberfroid MB. Introducing inulin-type fructans. Br J Nutr. 2005;93: (suppl. 1):S13-25.
6. Kuo SM. The interplay between fiber and the intestinal microbiome in the inflammatory response. Adv Nutr. 2013;4:16-28.
7. Davis LM, Martínez I, Walter J, Goin C, Hutkins R. Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS One. 2011;6:e25200.
8. Saxelin M, Tynkkynen S, Mattila-Sandholm T, de Vos W. Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol. 2005;16:204-11.
9. Vernazza CL, Gibson G, Rastall R. Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium. J Appl Microbiol. 2006;100:846-53.
10. Lin PW, Nasr T, Berardinelli A, Kumar A, Neish A. The probiotic Lactobacillus GG may augment intestinal host defense by regulating apoptosis and promoting cytoprotective responses in the developing murine gut. Pediatr Res. 2008;64:511-6.
11. Chen Q, Swist E, Beckstead J, Green J, Matias F, Roberts J, Qiao C, Raju J, Brooks S, Scoggan K. Dietary fructooligosaccharides and wheat bran elicit specific and dose-dependent gene expression profiles in the proximal colon epithelia of healthy Fischer 344 rats. J Nutr. 2011;141:790-7.
12. Ohtsuka Y, Kegami T, Izumi H, Namura M, Ikeda T, Ikuse T, Baba Y, Kudo T, Suzuki R, Shimizu T. Effects of Bifidobacterium breve on inflammatory gene expression in neonatal and weaning rat intestine. Pediatr Res. 2012;71:46-53.
13. Kuo SM, Merhige PM, Hagey LR. The effect of dietary prebiotics and probiotics on body weight, large intestine indices, and fecal bile acid profile in wildtype and IL102/2 mice. PLoS One. 2013;8:e60270.
14. Hooper LV, Littman D, Macpherson A. Interactions between the microbiota and the immune system. Science. 2012;336:1268-73.
15. Kamada N, Seo S, Chen G, Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13:321-35.
16. Patten DA, Collett A. Exploring the immunomodulatory potential of microbial-associated molecular patterns derived from the enteric bacterial microbiota. Microbiology. 2013;159:1535-44.
17. Valledor AF, Comalada M, Santamaría-Babi L, Lloberas J, Celada A. Macrophage proinflammatory activation and deactivation: a question of balance. Adv Immunol. 2010;108:1-20.
18. Danese S. Immune and nonimmune components orchestrate the pathogenesis of inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol. 2011;300:G716-22.
19. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol. 2010;10:131-44.
20. Moreau NM, Toquet C, Laboisse C, Nguyen P, Siliart B, Champ M, Dumon H, Martin L. Predominance of caecal injury in a new dextran sulphate sodium treatment in rats: histopathological and fermentative characteristics. Eur J Gastroenterol Hepatol. 2002;14:535-42.
21. Camuesco D, Peran L, Comalada M, Nieto A, Di Stasi L, Rodriguez- Cabezas M, Concha A, Zarzuelo A, Galvez J. Preventative effects of lactulose in the trinitrobenzenesulphonic acid model of rat colitis. Inflamm Bowel Dis. 2005;11:265-71.
22. Coussement PA. Inulin and oligofructose: safe intakes and legal status. J Nutr. 1999;129:1412S-7S.
23. Benjamin JL, Hedin C, Koutsoumpas A, Ng S, McCarthy N, Hart A, Kamm M, Sanderson J, Knight S, Forbes A, et al. Randomised, doubleblind, placebo-controlled trial of fructo-oligosaccharides in active Crohn's disease. Gut. 2011;60:923-9.
24. Pestka S, Krause C, Sarkar D, Walter M, Shi Y, Fisher P. Interleukin-10 and related cytokines and receptors. Annu Rev Immunol. 2004;22:929-79.
25. Berg DJ, Davidson N, Kühn R, MüllerW, Menon S, Holland G, Thompson- Snipes L, LeachM, Rennick D. Enterocolitis and colon cancer in interleukin- 10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J Clin Invest. 1996;98:1010-20.
26. Masso-Welch PA, Merhige PM, Veeranki OLM, Kuo SM. Loss of IL-10 decreases mouse postpubertal mammary gland development in the absence of inflammation. Immunol Invest. 2012;41:521-37.
27. Reeves PG, Nielsen FH, Fahey GCJ. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993;123:1939-51.
28. Roller M, Rechkemmer G, Watzl B. Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J Nutr. 2004;134:153-6.
29. Paradkar PN, Blum PS, Berhow MA, Baumann H, Kuo SM. Dietary isoflavones suppress endotoxin-induced inflammatory reaction in liver and intestine. Cancer Lett. 2004;215:21-8.
30. Kuo SM, MacLean ME, McCormick K, Wilson JX. Gender and sodium-ascorbate transporter isoforms determine ascorbate concentrations in mice. J Nutr. 2004;134:2216-21.
31. Howard M, Muchamuel T, Andrade S, Menon S. Interleukin 10 protects mice from lethal endotoxemia. J Exp Med. 1993;177:1205-8.
32. Kuo SM, Leavitt PS. Genistein increases metallothionein expression in human intestinal cells, Caco-2. Biochem Cell Biol. 1999;77:79-88.
33. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156-9.
34. Kuo SM, Burl LR, Hu Z. Cellular phenotype-dependent and-independent effects of vitamin C on the renewal and gene expression of mouse embryonic fibroblasts. PLoS One. 2012;7:e32957.
35. Baldi P, Long AD. A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics. 2001;17:509-19.
36. Rasmussen HE, Blobaum K, Park Y, Ehlers S, Lu F, Lee J. Lipid extract of Nostoc commune var. sphaeroides Kutzing, a blue-green alga, inhibits the activation of sterol regulatory element binding proteins in HepG2 cells. J Nutr. 2008;138:476-81.
37. Kingma SD, Li N, Sun F, Valladares R, Neu J, Lorca G. Lactobacillus johnsonii N6.2 stimulates the innate immune response through toll-like receptor 9 in caco-2 cells and increases intestinal crypt paneth cell number in biobreeding diabetes-prone rats. J Nutr. 2011;141:1023-8.
38. Yang Y, Seo J, Nguyen A, Pham T, Park H, Park Y, Kim B, Bruno R, Lee J. Astaxanthin-rich extract from the green alga Haematococcus pluvialis lowers plasma lipid concentrations and enhances antioxidant defense in apolipoprotein E knockout mice. J Nutr. 2011;141:1611-7.
39. VanGuilder HD, Vrana K, Freeman W. Twenty-five years of quantitative PCR for gene expression analysis. Biotechniques. 2008;44:619-26.
40. Schmittgen TD, Livak K. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3:1101-8.
41. Yasuda K, Maiorano R, Welch R, Miller D, Lei X. Cecum is the major degradation site of ingested inulin in young pigs. J Nutr. 2007;137:2399-404.
42. Majumdar MK, Chockalingam P, Bhat R, Sheldon R, Keohan C, Blanchet T, Glasson S,Morris E. Immortalized mouse articular cartilage cell lines retain chondrocyte phenotype and respond to both anabolic factor BMP-2 and pro-inflammatory factor IL-1. J Cell Physiol. 2008;215:68-76.
43. Sivapalaratnam S, Farrugia R, Nieuwdorp M, Langford C, van Beem R, Maiwald S, Zwaginga J, Gusnanto A,Watkins N, Trip M, et al. Identification of candidate genes linking systemic inflammation to atherosclerosis; results of a human in vivo LPS infusion study. BMC Med Genomics. 2011;4:64.
44. Sonnier DI, Bailey S, Schuster R, Gangidine M, Lentsch A, Pritts T. Proinflammatory chemokines in the intestinal lumen contribute to intestinal dysfunction during endotoxemia. Shock. 2012;37:63-9.
45. Dower K, Ellis D, Saraf K, Jelinsky S, Lin L. Innate immune responses to TREM-1 activation: overlap, divergence, and positive and negative crosstalk with bacterial lipopolysaccharide. J Immunol. 2008;180:3520-34.
46. Padidar S, Farquharson A, Williams L, Kelaiditi E, Hoggard N, Arthur J, Drew J. Leptin up-regulates pro-inflammatory cytokines in discrete cells within mouse colon. J Cell Physiol. 2011;226:2123-30.
47. Ohkawara T, Nishihira J, Takeda H, Hige S, Kato M, Sugiyama T, Iwanaga T, Nakamura H, Mizue Y, Asaka M. Amelioration of dextran sulfate sodium-induced colitis by anti-macrophage migration inhibitory factor antibody in mice. Gastroenterology. 2002;123:256-70.
48. Foell D, Wittkowski H, Roth J. Monitoring disease activity by stool analyses: from occult blood to molecular markers of intestinal inflammation and damage. Gut. 2009;58:859-68.
49. Tursi A, Elisei W, Brandimarte G, Giorgetti G, Inchingolo C, Nenna R, Picchio M, Giorgio F, Ierardi E. Musosal tumour necrosis factor a in diverticular disease of the colon is overexpressed with disease severity. Colorectal Dis. 2012;14:e258-63.
50. Ryan GR, Dai X, Dominguez M, Tong W, Chuan F, Chisholm O, Russell R, Pollard J, Stanley E. Rescue of the colony-stimulating factor 1 (CSF-1)- nullizygous mouse (Csf1(op)/Csf1(op)) phenotype with a CSF-1 transgene and identification of sites of local CSF-1 synthesis. Blood. 2001;98:74-84.
51. Ichikawa M, Williams R, Wang L, Vogl T, Srikrishna G. S100A8/A9 activate key genes and pathways in colon tumor progression. Mol Cancer Res. 2011;9:133-48.
52. Pamer EG. Immune responses to commensal and environmental microbes. Nat Immunol. 2007;8:1173-8.
53. Ganguli K, Meng D, Rautava S, Lu L, Walker W, Nanthakumar N. Probiotics prevent necrotizing enterocolitis by modulating enterocyte genes that regulate innate immune-mediated inflammation. Am J Physiol Gastrointest Liver Physiol. 2013;304:G132-41.
54. Xavier RJ, Podolsky D. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427-34.
55. Li Q, Wang C, Tang C, Li N, Li J. Molecular-phylogenetic characterization of the microbiota in ulcerated and non-ulcerated regions in the patients with Crohn's disease. PLoS ONE. 2012;7:e34939.
56. De Preter V, Joossens M, Ballet V, Shkedy Z, Rutgeerts P, Vermeire S, Verbeke Phd K. Metabolic profiling of the impact of oligofructoseenriched inulin in Crohn's disease patients: a double-blinded randomized controlled trial. Clin Transl Gastroenterol. 2013;4:e30.
57. Rodríguez-Cabezas ME, Gálvez JC, Camuesco D, Lorente M, Concha A, Martinez-Augustin O, Redondo L, Zarzuelo A. Intestinal antiinflammatory activity of dietary fiber (Plantago ovata seeds) in HLAB27 transgenic rats. Clin Nutr. 2003;22:463-71.
58. Neyrinck AM, Mouson A, Delzenne N. Dietary supplementation with laminarin, a fermentable marine beta (1-3) glucan, protects against hepatotoxicity induced by LPS in rat by modulating immune response in the hepatic tissue. Int Immunopharmacol. 2007;7:1497-506.
59. Arribas B, Rodríguez-Cabezas M, Camuesco D, Comalada M, Bailón E, Utrilla P, Nieto A, Concha A, Zarzuelo A, Gálvez J. A probiotic strain of Escherichia coli, Nissle 1917, given orally exerts local and systemic antiinflammatory effects in lipopolysaccharide-induced sepsis in mice. Br J Pharmacol. 2009;157:1024-33.
60. Arribas B, Rodríguez-Cabezas M, Comalada M, Bailón E, Camuesco D, Olivares M, Xaus J, Zarzuelo A, Gálvez J. Evaluation of the preventative effects exerted by Lactobacillus fermentum in an experimental model of septic shock induced in mice. Br J Nutr. 2009;101:51-8.
61. Faghfoori Z, Navai L, Shakerhosseini R, Somi M, Nikniaz Z, Norouzi M. Effects of an oral supplementation of germinated barley foodstuff on serum tumour necrosis factor-alpha, interleukin-6 and-8 in patients with ulcerative colitis. Ann Clin Biochem. 2011;48:233-7.