The impact of fructo-oligosaccharides on gut permeability and inflammatory responses in the cecal mucosa quite differs between rats fed semi-purified and non-purified diets

Journal of Nutritional Science and Vitaminology

Volumn 64, Issue 5, 2018, Pages 357-366

  Genda, Tomomi ^a   Kondo, Takashi ^a   Hino, Shingo ^a   Sugiura, Shunsaku ^a   Nishimura, Naomichi ^a   Morita, Tatsuya ^a  

^a SHIZUOKA UNIVERSITY   (Japan)

Author keywords

Fructo oligosaccharides; Gut permeability; Non purified diet; Rats; Semi purified diet

Indexed keywords

BACTERIAL DNA; CYTOKINE; EDETATE CHROMIUM; FRUCTOSE OLIGOSACCHARIDE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; MYELOPEROXIDASE; RNA 16S; SECRETORY COMPONENT; TUMOR NECROSIS FACTOR; CHROMIUM; EDETIC ACID; FRUCTOSE; LACTIC ACID; OLIGOSACCHARIDE; PEROXIDASE; PREBIOTIC AGENT; SUCCINIC ACID; VOLATILE FATTY ACID;

ACTINOBACTERIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; BIFIDOBACTERIUM; CECUM MUCOSA; DIET SUPPLEMENTATION; ENZYME ACTIVITY; FECES ANALYSIS; FOOD INTAKE; GENE EXPRESSION; HISTOPATHOLOGY; INFLAMMATION; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; INTESTINE TRANSIT TIME; LACTOBACILLUS; MALE; MICROBIAL GROWTH; NONHUMAN; ORGAN WEIGHT; PROTEIN EXPRESSION; PROTEOBACTERIA; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPECIES RICHNESS; UNHEALTHY DIET; URINALYSIS; VERRUCOMICROBIA; ANIMAL; ANIMAL FOOD; CECUM; DIET; DIGESTION; DRUG EFFECT; FERMENTATION; GASTROINTESTINAL TRANSIT; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOLOGY; PERMEABILITY; URINE; WISTAR RAT;

ANIMAL FEED; ANIMALS; BACTERIAL TRANSLOCATION; CECUM; CHROMIUM; CYTOKINES; DIET; DIGESTION; EDETIC ACID; FATTY ACIDS, VOLATILE; FERMENTATION; FRUCTOSE; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRANSIT; INFLAMMATION; INTESTINAL MUCOSA; LACTIC ACID; MALE; OLIGOSACCHARIDES; PERMEABILITY; PEROXIDASE; PREBIOTICS; RATS, WISTAR; SUCCINIC ACID;

EID: 85055779809     PISSN: 03014800     EISSN: 18817742     Source Type: Journal    
DOI: 10.3177/jnsv.64.357     Document Type: Article

References (42)

1. Guarner F. 2007. Studies with inulin-type fructans on intestinal infections, permeability, and inflammation. J Nutr 137: 2568S–2571S.
2. Colomé G, Sierra C, Blasco J, García MV, Valverde E, Sánchez E. 2007. Intestinal permeability in different feedings in infancy. Acta Paediatr 96: 69–72.
3. Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, Van der Meer R. 2003. Dietary fructo-oligosaccharides dose-dependently increase translocation of salmonella in rats. J Nutr 133: 2313–2318.
4. Schepens MA, Rijnierse A, Schonewille AJ, Vink C, Brummer RJ, Willemsen LE, van der Meer R, Bovee-Oudenhoven IM. 2010. Dietary calcium decreases but short-chain fructo-oligosaccharides increase colonic permeability in rats. Br J Nutr 104: 1780–1786.
5. Barrat E, Michel C, Poupeau G, David-Sochard A, Rival M, Pagniez A, Champ M, Darmaun D. 2008. Supplementation with galactooligosaccharides and inulin increases bacterial translocation in artificially reared newborn rats. Pediatr Res 64: 34–39.
6. Petersen A, Heegaard PM, Pedersen AL, Andersen JB, Sørensen RB, Frøkiaer H, Lahtinen SJ, Ouwehand AC, Poulsen M, Licht TR. 2009. Some putative prebiotics increase the severity of Salmonella enterica serovar Typhimurium infection in mice. BMC Microbiol 9: 245.
7. Fontaine N, Meslin JC, Lory S, Andrieux C. 1996. Intestinal mucin distribution in the germ-free rat and in the heteroxenic rat harbouring a human bacterial flora: effect of inulin in the diet. Br J Nutr 75: 881–892.
8. Kleessen B, Hartmann L, Blaut M. 2003. Fructans in the diet cause alterations of intestinal mucosal architecture, released mucins and mucosa-associated bifidobacteria in gnotobiotic rats. Br J Nutr 89: 597–606.
9. Kleessen B, Blaut M. 2005. Modulation of gut mucosal biofilms. Br J Nutr 93 (Suppl 1): S35–40.
10. Johnson-Henry KC, Pinnell LJ, Waskow AM, Irrazabal T, Martin A, Hausner M, Sherman PM. 2014. Short-chain fructo-oligosaccharide and inulin modulate inflammatory responses and microbial communities in Caco2-bbe cells and in a mouse model of intestinal injury. J Nutr 144: 1725–1733.
11. Genda T, Sasaki Y, Kondo T, Hino S, Nishimura N, Tsukahara T, Sonoyama K, Morita T. 2017. Fructo-oligo-saccharide-induced transient increases in cecal immunoglobulin A concentrations in rats are associated with mucosal inflammation in response to increased gut permeability. J Nutr 147: 1900–1908.
12. Umesaki Y, Yajima T, Yokokura T, Mutai M. 1979. Effect of organic acid absorption on bicarbonate transport in rat colon. Pflugers Arch 14(379): 43–47.
13. Morita T, Kasaoka S, Ohhashi A, Ikai M, Numasaki Y, Kiriyama S. 1998. Resistant proteins alter cecal short-chain fatty acid profiles in rats fed high amylose cornstarch. J Nutr 128: 1156–1164.
14. Morita T, Kasaoka S, Hase K, Kiriyama S. 1999. Oligo-L-methionine and resistant protein promote cecal buty-rate production in rats fed resistant starch and fructooli-gosaccharide. J Nutr 129: 1333–1339.
15. Morita T, Kasaoka S, Hase K, Kiriyama S. 1999. Psyl-lium shifts the fermentation site of high-amylose cornstarch toward the distal colon and increases fecal buty-buty-rate concentration in rats. J Nutr 129: 2081–2087. rate
16. Vogt L, Meyer D, Pullens G, Faas M, Smelt M, Venema K, Ramasamy U, Schols HA, De Vos P. 2015. Immunological properties of inulin-type fructans. Crit Rev Food Sci Nutr 55: 414–436.
17. American Institute of Nutrition. 1977. Report of the American Institute of Nutrition ad hoc committee on standards for nutritional studies. J Nutr 107: 1340–1348.
18. Prosky L, Asp NG, Furda I, DeVries JW, Schweizer TF, Harland BF. 1985. Determination of total dietary fiber in foods and food products: collaborative study. J Assoc Off Anal Chem 68: 677–679.
19. Hoshi S, Sakata T, Mikuni K, Hashimoto H, Kimura S. 1994. Galactosylsucrose and xylosylfructoside alter digestive tract size and concentrations of cecal organic acids in rats fed diets containing cholesterol and cholic acid. J Nutr 124: 52–60.
20. Binnerts W, Van het Klooster A, Frens A. 1968. Soluble chromium indicator measured by atomic absorption in digestion experiments. Vet Rec 82: 470.
21. Kondo T, Handa K, Genda T, Hino S, Hamaguchi N, Morita T. 2017. Digestion-resistant dextrin derivatives are moderately digested in the small intestine and contribute more to energy production than predicted from large-bowel fermentation in rats. J Nutr 147: 330–336.
22. Bradley PP, Priebat DA, Christensen RD, Rothstein G. 1982. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 78: 206–209.
23. Ito H, Takemura N, Sonoyama K, Kawagishi H, Topping DL, Conlon MA, Morita T. 2011. Degree of polymerization of inulin-type fructans differentially affects number of lactic acid bacteria, intestinal immune functions, and immunoglobulin A secretion in the rat cecum. J Agric Food Chem 59: 5771–5778.
24. Heid CA, Stevens J, Livak KJ, Williams PM. 1996. Real time quantitative PCR. Genome Res 6: 986–994.
25. Rinttilä T, Kassinen A, Malinen E, Krogius L, Palva A. 2004. Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97: 1166–1177.
26. Byun R, Nadkarni MA, Chhour KL, Martin FE, Jacques NA, Hunter N. 2004. Quantitative analysis of diverse Lactobacillus species present in advanced dental caries. J Clin Microbiol 42: 3128–3136.
27. Makker HPS, McSweeney CS, eds. 2010. Methods in Gut Microbial Ecology for Ruminants. Springer, Dordrecht.
28. Tsukahara T, Iwasaki Y, Nakayama K, Ushida K. 2002. An improved technique for the histological evaluation of the mucus-secreting status in rat cecum. J Nutr Sci Vitaminol 48: 311–314.
29. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pir-rung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336.
30. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461.
31. Komura M, Fukuta T, Genda T, Hino S, Aoe S, Kawagishi H, Morita T. 2014. A short-term ingestion of fructo-oli-gosaccharides increases immunoglobulin A and mucin concentrations in the rat cecum, but the effects are attenuated with the prolonged ingestion. Biosci Biotechnol Biochem 78: 1592–1602.
32. Sakata T, Setoyama H. 1995. Local stimulatory effect of short-chain fatty acids on the mucus release from the hindgut mucosa of rats (Rattus norvegicus). Comp Biochem Physiol A Physiol 111: 429–432.
33. Kelly CJ, Zheng L, Campbell EL, Saeedi B, Scholz CC, Bay-less AJ, Wilson KE, Glover LE, Kominsky DJ, Magnuson A, Weir TL, Ehrentraut SF, Pickel C, Kuhn KA, Lanis JM, Nguyen V, Taylor CT, Colgan SP. 2015. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe 17: 662–671.
34. Johansen FE, Brandtzaeg P. 2004. Transcriptional regulation of the mucosal IgA system. Trends Immunol 25: 150–157.
35. Kaetzel CS. 2005. The polymeric immunoglobulin receptor: bridging innate and adaptive immune responses at mucosal surfaces. Immunol Rev 206: 83–99.
36. Moreau NM, Martin LJ, Toquet CS, Laboisse CL, Nguyen PG, Siliart BS, Dumon HJ, Champ MM. 2003. Restoration of the integrity of rat caeco-colonic mucosa by resistant starch, but not by fructo-oligosaccharides, in dextran sulfate sodium-induced experimental colitis. Br J Nutr 90: 75–85.
37. Goto H, Takemura N, Ogasawara T, Sasajima N, Wata-nabe J, Ito H, Morita T, Sonoyama K. 2010. Effects of fructo-oligosaccharide on DSS-induced colitis differ in mice fed nonpurified and purified diets. J Nutr 140: 2121–2127.
38. Videla S, Vilaseca J, Antolín M, García-Lafuente A, Guarner F, Crespo E, Casalots J, Salas A, Malagelada JR. 2001. Dietary inulin improves distal colitis induced by dextran sodium sulfate in the rat. Am J Gastroenterol 96: 1486–1493.
39. Lidell ME, Johansson ME, Hansson GC. 2003. An auto-catalytic cleavage in the C terminus of the human MUC2 mucin occurs at the low pH of the late secretory pathway. J Biol Chem 278: 13944–13951.
40. Sakaguchi E, Sakoda C, Toramaru Y. 1998. Caecal fermentation and energy accumulation in the rat fed on indigestible oligosaccharides. Br J Nutr 80: 469–476.
41. Diehl GE, Longman RS, Zhang JX, Breart B, Galan C, Cuesta A, Schwab SR, Littman DR. 2013. Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX(3) CR1(hi) cells. Nature 494(7435): 116–120.
42. Liu TW, Cephas KD, Holscher HD, Kerr KR, Mangian HF, Tappenden KA, Swanson KS. 2016. Nondigestible fructans alter gastrointestinal barrier function, gene expression, histomorphology, and the microbiota profiles of diet-induced obese C57BL/6J mice. J Nutr 146: 949–956.