The Delay in the Development of Experimental Colitis from Isomaltosyloligosaccharides in Rats Is Dependent on the Degree of Polymerization

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Iwaya, Hitoshi ^a   Lee, Jae Sung ^a   Yamagishi, Shinya ^a   Shinoki, Aki ^a   Lang, Weeranuch ^a   Thawornkuno, Charin ^a   Kang, Hee Kwon ^a   Kumagai, Yuya ^a   Suzuki, Shiho ^b   Kitamura, Shinichi ^b   Hara, Hiroshi ^a   Okuyama, Masayuki ^a   Mori, Haruhide ^a   Kimura, Atsuo ^a   Ishizuka, Satoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b Osaka Prefecture University   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; BUTYRIC ACID; CD161 ANTIGEN; CD45 ANTIGEN; CD8 ANTIGEN; DEXTRAN; DEXTRAN SULFATE; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 43; GAMMA INTERFERON; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 2; INTERLEUKIN 1BETA; LONG SIZED ISOMALTOSYLOLIGOSACCHARIDE; MESSENGER RNA; MYELOPEROXIDASE; OLIGOSACCHARIDE; PROPIONIC ACID; SHORT SIZED ISOMALTOSYLOLIGOSACCHARIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CECUM; CELL POPULATION; COLITIS; COLON MUCOSA; COLON WEIGHT; CONTROLLED STUDY; DEGREE OF POLYMERIZATION; ENZYME ACTIVITY; EXPERIMENTAL MODEL; FECES ANALYSIS; GENE EXPRESSION; HISTOCHEMISTRY; IMMUNOCOMPETENT CELL; MALE; NEUTROPHIL; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGAN WEIGHT; POLYMERIZATION; PROTEIN EXPRESSION; RAT; RECTUM HEMORRHAGE; WEIGHT REDUCTION;

ANIMALS; COLITIS; DEXTRAN SULFATE; DEXTRANS; MALE; OLIGOSACCHARIDES; RATS; RATS, WISTAR; STRUCTURE-ACTIVITY RELATIONSHIP;

RATTUS; RATTUS NORVEGICUS;

EID: 84870514388     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050658     Document Type: Article

References (53)

1. Chen HL, Lu YH, Lin JJ, Ko LY, (2001) Effects of isomalto-oligosaccharides on bowel functions and indicators of nutritional status in constipated elderly men. J Am Coll Nutr 20: 44-49.
2. Ketabi A, Dieleman LA, Ganzle MG, (2011) Influence of isomalto-oligosaccharides on intestinal microbiota in rats. J Appl Microbiol 110: 1297-1306.
3. Ito H, Takemura N, Sonoyama K, Kawagishi H, Topping DL, et al. (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.
4. Mizubuchi H, Yajima T, Aoi N, Tomita T, Yoshikai Y, (2005) Isomalto-oligosaccharides polarize Th1-like responses in intestinal and systemic immunity in mice. J Nutr 135: 2857-2861.
5. Shih DQ, Targan SR, (2008) Immunopathogenesis of inflammatory bowel disease. World J Gastroenterol 14: 390-400.
6. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, et al. (1990) A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98: 694-702.
7. Dieleman LA, Ridwan BU, Tennyson GS, Beagley KW, Bucy RP, et al. (1994) Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology 107: 1643-1652.
8. Kucharzik T, Hudson J, Lügering A, Abbas J, Bettini M, et al. (2005) Acute induction of human IL-8 production by intestinal epithelium triggers neutrophil infiltration without mucosal injury. Gut 54: 1565-1572.
9. Videla S, Vilaseca J, Antolin M, Garcia-Lafuente A, Guarner F, et al. (2001) Dietary inulin improves distal colitis induced by dextran sodium sulfate in the rat. Am J Gastroenterol 96: 1486-1493.
10. Cherbut C, Michel C, Lecannu G, (2003) The prebiotic characteristics of fructooligosaccharides are necessary for reduction of TNBS-induced colitis in rats. J Nutr 133: 21-27.
11. Moreau NM, Martin LJ, Toquet CS, Laboisse CL, Nguyen PG, et al. (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.
12. Holma R, Juvonen P, Asmawi MZ, Vapaatalo H, Korpela R, (2002) Galacto-oligosaccharides stimulate the growth of bifidobacteria but fail to attenuate inflammation in experimental colitis in rats. Scand J Gastroenterol 37: 1042-1047.
13. Holst JJ, (2007) The physiology of glucagon-like peptide 1. Physiol Rev 87: 1409-1439.
14. Drucker DJ, (2002) Biological actions and therapeutic potential of the glucagon-like peptides. Gastroenterology 122: 531-544.
15. Orskov C, Holst JJ, Knuhtsen S, Baldissera FG, Poulsen SS, et al. (1986) Glucagon-like peptides GLP-1 and GLP-2, predicted products of the glucagon gene, are secreted separately from pig small intestine but not pancreas. Endocrinology 119: 1467-1475.
16. Parker HE, Reimann F, Gribble FM, (2010) Molecular mechanisms underlying nutrient-stimulated incretin secretion. Expert Rev Mol Med 12: e1.
17. Caspary WF, (1992) Physiology and pathophysiology of intestinal absorption. Am J Clin Nutr 55: 299S-308S.
18. Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, et al. (2012) Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 61: 364-371.
19. Drucker DJ, Shi Q, Crivici A, Sumner-Smith M, Tavares W, et al. (1997) Regulation of the biological activity of glucagon-like peptide 2 in vivo by dipeptidyl peptidase IV. Nat Biotechnol 15: 673-677.
20. Tsai C, Hill M, Asa S, Brubaker P, Drucker D, (1997) Intestinal growth-promoting properties of glucagon-like peptide-2 in mice. Am J Physiol 273: E77-84.
21. Drucker DJ, Yusta B, Boushey RP, DeForest L, Brubaker PL, (1999) Human [Gly2]GLP-2 reduces the severity of colonic injury in a murine model of experimental colitis. Am J Physiol 276: G79-91.
22. Reeves P, Nielsen F, Fahey GJ, (1993) 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 123: 1939-1951.
23. Hehre EJ, (1951) The biological synthesis of dextran from dextrins. J Biol Chem 192: 161-174.
24. Iwaya H, Kashiwaya M, Shinoki A, Lee JS, Hayashi K, et al. (2011) Marginal zinc deficiency exacerbates experimental colitis induced by dextran sulfate sodium in rats. J Nutr 141: 1077-1082.
25. Bozeman P, Learn D, Thomas E, (1990) Assay of the human leukocyte enzymes myeloperoxidase and eosinophil peroxidase. J Immunol Methods 126: 125-133.
26. 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.
27. Shiga K, Hara H, Okano G, Aoyama Y, (2003) Ingestion of water-soluble soybean fiber prevents gastrectomy-induced iron malabsorption, anemia and impairment of voluntary running exercise performance in rats. J Nutr 133: 1120-1126.
28. Steinhoff U, Brinkmann V, Klemm U, Aichele P, Seiler P, et al. (1999) Autoimmune intestinal pathology induced by hsp60-specific CD8 T cells. Immunity 11: 349-358.
29. Nancey S, Holvoet S, Graber I, Joubert G, Philippe D, et al. (2006) CD8+ cytotoxic T cells induce relapsing colitis in normal mice. Gastroenterology 131: 485-496.
30. Kontoyiannis D, Boulougouris G, Manoloukos M, Armaka M, Apostolaki M, et al. (2002) Genetic dissection of the cellular pathways and signaling mechanisms in modeled tumor necrosis factor-induced Crohn's-like inflammatory bowel disease. J Exp Med 196: 1563-1574.
31. O'Keeffe J, Doherty DG, Kenna T, Sheahan K, O'Donoghue DP, et al. (2004) Diverse populations of T cells with NK cell receptors accumulate in the human intestine in health and in colorectal cancer. Eur J Immunol 34: 2110-2119.
32. Kleessen B, Hartmann L, Blaut M, (2001) Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. Br J Nutr 86: 291-300.
33. Nilsson U, Nyman M, (2005) Short-chain fatty acid formation in the hindgut of rats fed oligosaccharides varying in monomeric composition, degree of polymerisation and solubility. Br J Nutr 94: 705-713.
34. Klebanoff S, (2005) Myeloperoxidase: friend and foe. J Leukoc Biol 77: 598-625.
35. Shaikh RB, Santee S, Granger SW, Butrovich K, Cheung T, et al. (2001) Constitutive expression of LIGHT on T cells leads to lymphocyte activation, inflammation, and tissue destruction. J Immunol 167: 6330-6337.
36. Wang J, Lo JC, Foster A, Yu P, Chen HM, et al. (2001) The regulation of T cell homeostasis and autoimmunity by T cell-derived LIGHT. J Clin Invest 108: 1771-1780.
37. Cohavy O, Shih DQ, Doherty TM, Ware CF, Targan SR, (2011) CD161 Defines Effector T Cells That Express Light and Respond to TL1a-DR3 Signaling. Eur J Microbiol Immunol (Bp) 1: 70-79.
38. Jungbeck M, Daller B, Federhofer J, Wege AK, Wimmer N, et al. (2009) Neutralization of LIGHT ameliorates acute dextran sodium sulphate-induced intestinal inflammation. Immunology 128: 451-458.
39. Iwaya H, Maeta K, Hara H, Ishizuka S, (2012) Mucosal permeability is an intrinsic factor in susceptibility to dextran sulfate sodium-induced colitis in rats. Exp Biol Med (Maywood) 237: 451-460.
40. Okada Y, Maeda N, Takakura S, Miyata K, Koshiba M, (2011) Tacrolimus ameliorates dextran sulfate sodium-induced colitis in mice: implication of interferon-gamma and interleukin-1beta suppression. Biol Pharm Bull 34: 1823-1827.
41. Arai Y, Takanashi H, Kitagawa H, Okayasu I, (1998) Involvement of interleukin-1 in the development of ulcerative colitis induced by dextran sulfate sodium in mice. Cytokine 10: 890-896.
42. Segain JP, Raingeard de la Bletiere D, Bourreille A, Leray V, Gervois N, et al. (2000) Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 47: 397-403.
43. Inan MS, Rasoulpour RJ, Yin L, Hubbard AK, Rosenberg DW, et al. (2000) The luminal short-chain fatty acid butyrate modulates NF-kappaB activity in a human colonic epithelial cell line. Gastroenterology 118: 724-734.
44. Andoh A, Fujiyama Y, Hata K, Araki Y, Takaya H, et al. (1999) Counter-regulatory effect of sodium butyrate on tumour necrosis factor-alpha (TNF-alpha)-induced complement C3 and factor B biosynthesis in human intestinal epithelial cells. Clin Exp Immunol 118: 23-29.
45. Place RF, Noonan EJ, Giardina C, (2005) HDAC inhibition prevents NF-kappa B activation by suppressing proteasome activity: down-regulation of proteasome subunit expression stabilizes I kappa B alpha. Biochem Pharmacol 70: 394-406.
46. Jobin C, Sartor RB, (2000) The I kappa B/NF-kappa B system: a key determinant of mucosalinflammation and protection. Am J Physiol Cell Physiol 278: C451-462.
47. Karaki S, Tazoe H, Hayashi H, Kashiwabara H, Tooyama K, et al. (2008) Expression of the short-chain fatty acid receptor, GPR43, in the human colon. J Mol Histol 39: 135-142.
48. Tazoe H, Otomo Y, Kaji I, Tanaka R, Karaki SI, et al. (2008) Roles of short-chain fatty acids receptors, GPR41 and GPR43 on colonic functions. J Physiol Pharmacol 59Suppl 2: 251-262.
49. Brown A, Goldsworthy S, Barnes A, Eilert M, Tcheang L, et al. (2003) The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278: 11312-11319.
50. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, et al. (2009) Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461: 1282-1286.
51. Arakawa M, Mita T, Azuma K, Ebato C, Goto H, et al. (2010) Inhibition of monocyte adhesion to endothelial cells and attenuation of atherosclerotic lesion by a glucagon-like peptide-1 receptor agonist, exendin-4. Diabetes 59: 1030-1037.
52. Boushey R, Yusta B, Drucker D, (1999) Glucagon-like peptide 2 decreases mortality and reduces the severity of indomethacin-induced murine enteritis. Am J Physiol 277: E937-947.
53. L'Heureux M, Brubaker P, (2003) Glucagon-like peptide-2 and common therapeutics in a murine model of ulcerative colitis. J Pharmacol Exp Ther 306: 347-354.