Intestinal anti-inflammatory effects of oligosaccharides derived from lactulose in the trinitrobenzenesulfonic acid model of rat colitis

Journal of Agricultural and Food Chemistry

Volumn 62, Issue 19, 2014, Pages 4285-4297

  Algieri, Francesca ^a   Rodríguez Nogales, Alba ^a   Garrido Mesa, Natividad ^a   Vezza, Teresa ^a   Garrido Mesa, José ^a   Utrilla, M Pilar ^a   Montilla, Antonia ^b   Cardelle Cobas, Alejandra ^b   Olano, Agustín ^b   Corzo, Nieves ^b   Guerra Hernández, Eduardo ^a   Zarzuelo, Antonio ^a   Rodriguez Cabezas, M Elena ^a   Galvez, Julio ^a  

^a UNIVERSITY OF GRANADA   (Spain)

^b INSTITUTE OF FOOD SCIENCE RESEARCH CIAL   (Spain)

Author keywords

intestinal anti inflammatory effect; lactulose derived oligosaccharides; prebiotic; TNBS rat colitis

Indexed keywords

MOLECULAR BIOLOGY; OLIGOSACCHARIDES; RATS; DISEASES;

ANTI-INFLAMMATORIES; ANTI-INFLAMMATORY EFFECTS; INFLAMMATORY BOWEL DISEASE; INTESTINAL MUCOSA BARRIER; PREBIOTICS; PREVENTATIVE EFFECT; SHORT-CHAIN FATTY ACIDS; TNBS RAT COLITIS; LACTULOSE;

DISEASES; FATTY ACIDS;

ANTIINFLAMMATORY AGENT; CHEMOKINE; INTERLEUKIN DERIVATIVE; LACTULOSE; OLIGOSACCHARIDE; PREBIOTIC AGENT; TRINITROBENZENESULFONIC ACID;

ANIMAL; CHEMICALLY INDUCED; CHEMISTRY; COLITIS; DISEASE MODEL; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; INTESTINE; MICROBIOLOGY; MICROFLORA; RAT; WISTAR RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CHEMOKINES; COLITIS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INTERLEUKINS; INTESTINES; LACTULOSE; MICROBIOTA; OLIGOSACCHARIDES; PREBIOTICS; RATS; RATS, WISTAR; TRINITROBENZENESULFONIC ACID;

BACTERIA (MICROORGANISMS); RATTUS;

EID: 84900826640     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf500678p     Document Type: Article

References (43)

1. Sartor, R. B. Mechanisms of disease: pathogenesis of Crohns disease and ulcerative colitis Nat. Clin. Pract. Gastroenterol. Hepatol. 2006, 3, 390-407
2. Frank, D. N.; St Amand, A. L.; Feldman, R. A.; Boedeker, E. C.; Harpaz, N.; Pace, N. R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 13780-13785
3. Khan, K. J.; Ullman, T. A.; Ford, A. C.; Abreu, M. T.; Abadir, A.; Marshall, J. K.; Talley, N. J.; Moayyedi, P. Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis Am. J. Gastroenterol. 2011, 106, 661-673
4. Roberfroid, M.; Gibson, G. R.; Hoyles, L.; McCartney, A. L.; Rastall, R.; Rowland, I.; Wolvers, D.; Watzl, B.; Szajewska, H.; Stahl, B.; Guarner, F.; Respondek, F.; Whelan, K.; Coxam, V.; Davicco, M. J.; Léotoing, L.; Wittrant, Y.; Delzenne, N. M.; Cani, P. D.; Neyrinck, A. M.; Meheust, A. Prebiotic effects: metabolic and health benefits Br. J. Nutr. 2010, 104, S1-S63
5. Looijer-van Langen, M. A.; Dieleman, L. A. Prebiotics in chronic intestinal inflammation Inflamm. Bowel Dis. 2009, 15, 454-462
6. Wong, J. M.; de Souza, R.; Kendall, C. W.; Emam, A.; Jenkins, D. J. Colonic health: fermentation and short chain fatty acids J. Clin. Gasgroenterol. 2006, 40, 235-2243
7. Swennen, K.; Courtin, C. M.; Delcour, J. A. Non-digestible oligosaccharides with prebiotic properties Crit. Rev. Food Sci. Nutr. 2006, 46, 459-471
8. Schumann, C. Medical, nutritional and technological properties of lactulose. An update Eur. J. Nutr. 2002, 41 (Suppl. 1) I17-I25
9. Olano, A.; Corzo, N. Lactulose as a food ingredient J. Sci. Food Agric. 2009, 89, 1987-1990
10. Panesar, P. S.; Kumari, S. Lactulose: production, purification and potential applications Biotechnol. Adv. 2011, 29, 940-948
11. Rumi, G.; Tsubouchi, R.; Okayama, M.; Kato, S.; Mózsik, G.; Takeuchi, K. Protective effect of lactulose on dextran sulfate sodium-induced colonic inflammation in rats Dig. Dis. Sci. 2004, 49, 1466-1472
12. Camuesco, D.; Peran, L.; Comalada, M.; Nieto, A.; Di Stasi, L. C.; Rodriguez-Cabezas, M. E.; Concha, A.; Zarzuelo, A.; Galvez, J. Preventative effects of lactulose in the trinitrobenzenesulphonic acid model of rat colitis Inflamm. Bowel Dis. 2005, 11, 265-271
13. Chen, X.; Zhai, X.; Shi, J.; Liu, W. W.; Tao, H.; Sun, X.; Kang, Z. Lactulose mediates suppression of dextran sodium sulfate-induced colon inflammation by increasing hydrogen production Dig. Dis. Sci. 2013, 58, 1560-1568
14. Hafer, A.; Krämer, S.; Duncker, S.; Krüger, M.; Manns, M. P.; Bischoff, S. C. Effect of oral lactulose on clinical and immunohistochemical parameters in patients with inflammatory bowel disease: a pilot study BMC Gastroenterol. 2007, 7, 36
15. Munoz, S. J. Hepatic encephalopathy Med. Clin. North Am. 2008, 92, 795-812
16. Cardelle-Cobas, A.; Martínez Villaluenga, C.; Villamiel, M.; Olano, A.; Corzo, N. Synthesis of oligosaccharides derived from lactulose and Pectinex Ultra SP-L J. Agric. Food Chem. 2008, 56, 3328-3333
17. Cardelle-Cobas, A.; Villamiel, M.; Olano, A.; Corzo, N. Isomerization of lactose-derived oligosaccharides. A case study using sodium aluminate J. Agric. Food Chem. 2008, 56, 10954-10959
18. Martínez-Villaluenga, C.; Cardelle-Cobas, A.; Olano, A.; Corzo, N.; Villamiel, M.; Jimeno, M. L. Enzymatic synthesis and identification of two trisaccharides produced from lactulose by transgalactosylation J. Agric. Food Chem. 2008, 56, 557-563
19. Cardelle-Cobas, A.; Corzo, N.; Olano, A.; Pélaez, C.; Requena, T.; ávila, M. Galactooligosaccharides derived from lactose and lactulose: influence of linkage and composition on Streptococcus, Lactobacillus and Bifidobacterium strains growth Int. J. Food Microbiol. 2011, 149, 81-87
20. Cardelle-Cobas, A.; Olano, A.; Corzo, N.; Villamiel, M.; Collins, M.; Kolida, S.; Rastall, R. A. In vitro fermentation of lactulose-derived oligosaccharides by mixed fecal microbiota J. Agric. Food Chem. 2012, 60, 2024-2032
21. Marín-Manzano, M. C.; Abecia, L.; Hernández- Hernández, O.; Sanz, M. L.; Montilla, A.; Olano, A.; Rubio, L. A.; Moreno, F. J.; Clemente, A. Galacto-oligosaccharides derived from lactulose exert a selective stimulation on the growth of Bifidobacterium animalis in the large intestine of growing rats J. Agric. Food Chem. 2013, 61, 7560-7567
22. Elson, C. O.; Sartor, R. B.; Tennyson, G. S.; Riddell, R. H. Experimental models of inflammatory bowel disease Gastroenterology 1995, 109, 1344-1367
23. Sanz, M. L.; Polemis, N.; Morales, V.; Corzo, N.; Drakoularakou, A.; Gibson, G. R.; Rastall, R. A. In vitro investigation into the potential prebiotic activity of honey oligosaccharides J. Agric. Food Chem. 2005, 53, 2914-2921
24. Anadón, A.; Martínez, M. A.; Ares, I.; Castellano, V.; Martínez-Larranaga, M. R.; Corzo, N.; Olano, A.; Montilla, A.; Recio, I.; Martínez-Maqueda, D.; Miralles, B.; Fornari, T.; García-Risco, M. R.; Gonzalez, M.; Reglero, G. Acute and repeated dose (28 days) oral safety studies of ALIBIRD in rats J. Food Prot. 2013, 76, 1226-1239
25. Arribas, B.; Suárez-Pereira, E.; Ortiz Mellet, C.; García Fernández, J. M.; Buttersack, C.; Rodríguez-Cabezas, M. E.; Garrido-Mesa, N.; Bailon, E.; Guerra-Hernández, E.; Zarzuelo, A.; Gálvez, J. Di- d -fructose dianhydride-enriched caramels: effect on colon microbiota, inflammation, and tissue damage in trinitrobenzenesulfonic acid-induced colitic rats J. Agric. Food Chem. 2010, 58, 6476-6484
26. Krawisz, J. E.; Sharon, P.; Stenson, W. F. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models Gastroenterology 1984, 87, 1344-1350
27. Anderson, M. E. Determination of glutathione and glutathione disulfide in biological samples Methods Enzymol. 1985, 113, 548-555
28. Collado, M. C.; Delgado, S.; Maldonado, A.; Rodríguez, J. M. Assessment of the bacterial diversity of breast milk of healthy women by quantitative real-time PCR Lett. Appl. Microbiol. 2009, 48, 523-528
29. Veljaca, M.; Lesch, C. A.; Pllana, R.; Sanchez, B.; Chan, K.; Guglietta, A. BPC-15 reduces trinitrobenzene sulfonic-induced colonic damage in rats J. Pharmacol. Exp. Ther. 1995, 272, 417-422
30. Lara-Villoslada, F.; Debras, E.; Nieto, A.; Concha, A.; Gálvez, J.; López-Huertas, E.; Boza, J.; Obled, C.; Xaus, J. Oligosaccharides isolated from goat milk reduce intestinal inflammation in a rat model of dextran sodium sulfate-induced colitis Clin. Nutr. 2006, 25, 477-488
31. Koleva, P. T.; Valcheva, R. S.; Sun, X.; Gänzle, M. G.; Dieleman, L. A. Inulin and fructo-oligosaccharides have divergent effects on colitis and commensal microbiota in HLA-B27 transgenic rats Br. J. Nutr. 2012, 108, 1633-1643
32. Obermeier, F.; Dunger, N.; Deml, L.; Herfarth, H.; Schölmerich, J.; Falk, W. CpG motifs of bacterial DNA exacerbate colitis of dextran sulfate sodium-treated mice Eur. J. Immunol. 2002, 32, 2084-2092
33. Tytgat, K. M.; Bovelander, F. J.; Opdam, F. J.; Einerhand, A. W.; Büller, H. A.; Dekker, J. Biosynthesis of rat MUC2 in colon and its analogy with human MUC2 Biochem. J. 1995, 309, 221-229
34. Mashimo, H.; Wu, D. C.; Podolsky, D. K.; Fishman, M. C. Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor Science 1996, 274, 262-265
35. Mankertz, J.; Schulzke, J. D. Altered permeability in inflammatory bowel disease: pathophysiology and clinical implications Curr. Opin. Gastroenterol. 2007, 23, 379-383
36. Su, L.; Shen, L.; Clayburgh, D. R.; Nalle, S. C.; Sullivan, E. A.; Meddings, J. B.; Abraham, C.; Turner, J. R. Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis Gastroenterology 2009, 136, 551-563
37. Gersemann, M.; Becker, S.; Kübler, I.; Koslowski, M.; Wang, G.; Herrlinger, K. R.; Griger, J.; Fritz, P.; Fellermann, K.; Schwab, M.; Wehkamp, J.; Stange, E. F. Differences in goblet cell differentiation between Crohns disease and ulcerative colitis Differentiation 2009, 77, 84-94
38. Arpaia, N.; Campbell, C.; Fan, X.; Dikiy, S.; van der Veeken, J.; deRoos, P.; Liu, H.; Cross, J. R.; Pfeffer, K.; Coffer, P. J.; Rudensky, A. Y. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation Nature 2013, 504, 451-455
39. Sarra, M.; Pallone, F.; Macdonald, T. T.; Monteleone, G. IL-23/IL-17 axis in IBD Inflamm. Bowel Dis. 2010, 16, 1808-1813
40. Camuesco, D.; Rodríguez-Cabezas, M. E.; Garrido-Mesa, N.; Cueto-Sola, M.; Bailón, E.; Comalada, M.; Arribas, B.; Merlos, M.; Balsa, D.; Zarzuelo, A.; Janer, G.; Xaus, J.; Román, J.; Gálvez, J. The intestinal anti-inflammatory effect of dersalazine sodium is related to a down-regulation in IL-17 production in experimental models of rodent colitis Br. J. Pharmacol. 2012, 165, 729-740
41. Zhang, Z.; Zheng, M.; Bindas, J.; Schwarzenberger, P.; Kolls, J. K. Critical role of IL-17 receptor signaling in acute TNBS-induced colitis Inflamm. Bowel Dis. 2006, 12, 382-388
42. Garcia-Ramallo, E.; Marques, T.; Prats, N.; Beleta, J.; Kunkel, S. L.; Godessart, N. Resident cell chemokine expression serves as the major mechanism for leukocyte recruitment during local inflammation J. Immunol. 2002, 169, 6467-6473
43. Pavlick, K. P.; Laroux, F. S.; Fuseler, J.; Wolf, R. E.; Gray, L.; Hoffman, J.; Grisham, M. B. Role of reactive metabolites of oxygen and nitrogen in inflammatory bowel disease Free Radical Biol. Med. 2002, 33, 311-322