A galacto-oligosaccharides preparation derived from lactulose protects against colorectal cancer development in an animal model

Frontiers in Microbiology

Volumn 9, Issue AUG, 2018, Pages

  Fernández, Javier ^a,b   Moreno, F J ^c   Olano, Agustín ^c   Clemente, Alfonso ^d   Villar, Claudio J ^a,b   Lombó, Felipe ^a,b  

^a DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

^b INSTITUTO DE INVESTIGACIÓN SANITARIA DEL PRINCIPADO DE ASTURIAS ISPA   (Spain)

^c INSTITUTE OF FOOD SCIENCE RESEARCH CIAL   (Spain)

^d CSIC   (Spain)

Author keywords

Colorectal cancer; Galacto oligosaccharides; Gut microbiota; Prebiotic; Prevention

Indexed keywords

AZOXYMETHANE; BUTYRIC ACID; DEXTRAN SULFATE; GALACTOSE OLIGOSACCHARIDE; GENOMIC DNA; ISOBUTYRIC ACID; ISOVALERIC ACID; LACTULOSE; PREBIOTIC AGENT; PROPIONIC ACID; VALERIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDACEAE; BIFIDOBACTERIUM; CANCER GROWTH; CANCER PREVENTION; CHEMOPROPHYLAXIS; CLOSTRIDIACEAE; COHORT ANALYSIS; COLORECTAL CANCER; CONTROLLED STUDY; DNA EXTRACTION; FIRMICUTES; FLAME IONIZATION DETECTION; GAS CHROMATOGRAPHY; INTESTINE FLORA; LACHNOSPIRACEAE; LACTOBACILLACEAE; MALE; MASS FRAGMENTOGRAPHY; METAGENOMICS; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYP; PORPHYROMONADACEAE; RAT; RECTUM HEMORRHAGE; RNA SEQUENCE; ULCERATIVE COLITIS;

EID: 85052635075     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2018.02004     Document Type: Article

References (67)

1. Algieri, F., Rodríguez-Nogales, A., Garrido-Mesa, N., Vezza, T., Garrido-Mesa, J., Utrilla, M. P., et al. (2014). Intestinal anti-inflammatory Effects of Oligosaccharides derived from Lactulose in the Trinitrobenzenesulfonic acid model of rat colitis. J. Agric. Food Chem. 62, 4285-4297. doi: 10.1021/jf500678p
2. Arnold, M., Sierra, M. S., Laversanne, M., Soerjomataram, I., Jemal, A., and Bray, F. (2017). Global patterns and trends in colorectal cancer incidence and mortality. Gut 66, 683-691. doi: 10.1136/gutjnl-2015-310912
3. Bindels, L. B., Delzenne, N. M., Cani, P. D., and Walter, J. (2015). Towards a more comprehensive concept for prebiotics. Nat. Rev. Gastroenterol. Hepatol. 12, 303-310. doi: 10.1038/nrgastro.2015.47
4. Bosscher, D., Breynaert, A., Pieters, L., and Hermans, N. (2009). Food-based strategies to modulate the composition of the intestinal microbiota and their associated health effects. J. Physiol. Pharmacol. 60(Suppl. 6), 5-11
5. Bray, F., Ren, J.-S., Masuyer, E., and Ferlay, J. (2013). Global estimates of cancer prevalence for 27 sites in the adult population in 2008. Int. J. cancer 132, 1133-1145. doi: 10.1002/ijc.27711
6. Brenner, H., Kloor, M., and Pox, C. P. (2014). Colorectal cancer. Lancet 383, 1490-1502. doi: 10.1016/S0140-6736(13)61649-9
7. Canfora, E. E., Jocken, J. W., and Blaak, E. E. (2015). Short-chain fatty acids in control of body weight and insulin sensitivity. Nat. Rev. Endocrinol. 11, 577-591. doi: 10.1038/nrendo.2015.128
8. Cardelle-Cobas, A., Corzo, N., Olano, A., Peláez, C., Requena, T., and ávila, M. (2011). Galactooligosaccharides derived from lactose and lactulose: influence of structure on Lactobacillus, Streptococcus and Bifidobacterium growth. Int. J. Food Microbiol. 149, 81-87. doi: 10.1016/j.ijfoodmicro.2011.05.026
9. Cardelle-Cobas, A., Fernández, M., Salazar, N., Martínez-Villaluenga, C., Villamiel, M., Ruas-Madiedo, P., et al. (2009). Bifidogenic effect and stimulation of short chain fatty acid production in human faecal slurry cultures by oligosaccharides derived from lactose and lactulose. J. Dairy Res. 76, 317-325. doi: 10.1017/S0022029909004063
10. Cardelle-Cobas, A., Martínez-Villaluenga, C., Villamiel, M., Olano, A., and Corzo, N. (2008). Synthesis of oligosaccharides derived from lactulose and pectinex ultra SP-L. J. Agric. Food Chem. 56, 3328-3333. doi: 10.1021/jf073355b
11. Cardelle-Cobas, A., Olano, A., Corzo, N., Villamiel, M., Collins, M., Kolida, S., et al. (2012). in vitro fermentation of lactulose-derived oligosaccharides by mixed fecal microbiota. J. Agric. Food Chem. 60, 2024-2032. doi: 10.1021/jf203622d
12. Celiberto, L. S., Bedani, R., Dejani, N. N., Ivo de Medeiros, A., Sampaio Zuanon, J. A., Spolidorio, L. C., et al. (2017). Effect of a probiotic beverage consumption (Enterococcus faecium CRL 183 and Bifidobacterium longum ATCC 15707) in rats with chemically induced colitis. PLoS One 12:e0175935. doi: 10.1371/journal.pone.0175935
13. Chen, Q., Swist, E., Beckstead, J., Green, J., Matias, F., Roberts, J., et al. (2011). 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. 141, 790-797. doi: 10.3945/jn.110.133421
14. Clemente, A. (2014). "In vivo assessment of the bioactivity of food oligosaccharides," in Food Oligosaccharides: Production, Analysis and Bioactivity, eds F. J. Moreno and M. L. Sanz (Hoboken, NJ: John Wiley & Sons), 238-254. doi: 10.1002/9781118817360.ch14
15. Coutinho, C. M. L. M., Coutinho-Silva, R., Zinkevich, V., Pearce, C. B., Ojcius, D. M., and Beech, I. (2017). Sulphate-reducing bacteria from ulcerative colitis patients induce apoptosis of gastrointestinal epithelial cells. Microb. Pathog. 112, 126-134. doi: 10.1016/j.micpath.2017.09.054
16. Devkota, S., and Chang, E. B. (2015). Interactions between diet, bile acid metabolism, gut microbiota, and inflammatory bowel diseases. Dig. Dis. 33, 351-356. doi: 10.1159/000371687
17. Devkota, S., Wang, Y., Musch, M. W., Leone, V., Fehlner-Peach, H., Nadimpalli, A., et al. (2012). Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/-mice. Nature 487, 104-108. doi: 10.1038/nature11225
18. Díez-Municio, M., Herrero, M., Olano, A., and Moreno, F. J. (2014). Synthesis of novel bioactive lactose-derived oligosaccharides by microbial glycoside hydrolases. Microb. Biotechnol. 7, 315-331. doi: 10.1111/1751-7915.12124
19. Eun, C. S., Mishima, Y., Wohlgemuth, S., Liu, B., Bower, M., Carroll, I. M., et al. (2014). Induction of bacterial antigen-specific colitis by a simplified human microbiota consortium in gnotobiotic interleukin-10-/-mice. Infect. Immun. 82, 2239-2246. doi: 10.1128/IAI.01513-13
20. Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., et al. (2015). Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. cancer 136, E359-E386. doi: 10.1002/ijc.29210
21. Fernández, J., Redondo-Blanco, S., Miguélez, E. M., Villar, C. J., Clemente, A., and Lombó, F. (2015). Healthy effects of prebiotics and their metabolites against intestinal diseases and colorectal cancer. AIMS Microbiol. 1, 48-71. doi: 10.3934/microbiol.2015.1.48
22. Ferreira-Lazarte, A., Olano, A., Villamiel, M., and Moreno, F. J. (2017). Assessment of in vitro digestibility of dietary carbohydrates using rat small intestinal extract. J. Agric. Food Chem. 65, 8046-8053. doi: 10.1021/acs.jafc.7b01809
23. Gibson, G. R., Hutkins, R., Sanders, M. E., Prescott, S. L., Reimer, R. A., Salminen, S. J., et al. (2017). Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 14, 491-502. doi: 10.1038/nrgastro.2017.75
24. Gibson, G. R., and Roberfroid, M. B. (1995). Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr. 125, 1401-1412
25. Goodrich, J. K., Waters, J. L., Poole, A. C., Sutter, J. L., Koren, O., Blekhman, R., et al. (2014). Human genetics shape the gut microbiome. Cell 159, 789-799. doi: 10.1016/j.cell.2014.09.053
26. Han, Y.-M., Jeong, M., Park, J.-M., Kim, M.-Y., Go, E.-J., Cha, J. Y., et al. (2016). The ω-3 polyunsaturated fatty acids prevented colitis-associated carcinogenesis through blocking dissociation of β-catenin complex, inhibiting COX-2 through repressing NF-κB, and inducing 15-prostaglandin dehydrogenase. Oncotarget 7, 63583-63595. doi: 10.18632/oncotarget.11544
27. Hernández-Hernández, O., Marín-Manzano, M. C., Rubio, L. A., Moreno, F. J., Sanz, M. L., and Clemente, A. (2012). Monomer and linkage type of galacto-oligosaccharides affect their resistance to ileal digestion and prebiotic properties in rats. J. Nutr. 142, 1232-1239. doi: 10.3945/jn.111.155762
28. Huang, T.-H., Wu, S.-Y., Huang, Y.-J., Wei, P.-L., Wu, A. T., and Chao, T.-Y. (2017). The identification and validation of Trichosstatin A as a potential inhibitor of colon tumorigenesis and colon cancer stem-like cells. Am. J. Cancer Res. 7, 1227-1237
29. Jemal, A., Bray, F., Center, M. M., Ferlay, J., Ward, E., and Forman, D. (2011). Global cancer statistics. CA Cancer J. Clin. 61, 69-90. doi: 10.3322/caac.20107
30. Joossens, M., Huys, G., Cnockaert, M., Preter, V., De Verbeke, K., Rutgeerts, P., et al. (2011). Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives. Gut 60, 631-637. doi: 10.1136/gut.2010.223263
31. Kim, S. W., Kim, H. M., Yang, K. M., Kim, S.-A., Kim, S.-K., An, M. J., et al. (2010). Bifidobacterium lactis inhibits NF-kappaB in intestinal epithelial cells and prevents acute colitis and colitis-associated colon cancer in mice. Inflamm. Bowel Dis. 16, 1514-1525. doi: 10.1002/ibd.21262
32. Kim, Y. S., and Milner, J. A. (2007). Dietary modulation of colon cancer risk. J. Nutr. 137, 2576S-2579S. doi: 10.1093/jn/137.11.2576S
33. Koh, A., De Vadder, F., Kovatcheva-Datchary, P., and Bäckhed, F. (2016). From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165, 1332-1345. doi: 10.1016/j.cell.2016.05.041
34. Laparra, J. M., Díez-Municio, M., Herrero, M., and Moreno, F. J. (2014). Structural differences of prebiotic oligosaccharides influence their capability to enhance iron absorption in deficient rats. Food Funct. 5, 2430-2437. doi: 10.1039/c4fo00504j
35. Laparra, J. M., Hernandez-Hernandez, O., Moreno, F. J., and Sanz, Y. (2013). Neoglycoconjugates of caseinomacropeptide and galactooligosaccharides modify adhesion of intestinal pathogens and inflammatory response(s) of intestinal (Caco-2) cells. Food Res. Int. 54, 1096-1102. doi: 10.1016/j.foodres.2012.10.034
36. Lennon, G., Balfe,á, Bambury, N., Lavelle, A., Maguire, A., Docherty, N. G., et al. (2014). Correlations between colonic crypt mucin chemotype, inflammatory grade and Desulfovibrio species in ulcerative colitis. Colorectal Dis. 16,O161-O169. doi: 10.1111/codi.12503
37. Ley, R. E., Bäckhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., and Gordon, J. I. (2005). Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. U.S.A. 102, 11070-11075. doi: 10.1073/pnas.0504978102
38. Ley, R. E., Turnbaugh, P. J., Klein, S., and Gordon, J. I. (2006). Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022-1023. doi: 10.1038/4441022a
39. López-Sanz, S., Montilla, A., Moreno, F. J., and Villamiel, M. (2015). Stability of oligosaccharides derived from lactulose during the processing of milk and apple juice. Food Chem. 183, 64-71. doi: 10.1016/j.foodchem.2015.03.020
40. Louis, P., Hold, G. L., and Flint, H. J. (2014). The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol. 12, 661-672. doi: 10.1038/nrmicro3344
41. Marín-Manzano, M. C., Abecia, L., Hernández-Hernández, O., Sanz, M. L., Montilla, A., Olano, A., et al. (2013). 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. 61, 7560-7567. doi: 10.1021/jf402218z
42. Martínez-Villaluenga, C., Cardelle-Cobas, A., Olano, A., Corzo, N., Villamiel, M., and Jimeno, M. L. (2008). Enzymatic synthesis and identification of two trisaccharides produced from lactulose by transgalactosylation. J. Agric. Food Chem. 56, 557-563. doi: 10.1021/jf0721343
43. Merrill, R. M., and Anderson, A. E. (2011). Risk-adjusted colon and rectal cancer incidence rates in the United States. Dis. Colon Rectum 54, 1301-1306. doi: 10.1097/DCR.0b013e3182242bd3
44. Moreno, F. J., Montilla, A., Villamiel, M., Corzo, N., and Olano, A. (2014). Analysis, structural characterization, and bioactivity of oligosaccharides derived from lactose. Electrophoresis 35, 1519-1534. doi: 10.1002/elps.201300567
45. Omori, M., Maeda, S., Igarashi, H., Ohno, K., Sakai, K., Yonezawa, T., et al. (2017). Fecal microbiome in dogs with inflammatory bowel disease and intestinal lymphoma. J. Vet. Med. Sci. 79, 1840-1847. doi: 10.1292/jvms.17-0045
46. Ooi, C. C., Good, N. M., Williams, D. B., Lewanowitsch, T., Cosgrove, L. J., Lockett, T. J., et al. (2010). Efficacy of butyrate analogues in HT-29 cancer cells. Clin. Exp. Pharmacol. Physiol. 37, 482-489. doi: 10.1111/j.1440-1681.2009.05335.x
47. Paveljšek, D., Juvan, P., Košir, R., Rozman, D., Hacin, B., Ivicak-Kocjan, K., et al. (2018). Lactobacillus fermentum L930BB and Bifidobacterium animalis subsp. animalis IM386 initiate signalling pathways involved in intestinal epithelial barrier protection. Benef. Microbes 9, 515-525. doi: 10.3920/BM2017.0107
48. Perrin, S., Fougnies, C., Grill, J. P., Jacobs, H., and Schneider, F. (2002). Fermentation of chicory fructo-oligosaccharides in mixtures of different degrees of polymerization by three strains of bifidobacteria. Can. J. Microbiol. 48, 759-763. doi: 10.1139/w02-065
49. Png, C. W., Lindén, S. K., Gilshenan, K. S., Zoetendal, E. G., McSweeney, C. S., Sly, L. I., et al. (2010). Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am. J. Gastroenterol. 105, 2420-2428. doi: 10.1038/ajg.2010.281
50. Polansky, O., Sekelova, Z., Faldynova, M., Sebkova, A., Sisak, F., and Rychlik, I. (2016). Important metabolic pathways and biological processes expressed by chicken cecal microbiota. Appl. Environ. Microbiol. 82, 1569-1576. doi: 10.1128/AEM.03473-15
51. Pompei, A., Cordisco, L., Raimondi, S., Amaretti, A., Pagnoni, U. M., Matteuzzi, D., et al. (2008). in vitro comparison of the prebiotic effects of two inulin-type fructans. Anaerobe 14, 280-286. doi: 10.1016/j.anaerobe.2008.07.002
52. Pool-Zobel, B. L. (2005). Inulin-type fructans and reduction in colon cancer risk: review of experimental and human data. Br. J. Nutr. 93(Suppl. 1), S73-S90. doi: 10.1079/BJN20041349
53. Rastall, R. A. (2013). Gluco and galacto-oligosaccharides in food: update on health effects and relevance in healthy nutrition. Curr. Opin. Clin. Nutr. Metab. Care 16, 675-678. doi: 10.1097/MCO.0b013e328365b5fd
54. Rennick, D. M., Fort, M. M., and Davidson, N. J. (1997). Studies with IL-10-/-mice: an overview. J. Leukoc. Biol. 61, 389-396. doi: 10.1002/jlb.61.4.389
55. Roberfroid, M. B. (2007). Inulin-type fructans: functional food ingredients. J. Nutr. 137, 2493S-2502S. doi: 10.1093/jn/137.11.2493S
56. Roller, M., Pietro Femia, A., Caderni, G., Rechkemmer, G., and Watzl, B. (2004a). Intestinal immunity of rats with colon cancer is modulated by oligofructose-enriched inulin combined with Lactobacillus rhamnosus and Bifidobacterium lactis. Br. J. Nutr. 92, 931-938
57. Roller, M., Rechkemmer, G., and Watzl, B. (2004b). Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J. Nutr. 134, 153-156
58. Rumessen, J. J., Bodé, S., Hamberg, O., and Gudmand-Høyer, E. (1990). Fructans of Jerusalem artichokes: intestinal transport, absorption, fermentation, and influence on blood glucose, insulin, and C-peptide responses in healthy subjects. Am. J. Clin. Nutr. 52, 675-681. doi: 10.1093/ajcn/52.4.675
59. Scharlau, D., Borowicki, A., Habermann, N., Hofmann, T., Klenow, S., Miene, C., et al. (2009). Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre. Mutat. Res. 682, 39-53. doi: 10.1016/j.mrrev.2009.04.001
60. Sokol, H., Seksik, P., Rigottier-Gois, L., Lay, C., Lepage, P., Podglajen, I., et al. (2006). Specificities of the fecal microbiota in inflammatory bowel disease. Inflamm. Bowel Dis. 12, 106-111. doi: 10.1097/01.MIB.0000200323.38139.c6
61. Song, H., Wang, W., Shen, B., Jia, H., Hou, Z., Chen, P., et al. (2018). Pretreatment with probiotic Bifico ameliorates colitis-associated cancer in mice: transcriptome and gut flora profiling. Cancer Sci. 109, 666-677. doi: 10.1111/cas.13497
62. Stein, K., Borowicki, A., Scharlau, D., Schettler, A., Scheu, K., Obst, U., et al. (2012). Effects of synbiotic fermentation products on primary chemoprevention in human colon cells. J. Nutr. Biochem. 23, 777-784. doi: 10.1016/j.jnutbio.2011.03.022
63. Undseth, R., Jakobsdottir, G., Nyman, M., Berstad, A., and Valeur, J. (2015). Low serum levels of short-chain fatty acids after lactulose ingestion may indicate impaired colonic fermentation in patients with irritable bowel syndrome. Clin. Exp. Gastroenterol. 8, 303-308. doi: 10.2147/CEG.S94084
64. Venema, K., van Nuenen, M. H. M. C., van den Heuvel, E. G., Pool, W., and van der Vossen, J. M. B. M. (2003). The Effect of Lactulose on the composition of the intestinal microbiota and short-chain fatty acid production in human volunteers and a computer-controlled model of the proximal large intestine. Microb. Ecol. Health Dis. 15, 94-105. doi: 10.1080/08910600310019895
65. Verghese, M., Walker, L. T., Shackelford, L., and Chawan, C. B. (2005). Inhibitory effects of nondigestible carbohydrates of different chain lengths on azoxymethane-induced aberrant crypt foci in Fisher 344 rats. Nutr. Res. 25, 859-868. doi: 10.1016/j.nutres.2005.09.007
66. Wang, Y., Zeng, T., Wang, S., Wang, W., Wang, Q., and Yu, H.-X. (2010). Fructo-oligosaccharides enhance the mineral absorption and counteract the adverse effects of phytic acid in mice. Nutrition 26, 305-311. doi: 10.1016/j.nut.2009.04.014
67. Willing, B. P., Dicksved, J., Halfvarson, J., Andersson, A. F., Lucio, M., Zheng, Z., et al. (2010). A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139, 1844.e1-1854.e1. doi: 10.1053/j.gastro.2010.08.049