Effect of dietary fibers on cecal microbiota and intestinal tumorigenesis in azoxymethane treated A/J Min/+ mice

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Moen, Birgitte ^a   Henjum, Kristi ^b,c   Måge, Ingrid ^a   Knutsen, Svein Halvor ^a   Rud, Ida ^a   Hetland, Ragna Bogen ^c   Paulsen, Jan Erik ^d  

^a NOFIMA   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^d NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

AZOXYMETHANE; CELLULOSE; INULIN; RNA 16S;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDETES; BREWERS SPENT GRAIN; CARCINOGENESIS; CECUM; COLON TUMOR; DIETARY FIBER; FEMALE; FIRMICUTES; GRAIN; INTESTINE FLORA; INTESTINE TUMOR; MALE; MICROBIAL DIVERSITY; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; SMALL INTESTINE TUMOR; TAXONOMY; ANALYSIS OF VARIANCE; ANIMAL; BODY WEIGHT; C57BL MOUSE; CHEMICALLY INDUCED; CHEMISTRY; COLON; DIET; DIET THERAPY; DRUG EFFECTS; HIGH THROUGHPUT SEQUENCING; METABOLISM; MICROBIOLOGY; MICROFLORA; PATHOLOGY;

ANALYSIS OF VARIANCE; ANIMALS; AZOXYMETHANE; BACTEROIDETES; BODY WEIGHT; CARCINOGENESIS; CECUM; CELLULOSE; COLON; COLONIC NEOPLASMS; DIET; DIETARY FIBER; FIRMICUTES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INULIN; MALE; MICE; MICE, INBRED C57BL; MICROBIOTA; RNA, RIBOSOMAL, 16S;

EID: 84982131504     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0155402     Document Type: Article

References (79)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61(2):69-90. doi: 10.3322/caac.20107 PMID: 21296855.
2. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015; 136(5): E359-E86. WOS:000346350500015. doi: 10.1002/ijc.29210 PMID: 25220842
3. Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, Norat T, et al. Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet. 2003; 361(9368):1496-501. WOS:000182658900007. PMID: 12737858
4. Murphy N, Norat T, Ferrari P, Jenab M, Bueno-de-Mesquita B, Skeie G, et al. Dietary fibre intake and risks of cancers of the colon and rectum in the European prospective investigation into cancer and nutrition (EPIC). PLoS One. 2012; 7(6):e39361. doi: 10.1371/journal.pone.0039361 PMID: 22761771; PubMed Central PMCID: PMCPMC3382210.
5. Peters U, Sinha R, Chatterjee N, Subar AF, Ziegler RG, Kulldorff M, et al. Dietary fibre and colorectal adenoma in a colorectal cancer early detection programme. Lancet. 2003; 361(9368):1491-5. doi: 10.1016/S0140-6736(03)13173-X PMID: 12737857.
6. Johnson IT, Lund EK. Review article: nutrition, obesity and colorectal cancer. Aliment Pharmacol Ther. 2007; 26(2):161-81. doi: 10.1111/j.1365-2036.2007.03371.x PMID: 17593063.
7. Food, Nutrition, Physical Activity, and the Prevention of Colorectal Cancer. 2011.
8. Pericleous M, Mandair D, Caplin ME. Diet and supplements and their impact on colorectal cancer. J Gastrointest Oncol. 2013; 4(4):409-23. doi: 10.3978/j.issn.2078-6891.2013.003 PMID: 24294513; PubMed Central PMCID: PMC3819783.
9. Trowell H. Dietary fibre and coronary heart disease. Rev Eur Etud Clin Biol. 1972; 17(4):345-9. PMID: 4562450.
10. Jones JR, Lineback DM, Levine MJ. Dietary reference intakes: Implications for fiber labeling and consumption: A summary of the International Life Sciences Institute North America Fiber Workshop, June 1-2, 2004, Washington, DC. Nutr Rev. 2006; 64(1):31-8. WOS:000235127800003. PMID: 16491667
11. Cummings JH, Stephen AM. Carbohydrate terminology and classification. Eur J Clin Nutr. 2007; 61:S5-S18. WOS:000250894800002. PMID: 17992187
12. Blaut M. Relationship of prebiotics and food to intestinal microflora. Eur J Nutr. 2002; 41 Suppl 1:I11-6. doi: 10.1007/s00394-002-1102-7 PMID: 12420111.
13. Cummings JH, Macfarlane GT, Englyst HN. Prebiotic digestion and fermentation. Am J Clin Nutr. 2001; 73(2):415s-20s. WOS:000166608200010. PMID: 11157351
14. Zeng H, Lazarova DL, Bordonaro M. Mechanisms linking dietary fiber, gut microbiota and colon cancer prevention. World J Gastrointest Oncol. 2014; 6(2):41-51. doi: 10.4251/wjgo.v6.i2.41 PMID: 24567795; PubMed Central PMCID: PMCPMC3926973.
15. Fotiadis CI, Stoidis CN, Spyropoulos BG, Zografos ED. Role of probiotics, prebiotics and synbiotics in chemoprevention for colorectal cancer. World J Gastroenterol. 2008; 14(42):6453-7. PMID: 19030195; PubMed Central PMCID: PMCPMC2773329.
16. Saulnier DM, Spinler JK, Gibson GR, Versalovic J. Mechanisms of probiosis and prebiosis: considerations for enhanced functional foods. Curr Opin Biotechnol. 2009; 20(2):135-41. doi: 10.1016/j.copbio.2009.01.002 PMID: 19243931; PubMed Central PMCID: PMCPMC2713183.
17. Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nature Reviews Microbiology. 2014; 12(10):661-72. WOS:000342267900008. doi: 10.1038/nrmicro3344 MID: 25198138
18. Macfarlane GT, Steed H, Macfarlane S. Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. Journal of Applied Microbiology. 2008; 104(2):305-44. WOS:000252496100001. doi: 10.1111/j.1365-2672.2007.03520.x PMID: 18215222
19. Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer. 2013; 13(11):800-12. WOS:000326275700010. doi: 10.1038/nrc3610 PMID: 24132111
20. Zackular JP, Baxter NT, Chen GY, Schloss PD. Manipulation of the Gut Microbiota Reveals Role in Colon Tumorigenesis. mSphere. 2016; 1(1). doi: 10.1128/mSphere.00001-15
21. Donohoe DR, Holley D, Collins LB, Montgomery SA, Whitmore AC, Hillhouse A, et al. A Gnotobiotic Mouse Model Demonstrates That Dietary Fiber Protects against Colorectal Tumorigenesis in a Microbiota- and Butyrate-Dependent Manner. Cancer Discov. 2014; 4(12):1387-97. WOS:000346501900023. doi: 10.1158/2159-8290.CD-14-0501 PMID: 25266735
22. Fodde R. The APC gene in colorectal cancer. Eur J Cancer. 2002; 38(7):867-71. WOS:000175977900003. PMID: 11978510
23. Half E, Bercovich D, Rozen P. Familial adenomatous polyposis. Orphanet J Rare Dis. 2009; 4. WOS:000272055900001.
24. Fearnhead NS, Britton MP, Bodmer WF. The ABC of APC. Hum Mol Genet. 2001; 10(7):721-33. WOS:000168224100011. PMID: 11257105
25. Paulsen JE. Modulation by dietary factors in murine FAP models. Toxicology Letters. 2000; 112:403-9. WOS:000086260200055. PMID: 10720759
26. van Es JH, Giles RH, Clevers HC. The many faces of the tumor suppressor gene APC. Exp Cell Res. 2001; 264(1):126-34. WOS:000167623600012. PMID: 11237529
27. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C, et al. Multiple Intestinal Neoplasia Caused by a Mutation in the Murine Homolog of the Apc Gene. Science. 1992; 256(5057):668-70. WOS:A1992HR18500033. PMID: 1350108
28. Fodde R, Smits R. Disease model: familial adenomatous polyposis. Trends Mol Med. 2001; 7(8):369-73. WOS:000170534000007. PMID: 11516998
29. Sodring M, Gunnes G, Paulsen JE. Spontaneous initiation, promotion, and progression of colorectal cancer in the novel A/J Min/+ mouse. Int J Cancer. 2015. doi: 10.1002/ijc.29928 PMID: 26566853.
30. Ølstørn HBA. The effect of acrylamide and glycidamide on intestinal carcinogenesis in mice. PhD dissertation University of Oslo: Faculty of Mathematics and Natural Sciences. 2009.
31. Mollersen L, Paulsen JE, Alexander J. Loss of heterozygosity and nonsense mutation in Apc in azoxymethane-induced colonic tumours in min mice. Anticancer Res. 2004; 24(5A):2595-9. PMID: 15517863.
32. Rosenberg DW, Giardina C, Tanaka T. Mouse models for the study of colon carcinogenesis. Carcinogenesis. 2009; 30(2):183-96. doi: 10.1093/carcin/bgn267 PMID: 19037092; PubMed Central PMCID: PMCPMC2639048.
33. Meunier C, Kwan T, Turbide C, Beauchemin N, Gros P. Genetic control of susceptibility to carcinogen-induced colorectal cancer in mice: the Ccs3 and Ccs5 loci regulate different aspects of tumorigenesis. Cell Cycle. 2011; 10(11):1739-49. PMID: 21543896.
34. Meunier C, Van Der Kraak L, Turbide C, Groulx N, Labouba I, Cingolani P, et al. Positional mapping and candidate gene analysis of the mouse Ccs3 locus that regulates differential susceptibility to carcinogen-induced colorectal cancer. PLoS One. 2013; 8(3):e58733. doi: 10.1371/journal.pone.0058733 PMID: 23516545; PubMed Central PMCID: PMCPMC3597735.
35. Gu S, Chen D, Zhang JN, Lv X, Wang K, Duan LP, et al. Bacterial community mapping of the mouse gastrointestinal tract. PLoS One. 2013; 8(10):e74957. doi: 10.1371/journal.pone.0074957 PMID: 24116019; PubMed Central PMCID: PMCPMC3792069.
36. Zeng H, Grapov D, Jackson MI, Fahrmann J, Fiehn O, Combs GF. Integrating Multiple Analytical Datasets to Compare Metabolite Profiles of Mouse Colonic-Cecal Contents and Feces. Metabolites. 2015; 5(3):489-501. doi: 10.3390/metabo5030489 PMID: 26378591; PubMed Central PMCID: PMCPMC4588808.
37. Svendsen C, Alexander J, Paulsen JE, Knutsen HK, Hjertholm H, Brantsaeter AL, et al. The impact of commercial rodent diets on the induction of tumours and flat aberrant crypt foci in the intestine of multiple intestinal neoplasia mice. Lab Anim. 2012; 46(3):207-14. doi: 10.1258/la.2012.011055 PMID: 22522416.
38. Denstadli V, Ballance S, Knutsen SH, Westereng B, Svihus B. Influence of graded levels of brewers dried grains on pellet quality and performance in broiler chickens. Poultry Science. 2010; 89(12):2640-5. WOS:000284149800012. doi: 10.3382/ps.2010-00724 PMID: 21076102
39. Svendsen C, Husoy T, Glatt H, Paulsen JE, Alexander J. 5-Hydroxymethylfurfural and 5-sulfooxymethylfurfural increase adenoma and flat ACF number in the intestine of Min/+ mice. Anticancer Res. 2009; 29(6):1921-6. PMID: 19528448.
40. Paulsen JE, Steffensen IL, Olstorn HB, Alexander J. Prevalent location of flat dysplastic aberrant crypt foci near lymphoid follicles in the colon of azoxymethane-treated rats. Anticancer Res. 2006; 26(3A):1803-7. PMID: 16827110.
41. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. Isme J. 2012; 6(8):1621-4. doi: 10.1038/Ismej.2012.8 ISI:000306495800018. PMID: 22402401
42. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7(5):335-6. doi: 10.1038/Nmeth.F.303 ISI:000277175100003. PMID: 20383131
43. Rideout JR, He Y, Navas-Molina JA, Walters WA, Ursell LK, Gibbons SM, et al. Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. Peerj. 2014; 2. ARTN e545. doi: 10.7717/peerj.545 ISI:000347618000003.
44. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010; 26(19):2460-1. WOS:000282170000016. doi: 10.1093/bioinformatics/btq461 PMID: 20709691
45. Langsrud Ø. 50-50 multivariate analysis of variance for collinear responses. J Roy Stat Soc D-Sta. 2002; 51:305-17. ISI:000177528200001.
46. Martens H, Næs T. Multivariate calibration. Chichester: Wiley; 1989. XVII, 419 s. p.
47. Tran TN, Afanador NL, Buydens LMC, Blanchet L. Interpretation of variable importance in Partial Least Squares with Significance Multivariate Correlation (sMC). Chemometrics and Intelligent Laboratory Systems. 2014; 138:153-60. WOS:000343961200017.
48. Pool-Zobel BL. Inulin-type fructans and reduction in colon cancer risk: review of experimental and human data. Br J Nutr. 2005; 93 Suppl 1:S73-90. PMID: 15877900.
49. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I, et al. Prebiotic effects: metabolic and health benefits. Br J Nutr. 2010; 104 Suppl 2:S1-63. doi: 10.1017/S0007114510003363 PMID: 20920376.
50. Mauro MO, Monreal MT, Silva MT, Pesarini JR, Mantovani MS, Ribeiro LR, et al. Evaluation of the antimutagenic and anticarcinogenic effects of inulin in vivo. Genet Mol Res. 2013; 12(3):2281-93. doi: 10.4238/2013.July.8.9 PMID: 23884771.
51. Reddy BS, Hamid R, Rao CV. Effect of dietary oligofructose and inulin on colonic preneoplastic aberrant crypt foci inhibition. Carcinogenesis. 1997; 18(7):1371-4. WOS:A1997XJ97200014. PMID: 9230282
52. Rowland IR, Rumney CJ, Coutts JT, Lievense LC. Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis. 1998; 19(2):281-5. WOS:000072109000007. PMID: 9498277
53. Verghese M, Rao DR, Chawan CB, Shackelford L. Dietary inulin suppresses azoxymethane-induced preneoplastic aberrant crypt foci in mature Fisher 344 rats. J Nutr. 2002; 132(9):2804-8. PMID: 12221249.
54. Verghese M, Rao DR, Chawan CB, Williams LL, Shackelford L. Dietary inulin suppresses azoxymethane-induced aberrant crypt foci and colon tumors at the promotion stage in young Fisher 344 rats. J Nutr. 2002; 132(9):2809-13. PMID: 12221250.
55. Femia AP, Luceri C, Dolara P, Giannini A, Biggeri A, Salvadori M, et al. Antitumorigenic activity of the prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis on azoxymethane-induced colon carcinogenesis in rats. Carcinogenesis. 2002; 23(11):1953-60. PMID: 12419846.
56. Mutanen M, Pajari AM, Oikarinen SI. Beef induces and rye bran prevents the formation of intestinal polyps in Apc(Min) mice: relation to beta-catenin and PKC isozymes. Carcinogenesis. 2000; 21(6):1167-73. WOS:000087819100014. PMID: 10837006
57. Pajari AM, Rajakangas J, Paivarinta E, Kosma VM, Rafter J, Mutanen M. Promotion of intestinal tumor formation by inulin is associated with an accumulation of cytosolic beta-catenin in Min mice. Int J Cancer. 2003; 106(5):653-60. WOS:000184792300003. PMID: 12866023
58. Misikangas M, Tanayama H, Rajakangas J, Linden J, Pajari AM, Mutanen M. Inulin results in increased levels of beta-catenin and cyclin D1 as the adenomas increase in size from small to large in the Min/+ mouse. Brit J Nutr. 2008; 99(5):963-70. WOS:000255413600005. PMID: 17977470
59. Pierre F, Perrin P, Champ M, Bornet F, Meflah K, Menanteau J. Short-chain fructo-oligosaccharides reduce the occurrence of colon tumors and develop gut-associated lymphoid tissue in Min mice. Cancer Res. 1997; 57(2):225-8. WOS:A1997WC72100009. PMID: 9000559
60. Gibson GR, Probert HM, Van Loo J, Rastall RA, Roberfroid MB. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev. 2004; 17(2):259-75. doi: 10.1079/nrr200479 WOS:000225865600010. PMID: 19079930
61. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995; 125(6):1401-12. PMID: 7782892.
62. Campbell JM, Fahey GC Jr, Wolf BW. Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. J Nutr. 1997; 127(1):130-6. PMID: 9040556.
63. Chassaing B, Miles-Brown J, Pellizzon M, Ulman E, Ricci M, Zhang L, et al. Lack of soluble fiber drives diet-induced adiposity in mice. Am J Physiol Gastrointest Liver Physiol. 2015; 309(7):G528-41. doi: 10.1152/ajpgi.00172.2015 PMID: 26185332; PubMed Central PMCID: PMCPMC4593822.
64. Scott KP, Antoine JM, Midtvedt T, van Hemert S. Manipulating the gut microbiota to maintain health and treat disease. Microb Ecol Health Dis. 2015; 26:25877. doi: 10.3402/mehd.v26.25877 PMID: 25651995; PubMed Central PMCID: PMC4315778.
65. Feng Q, Liang SS, Jia HJ, Stadlmayr A, Tang LQ, Lan Z, et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun. 2015; 6. WOS:000352720000018.
66. Freilich S, Kreimer A, Borenstein E, Yosef N, Sharan R, Gophna U, et al. Metabolic-network-driven analysis of bacterial ecological strategies. Genome Biology. 2009; 10(6). Artn R61. doi: 10.1186/Gb-2009-10-6-R61 ISI:000267604300011.
67. Hansen NC, Avershina E, Mydland LT, Naesset JA, Austbo D, Moen B, et al. High nutrient availability reduces the diversity and stability of the equine caecal microbiota. Microb Ecol Health Dis. 2015; 26:27216. doi: 10.3402/mehd.v26.27216 PMID: 26246403.
68. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012; 489(7415):220-30. doi: 10.1038/nature11550 PMID: 22972295; PubMed Central PMCID: PMCPMC3577372.
69. Wolin MJ. Fermentation in the rumen and human large intestine. Science. 1981; 213(4515):1463-8. PMID: 7280665.
70. Nagy-Szakal D, Hollister EB, Luna RA, Szigeti R, Tatevian N, Smith CW, et al. Cellulose supplementation early in life ameliorates colitis in adult mice. PLoS One. 2013; 8(2):e56685. doi: 10.1371/journal.pone.0056685 PMID: 23437211; PubMed Central PMCID: PMCPMC3577696.
71. Tannock GW, Lawley B, Munro K, Sims IM, Lee J, Butts CA, et al. RNA-Stable-Isotope Probing Shows Utilization of Carbon from Inulin by Specific Bacterial Populations in the Rat Large Bowel. Appl Environ Microb. 2014; 80(7):2240-7. WOS:000332840700022.
72. Zhu QC, Jin ZM, Wu W, Gao RY, Guo BM, Gao ZG, et al. Analysis of the Intestinal Lumen Microbiota in an Animal Model of Colorectal Cancer. Plos One. 2014; 9(3). WOS:000332483600096.
73. Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Folsch UR, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004; 53(5):685-93. WOS:000220814100015. PMID: 15082587
74. Frank DN, Amand ALS, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104(34):13780-5. WOS:000249064700047. PMID: 17699621
75. Son JS, Khair S, Pettet DW, Ouyang NT, Tian XY, Zhang YH, et al. Altered Interactions between the Gut Microbiome and Colonic Mucosa Precede Polyposis in APC(Min/+) Mice. Plos One. 2015; 10(6). WOS:000358150400009.
76. Ou JH, Carbonero F, Zoetendal EG, DeLany JP, Wang M, Newton K, et al. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr. 2013; 98(1):111-20. WOS:000320909200015. doi: 10.3945/ajcn.112.056689 PMID: 23719549
77. Marquet P, Duncan SH, Chassard C, Bernalier-Donadille A, Flint HJ. Lactate has the potential to promote hydrogen sulphide formation in the human colon. Fems Microbiology Letters. 2009; 299(2):128-34. WOS:000269866500002. doi: 10.1111/j.1574-6968.2009.01750.x PMID: 19732152
78. Roediger WEW, Moore J, Babidge W. Colonic sulfide in pathogenesis and treatment of ulcerative colitis. Digest Dis Sci. 1997; 42(8):1571-9. WOS:A1997XT75500001. PMID: 9286219
79. Carbonero F, Benefiel AC, Gaskins HR. Contributions of the microbial hydrogen economy to colonic homeostasis. Nat Rev Gastro Hepat. 2012; 9(9):504-18. WOS:000308503900005.