Structural Change in Microbiota by a Probiotic Cocktail Enhances the Gut Barrier and Reduces Cancer via TLR2 Signaling in a Rat Model of Colon Cancer

Digestive Diseases and Sciences

Volumn 61, Issue 10, 2016, Pages 2908-2920

  Kuugbee, Eugene Dogkotenge ^a,b   Shang, Xueqi ^a   Gamallat, Yaser ^a   Bamba, Djibril ^a   Awadasseid, Annoor ^a   Suliman, Mohammed Ahmed ^a   Zang, Shizhu ^a   Ma, Yufang ^a   Chiwala, Gift ^a   Xin, Yi ^a   Shang, Dong ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

^b Tamale Teaching Hospital   (Ghana)

Author keywords

Bifidobacteria; Colorectal cancer; Lactobacillus; Microbiota; Probiotics; Toll like receptors (TLRs)

Indexed keywords

1,2 DIMETHYLHYDRAZINE; AMPICILLIN; BETA CATENIN; CASPASE 3; CYCLOOXYGENASE 2; FRUCTOSE OLIGOSACCHARIDE; MALTODEXTRIN; MUCIN 2; OCCLUDIN; PROBIOTIC AGENT; PROTEIN ZO1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; CARCINOGEN; MUC2 PROTEIN, RAT; PTGS2 PROTEIN, RAT; TLR2 PROTEIN, RAT; TLR4 PROTEIN, RAT;

ANIMAL EXPERIMENT; ARTICLE; CANCER CONTROL; CANCER GROWTH; CANCER INCIDENCE; CLOSTRIDIUM; COLORECTAL CANCER; CONTROLLED STUDY; ESCHERICHIA; HELICOBACTER; HUMAN; INTESTINE FLORA; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS GASSERI; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS; PYROSEQUENCING; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TUMOR VOLUME; ANIMAL; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM LONGUM SUBSP. INFANTIS; CHEMICALLY INDUCED; COLON; COLON TUMOR; DISEASE COURSE; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL NEOPLASM; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MICROBIOLOGY; PATHOLOGY;

1,2-DIMETHYLHYDRAZINE; ANIMALS; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM LONGUM SUBSPECIES INFANTIS; CARCINOGENS; COLON; COLONIC NEOPLASMS; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GASTROINTESTINAL MICROBIOME; IMMUNOHISTOCHEMISTRY; LACTOBACILLUS ACIDOPHILUS; MALE; MUCIN-2; NEOPLASMS, EXPERIMENTAL; PROBIOTICS; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TUMOR BURDEN;

EID: 84978175747     PISSN: 01632116     EISSN: 15732568     Source Type: Journal    
DOI: 10.1007/s10620-016-4238-7     Document Type: Article

References (77)

1. Cenit MC, Matzaraki V, Tigchelaar EF, Zhernakova A. Rapidly expanding knowledge of the role of the gut microbiome in health and diseases. Biochim Biophys Acta. 2014;1842:1981–1992.
2. Compare D, Nardone G. The bacteria-hypothesis of colorectal cancer: pathogenetic and therapeutic implications. Transl Gastrointest Cancer. 2013;3:44–53.
3. Sonnenburg JL, Xu J, Leip DD, et al. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science. 2005;307:1955–1959.
4. LeBlanc JG, Milani C, De Giori GS, et al. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol. 2013;24:160–168.
5. Littman DR, Pamer EG. Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host Microbe. 2011;10:311–323.
6. Zackular JP, Baxter NT, Iverson KD, et al. The gut microbiome modulates colon tumorigenesis. mBio. 2013;4:e00692–e00613.
7. Liong MT. Role of probiotics and prebiotics in colon cancer prevention: postulated mechanisms and in-vivo evidence. Int J Mol Sci. 2008;9:854–863.
8. IOM (Institute of Medicine). The human microbiome, diet, and health; workshop summary. The National Academy of Science 2013.
9. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.
10. Dejea C, Wick E, Sears CL. Bacterial oncogenesis in the colon. Future Microbiol. 2013;8:445–460.
11. Allegra CJ, Paik S, Colangelo LH, et al. Prognostic value of thymidylate kinase synthase, Ki-67 and p53 in patients with Dukes B and C colon Cancer: a national cancer institute-National surgical Adjuvant Breast and bowel project collaborative study. J Clin Oncol. 2003;21:241–250.
12. Kranz D, Dobbelstein M. A killer promoting survival: p53 as a selective means to avoid side effects of chemotherapy. Cell Cycle. 2012;11:2053–2054.
13. Huxley RR, Ansary-Moghaddam A, Clifton P, Czernichow S, Parr CL, Woodward M. The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence. Int J Cancer. 2009;125:171–180.
14. McCullough ML, Patel AV, Kushi LH, et al. Following cancer prevention guidelines reduces risk of cancer, cardiovascular disease, and all-cause mortality. Cancer Epidemiol Biomarkers Prev. 2011;20:1089–1097.
15. Xinli L, Dachang W, Cuili Z, Yi X. Side effects of antibiotics on the intestinal microflora by PCR-DGGE. Pak J Pharm Sci. 2013;26:339–343.
16. Zhu Q, Jin Z, Wu W, et al. Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLoS ONE. 2014;9:e90849.
17. El-Mowafy AM, Al-Gayyar MM, Salem HA, et al. Novel chemotherapeutic and renal protective effects for the green tea (EGCG): role of oxidative stress and inflammatory-cytokine signaling. Phytomedicine. 2010;17:1067–1075.
18. Magoc T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27:2957–2963.
19. Bokulich NA, Subramanian S, Faith JJ, et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods. 2013;10:57–59.
20. Haas BJ, Gevers D, Earl AM, et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 2011;21:494–504.
21. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–336.
22. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–2200.
23. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–998.
24. DeSantis TZ, Hugenholtz P, Larsen N, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–5072.
25. Wang Q, Garrity GM, Tiedje JM, Cold JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–5267.
26. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797.
27. Lee JTY, Tasang WH, Chow JR. Simple modifications to standard TRizol protocol allow high yield RNA extraction from cells on resorbable materials. J Biomater Nanobiotechnol. 2011;2:41–48.
28. Gupta RA, Dubois RN. Colorectal Cancer Prevention and treatment by inhibition of Cyclooxygenase-2. Nutr Rev Cancer. 2001;1:11–21.
29. Li Y, Lu W, Saini S, Moukha-Chafiq O, Pathak V, Ananthan S. Identification of quinazoline compounds as novel potent inhibitors of Wnt/β-catenin signaling in colorectal cancer cells. Oncotarget. 2016;7:11263–11270.
30. Paul S, DeCastro AJ, Lee HJ, et al. Dietary intake of pterostilbene, a constituent of blueberries, inhibits the β -catenin/p65 downstream signaling pathway and colon carcinogenesis in rats. Carcin. 2010;31:1272–1278.
31. Hajrezaie M, Shams K, Moghadamtousi SZ, et al. Chemoprevention of colonic aberrant crypt foci by novel Schiff based dichlorido(4-methoxy-2-{[2-(piperazin-4-ium-1-yl)ethyl]iminomethyl}phenolate)Cd complex in azoxymethane-induced colorectal cancer in rats. SCI Rep. 2015;5:12379. doi:10.1038/srep12379.
32. Sohini W, Rozy K, Sarbjit SK, Davinder KD. Cyclooxygenase as a target in chemoprevention by probiotics during 1,2-dimethylhydrazine induced colon carcinogenesis in rats. Nutr Cancer. 2015;67:603–611.
33. Singh J, Rivenson A, Tomita M, Shimamura S, Ishibashi N, Reddy BS. Bifidobacterium longum, a lactic acid-producing intestinal bacterium inhibits colon cancer and modulates the intermediate biomarkers of colon carcinogenesis. Carcinogenesis. 1997;18:833–841.
34. Gallaher DD, Khil J. The effect of synbiotics on colon carcinogenesis in rats. J Nutr. 1999;129:1483S–1487S.
35. Xenoulis PG, Palculict B, Allenspach K, et al. Molecular-phylogenetic characterization of microbial communities imbalances in the small intestine of dogs with inflammatory bowel disease. FEMS Microbiol Ecol. 2008;66:579–589.
36. Coburn B, Sekirov I. Finlay BB: type III secretion systems and diseases. Clin Microbiol Rev. 2007;20:535–549.
37. Kessler M, Zielecki J, Thieck O, Mollenkopf HJ, Fotopoulou C, Meyer TF. Chlamydia trachomatis disturbs epithelial tissue homeostasis in fallopian tubes via paracrine Wnt signaling. Am J Pathol. 2012;180:186–198.
38. Chumduri C, Gurumurthy RK, Zadora PK, Mi Y, Meyer TF. Chlamydia infection promotes host DNA damage and proliferation but impairs the DNA damage response. Cell Host Microbe. 2013;13:746–758.
39. Kun D, Xiang-Lin C, Ming Z, Qi L. Chlamydia inhibit host cell apoptosis by inducing Bag-1 via the MAPK/ERK survival pathway. Apoptosis Int J Program Cell Death. 2013;18:1083–1092.
40. Chlamydia Can Cause DNA Damage Linked With Cancer Risk, Study Finds. http://www.huffingtonpost.com/2013/06/21/chlamydia-cancer-dna-damage_n_3479859.html.
41. Jenkins WD, LeVault K, Sutcliffe S. Chamydia trachonatis infection: possible co-factor for oropharyngeal cancer development. Oral Oncol. 2015;51:e8–e9.
42. Wu S, Rhee KJ, Albesiano E, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med. 2009;15:1016–1022.
43. Sokol SY. Wnt signaling and dorso-ventral axis specification in vertebrates. Curr Opin Genet Dev. 1999;9:405–410.
44. Dulal S, Keku OT. Gut microbiome and colorectal adenomas. Cancer J. 2014;20:225–231.
45. Shiryaev SA, Remacle AG, Chernov AV, et al. Substrate cleavage profiling suggests a distinct function of Bacteroides fragilis metalloproteinases (fragilysin and metalloproteinase II) at the microbiome-inflammation-cancer interface. J Biol Chem. 2013;288:34956–34967.
46. Sears CL. Enterotoxigenic Bacteroides fragilis: a rogue among symbiotes. Clin Microbiol Rev. 2009;22:349–369.
47. Tosolini M, Kirilovsky A, Mlecnik B, et al. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res. 2011;71:1263–1271.
48. Goodwin AC, Destefano Shields CE, Wu S, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA. 2011;108:15354–15359.
49. Satishchandran C, Markham GD, Moore RC, Boyle SM. Location of SpeA, SpeB, SpeC and Metk genes on the physical map of Escherichia coli. J Bacteriol. 1990;172:4748.
50. Stover CK, Pham X-QT, Erwin AL, et al. Complete genome sequence of pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature. 2000;406:956–964.
51. Shogan BD, Smith DP, Christley S, Gilbert JA, Zaborina O, Averdy JC. Intestinal anastomotic injury alters spatially defined microbiome composition and function. Microbiome. 2014;2:35.
52. Torres AG. Adhesion of enteropathogenic Escherichia coli. Ecosal Plus. 2006. doi:10.1128/ecosaplus.8.3.2.4.
53. Bernstein C, Holubec H, Bhattacharyya AK, et al. Carcinogenicity of deoxycholate, a secondary bile acid. Arch Toxicol. 2011;85:863–871.
54. Sirinathsinghji Eva. Gut microbiota and cancer. ISIS Report 2014. http://www.i-sis.org.uk/The_Gut_Microbiome_and_cancer.php. Retrieved: 20/10/2016.
55. Fujimori S, Kishida T, Kobayashi T, et al. Helicobacter pylori infection increases the risk of colorectal adenoma and adenocarcinoma, especially in women. J Gastroenterol. 2005;40:887–893.
56. Galdeano M, Perdigon G. The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol. 2006;13:219–226.
57. Rafter J, Bennett M, Caderni G, et al. Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients. Am J Clin Nutr. 2007;85:488–496.
58. Hamilton MK, Boundry G, Lemay DG, Raybould HE. Changes in intestinal barrier function and gut microbiota in high-fat-diet-fed rats are dynamic and region dependent. Am J Physiol Gastroenterol Liver Physiol. 2015;308:G840–G851.
59. Yuhara H, Steinmaus C, Cohen SE, Corley DA, Tei Y, Buffer PA. Is diabetes mellitus an independent risk factor for colon cancer and rectal cancer? Am J Gastroenterol. 2011;106:1911–1922.
60. Krych T, Nielsen DS, Hansen AK, Hansen CH. Gut microbial markers are associated with diabetes onset, regulatory imbalance, and INF-y lelel in NOD mice. Gut Microbes. 2015;6:101–109.
61. Yang K, Popova NV, Yang WC, et al. Interaction of Muc2 and Apc on Wnt signaling and in intestinal tumorigenesis: potential role of chronic inflammation. Cancer Res. 2008;68:7313–7322.
62. Cario E. Barrier-protective function of intestinal epithelial Toll-like receptor 2. Mucosal Immunol. 2008;1:S62–S66.
63. Mennigen R, Nolte K, Rijcken E, et al. Probiotic mixture VSL# 3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am J Physiol Gastrointest Liver Physiol. 2009;296:G1140–G1149.
64. Ohland CL, MacNaughton WK. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol. 2010;298:G807–G819.
65. Prisciandaro LD, Geier MS, Butler RN, Cummins AG, Howarth GS. Evidence supporting the use of probiotics for the prevention and treatment of chemotherapy-induced intestinal mucositis. Crit Rev Food Sci Nutr. 2011;51:239–247.
66. Lowe EL, Crother TR, Rabizadeh S, et al. Toll-like receptor 2 signaling protects mice from tumor development in a mouse model of colitis-induced cancer. PLoS ONE. 2010;5:e13027.
67. Cario E, Gerken G, Podolsky D. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology. 2007;132:1359–1374.
68. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol. 2010;10:131–144.
69. Nurmi JT, Puolakkainen PA, Rautonen NE. Bifidobacterium lactis sp. 420 up-regulates cyclooxygenase(Cox)-1 and down-regulates Cox-2 gene expression in Caco-2 cell culture model. Nutr Cancer. 2005;51:83–93.
70. Otte JM, Mahjurian-Namari R, Brand S, Werner I, Schmidt WE, Schmitz F. Probiotics regulate the expression of Cox-2 in intestinal epithelial cells. Nutr Cancer. 2009;61:103–113.
71. Poijakovic M, Svensson M, Svanborg C, Johansson K, Larsson B, Persson KP. Escherichia coli-induced inducible nitric oxide synthase and cyclooxygenase expression in the mouse bladder and kidney. Kidney Int. 2001;59:893–904.
72. Sadikot RT, Zeng H, Azim AC, et al. Bacterial clearance of Pseudomonas aeruginosa is enhanced by the inhibition of Cox-2. Eur J Immunol. 2007;37:1001–1009.
73. Rupp J, Berger M, Reiling N, et al. Cox-2 inhibition abrogates Chlamydia pneumoniae-induced PGE2 and MMP-1 expression. Biochem Biophys Res Commun. 2004;320:738–744.
74. Sierra JC, Hobbs S, Chaturvedi R, et al. Induction of Cox-2 expression by Helicobacter pylori is mediated by activation of epidermal growth factor receptor in gastric epithelial cells. Am J Physiol Gastrointest Liver. 2013;305:G196–G203.
75. Sz-Jie W, Jong-Yi F, Chang-chai N, Chong-Yi W, Yuan-Tay S. Anti-inflammatory activity of lactobacillus-fermented adlay-soymilk in LPS-induced macrophages through suppression of NF-kB pathways. Food Res Int. 2013;52:262–268.
76. Roy B, Subramaniam D, Ahmed I, et al. Role of bacterial infection in the epigenetic regulation of Wnt antagonist WIF1 by PRC2 protein EZH2. Oncogene. 2015;34:4519–4530.
77. Umar S. Citrobacter infection and wnt signaling. Curr Colorectal Cancer Rep. 2012;8:298–306.