1887

Abstract

Tools that predict the risk of colorectal cancer are important for early diagnosis, given the high mortality rate for this cancer. The composition of the intestinal microbiota is now considered to be a risk factor for the development of colorectal cancer. This discovery has motivated a growing number of studies to identify the micro-organisms responsible for the onset and/or progression of colorectal cancer. With this in mind, this review discusses the relationship between the composition of the intestinal microbiota and colorectal cancer risk. Prospective and case–control studies indicate that the intestinal microbiota of individuals with colorectal cancer usually contains a greater proportion of bacteria responsible for gastrointestinal tract inflammatory diseases, as well as bacteria that produce toxins and carcinogenic metabolites. In contrast, there tends to be a reduced presence of butyric acid-producing bacteria, probiotic bacteria and potentially probiotic bacteria. Despite these differences, the onset and development of colorectal cancer cannot be attributed to a specific micro-organism. Thus, studies focused on the formation of the intestinal microbiota and factors that modulate its composition are important for the development of approaches for colorectal cancer prevention.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001049
2019-08-19
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jmm/68/10/1391.html?itemId=/content/journal/jmm/10.1099/jmm.0.001049&mimeType=html&fmt=ahah

References

  1. Fearon ER. Molecular genetics of colorectal cancer. Annu Rev Pathol 2011; 6:479–507 [View Article]
    [Google Scholar]
  2. WHO World Health Organization 2016; Global health observatory: cancer mortality and morbidity. [Internet] http://www.who.int/gho/ncd/mortality_morbidity/cancer_text/en/
    [Google Scholar]
  3. Reddy BS, Weisburger JH, Narisawa T, Wynder EL. Colon carcinogenesis in germ-free rats with 1,2-dimethylhydrazine and N-methyl-N'-nitro-N-nitrosoguanidine. Cancer Res 1974; 34:2368–2372
    [Google Scholar]
  4. Kado S, Uchida K, Funabashi H, Iwata S, Nagata Y et al. Intestinal microflora are necessary for development of spontaneous adenocarcinoma of the large intestine in T-cell receptor beta chain and p53 double-knockout mice. Cancer Res 2001; 61:2395–2398
    [Google Scholar]
  5. Erdman SE, Poutahidis T, Tomczak M, Rogers AB, Cormier K et al. Cd4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol 2003; 162:691–702 [View Article]
    [Google Scholar]
  6. Wong SH, Zhao L, Zhang X, Nakatsu G, Han J et al. Gavage of fecal samples from patients with colorectal cancer promotes intestinal carcinogenesis in germ-free and conventional mice. Gastroenterology 2017; 153:1621–1633 [View Article]
    [Google Scholar]
  7. Sears CL, Pardoll DM. Perspective: alpha-bugs, their microbial partners, and the link to colon cancer. J Infect Dis 2011; 203:306–311 [View Article]
    [Google Scholar]
  8. Tjalsma H, Boleij A, Marchesi JR, Dutilh BE. A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat Rev Microbiol 2012; 10:575–582 [View Article]
    [Google Scholar]
  9. Flemer B, Lynch DB, Brown JMR, Jeffery IB, Ryan FJ et al. Tumour-associated and non-tumour-associated microbiota in colorectal cancer. Gut 20161–11
    [Google Scholar]
  10. Gao Z, Guo B, Gao R, Zhu Q, Qin H. Microbiota disbiosis is associated with colorectal cancer. Fronst Microbiol 2015; 6:1–9
    [Google Scholar]
  11. Mima K, Nishihara R, Qian ZR, Cao Y, Sukawa Y et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 2015; 0:1–8
    [Google Scholar]
  12. Allali I, Delgado S, Marron PI, Astudillo A, Yeh JJ et al. Gut microbiome compositional and functional differences between tumor and non-tumor adjacent tissues from cohorts from the US and Spain. Gut Microbes 2015; 6:161–172 [View Article]
    [Google Scholar]
  13. Ito M, Kanno S, Nosho K, Sukawa Y, Mitsuhashi K et al. Association of Fusobacterium nucleatum with clinical and molecular features in colorectal serrated pathway. Int J Antimicrob Agents 20151–11
    [Google Scholar]
  14. Viljoen KS, Dakshinamurthy A, Goldberg P, Blackburn JM. Quantitative profiling of colorectal cancer-associated bacteria reveals associations between Fusobacterium spp., enterotoxigenic Bacteroides fragilis (ETBF) and clinicopathological features of colorectal cancer. PLoS One 2015; 10:e0119462–21 [View Article]
    [Google Scholar]
  15. Tahara T, Yamamoto E, Suzuki H, Maruyama R, Chung W et al. Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Cancer Res 2014; 74:1311–1318 [View Article]
    [Google Scholar]
  16. Flanagan L, Schmid J, Ebert M, Soucek P, Kunicka T et al. Fusobacterium nucleatum associates with stages of colorectal neoplasia development, colorectal cancer and disease outcome. Eur J Clin Microbiol Infect Dis 2014; 33:1381–1390 [View Article]
    [Google Scholar]
  17. Geng J, Fan H, Tang X, Zhai H, Zhang Z. Diversified pattern of the human colorectal cancer microbiome. Pathogens 2013; 5:1–5
    [Google Scholar]
  18. Warren RL, Freeman DJ, Pleasance S, Watson P, Moore RA et al. Co-Occurrence of anaerobic bacteria in colorectal carcinomas. Microbiome 2013; 1:16 [View Article]
    [Google Scholar]
  19. McCoy AN, Araújo-Pérez F, Azcárate-Peril A, Yeh JJ, Sandler RS et al. Fusobacterium is associated with colorectal adenomas. PLoS One 2013; 8:e53653–53658 [View Article]
    [Google Scholar]
  20. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 2013; 14:207–215 [View Article]
    [Google Scholar]
  21. Eklöf V, Löfgren-Burström A, Zingmark C, Edin S, Larsson P et al. Cancer-Associated fecal microbial markers in colorectal cancer detection. Int J Cancer 2017; 141:2528–2536 [View Article]
    [Google Scholar]
  22. Allali I, Boukhatem N, Bouguenouch L, Hardi H, Boudouaya HA et al. Gut microbiome of Moroccan colorectal cancer patients. Med Microbiol Immunol 2018; 207:211–225 [View Article]
    [Google Scholar]
  23. Hale VL, Chen J, Johnson S, Harrington SC, Yab TC et al. Shifts in the fecal microbiota associated with adenomatous polyps. Cancer Epidemiol Biomarkers Prev 2017; 26:85–94 [View Article]
    [Google Scholar]
  24. Liang Q, Chiu J, Chen Y, Huang Y, Higashimori A et al. Fecal bacteria act as novel biomarkers for noninvasive diagnosis of colorectal cancer. Clin Cancer Res 2017; 23:2061–2070 [View Article]
    [Google Scholar]
  25. Sinha R, Ahn J, Sampson JN, Shi J, Yu G et al. Fecal microbiota, fecal metabolome, and colorectal cancer interrelations. PLoS One 2016; 11:e0152126–13 [View Article]
    [Google Scholar]
  26. Fukugaiti MH, Ignacio A, Fernandes MR, Ribeiro Júnior U, Nakano V et al. High occurrence of Fusobacterium nucleatum and Clostridium difficile in the intestinal microbiota of colorectal carcinoma patients. Braz J Microbiol 2015; 46:1135–1140 [View Article]
    [Google Scholar]
  27. Feng Q, Liang S, Jia H, Stadlmayr A, Tang L et al. Gut microbiome development along the colorectal adenoma–carcinoma sequence. Nat Commun 2015; 6:1–13 [View Article]
    [Google Scholar]
  28. Mira-Pascual L, Cabrera-Rubio R, Ocon S, Costales P, Parra A et al. Microbial mucosal colonic shifts associated with the development of colorectal cancer reveal the presence of different bacterial and archaeal biomarkers. J Gastroenterol 2015; 50:167–179 [View Article]
    [Google Scholar]
  29. Goedert JJ, Gong Y, Hua X, Zhong H, He Y et al. Fecal microbiota characteristics of patients with colorectal adenoma detected by screening: a population-based study. EBioMedicine 2015; 2:597–603 [View Article]
    [Google Scholar]
  30. Zackular JP, Rogers MAM, Ruffin IV MT, Schloss PD. The human gut microbiome as a screening tool for colorectal cancer. Cancer Prev Res 20141–11
    [Google Scholar]
  31. Ahn J, Sinha R, Pei Z, Dominianni C, Wu J et al. Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst 2013; 105:1907–1911 [View Article]
    [Google Scholar]
  32. Brim H, Yooseph S, Zoetendal EG, Lee E, Torralbo M et al. Microbiome analysis of stool samples from African Americans with colon polyps. PLoS One 2013; 8:e81352–10 [View Article]
    [Google Scholar]
  33. Weir TL, Manter DK, Sheflin AM, Barnett BA, Heuberger AL et al. Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS One 2013; 8:e70803–70810 [View Article]
    [Google Scholar]
  34. Chen H-M, Yu Y-N, Wang J-L, Lin Y-W, Kong X et al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am J Clin Nutr 2013; 97:1044–1052 [View Article]
    [Google Scholar]
  35. Wu N, Yang X, Zhang R, Li J, Xiao X et al. Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol 2013; 66:462–470 [View Article]
    [Google Scholar]
  36. Hibberd AA, Lyra A, Ouwehand AC, Rolny P, Lindegren H et al. Intestinal microbiota is altered in patients with colon cancer and modified by probiotic intervention. BMJ Open Gastroenterol 2017; 4:e000145–12 [View Article]
    [Google Scholar]
  37. Xu K, Jiang B. Analysis of mucosa-associated microbiota in colorectal cancer. Med Sci Monit 2017; 23:4422–4430 [View Article]
    [Google Scholar]
  38. Yazici C, Wolf PG, Kim H, Cross T-WL, Vermillion K et al. Race-dependent association of sulfidogenic bacteria with colorectal cancer. Gut 2017; 66:1983–1994 [View Article]
    [Google Scholar]
  39. Geng J, Song Q, Tang X, Liang X, Fan H et al. Co-Occurrence of driver and passenger bacteria in human colorectal cancer. Gut Pathog 2014; 6:26–5 [View Article]
    [Google Scholar]
  40. Wei Z, Cao S, Liu S, Yao Z, Sun T et al. Could gut microbiota serve as prognostic biomarker associated with colorectal cancer patients' survival? A pilot study on relevant mechanism. Oncotarget 2016; 7:1–15 [View Article]
    [Google Scholar]
  41. Kohoutova D, Smajs D, Moravkova P, Cyrany J, Moravkova M et al. Escherichia coli strains of phylogenetic group B2 and D and bacteriocin production are associated with advanced colorectal neoplasia. BMC Infect Dis 2014; 13:1–8
    [Google Scholar]
  42. Buc E, Dubois D, Sauvanet P, Raisch J, Delmas J et al. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One 2013; 8:e56964–10 [View Article]
    [Google Scholar]
  43. Nugent JL, McCoy AN, Addamo CJ, Jia W, Sandler RS et al. Altered tissue metabolites correlate with microbial dysbiosis in colorectal adenomas. J Proteome Res 2014; 13:1921–1929 [View Article]
    [Google Scholar]
  44. Bonnet M, Buc E, Sauvanet P, Darcha C, Dubois D et al. Colonization of the human gut by E. coli and colorectal cancer risk. Clin Cancer Res 2014; 20:859–867 [View Article]
    [Google Scholar]
  45. Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012; 338:120–123 [View Article]
    [Google Scholar]
  46. Arthur JC, Gharaibeh RZ, Muhlbauer M, Perez-Chanona E, Uronis JM et al. Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat Commun 2014; 4724:1–11
    [Google Scholar]
  47. Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 2012; 22:299–306 [View Article]
    [Google Scholar]
  48. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 2012; 22:292–298 [View Article]
    [Google Scholar]
  49. Rubinstein MR, Wang X, Liu W, Hao Y, Cai G et al. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe 2013; 14:195–206 [View Article]
    [Google Scholar]
  50. Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 2015; 42:344–355 [View Article]
    [Google Scholar]
  51. Amitay EL, Werner S, Vital M, Pieper DH, Höfler D et al. Fusobacterium and colorectal cancer: causal factor or passenger? Results from a large colorectal cancer screening study. Carcinogenesis 2017; 38:781–788 [View Article]
    [Google Scholar]
  52. Pasquereau-Kotula E, Martins M, Aymeric L, Dramsi S. Significance of Streptococcus gallolyticus subsp. gallolyticus association with colorectal cancer. Front Microbiol 2018; 9:1–8 [View Article]
    [Google Scholar]
  53. Sears CL, Garrett WS. Microbes, microbiota, and colon cancer. Cell Host Microbe 2014; 15:317–328 [View Article]
    [Google Scholar]
  54. Kwong TNY, Wang X, Nakatsu G, Chow TC, Tipoe T et al. Association between bacteremia from specific microbes and subsequent diagnosis of colorectal cancer. Gastroenterology 2018; 155:383–390 [View Article]
    [Google Scholar]
  55. Corredoira-Sánchez J, García-Garrote F, Rabuñal R, López-Roses L, García-País MJ et al. Association between bacteremia due to Streptococcus gallolyticus subsp. gallolyticus (Streptococcus bovis I) and colorectal neoplasia: A case-control study. Clin Infect Dis 2012; 55:491–496 [View Article]
    [Google Scholar]
  56. Boleij A, Muytjens CMJ, Bukhari SI, Cayet N, Glaser P et al. Novel clues on the specific association of Streptococcus gallolyticus subsp gallolyticus with colorectal cancer. J Infect Dis 2011; 203:1101–1109 [View Article]
    [Google Scholar]
  57. Rusniok C, Couvé E, Da Cunha V, El Gana R, Zidane N et al. Genome sequence of Streptococcus gallolyticus: insights into its adaptation to the bovine rumen and its ability to cause endocarditis. J Bacteriol 2010; 192:2266–2276 [View Article]
    [Google Scholar]
  58. Martins M, Aymeric L, du Merle L, Danne C, Robbe-Masselot C et al. Streptococcus gallolyticus Pil3 pilus is required for adhesion to colonic mucus and for colonization of mouse distal colon. J Infect Dis 2015; 212:1646–1655 [View Article]
    [Google Scholar]
  59. Martins M, Porrini C, du Merle L, Danne C, Robbe-Masselot C et al. The Pil3 pilus of Streptococcus gallolyticus binds to intestinal mucins and to fibrinogen. Gut Microbes 2016; 7:526–532 [View Article]
    [Google Scholar]
  60. Kumar R, Herold JL, Taylor J, Xu J, Xu Y. Variations among Streptococcus gallolyticus subsp. gallolyticus strains in connection with colorectal cancer. Sci Rep 2018; 8:1–10 [View Article]
    [Google Scholar]
  61. Aymeric L, Donnadieu F, Mulet C, du Merle L, Nigro G et al. Colorectal cancer specific conditions promote Streptococcus gallolyticus gut colonization. PNAS 2017; 26:283–291
    [Google Scholar]
  62. Butt J, Werner S, Willhauck-Fleckenstein M, Michel A, Waterboer T et al. Serology of Streptococcus gallolyticus subspecies gallolyticus and its association with colorectal cancer and precursors. Int J Cancer 2017; 141:897–904 [View Article]
    [Google Scholar]
  63. Boleij A, Dutilh BE, Kortman GAM, Roelofs R, Laarakkers CM et al. Bacterial responses to a simulated colon tumor microenvironment. Mol Cell Proteomics 2012; 11:851–862 [View Article]
    [Google Scholar]
  64. Abdulamir AS, Hafidh RR, Bakar FA. The association of Streptococcus bovis/gallolyticus with colorectal tumors: The nature and the underlying mechanisms of its etiological role. J Exp Clin Cancer Res 2011; 30:1–13 [View Article]
    [Google Scholar]
  65. Abdulamir AS, Hafidh RR, Mahdi LK, Al-jeboori T, Abubaker F. Investigation into the controversial association of Streptococcus gallolyticus with colorectal cancer and adenoma. BMC Cancer 2009; 9:1–12 [View Article]
    [Google Scholar]
  66. Abdulamir AS, Hafidh RR, Bakar FA. Molecular detection, quantification, and isolation of Streptococcus gallolyticus bacteria colonizing colorectal tumors: inflammation-driven potential of carcinogenesis via IL-1, COX-2, and IL-8. Mol Cancer 2010; 9:249–18 [View Article]
    [Google Scholar]
  67. Kumar R, Herold JL, Schady D, Davis J, Kopetz S et al. Streptococcus gallolyticus subsp. gallolyticus promotes colorectal tumor development. PLoS Pathog 2017; 13:e1006440–31 [View Article]
    [Google Scholar]
  68. Altonsy MO, Andrews SC, Tuohy KM. Differential induction of apoptosis in human colonic carcinoma cells (Caco-2) by Atopobium, and commensal, probiotic and enteropathogenic bacteria: mediation by the mitochondrial pathway. Int J Food Microbiol 2010; 137:190–203 [View Article]
    [Google Scholar]
  69. Ahn J, Sinha R, Pei Z, Dominianni C, Wu J et al. Human gut microbiome and risk of colorectal cancer. J Natl Cancer Inst 20131–5
    [Google Scholar]
  70. Chen W, Liu F, Ling Z, Tong X, Xiang C. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One 2012; 7:e39743–39749 [View Article]
    [Google Scholar]
  71. Newman JV, Kosaka T, Sheppard BJ, Fox JG, Schauer DB. Bacterial infection promotes colon tumorigenesis in Apc Min/+ mice. J Infect Dis 2001; 184:227–230 [View Article]
    [Google Scholar]
  72. Marchesi JR, Dutilh BE, Hall N, Peters WHM, Roelofs R et al. Towards the human colorectal cancer microbiome. PLoS One 2011; 6:e20447 [View Article]
    [Google Scholar]
  73. Zhu Q, Gao R, Wu W, Qin H. The role of gut microbiota in the pathogenesis of colorectal cancer. Tumor Biol. 2013; 34:1285–1300 [View Article]
    [Google Scholar]
  74. Wu S, Rhee K-J, Albesiano E, Rabizadeh S, Wu X 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 [View Article]
    [Google Scholar]
  75. Remacle AG, Shiryaev SA, Strongin AY. Distinct interactions with cellular E-cadherin of the two virulent metalloproteinases encoded by a Bacteroides fragilis pathogenicity island. PLoS One 2014; 9:e113896–113897 [View Article]
    [Google Scholar]
  76. Housseau F, Sears CL. Enterotoxigenic Bacteroides fragilis (ETBF)-mediated colitis in Min (Apc+/-) mice: a human commensal-based murine model of colon carcinogenesis. Cell Cycle 2010; 9:3–5 [View Article]
    [Google Scholar]
  77. Wick EC, Rabizadeh S, Albesiano E, Wu X, Wu S et al. Stat3 activation in murine colitis induced by enterotoxigenic Bacteroides fragilis . Inflamm Bowel Dis 2014; 20:821–834 [View Article]
    [Google Scholar]
  78. Housseau F, Wu S, Wick EC, Fan H, Wu X et al. Redundant innate and adaptive sources of IL-17 production drive colon tumorigenesis. Cancer Res 2016; 76:2115–2124 [View Article]
    [Google Scholar]
  79. Hovhannisyan Z, Treatman J, Littman DR, Mayer L. Characterization of IL-17-producing regulatory T cells in inflamed intestinal mucosa from patients with inflammatory bowel diseases. Gastroenterology 2011; 140:957–965 [View Article]
    [Google Scholar]
  80. Miyara M, Yoshioka Y, Kitoh A, Shima T, Wing K et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FOXP3 transcription factor. Immunity 2009; 30:899–911 [View Article]
    [Google Scholar]
  81. Omenetti S, Pizarro TT. The Treg/Th17 axis: a dynamic balance regulated by the gut microbiome. Front Immunol 2015; 6:1–8 [View Article]
    [Google Scholar]
  82. Chung L, Thiele Orberg E, Geis AL, Chan JL, Fu K et al. Bacteroides fragilis toxin coordinates a pro-carcinogenic inflammatory cascade via targeting of colonic epithelial cells. Cell Host Microbe 2018; 23:203–214 [View Article]
    [Google Scholar]
  83. Thiele Orberg E, Fan H, Tam AJ, Dejea CM, Destefano Shields CE et al. The myeloid immune signature of enterotoxigenic Bacteroides fragilis-induced murine colon tumorigenesis. Mucosal Immunol 2017; 10:421–433 [View Article]
    [Google Scholar]
  84. Song X, Gao H, Lin Y, Yao Y, Zhu S et al. Alterations in the microbiota drive interleukin-17C production from intestinal epithelial cells to promote tumorigenesis. Immunity 2014; 40:140–152 [View Article]
    [Google Scholar]
  85. Goodwin AC, Destefano Shields CE, Wu S, Huso DL, Wu X et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA 2011; 108:15354–15359 [View Article]
    [Google Scholar]
  86. Faïs T, Delmas J, Barnich N, Bonnet R, Dalmasso G. Colibactin: more than a new bacterial toxin. Toxins 2018; 10:151–16 [View Article]
    [Google Scholar]
  87. Wassenaar TM. E. coli and colorectal cancer: a complex relationship that deserves a critical mindset. Crit Rev Microbiol 2018; 44:619–632 [View Article]
    [Google Scholar]
  88. Bossuet-Greif N, Vignard J, Taieb F, Mirey G, Dubois D et al. The colibactin genotoxin generates DNA interstrand crosslinks in infected cells. American Society for Microbiology 2018; 9:
    [Google Scholar]
  89. Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E et al. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci U S A 2010; 107:11537–11542 [View Article]
    [Google Scholar]
  90. Gagnière J, Bonnin V, Jarrousse A-S, Cardamone E, Agus A et al. Interactions between microsatellite instability and human gut colonization by Escherichia coli in colorectal cancer. Clin Sci 2017; 131:471–485 [View Article]
    [Google Scholar]
  91. Secher T, Samba-Louaka A, Oswald E, Nougayrède J-P. Escherichia coli producing colibactin triggers premature and transmissible senescence in mammalian cells. PLoS One 2013; 8:e77157–17 [View Article]
    [Google Scholar]
  92. Dalmasso G, Cougnoux A, Delmas J, Darfeuille-Michaud A, Bonnet R. The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment. Gut Microbes 2014; 5:675–680 [View Article]
    [Google Scholar]
  93. Allen-Vercoe E, Jobin C, Fusobacterium JC. Fusobacterium and Enterobacteriaceae: important players for CRC?. Immunol Lett 2014; 162:54–61 [View Article]
    [Google Scholar]
  94. McIntosh FM, Maison N, Holtrop G, Young P, Stevens VJ et al. Phylogenetic distribution of genes encoding β-glucuronidase activity in human colonic bacteria and the impact of diet on faecal glycosidase activities. Environ Microbiol 2012; 14:1876–1887 [View Article]
    [Google Scholar]
  95. Kim DH, Jin YH. Intestinal bacterial beta-glucuronidase activity of patients with colon cancer. Arch Pharm Res 2001; 24:564–567 [View Article]
    [Google Scholar]
  96. Dabek M, McCrae SI, Stevens VJ, Duncan SH, Louis P. Distribution of beta-glucosidase and beta-glucuronidase activity and of beta-glucuronidase gene Gus in human colonic bacteria. FEMS Microbiol Ecol 2008; 66:487–495 [View Article]
    [Google Scholar]
  97. Michlmayr H, Kneifel W. β-Glucosidase activities of lactic acid bacteria: mechanisms, impact on fermented food and human health. FEMS Microbiol Lett 2014; 352:1–10 [View Article]
    [Google Scholar]
  98. Pollet RM, D'Agostino EH, Walton WG, Xu Y, Little MS et al. An atlas of β-glucuronidases in the human intestinal microbiome. Structure 2017; 25:967–977 [View Article]
    [Google Scholar]
  99. Azcárate-Peril MA, Sikes M, Bruno-Bárcena JM. The intestinal microbiota, gastrointestinal environment and colorectal cancer: a putative role for probiotics in prevention of colorectal cancer?. Am J Physiol Gastrointest Liver Physiol 2011; 301:G401–G424 [View Article]
    [Google Scholar]
  100. Guillén H, Curiel JA, Landete JM, Muñoz R, Herraiz T. Characterization of a nitroreductase with selective nitroreduction properties in the food and intestinal lactic acid bacterium Lactobacillus plantarum WCFS1. J Agric Food Chem 2009; 57:10457–10465 [View Article]
    [Google Scholar]
  101. Golka K, Kopps S, Myslak ZW. Carcinogenicity of azo colorants: influence of solubility and bioavailability. Toxicol Lett 2004; 151:203–210 [View Article]
    [Google Scholar]
  102. Feng J, Cerniglia CE, Chen H. Toxicological significance of azo dye metabolism by human intestinal microbiota. Front Biosci 2018; 4:568–586
    [Google Scholar]
  103. Bernstein H, Bernstein C, Payne CM, Dvorakova K, Garewal H. Bile acids as carcinogens in human gastrointestinal cancers. Mutat Res 2005; 589:47–65 [View Article]
    [Google Scholar]
  104. Ridlon JM, Kang D-J, Hylemon PB. Bile salt biotransformations by human intestinal bacteria. J Lipid Res 2006; 47:241–259 [View Article]
    [Google Scholar]
  105. Boleij A, Tjalsma H. Gut bacteria in health and disease: a survey on the interface between intestinal microbiology and colorectal cancer. Biol Rev Camb Philos Soc 2012; 87:701–730 [View Article]
    [Google Scholar]
  106. Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 20141–12
    [Google Scholar]
  107. de Almeida CV, Taddei A, Amedei A. The controversial role of Enterococcus faecalis in colorectal cancer. Therap Adv Gastroenterol 2018; 11:175628481878360–11 [View Article]
    [Google Scholar]
  108. Ratajczak W, Rył A, Mizerski A, Walczakiewicz K, Sipak O et al. Immunomodulatory potential of gut microbiome-derived short-chain fatty acids (SCFAs). Acta Biochim Pol 2019; 66:1–12 [View Article]
    [Google Scholar]
  109. Guilloteau P, Martin L, Eeckhaut V, Ducatelle R, Zabielski R et al. From the gut to the peripheral tissues: the multiple effects of butyrate. Nutr Res Rev 2010; 23:366–384 [View Article]
    [Google Scholar]
  110. Corrêa RO, Fachi JL, Vieira A, Sato FT, Vinolo MAR. Regulation of immune cell function by short-chain fatty acids. Clin Transl Immunology 2016; 5:1–8
    [Google Scholar]
  111. Lin MY, de Zoete MR, van Putten JPM, Strijbis K. Redirection of epithelial immune responses by short-chain fatty acids through inhibition of histone deacetylases. Front Immunol 2015; 6:1–11 [View Article]
    [Google Scholar]
  112. Elce A, Amato F, Zarrilli F, Calignano A, Troncone R et al. Butyrate modulating effects on pro-inflammatory pathways in human intestinal epithelial cells. Benef Microbes 20171–8
    [Google Scholar]
  113. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ et al. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 2008; 27:104–119 [View Article]
    [Google Scholar]
  114. Dos Reis SA, da Conceição LL, Siqueira NP, Rosa DD, da Silva LL et al. Review of the mechanisms of probiotic actions in the prevention of colorectal cancer. Nutr Res 2017; 37:1–19 [View Article]
    [Google Scholar]
  115. FAO. Food and Agriculture Organization of the United Nations Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria; 2001
  116. Ohigashi S, Sudo K, Kobayashi D, Takahashi O, Takahashi T et al. Changes of the intestinal microbiota, short chain fatty acids, and fecal pH in patients with colorectal cancer. Dig Dis Sci 2013; 58:1717–1726 [View Article]
    [Google Scholar]
  117. Shen XJ, Rawls JF, Randall T, Burcal L, Mpande CN et al. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes 2010; 1:138–147 [View Article]
    [Google Scholar]
  118. Sanapareddy N, Legge RM, Jovov B, McCoy A, Burcal L et al. Increased rectal microbial richness is associated with the presence of colorectal adenomas in humans. Isme J 2012; 6:1858–1868 [View Article]
    [Google Scholar]
  119. Zmora N, Suez J, Elinav E. You are what you eat: diet, health and the gut microbiota. Nat Rev Gastroenterol Hepatol 2019; 16:35–56 [View Article]
    [Google Scholar]
  120. Wu Y, Wan J, Choe U, Pham Q, Schoene NW et al. Interactions between food and gut microbiota: impact on human health. Annu Rev Food Sci Technol 2019; 10:389–408 [View Article]
    [Google Scholar]
  121. Sommer F, Bäckhed F. The gut microbiota--masters of host development and physiology. Nat Rev Microbiol 2013; 11:227–238 [View Article]
    [Google Scholar]
  122. Zur Hausen H, Hausen HZ. The search for infectious causes of human cancers: where and why. Virology 2009; 392:1–10 [View Article]
    [Google Scholar]
  123. de Martel C, Franceschi S. Infections and cancer: established associations and new hypotheses. Crit Rev Oncol Hematol 2009;70:183-194. 102. Luan C, Xie L, Yang X, Miao H, Lv N, et al. Dysbiosis of fungal microbiota in the intestinal mucosa of patients with colorectal adenomas. SciRep 20151–9
    [Google Scholar]
  124. Ramos A, Hemann MT. Drugs, bugs, and cancer: Fusobacterium nucleatum promotes chemoresistance in colorectal cancer. Cell 2017; 170:411–413 [View Article]
    [Google Scholar]
  125. Zhou Y, He H, Xu H, Li Y, Li Z et al. Association of oncogenic bacteria with colorectal cancer in South China. Oncotarget 2016; 7:80794–80802 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001049
Loading
/content/journal/jmm/10.1099/jmm.0.001049
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error