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Published in:

01-06-2013 | Review

The role of gut microbiota in the pathogenesis of colorectal cancer

Authors: Qingchao Zhu, Renyuan Gao, Wen Wu, Huanlong Qin

Published in: Tumor Biology | Issue 3/2013

Abstract

The human gastrointestinal tract harbors a complex and abundant microbial community that can reach levels as high as 10¹³–10¹⁴ microorganisms in the colon. These microorganisms are essential to a host’s well-being in terms of nutrition and mucosa immunity. However, numerous studies have also implicated members of the colonic microbiota in the development of colorectal cancer (CRC). While CRC involves a genetic component where damaged DNA and genetic instability initiates a malignant transformation, environmental factors can also contribute to the onset of CRC. Furthermore, considering the constant exposure of the colonic mucosa to the microbiome and/or its metabolites, the mucosa has long been proposed to contribute to colon tumorigenesis. However, the mechanistic details of these associations remain unknown. Fortunately, due to technical and conceptual advances, progress in characterizing the taxonomic composition, metabolic capacity, and immunomodulatory activity of human gut microbiota have been made, thereby elucidating its role in human health and disease. Furthermore, the use of experimental animal models and clinical/epidemiological studies of environmental etiological factors has identified a correlation between gut microbiota composition and gastrointestinal cancers. Bacteria continuously stimulate activated immunity in the gut mucosa and also contribute to the metabolism of bile and food components. However, the highest levels of carcinogen production are also associated with gut anaerobic bacteria and can be lowered with live lactobacilli supplements. In this review, evidence regarding the relationship between microbiota and the development of CRC will be discussed, as well as the role for microbial manipulation in affecting disease development.

Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 2012;22(2):292–8.PubMedCrossRef

Zur Hausen H. The search for infectious causes of human cancers: where and why. Virology. 2009;392(1):1–10.PubMedCrossRef

Warren JR. Helicobacter: the ease and difficulty of a new discovery. Chem Med Chem. 2006;1(7):672–85.PubMed

Rowland IR. The role of the gastrointestinal microbiota in colorectal cancer. Curr Pharm Des. 2009;15(13):1524–7.PubMedCrossRef

Proctor LM. The Human Microbiome Project in 2011 and beyond. Cell Host Microbe. 2011;10(4):287–91.PubMedCrossRef

Greer JB, O'Keefe SJ. Microbial induction of immunity, inflammation, and cancer. Front Physiol. 2011;1:168.PubMedCrossRef

Zhu Y, Michelle Luo T, Jobin C, Young HA. Gut microbiota and probiotics in colon tumorigenesis. Cancer Lett. 2011;309(2):119–27.PubMedCrossRef

Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65.PubMedCrossRef

Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol. 1977;31:107–33.PubMedCrossRef

10.

Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD, et al. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol. 1999;65(11):4799–807.PubMed

11.

Neish AS. Microbes in gastrointestinal health and disease. Gastroenterology. 2009;136(1):65–80.PubMedCrossRef

12.

Hakansson A, Molin G. Gut microbiota and inflammation. Nutrients. 2011;3(6):637–82.PubMedCrossRef

13.

Dethlefsen L, Eckburg PB, Bik EM, Relman DA. Assembly of the human intestinal microbiota. Trends Ecol Evol. 2006;21(9):517–23.PubMedCrossRef

14.

Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci USA. 2011;108 Suppl 1:4586–91.PubMedCrossRef

15.

Marchesi JR. Human distal gut microbiome. Environ Microbiol. 2011;13(12):3088–102.PubMedCrossRef

16.

Goncharova GI, Dorofeĭchuk VG, Smolianskaia AZ, Sokolova KIA. Microbial ecology of the intestines in health and in pathology. Antibiot Khimioter. 1989;34(6):462–6.PubMed

17.

Stanghellini V, Barbara G, Cremon C, Cogliandro R, Antonucci A, Gabusi V, et al. Gut microbiota and related diseases: clinical features. Intern Emerg Med. 2010;5 Suppl 1:S57–63.PubMedCrossRef

18.

Tlaskalová-Hogenová H, Stepánková R, Hudcovic T, Tucková L, Cukrowska B, Lodinová-Zádníková R, et al. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett. 2004;93(2–3):97–108.PubMedCrossRef

19.

Rastall RA. Bacteria in the gut: friends and foes and how to alter the balance. J Nutr. 2004;134(8 Suppl):2022S–6S.PubMed

20.

Mai V. Dietary modification of the intestinal microbiota. Nutr Rev. 2004;62(6 Pt 1):235–42.PubMedCrossRef

21.

Peek Jr RM, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer. 2002;2(1):28–37.PubMedCrossRef

22.

Gold JS, Bayar S, Salem RR. Association of Streptococcus bovis bacteremia with colonic neoplasia and extracolonic malignancy. Arch Surg. 2004;139(7):760–5.PubMedCrossRef

23.

Moore WE, Moore LH. Intestinal floras of populations that have a high risk of colon cancer. Appl Environ Microbiol. 1995;61(9):3202–7.PubMed

24.

Nakamura J, Kubota Y, Miyaoka M, Saitoh T, Mizuno F, Benno Y. Comparison of four microbial enzymes in Clostridia and Bacteroides isolated from human feces. Microbiol Immunol. 2002;46(7):487–90.PubMed

25.

McIntosh GH, Royle PJ, Playne MJ. A probiotic strain of L. acidophilus reduces DMH-induced large intestinal tumors in male Sprague-Dawley rats. Nutr Cancer. 1999;35(2):153–9.PubMedCrossRef

26.

Rowland IR, Bearne CA, Fischer R, Pool-Zobel BL. The effect of lactulose on DNA damage induced by DMH in the colon of human flora-associated rats. Nutr Cancer. 1996;26(1):37–47.PubMedCrossRef

27.

Swidsinski A, Khilkin M, Kerjaschki D, Schreiber S, Ortner M, Weber J, et al. Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology. 1998;115(2):281–6.PubMedCrossRef

28.

de Martel C, Franceschi S. Infections and cancer: established associations and new hypotheses. Crit Rev Oncol Hematol. 2009;70(3):183–94.PubMedCrossRef

29.

Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrède JP. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA. 2010;107(25):11537–42.PubMedCrossRef

30.

Ellmerich S, Djouder N, Schöller M, Klein JP. Production of cytokines by monocytes, epithelial and endothelial cells activated by Streptococcus bovis. Cytokine. 2000;12(1):26–31.PubMedCrossRef

31.

Marchesi JR, Dutilh BE, Hall N, Peters WH, Roelofs R, Boleij A, et al. Towards the human colorectal cancer microbiome. PLoS One. 2011;6(5):e20447.PubMedCrossRef

32.

Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012;22(2):299–306.PubMedCrossRef

33.

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(6):e39743.PubMedCrossRef

34.

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(8):575–82.PubMedCrossRef

35.

Gueimonde M, Ouwehand A, Huhtinen H, Salminen E, Salminen S. Qualitative and quantitative analyses of the bifidobacterial microbiota in the colonic mucosa of patients with colorectal cancer, diverticulitis and inflammatory bowel disease. World J Gastroenterol. 2007;13(29):3985–9.PubMed

36.

Shen XJ, Rawls JF, Randall T, Burcal L, Mpande CN, Jenkins N, et al. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes. 2010;1(3):138–47.PubMedCrossRef

37.

Sobhani I, Tap J, Roudot-Thoraval F, Roperch JP, Letulle S, Langella P, et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One. 2011;6(1):e16393.PubMedCrossRef

38.

Cummings JH, Macfarlane GT. The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol. 1991;70(6):443–59.PubMedCrossRef

39.

Hope ME, Hold GL, Kain R, El-Omar EM. Sporadic colorectal cancer—role of the commensal microbiota. FEMS Microbiol Lett. 2005;244(1):1–7.PubMedCrossRef

40.

Reddy BS, Mastromarino A, Wynder EL. Further leads on metabolic epidemiology of large bowel cancer. Cancer Res. 1975;35(11 Pt. 2):3403–6.PubMed

41.

Marteau PR, de Vrese M, Cellier CJ, Schrezenmeir J. Protection from gastrointestinal diseases with the use of probiotics. Am J Clin Nutr. 2001;73(2 Suppl):430S–6S.PubMed

42.

Balish E, Warner T. Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol. 2002;160(6):2253–7.PubMedCrossRef

43.

Kado S, Uchida K, Funabashi H, Iwata S, Nagata Y, Ando M, 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(6):2395–8.PubMed

44.

Takaku K, Oshima M, Miyoshi H, Matsui M, Seldin MF, Taketo MM. Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell. 1998;92(5):645–56.PubMedCrossRef

45.

Engle SJ, Ormsby I, Pawlowski S, Boivin GP, Croft J, Balish E, et al. Elimination of colon cancer in germ-free transforming growth factor beta 1-deficient mice. Cancer Res. 2002;62(22):6362–6.PubMed

46.

Erdman SE, Poutahidis T, Tomczak M, Rogers AB, Cormier K, Plank B, et al. CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol. 2003;162(2):691–702.PubMedCrossRef

47.

Owen RW. Faecal steroids and colorectal carcinogenesis. Scand J Gastroenterol Suppl. 1997;222:76–82.PubMed

48.

Rubin DC, Shaker A, Levin MS. Chronic intestinal inflammation: inflammatory bowel disease and colitis-associated colon cancer. Front Immunol. 2012;3:107.PubMedCrossRef

49.

Moossavi S, Bishehsari F. Inflammation in sporadic colorectal cancer. Arch Iran Med. 2012;15(3):166–70.PubMed

50.

Virchow R. Cellular pathology. As based upon physiological and pathological histology. Lecture XVI—atheromatous affection of arteries. 1858. Nutr Rev. 1989;47(1):23–5.PubMedCrossRef

51.

Compare D, Nardone G. Contribution of gut microbiota to colonic and extracolonic cancer development. Dig Dis. 2011;29(6):554–61.PubMedCrossRef

52.

Terzić J, Grivennikov S, Karin E, Karin M. Inflammation and colon cancer. Gastroenterology. 2010;138(6):2101.e5–14.e5.CrossRef

53.

Uronis JM, Mühlbauer M, Herfarth HH, Rubinas TC, Jones GS, Jobin C. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS One. 2009;4(6):e6026.PubMedCrossRef

54.

Fasano A. Cellular microbiology: can we learn cell physiology from microorganisms? Am J Physiol. 1999;276(4 Pt 1):C765–76.PubMed

55.

Rhee KJ, Wu S, Wu X, Huso DL, Karim B, Franco AA, et al. Induction of persistent colitis by a human commensal, enterotoxigenic Bacteroides fragilis, in wild-type C57BL/6 mice. Infect Immun. 2009;77(4):1708–18.PubMedCrossRef

56.

Wu S, Morin PJ, Maouyo D, Sears CL. Bacteroides fragilis enterotoxin induces c-Myc expression and cellular proliferation. Gastroenterology. 2003;124(2):392–400.PubMedCrossRef

57.

Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, Yen HR, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med. 2009;15(9):1016–22.PubMedCrossRef

58.

DuPont AW, DuPont HL. The intestinal microbiota and chronic disorders of the gut. Nat Rev Gastroenterol Hepatol. 2011;8(9):523–31.PubMedCrossRef

59.

Chen GY, Shaw MH, Redondo G, Núñez G. The innate immune receptor Nod1 protects the intestine from inflammation-induced tumorigenesis. Cancer Res. 2008;68(24):10060–7.PubMedCrossRef

60.

Zhang G, Ghosh S. Toll-like receptor-mediated NF-kappaB activation: a phylogenetically conserved paradigm in innate immunity. J Clin Invest. 2001;107(1):13–9.PubMedCrossRef

61.

Wald D, Qin J, Zhao Z, Qian Y, Naramura M, Tian L, et al. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol. 2003;4(9):920–7.PubMedCrossRef

62.

Xiao H, Gulen MF, Qin J, Yao J, Bulek K, Kish D, et al. The Toll-interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis. Immunity. 2007;26(4):461–75.PubMedCrossRef

63.

Kadota C, Ishihara S, Aziz MM, Rumi MA, Oshima N, Mishima Y, et al. Down-regulation of single immunoglobulin interleukin-1R-related molecule (SIGIRR)/TIR8 expression in intestinal epithelial cells during inflammation. Clin Exp Immunol. 2010;162(2):348–61.PubMedCrossRef

64.

Gong J, Wei T, Stark RW, Jamitzky F, Heckl WM, Anders HJ, et al. Inhibition of Toll-like receptors TLR4 and 7 signaling pathways by SIGIRR: a computational approach. J Struct Biol. 2010;169(3):323–30.PubMedCrossRef

65.

Salcedo R, Worschech A, Cardone M, Jones Y, Gyulai Z, Dai RM, et al. MyD88-mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18. J Exp Med. 2010;207(8):1625–36.PubMedCrossRef

66.

Fukata M, Chen A, Vamadevan AS, Cohen J, Breglio K, Krishnareddy S, et al. Toll-like receptor-4 promotes the development of colitis-associated colorectal tumors. Gastroenterology. 2007;133(6):1869–81.PubMedCrossRef

67.

Sears CL, Pardoll DM. Perspective: alpha-bugs, their microbial partners, and the link to colon cancer. J Infect Dis. 2011;203(3):306–11.PubMedCrossRef

68.

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(3):701–30.PubMedCrossRef

69.

Huycke MM, Abrams V, Moore DR. Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA. Carcinogenesis. 2002;23(3):529–36.PubMedCrossRef

70.

Wang X, Huycke MM. Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells. Gastroenterology. 2007;132(2):551–61.PubMedCrossRef

71.

Wang X, Allen TD, May RJ, Lightfoot S, Houchen CW, Huycke MM. Enterococcus faecalis induces aneuploidy and tetraploidy in colonic epithelial cells through a bystander effect. Cancer Res. 2008;68(23):9909–17.PubMedCrossRef

72.

Nougayrède JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 2006;313(5788):848–51.PubMedCrossRef

73.

Wu S, Shin J, Zhang G, Cohen M, Franco A, Sears CL. The Bacteroides fragilis toxin binds to a specific intestinal epithelial cell receptor. Infect Immun. 2006;74(9):5382–90.PubMedCrossRef

74.

Toprak NU, Yagci A, Gulluoglu BM, Akin ML, Demirkalem P, Celenk T, et al. A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clin Microbiol Infect. 2006;12(8):782–6.PubMed

75.

Goodwin AC, Destefano Shields CE, Wu S, Huso DL, Wu X, Murray-Stewart TR, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA. 2011;108(37):15354–9.PubMedCrossRef

76.

Wu S, Rhee KJ, Zhang M, Franco A, Sears CL. Bacteroides fragilis toxin stimulates intestinal epithelial cell shedding and gamma-secretase-dependent E-cadherin cleavage. J Cell Sci. 2007;120(Pt 11):1944–52.PubMedCrossRef

77.

McCart AE, Vickaryous NK, Silver A. Apc mice: models, modifiers and mutants. Pathol Res Pract. 2008;204(7):479–90.PubMedCrossRef

78.

Näthke IS. The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu Rev Cell Dev Biol. 2004;20:337–66.PubMedCrossRef

79.

Wang L, Yi T, Kortylewski M, Pardoll DM, Zeng D, Yu H. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J Exp Med. 2009;206(7):1457–64.PubMedCrossRef

80.

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(1):3–5.PubMedCrossRef

81.

Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, Elson CO, et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature. 2006;441(7090):231–4.PubMedCrossRef

82.

DuPont HL. Clinical practice. Bacterial diarrhea. N Engl J Med. 2009;361(16):1560–9.PubMedCrossRef

83.

Karin M. Nuclear factor-kappaB in cancer development and progression. Nature. 2006;441(7092):431–6.PubMedCrossRef

84.

Yu H, Kortylewski M, Pardoll D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol. 2007;7(1):41–51.PubMedCrossRef

85.

Cole CB, Fuller R, Mallet AK, Rowland IR. The influence of the host on expression of intestinal microbial enzyme activities involved in metabolism of foreign compounds. J Appl Bacteriol. 1985;59(6):549–53.PubMedCrossRef

86.

Steer TE, Johnson IT, Gee JM, Gibson GR. Metabolism of the soybean isoflavone glycoside genistin in vitro by human gut bacteria and the effect of prebiotics. Br J Nutr. 2003;90(3):635–42.PubMedCrossRef

87.

Takada H, Hirooka T, Hiramatsu Y, Yamamoto M. Effect of beta-glucuronidase inhibitor on azoxymethane-induced colonic carcinogenesis in rats. Cancer Res. 1982;42(1):331–34.PubMed

88.

Kim DH, Jin YH. Intestinal bacterial beta-glucuronidase activity of patients with colon cancer. Arch Pharm Res. 2001;24(6):564–7.PubMedCrossRef

89.

Rowland IR, Tanaka R. The effects of transgalactosylated oligosaccharides on gut flora metabolism in rats associated with a human faecal microflora. J Appl Bacteriol. 1993;74(6):667–74.PubMedCrossRef

90.

Davis CD, Milner JA. Gastrointestinal microflora, food components and colon cancer prevention. J Nutr Biochem. 2009;20(10):743–52.PubMedCrossRef

91.

Gill CI, Rowland IR. Diet and cancer: assessing the risk. Br J Nutr. 2002;88 Suppl 1:S73–87.PubMedCrossRef

92.

Reddy BS, Mangat S, Weisburger JH, Wynder EL. Effect of high-risk diets for colon carcinogenesis on intestinal mucosal and bacterial beta-glucuronidase activity in F344 rats. Cancer Res. 1977;37(10):3533–6.PubMed

93.

Mazière S, Meflah K, Tavan E, Champ M, Narbonne JF, Cassand P. Effect of resistant starch and/or fat-soluble vitamins A and E on the initiation stage of aberrant crypts in rat colon. Nutr Cancer. 1998;31(3):168–77.PubMedCrossRef

94.

Gråsten SM, Juntunen KS, Poutanen KS, Gylling HK, Miettinen TA, Mykkänen HM. Rye bread improves bowel function and decreases the concentrations of some compounds that are putative colon cancer risk markers in middle-aged women and men. J Nutr. 2000;130(9):2215–21.PubMed

95.

Lee JW, Shin JG, Kim EH, Kang HE, Yim IB, Kim JY, et al. Immunomodulatory and antitumor effects in vivo by the cytoplasmic fraction of Lactobacillus casei and Bifidobacterium longum. J Vet Sci. 2004;5(1):41–8.PubMed

96.

de Giorgio R, Blandizzi C. Targeting enteric neuroplasticity: diet and bugs as new key factors. Gastroenterology. 2010;138(5):1663–6.PubMedCrossRef

97.

Powolny A, Xu J, Loo G. Deoxycholate induces DNA damage and apoptosis in human colon epithelial cells expressing either mutant or wild-type p53. Int J Biochem Cell Biol. 2001;33(2):193–203.PubMedCrossRef

98.

Narahara H, Tatsuta M, Iishi H, Baba M, Uedo N, Sakai N, et al. K-ras point mutation is associated with enhancement by deoxycholic acid of colon carcinogenesis induced by azoxymethane, but not with its attenuation by all-trans-retinoic acid. Int J Cancer. 2000;88(2):157–61.PubMedCrossRef

99.

Radley S, Davis AE, Imray CH, Barker G, Morton DG, Baker PR, et al. Biliary bile acid profiles in familial adenomatous polyposis. Br J Surg. 1992;79(1):89–90.PubMedCrossRef

100.

Imray CH, Radley S, Davis A, Barker G, Hendrickse CW, Donovan IA, et al. Faecal unconjugated bile acids in patients with colorectal cancer or polyps. Gut. 1992;33(9):1239–45.PubMedCrossRef

101.

de Kok TM, van Maanen JM. Evaluation of fecal mutagenicity and colorectal cancer risk. Mutat Res. 2000;463(1):53–101.PubMedCrossRef

102.

Deschner EE, Cohen BI, Raicht RF. Acute and chronic effect of dietary cholic acid on colonic epithelial cell proliferation. Digestion. 1981;21(6):290–6.PubMedCrossRef

103.

Deschner EE, Raicht RF. Influence of bile on kinetic behavior of colonic epithelial cells of the rat. Digestion. 1979;19(5):322–7.PubMedCrossRef

104.

DeRubertis FR, Craven PA, Saito R. Bile salt stimulation of colonic epithelial proliferation. Evidence for involvement of lipoxygenase products. J Clin Invest. 1984;74(5):1614–24.PubMedCrossRef

105.

Hughes R, Kurth MJ, McGilligan V, McGlynn H, Rowland I. Effect of colonic bacterial metabolites on Caco-2 cell paracellular permeability in vitro. Nutr Cancer. 2008;60(2):259–66.PubMedCrossRef

106.

Heavey PM, Rowland IR. Microbial–gut interactions in health and disease. Gastrointestinal cancer. Best Pract Res Clin Gastroenterol. 2004;18(2):323–36.PubMedCrossRef

107.

Orrhage K, Sillerström E, Gustafsson JA, Nord CE, Rafter J. Binding of mutagenic heterocyclic amines by intestinal and lactic acid bacteria. Mutat Res. 1994;311(2):239–48.PubMedCrossRef

108.

Carman RJ, Van Tassell RL, Kingston DG, Bashir M, Wilkins TD. Conversion of IQ, a dietary pyrolysis carcinogen to a direct-acting mutagen by normal intestinal bacteria of humans. Mutat Res. 1988;206(3):335–42.PubMedCrossRef

109.

Owen RW, Spiegelhalder B, Bartsch H. Generation of reactive oxygen species by the faecal matrix. Gut. 2000;46(2):225–32.PubMedCrossRef

110.

Marnett LJ. Oxyradicals and DNA damage. Carcinogenesis. 2000;21(3):361–70.PubMedCrossRef

111.

Shacter E, Weitzman SA. Chronic inflammation and cancer. Oncology (Williston Park). 2002; 16(2):217–26, 229.

112.

Hughes R, Cross AJ, Pollock JR, Bingham S. Dose-dependent effect of dietary meat on endogenous colonic N-nitrosation. Carcinogenesis. 2001;22(1):199–202.PubMedCrossRef

113.

Massey RC, Key PE, Mallett AK, Rowland IR. An investigation of the endogenous formation of apparent total N-nitroso compounds in conventional microflora and germ-free rats. Food Chem Toxicol. 1988;26(7):595–600.PubMedCrossRef

114.

Rowland IR, Granli T, Bøckman OC, Key PE, Massey RC. Endogenous N-nitrosation in man assessed by measurement of apparent total N-nitroso compounds in faeces. Carcinogenesis. 1991;12(8):1395–401.PubMedCrossRef

115.

Pala V, Sieri S, Berrino F, Vineis P, Sacerdote C, Palli D, et al. Yogurt consumption and risk of colorectal cancer in the Italian European prospective investigation into cancer and nutrition cohort. Int J Cancer. 2011;129(11):2712–9.PubMedCrossRef

116.

de Vrese M, Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol. 2008;111:1–66.PubMed

117.

Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–80.PubMedCrossRef

118.

Corthésy B, Gaskins HR, Mercenier A. Cross-talk between probiotic bacteria and the host immune system. J Nutr. 2007;137(3 Suppl 2):781S–90S.PubMed

119.

Orlando A, Messa C, Linsalata M, Cavallini A, Russo F. Effects of Lactobacillus rhamnosus GG on proliferation and polyamine metabolism in HGC-27 human gastric and DLD-1 colonic cancer cell lines. Immunopharmacol Immunotoxicol. 2009;31(1):108–16.PubMedCrossRef

120.

Lee NK, Park JS, Park E, Paik HD. Adherence and anticarcinogenic effects of Bacillus polyfermenticus SCD in the large intestine. Lett Appl Microbiol. 2007;44(3):274–8.PubMedCrossRef

121.

Kim Y, Lee D, Kim D, Cho J, Yang J, Chung M, et al. Inhibition of proliferation in colon cancer cell lines and harmful enzyme activity of colon bacteria by Bifidobacterium adolescentis SPM0212. Arch Pharm Res. 2008;31(4):468–73.PubMedCrossRef

122.

Pool-Zobel BL, Neudecker C, Domizlaff I, Ji S, Schillinger U, Rumney C, et al. Lactobacillus- and Bifidobacterium-mediated antigenotoxicity in the colon of rats. Nutr Cancer. 1996;26(3):365–80.PubMedCrossRef

123.

Le Leu RK, Brown IL, Hu Y, Bird AR, Jackson M, Esterman A, et al. A synbiotic combination of resistant starch and Bifidobacterium lactis facilitates apoptotic deletion of carcinogen-damaged cells in rat colon. J Nutr. 2005;135(5):996–1001.PubMed

124.

Tlaskalová-Hogenová H, Stěpánková R, Kozáková H, Hudcovic T, Vannucci L, Tučková L, et al. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol. 2011;8(2):110–20.PubMedCrossRef

Title: The role of gut microbiota in the pathogenesis of colorectal cancer
Authors: Qingchao Zhu
Renyuan Gao
Wen Wu
Huanlong Qin
Publication date: 01-06-2013
Publisher: Springer Netherlands
Published in: Tumor Biology / Issue 3/2013
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI: https://doi.org/10.1007/s13277-013-0684-4

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Optimization of apparent diffusion coefficient measured by diffusion-weighted MRI for diagnosis of breast lesions presenting as mass and non-mass-like enhancement

Overexpression of immunoglobulin G prompts cell proliferation and inhibits cell apoptosis in human urothelial carcinoma

Overexpression of microRNA-21 regulating PDCD4 during tumorigenesis of liver fluke-associated cholangiocarcinoma contributes to tumor growth and metastasis

Methylenetetrahydrofolate reductase gene polymorphisms association with the risk of follicular lymphoma: a meta-analysis

Keynote webinar | Spotlight on antibody–drug conjugates in cancer