Bacterial oncogenesis in the colon

Future Microbiology

Volumn 8, Issue 4, 2013, Pages 445-460

  Dejea, Christine ^a   Wick, Elizabeth ^b   Sears, Cynthia L ^a,b,c  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

bacterial toxin; chronic inflammation; colonic microbiome; colorectal cancer; genotoxins; oncogenesis

Indexed keywords

AZOXYMETHANE; BACTERIAL TOXIN; DEXTRAN SULFATE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 6; NITRIC OXIDE; RAG2 PROTEIN; REACTIVE OXYGEN METABOLITE; TOXIN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; APOPTOSIS; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTEROIDES FRAGILIS; BURKHOLDERIA PSEUDOMALLEI; CAMPYLOBACTER; CANCER GROWTH; CHROMOSOME; CHRONIC INFLAMMATION; CITROBACTER RODENTIUM; COLON CARCINOGENESIS; COLON FLORA; COLORECTAL CANCER; DISEASE ASSOCIATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; HAEMOPHILUS; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; INFLAMMATION; MICROBIOME; NONHUMAN; PHAGOCYTE; PHOTORHABDUS; PHOTORHABDUS LUMINESCENS; PRIORITY JOURNAL; REVIEW; SALMONELLA; SHIGELLA; YERSINIA PSEUDOTUBERCULOSIS;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; BACTERIAL PHYSIOLOGICAL PHENOMENA; COLON; COLORECTAL NEOPLASMS; HUMANS;

ANIMALIA; BACTERIA (MICROORGANISMS); BACTEROIDES FRAGILIS;

EID: 84875731587     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.13.17     Document Type: Review

References (132)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J. Clin. 61(2), 69-90 (2011).
2. Center MM, Jemal A, Ward E. International trends in colorectal cancer incidence rates. Cancer Epidemiol. Biomarkers Prev. 18(6), 1688-1694 (2009).
3. Center MM, Jemal A, Smith RA, Ward E. Worldwide variations in colorectal cancer. CA Cancer J. Clin. 59(6), 366-378 (2009).
4. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 61(5), 759-767 (1990).
5. Vogelstein B, Kinzler KW. The multistep nature of cancer. Trends Genet. 9(4), 138-141 (1993).
6. Eckburg PB, Bik EM, Bernstein CN et al. Diversity of the human intestinal microbial flora. Science 308(5728), 1635-1638 (2005).
7. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122(1), 107-118 (2005).
8. Reikvam DH, Erofeev A, Sandvik A et al. Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression. PLoS ONE 6(3), e17996 (2011).
9. Kleessen B, Kroesen AJ, Buhr HJ, Blaut M. Mucosal and invading bacteria in patients with inflammatory bowel disease compared with controls. Scand. J. Gastroenterol. 37(9), 1034-1041 (2002).
10. Rowland IR. The role of the gastrointestinal microbiota in colorectal cancer. Curr. Pharm. Des. 15(13), 1524-1527 (2009).
11. Sheng YH, Hasnain SZ, Florin TH, McGuckin MA. Mucins in inflammatory bowel diseases and colorectal cancer. J. Gastroenterol. Hepatol. 27(1), 28-38 (2012).
12. McGuckin MA, Linden SK, Sutton P, Florin TH. Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 9(4), 265-278 (2011).
13. Johansson ME, Larsson JM, Hansson GC. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc. Natl Acad. Sci. USA 108(Suppl. 1), 4659-4665 (2011).
14. Matsuo K, Ota H, Akamatsu T, Sugiyama A, Katsuyama T. Histochemistry of the surface mucous gel layer of the human colon. Gut 40(6), 782-789 (1997).
15. Turnbaugh PJ, Ley RE, Hamady M, Fraser- Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature 449(7164), 804-810 (2007).
16. Ahmed S, Macfarlane GT, Fite A, McBain AJ, Gilbert P, Macfarlane S. Mucosa-associated bacterial diversity in relation to human terminal ileum and colonic biopsy samples. Appl. Environ. Microbiol. 73(22), 7435-7442 (2007).
17. Shen XJ, Rawls JF, Randall T et al. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes 1(3), 138-147 (2010).
18. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl Acad. Sci. USA 104(34), 13780-13785 (2007).
19. Swidsinski A, Loening-Baucke V, Herber A. Mucosal flora in Crohn's disease and ulcerative colitis - an overview. J. Physiol. Pharmacol. 60(Suppl. 6), 61-71 (2009).
20. Tarmin L, Yin J, Harpaz N et al. Adenomatous polyposis coli gene mutations in ulcerative colitis-associated dysplasias and cancers versus sporadic colon neoplasms. Cancer Res. 55(10), 2035-2038 (1995).
21. Xie J, Itzkowitz SH. Cancer in inflammatory bowel disease. World J. Gastroenterol. 14(3), 378-389 (2008).
22. Marchesi JR, Dutilh BE, Hall N et al. Towards the human colorectal cancer microbiome. PLoS ONE 6(5), e20447 (2011).
23. Kostic AD, Gevers D, Pedamallu CS et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 22(2), 292-298 (2012).
24. Pitari GM, Zingman LV, Hodgson DM et al. Bacterial enterotoxins are associated with resistance to colon cancer. Proc. Natl Acad. Sci. USA 100(5), 2695-2699 (2003).
25. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet 357(9255), 539-545 (2001).
26. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 140(6), 883-899 (2010).
27. Coussens LM, Werb Z. Inflammation and cancer. Nature 420(6917), 860-867 (2002).
28. Karin M, Greten FR. NFkB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 5(10), 749-759 (2005).
29. Nath G, Gulati AK, Shukla VK. Role of bacteria in carcinogenesis, with special reference to carcinoma of the gallbladder. World J. Gastroenterol. 16(43), 5395-5404 (2010).
30. Goodwin AC, Destefano Shields CE, Wu S et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc. Natl Acad. Sci. USA 108(37), 15354-15359 (2011).
31. Waris G, Ahsan H. Reactive oxygen species. role in the development of cancer and various chronic conditions. J. Carcinog. 5, 14 (2006).
32. Lax AJ. Opinion. Bacterial toxins and cancer - a case to answer? Nat. Rev. Microbiol. 3(4), 343-349 (2005).
33. Huang JQ, Zheng GF, Sumanac K, Irvine EJ, Hunt RH. Meta-analysis of the relationship between cagA seropositivity and gastric cancer. Gastroenterology 125(6), 1636-1644 (2003).
34. Peek RM Jr, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2(1), 28-37 (2002).
35. Hatakeyama M, Higashi H. Helicobacter pylori CagA: a new paradigm for bacterial carcinogenesis. Cancer Sci. 96(12), 835-843 (2005).
36. Brandt S, Kwok T, Hartig R, Konig W, Backert S. NFkB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc. Natl Acad. Sci. USA 102(26), 9300-9305 (2005).
37. Lamb A, Yang XD, Tsang YH et al. Helicobacter pylori CagA activates NF-kappaB by targeting TAK1 for TRAF6-mediated Lys 63 ubiquitination. EMBO Rep. 10(11), 1242-1249 (2009).
38. Franco AT, Israel DA, Washington MK et al. Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc. Natl Acad. Sci. USA 102(30), 10646-10651 (2005).
39. Buti L, Spooner E, Van der Veen AG, Rappuoli R, Covacci A, Ploegh HL. Helicobacter pylori cytotoxin-associated gene A (CagA) subverts the apoptosis-stimulating protein of p53 (ASPP2) tumor suppressor pathway of the host. Proc. Natl Acad. Sci. USA 108(22), 9238-9243 (2011).
40. Miehlke S, Kirsch C, Agha-Amiri K et al. The Helicobacter pylori vacA s1, m1 genotype and cagA is associated with gastric carcinoma in Germany. Int. J. Cancer 87(3), 322-327 (2000).
41. Strowski MZ, Cramer T, Schafer G et al. Helicobacter pylori stimulates host vascular endothelial growth factor-A (vegf-A) gene expression via MEK/ERK-dependent activation of Sp1 and Sp3. FASEB J. 18(1), 218-220 (2004).
42. Gebert B, Fischer W, Weiss E, Hoffmann R, Haas R. Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301(5636), 1099-1102 (2003).
43. Cover TL, Krishna US, Israel DA, Peek RM Jr. Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res. 63(5), 951-957 (2003).
44. Preuss I, Hildebrand D, Orth JH, Aktories K, Kubatzky KF. Pasteurella multocida toxin is a potent activator of anti-apoptotic signalling pathways. Cell. Microbiol. 12(8), 1174-1185 (2010).
45. Orth JH, Aktories K. Molecular biology of Pasteurella multocida toxin. Curr. Top. Microbiol. Immunol. 361, 73-92 (2012).
46. Orth JH, Preuss I, Fester I, Schlosser A, Wilson BA, Aktories K. Pasteurella multocida toxin activation of heterotrimeric G proteins by deamidation. Proc. Natl Acad. Sci. USA 106(17), 7179-7184 (2009).
47. Jinadasa RN, Bloom SE, Weiss RS, Duhamel GE. Cytolethal distending toxin: a conserved bacterial genotoxin that blocks cell cycle progression, leading to apoptosis of a broad range of mammalian cell lineages. Microbiology 157(Pt 7), 1851-1875 (2011).
48. Elwell C, Chao K, Patel K, Dreyfus L. Escherichia coli CdtB mediates cytolethal distending toxin cell cycle arrest. Infect. Immun. 69(5), 3418-3422 (2001).
49. Nougayrede JP, Homburg S, Taieb F et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313(5788), 848-851 (2006).
50. Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrede JP. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc. Natl Acad. Sci. USA 107(25), 11537-11542 (2010).
51. Arthur JC, Perez-Chanona E, Muhlbauer M et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338(6103), 120-123 (2012).
52. Miraglia AG, Travaglione S, Meschini S et al. Cytotoxic necrotizing factor 1 prevents apoptosis via the Akt/IkB kinase pathway. role of nuclear factor-kappaB and Bcl-2. Mol. Biol. Cell 18(7), 2735-2744 (2007).
53. Samba-Louaka A, Nougayrede JP, Watrin C, Oswald E, Taieb F. The enteropathogenic Escherichia coli effector Cif induces delayed apoptosis in epithelial cells. Infect. Immun. 77(12), 5471-5477 (2009).
54. 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. 15(9), 1016-1022 (2009).
55. Toprak NU, Yagci A, Gulluoglu BM et al. A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clin. Microbiol. Infect. 12(8), 782-786 (2006).
56. Moore WE, Holdeman LV. Human fecal flora: the normal flora of 20 Japanese- Hawaiians. Appl. Microbiol. 27(5), 961-979 (1974).
57. Polk BF, Kasper DL. Bacteroides fragilis subspecies in clinical isolates. Ann. Intern. Med. 86(5), 569-571 (1977).
58. Rhee KJ, Wu S, Wu X et al. Induction of persistent colitis by a human commensal, enterotoxigenic Bacteroides fragilis, in wild-type C57BL/6 mice. Infect. Immun. 77(4), 1708-1718 (2009).
59. Basset C, Holton J, Bazeos A, Vaira D, Bloom S. Are Helicobacter species and enterotoxigenic Bacteroides fragilis involved in inflammatory bowel disease? Dig. Dis. Sci. 49(9), 1425-1432 (2004).
60. Prindiville TP, Sheikh RA, Cohen SH, Tang YJ, Cantrell MC, Silva J Jr. Bacteroides fragilis enterotoxin gene sequences in patients with inflammatory bowel disease. Emerg. Infect. Dis. 6(2), 171-174 (2000).
61. Sears CL. Enterotoxigenic Bacteroides fragilis: a rogue among symbiotes. Clin. Microbiol. Rev. 22(2), 349-369 (2009).
62. Zitomersky NL, Coyne MJ, Comstock LE. Longitudinal analysis of the prevalence, maintenance, and IgA response to species of the order Bacteroidales in the human gut. Infect. Immun. 79(5), 2012-2020 (2011).
63. Franco AA, Mundy LM, Trucksis M, Wu S, Kaper JB, Sears CL. Cloning and characterization of the Bacteroides fragilis metalloprotease toxin gene. Infect. Immun. 65(3), 1007-1013 (1997).
64. Franco AA. The Bacteroides fragilis pathogenicity island is contained in a putative novel conjugative transposon. J. Bacteriol. 186(18), 6077-6092 (2004).
65. Wu S, Lim KC, Huang J, Saidi RF, Sears CL. Bacteroides fragilis enterotoxin cleaves the zonula adherens protein, E-cadherin. Proc. Natl Acad. Sci. USA 95(25), 14979-14984 (1998).
66. Wu S, Morin PJ, Maouyo D, Sears CL. Bacteroides fragilis enterotoxin induces c-Myc expression and cellular proliferation. Gastroenterology 124(2), 392-400 (2003).
67. Wu S, Powell J, Mathioudakis N, Kane S, Fernandez E, Sears CL. Bacteroides fragilis enterotoxin induces intestinal epithelial cell secretion of interleukin-8 through mitogen-activated protein kinases and a tyrosine kinase-regulated nuclear factor-kappaB pathway. Infect. Immun. 72(10), 5832-5839 (2004).
68. Su LK, Kinzler KW, Vogelstein B et al. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 256(5057), 668-670 (1992).
69. Fodde R, Edelmann W, Yang K et al. A targeted chain-termination mutation in the mouse Apc gene results in multiple intestinal tumors. Proc. Natl Acad. Sci. USA 91(19), 8969-8973 (1994).
70. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487(7407), 330-337 (2012).
71. Liu J, Duan Y, Cheng X et al. IL-17 is associated with poor prognosis and promotes angiogenesis via stimulating VEGF production of cancer cells in colorectal carcinoma. Biochem. Biophys. Res. Commun. 407(2), 348-354 (2011).
72. Chae WJ, Gibson TF, Zelterman D, Hao L, Henegariu O, Bothwell AL. Ablation of IL-2011;17A abrogates progression of spontaneous intestinal tumorigenesis. Proc. Natl Acad. Sci. USA 107(12), 5540-5544 (2010).
73. Su X, Ye J, Hsueh EC, Zhang Y, Hoft DF, Peng G. Tumor microenvironments direct the recruitment and expansion of human Th17 cells. J. Immunol. 184(3), 1630-1641 (2010).
74. Sobhani I, Tap J, Roudot-Thoraval F et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS ONE 6(1), e16393 (2011).
75. Morikawa T, Baba Y, Yamauchi M et al. STAT3 expression, molecular features, inflammation patterns, and prognosis in a database of 724 colorectal cancers. Clin. Cancer Res. 17(6), 1452-1462 (2011).
76. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 247(4940), 322-324 (1990).
77. Oshima M, Oshima H, Kitagawa K, Kobayashi M, Itakura C, Taketo M. Loss of Apc heterozygosity and abnormal tissue building in nascent intestinal polyps in mice carrying a truncated Apc gene. Proc. Natl Acad. Sci. USA 92(10), 4482-4486 (1995).
78. Velcich A, Yang W, Heyer J et al. Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 295(5560), 1726-1729 (2002).
79. Berg DJ, Davidson N, Kuhn R et al. Enterocolitis and colon cancer in interleukin-2011;10-deficient mice are associated with aberrant cytokine production and CD4+ Th1-like responses. J. Clin. Invest. 98(4), 1010-1020 (1996).
80. Zhu Y, Richardson JA, Parada LF, Graff JM. Smad3 mutant mice develop metastatic colorectal cancer. Cell 94(6), 703-714 (1998).
81. Rudolph U, Finegold MJ, Rich SS et al. Ulcerative colitis and adenocarcinoma of the colon in G alpha i2-deficient mice. Nat. Genet. 10(2), 143-150 (1995).
82. 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 92(5), 645-656 (1998).
83. Funabashi H, Uchida K, Kado S, Matsuoka Y, Ohwaki M. Establishment of a Tcrb and Trp53 genes deficient mouse strain as an animal model for spontaneous colorectal cancer. Exp. Anim. 50(1), 41-47 (2001).
84. Chu FF, Esworthy RS, Chu PG et al. Bacteria-induced intestinal cancer in mice with disrupted Gpx1 and Gpx2 genes. Cancer Res. 64(3), 962-968 (2004).
85. Engle SJ, Ormsby I, Pawlowski S et al. Elimination of colon cancer in germ-free transforming growth factor b 1-deficient mice. Cancer Res. 62(22), 6362-6366 (2002).
86. Taketo MM, Edelmann W. Mouse models of colon cancer. Gastroenterology 136(3), 780-798 (2009).
87. Balish E, Warner T. Enterococcus faecalis induces inflammatory bowel disease in IL-10 knockout mice. Am. J. Pathol. 160(6), 2253-2257 (2002).
88. Dove WF, Clipson L, Gould KA et al. Intestinal neoplasia in the ApcMin mouse. independence from the microbial and natural killer (beige locus) status. Cancer Res. 57(5), 812-814 (1997).
89. Li Y, Kundu P, Seow SW et al. Gut microbiota accelerate tumor growth via c-jun and STAT3 phosphorylation in APCMin/+ mice. Carcinogenesis 33(6), 1231-1238 (2012).
90. Kado S, Uchida K, Funabashi H 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. 61(6), 2395-2398 (2001).
91. Uronis JM, Muhlbauer M, Herfarth HH, Rubinas TC, Jones GS, Jobin C. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS ONE 4(6), e6026 (2009).
92. Johansson ME, Gustafsson JK, Sjoberg KE et al. Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model. PLoS ONE 5(8), e12238 (2010).
93. Perse M, Cerar A. Dextran sodium sulphate colitis mouse model: traps and tricks. J. Biomed. Biotechnol. 2012, 718617 (2012).
94. Elinav E, Strowig T, Kau AL et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145(5), 745-757 (2011).
95. Wu GD, Chen J, Hoffmann C et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334(6052), 105-108 (2011).
96. Garrett WS, Lord GM, Punit S et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 131(1), 33-45 (2007).
97. Vijay-Kumar M, Aitken JD, Carvalho FA et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328(5975), 228-231 (2010).
98. Hans W, Scholmerich J, Gross V, Falk W. The role of the resident intestinal flora in acute and chronic dextran sulfate sodium-induced colitis in mice. Eur. J. Gastroenterol. Hepatol. 12(3), 267-273 (2000).
99. Rath HC, Schultz M, Freitag R et al. Different subsets of enteric bacteria induce and perpetuate experimental colitis in rats and mice. Infect. Immun. 69(4), 2277-2285 (2001).
100. Fukuda M, Kanauchi O, Araki Y et al. Prebiotic treatment of experimental colitis with germinated barley foodstuff: a comparison with probiotic or antibiotic treatment. Int. J. Mol. Med. 9(1), 65-70 (2002).
101. Kitajima S, Morimoto M, Sagara E, Shimizu C, Ikeda Y. Dextran sodium sulfate-induced colitis in germ-free IQI/Jic mice. Exp. Anim. 50(5), 387-395 (2001).
102. Ellmerich S, Scholler M, Duranton B et al. Promotion of intestinal carcinogenesis by Streptococcus bovis. Carcinogenesis 21(4), 753-756 (2000).
103. 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. 87(3), 701-730 (2012).
104. Fox JG, Ge Z, Whary MT, Erdman SE, Horwitz BH. Helicobacter hepaticus infection in mice: models for understanding lower bowel inflammation and cancer. Mucosal Immunol. 4(1), 22-30 (2011).
105. Erdman SE, Rao VP, Poutahidis T et al. Nitric oxide and TNF-alpha trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2- deficient mice. Proc. Natl Acad. Sci. USA 106(4), 1027-1032 (2009).
106. Mangerich A, Knutson CG, Parry NM et al. Infection-induced colitis in mice causes dynamic and tissue-specific changes in stress response and DNA damage leading to colon cancer. Proc. Natl Acad. Sci. USA 109(27), E1820-E1829 (2012).
107. Balagopal A, Philp FH, Astemborski J et al. Human immunodeficiency virus-related microbial translocation and progression of hepatitis C. Gastroenterology 135(1), 226-233 (2008).
108. Klatt NR, Funderburg NT, Brenchley JM. Microbial translocation, immune activation, and HIV disease. Trends Microbiol. 21(1), 6-13 (2013).
109. Huycke MM, Moore D, Joyce W et al. Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol. Microbiol. 42(3), 729-740 (2001).
110. 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. 68(23), 9909-9917 (2008).
111. Ruiz PA, Shkoda A, Kim SC, Sartor RB, Haller D. IL-10 gene-deficient mice lack TGF-beta/Smad signaling and fail to inhibit proinflammatory gene expression in intestinal epithelial cells after the colonization with colitogenic Enterococcus faecalis. J. Immunol. 174(5), 2990-2999 (2005).
112. Winters MD, Schlinke TL, Joyce WA, Glore SR, Huycke MM. Prospective case-cohort study of intestinal colonization with enterococci that produce extracellular superoxide and the risk for colorectal adenomas or cancer. Am. J. Gastroenterol. 93(12), 2491-2500 (1998).
113. Barthold SW, Osbaldiston GW, Jonas AM. Dietary, bacterial, and host genetic interactions in the pathogenesis of transmissible murine colonic hyperplasia. Lab. Anim. Sci. 27(6), 938-945 (1977).
114. Newman JV, Kosaka T, Sheppard BJ, Fox JG, Schauer DB. Bacterial infection promotes colon tumorigenesis in ApcMin/+ mice. J. Infect. Dis. 184(2), 227-230 (2001).
115. Maddocks OD, Short AJ, Donnenberg MS, Bader S, Harrison DJ. Attaching and effacing Escherichia coli downregulate DNA mismatch repair protein in vitro and are associated with colorectal adenocarcinomas in humans. PLoS ONE 4(5), e5517 (2009).
116. Keusch GT. Opportunistic infections in colon carcinoma. Am. J. Clin. Nutr. 27(12), 1481-1485 (1974).
117. Kok H, Jureen R, Soon CY, Tey BH. Colon cancer presenting as Streptococcus gallolyticus infective endocarditis. Singapore Med. J. 48(2), e43-e45 (2007).
118. Klein RS, Recco RA, Catalano MT, Edberg SC, Casey JI, Steigbigel NH. Association of Streptococcus bovis with carcinoma of the colon. N. Engl. J. Med. 297(15), 800-802 (1977).
119. Boleij A, van Gelder MM, Swinkels DW, Tjalsma H. Clinical importance of Streptococcus gallolyticus infection among colorectal cancer patients: systematic review and meta-analysis. Clin. Infect. Dis. 53(9), 870-878 (2011).
120. Boleij A, Muytjens CM, Bukhari SI et al. Novel clues on the specific association of Streptococcus gallolyticus subsp gallolyticus with colorectal cancer. J. Infect. Dis. 203(8), 1101-1109 (2011).
121. Corredoira-Sanchez J, Garcia-Garrote F, Rabunal R et al. Association between bacteremia due to Streptococcus gallolyticus subsp. gallolyticus (Streptococcus bovis I) and colorectal neoplasia: a case-control study. Clin. Infect. Dis. 55(4), 491-496 (2012).
122. Schlegel L, Grimont F, Ageron E, Grimont PA, Bouvet A. Reappraisal of the taxonomy of the Streptococcus bovis/Streptococcus equinus complex and related species: description of Streptococcus gallolyticus subsp. gallolyticus subsp. nov., S. gallolyticus subsp. macedonicus subsp. nov. and S. gallolyticus subsp. pasteurianus subsp. nov. Int. J. Syst. Evol. Microbiol. 53(Pt 3), 631-645 (2003).
123. Seder CW, Kramer M, Long G, Uzieblo MR, Shanley CJ, Bove P. Clostridium septicum aortitis: report of two cases and review of the literature. J. Vasc. Surg. 49(5), 1304-1309 (2009).
124. Wang T, Cai G, Qiu Y et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 6(2), 320-329 (2012).
125. Chen W, Liu F, Ling Z, Tong X, Xiang C. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS ONE 7(6), e39743 (2012).
126. Castellarin M, Warren RL, Freeman JD et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 22(2), 299-306 (2012).
127. Swidsinski A, Khilkin M, Kerjaschki D et al. Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology 115(2), 281-286 (1998).
128. Uemura N, Okamoto S, Yamamoto S et al. Helicobacter pylori infection and the development of gastric cancer. N. Engl. J. Med. 345(11), 784-789 (2001).
129. Sears CL, Pardoll DM. Perspective: alpha-bugs, their microbial partners, and the link to colon cancer. J. Infect. Dis. 203(3), 306-311 (2011).
130. Tjalsma H, Boleij A, Marchesi JR, Dutilh BE. A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat. Rev. Microbiol. 10(8), 575-582 (2012).
131. Hand TW, Dos Santos LM, Bouladoux N et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 337(6101), 1553-1556 (2012).
132. Evans AS. Causation and disease: the Henle-Koch postulates revisited. Yale J. Biol. Med. 49(2), 175-195 (1976).