Bacterial cyclomodulins: types and roles in carcinogenesis

References

• Abukhdeir AM, Park BH. 2008. P21 and p27: roles in carcinogenesis and drug resistance. Expert Rev Mol Med. 10:e19–e.
   PubMedGoogle Scholar
• Aktories K. 1997. Bacterial toxins that target Rho proteins. J Clin Invest. 99(5):827–829.
   PubMed Web of Science ®Google Scholar
• Altieri F, Grillo C, Maceroni M, Chichiarelli S. 2008. DNA damage and repair: from molecular mechanisms to health implications. Antioxid Redox Signal. 10(5):891–938.
   PubMed Web of Science ®Google Scholar
• Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM, Fan T-J, Campbell BJ, Abujamel T, Dogan B, Rogers AB, et al. 2012. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 338(6103):120–123.
   PubMed Web of Science ®Google Scholar
• Atherton JC, Cao P, Peek RM, Tummuru MK, Blaser MJ, Cover TL. 1995. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori association of specific vacA types with cytotoxin production and peptic ulceration. J Biol Chem. 270(30):17771–17777.
   PubMed Web of Science ®Google Scholar
• Bang DD, Madsen M. 2003. Cytolethal distending toxins of Campylobacter jejuni: genetics, structure, mode of action, epidemiology, and the role of CDT in Campylobacter pathogenesis. Genome Lett. 2(1):73–82.
   Google Scholar
• Banks KE, Humphreys TL, Li W, Katz BP, Wilkes DS, Spinola SM. 2007. Haemophilus ducreyi partially activates human myeloid dendritic cells. Infect Immun. 75(12):5678–5685.
   PubMed Web of Science ®Google Scholar
• Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou L-VF, Kolettas E, Niforou K, Zoumpourlis VC, et al. 2006. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature. 444(7119):633–637.
   PubMed Web of Science ®Google Scholar
• Bernstein H, Bernstein C, Payne CM, Dvorak K. 2009. Bile acids as endogenous etiologic agents in gastrointestinal cancer. World J Gastroenterol. 15(27):3329–3340.
   PubMed Web of Science ®Google Scholar
• Bollrath J, Phesse TJ, von Burstin VA, Putoczki T, Bennecke M, Bateman T, Nebelsiek T, Lundgren-May T, Canli O, Schwitalla S, et al. 2009. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell. 15(2):91–102.
   PubMed Web of Science ®Google Scholar
• Boquet P. 2001. The cytotoxic necrotizing factor 1 (CNF1) from Escherichia coli. Toxicon. 39(11):1673–1680.
   PubMed Web of Science ®Google Scholar
• Bossuet-Greif N, Dubois D, Petit C, Tronnet S, Martin P, Bonnet R, Oswald E, Nougayrède J-P. 2016. Escherichia coli ClbS is a colibactin resistance protein. Mol Microbiol. 99(5):897–908.
   PubMed Web of Science ®Google Scholar
• Boulkroun S, Guenin-Macé L, Thoulouze M-I, Monot M, Merckx A, Langsley G, Bismuth G, Di Bartolo V, Demangel C. 2010. Mycolactone suppresses T cell responsiveness by altering both early signaling and posttranslational events. J Immunol. 184(3):1436–1444.
   PubMed Web of Science ®Google Scholar
• Boyer L, Travaglione S, Falzano L, Gauthier NC, Popoff MR, Lemichez E, Fiorentini C, Fabbri A. 2004. Rac GTPase instructs nuclear factor-kappaB activation by conveying the SCF complex and IkBalpha to the ruffling membranes . Mol Biol Cell. 15(3):1124–1133.
   PubMed Web of Science ®Google Scholar
• Brotherton CA. 2016. Investigations of the biosynthesis and structure of colibactin, a cytotoxin made by human-associated. Escherichia coli.
   Google Scholar
• Buc E, Dubois D, Sauvanet P, Raisch J, Delmas J, Darfeuille-Michaud A, Pezet D, Bonnet R. 2013. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One. 8(2):e56964.
   PubMed Web of Science ®Google Scholar
• Buetow L, Flatau G, Chiu K, Boquet P, Ghosh P. 2001. Structure of the Rho-activating domain of Escherichia coli cytotoxic necrotizing factor 1. Nat Struct Biol. 8(7):584–588.
   PubMedGoogle Scholar
• Cadet J, Davies KJ. 2017. Oxidative DNA damage & repair: an introduction. Free Radic Biol Med. 107:2–12.
   PubMed Web of Science ®Google Scholar
• Caprioli A, Donelli G, Falbo V, Possenti R, Roda LG, Roscetti G, Ruggeri FM. 1984. A cell division-active protein from E. coli. Biochem Biophys Res Commun. 118(2):587–593.
   PubMed Web of Science ®Google Scholar
• Caprioli A, Falbo V, Roda L, Ruggeri F, Zona C. 1983. Partial purification and characterization of an Escherichia coli toxic factor that induces morphological cell alterations. Infect Immun. 39(3):1300–1306.
   PubMed Web of Science ®Google Scholar
• Chan A, Fleming T, McGovern E, Chedid M, Miki T, Aaronson S. 1993. Expression cDNA cloning of a transforming gene encoding the wild-type G alpha 12 gene product. Mol Cell Biol. 13(2):762–768.
   PubMed Web of Science ®Google Scholar
• Chang PV, Hao L, Offermanns S, Medzhitov R. 2014. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci USA. 111(6):2247–2252.
   PubMed Web of Science ®Google Scholar
• Coleman ML, Marshall CJ, Olson MF. 2004. RAS and RHO GTPases in G1-phase cell-cycle regulation. Nat Rev Mol Cell Biol. 5(5):355–366.
   PubMed Web of Science ®Google Scholar
• Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. 2009. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis. 30(7):1073–1081.
   PubMed Web of Science ®Google Scholar
• Cortes-Bratti X, Frisan T, Thelestam M. 2001. The cytolethal distending toxins induce DNA damage and cell cycle arrest. Toxicon. 39(11):1729–1736.
   PubMed Web of Science ®Google Scholar
• Cougnoux A, Dalmasso G, Martinez R, Buc E, Delmas J, Gibold L, Sauvanet P, Darcha C, Déchelotte P, Bonnet M, et al. 2014. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype. Gut. 63(12):1932–1942.
   PubMed Web of Science ®Google Scholar
• Cover TL, Blaser MJ. 1992. Purification and characterization of the vacuolating toxin from Helicobacter pylori. J Biol Chem. 267(15):10570–10575.
   PubMed Web of Science ®Google Scholar
• Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrede JP. 2010. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci U S A. 107(25):11537–11542.
   PubMed Web of Science ®Google Scholar
• Dalmasso G, Cougnoux A, Delmas J, Darfeuille-Michaud A, Bonnet R. 2014. The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment. Gut Microbes. 5(5):675–680.
   PubMed Web of Science ®Google Scholar
• de Bernard M, Burroni D, Papini E, Rappuoli R, Telford J, Montecucco C. 1998. Identification of the Helicobacter pylori VacA toxin domain active in the cell cytosol. Infect Immun. 66(12):6014–6016.
   PubMed Web of Science ®Google Scholar
• de Martel C, Plummer M, Vignat J, Franceschi S. 2017. Worldwide burden of cancer attributable to HPV by site, country and HPV type. Int J Cancer. 141(4):664–670.
   PubMed Web of Science ®Google Scholar
• De Rycke J, Gonzalez E, Blanco J, Oswald E, Blanco M, Boivin R. 1990. Evidence for two types of cytotoxic necrotizing factor in human and animal clinical isolates of Escherichia coli. J Clin Microbiol. 28(4):694–699.
   PubMed Web of Science ®Google Scholar
• Del Bel Belluz L, Guidi R, Pateras IS, Levi L, Mihaljevic B, Rouf SF, Wrande M, Candela M, Turroni S, Nastasi C, et al. 2016. The typhoid toxin promotes host survival and the establishment of a persistent asymptomatic infection. PLoS Pathog. 12(4):e1005528.
   PubMed Web of Science ®Google Scholar
• DiRienzo JM. 2014. Cytolethal distending toxin: a unique variation on the AB toxin paradigm. New J Sci. 2014:1–26.
   Google Scholar
• Dubois D, Baron O, Cougnoux A, Delmas J, Pradel N, Boury M, Bouchon B, Bringer M-A, Nougayrède J-P, Oswald E, et al. 2011. ClbP is a prototype of a peptidase subgroup involved in biosynthesis of nonribosomal peptides. J Biol Chem. 286(41):35562–35570.
   PubMed Web of Science ®Google Scholar
• Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. 2005. Diversity of the human intestinal microbial flora. Science. 308(5728):1635–1638.
   PubMed Web of Science ®Google Scholar
• El-Aouar Filho RA, Nicolas A, De Paula Castro TL, Deplanche M, De Carvalho Azevedo VA, Goossens PL, et al. 2017. Heterogeneous family of cyclomodulins: smart weapons that allow bacteria to hijack the eukaryotic cell cycle and promote infections. Front Cell Infect Microbiol. 7:208.
   PubMed Web of Science ®Google Scholar
• Elkahwaji J, Hauke R, Brawner C. 2009. Chronic bacterial inflammation induces prostatic intraepithelial neoplasia in mouse prostate. Br J Cancer. 101(10):1740–1748.
   PubMed Web of Science ®Google Scholar
• En J, Goto M, Nakanaga K, Higashi M, Ishii N, Saito H, Yonezawa S, Hamada H, Small PLC. 2008. Mycolactone is responsible for the painlessness of Mycobacterium ulcerans infection (Buruli ulcer) in a murine study. Infect Immun. 76(5):2002–2007.
   PubMed Web of Science ®Google Scholar
• Fabbri A, Travaglione S, Ballan G, Loizzo S, Fiorentini C. 2013. The cytotoxic necrotizing factor 1 from E. coli: a Janus toxin playing with cancer regulators. Toxins. 5(8):1462–1474.
   PubMed Web of Science ®Google Scholar
• Faïs T, Delmas J, Barnich N, Bonnet R, Dalmasso G. 2018. Colibactin: more than a new bacterial toxin. Toxins. 10(4):151.
   PubMed Web of Science ®Google Scholar
• Falbo V, Pace T, Picci L, Pizzi E, Caprioli A. 1993. Isolation and nucleotide sequence of the gene encoding cytotoxic necrotizing factor 1 of Escherichia coli. Infect Immun. 61(11):4909–4914.
   PubMed Web of Science ®Google Scholar
• Fan Y, Mao R, Yang J. 2013. NF-κB and STAT3 signaling pathways collaboratively link inflammation to cancer. Protein Cell. 4(3):176–185.
   PubMed Web of Science ®Google Scholar
• Fedor Y, Vignard J, Nicolau-Travers M-L, Boutet-Robinet E, Watrin C, Salles B, Mirey G. 2013. From single-strand breaks to double-strand breaks during S-phase: a new mode of action of the Escherichia coli cytolethal distending toxin . Cell Microbiol. 15(1):1–15.
   PubMed Web of Science ®Google Scholar
• Ferreri AJ, Govi S, Ponzoni M. 2013. The role of Helicobacter pylori eradication in the treatment of diffuse large B-cell and marginal zone lymphomas of the stomach. Curr Opin Oncol. 25(5):470–479.
   PubMed Web of Science ®Google Scholar
• Fiorentini C, Fabbri A, Matarrese P, Falzano L, Boquet P, Malorni W. 1997. Hinderance of apoptosis and phagocytic behaviour induced by Escherichia coli cytotoxic necrotizing factor 1: two related activities in epithelial cells. Biochem Biophys Res Commun. 241(2):341–346.
   PubMed Web of Science ®Google Scholar
• Fischer W, Buhrdorf R, Gerland E, Haas R. 2001. Outer membrane targeting of passenger proteins by the vacuolating cytotoxin autotransporter of Helicobacter pylori. Infect Immun. 69(11):6769–6775.
   PubMed Web of Science ®Google Scholar
• Flatau G, Lemichez E, Gauthier M, Chardin P, Paris S, Fiorentini C, Boquet P. 1997. Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature. 387(6634):729–733.
   PubMed Web of Science ®Google Scholar
• Fowler CC, Chang S-J, Gao X, Geiger T, Stack G, Galán JE. 2017. Emerging insights into the biology of typhoid toxin. Curr Opin Microbiol. 35:70–77.
   PubMed Web of Science ®Google Scholar
• Frisan T, Cortes‐Bratti X, Chaves‐Olarte E, Stenerlöw B, Thelestam M. 2003. The Haemophilus ducreyi cytolethal distending toxin induces DNA double-strand breaks and promotes ATM-dependent activation of RhoA. Cell Microbiol. 5(10):695–707.
   PubMed Web of Science ®Google Scholar
• Gambhir S, Vyas D, Hollis M, Aekka A, Vyas A. 2015. Nuclear factor kappa B role in inflammation associated gastrointestinal malignancies. World J Gastroenterol. 21(11):3174–3183.
   PubMed Web of Science ®Google Scholar
• García A, Mannion A, Feng Y, Madden CM, Bakthavatchalu V, Shen Z, Ge Z, Fox JG. 2016. Cytotoxic Escherichia coli strains encoding colibactin colonize laboratory mice. Microbes Infect. 18(12):777–786.
   PubMed Web of Science ®Google Scholar
• Gholizadeh P, Eslami H, Kafil HS. 2017. Carcinogenesis mechanisms of Fusobacterium nucleatum. Biomed Pharmacother. 89:918–925.
   PubMed Web of Science ®Google Scholar
• Gonenc A, Ozkan Y, Torun M, Simsek B. 2001. Plasma malondialdehyde (MDA) levels in breast and lung cancer patients. J Clin Pharm Ther. 26(2):141–144.
   PubMed Web of Science ®Google Scholar
• González-Rivera C, Algood HMS, Radin JN, McClain MS, Cover TL. 2012. The intermediate region of Helicobacter pylori VacA is a determinant of toxin potency in a Jurkat T cell assay. Infect Immun. 80(8):2578–2588.
   PubMed Web of Science ®Google Scholar
• González-Rivera C, Gangwer KA, McClain MS, Eli IM, Chambers MG, Ohi MD, Lacy DB, Cover TL. 2010. Reconstitution of Helicobacter pylori VacA toxin from purified components. Biochemistry. 49(27):5743–5752.
   PubMed Web of Science ®Google Scholar
• Grasso F, Frisan T. 2015. Bacterial genotoxins: merging the DNA damage response into infection biology. Biomolecules. 5(3):1762–1782.
   PubMed Web of Science ®Google Scholar
• Griego RD, Rosen T, Orengo IF, Wolf JE. 1995. Dog, cat, and human bites: a review. J Am Acad Dermatol. 33(6):1019–1029.
   PubMed Web of Science ®Google Scholar
• Guenin-Macé L, Carrette F, Asperti-Boursin F, Le Bon A, Caleechurn L, Di Bartolo V, Fontanet A, Bismuth G, Demangel C. 2011. Mycolactone impairs T cell homing by suppressing microRNA control of L-selectin expression. Proc Natl Acad Sci USA. 108(31):12833–12838.
   PubMed Web of Science ®Google Scholar
• Guidi R, Guerra L, Levi L, Stenerlöw B, Fox JG, Josenhans C, Masucci MG, Frisan T. 2013. Chronic exposure to the cytolethal distending toxins of Gram-negative bacteria promotes genomic instability and altered DNA damage response . Cell Microbiol. 15(1):98–113.
   PubMed Web of Science ®Google Scholar
• Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J, Gamliel M, Enk J, Bar-On Y, Stanietsky-Kaynan N, Coppenhagen-Glazer S, et al. 2015. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity. 42(2):344–355.
   PubMed Web of Science ®Google Scholar
• Hatakeyama M. 2004. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat Rev Cancer. 4(9):688–694.
   PubMed Web of Science ®Google Scholar
• Hatakeyama M. 2017. Structure and function of Helicobacter pylori CagA, the first-identified bacterial protein involved in human cancer. Proc Jpn Acad Ser B Phys Biol Sci. 93(4):196–219.
   PubMed Web of Science ®Google Scholar
• Hazes B, Read RJ. 1995. A mosquitocidal toxin with a ricin-like cell-binding domain. Nat Struct Biol. 2(5):358–359.
   PubMedGoogle Scholar
• Heywood W, Henderson B, Nair SP. 2005. Cytolethal distending toxin: creating a gap in the cell cycle. J Med Microbiol. 54(Pt 3):207–216.
   PubMed Web of Science ®Google Scholar
• Higashi H, Nakaya A, Tsutsumi R, Yokoyama K, Fujii Y, Ishikawa S, Higuchi M, Takahashi A, Kurashima Y, Teishikata Y, et al. 2004. Helicobacter pylori CagA induces Ras-independent morphogenetic response through SHP-2 recruitment and activation. J Biol Chem. 279(17):17205–17216.
   PubMed Web of Science ®Google Scholar
• Hirata Y, Maeda S, Mitsuno Y, Akanuma M, Yamaji Y, Ogura K, Yoshida H, Shiratori Y, Omata M. 2001. Helicobacter pylori activates the cyclin D1 gene through mitogen-activated protein kinase pathway in gastric cancer cells. Infect Immun. 69(6):3965–3971.
   PubMed Web of Science ®Google Scholar
• Hoffmann C, Pop M, Leemhuis J, Schirmer J, Aktories K, Schmidt G. 2004. The Yersinia pseudotuberculosis cytotoxic necrotizing factor (CNFY) selectively activates RhoA. J Biol Chem. 279(16):16026–16032.
   PubMed Web of Science ®Google Scholar
• Homburg S, Oswald E, Hacker J, Dobrindt U. 2007. Expression analysis of the colibactin gene cluster coding for a novel polyketide in Escherichia coli. FEMS Microbiol Lett. 275(2):255–262.
   PubMed Web of Science ®Google Scholar
• Ito Y, Azuma T, Ito S, Suto H, Miyaji H, Yamazaki Y, Kohli Y, Kuriyama M. 1998. Full-length sequence analysis of the vacA gene from cytotoxic and noncytotoxic Helicobacter pylori. J Infect Dis. 178(5):1391–1398.
   PubMed Web of Science ®Google Scholar
• Jones KR, Whitmire JM, Merrell DS. 2010. A tale of two toxins: Helicobacter pylori CagA and VacA modulate host pathways that impact disease. Front Microbiol. 1:115.
   PubMed Web of Science ®Google Scholar
• Jubelin G, Chavez CV, Taieb F, Banfield MJ, Samba-Louaka A, Nobe R, Nougayrède J-P, Zumbihl R, Givaudan A, Escoubas J-M, et al. 2009. Cycle inhibiting factors (CIFs) are a growing family of functional cyclomodulins present in invertebrate and mammal bacterial pathogens. PLoS One. 4(3):e4855.
   PubMed Web of Science ®Google Scholar
• Karin M. 2006. NF-kappaB and cancer: mechanisms and targets. Mol Carcinog. 45(6):355–361.
   PubMed Web of Science ®Google Scholar
• Khansari N, Shakiba Y, Mahmoudi M. 2009. Chronic inflammation and oxidative stress as a major cause of age-related diseases and cancer. Recent Pat Inflamm Allergy Drug Discov. 3(1):73–80.
   PubMedGoogle Scholar
• Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, Clancy TE, Chung DC, Lochhead P, Hold GL, et al. 2013. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 14(2):207–215.
   PubMed Web of Science ®Google Scholar
• Kryston TB, Georgiev AB, Pissis P, Georgakilas AG. 2011. Role of oxidative stress and DNA damage in human carcinogenesis. Mutat Res. 711(1–2):193–201.
   PubMed Web of Science ®Google Scholar
• Kunzmann MH, Sieber SA. 2012. Target analysis of α-alkylidene-γ-butyrolactones in uropathogenic E. coli. Mol Biosyst. 8(11):3061–3067.
   PubMedGoogle Scholar
• Lacerda HM, Pullinger GD, Lax AJ, Rozengurt E. 1997. Cytotoxic necrotizing factor 1 from Escherichia coli and dermonecrotic toxin from Bordetella bronchiseptica induce p21(rho)-dependent tyrosine phosphorylation of focal adhesion kinase and paxillin in Swiss 3T3 cells . J Biol Chem. 272(14):9587–9596.
   PubMed Web of Science ®Google Scholar
• Lara-Tejero M, Galán JE. 2001. CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect Immun. 69(7):4358–4365.
   PubMed Web of Science ®Google Scholar
• Lax AJ. 2005. Opinion: bacterial toxins and cancer-a case to answer? Nat Rev Microbiol. 3(4):343–349.
   PubMed Web of Science ®Google Scholar
• Lax AJ. 2007. New genotoxin shows diversity of bacterial attack mechanisms. Trends Mol Med. 13(3):91–93.
   PubMed Web of Science ®Google Scholar
• Lax AJ, Grigoriadis AE. 2001. Pasteurella multocida toxin: the mitogenic toxin that stimulates signalling cascades to regulate growth and differentiation. Int J Med Microbiol. 291(4):261–268.
   PubMed Web of Science ®Google Scholar
• Lax AJ, Thomas W. 2002. How bacteria could cause cancer: one step at a time. Trends Microbiol. 10(6):293–299.
   PubMed Web of Science ®Google Scholar
• Lebrec H, Ponce R, Preston BD, Iles J, Born TL, Hooper M. 2015. Tumor necrosis factor, tumor necrosis factor inhibition, and cancer risk. Curr Med Res Opin. 31(3):557–574.
   PubMed Web of Science ®Google Scholar
• Lee HO, Davidson JM, Duronio RJ. 2009. Endoreplication: polyploidy with purpose. Genes Dev. 23(21):2461–2477.
   PubMed Web of Science ®Google Scholar
• Lee RB, Hassane DC, Cottle DL, Pickett CL. 2003. Interactions of Campylobacter jejuni cytolethal distending toxin subunits CdtA and CdtC with HeLa cells. Infect Immun. 71(9):4883–4890.
   PubMed Web of Science ®Google Scholar
• Lee S, Yang Y-A, Milano SK, Nguyen T, Ahn C, Sim JH, Thompson AJ, Hillpot EC, Yoo G, Paulson JC, et al. 2020. Salmonella typhoid toxin PltB subunit and its non-typhoidal Salmonella ortholog confer differential host adaptation and virulence. Cell Host Microbe. 27(6):937–949 e6.
   PubMed Web of Science ®Google Scholar
• Lerm M, Schmidt G, Aktories K. 2000. Bacterial protein toxins targeting rho GTPases. FEMS Microbiol Lett. 188(1):1–6.
   PubMed Web of Science ®Google Scholar
• Li J, Yuan X, Xu L, Wang Y. 2016. Biological function of cytolethal distending toxin (CDT) of Haemophilus parasuis. J Agric Biotech. 24(1):10–17.
   Google Scholar
• Liao JB. 2006. Viruses and human cancer. Yale J Biol Med. 79(3-4):115–122.
   PubMedGoogle Scholar
• Lim P, Wuenschell GE, Holland V, Lee D-H, Pfeifer GP, Rodriguez H, Termini J. 2004. Peroxyl radical mediated oxidative DNA base damage: implications for lipid peroxidation induced mutagenesis. Biochemistry. 43(49):15339–15348.
   PubMed Web of Science ®Google Scholar
• Liu J-F, Jamieson GG, Drew PA, Zhu G-J, Zhang S-W, Zhu T-N, Shan B-E, Wang Q-Z. 2005. Aspirin induces apoptosis in oesophageal cancer cells by inhibiting the pathway of NF-kappaB downstream regulation of cyclooxygenase-2 . ANZ J Surg. 75(11):1011–1016.
   PubMed Web of Science ®Google Scholar
• Livey I, Wardlaw AC. 1984. Production and properties of Bordetella pertussis heat-labile toxin. J Med Microbiol. 17(1):91–103.
   PubMed Web of Science ®Google Scholar
• Lockman HA, Gillespie RA, Baker BD, Shakhnovich E. 2002. Yersinia pseudotuberculosis produces a cytotoxic necrotizing factor. Infect Immun. 70(5):2708–2714.
   PubMed Web of Science ®Google Scholar
• Louis P, Hold GL, Flint HJ. 2014. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol. 12(10):661–672.
   PubMed Web of Science ®Google Scholar
• Lyon F. 1994. IARC monographs on the evaluation of carcinogenic risks to humans. Some Industrial Chemicals. Vol. 60. IARC. p. 389–433.
   Google Scholar
• Mager D. 2006. Bacteria and cancer: cause, coincidence or cure? A review. J Transl Med. 4(1):14.
   PubMedGoogle Scholar
• Marquet P, Duncan SH, Chassard C, Bernalier-Donadille A, Flint HJ. 2009. Lactate has the potential to promote hydrogen sulphide formation in the human colon. FEMS Microbiol Lett. 299(2):128–134.
   PubMed Web of Science ®Google Scholar
• Martin P, Marcq I, Magistro G, Penary M, Garcie C, Payros D, Boury M, Olier M, Nougayrède J-P, Audebert M, et al. 2013. Interplay between siderophores and colibactin genotoxin biosynthetic pathways in Escherichia coli. PLoS Pathog. 9(7):e1003437.
   PubMed Web of Science ®Google Scholar
• Martin OCB, Olier M, Ellero-Simatos S, Naud N, Dupuy J, Huc L, Taché S, Graillot V, Levêque M, Bézirard V, et al. 2019. Haem iron reshapes colonic luminal environment: impact on mucosal homeostasis and microbiome through aldehyde formation. Microbiome. 7(1):72.
   PubMedGoogle Scholar
• McClain M, Beckett A, Cover T. 2017. Helicobacter pylori vacuolating toxin and gastric cancer. Toxins. 9(10):316.
   PubMed Web of Science ®Google Scholar
• McClain MS, Cao P, Iwamoto H, Vinion-Dubiel AD, Szabo G, Shao Z, Cover TL. 2001. A 12-amino-acid segment, present in type s2 but not type s1 Helicobacter pylori VacA proteins, abolishes cytotoxin activity and alters membrane channel formation. J Bacteriol. 183(22):6499–6508.
   PubMed Web of Science ®Google Scholar
• Mezal EH, Bae D, Khan AA. 2014. Detection and functionality of the CdtB, PltA, and PltB from Salmonella enterica serovar Javiana. Pathog Dis. 72(2):95–103.
   PubMed Web of Science ®Google Scholar
• Michaud DS. 2013. Role of bacterial infections in pancreatic cancer. Carcinogenesis. 34(10):2193–2197.
   PubMed Web of Science ®Google Scholar
• Miller RA, Betteken MI, Guo X, Altier C, Duhamel GE, Wiedmann M. 2018. The typhoid toxin produced by the nontyphoidal Salmonella enterica serotype Javiana is required for induction of a DNA damage response in vitro and systemic spread in vivo. M Bio. 9(2):e00467–18.
   Google Scholar
• Mima K, Sukawa Y, Nishihara R, Qian ZR, Yamauchi M, Inamura K, Kim SA, Masuda A, Nowak JA, Nosho K, et al. 2015. Fusobacterium nucleatum and T cells in colorectal carcinoma. JAMA Oncol. 1(5):653–661.
   PubMed Web of Science ®Google Scholar
• Molinari M, Salio M, Galli C, Norais N, Rappuoli R, Lanzavecchia A, Montecucco C. 1998. Selective inhibition of Ii-dependent antigen presentation by Helicobacter pylori toxin VacA. J Exp Med. 187(1):135–140.
   PubMed Web of Science ®Google Scholar
• Monteleone G, Pallone F, Stolfi C. 2012. The dual role of inflammation in colon carcinogenesis. Int J Mol Sci. 13(9):11071–11084.
   PubMed Web of Science ®Google Scholar
• Morgan RN, Saleh SE, Farrag HA, Aboulwafa MM. 2019. Prevalence and pathologic effects of colibactin and cytotoxic necrotizing factor-1 (CNF 1) in Escherichia coli: experimental and bioinformatics analyses. Gut Pathog. 11(1):22.
   PubMedGoogle Scholar
• Mousa JJ, Yang Y, Tomkovich S, Shima A, Newsome RC, Tripathi P, Oswald E, Bruner SD, Jobin C. 2016. MATE transport of the E. coli-derived genotoxin colibactin. Nat Microbiol. 1:15009.
   PubMed Web of Science ®Google Scholar
• Nagaraja V, Eslick G. 2014. Systematic review with meta‐analysis: the relationship between chronic Salmonella typhi carrier status and gall‐bladder cancer. Aliment Pharmacol Ther. 39(8):745–750.
   PubMed Web of Science ®Google Scholar
• Nath G, Gulati AK, Shukla VK. 2010. Role of bacteria in carcinogenesis, with special reference to carcinoma of the gallbladder. World J Gastroenterol. 16(43):5395–5404.
   PubMed Web of Science ®Google Scholar
• Neal JT, Peterson TS, Kent ML, Guillemin KH. 2013. H. pylori virulence factor CagA increases intestinal cell proliferation by Wnt pathway activation in a transgenic zebrafish model. Dis Model Mech. 6(3):802–810.
   PubMed Web of Science ®Google Scholar
• Neurath MF. 2019. IL-23 in inflammatory bowel diseases and colon cancer. Cytokine Growth Factor Rev. 45:1–8.
   PubMed Web of Science ®Google Scholar
• Nougayrède J-P, Taieb F, De Rycke J, Oswald E. 2005. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol. 13(3):103–110.
   PubMed Web of Science ®Google Scholar
• Nougayrède J-P, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, Oswald E, et al. 2006. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 313(5788):848–851.
   PubMed Web of Science ®Google Scholar
• Ohnishi N, Yuasa H, Tanaka S, Sawa H, Miura M, Matsui A, Higashi H, Musashi M, Iwabuchi K, Suzuki M, et al. 2008. Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci USA. 105(3):1003–1008.
   PubMed Web of Science ®Google Scholar
• O’Riordan JM, Abdel-Latif MM, Ravi N, McNamara D, Byrne PJ, McDonald GSA, Keeling PWN, Kelleher D, Reynolds JV. 2005. Proinflammatory cytokine and nuclear factor kappa-B expression along the inflammation-metaplasia-dysplasia-adenocarcinoma sequence in the esophagus. Am J Gastroenterol. 100(6):1257–1264.
   PubMed Web of Science ®Google Scholar
• Orth JH, Lang S, Aktories K. 2004. Action of Pasteurella multocida toxin depends on the helical domain of Galphaq. J Biol Chem. 279(33):34150–34155.
   PubMed Web of Science ®Google Scholar
• Pagano JS, Blaser M, Buendia M-A, Damania B, Khalili K, Raab-Traub N, Roizman B. 2004. Infectious agents and cancer: criteria for a causal relation. Semin Cancer Biol. 14(6):453–471.
   PubMed Web of Science ®Google Scholar
• Plummer M, de Martel C, Vignat J, Ferlay J, Bray F, Franceschi S. 2016. Global burden of cancers attributable to infections in 2012: a synthetic analysis. Lancet Glob Health. 4(9):e609–e16.
   PubMed Web of Science ®Google Scholar
• Polk DB, Peek RM. 2010. Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer. 10(6):403–414.
   PubMed Web of Science ®Google Scholar
• Preuss I, Hildebrand D, Orth JHC, Aktories K, Kubatzky KF. 2010. Pasteurella multocida toxin is a potent activator of anti-apoptotic signalling pathways . Cell Microbiol. 12(8):1174–1185.
   PubMed Web of Science ®Google Scholar
• Pumirat P, Broek CV, Juntawieng N, Muangsombut V, Kiratisin P, Pattanapanyasat K, Stevens JM, Stevens MP, Korbsrisate S. 2014. Analysis of the prevalence, secretion and function of a cell cycle-inhibiting factor in the melioidosis pathogen Burkholderia pseudomallei. PLoS One. 9(5):e96298.
   PubMed Web of Science ®Google Scholar
• Raisch J, Buc E, Bonnet M, Sauvanet P, Vazeille E, de Vallée A, Déchelotte P, Darcha C, Pezet D, Bonnet R, et al. 2014. Colon cancer-associated B2 Escherichia coli colonize gut mucosa and promote cell proliferation. World J Gastroenterol. 20(21):6560–6572.
   PubMed Web of Science ®Google Scholar
• Rippere-Lampe KE, Lang M, Ceri H, Olson M, Lockman HA, O’Brien A. 2001. Cytotoxic necrotizing factor type 1-positive Escherichia coli causes increased inflammation and tissue damage to the prostate in a rat prostatitis model. Infect Immun. 69(10):6515–6519.
   PubMed Web of Science ®Google Scholar
• Rippere-Lampe KE, O’Brien AD, Conran R, Lockman HA. 2001. Mutation of the gene encoding cytotoxic necrotizing factor type 1 (cnf(1)) attenuates the virulence of uropathogenic Escherichia coli. Infect Immun. 69(6):3954–3964.
   PubMed Web of Science ®Google Scholar
• Rozengurt E, Higgins T, Chanter N, Lax AJ, Staddon JM. 1990. Pasteurella multocida toxin: potent mitogen for cultured fibroblasts. Proc Natl Acad Sci U S A. 87(1):123–127.
   PubMed Web of Science ®Google Scholar
• Russell WR, Gratz SW, Duncan SH, Holtrop G, Ince J, Scobbie L, Duncan G, Johnstone AM, Lobley GE, Wallace RJ, et al. 2011. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr. 93(5):1062–1072.
   PubMed Web of Science ®Google Scholar
• Sahai E, Marshall CJ. 2002. RHO-GTPases and cancer. Nat Rev Cancer. 2(2):133–142.
   PubMed Web of Science ®Google Scholar
• Samba‐Louaka A, Nougayrède JP, Watrin C, Jubelin G, Oswald E, Taieb F. 2008. Bacterial cyclomodulin Cif blocks the host cell cycle by stabilizing the cyclin-dependent kinase inhibitors p21 and p27. Cell Microbiol. 10(12):2496–2508.
   PubMed Web of Science ®Google Scholar
• Satin B, Norais N, Telford J, Rappuoli R, Murgia M, Montecucco C, Papini E. 1997. Effect of Helicobacter pylori vacuolating toxin on maturation and extracellular release of procathepsin D and on epidermal growth factor degradation. J Biol Chem. 272(40):25022–25028.
   PubMed Web of Science ®Google Scholar
• Schistosomes, liver flukes and Helicobacter pylori. 1994. IARC working group on the evaluation of carcinogenic risks to humans. IARC Monogr Eval Carcinog Risks Hum. 61:1–241.
   PubMedGoogle Scholar
• Schmidt G, Sehr P, Wilm M, Selzer J, Mann M, Aktories K. 1997. Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature. 387(6634):725–729.
   PubMed Web of Science ®Google Scholar
• Schmidt G, Selzer J, Lerm M, Aktories K. 1998. The Rho-deamidating cytotoxic necrotizing factor 1 from Escherichia coli possesses transglutaminase activity cysteine 866 and histidine 881 are essential for enzyme activity. J Biol Chem. 273(22):13669–13674.
   PubMed Web of Science ®Google Scholar
• Sears CL. 2009. Enterotoxigenic Bacteroides fragilis: a rogue among symbiotes. Clin Microbiol Rev. 22(2):349–369.
   PubMed Web of Science ®Google Scholar
• Sears CL, Garrett WS. 2014. Microbes, microbiota, and colon cancer. Cell Host Microbe. 15(3):317–328.
   PubMed Web of Science ®Google Scholar
• Sfanos KS, De Marzo AM. 2012. Prostate cancer and inflammation: the evidence. Histopathology. 60(1):199–215.
   PubMed Web of Science ®Google Scholar
• Shenker BJ, Datar S. 1995. Fusobacterium nucleatum inhibits human T-cell activation by arresting cells in the mid-G1 phase of the cell cycle. Infect Immun. 63(12):4830–4836.
   PubMed Web of Science ®Google Scholar
• Shenker BJ, Ojcius DM, Walker LP, Zekavat A, Scuron MD, Boesze-Battaglia K. 2015. Aggregatibacter actinomycetemcomitans cytolethal distending toxin activates the NLRP3 inflammasome in human macrophages, leading to the release of proinflammatory cytokines. Infect Immun. 83(4):1487–1496.
   PubMed Web of Science ®Google Scholar
• Shield KD, Marant Micallef C, de Martel C, Heard I, Megraud F, Plummer M, Vignat J, Bray F, Soerjomataram I. 2018. New cancer cases in France in 2015 attributable to infectious agents: a systematic review and meta-analysis. Eur J Epidemiol. 33(3):263–274.
   PubMed Web of Science ®Google Scholar
• Simmonds RE, Lali FV, Smallie T, Small PL, Foxwell BM. 2009. Mycolactone inhibits monocyte cytokine production by a posttranscriptional mechanism. J Immunol. 182(4):2194–2202.
   PubMed Web of Science ®Google Scholar
• Spanò S, Ugalde JE, Galán JE. 2008. Delivery of a Salmonella typhi exotoxin from a host intracellular compartment. Cell Host Microbe. 3(1):30–38.
   PubMed Web of Science ®Google Scholar
• Staddon JM, Chanter N, Lax A, Higgins TE, Rozengurt E. 1990. Pasteurella multocida toxin, a potent mitogen, stimulates protein kinase C-dependent and -independent protein phosphorylation in Swiss 3T3 cells. J Biol Chem. 265(20):11841–11848.
   PubMed Web of Science ®Google Scholar
• Stoll T, Markwirth G, Reipschläger S, Schmidt G. 2009. A new member of a growing toxin family-Escherichia coli cytotoxic necrotizing factor 3 (CNF3). Toxicon. 54(6):745–753.
   PubMed Web of Science ®Google Scholar
• Swann JB, Vesely MD, Silva A, Sharkey J, Akira S, Schreiber RD, Smyth MJ. 2008. Demonstration of inflammation-induced cancer and cancer immunoediting during primary tumorigenesis. Proc Natl Acad Sci USA. 105(2):652–656.
   PubMed Web of Science ®Google Scholar
• Taieb F, Petit C, Nougayrède J-P, Oswald E, Donnenberg MS. 2016. The Enterobacterial genotoxins: cytolethal distending toxin and colibactin. EcoSal Plus. 7(1). DOI:https://doi.org/10.1128/ecosalplus.ESP-0008-2016.
   PubMedGoogle Scholar
• Tan S, Noto JM, Romero-Gallo J, Peek RM, Jr, Amieva MR. 2011. Helicobacter pylori perturbs iron trafficking in the epithelium to grow on the cell surface. PLoS Pathog. 7(5):e1002050.
   PubMed Web of Science ®Google Scholar
• Tezal M, Sullivan MA, Reid ME, Marshall JR, Hyland A, Loree T, Lillis C, Hauck L, Wactawski-Wende J, Scannapieco FA, et al. 2007. Chronic periodontitis and the risk of tongue cancer. Arch Otolaryngol Head Neck Surg. 133(5):450–454.
   PubMedGoogle Scholar
• Thomas W, Ascott ZK, Harmey D, Slice LW, Rozengurt E, Lax AJ. 2001. Cytotoxic necrotizing factor from Escherichia coli induces RhoA-dependent expression of the cyclooxygenase-2 gene. Infect Immun. 69(11):6839–6845.
   PubMed Web of Science ®Google Scholar
• Tommasino M. 2014. The human papillomavirus family and its role in carcinogenesis. Semin Cancer Biol. 26:13–21.
   PubMed Web of Science ®Google Scholar
• Toro TB, Toth JI, Petroski MD. 2013. The cyclomodulin cycle inhibiting factor (CIF) alters cullin neddylation dynamics. J Biol Chem. 288(21):14716–14726.
   PubMed Web of Science ®Google Scholar
• Torres VJ, Ivie SE, McClain MS, Cover TL. 2005. Functional properties of the p33 and p55 domains of the Helicobacter pylori vacuolating cytotoxin. J Biol Chem. 280(22):21107–21114.
   PubMed Web of Science ®Google Scholar
• Tsugawa H, Suzuki H, Saya H, Hatakeyama M, Hirayama T, Hirata K, Nagano O, Matsuzaki J, Hibi T. 2012. Reactive oxygen species-induced autophagic degradation of Helicobacter pylori CagA is specifically suppressed in cancer stem-like cells. Cell Host Microbe. 12(6):764–777.
   PubMed Web of Science ®Google Scholar
• Vaca C, Wilhelm J, Harms-Ringdahl M. 1988. Interaction of lipid peroxidation products with DNA. A review. Mutation Res/Rev Genetic Toxicol. 195(2):137–149.
   PubMed Web of Science ®Google Scholar
• Walker KE, Weiss AA. 1994. Characterization of the dermonecrotic toxin in members of the genus Bordetella. Infect Immun. 62(9):3817–3828.
   PubMed Web of Science ®Google Scholar
• Wallace SS. 2002. Biological consequences of free radical-damaged DNA bases. Free Radic Biol Med. 33(1):1–14.
   PubMed Web of Science ®Google Scholar
• Wang F, Meng W, Wang B, Qiao L. 2014. Helicobacter pylori-induced gastric inflammation and gastric cancer. Cancer Lett. 345(2):196–202.
   PubMed Web of Science ®Google Scholar
• Ward JF, Blakely WF, Joner EI. 1985. Mammalian cells are not killed by DNA single-strand breaks caused by hydroxyl radicals from hydrogen peroxide. Radiat Res. 103(3):383–392.
   PubMed Web of Science ®Google Scholar
• White MK, Pagano JS, Khalili K. 2014. Viruses and human cancers: a long road of discovery of molecular paradigms. Clin Microbiol Rev. 27(3):463–481.
   PubMed Web of Science ®Google Scholar
• Wilson BA, Aminova LR, Ponferrada VG, Ho M. 2000. Differential modulation and subsequent blockade of mitogenic signaling and cell cycle progression by Pasteurella multocida toxin. Infect Immun. 68(8):4531–4538.
   PubMed Web of Science ®Google Scholar
• Wilson BA, Zhu X, Ho M, Lu L. 1997. Pasteurella multocida toxin activates the inositol triphosphate signaling pathway in Xenopus oocytes via G(q)alpha-coupled phospholipase C-beta1. J Biol Chem. 272(2):1268–1275.
   PubMed Web of Science ®Google Scholar
• Windey K, De Preter V, Verbeke K. 2012. Relevance of protein fermentation to gut health. Mol Nutr Food Res. 56(1):184–196.
   PubMed Web of Science ®Google Scholar
• Xiong H, Du W, Sun T-T, Lin Y-W, Wang J-L, Hong J, Fang J-Y. 2014. A positive feedback loop between STAT3 and cyclooxygenase-2 gene may contribute to Helicobacter pylori-associated human gastric tumorigenesis. Int J Cancer. 134(9):2030–2040.
   PubMed Web of Science ®Google Scholar
• Xu M, Mizoguchi I, Morishima N, Chiba Y, Mizuguchi J, Yoshimoto T. 2010. Regulation of antitumor immune responses by the IL-12 family cytokines, IL-12, IL-23, and IL-27. Clin Dev Immunol. 2010:1–9.
   Google Scholar
• Yamaoka Y, Osato MS, Sepulveda AR, Gutierrez O, Figura N, Kim JG, Kodama T, Kashima K, Graham DY. 2000. Molecular epidemiology of Helicobacter pylori: separation of H. pylori from East Asian and non-Asian countries. Epidemiol Infect. 124(1):91–96.
   PubMed Web of Science ®Google Scholar
• Yan J, Smyth MJ, Teng MW. 2018. Interleukin (IL)-12 and IL-23 and their conflicting roles in cancer. Cold Spring Harb Perspect Biol. 10(7):a028530.
   PubMed Web of Science ®Google Scholar
• Ye D, Willhite DC, Blanke SR. 1999. Identification of the minimal intracellular vacuolating domain of the Helicobacter pylori vacuolating toxin. J Biol Chem. 274(14):9277–9282.
   PubMed Web of Science ®Google Scholar
• Yeh E, Kohli RM, Bruner SD, Walsh CT. 2004. Type II thioesterase restores activity of a NRPS module stalled with an aminoacyl-S-enzyme that cannot be elongated. Chembiochem. 5(9):1290–1293.
   PubMed Web of Science ®Google Scholar
• Yokoyama K, Higashi H, Ishikawa S, Fujii Y, Kondo S, Kato H, Azuma T, Wada A, Hirayama T, Aburatani H, et al. 2005. Functional antagonism between Helicobacter pylori CagA and vacuolating toxin VacA in control of the NFAT signaling pathway in gastric epithelial cells. Proc Natl Acad Sci USA. 102(27):9661–9666.
   PubMed Web of Science ®Google Scholar
• Yu H, Kortylewski M, Pardoll D. 2007. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol. 7(1):41–51.
   PubMed Web of Science ®Google Scholar
• Zeisel SH, Warrier M. 2017. Trimethylamine N-oxide, the microbiome, and heart and kidney disease. Annu Rev Nutr. 37:157–181.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Aung KM, Uhlin BE, Wai SN. 2018. Reversible senescence of human colon cancer cells after blockage of mitosis/cytokinesis caused by the CNF1 cyclomodulin from. Sci Rep. 8(1):17780.
   PubMedGoogle Scholar