Do bacterial genotoxins contribute to chronic inflammation, genomic instability and tumor progression?

FEBS Journal

Volumn 278, Issue 23, 2011, Pages 4577-4588

  Guerra, Lina ^a   Guidi, Riccardo ^a   Frisan, Teresa ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

bacterial genotoxin; chronic inflammation; colibactin, cytolethal distending toxin; DNA damage; DNA damage response; genomic instability; tumor induction progression

Indexed keywords

BACTERIAL TOXIN; COLIBACTIN; CYTOLETHAL DISTENDING TOXIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

APOPTOSIS; BACTERIAL INFECTION; CARCINOGENESIS; CELL CYCLE; CELL SURVIVAL; CELLULAR PARAMETERS; CHROMOSOME ABERRATION; CHRONIC INFLAMMATION; DNA DAMAGE; DNA DAMAGE RESPONSE; DNA STRAND BREAKAGE; GENE EXPRESSION; GENE MUTATION; GENOMIC INSTABILITY; GRAM NEGATIVE BACTERIUM; HOST PATHOGEN INTERACTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; REVIEW; TOXIN ANALYSIS; TOXIN STRUCTURE; TOXIN SYNTHESIS; TUMOR GROWTH;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; NEGIBACTERIA;

EID: 81555216786     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08125.x     Document Type: Review

References (72)

1. Humans IWGotEoCRt (1994) Schistosomes, Liver Flukes and Helicobacter pylori. Lyon, France.
2. Vogelmann R, &, Amieva MR, (2007) The role of bacterial pathogens in cancer. Curr Opin Microbiol 10, 76-81. (Pubitemid 46223641)
3. Raptis S, &, Bapat B, (2006) Genetic instability in human tumors. EXS 96, 303-320.
4. Smith JL, &, Bayles DO, (2006) The contribution of cytolethal distending toxin to bacterial pathogenesis. Crit Rev Microbiol 32, 227-248. (Pubitemid 44851409)
5. Scott DA, &, Kaper JB, (1994) Cloning and sequencing of the genes encoding Escherichia coli cytolethal distending toxins. Infect Immun 62, 244-251. (Pubitemid 24011966)
6. Lara-Tejero M, &, Galan JE, (2001) CdtA, CdtB and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect Immun 69, 4358-4365. (Pubitemid 32574433)
7. Nesic D, Hsu Y, &, Stebbins CE, (2004) Assembly and function of a bacterial genotoxin. Nature 429, 429-433. (Pubitemid 38715135)
8. McSweeney LA, &, Dreyfus LA, (2004) Nuclear localization of the Escherichia coli cytolethal distending toxin CdtB subunit. Cell Microbiol 6, 447-458. (Pubitemid 38488937)
9. Hassane DC, Lee RB, &, Pickett CL, (2003) Campylobacter jejuni cytolethal distending toxin promotes DNA repair responses in normal human cells. Infect Immun 71, 541-545. (Pubitemid 36026062)
10. McSweeney LA, &, Dreyfus LA, (2005) Carbohydrate-binding specificity of the Escherichia coli cytolethal distending toxin CdtA-II and CdtC-II subunits. Infect Immun 73, 2051-2060. (Pubitemid 40470803)
11. Elwell CA, &, Dreyfus LA, (2000) DNAase I homologous residues in CdtB are critical for cytolethal distending toxin-mediated cell cycle arrest. Mol Microbiol 37, 952-963. (Pubitemid 30618154)
12. Lara-Tejero M, &, Galan JE, (2000) A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science 290, 354-357.
13. Hassane DC, Lee RB, Mendenhall MD, &, Pickett CL, (2001) Cytolethal distending toxin demonstrates genotoxic activity in a yeast model. Infect Immun 69, 5752-5759. (Pubitemid 32786514)
14. Guerra L, Teter K, Lilley BN, Stenerlow B, Holmes RK, Ploegh HL, Sandvig K, Thelestam M, &, Frisan T, (2005) Cellular internalization of cytolethal distending toxin: a new end to a known pathway. Cell Microbiol 7, 921-934. (Pubitemid 40908870)
15. Shenker BJ, Dlakic M, Walker LP, Besack D, Jaffe E, LaBelle E, &, Boesze-Battaglia K, (2007) A novel mode of action for a microbial-derived immunotoxin: the cytolethal distending toxin subunit B exhibits phosphatidylinositol 3,4,5-triphosphate phosphatase activity. J Immunol 178, 5099-5108. (Pubitemid 46595293)
16. Matangkasombut O, Wattanawaraporn R, Tsuruda K, Ohara M, Sugai M, &, Mongkolsuk S, (2010) Cytolethal distending toxin from Aggregatibacter actinomycetemcomitans induces DNA damage, S/G2 cell cycle arrest, and caspase- independent death in a Saccharomyces cerevisiae model. Infect Immun 78, 783-792.
17. Rabin SD, Flitton JG, &, Demuth DR, (2009) Aggregatibacter actinomycetemcomitans cytolethal distending toxin induces apoptosis in nonproliferating macrophages by a phosphatase-independent mechanism. Infect Immun 77, 3161-3169.
18. Haghjoo E, &, Galan JE, (2004) Salmonella typhi encodes a functional cytolethal distending toxin that is delivered into host cells by a bacterial-internalization pathway. Proc Natl Acad Sci USA 101, 4614-4619. (Pubitemid 38437459)
19. Spano S, Ugalde JE, &, Galan JE, (2008) Delivery of a Salmonella typhi exotoxin from a host intracellular compartment. Cell Host Microbe 3, 30-38.
20. Boesze-Battaglia K, Besack D, McKay T, Zekavat A, Otis L, Jordan-Sciutto K, &, Shenker BJ, (2006) Cholesterol-rich membrane microdomains mediate cell cycle arrest induced by Actinobacillus actinomycetemcomitans cytolethal-distending toxin. Cell Microbiol 8, 823-836.
21. Carette JE, Guimaraes CP, Varadarajan M, Park AS, Wuethrich I, Godarova A, Kotecki M, Cochran BH, Spooner E, Ploegh HL, et al. (2009) Haploid genetic screens in human cells identify host factors used by pathogens. Science 326, 1231-1235.
22. Mise K, Akifusa S, Watarai S, Ansai T, Nishihara T, &, Takehara T, (2005) Involvement of ganglioside GM3 in G(2)/M cell cycle arrest of human monocytic cells induced by Actinobacillus actinomycetemcomitans cytolethal distending toxin. Infect Immun 73, 4846-4852. (Pubitemid 41105641)
23. Eshraghi A, Maldonado-Arocho FJ, Gargi A, Cardwell MM, Prouty MG, Blanke SR, &, Bradley KA, (2010) Cytolethal distending toxin family members are differentially affected by alterations in host glycans and membrane cholesterol. J Biol Chem 285, 18199-18207.
24. Cortes-Bratti X, Chaves-Olarte E, Lagergård T, &, Thelestam M, (2000) Cellular internalization of cytolethal distending toxin from Haemophilus ducreyi. Infect Immun 68, 6903-6911. (Pubitemid 32463401)
25. Guerra L, Nemec KN, Massey S, Tatulian SA, Thelestam M, Frisan T, &, Teter K, (2009) A novel mode of translocation for cytolethal distending toxin. Biochim Biophys Acta 1793, 489-495.
26. Nishikubo S, Ohara M, Ueno Y, Ikura M, Kurihara H, Komatsuzawa H, Oswald E, &, Sugai M, (2003) An N-terminal segment of the active component of the bacterial genotoxin cytolethal distending toxin B (CDTB) directs CDTB into the nucleus. J Biol Chem 278, 50671-50681. (Pubitemid 37548916)
27. Pickett CL, &, Whitehouse CA, (1999) The cytolethal distending toxin family. Trends Microbiol 7, 292-297. (Pubitemid 29304565)
28. Nougayrede JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, &, Oswald E, (2006) Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313, 848-851. (Pubitemid 44223356)
29. Putze J, Hennequin C, Nougayrede JP, Zhang W, Homburg S, Karch H, Bringer MA, Fayolle C, Carniel E, Rabsch W, et al. (2009) Genetic structure and distribution of the colibactin genomic island among members of the family Enterobacteriaceae. Infect Immun 77, 4696-4703.
30. 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, 255-262. (Pubitemid 47437858)
31. Ciccia A, &, Elledge SJ, (2010) The DNA damage response: making it safe to play with knives. Mol Cell 40, 179-204.
32. Smith J, Tho LM, Xu N, &, Gillespie DA, (2010) The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv Cancer Res 108, 73-112.
33. Meek DW, (2009) Tumour suppression by p53: a role for the DNA damage response? Nat Rev Cancer 9, 714-723.
34. Jiricny J, (2006) The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 7, 335-346.
35. van Loon B, Markkanen E, &, Hubscher U, (2010) Oxygen as a friend and enemy: how to combat the mutational potential of 8-oxo-guanine. DNA Repair (Amst) 9, 604-616.
36. Nouspikel T, (2009) DNA repair in mammalian cells: nucleotide excision repair: variations on versatility. Cell Mol Life Sci 66, 994-1009.
37. Kass EM, &, Jasin M, (2010) Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett 584, 3703-3708.
38. Stracker TH, &, Petrini JH, (2011) The MRE11 complex: starting from the ends. Nat Rev Mol Cell Biol 12, 90-103.
39. You Z, &, Bailis JM, (2010) DNA damage and decisions: CtIP coordinates DNA repair and cell cycle checkpoints. Trends Cell Biol 20, 402-409.
40. Lieber MR, (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 79, 181-211.
41. Negrini S, Gorgoulis VG, &, Halazonetis TD, (2010) Genomic instability-an evolving hallmark of cancer. Nat Rev Mol Cell Biol 11, 220-228.
42. Pino MS, &, Chung DC, (2010) The chromosomal instability pathway in colon cancer. Gastroenterology 138, 2059-2072.
43. Thelestam M, &, Frisan T, (2006) Cytolethal distending toxins. In The Comprehensive Sourcebook of Bacterial Protein Toxins (, Alouf J, &, Popoff M, eds), pp. 448-467. Elsevier, Academic Press, San Diego.
44. Guerra L, Cortes-Bratti X, Guidi R, &, Frisan T, (2011) The biology of the cytolethal distending toxin. Toxins 3, 172-190.
45. 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, 695-707. (Pubitemid 37185046)
46. Cortes-Bratti X, Karlsson C, Lagergard T, Thelestam M, &, Frisan T, (2001) The Haemophilus ducreyi cytolethal distending toxin induces cell cycle arrest and apoptosis via the DNA damage checkpoint pathways. J Biol Chem 276, 5296-5302.
47. Li L, Sharipo A, Chaves-Olarte E, Masucci MG, Levitsky V, Thelestam M, &, Frisan T, (2002) The Haemophilus ducreyi cytolethal distending toxin activates sensors of DNA damage and repair complexes in proliferating and non-proliferating cells. Cell Microbiol 4, 87-99. (Pubitemid 34228966)
48. Yamamoto K, Tominaga K, Sukedai M, Okinaga T, Iwanaga K, Nishihara T, &, Fukuda J, (2004) Delivery of cytolethal distending toxin B induces cell cycle arrest and apoptosis in gingival squamous cell carcinoma in vitro. Eur J Oral Sci 112, 445-451. (Pubitemid 39456962)
49. Sato T, Koseki T, Yamato K, Saiki K, Konishi K, Yoshikawa M, Ishikawa I, &, Nishihara T, (2002) p53-independent expression of p21(CIP1/WAF1) in plasmacytic cells during G(2) cell cycle arrest induced by Actinobacillus actinomycetemcomitans cytolethal distending toxin. Infect Immun 70, 528-534. (Pubitemid 34083810)
50. 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 USA 107, 11537-11542.
51. Sert V, Cans C, Tasca C, Bret-Bennis L, Oswald E, Ducommun B, &, De Rycke J, (1999) The bacterial cytolethal distending toxin (CDT) triggers a G2 cell cycle checkpoint in mammalian cells without preliminary induction of DNA strand breaks. Oncogene 18, 6296-6304.
52. Guerra L, Albihn A, Tronnersjö S, Yan Q, Guidi R, Stenerlöw B, Sterzenbach T, Josenhans C, Fox JG, Schauer DB, et al. (2010) Myc is required for activation of the ATM-dependent checkpoints in response to DNA damage. PLoS ONE 5, e892.
53. Blazkova H, Krejcikova K, Moudry P, Frisan T, Hodny Z, &, Bartek J, (2010) Bacterial intoxication evokes cellular senescence with persistent DNA damage and cytokine signaling. J Cell Mol Med 14, 357-367.
54. Kitagawa T, Hoshida H, &, Akada R, (2007) Genome-wide analysis of cellular response to bacterial genotoxin CdtB in yeast. Infect Immun 75, 1393-1402. (Pubitemid 46385833)
55. Kastan MB, &, Bartek J, (2004) Cell-cycle checkpoints and cancer. Nature 432, 316-323. (Pubitemid 39551659)
56. Shiloh Y, (2003) ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3, 155-168. (Pubitemid 37328868)
57. Guerra L, Carr HS, Richter-Dahlfors A, Masucci MG, Thelestam M, Frost JA, &, Frisan T, (2008) A bacterial cytotoxin identifies the RhoA exchange factor Net1 as a key effector in the response to DNA damage. PLoS ONE 3, e2254.
58. Grivennikov SI, Greten FR, &, Karin M, (2010) Immunity, inflammation, and cancer. Cell 140, 883-899.
59. Karin M, Lawrence T, &, Nizet V, (2006) Innate immunity gone awry: linking microbial infections to chronic inflammation and cancer. Cell 124, 823-835. (Pubitemid 43261455)
60. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, Kagnoff MF, &, Karin M, (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118, 285-296. (Pubitemid 39061110)
61. Pikarsky E, Porat RM, Stein I, Abramovitch R, Amit S, Kasem S, Gutkovich-Pyest E, Urieli-Shoval S, Galun E, &, Ben-Neriah Y, (2004) NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 431, 461-466. (Pubitemid 39329586)
62. Polk DB, &, Peek RM Jr, (2010) Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer 10, 403-414.
63. Machado AM, Figueiredo C, Seruca R, &, Rasmussen LJ, (2010) Helicobacter pylori infection generates genetic instability in gastric cells. Biochim Biophys Acta 1806, 58-65.
64. Touati E, Michel V, Thiberge JM, Wuscher N, Huerre M, &, Labigne A, (2003) Chronic Helicobacter pylori infections induce gastric mutations in mice. Gastroenterology 124, 1408-1419. (Pubitemid 36531814)
65. Toprak NU, Yagci A, Gulluoglu BM, Akin ML, Demirkalem P, Celenk T, &, Soyletir G, (2006) A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clin Microbiol Infect 12, 782-786. (Pubitemid 43983804)
66. Rakoff-Nahoum S, &, Medzhitov R, (2007) Regulation of spontaneous intestinal tumorigenesis through the adaptor protein MyD88. Science 317, 124-127. (Pubitemid 47056471)
67. Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, Yen HR, Huso DL, Brancati FL, Wick E, McAllister F, et al. (2009) A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 15, 1016-1022.
68. Fox JG, Rogers AB, Whary MT, Ge Z, Taylor NS, Xu S, Horwitz BH, &, Erdman SE, (2004) Gastroenteritis in NF-kappaB-deficient mice is produced with wild-type Camplyobacter jejuni but not with C. jejuni lacking cytolethal distending toxin despite persistent colonization with both strains. Infect Immun 72, 1116-1125. (Pubitemid 38166694)
69. Ge Z, Feng Y, Whary MT, Nambiar PR, Xu S, Ng V, Taylor NS, &, Fox JG, (2005) Cytolethal distending toxin is essential for Helicobacter hepaticus colonization in outbred Swiss Webster mice. Infect Immun 73, 3559-3567. (Pubitemid 40745900)
70. Ge Z, Rogers AB, Feng Y, Lee A, Xu S, Taylor NS, &, Fox JG, (2007) Bacterial cytolethal distending toxin promotes the development of dysplasia in a model of microbially induced hepatocarcinogenesis. Cell Microbiol 9, 2070-2080. (Pubitemid 47087096)
71. Brauner A, Brandt L, Frisan T, Thelestam M, &, Ekbom A, (2010) Is there a risk of cancer development after Campylobacter infection? Scand J Gastroenterol 45, 893-897.
72. Lecuit M, Abachin E, Martin A, Poyart C, Pochart P, Suarez F, Bengoufa D, Feuillard J, Lavergne A, Gordon JI, et al. (2004) Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N Engl J Med 350, 239-248. (Pubitemid 38067636)