Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype

Gut

Volumn 63, Issue 12, 2014, Pages 1932-1942

  Cougnoux, Antony ^a,b   Dalmasso, Guillaume ^a,b   Martinez, Ruben ^c   Buc, Emmanuel ^a,b,d   Delmas, Julien ^a,b,d   Gibold, Lucie ^a,b,d   Sauvanet, Pierre ^a,b,d   Darcha, Claude ^d   Déchelotte, Pierre ^d   Bonnet, Mathilde ^a,b   Pezet, Denis ^a,b,d   Wodrich, Harald ^c   Darfeuille Michaud, Arlette ^a,b   Bonnet, Richard ^a,b,d  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b CEMAGREF   (France)

^c University Victor Segalen   (France)

^d UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COLIBACTIN; MUTAGENIC AGENT; NUCLEAR PROTEIN; PEPTIDE; POLYKETIDE; PROTEINASE; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SENP1 PROTEIN, MOUSE;

ANIMAL; CARCINOGENESIS; CELL AGING; COLON TUMOR; ESCHERICHIA COLI; EXPERIMENTAL NEOPLASM; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; MOUSE; MUTATION; PATHOGENICITY; PATHOLOGY;

ANIMALS; CARCINOGENESIS; CELL AGING; COLONIC NEOPLASMS; ENDOPEPTIDASES; ESCHERICHIA COLI; HEPATOCYTE GROWTH FACTOR; HUMANS; MICE; MUTAGENS; MUTATION; NEOPLASMS, EXPERIMENTAL; NUCLEAR PROTEINS; PEPTIDES; POLYKETIDES; PROTO-ONCOGENE PROTEINS C-MET;

EID: 84896414707     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2013-305257     Document Type: Article

References (44)

1. Esteller M. Cancer epigenomics: DNA methylomes and histone-modi fication maps. Nat Rev Genet 2007;8:286-98.
2. Stratton MR, Campbell PJ, Futreal PA. The cancer genome. Nature 2009;458:719-24.
3. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990;61:759-67.
4. De Martel C, Ferlay J, Franceschi S, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 2012;13:607-15.
5. Tjalsma H, Boleij A, Marchesi JR, et al. A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat Rev Microbiol 2012;10:575-82.
6. Ferlay J, Shin H-R, Bray F, et al . Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010;127:2893-917.
7. 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 1997;57:812-14.
8. Uronis JM, Mühlbauer M, Herfarth HH, et al. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS ONE 2009;4:e6026.
9. Lax AJ. Opinion: bacterial toxins and cancer - a case to answer? Nat Rev Microbiol 2005;3:343-9.
10. Goodwin AC, Destefano Shields CE, Wu S, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA 2011;108:15354-9.
11. Wang X, Huycke MM. Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells. Gastroenterology 2007;132:551-61.
12. Wu S, Rhee K-J, Zhang M, et al. Bacteroides fragilis toxin stimulates intestinal epithelial cell shedding and gamma-secretase-dependent E-cadherin cleavage. J Cell Sci 2007;120:1944-52.
13. Wu S, Rhee K-J, Albesiano E, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 2009;15:1016-22.
14. Abdulamir AS, Hafidh RR, Bakar FA. Molecular detection, quantification, and isolation of Streptococcus gallolyticus bacteria colonizing colorectal tumors: inflammation-driven potential of carcinogenesis via IL-1, COX-2, and IL-8. Mol Cancer 2010;9:249.
15. Swidsinski A, Khilkin M, Kerjaschki D, et al. Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology 1998;115:281-6.
16. Martin HM, Campbell BJ, Hart CA, et al. Enhanced Escherichia coli adherence and invasion in Crohn' s disease and colon cancer. Gastroenterology 2004;127:80-93.
17. Maddocks ODK, Short AJ, Donnenberg MS, et al. Attaching and effacing Escherichia coli downregulate DNA mismatch repair protein in vitro and are associated with colorectal adenocarcinomas in humans. PLoS ONE 2009;4:e5517.
18. Nougayrède J-P, Taieb F, De Rycke J, et al. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol 2005;13:103-10.
19. Nougayrède J-P, Homburg S, Taieb F, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 2006;313:848-51.
20. Cuevas-Ramos G, Petit CR, Marcq I, et al. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA 2010;107:11537-42.
21. Arthur JC, Perez-Chanona E, Mühlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012;338:120-3.
22. Buc E, Dubois D, Sauvanet P, et al. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS ONE 2013;8:e56964.
23. Tanaka T, Kohno H, Suzuki R, et al. A novel in flammation-related mouse colon carcinogenesis model induced by azoxymethane and dextran sodium sulfate. Cancer Sci 2003;94:965-73.
24. Dreux N, Denizot J, Martinez-Medina M, et al. Point mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response. PLoS Pathog 2013;9:e1003141.
25. Debacq-Chainiaux F, Erusalimsky JD, Campisi J, et al. Protocols to detect senescence-associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and in vivo. Nat Protoc 2009;4:1798-806.
26. Rodier F, Campisi J. Four faces of cellular senescence. J Cell Biol 2011;192:547-56.
27. Ben-Porath I, Weinberg RA. The signals and pathways activating cellular senescence. Int J Biochem Cell Biol 2005;37:961-76.
28. Kuilman T, Peeper DS. Senescence-messaging secretome: SMS-ing cellular stress. Nat Rev Cancer 2009;9:81-94.
29. Bischof O, Dejean A. SUMO is growing senescent. Cell Cycle 2007;6:677-81.
30. Yates KE, Korbel GA, Shtutman M, et al. Repression of the SUMO-specifi c protease Senp1 induces p53-dependent premature senescence in normal human fibroblasts. Aging Cell 2008;7:609-21.
31. Witty J, Aguilar-Martinez E, Sharrocks AD. SENP1 participates in the dynamic regulation of Elk-1 SUMOylation. Biochem J 2010;428:247-54.
32. Bonifacio LN, Jarstfer MB. MiRNA profile associated with replicative senescence, extended cell culture, and ectopic telomerase expression in human foreskin fibroblasts. PLoS ONE 2010;5:pii: e12519.
33. O'Donnell KA, Wentzel EA, Zeller KI, et al. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005;435:839-43.
34. Guerra L, Albihn A, Tronnersjö S, et al. Myc is required for activation of the ATMdependent checkpoints in response to DNA damage. PLoS ONE 2010;5:e8924.
35. Muehlbauer M, Gharaibeh R, Arthur JC, et al. Intestinal in flammation targets E. coli NC101 transcriptome response and promotes development of colorectal cancer (CRC). Gastroenterology 2013;144:S144-5.
36. Campbell BJ, Finnie IA, Hounsell EF, et al. Direct demonstration of increased expression of Thomsen-Friedenreich (TF) antigen in colonic adenocarcinoma and ulcerative colitis mucin and its concealment in normal mucin. J Clin Invest 1995;95:571-6.
37. Matsuo K, Ota H, Akamatsu T, et al . Histochemistry of the surface mucous gel layer of the human colon. Gut 1997;40:782-9.
38. Boland CR, Deshmukh GD. The carbohydrate composition of mucin in colonic cancer. Gastroenterology 1990;98:1170-7.
39. Greten FR, Eckmann L, Greten TF, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004;118:285-96.
40. Krtolica A, Parrinello S, Lockett S, et al. Senescent fibroblasts promote epithelial cell growth and tumorigenesis: a link between cancer and aging. Proc Natl Acad Sci USA 2001;98:12072-7.
41. Stein U, Walther W, Arlt F, et al. MACC1, a newly identified key regulator of HGF-MET signaling, predicts colon cancer metastasis. Nat Med 2009;15:59-67.
42. Matsui S, Osada S, Tomita H, et al. Clinical significance of aggressive hepatectomy for colorectal liver metastasis, evaluated from the HGF/c-Met pathway. Int J Oncol 2010;37:289-97.
43. Sliwinska MA, Mosieniak G, Wolanin K, et al. Induction of senescence with doxorubicin leads to increase genomic instability of HCT166 cells. Mech Ageing Dev 2009;130:24-32.
44. Mikolajczyk J, Drag M, Békés M, et al. Small ubiquitin-related modifier (SUMO)-specific proteases: profiling the speci ficities and activities of human SENPs. J Biol Chem 2007;282:26217-24.