The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment

Gut Microbes

Volumn 5, Issue 5, 2014, Pages 675-680

  Dalmasso, Guillaume ^a   Cougnoux, Antony ^a   Delmas, Julien ^a,b   Darfeuille Michaud, Arlette ^a,b   Bonnet, Richard ^a,b  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

Author keywords

Colibactin; Colorectal cancer; Escherichia coli; Micro RNA; Microbiota; SENP1; SUMO; Toxin

Indexed keywords

BACTERIAL TOXIN; BETA GALACTOSIDASE; COLIBACTIN; GROWTH FACTOR; MICRORNA; MICRORNA 20A 5P; MYC PROTEIN; PROTEIN; SENTRIN SPECIFIC PEPTIDASE 1; UNCLASSIFIED DRUG; MIRN20 MICRORNA, MOUSE; MUTAGENIC AGENT; PEPTIDE; POLYKETIDE; PROTEIN P53; PROTEINASE; SENP1 PROTEIN, MOUSE;

ARTICLE; CANCER CELL; CARCINOGENESIS; CELL PROLIFERATION; COLON TUMOR; COLORECTAL CANCER; DNA DAMAGE; ESCHERICHIA COLI; GENE PRODUCT; GENOMIC ISLAND; GENOTOXICITY; HUMAN; INTESTINE FLORA; INTRACELLULAR SIGNALING; MISMATCH REPAIR; NONHUMAN; PHENOTYPE; PROTEIN PROCESSING; SENESCENCE; SENESCENCE ASSOCIATED SECRETORY PHENOTYPE; SUMOYLATION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; BIOLOGICAL MODEL; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; PATHOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

ANIMALS; COLONIC NEOPLASMS; ENDOPEPTIDASES; ESCHERICHIA COLI; MICE; MICRORNAS; MODELS, BIOLOGICAL; MUTAGENS; PEPTIDES; POLYKETIDES; SUMOYLATION; TUMOR MICROENVIRONMENT; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84922032680     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/19490976.2014.969989     Document Type: Article

References (30)

1. Ferlay J, Shin H-R, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010; 127:2893-917; PMID:21351269; http://dx.doi.org/ 10.1002/ijc.25516
2. The Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486:207-14; PMID:22699609; http://dx.doi.org/10.1038/nature 11234
3. Clements A, Young JC, Constantinou N, Frankel G. Infection strategies of enteric pathogenic Escherichia coli. Gut Microbes 2012; 3:71-87; PMID:22555463; http://dx.doi.org/10.4161/gmic.19182
4. Maddocks ODK, 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 2009; 4:e5517; PMID:19436735; http://dx.doi.org/10.1371/journal.pone.0005517
5. Nougayréde J-P, Taieb F, De Rycke J, Oswald E. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol 2005; 13:103- 10; http://dx.doi.org/10.1016/j.tim.2005.01.002
6. Lax AJ. Opinion: bacterial toxins and cancer-a case to answer? Nat Rev Microbiol 2005; 3:343-9; PMID: 15806096; http://dx.doi.org/10.1038/nrmicro1130
7. Buc E, Dubois D, Sauvanet P, Raisch J, Delmas J, Darfeuille- Michaud A, Pezet D, Bonnet R. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS ONE 2013; 8: e56964; PMID:23457644; http://dx.doi.org/10.1371/ journal.pone.0056964
8. Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM, Fan T-J, Campbell BJ, Abujamel T, Dogan B, Rogers AB, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012; 338:120-3; PMID:22903521; http://dx.doi.org/ 10.1126/science.1224820
9. Nougayréde J-P, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, Oswald E. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 2006; 313:848-51; http://dx.doi.org/10.1126/science. 1127059
10. Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayréde J-P. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA 2010; 107:11537-42; PMID:20534522
11. Cougnoux A, Dalmasso G, Martinez R, Buc E, Delmas J, Gibold L, Sauvanet P, Darcha C, Dechelotte P, Bonnet M, et al. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype. Gut [Internet] 2014 [cited 2014 Jul 18]; Available from: http://gut.bmj.com/cgi/ doi/10.1136/gutjnl-2013-305257
12. Ben-Porath I, Weinberg RA. The signals and pathways activating cellular senescence. Int J Biochem Cell Biol 2005; 37:961-76; PMID:15743671; http://dx.doi.org/ 10.1016/j.biocel.2004.10.013
13. Stein U, Walther W, Arlt F, Schwabe H, Smith J, Fichtner I, Birchmeier W, Schlag PM. MACC1, a newly identified key regulator of HGF-MET signaling, predicts colon cancer metastasis. Nat Med 2009; 15:59- 67; PMID:19098908; http://dx.doi.org/10.1038/ nm.1889
14. Matsui S, Osada S, Tomita H, Komori S, Mori R, Sanada Y, Takahashi T, Yamaguchi K, Yoshida K. Clinical significance of aggressive hepatectomy for colorectal liver metastasis, evaluated from the HGF/c-Met pathway. Int J Oncol 2010; 37:289-97; PMID:20596656
15. Bischof O, Dejean A. SUMO is growing senescent. Cell Cycle 2007; 6:677-81; PMID:17374992; http://dx.doi. org/10.4161/cc.6.6.4021
16. Fukuda I, Ito A, Hirai G, Nishimura S, Kawasaki H, Saitoh H, Kimura K-I, Sodeoka M, Yoshida M. Ginkgolic acid inhibits protein SUMOylation by blocking formation of the E1-SUMO intermediate. Chem Biol 2009; 16:133-40; PMID:19246003; http://dx.doi.org/ 10.1016/j.chembiol.2009.01.009
17. Yates KE, Korbel GA, Shtutman M, Roninson IB, DiMaio D. Repression of the SUMO-specific protease Senp1 induces p53-dependent premature senescence in normal human fibroblasts. Aging Cell 2008; 7:609-21; PMID:18616636; http://dx.doi.org/10.1111/j.1474- 9726.2008.00411.x
18. 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:e12519; PMID:20824140; http://dx.doi.org/10.1371/journal.pone.0012519
19. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005; 435:839-43; http://dx. doi.org/10.1038/nature03677
20. Guerra L, Albihn A, Tronnersjö S, Yan Q, Guidi R, Stenerlöw B, Sterzenbach T, Josenhans C, Fox JG, Schauer DB, et al. Myc is required for activation of the ATM-dependent checkpoints in response to DNA damage. PLoS ONE 2010; 5:e8924; PMID:20111719; http://dx.doi.org/10.1371/journal.pone.0008924
21. Rodier F, Campisi J. Four faces of cellular senescence. J Cell Biol 2011; 192:547-56; PMID:21321098; http:// dx.doi.org/10.1083/jcb.201009094
22. Collado M, Gil J, Efeyan A, Guerra C, Schuhmacher AJ, Barradas M, Benguría A, Zaballos A, Flores JM, Barbacid M, et al. Tumour biology: senescence in premalignant tumours. Nature 2005; 436:642; PMID:16079833; http://dx.doi.org/10.1038/436642a
23. Bonnet M, Buc E, Sauvanet P, Darcha C, Dubois D, Pereira B, Déchelotte P, Bonnet R, Pezet D, Darfeuille- Michaud A. Colonization of the human gut by E. coli and colorectal cancer risk. Clin Cancer Res 2014; 20:859-67; PMID:24334760; http://dx.doi.org/ 10.1158/1078-0432.CCR-13-1343
24. Hecht M, Papoutsi M, Tran HD, Wilting J, Schweigerer L. Hepatocyte growth factor/c-Met signaling promotes the progression of experimental human neuroblastomas. Cancer Res 2004; 64:6109-18; PMID:15342394; http://dx.doi.org/10.1158/0008- 5472.CAN-04-1014
25. Kermorgant S, Aparicio T, Dessirier V, Lewin MJ, Lehy T. Hepatocyte growth factor induces colonic cancer cell invasiveness via enhanced motility and protease overproduction. Evidence for PI3 kinase and PKC involvement. Carcinogenesis 2001; 22:1035-42; PMID:11408346; http://dx.doi.org/10.1093/carcin/22.7.1035
26. Binefa G, Rodríguez-Moranta F, Teule A, Medina- Hayas M. Colorectal cancer: From prevention to personalized medicine. World J Gastroenterol 2014; 20:6786-808; PMID:24944469; http://dx.doi.org/ 10.3748/wjg.v20.i22.6786
27. Di X, Shiu RP, Newsham IF, Gewirtz DA. Apoptosis, autophagy, accelerated senescence and reactive oxygen in the response of human breast tumor cells to adriamycin. Biochem Pharmacol 2009; 77:1139-50; PMID: 19185564; http://dx.doi.org/10.1016/j.bcp.2008.12.016
28. Biggers JW, Nguyen T, Di X, Gupton JT, Henderson SC, Emery SM, Alotaibi M, White KL Jr, Brown R, Almenara J, et al. Autophagy, cell death and sustained senescence arrest in B16/F10 melanoma cells and HCT-116 colon carcinoma cells in response to the novel microtubule poison, JG-03-14. Cancer Chemother Pharmacol 2013; 71:441-55; PMID:23178952; http://dx.doi.org/10.1007/s00280-012-2024-6
29. Campisi J. Cellular senescence as a tumor-suppressor mechanism. Trends Cell Biol 2001; 11:S27-31; PMID:11684439; http://dx.doi.org/10.1016/S0962- 8924(01)02151-1
30. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, Cordon-Cardo C, Lowe SW. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007; 445:656-60; PMID:17251933; http://dx.doi.org/ 10.1038/nature05529