Intracellular colon cancer-associated Escherichia coli promote protumoral activities of human macrophages by inducing sustained COX-2 expression

Laboratory Investigation

Volumn 95, Issue 3, 2015, Pages 296-307

  Raisch, Jennifer ^a,b,c   Rolhion, Nathalie ^d   DuBois, Anaëlle ^a,b,c   Darfeuille Michaud, Arlette ^a,b,c   Bringer, Marie Agnès ^a,b,c  

^a CRNH Auvergne   (France)

^b CEMAGREF   (France)

^c UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

^d MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; GENTAMICIN; OFLOXACIN; COLIBACTIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PEPTIDE; POLYKETIDE; PROSTAGLANDIN E2;

ARTICLE; AUTOPHAGY; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM MUTANT; CANCER GROWTH; CELL ACTIVITY; COLON CANCER; COLON CANCER ASSOCIATED ESCHERICHIA COLI; COLON FLORA; COMMENSAL ESCHERICHIA COLI; CONTROLLED STUDY; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTRACELLULAR BACTERIUM; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR PROMOTION; WILD TYPE; CELL VACUOLE; COLON TUMOR; CONFOCAL MICROSCOPY; GENETICS; IMMUNOBLOTTING; IMMUNOLOGY; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL LINE; ULTRASTRUCTURE;

CELL LINE, TUMOR; COLONIC NEOPLASMS; CYCLOOXYGENASE 2; DINOPROSTONE; ESCHERICHIA COLI; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOBLOTTING; MACROPHAGES; MICROBIAL VIABILITY; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDES; POLYKETIDES; VACUOLES;

EID: 84928621098     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2014.161     Document Type: Article

References (62)

1. Ferlay J, Shin HR, Bray F, et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2012;127:2893-2917.
2. Huxley RR, Ansary-Moghaddam A, Clifton P, et al. The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence. Int J Cancer 2009;125:171-180.
3. Rasool S, Kadla SA, Rasool V, et al. A comparative overview of general risk factors associated with the incidence of colorectal cancer. Tumour Biol 2013;34:2469-2476.
4. Dejea C, Wick E, Sears CL. Bacterial oncogenesis in the colon. Future Microbiol 2013;8:445-460.
5. Zackular JP, Baxter NT, Iverson KD, et al. The gut microbiome modulates colon tumorigenesis. MBio 2013;4:e00692-13.
6. Zhu Q, Gao R, Wu W, et al. The role of gut microbiota in the pathogenesis of colorectal cancer. Tumour Biol 2013;34:1285-1300.
7. Irrazabal T, Belcheva A, Girardin SE, et al. The multifaceted role of the intestinal microbiota in colon cancer. Mol Cell 2014;54:309-320.
8. Sears CL, Garrett WS. Microbes, microbiota, and colon cancer. Cell Host Microbe 2014;15:317-328.
9. Sobhani I, Tap J, Roudot-Thoraval F, et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One 2011;6:e16393.
10. 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 2009;15:1016-1022.
11. Kostic AD, Gevers D, Pedamallu CS, et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 2012;22:292-298.
12. Kostic AD, Chun E, Robertson L, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumorimmune microenvironment. Cell Host Microbe 2013;14:207-215.
13. Castellarin M, Warren RL, Freeman JD, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 2012;22:299-306.
14. Toprak NU, Yagci A, Gulluoglu BM, et al. A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clin Microbiol Infect 2006;12:782-786.
15. Maddocks OD, 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.
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. Swidsinski A, Khilkin M, Kerjaschki D, et al. Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology 1998;115:281-286.
18. Arthur JC, Perez-Chanona E, Muhlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012;338:120-123.
19. Buc E, Dubois D, Sauvanet P, et al. High prevalence of mucosaassociated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One 2013;8:e56964.
20. Nougayrede JP, Homburg S, Taieb F, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 2006;313:848-851.
21. Secher T, Samba-Louaka A, Oswald E, et al. Escherichia coli producing colibactin triggers premature and transmissible senescence in mammalian cells. PLoS One 2013;8:e77157.
22. Cougnoux A, Dalmasso G, Martinez R, et al. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescenceassociated secretory phenotype. Gut [Internet] 2014;63:1932-1942.
23. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010;141:39-51.
24. Sica A, Larghi P, Mancino A, et al. Macrophage polarization in tumour progression. Semin Cancer Biol 2008;18:349-355.
25. Wu WK, Sung JJ, Lee CW, et al. Cyclooxygenase-2 in tumorigenesis of gastrointestinal cancers: an update on the molecular mechanisms. Cancer Lett 2010;295:7-16.
26. Wang D, DuBois RN. Pro-inflammatory prostaglandins and progression of colorectal cancer. Cancer Lett 2008;267:197-203.
27. Eberhart CE, Coffey RJ, Radhika A, et al. Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology 1994;107:1183-1188.
28. Ogino S, Kirkner GJ, Nosho K, et al. Cyclooxygenase-2 expression is an independent predictor of poor prognosis in colon cancer. Clin Cancer Res 2008;14:8221-8227.
29. Wang D, Dubois RN. The role of COX-2 in intestinal inflammation and colorectal cancer. Oncogene 2010;29:781-788.
30. Dixon DA, Blanco FF, Bruno A, et al. Mechanistic aspects of COX-2 expression in colorectal neoplasia. Recent Results Cancer Res 2013;191:7-37.
31. Young LE, Dixon DA. Posttranscriptional regulation of cyclooxygenase 2 expression in colorectal cancer. Curr Colorectal Cancer Rep 2010;6:60-67.
32. Chun KS, Surh YJ. Signal transduction pathways regulating cyclooxygenase-2 expression: potential molecular targets for chemoprevention. Biochem Pharmacol 2004;68:1089-1100.
33. Raisch J, Buc E, Bonnet M, et al. Colon cancer-associated B2 Escherichia coli colonize gut mucosa and promote cell proliferation. World J Gastroenterol 2014;20:6560-6572.
34. Chaveroche MK, Ghigo JM, d'Enfert C. A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 2000;28:E97.
35. Helaine S, Thompson JA, Watson KG, et al. Dynamics of intracellular bacterial replication at the single cell level. Proc Natl Acad Sci USA 2010;107:3746-3751.
36. Bringer MA, Barnich N, Glasser AL, et al. HtrA stress protein is involved in intramacrophagic replication of adherent and invasive Escherichia coli strain LF82 isolated from a patient with Crohn's disease. Infect Immun 2005;73:712-721.
37. Glasser AL, Boudeau J, Barnich N, et al. Adherent invasive Escherichia coli strains from patients with Crohn's disease survive and replicate within macrophages without inducing host cell death. Infect Immun 2001;69:5529-5537.
38. Chen TC, Tsai JP, Huang HJ, et al. Regulation of cyclooxygenase-2 expression in human bladder epithelial cells infected with type I fimbriated uropathogenic E. coli. Cell Microbiol 2011;13:1703-1713.
39. Brown JR, DuBois RN. COX-2: a molecular target for colorectal cancer prevention. J Clin Oncol 2005;23:2840-2855.
40. Thi EP, Lambertz U, Reiner NE. Sleeping with the enemy: how intracellular pathogens cope with a macrophage lifestyle. PLoS Pathog 2012;8:e1002551.
41. Kumar Y, Valdivia RH. Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 2009;5:593-601.
42. Stein MP, Muller MP, Wandinger-Ness A. Bacterial pathogens commandeer Rab GTPases to establish intracellular niches. Traffic 2012;13:1565-1588.
43. Friedrich N, Hagedorn M, Soldati-Favre D, et al. Prison break: pathogens' strategies to egress from host cells. Microbiol Mol Biol Rev 2012;76:707-720.
44. Fratti RA, Chua J, Deretic V. Induction of p38 mitogen-activated protein kinase reduces early endosome autoantigen 1 (EEA1) recruitment to phagosomal membranes. J Biol Chem 2003;278:46961-46967.
45. Cavalli V, Vilbois F, Corti M, et al. The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol Cell 2001;7:421-432.
46. Marjuki H, Gornitzky A, Marathe BM, et al. Influenza A virus-induced early activation of ERK and PI3K mediates V-ATPase-dependent intracellular pH change required for fusion. Cell Microbiol 2011;13:587-601.
47. Webber JL, Tooze SA. Coordinated regulation of autophagy by p38alpha MAPK through mAtg9 and p38IP. EMBO J 2010;29:27-40.
48. Corcelle E, Djerbi N, Mari M, et al. Control of the autophagy maturation step by the MAPK ERK and p38: lessons from environmental carcinogens. Autophagy 2007;3:57-59.
49. Klug K, Ehlers S, Uhlig S, et al. Mitogen-activated protein kinases p38 and ERK1/2 regulated control of Mycobacterium avium replication in primary murine macrophages is independent of tumor necrosis factoralpha and interleukin-10. Innate Immun 2011;17:470-485.
50. Dimitrakopoulos O, Liopeta K, Dimitracopoulos G, et al. Replication of Brucella melitensis inside primary human monocytes depends on mitogen activated protein kinase signaling. Microbes Infect 2013;15: 450-460.
51. Helaine S, Cheverton AM, Watson KG, et al. Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science 2014;343:204-208.
52. Bringer MA, Glasser AL, Tung CH, et al. The Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 replicates in mature phagolysosomes within J774 macrophages. Cell Microbiol 2006;8: 471-484.
53. Moreau K, Lacas-Gervais S, Fujita N, et al. Autophagosomes can support Yersinia pseudotuberculosis replication in macrophages. Cell Microbiol 2010;12:1108-1123.
54. Starr T, Child R, Wehrly TD, et al. Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe 2012;11:33-45.
55. Kim JM, Lee JY, Yoon YM, et al. Bacteroides fragilis enterotoxin induces cyclooxygenase-2 and fluid secretion in intestinal epithelial cells through NF-kappaB activation. Eur J Immunol 2006;36:2446-2456.
56. Hisatsune J, Yamasaki E, Nakayama M, et al. Helicobacter pylori VacA enhances prostaglandin E2 production through induction of cyclooxygenase 2 expression via a p38 mitogen-activated protein kinase/activating transcription factor 2 cascade in AZ-521 cells. Infect Immun 2007;75:4472-4481.
57. Thomas W, Ascott ZK, Harmey D, et al. Cytotoxic necrotizing factor from Escherichia coli induces RhoA-dependent expression of the cyclooxygenase-2 Gene. Infect Immun 2001;69:6839-6845.
58. Bamba H, Ota S, Kato A, et al. High expression of cyclooxygenase-2 in macrophages of human colonic adenoma. Int J Cancer 1999; 83:470-475.
59. Hull MA, Booth JK, Tisbury A, et al. Cyclooxygenase 2 is up-regulated and localized to macrophages in the intestine of Min mice. Br J Cancer 1999;79:1399-1405.
60. Hull MA, Faluyi OO, Ko CW, et al. Regulation of stromal cell cyclooxygenase-2 in the ApcMin/+ mouse model of intestinal tumorigenesis. Carcinogenesis 2006;27:382-391.
61. Hardwick JC, van den Brink GR, Offerhaus GJ, et al. NF-kappaB, p38 MAPK and JNK are highly expressed and active in the stroma of human colonic adenomatous polyps. Oncogene 2001;20:819-827.
62. Chang YJ, Wu MS, Lin JT, et al. Induction of cyclooxygenase-2 overexpression in human gastric epithelial cells by Helicobacter pylori involves TLR2/TLR9 and c-Src-dependent nuclear factor-kappaB activation. Mol Pharmacol 2004;66:1465-1477.