Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells - PubMed (original) (raw)
Comparative Study
. 2007 Feb;132(2):551-61.
doi: 10.1053/j.gastro.2006.11.040. Epub 2006 Nov 29.
Affiliations
- PMID: 17258726
- DOI: 10.1053/j.gastro.2006.11.040
Comparative Study
Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells
Xingmin Wang et al. Gastroenterology. 2007 Feb.
Abstract
Background & aims: We investigated whether Enterococcus faecalis, a Gram-positive intestinal commensal that produces extracellular superoxide, could promote chromosomal instability (CIN) in mammalian cells.
Methods: We measured the ability of E faecalis to promote CIN using hybrid hamster cells (A(L)N) containing human chromosome 11.
Results: E faecalis promoted CIN in A(L)N cells with average mutant fractions per 10(5) survivors (+/-SD) of 72.3 +/- 6.7 at 1 x 10(9) cfu mL(-1) compared with 22.2 degrees +/- 4.5 for the no bacteria control. Gamma-irradiation at 2 Gray similarly resulted in 74.7 +/- 5.7 mutant clones per 10(5) survivors. Deletions in chromosome 11 consistent with CIN were verified in 80% of mutant clones. E faecalis-treated A(L)N cells were protected from CIN by superoxide dismutase, gamma-tocopherol, and cyclooxygenase-2 (COX-2) inhibitors. In a dual-chamber tissue culture model designed to mimic stromal-epithelial cell interactions, macrophages pretreated with E faecalis grown on permeable supports increased mutant fractions 2.5-fold for A(L)N cells. COX-2 was up-regulated by superoxide from E faecalis and mutant fractions decreased when COX-2 was silenced using short interfering RNA. Escherichia coli, a Gram-negative commensal that produces negligible extracellular superoxide, only modestly promoted CIN in this model.
Conclusions: These findings indicate that macrophage COX-2 is induced by superoxide from E faecalis and promotes CIN in mammalian cells through diffusible factors. This mechanism links the oxidative physiology of E faecalis to propagation of genomic instability through a bystander effect, and offers a novel theory for the role of commensal bacteria in the etiology of sporadic colorectal cancer.
Comment in
- In the beginning was Helicobacter pylori: roles for microbes in other intestinal disorders.
Hecht G. Hecht G. Gastroenterology. 2007 Feb;132(2):481-3. doi: 10.1053/j.gastro.2007.01.013. Gastroenterology. 2007. PMID: 17258742 No abstract available. - Sporadic colorectal cancer: an infectious disease?
Sinicrope FA. Sinicrope FA. Gastroenterology. 2007 Feb;132(2):797-801. doi: 10.1053/j.gastro.2007.01.012. Gastroenterology. 2007. PMID: 17261304 No abstract available.
Similar articles
- Sporadic colorectal cancer: an infectious disease?
Sinicrope FA. Sinicrope FA. Gastroenterology. 2007 Feb;132(2):797-801. doi: 10.1053/j.gastro.2007.01.012. Gastroenterology. 2007. PMID: 17261304 No abstract available. - Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA.
Huycke MM, Abrams V, Moore DR. Huycke MM, et al. Carcinogenesis. 2002 Mar;23(3):529-36. doi: 10.1093/carcin/23.3.529. Carcinogenesis. 2002. PMID: 11895869 - 4-hydroxy-2-nonenal mediates genotoxicity and bystander effects caused by Enterococcus faecalis-infected macrophages.
Wang X, Yang Y, Moore DR, Nimmo SL, Lightfoot SA, Huycke MM. Wang X, et al. Gastroenterology. 2012 Mar;142(3):543-551.e7. doi: 10.1053/j.gastro.2011.11.020. Epub 2011 Nov 19. Gastroenterology. 2012. PMID: 22108198 Free PMC article. - Colorectal cancer: role of commensal bacteria and bystander effects.
Wang X, Huycke MM. Wang X, et al. Gut Microbes. 2015;6(6):370-6. doi: 10.1080/19490976.2015.1103426. Gut Microbes. 2015. PMID: 26727419 Free PMC article. Review. - JC virus and colorectal cancer: a possible trigger in the chromosomal instability pathways.
Niv Y, Goel A, Boland CR. Niv Y, et al. Curr Opin Gastroenterol. 2005 Jan;21(1):85-9. Curr Opin Gastroenterol. 2005. PMID: 15687890 Review.
Cited by
- Dietary Emulsifier-Induced Low-Grade Inflammation Promotes Colon Carcinogenesis.
Viennois E, Merlin D, Gewirtz AT, Chassaing B. Viennois E, et al. Cancer Res. 2017 Jan 1;77(1):27-40. doi: 10.1158/0008-5472.CAN-16-1359. Epub 2016 Nov 7. Cancer Res. 2017. PMID: 27821485 Free PMC article. - Microbiota in cancer development and treatment.
Raza MH, Gul K, Arshad A, Riaz N, Waheed U, Rauf A, Aldakheel F, Alduraywish S, Rehman MU, Abdullah M, Arshad M. Raza MH, et al. J Cancer Res Clin Oncol. 2019 Jan;145(1):49-63. doi: 10.1007/s00432-018-2816-0. Epub 2018 Dec 12. J Cancer Res Clin Oncol. 2019. PMID: 30542789 Review. - The role of antioxidants and pro-oxidants in colon cancer.
Stone WL, Krishnan K, Campbell SE, Palau VE. Stone WL, et al. World J Gastrointest Oncol. 2014 Mar 15;6(3):55-66. doi: 10.4251/wjgo.v6.i3.55. World J Gastrointest Oncol. 2014. PMID: 24653795 Free PMC article. Review. - Enterococcus faecalis induces aneuploidy and tetraploidy in colonic epithelial cells through a bystander effect.
Wang X, Allen TD, May RJ, Lightfoot S, Houchen CW, Huycke MM. Wang X, et al. Cancer Res. 2008 Dec 1;68(23):9909-17. doi: 10.1158/0008-5472.CAN-08-1551. Cancer Res. 2008. PMID: 19047172 Free PMC article. - Tumorigenic bacteria in colorectal cancer: mechanisms and treatments.
Li S, Liu J, Zheng X, Ren L, Yang Y, Li W, Fu W, Wang J, Du G. Li S, et al. Cancer Biol Med. 2021 Sep 30;19(2):147-62. doi: 10.20892/j.issn.2095-3941.2020.0651. Online ahead of print. Cancer Biol Med. 2021. PMID: 34586760 Free PMC article. Review.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Molecular Biology Databases
Research Materials