Gastroenterology
Volume 132, Issue 2 , Pages 551-561 , February 2007

Extracellular Superoxide Production by Enterococcus faecalis Promotes Chromosomal Instability in Mammalian Cells

  • Xingmin Wang
  • ,
  • Mark M. Huycke

      Affiliations

    • Corresponding Author InformationAddress reprint requests to: Mark M. Huycke, MD, Medical Service (111), 921 NE 13th Street, Oklahoma City, Oklahoma 73104. fax: (405) 297-5948.

Received 28 July 2006 ,Accepted 19 October 2006.

References 

  1. Colorectal cancer. In: Stewart BW, Kleihues P, eds. World cancer report. Lyon: IARC Press; 2003.
  2. Grady WM. Genomic instability and colon cancer. Cancer Metastasis Rev. 2004;23:11–27
  3. Nowak MA, Komarova NL, Sengupta A, Jallepalli PV, Shih IM, Vogelstein B, et al. The role of chromosomal instability in tumor initiation. Proc Natl Acad Sci U S A. 2002;99:16226–16231
  4. Stoler DL, Chen N, Basik M, Kahlenberg MS, Rodiguez-Bigas MA, Petrelli NJ, et al. The onset and extent of genomic instability in sporadic colorectal tumor progression. Proc Natl Acad Sci U S A. 1999;96:15121–15126
  5. Shih I-M, Zhou W, Goodman SN, Lengauer C, Kinzler KW, Vogelstein B. Evidence that genetic instability occurs at an early stage of colorectal tumorigenesis. Cancer Res. 2001;61:818–822
  6. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nat Med. 2004;10:789–799
  7. Moore WEC, Moore LH. Intestinal floras of populations that have a high risk of colon cancer. Appl Environ Microbiol. 1995;61:3202–3207
  8. McGarr SE, Ridlon JM, Hylemon PB. Diet, anaerobic bacterial metabolism, and colon cancer: a review of the literature. J Clin Gastroenterol. 2005;39:98–109
  9. Augenlicht LH, Mariadason JM, Wilson A, Arango D, Yang W, Heerdt BG, et al. Short chain fatty acids and colon cancer. J Nutr. 2002;132:3804S–3808S
  10. Huycke MM, Moore D, Shepard L, Joyce W, Wise P, Kotake Y, et al. Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol Microbiol. 2001;42:729–740
  11. Huycke MM. Physiology of enterococci. In:  Gilmore MS editors. Enterococci: pathogenesis, molecular biology and antibiotic resistance. Washington, DC: ASM Press; 2002;p. 133–175
  12. Winters MD, Schlinke TL, Joyce WA, Glore WR, Huycke MM. Prospective case–cohort control study of intestinal colonization with enterococci that produce extracellular superoxide and the risk for colorectal adenomas or cancer. Am J Gastroenterol. 1998;93:2491–2500
  13. Huycke MM, Moore DR. In vivo production of hydroxyl radical by Enterococcus faecalis colonizing the intestinal tract using aromatic hydroxylation. Free Radic Biol Med. 2002;33:818–826
  14. Huycke MM, Abrams V, Moore DR. Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA. Carcinogenesis. 2002;23:529–536
  15. Zhou H, Ivanov VN, Gillespie J, Geard CR, Amundson SA, Brenner DJ, et al. Mechanism of radiation-induced bystander effect: role of the cyclooxygenase-2 signaling pathway. Proc Natl Acad Sci U S A. 2005;102:14641–14646
  16. Little JB. Genomic instability and bystander effects: a historical perspective. Oncogene. 2003;22:6978–6987
  17. Lorimore SA, Wright EG. Radiation-induced genomic instability and bystander effects: related inflammatory-type responses to radiation-induced stress and injury? A review. Int J Radiat Biol. 2003;79:15–25
  18. Emerit I. Reactive oxygen species, chromosome mutation, and cancer: possible role of clastogenic factors in carcinogenesis. Free Radic Biol Med. 1994;16:99–109
  19. Huycke MM, Joyce W, Wack MF. Augmented production of extracellular superoxide production by blood isolates of Enterococcus faecalis. J Infect Dis. 1996;173:743–746
  20. Korshunov S, Imlay JA. Detection and quantification of superoxide formed within the periplasm of Escherichia coli. J Bacteriol. 2006;188:6326–6334
  21. McGuinness SM, Shibuya ML, Ueno AM, Vannais DB, Waldren CA. Mutant quantity and quality in mammalian cells (AL) exposed to cesium-137 gamma radiation: effect of caffeine. Radiat Res. 1995;142:247–255
  22. Waldren CA, Vannais DB, Ueno AM. A role for long-lived radicals (LLR) in radiation-induced mutation and persistent chromosomal instability: counteraction by ascorbate and RibCys but not DMSO. Mutat Res. 2004;551:255–265
  23. Kraemer SM, Vannais DB, Kronenberg A, Ueno A, Waldren CA. Gamma-ray mutagenesis studies in a new human–hamster hybrid, ALCD59+/-, which has two human chromosomes 11 but is hemizygous for the CD59 gene. Radiat Res. 2001;156:10–19
  24. Buettner GR. The pecking order of free radicals and antioxidants: lipid peroxidation, α-tocopherol, and ascorbate. Arch Biochem Biophys. 1993;300:535–543
  25. Hensley HH, Chang WC, Clapper ML. Detection and volume determination of colonic tumors in Min mice by magnetic resonance micro-imaging. Magn Reson Med. 2004;524–529
  26. Jiang Q, Elson-Schwab I, Courtemanche C, Ames BN. γ-Tocopherol and its major metabolite, in contrast to α-tocopherol, inhibit cyclooxygenase activity in macrophages and epithelial cells. Proc Natl Acad Sci U S A. 2000;97:11494–11499
  27. Marnett LJ, DuBois RN. COX-2: a target for colon cancer prevention. Annu Rev Pharmacol Toxicol. 2002;42:55–80
  28. Kraehenbuhl J-P, Neutra MR. Epithelial M cells: differentiation and function. Annu Rev Cell Dev Biol. 2000;16:301–332
  29. Gentry-Weeks CR, Karkhoff-Schweizer R, Pikis A, Estay M, Keith JM. Survival of Enterococcus faecalis in mouse peritoneal macrophages. Infect Immun. 1999;67:2160–2165
  30. Saran M, Bors W. Oxygen radicals acting as chemical messengers: a hypothesis. Free Radic Res Commun. 1989;7:213–220
  31. Balish E, Warner T. Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol. 2002;160:2253–2257
  32. Kim SC, Tonkonogy SL, Albright CA, Tsang J, Balish EJ, Braun J, et al. Variable phenotypes of enterocolitis in IL-10 deficient mice monoassociated with two different commensal bacteria. Gastroenterology. 2005;128:891–906
  33. Marnett LJ, Riggins JN, West JD. Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein. J Clin Invest. 2003;111:583–593
  34. Macarthur M, Hold GL, El-Omar EM. Inflammation and Cancer II (Role of chronic inflammation and cytokine gene polymorphisms in the pathogenesis of gastrointestinal malignancy). Am J Physiol Gastrointest Liver Physiol. 2004;286:G515–G520
  35. Hussain Z, Kuhn M, Lannigan R, Austin TW. Microbiological investigation of an outbreak of bacteraemia due to Streptococcus faecalis in an intensive care unit. J Hosp Infect. 1988;12:263–271
  36. Wells CL, Erlandsen SL. Localization of translocating Escherichia coli, Proteus mirabilis, and Enterococcus faecalis within cecal and colonic tissues of monoassociated mice. Infect Immun. 1991;59:4693–4697
  37. Dukes C, Bussey HJR. The number of lymphoid follicles of the human large intestine. J Pathol. 1926;29:111–116
  38. Didierlaurent A, Sirard J-C, Kraehenbuhl J-P, Neutra MR. How the gut senses its content. Cell Microbiol. 2002;4:61–72
  39. Plackett TP, Boehmer ED, Faunce DE, Kovacs EJ. Aging and innate immune cells. J Leukoc Biol. 2004;76:291–299
  40. Oshima M, Dinchuk JE, Kargman SL, Oshima H, Hancock B, Kwong E, et al. Suppression of intestinal polyposis in ApcΔ716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell. 1996;87:803–809
  41. Chulada PC, Thompson MB, Mahler JF, Doyle CM, Gaul BW, Lee C, et al. Genetic disruption of Ptgs-1, as well as of Ptgs-2, reduces intestinal tumorigenesis in Min mice. Cancer Res. 2000;60:4705–4708
  42. Bamba H, Ota S, Kato A, Adachi A, Itoyama S, Matsuaki F. High expression of cyclooxygenase-2 in macrophages of human colonic adenoma. Int J Cancer. 1999;83:470–475
  43. Chapple KS, Cartwright EJ, Hawcroft G, Tisbury A, Bonifer C, Scott N, et al. Localization of cyclooxygenase-2 in human sporadic colorectal adenomas. Am J Pathol. 2000;156:545–553
  44. Shih I-M, Wang T-L, Traverso G, Romans K, Hamilton SR, Ben-Sasson S, et al. Top-down morphogenesis of colorectal tumors. Proc Natl Acad Sci U S A. 2001;98:2640–2645
  45. Wang D, Dubois RN. Prostaglandins and cancer. Gut. 2006;55:115–122
  46. Landino LM, Crews BC, Gierse JK, Hauser SD, Marnett LJ. Mutational analysis of the role of the distal histidine and glutamine residues of prostaglandin-endoperoxide synthase-2 in peroxidase catalysis, hydroperoxide reduction, and cyclooxygenase activation. J Biol Chem. 1997;272:21565–21574
  47. Salisbury BA, Pungliya M, Choi JY, Jiang R, Sun XJ, Stephens JC. SNP and haplotype variation in the human genome. Mutat Res. 2003;526:53–61
  48. Popov SG, Villasmil R, Bernardi J, Grene E, Cardwell J, Wu A, et al. Lethal toxin of Bacillus anthracis causes apoptosis of macrophages. Biochem Biophys Res Commun. 2002;293:349–355
  49. Greenberg ER, Baron JA, Tosteson TD, Freeman DHJ, Beck GJ, Bond JH, et al. A clinical trial of antioxidant vitamins to prevent colorectal adenoma. N Engl J Med. 1994;331:141–147
  50. Jacobs EJ, Connell CJ, Patel AV, Chao A, Rodriguez C, Seymour J, et al. Vitamin C and vitamin E supplement use and colorectal cancer mortality in a large American Cancer Society cohort. Cancer Epidemiol Biomarkers Prev. 2001;10:17–23
  51. Rhee SH, Hwang D. Murine TOLL-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NF kappa B and expression of the inducible cyclooxygenase. J Biol Chem. 2000;275:34035–34040
  52. Fukata M, Chen A, Klepper A, Krishnareddy S, Vamadevan AS, Thomas LS, et al. Cox-2 is regulated by Toll-like receptor-4 (TLR4) signaling: role in proliferation and apoptosis in the intestine. Gastroenterology. 2006;131:862–877
  53. Oshima H, Oshima M, Inaba K, Taketo MM. Hyperplastic gastric tumors induced by activated macrophages in COX-2/mPGES-1 transgenic mice. EMBO J. 2004;23:1669–1678
  54. Hwang D. Modulation of the expression of cyclooxygenase-2 by fatty acids mediated through toll-like receptor 4-derived signaling pathways. Faseb J. 2001;15:2556–2564
  55. Lien E, Means TK, Heine H, Yoshimura A, Kusumoto S, Fukase K, et al. Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide. J Clin Invest. 2000;105:497–504
  56. Nougayrede JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 2006;313:848–851

 Supported by Department of Veterans Affairs Merit Review Program (to M.M.H.) and the Frances Duffy Endowment.

PII: S0016-5085(06)02521-2

doi: 10.1053/j.gastro.2006.11.040

Gastroenterology
Volume 132, Issue 2 , Pages 551-561 , February 2007