Enterococcus faecalis Infection Causes Inflammation, Intracellular Oxphos-Independent ROS Production, and DNA Damage in Human Gastric Cancer Cells

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Strickertsson, Jesper A B ^a,b   Desler, Claus ^b   Martin Bertelsen, Tomas ^c   Machado, Ana Manuel Dantas ^b   Wadstrøm, Torkel ^d   Winther, Ole ^c,e   Rasmussen, Lene Juel ^b   Friis Hansen, Lennart ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d LUND UNIVERSITY   (Sweden)

^e TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ARTICLE; BACTERIAL VIABILITY; CANCER CELL CULTURE; CELL CYCLE REGULATION; CELL GROWTH; CELL LYSATE; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; ENTEROCOCCAL INFECTION; ENTEROCOCCUS FAECALIS; GENE CONTROL; GENE EXPRESSION REGULATION; GENE MUTATION; GENE SEQUENCE; GENETIC CODE; GENETIC STABILITY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INFLAMMATION; INFLAMMATORY CELL; INTRACELLULAR SIGNALING; MITOCHONDRIAL GENETICS; MITOCHONDRIAL GENOME; MITOCHONDRIAL RESPIRATION; MUCOSA CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; STOMACH CARCINOMA; STOMACH MUCOSA; BIOLOGICAL MODEL; CELL CYCLE; CELL PROLIFERATION; CLUSTER ANALYSIS; COMPLICATION; DNA REPAIR; GENE EXPRESSION PROFILING; GENETICS; GRAM POSITIVE INFECTION; INTRACELLULAR SPACE; METABOLISM; MICROBIOLOGY; MITOCHONDRION; PATHOLOGY; SIGNAL TRANSDUCTION; STOMACH TUMOR; TUMOR CELL LINE;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS;

CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CLUSTER ANALYSIS; DNA DAMAGE; DNA REPAIR; ENTEROCOCCUS FAECALIS; GASTRIC MUCOSA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; INFLAMMATION; INTRACELLULAR SPACE; MITOCHONDRIA; MODELS, BIOLOGICAL; NF-KAPPA B; OXIDATIVE PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; SUPEROXIDES;

EID: 84876988604     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063147     Document Type: Article

References (68)

1. Parkin DM, Bray F, Ferlay J, Pisani P, (2005) Global cancer statistics, 2002. CA Cancer J Clin 55: 74-108.
2. Fox JG, Wang TC, (2007) Inflammation, atrophy, and gastric cancer. J Clin Invest 117: 60-69.
3. Mantovani A, Allavena P, Sica A, Balkwill F, (2008) Cancer-related inflammation. Nature 454: 436-444.
4. Hussain SP, Harris CC, (2007) Inflammation and cancer: an ancient link with novel potentials. Int J Cancer 121: 2373-2380.
5. Coussens LM, Werb Z, (2002) Inflammation and cancer. Nature 420: 860-867.
6. Maeda S, Omata M, (2008) Inflammation and cancer: role of nuclear factor-kappaB activation. Cancer Sci 99: 836-842.
7. Bellance N, Lestienne P, Rossignol R, (2009) Mitochondria: from bioenergetics to the metabolic regulation of carcinogenesis. Front Biosci 14: 4015-4034.
8. Brown DI, Griendling KK, (2009) Nox proteins in signal transduction. Free Radic Biol Med 47: 1239-1253.
9. Thannickal VJ, Fanburg BL, (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279: L1005-1028.
10. Huang JQ, Sridhar S, Chen Y, Hunt RH, (1998) Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer. Gastroenterology 114: 1169-1179.
11. Amieva MR, El-Omar EM, (2008) Host-bacterial interactions in Helicobacter pylori infection. Gastroenterology 134: 306-323.
12. Hansson LE, (2000) Risk of stomach cancer in patients with peptic ulcer disease. World J Surg 24: 315-320.
13. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, et al. (2001) Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 345: 784-789.
14. Argent RH, Thomas RJ, Aviles-Jimenez F, Letley DP, Limb MC, et al. (2008) Toxigenic Helicobacter pylori infection precedes gastric hypochlorhydria in cancer relatives, and H. pylori virulence evolves in these families. Clin Cancer Res 14: 2227-2235.
15. Dicksved J, Lindberg M, Rosenquist M, Enroth H, Jansson JK, et al. (2009) Molecular characterization of the stomach microbiota in patients with gastric cancer and in controls. J Med Microbiol 58: 509-516.
16. Huycke MM, Moore D, Joyce W, Wise P, Shepard L, et al. (2001) Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol Microbiol 42: 729-740.
17. Friis-Hansen L, (2006) Achlorhydria is associated with gastric microbial overgrowth and development of cancer: lessons learned from the gastrin knockout mouse. Scand J Clin Lab Invest 66: 607-621.
18. Zavros Y, Eaton KA, Kang W, Rathinavelu S, Katukuri V, et al. (2005) Chronic gastritis in the hypochlorhydric gastrin-deficient mouse progresses to adenocarcinoma. Oncogene 24: 2354-2366.
19. Fisher K, Phillips C, (2009) The ecology, epidemiology and virulence of Enterococcus. Microbiology 155: 1749-1757.
20. Friis-Hansen L, Rieneck K, Nilsson HO, Wadstrom T, Rehfeld JF, (2006) Gastric inflammation, metaplasia, and tumor development in gastrin-deficient mice. Gastroenterology 131: 246-258.
21. Pillar CM, Gilmore MS, (2004) Enterococcal virulence - pathogenicity island of E. Faecalis. Front Biosci 9: 2335-2346.
22. Balamurugan R, Rajendiran E, George S, Samuel GV, Ramakrishna BS, (2008) Real-time polymerase chain reaction quantification of specific butyrate-producing bacteria, Desulfovibrio and Enterococcus faecalis in the feces of patients with colorectal cancer. J Gastroenterol Hepatol 23: 1298-1303.
23. Boonanantanasarn K, Gill AL, Yap Y, Jayaprakash V, Sullivan MA,et al. (2012) Enterococcus faecalis Enhances Cell Proliferation Through Hydrogen Peroxide Mediated Epidermal Growth Factor Receptor Activation. Infect Immun.
24. Wang X, Allen TD, May RJ, Lightfoot S, Houchen CW, et al. (2008) Enterococcus faecalis induces aneuploidy and tetraploidy in colonic epithelial cells through a bystander effect. Cancer Res 68: 9909-9917.
25. Huycke MM, Joyce W, Wack MF, (1996) Augmented production of extracellular superoxide by blood isolates of Enterococcus faecalis. J Infect Dis 173: 743-746.
26. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
27. R_Development_Core_Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/. Accessed 2012 Nov 22.
28. Wu Z, Irizarry RA, Gentleman R, Martinez-Murillo., Spencer F, (2004) A Model Based backgound adjustment for oligonucleotide expression arrays. Journal of the American Statistical Association 99: 909-917.
29. Rozen S, Skaletsky H, (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
30. Luo W, Friedman MS, Shedden K, Hankenson KD, Woolf PJ, (2009) GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics 10: 161.
31. Liberzon A, Subramanian A, Pinchback R, Thorvaldsdottir H, Tamayo P, et al. (2011) Molecular signatures database (MSigDB) 3.0. Bioinformatics 27: 1739-1740.
32. Zavros Y, Rieder G, Ferguson A, Samuelson LC, Merchant JL, (2002) Genetic or chemical hypochlorhydria is associated with inflammation that modulates parietal and G-cell populations in mice. Gastroenterology 122: 119-133.
33. Huycke MM, Abrams V, Moore DR, (2002) Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA. Carcinogenesis 23: 529-536.
34. Spooner R, Yilmaz O, (2011) The role of reactive-oxygen-species in microbial persistence and inflammation. Int J Mol Sci 12: 334-352.
35. Ding SZ, Minohara Y, Fan XJ, Wang J, Reyes VE, et al. (2007) Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect Immun 75: 4030-4039.
36. Machado AM, Figueiredo C, Touati E, Maximo V, Sousa S, et al. (2009) Helicobacter pylori infection induces genetic instability of nuclear and mitochondrial DNA in gastric cells. Clin Cancer Res 15: 2995-3002.
37. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550.
38. Gargalovic PS, Imura M, Zhang B, Gharavi NM, Clark MJ, et al. (2006) Identification of inflammatory gene modules based on variations of human endothelial cell responses to oxidized lipids. Proc Natl Acad Sci U S A 103: 12741-12746.
39. Adibhatla RM, Hatcher JF, (2010) Lipid oxidation and peroxidation in CNS health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 12: 125-169.
40. Bulua AC, Simon A, Maddipati R, Pelletier M, Park H, et al. (2011) Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J Exp Med 208: 519-533.
41. Karin M, Cao Y, Greten FR, Li ZW, (2002) NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2: 301-310.
42. Takaesu G, Ninomiya-Tsuji J, Kishida S, Li X, Stark GR, et al. (2001) Interleukin-1 (IL-1) receptor-associated kinase leads to activation of TAK1 by inducing TAB2 translocation in the IL-1 signaling pathway. Mol Cell Biol 21: 2475-2484.
43. El-Omar EM, (2001) The importance of interleukin 1beta in Helicobacter pylori associated disease. Gut 48: 743-747.
44. Kido S, Kitadai Y, Hattori N, Haruma K, Kido T, et al. (2001) Interleukin 8 and vascular endothelial growth factor - prognostic factors in human gastric carcinomas? Eur J Cancer 37: 1482-1487.
45. Mueller A, Merrell DS, Grimm J, Falkow S, (2004) Profiling of microdissected gastric epithelial cells reveals a cell type-specific response to Helicobacter pylori infection. Gastroenterology 127: 1446-1462.
46. Langowski JL, Zhang X, Wu L, Mattson JD, Chen T, et al. (2006) IL-23 promotes tumour incidence and growth. Nature 442: 461-465.
47. Caruso R, Pallone F, Monteleone G, (2007) Emerging role of IL-23/IL-17 axis in H pylori-associated pathology. World J Gastroenterol 13: 5547-5551.
48. Howlett M, Judd LM, Jenkins B, La Gruta NL, Grail D, et al. (2005) Differential regulation of gastric tumor growth by cytokines that signal exclusively through the coreceptor gp130. Gastroenterology 129: 1005-1018.
49. Howlett M, Chalinor HV, Buzzelli JN, Nguyen N, van Driel IR, et al. (2012) IL-11 is a parietal cell cytokine that induces atrophic gastritis. Gut 61: 1398-1409.
50. Park DI, Park SH, Kim SH, Kim JW, Cho YK, et al. (2005) Effect of Helicobacter pylori infection on the expression of DNA mismatch repair protein. Helicobacter 10: 179-184.
51. Kim JJ, Tao H, Carloni E, Leung WK, Graham DY, et al. (2002) Helicobacter pylori impairs DNA mismatch repair in gastric epithelial cells. Gastroenterology 123: 542-553.
52. Lee W, Lim S, Son HH, Bae KS, (2004) Sonicated extract of Enterococcus faecalis induces irreversible cell cycle arrest in phytohemagglutinin-activated human lymphocytes. J Endod 30: 209-212.
53. Judd LM, Andringa A, Rubio CA, Spicer Z, Shull GE, et al. (2005) Gastric achlorhydria in H/K-ATPase-deficient (Atp4a(-/-)) mice causes severe hyperplasia, mucocystic metaplasia and upregulation of growth factors. J Gastroenterol Hepatol 20: 1266-1278.
54. Kang W, Rathinavelu S, Samuelson LC, Merchant JL, (2005) Interferon gamma induction of gastric mucous neck cell hypertrophy. Lab Invest 85: 702-715.
55. Andersson AF, Lindberg M, Jakobsson H, Backhed F, Nyren P, et al. (2008) Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 3: e2836.
56. Kamada T, Hata J, Sugiu K, Kusunoki H, Ito M, et al. (2005) Clinical features of gastric cancer discovered after successful eradication of Helicobacter pylori: results from a 9-year prospective follow-up study in Japan. Aliment Pharmacol Ther 21: 1121-1126.
57. Correa P, Haenszel W, Cuello C, Zavala D, Fontham E, et al. (1990) Gastric precancerous process in a high risk population: cohort follow-up. Cancer Res 50: 4737-4740.
58. Nauseef WM, (2008) Biological roles for the NOX family NADPH oxidases. J Biol Chem 283: 16961-16965.
59. Bedard K, Krause KH, (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313.
60. Salles N, Szanto I, Herrmann F, Armenian B, Stumm M, et al. (2005) Expression of mRNA for ROS-generating NADPH oxidases in the aging stomach. Exp Gerontol 40: 353-357.
61. Hirano T, (2008) Repair system of 7, 8-dihydro-8-oxoguanine as a defense line against carcinogenesis. J Radiat Res (Tokyo) 49: 329-340.
62. Davies GR, Simmonds NJ, Stevens TR, Sheaff MT, Banatvala N, et al. (1994) Helicobacter pylori stimulates antral mucosal reactive oxygen metabolite production in vivo. Gut 35: 179-185.
63. Handa O, Naito Y, Yoshikawa T, (2011) Redox biology and gastric carcinogenesis: the role of Helicobacter pylori. Redox Rep 16: 1-7.
64. Rokutan K, Kawahara T, Kuwano Y, Tominaga K, Sekiyama A, et al. (2006) NADPH oxidases in the gastrointestinal tract: a potential role of Nox1 in innate immune response and carcinogenesis. Antioxid Redox Signal 8: 1573-1582.
65. Maximo V, Soares P, Seruca R, Rocha AS, Castro P, et al. (2001) Microsatellite instability, mitochondrial DNA large deletions, and mitochondrial DNA mutations in gastric carcinoma. Genes Chromosomes Cancer 32: 136-143.
66. Carew JS, Huang P, (2002) Mitochondrial defects in cancer. Mol Cancer 1: 9.
67. Karin M, (2006) Nuclear factor-kappaB in cancer development and progression. Nature 441: 431-436.
68. Yamaoka Y, (2010) Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol 7: 629-641.