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Enterobacter Strains Might Promote Colon Cancer

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Abstract

Many studies have been performed to determine the interaction between bacterial species and cancer. However, there has been no attempts to demonstrate a possible relationship between Enterobacter spp. and colon cancer so far. Therefore, in the present study, it is aimed to investigate the effects of Enterobacter strains on colon cancer. Bacterial proteins were isolated from 11 Enterobacter spp., one Morganella morganii, and one Escherichia coli strains, and applied onto NCM460 (Incell) and CRL1790 (ATCC) cell lines. Cell viability and proliferation were determined in MTS assay. Flow Cytometry was used to detect CD24 level and apoptosis. Real-Time PCR studies were performed to determine NFKB and Bcl2 expression. Graphpad Software was used for statistical analysis. The results showed that proteins, isolated from the Enterobacter spp., have significantly increased cell viability and proliferation, while decreasing the apoptosis of the cell lines tested. The data in the present study indicated that Enterobacter strains might promote colon cancer. Moreover, Enterobacter spp. could be a clinically important factor for colon cancer initiation and progression. Studies can be extended on animal models in order to develop new strategies for treatment.

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References

  1. Ahmed S, Macfarlane GT, Fite A, McBain AJ, Gilbert P, Macfarlane S (2007) Mucosa-associated bacterial diversity in relation to human terminal ileum and colonic biopsy samples. Appl Environ Microb 73(22):7435–7442. doi:10.1128/Aem.01143-07

    Article  CAS  Google Scholar 

  2. Balish E, Warner T (2002) Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol 160(6):2253–2257

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Biarc J, Nguyen IS, Pini A, Gosse F, Richert S, Thierse D, Van DA, Leize-Wagner E, Raul F, Klein JP, Scholler-Guinard M (2004) Carcinogenic properties of proteins with pro-inflammatory activity from Streptococcus infantarius (formerly S. bovis). Carcinogenesis 25(8):1477–1484. doi:10.1093/carcin/bgh091

    Article  CAS  PubMed  Google Scholar 

  4. Breathnach SARA, Shad S, Jownally MS, Law R, Chin CP, Kaufmann EM, Smith JE (2006) An outbreak of wound infection in cardiac surgery patients caused by Enterobacter cloacae arising from cardioplegia ice. J Hosp Infect 64:124–128

    Article  CAS  PubMed  Google Scholar 

  5. Bronner PMCC, Reed CJ, Furth EE (1995) The Bcl2 protooncogene and the gastrointestinal epithelial tumor progression model. AJP January 146(1):20–26

    CAS  Google Scholar 

  6. Buyer JS (2002) Rapid sample processing and fast gas chromatography for identification of bacteria by fatty acid analysis. J Microbiol Meth 51(2):209–215. doi:10.1016/S0167-7012(02)00081-7

    Article  CAS  Google Scholar 

  7. Choi YXH, Lee S, Park MS, Kim JW, Kim H, Kim S (2006) Enhanced CD24 expression in colorectal cancer correlates with prognostic factors. Korean J Pathol 40:103–111

    Google Scholar 

  8. Cotter TG (2009) Apoptosis and cancer: the genesis of a research field. Nat Rev Cancer 9(7):501–507

    Article  CAS  PubMed  Google Scholar 

  9. Datasheet BT FITC Annexin V Apoptosis Detection Kit 1

  10. Dolcet XLD, Pallares J, Matras-Guiu X (2005) NFKB in development and progression of human cancer. Virchows Arch 446:475–482

    Article  CAS  PubMed  Google Scholar 

  11. Faherty CS, Maurelli AT (2008) Staying alive: bacterial inhibition of apoptosis during infection. Trends Microbiol 16(4):173–180

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Grimont F, Grimont PA (2006) The genus Enterobacter. The prokaryotes. Springer, New York, pp 197–214

    Chapter  Google Scholar 

  13. Hao LW, Lee YK (2004) Microflora of the gastrointestinal tract: a review. Methods in molecular biology, public health microbiology methods and protocols, vol 268. Humana Press, Totowa

    Google Scholar 

  14. Higgins DG, Bleasby AJ, Fuchs R (1992) CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci CABIOS 8(2):189–191

    CAS  PubMed  Google Scholar 

  15. Huerta S, Goulet EJ, Livingston EH (2006) Colon cancer and apoptosis. Am J Surg 191(4):517–526

    Article  CAS  PubMed  Google Scholar 

  16. Felsenstein J (1989) PHYLIP-phylogeny inference package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  17. Kojima M, Morisaki T, Sasaki N, Nakano K, Mibu R, Tanaka M, Katano M (2004) Increased nuclear factor-kB activation in human colorectal carcinoma and its correlation with tumor progression. Anticancer Res 24(2B):675–682

    CAS  PubMed  Google Scholar 

  18. Laurila AL, Anttila T, Laara E, Bloigu A, Virtamo J, Albanes D, Leinonen M, Saikku P (1997) Serological evidence of an association between Chlamydia pneumoniae infection and lung cancer. Int J Cancer 74(1):31–34. doi:10.1002/(Sici)1097-0215(19970220)74

    Article  CAS  PubMed  Google Scholar 

  19. Lax AJ (2005) Bacterial toxins and cancer: a case to answer? Nat Rev Microbiol 3(4):343–349. doi:10.1038/Nrmicro1130

    Article  CAS  PubMed  Google Scholar 

  20. Lax AJ, Thomas W (2002) How bacteria could cause cancer: one step at a time. Trends Microbiol 10(6):293–299. doi:10.1016/S0966-842x(02)02360-0

    Article  CAS  PubMed  Google Scholar 

  21. Levine DS, Haggitt RC (1989) Normal histology of the colon. Am J Surg Pathol 13(11):966–984. doi:10.1097/00000478-198911000-00008

    Article  CAS  PubMed  Google Scholar 

  22. Lu H, Ouyang W, Huang C (2006) Inflammation, a key event in cancer development. Mol Cancer Res 4(4):221–233

    Article  PubMed  Google Scholar 

  23. Martin MHCJ, Hart AC, Mpofu C, Nayar M, Singh R, Englyst H, Williams FH, Rhodes MJ (2004) Enhanced Esherichia coli adherence and invasion in Crohn’s disease and colon cancer. Gastroenterology 127:80–93

    Article  CAS  PubMed  Google Scholar 

  24. Newman JV, Kosaka T, Sheppard BJ, Fox JG, Schauer DB (2001) Bacterial infection promotes colon tumorigenesis in Apc(Min/+) mice. J Infect Dis 184(2):227–230. doi:10.1086/321998

    Article  CAS  PubMed  Google Scholar 

  25. Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, Sibley RK (1991) Helicobacter pylori infection and the risk of gastric carcinoma. New Engl J Med 325(16):1127–1131. doi:10.1056/Nejm199110173251603

    Article  CAS  PubMed  Google Scholar 

  26. Pincus HD (2006) Microbial identification using the Biomerieux Vitek 2 system. Encyclopedia of rapid microbiological methods. Parenteral Drug Association, Bethesda

    Google Scholar 

  27. Riss TL, Moravec RA (1992) Comparison of MTT, XTT and a novel tetrazolium compound for MTS for in vitro proliferation and chemosensitivity assays. Mol Biol Cell 3:184

    Google Scholar 

  28. Rupnarain C, Dlamini Z, Naicker S, Bhoola K (2004) Colon cancer: genomics and apoptotic events. Biol Chem 385(6):449–464

    Article  CAS  PubMed  Google Scholar 

  29. Sagiv E, Memeo L, Karin A, Kazanov D, Jacob-Hirsch J, Mansukhani M, Rechavi G, Hibshoosh H, Arber N (2006) CD24 is a new oncogene, early at the multistep process of colorectal cancer carcinogenesis. Gastroenterology 131(2):630–639

    Article  CAS  PubMed  Google Scholar 

  30. Sanders W, Sanders CC (1997) Enterobacter spp.: pathogens poised to flourish at the turn of the century. Clin Microbiol Rev 10(2):220–241

    PubMed Central  PubMed  Google Scholar 

  31. Shishodia S, Aggarwal BB (2004) Nuclear factor-κB: a friend or a foe in cancer? Biochem Pharmacol 68(6):1071–1080

    Article  CAS  PubMed  Google Scholar 

  32. Sinicrope FA, Hart J, Michelassi F, Lee JJ (1995) Prognostic value of bcl-2 oncoprotein expression in stage II colon carcinoma. Clin Cancer Res 1(10):1103–1110

    CAS  PubMed  Google Scholar 

  33. Terzić J, Grivennikov S, Karin E, Karin M (2010) Inflammation and colon cancer. Gastroenterology 138(6):2101–2114

    Article  PubMed  Google Scholar 

  34. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Wang S, Liu Z, Wang L, Zhang X (2009) NF-kappaB signaling pathway, inflammation and colorectal cancer. Cell Mol Immunol 6(5):327–334

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16s ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703

    CAS  PubMed Central  PubMed  Google Scholar 

  37. Wilkins A, Kemp K, Ginty M, Hares K, Mallam E, Scolding N (2009) Human bone marrow-derived mesenchymal stem cells secrete brain-derived neurotrophic factor which promotes neuronal survival in vitro. Stem Cell Res 3(1):63–70

    Article  CAS  PubMed  Google Scholar 

  38. Wong RSY (2011) Apoptosis in cancer: from pathogenesis to treatment. J Exp Clin Cancer Res. doi:10.1186/1756-9966-30-87

    Google Scholar 

  39. Wright SC, Zhong J, Larrick JW (1994) Inhibition of apoptosis as a mechanism of tumor promotion. Faseb J 8(9):654–660

    CAS  PubMed  Google Scholar 

  40. Yalvac ME, Yarat A, Mercan D, Rizvanov AA, Palotas A, Sahin F (2013) Characterization of the secretome of human tooth germ stem cells (hTGSCs) reveals neuro-protection by fine-tuning micro-environment. Brain Behav Immun 32:122–130

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are thankful to Ali Umman Doğan, Nilsu Atay, Assoc. Prof. Dr. Dilek Telci, Prof. Dr. Ufuk Hasdemir, Prof. Dr. Necmettin Sökücü, Prof. Dr. Adile Çevikbaş, and Assoc. Prof. Dr. Ümran Soyoğul Gürer for their help and support. The authors are grateful to INCELL Corporation, LLC for providing NCM460 Cell Lines. The authors also would like to thank Yeditepe University, Genetics and Bioengineering Department and Istanbul Technical University, Scientific Research Foundations.

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Correspondence to Fikrettin Şahin.

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Yurdakul, D., Yazgan-Karataş, A. & Şahin, F. Enterobacter Strains Might Promote Colon Cancer. Curr Microbiol 71, 403–411 (2015). https://doi.org/10.1007/s00284-015-0867-x

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