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Molecular Cancer
Published in: Molecular Cancer 1/2010

Open Access 01-12-2010 | Research

Molecular detection, quantification, and isolation of Streptococcus gallolyticus bacteria colonizing colorectal tumors: inflammation-driven potential of carcinogenesis via IL-1, COX-2, and IL-8

Authors: Ahmed S Abdulamir, Rand R Hafidh, Fatimah Abu Bakar

Published in: Molecular Cancer | Issue 1/2010

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Abstract

Background

Colorectal cancer (CRC) has long been associated with bacteremia and/or endocarditis by Streptococcus gallolyticus member bacteria (SGMB) but the direct colonization of SGMB along with its molecular carcinogenic role, if any, has not been investigated. We assessed the colonization of SGMB in CRC patients with history of bacteremia (CRC-w/bac) and without history of bacteremia (CRC-wo/bac) by isolating SGMB from feces, mucosal surfaces of colorectum, and colorectal tissues and detecting SGMB DNA, via PCR and in situ hybridization (ISH) assays targeting SodA gene in colorectal tissues. Moreover, mRNA of IL1, IL-8, COX-2, IFN-γ, c-Myc, and Bcl-2 in colorectal tissues of studied groups was assessed via ISH and RT-PCR.

Results

SGMB were found to be remarkably isolated in tumorous (TU) and non-tumorous (NTU) tissues of CRC-w/bac, 20.5% and 17.3%, and CRC-wo/bac, 12.8% and 11.5%, respectively while only 2% of control tissues revealed SGMB (P < 0.05); such contrast was not found in mucosal and fecal isolation of SGMB. The positive detection of SGMB DNA in TU and NTU of CRC-w/bac and CRC-wo/bac via PCR, 48.7%, 35.9%, 32.7%, and 23%, respectively, and ISH, 46.1%, 30.7%, 28.8%, and 17.3%, respectively, was higher than in control tissues, 4 and 2%, respectively (P < 0.05). SGMB count measured via quantitative PCR of SGMB DNA in terms of copy number (CN), in TU and NTU of CRC-w/bac and CRC-wo/bac, 2.96-4.72, 1.29-2.81, 2.16-2.92, and 0.67-2.07 log10 CN/g respectively, showed higher colonization in TU than in NTU and in CRC-w/bac than in CRC-wo/bac (P < 0.05). The PCR-based mRNA ratio and ISH-based percentage of positively stained cells of IL-1, 1.77 and 70.3%, COX-2, 1.63 and 44.8%, and IL-8, 1.73 and 70.3%, respectively, rather than IFN-γ, c-Myc, and Bcl-2, were higher in SGMB positive patients than in control or SGMB negative patients (P < 0.05).

Conclusions

The current study indicated that colorectal cancer is remarkably associated with SGMB; moreover, molecular detection of SGMB in CRC was superior to link SGMB with CRC tumors highlighting a possible direct and active role of SGMB in CRC development through most probably inflammation-based sequel of tumor development or propagation via, but not limited to, IL-1, COX-2, and IL-8.
Appendix
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Literature
1.
Triantafillidis JK, Nasioulas G, Kosmidis PA: Colorectal cancer and inflammatory bowel disease: epidemiology, risk factors, mechanisms of carcinogenesis and prevention strategies. Anticancer Res. 2009, 29 (7): 2727-2737.PubMed
2.
Ablashi DV, Chatlynne LG, Whitman JE, Cesarman E: Spectrum of Kaposi's sarcoma-associated herpesvirus, or human herpesvirus 8, diseases. Clin Microbiol Rev. 2002, 15 (3): 439-464. 10.1128/CMR.15.3.439-464.2002PubMedCentralCrossRefPubMed
3.
Boshoff C, Weiss R: AIDS-related malignancies. Nat Rev Cancer. 2002, 2 (5): 373-382. 10.1038/nrc797CrossRefPubMed
4.
5.
Malfertheiner P, Sipponen P, Naumann M, Moayyedi P, Megraud F, Xiao SD, Sugano K, Nyren O: Helicobacter pylori eradication has the potential to prevent gastric cancer: a state-of-the-art critique. Am J Gastroenterol. 2005, 100 (9): 2100-2115. 10.1111/j.1572-0241.2005.41688.xCrossRefPubMed
6.
Wilson WR, Thompson RL, Wilkowske CJ, Washington JA, Giuliani ER, Geraci JE: Short-term therapy for streptococcal infective endocarditis. Combined intramuscular administration of penicillin and streptomycin. JAMA. 1981, 245 (4): 360-363. 10.1001/jama.245.4.360CrossRefPubMed
7.
Reynolds JG, Silva E, McCormack WM: Association of Streptococcus bovis bacteremia with bowel disease. J Clin Microbiol. 1983, 17 (4): 696-697.PubMedCentralPubMed
8.
Leport C, Bure A, Leport J, Vilde JL: Incidence of colonic lesions in Streptococcus bovis and enterococcal endocarditis. Lancet. 1987, 1 (8535): 748- 10.1016/S0140-6736(87)90391-6CrossRefPubMed
9.
Zarkin BA, Lillemoe KD, Cameron JL, Effron PN, Magnuson TH, Pitt HA: The triad of Streptococcus bovis bacteremia, colonic pathology, and liver disease. Ann Surg. 1990, 211 (6): 786-791. discussion 791-782, 10.1097/00000658-199006000-00019PubMedCentralCrossRefPubMed
10.
Murray PR, Baron EJ: Manual of clinical microbiology. 2007, ASM Press, Washington, D.C, USA
11.
Osawa R, Fujisawa T, Sly LI: Streptococcus gallolyticus sp. nov.: gallate degrading organisms formerly assigned to Streptococcus bovis. Syst Appl Microbiol. 1995, 18: 74-78.CrossRef
12.
Devriese LA, Vandamme P, Pot B, Vanrobaeys M, Kersters K, Haesebrouck F: Differentiation between Streptococcus gallolyticus strains of human clinical and veterinary origins and Streptococcus bovis strains from the intestinal tracts of ruminants. J Clin Microbiol. 1998, 36 (12): 3520-3523.PubMedCentralPubMed
13.
Schlegel L, Grimont F, Ageron E, Grimont PA, Bouvet A: Reappraisal of the taxonomy of the Streptococcus bovis/Streptococcus equinus complex and related species: description of Streptococcus gallolyticus subsp. gallolyticus subsp. nov., S. gallolyticus subsp. macedonicus subsp. nov. and S. gallolyticus subsp. pasteurianus subsp. nov. Int J Syst Evol Microbiol. 2003, 53 (Pt 3): 631-645. 10.1099/ijs.0.02361-0CrossRefPubMed
14.
Lee RA, Woo PC, To AP, Lau SK, Wong SS, Yuen KY: Geographical difference of disease association in Streptococcus bovis bacteraemia. J Med Microbiol. 2003, 52: 903-908. 10.1099/jmm.0.05199-0CrossRefPubMed
15.
Jean SS, Teng LJ, Hsueh PR, Ho SW, Luh KT: Bacteremic Streptococcus bovis infections at a university hospital, 1992-2001. J Formos Med Assoc. 2004, 103: 118-123.PubMed
16.
Abdulamir AS, Hafidh RR, Mahdi LK, Al-jeboori T, Abubaker F: Investigation into the controversial association of Streptococcus gallolyticus with colorectal cancer and adenoma. BMC Cancer. 2009, 9: 403- 10.1186/1471-2407-9-403PubMedCentralCrossRefPubMed
17.
Beck M, Frodl R, Funke G: Comprehensive study of strains previously designated Streptococcus bovis consecutively isolated from human blood cultures and emended description of Streptococcus gallolyticus and Streptococcus infantarius subsp. coli. J Clin Microbiol. 2008, 46: 2966-2972. 10.1128/JCM.00078-08PubMedCentralCrossRefPubMed
18.
Corredoira J, Alonso MP, Coira A, Casariego E, Arias C, Alonso D, Pita J, Rodriguez A, Lopez MJ, Varela J: Characteristics of Streptococcus bovis endocarditis and its differences with Streptococcus viridans endocarditis. Eur J Clin Microbiol Infect Dis. 2008, 27: 285-291. 10.1007/s10096-007-0441-yCrossRefPubMed
19.
Ellmerich S, Scholler M, Duranton B, Gosse F, Galluser M, Klein JP, Raul F: Promotion of intestinal carcinogenesis by Streptococcus bovis. Carcinogenesis. 2000, 21 (4): 753-756. 10.1093/carcin/21.4.753CrossRefPubMed
20.
Biarc J, Nguyen IS, Pini A, Gosse F, Richert S, Thierse D, Van Dorsselaer A, Leize-Wagner E, Raul F, Klein JP, Scholler-Guinard M: Carcinogenic properties of proteins with pro-inflammatory activity from Streptococcus infantarius (formerly S.bovis). Carcinogenesis. 2004, 25 (8): 1477-1484. 10.1093/carcin/bgh091CrossRefPubMed
21.
Wentling GK, Metzger PP, Dozois EJ, Chua HK, Krishna M: Unusual bacterial infections and colorectal carcinoma--Streptococcus bovis and Clostridium septicum: report of three cases. Dis Colon Rectum. 2006, 49 (8): 1223-1227. 10.1007/s10350-006-0576-4CrossRefPubMed
22.
Rochlitz CF, Herrmann R, de Kant E: Overexpression and amplification of c-myc during progression of human colorectal cancer. Oncology. 1996, 53 (6): 448-454. 10.1159/000227619CrossRefPubMed
23.
Manne U, Myers RB, Moron C, Poczatek RB, Dillard S, Weiss H, Brown D, Srivastava S, Grizzle WE: Prognostic significance of Bcl-2 expression and p53 nuclear accumulation in colorectal adenocarcinoma. Int J Cancer. 1997, 74 (3): 346-358. 10.1002/(SICI)1097-0215(19970620)74:3<346::AID-IJC19>3.0.CO;2-9CrossRefPubMed
24.
Burns CA, McCaughey R, Lauter CB: The association of Streptococcus bovis fecal carriage and colon neoplasia: possible relationship with polyps and their premalignant potential. Am J Gastroenterol. 1985, 80 (1): 42-46.PubMed
25.
Beeching NJ, Christmas TI, Ellis-Pegler RB, Nicholson GI: Streptococcus bovis bacteraemia requires rigorous exclusion of colonic neoplasia and endocarditis. Q J Med. 1985, 56 (220): 439-450.PubMed
26.
Norfleet RG, Mitchell PD: Streptococcus bovis does not selectively colonise colorectal cancer and rectal polyps. J Clin Gastroenterol. 1993, 17: 25-28. 10.1097/00004836-199307000-00008CrossRefPubMed
27.
Potter MA, Cunliffe NA, Smith M, Miles RS, Flapan AD, Dunlop MG: A prospective controlled study of the association of Streptococcus bovis with colorectal carcinoma. J Clin Pathol. 1998, 51 (6): 473-474. 10.1136/jcp.51.6.473PubMedCentralCrossRefPubMed
28.
Klein RS, Recco RA, Catalano MT, Edberg SC, Casey JI, Steigbigel NH: Association of Streptococcus bovis with carcinoma of the colon. N Engl J Med. 1977, 297 (15): 800-802. 10.1056/NEJM197710132971503CrossRefPubMed
29.
Tjalsma H, Scholler-Guinard M, Lasonder E, Ruers TJ, Willems HL, Swinkels DW: Profiling the humoral immune response in colon cancer patients: diagnostic antigens from Streptococcus bovis. Int J Cancer. 2006, 119 (9): 2127-2135. 10.1002/ijc.22116CrossRefPubMed
30.
Kaplan MH, Chmel H, Stephens A, Hsieh HC, Tenenbaum MJ, Rothenberg IR, Joachim GR: Humoral reactions in human endocarditis due to Streptococcus bovis: evidence for a common S bovis antigen. J Infect Dis. 1983, 148 (2): 266-274.CrossRefPubMed
31.
Boleij A, Schaeps RM, de Kleijn S, Hermans PW, Glaser P, Pancholi V, Swinkels DW, Tjalsma H: Surface-exposed histone-like protein a modulates adherence of Streptococcus gallolyticus to colon adenocarcinoma cells. Infect Immun. 2009, 77 (12): 5519-5527. 10.1128/IAI.00384-09PubMedCentralCrossRefPubMed
32.
Sillanpaa J, Nallapareddy SR, Singh KV, Ferraro MJ, Murray BE: Adherence characteristics of endocarditis-derived Streptococcus gallolyticus ssp. gallolyticus (Streptococcus bovis biotype I) isolates to host extracellular matrix proteins. FEMS Microbiol Lett. 2008, 289 (1): 104-109. 10.1111/j.1574-6968.2008.01378.xCrossRefPubMed
33.
Ellmerich S, Djouder N, Scholler M, Klein JP: Production of cytokines by monocytes, epithelial and endothelial cells activated by Streptococcus bovis. Cytokine. 2000, 12 (1): 26-31. 10.1006/cyto.1999.0521CrossRefPubMed
34.
Janeway C: Immunobiology: the immune system in health and disease. 2005, Garland Science, New York, USA
35.
Ohshima H, Bartsch H: Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis. Mutat Res. 1994, 305 (2): 253-264.CrossRefPubMed
36.
Jung HC, Eckmann L, Yang SK, Panja A, Fierer J, Morzycka-Wroblewska E, Kagnoff MF: A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest. 1995, 95 (1): 55-65. 10.1172/JCI117676PubMedCentralCrossRefPubMed
37.
Mahida YR, Makh S, Hyde S, Gray T, Borriello SP: Effect of Clostridium difficile toxin A on human intestinal epithelial cells: induction of interleukin 8 production and apoptosis after cell detachment. Gut. 1996, 38 (3): 337-347. 10.1136/gut.38.3.337PubMedCentralCrossRefPubMed
38.
Spehlmann ME, Eckmann L: Nuclear factor-kappa B in intestinal protection and destruction. Curr Opin Gastroenterol. 2009, 25 (2): 92-99. 10.1097/MOG.0b013e328324f857CrossRefPubMed
39.
Sasaki E, Osawa R, Nishitani Y, Whiley RA: Development of a diagnostic PCR assay targeting the Mn-dependent superoxide dismutase gene (sodA) for identification of Streptococcus gallolyticus. J Clin Microbiol. 2004, 42 (3): 1360-1362. 10.1128/JCM.42.3.1360-1362.2004PubMedCentralCrossRefPubMed
40.
Chomczynski P, Mackey K: Short technical report. Modification of the TRIZOL reagent procedure for isolation of RNA from Polysaccharide-and proteoglycan-rich sources. Biotechniques. 1995, 19: 942-5.PubMed
41.
42.
Chomczynski P, Bowser-Finn R, Sabatini L: A reagent for the single-step isolation of viral RNA from human serum and biopsy samples. J NIH Res. 1994, 6: 83-
43.
44.
Schostak M, Krause H, Miller K, Schrader M, Weikert S, Christoph F, Kempkensteffen C, Kollermann J: Quantitative real-time RT-PCR of CD24 mRNA in the detection of prostate cancer. BMC Urol. 2006, 6: 7- 10.1186/1471-2490-6-7PubMedCentralCrossRefPubMed
45.
Srinivasan M, Sedmak D, Jewell S: Effect of fixatives and tissue processing on the content and integrity of nucleic acids. Am J Pathol. 2002, 161 (6): 1961-1971.PubMedCentralCrossRefPubMed
46.
Lisowski AR, English ML, Opsahl AC, Bunch RT, Blomme EA: Effect of the storage period of paraffin sections on the detection of mRNAs by in situ hybridization. J Histochem Cytochem. 2001, 49 (7): 927-928.CrossRefPubMed
47.
Drake D: Assessment of antimicrobial activity against biofilms. Methods Enzymol. 2001, 337: 385-389. 10.1016/S0076-6879(01)37027-1CrossRefPubMed
48.
Cui X, Yang SC, Sharma S, Heuze-Vourc'h N, Dubinett SM: IL-4 regulates COX-2 and PGE2 production in human non-small cell lung cancer. Biochem Biophys Res Commun. 2006, 343 (4): 995-1001. 10.1016/j.bbrc.2006.03.073CrossRefPubMed
49.
Welsh N, Cnop M, Kharroubi I, Bugliani M, Lupi R, Marchetti P, Eizirik DL: Is there a role for locally produced interleukin-1 in the deleterious effects of high glucose or the type 2 diabetes milieu to human pancreatic islets?. Diabetes. 2005, 54 (11): 3238-3244. 10.2337/diabetes.54.11.3238CrossRefPubMed
50.
McLachlan JL, Sloan AJ, Smith AJ, Landini G, Cooper PR: S100 and cytokine expression in caries. Infect Immun. 2004, 72 (7): 4102-4108. 10.1128/IAI.72.7.4102-4108.2004PubMedCentralCrossRefPubMed
51.
Steger K, Wilhelm J, Konrad L, Stalf T, Greb R, Diemer T, Kliesch S, Bergmann M, Weidner W: Both protamine-1 to protamine-2 mRNA ratio and Bcl2 mRNA content in testicular spermatids and ejaculated spermatozoa discriminate between fertile and infertile men. Hum Reprod. 2008, 23 (1): 11-16. 10.1093/humrep/dem363CrossRefPubMed
52.
Zhang Y, Wang YL, Liu YW, Li Q, Yuan YH, Niu WY, Sun LY, Zhu ZJ, Shen ZY, Han RF: Change of peripheral blood mononuclear cells IFN-gamma, IL-10, and TGF-beta1 mRNA expression levels with active human cytomegalovirus infection in orthotopic liver transplantation. Transplant Proc. 2009, 41 (5): 1767-1769. 10.1016/j.transproceed.2009.03.064CrossRefPubMed
Metadata
Title
Molecular detection, quantification, and isolation of Streptococcus gallolyticus bacteria colonizing colorectal tumors: inflammation-driven potential of carcinogenesis via IL-1, COX-2, and IL-8
Authors
Ahmed S Abdulamir
Rand R Hafidh
Fatimah Abu Bakar
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Molecular Cancer / Issue 1/2010
Electronic ISSN: 1476-4598
DOI
https://doi.org/10.1186/1476-4598-9-249

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