Chlamydia trachomatis infection increases the expression of inflammatory tumorigenic cytokines and chemokines as well as components of the Toll-like receptor and NF-κB pathways in human prostate epithelial cells

Molecular and Cellular Probes

Volumn 28, Issue 4, 2014, Pages 147-154

  Sellami, Hanen ^a   Said Sadier, Najwane ^b,d   Znazen, Abir ^a   Gdoura, Radhouane ^c   Ojcius, David M ^b   Hammami, Adnene ^a  

^a UNIVERSITY OF SFAX   (Tunisia)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Faculté des Sciences de Sfax   (Tunisia)

^d BEIRUT ARAB UNIVERSITY   (Lebanon)

Author keywords

Chemokines; Chlamydia trachomatis; Cytokines; Inflammation; Prostate cancer epithelial cells

Indexed keywords

CD14 ANTIGEN; CHEMOKINE; CYTOKINE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; RANTES; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ARTICLE; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE SYSTEM; IN VITRO STUDY; INFLAMMATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER CELL LINE; PROSTATE EPITHELIUM; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEROTYPE; TUMOR GROWTH; UPREGULATION; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PROSTATE TUMOR; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

BACTERIA (MICROORGANISMS); CHLAMYDIA TRACHOMATIS;

CELL LINE, TUMOR; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; CYTOKINES; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IN VITRO TECHNIQUES; INFLAMMATION; MALE; NF-KAPPA B; PROSTATIC NEOPLASMS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84901280717     PISSN: 08908508     EISSN: 10961194     Source Type: Journal    
DOI: 10.1016/j.mcp.2014.01.006     Document Type: Article

References (67)

1. Jemal A., Center M.M., De Santis C., Ward E.M. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev 2010, 19:1893-1907.
2. Hsairi M., Fakhfakh R., Ben Abdallah M., Jlidi R., Sellami A., Zheni S., et al. Assessment of cancer incidence in Tunisia 1993-1997. Tunis Med 2002, 2:57-64.
3. Landis S.H., Murray T., Bolden S., Wingo P.A. Cancer statistics. CA Cancer J Clin 1999, 49:8-31.
4. Klein E.A., Silverman R. Inflammation, infection and prostate cancer. Curr Opin Urol 2008, 18:315-319.
5. Platz E.A., De Marzo A.M. Epidemiology of inflammation and prostate cancer. JUrol 2004, 171:S36-S40.
6. Wagenlehner F.M., Elkahwaji J.E., Algaba F., Bjerklund-Johansen T., Naber K.G., Hartung R., et al. The role of inflammation and infection in the pathogenesis of prostate carcinoma. BJU Int 2007, 100:733-737.
7. Eckmann L., Kagnoff M.F., Fierer J. Intestinal epithelial cells as watchdogs for the natural immune system. Trends Microbiol 1995, 3:118-120.
8. Pate M.S., Hedges S.R., Sibley D.A., Russell M.W., Hook E.W., Mestecky J. Urethral cytokine and immune responses in Chlamydia trachomatis-infected males. Infect Immun 2001, 69:7178-7181.
9. Gerbase A.C., Rowley J.T., Mertens T.E. Global epidemiology of sexually transmitted diseases. Sex Transm Infect 1998, 1:S12-S16.
10. Motrich R.D., Cuffini C., Mackern Oberti J.P., Maccioni M., Rivero V.E. Chlamydia trachomatis occurrence and its impact on sperm quality in chronic prostatitis patients. JInfect 2005, 53:175-183.
11. Cunningham K.A., Beagley K.W. Male genital tract chlamydial infection: implications for pathology and infertility. Biol Reprod 2008, 2:180-189.
12. Stephens R.S. The cellular paradigm of chlamydial pathogenesis. Trends Microbiol 2003, 11:44-51.
13. Rasmussen S.J., Eckmann L., Quayle A.J., Shen L., Zhang L.Y., Anderson J.A., et al. Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis. JClin Invest 1997, 99:77-87.
14. Dessus-Babus S., Darville T.L., Cuozzo F.P., Ferguson K., Wyrick P.B. Differences in innate immune responses (invitro) to HeLa cells infected with nondisseminating serovar E and disseminating serovar L2 of Chlamydia trachomatis. Infect Immun 2002, 70:3234-3248.
15. Mackern-Oberti J.P., Maccioni M., Cuffini C., Gatti G., Rivero V.E. Susceptibility of prostate epithelial cells to Chlamydia muridarum infection and their role in innate immunity by recruitment of intracellular Toll-like receptors 4 and 2 and MyD88 to the inclusion. Infect Immun 2006, 74:6973-6981.
16. Mackern-Oberti J.P., Motrich R.D., Breser M.L., Cejas H., Cuffini C., Maccioni M., et al. Male rodent genital tract infection with Chlamydia muridarum: persistence in the prostate gland that triggers self-immune reactions in genetically susceptible hosts. JUrol 2011, 186:1100-1106.
17. Mackern-Oberti J.P., Maccioni M., Breser M.L., Eley A., Miethke T., Rivero V.E. Innate immunity in the male genital tract: Chlamydia trachomatis induces keratinocyte-derived chemokine production in prostate, seminal vesicle and epididymis/vas deferens primary cultures. JMed Microbiol 2011, 60:307-316.
18. Caldwell H.D., Kromhout J., Schachter J. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect Immun 1981, 3:1161-1176.
19. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
20. Toni D., O'Neill Joshua M., Andrews Charles W., Nagarajan Uma M., Stahl Lynn, Ojcius David M. Toll-like Receptor-2, but not toll-like Receptor-4, is essential for development of oviduct pathology in chlamydial genital tract infection. JImmunol 2003, 171:6187-6197.
21. Brunham R.C., Rey-Ladino J. Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat Rev Immunol 2005, 5:149-161.
22. Morré S.A., Rozendaal L., van Valkengoed I.G., Boeke A.J., van Voorst Vader P.C., Schirm J., de Blok S., van Den Hoek J.A., van Doornum G.J., Meijer C.J., van Den Brule A.J. Urogenital Chlamydia trachomatis serovars in men and women with a symptomatic or asymptomatic infection: an association with clinical manifestations?. JClin Microbiol 2000, 38:2292-2296.
23. Gatti G., Quintar A.A., Andreani V., Nicola J.P., Maldonado C.A., Masini-Repiso A.M., et al. Expression of Toll-like receptor 4 in the prostate gland and its association with the severity of prostate cancer. Prostate 2009, 69:1387-1397.
24. Oberley R.E., Goss K.L., Dahmoush L., Ault K.A., Crouch E.C., Snyder J.M. Arole for surfactant protein D in innate immunity of the human prostate. Prostate 2005, 65:241-251.
25. Doak S.H., Zaïr Z.M. Real-time reverse-transcription polymerase chain reaction: technical considerations for gene expression analysis. Methods Mol Biol 2012, 817:251-270.
26. Takeda K., Kaisho T., Akira S. Toll-like receptors. Annu Rev Immunol 2003, 21:335-376.
27. Spitzer J.H., Visintin A., Mazzoni A., Kennedy M.N., Segal D.M. Toll-like receptor 1 inhibits Toll-like receptor 4 signaling in endothelial cells. Eur J Immunol 2002, 32:1182-1187.
28. Shiraki R., Inoue N., Kawasaki S., Takei A., Kadotani M., Ohnishi Y., et al. Expression of Toll-like receptors on human platelets. Thromb Res 2004, 113:379-385.
29. Barton G.M., Medzhitov R. Toll-like receptor signaling pathways. Science 2003, 5625:1524-1525.
30. Gatti G., Rivero V., Motrich R.D., Maccioni M. Prostate epithelial cells can act as early sensors of infection by up-regulating TLR4 expression and proinflammatory mediators upon LPS stimulation. JLeukoc Biol 2006, 79:989-998.
31. Takeyama K., Mitsuzawa H., Shimizu T., Konishi M., Nishitani C., Sano H., et al. Prostate cell lines secrete IL-8 in response to Mycoplasma hominis through Toll-like receptor 2-mediated mechanism. Prostate 2006, 66:386-391.
32. González-Reyes S., Fernández J.M., González L.O., Aguirre A., Suárez A., González J.M., et al. Study of TLR3, TLR4, and TLR9 in prostate carcinomas and their association with biochemical recurrence. Cancer Immunol Immunother 2011, 60:217-226.
33. Qureshi N., Kaltashov I., Walker K., Doroshenko V., Cotter R.J., Takayama K., et al. Structure of the monophosphoryl lipid A moiety obtained from the lipopolysaccharide of Chlamydia trachomatis. JBiol Chem 1997, 272:10594-10600.
34. Kol A., Lichtman A.H., Finberg R.W., Libby P., Kurt-Jones E.A. Cutting edge: heat shock protein (HSP) 60 activates the innate immune response: CD14 is an essential receptor for HSP60 activation of mononuclear cells. JImmunol 2000, 164:13-17.
35. Kundu S.D., Lee C., Billips B.K., Habermacher G.M., Zhang Q., Liu V., et al. The toll-like receptor pathway: a novel mechanism of infection-induced carcinogenesis of prostate epithelial cells. Prostate 2008, 68:223-229.
36. Hua D., Liu M.Y., Cheng Z.D., Qin X.J., Zhang H.M., Chen Y., et al. Small interfering RNA-directed targeting of Toll-like receptor 4 inhibits human prostate cancer cell invasion, survival, and tumorigenicity. Mol Immunol 2009, 46:2876-2884.
37. Akira S., Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004, 4:499-511.
38. Palayoor S.T., Youmell M.Y., Calderwood S.K., Coleman C.N., Price B.D. Constitutive activation of IkappaB kinase alpha and NF-kappaB in prostate cancer cells is inhibited by ibuprofen. Oncogene 1999, 18:7389-7394.
39. Savli H., Szendröi A., Romics I., Nagy B. Gene network and canonical pathway analysis in prostate cancer: a microarray study. Exp Mol Med 2008, 40:176-185.
40. Kojima M., Morisaki T., Izuhara K., Uchiyama A., Matsunari Y., Katano M., et al. Lipopolysaccharide increases cyclooxygenase- 2 expression in a colon carcinoma cell line through nuclear factor-KB activation. Oncogene 2000, 19:1225-1231.
41. Kapral M., Weglarz L., Parfiniewicz B., Lodowska J., Jaworska-Kik M. Quantitative evaluation of transcriptional activation of NF-kB p65 and p50 subunits and IκBα encoding genes in colon cancer cells by Desulfovibrio desulfuricans endotoxin. Folia Microbiol 2010, 55:657-661.
42. Gilmore T.D. Introduction to NF-KB: players, pathways, perspectives. Oncogene 2006, 25:6680-6684.
43. Yang L., Ross K., Qwarnstrome E. RelA control of IκBα phosphorylation: a positive feedback loop for high affinity NF-KB complexes. JBiol Chem 2003, 278:30881-30888.
44. Kapral M., Parfiniewicz B., Strzalka-Mrozik B., Zachacz A., Weglarz L. Evaluation of the expression of transcriptional factor NF-KB induced by phytic acid in colon cancer cells. Acta Pol Pharm 2008, 65:697-702.
45. Franklin R.B., Feng P., Milon B., Desouki M.M., Singh K.K., Kajdacsy-Balla A., et al. hZIP1: zinc uptake transporter down regulation and zinc depletion in prostate cancer. Mol Cancer 2005, 4:32.
46. Aggarwal B.B., Shishodia S., Sandur S.K., Pandey M.K., Sethi G. Inflammation and cancer: how hot is the link?. Biochem Pharmacol 2006, 72:1605-1621.
47. Inoue K., Slaton J.W., Eve B.Y., Kim S.J., Perrotte P., Balbay M.D., et al. Interleukin expression regulates tumorigenicity and metastases in androgen- independent prostate cancer. Clin Cancer Res 2000, 6:2104-2119.
48. Coussens L.M., Werb Z. Inflammation and cancer. Nature 2002, 420:860-867.
49. Taichman R.S., Cooper C., Keller E.T., Pienta K.J., Taichman N.S., McCauley L.K. Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res 2002, 62:1832-1837.
50. Manes S., Mira E., Colomer R., Montero S., Real L.M., Gomez- Mouton C., et al. CCR5 expression influences the progression of human breast cancer in a p53-dependent manner. JExp Med 2003, 198:1381-1389.
51. Pei Z., Lin D., Song X., Li H., Yao H. TLR4 signaling promotes the expression of VEGF and TGFbeta1 in human prostate epithelial PC3 cells induced by lipopolysaccharide. Cell Immunol 2009, 254:20-27.
52. Drott J.B., Alexeyev O., Bergstrom P., Elgh F., Olsson J. Propionibacterium acnes infection induces upregulation of inflammatory genes and cytokine secretion in prostate epithelial cells. BMC Microbiol 2010, 10:126.
53. Ferrer F.A., Miller L.J., Andrawis R.I., Kurtzman S.H., Albertsen P.C., Laudone V.P., et al. Angiogenesis and prostate cancer: invivo and invitro expression of angiogenesis factors by prostate cancer cells. Urology 1998, 51:161-167.
54. Strohmeyer D., Rossing C., Bauerfeind A., Kaufmann O., Schlechte H., Bartsch G., et al. Vascular endothelial growth factor and its correlation with angiogenesis and p53 expression in prostate cancer. Prostate 2000, 45:216-224.
55. Guo Y., Wang S., Hoot D.R., Clinton S.K. Suppression of VEGF-mediated autocrine and paracrine interactions between prostate cancer cells and vascular endothelial cells by soy isoflavones. JNutr Biochem 2007, 18:408-417.
56. Yoo N.C., Chung H.C., Chung H.C., Park J.O., Rha S.Y., Kim J.H., et al. Synchronous elevation of soluble intercellular adhesion molecule-1 (ICAM-1) and vascular cell adhesion molecule-1 (VCAM-1) correlates with gastric cancer progression. Yonsei Med J 1998, 39:27-36.
57. Hodge D.R., Hurt E.M., Farrar W.L. The role of IL-6 and STAT3 in inflammation and cancer. Eur J Cancer 2005, 41:2502-2512.
58. Lu H., Ouyang W., Huang C. Inflammation, a key event in cancer development. Mol Cancer Res 2006, 4:221-233.
59. Di J.M., Pang J., Pu X.Y., Zhang Y., Liu X.P., Fang Y.Q., et al. Toll-like receptor 9 agonists promote IL-8 and TGF-beta1 production via activation of nuclear factor kappaB in PC-3 cells. Cancer Genet Cytogenet 2009, 192:60-67.
60. Youngs S.J., Ali S.A., Taub D.D., Rees R.C. Chemokines induce migrational responses in human breast carcinoma cell lines. Int J Cancer 1997, 71:257-266.
61. Konig J.E., Senge T., Allhoff E.P., Konig W. Analysis of inflammatory network in benign prostate hyperplasia and prostate cancer. Prostate 2004, 58:121-129.
62. Loberg R.D., Day L.L., Harwood J., Ying C., St John L.N., Giles R., et al. CCL2 is a potent regulator of prostate cancer cell migration and proliferation. Neoplasia 2006, 8:578-586.
63. Harper C.E., Patel B.B., Wang J., Eltoum I.A., Lamartiniere C.A. Epigallocatechin-3-Gallate suppresses early stage, but not late stage prostate cancer in TRAMP mice: mechanisms of action. Prostate 2007, 67:1576-1589.
64. Aaltoma S.H., Lipponen P.K., Kosma V.M. Inducible nitric oxide synthase (iNOS) expression and its prognostic value in prostate cancer. Anticancer Res 2001, 21:3101-3106.
65. Burke F., Relf M., Negus R., Balkwill F. Acytokine profile of normal and malignant ovary. Cytokine 1996, 8:578-585.
66. Harada S., Keller E.T., Fujimoto N., Koshida K., Namiki M., Matsumoto T., et al. Long-term exposure of tumor necrosis factor alpha causes hypersensitivity to androgen and anti-androgen withdrawal phenomenon in LNCaP prostate cancer cells. Prostate 2001, 46:319-326.
67. Apte R.N., Voronov E. Interleukin-1-a major pleiotropic cytokine in tumor-host interactions. Semin Cancer Biol 2002, 12:277-290.