Lactobacillus crispatus mediates anti-inflammatory cytokine interleukin-10 induction in response to Chlamydia trachomatis infection in vitro

International Journal of Medical Microbiology

Volumn 305, Issue 8, 2015, Pages 815-827

  Rizzo, Antonietta ^a   Fiorentino, Margherita ^a   Buommino, Elisabetta ^a   Donnarumma, Giovanna ^a   Losacco, Antonio ^a   Bevilacqua, Nazario ^b  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b CARDARELLI HOSPITAL   (Italy)

Author keywords

Chlamydia trachomatis; IL 10; IL 6; IL 8; Lactobacillus crispatus; TNF

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; PROBIOTIC AGENT; RECOMBINANT INTERLEUKIN 10; TUMOR NECROSIS FACTOR ALPHA; ANTIINFLAMMATORY AGENT;

ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL VIABILITY; CHLAMYDIASIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; CYTOTOXICITY; DRUG EFFICACY; EPITHELIUM CELL; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; INNATE IMMUNITY; LACTOBACILLUS CRISPATUS; MACROPHAGE; MOUSE; NONHUMAN; SUPERNATANT; UPREGULATION; ANIMAL; CELL LINE; CHLAMYDIA TRACHOMATIS; IMMUNOLOGY; LACTOBACILLUS; METABOLISM; MICROBIOLOGY; ORGANISMAL INTERACTION; PHYSIOLOGY; SECRETION (PROCESS);

ANIMALS; ANTI-INFLAMMATORY AGENTS; BACTERIAL ADHESION; CELL LINE; CHLAMYDIA TRACHOMATIS; EPITHELIAL CELLS; FEMALE; HUMANS; INTERLEUKIN-10; LACTOBACILLUS; MACROPHAGES; MICE; MICROBIAL INTERACTIONS;

EID: 84983096254     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2015.07.005     Document Type: Article

References (50)

1. Abramov V., Khlebnikov V., Kosarev I., Bairamova G., Vasilenko R., Suzina N., Machulin A., Sakulin V., Kulikova N., Vasilenko N., Karlyshev A., Uversky V., Chikindas M.L., Melnikov V. Probiotic properties of Lactobacillus crispatus 2,029: homeostatic interaction with cervicovaginal epithelial cells and antagonistic activity to genitourinary pathogens. Probiotics Antimicrob. Proteins 2014, 6:165-176.
2. Aroutcheva A., Gariti D., Simon M., Shott S., Faro J., Simoes J.A., Gurguis A., Faro S. Defense factors of vaginal lactobacilli. Am. J. Obstet. Gynecol. 2001, 185:375-379.
3. Barlow R.E., Cooke I.D., Odukoya O., Heatley M.K., Jenkins J., Narayansingh G., Ramsewak S.S., Eley A. The prevalence of Chlamydia trachomatis in fresh tissue specimens from patients with ectopic pregnancy or tubal factor infertility as determined by PCR and in-situ hybridization. J. Med. Microbiol. 2001, 50:902-908.
4. Barton B.E., Shortall J., Jackson J.V. Interleukins 6 and 11 protect mice from mortality in a staphylococcal enterotoxin induced toxic shock model. Infect. Immun. 1996, 64:714-718.
5. Boris S., Barbés C. Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect. 2000, 2:543-546.
6. Buchholz K.R., Stephens R.S. The extracellular signal regulated kinase/mitogen-activated protein kinase pathway induces the inflammatory factor interleukin-8 following Chlamydia trachomatis infection. Infect. Immun. 2007, 75:5924-5929.
7. Christensen H.R., Frokiaer H., Pestka J.J. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J. Immunol. 2002, 168:171-178.
8. Clarke C.J., Hales A., Hunt A., Foxwell B.M. IL-10 mediated suppression of TNF-α production is independent of its ability to inhibit NF-kB activity. Eur. J. Immunol. 1998, 28:1719-1726.
9. Crane-Godreau M.A., Wira C.R. Effect of Escherichia coli and Lactobacillus rhamnosus on macrophage inflammatory protein 3 alpha, tumor necrosis factor alpha, and transforming growth factor beta release by polarized rat uterine epithelial cells in culture. Infect. Immun. 2004, 72:1866-1873.
10. Derbigny W.A., Shobe L.R., Kamran J.C., Toomey K.S., Ofner S. Identifying a role for toll-like receptor 3 in the innate immune response to Chlamydia muridarum infect. Infect. Immun. 2012, 80:254-265.
11. Dessus-Babus S., Darville T.L., Cuozzo F.P., Ferguson K., Wyrick P.B. Differences in innate immune responses (in vitro) to HeLa cells infected with nondisseminating serovar E and disseminating serovar L2 of Chlamydia trachomatis. Infect. Immun. 2002, 70:3234-3248.
12. Doerflinger S.Y., Throop A.L., Herbst-Kralovetz M.M. Bacteria in the vaginal microbiome alter the innate immune response and barrier properties of the human vaginal epithelia in a species-specific manner. J. Infect. Dis. 2014, 209:1989-1999.
13. Dolfini E., Elli L., Roncoroni L., Costa B., Colleoni M.P., Lorusso V., Ramponi S. Damaging effects of gliadin on three-dimensional cell culture model. World J. Gastroenterol. 2005, 11:5973-5977.
14. Duary R.K., Batish V.K., Grover S. Immunomodulatory activity of two potential probiotic strains in LPS-stimulated HT-29 cells. Genes Nutr. 2014, 9:398.
15. Filippi C.M., Von Herrath M.G. IL-10 and the resolution of infections. J. Pathol. 2008, 214:224-230.
16. Fischer S.F., Harlander T., Vier J., Häcker G. Protection against CD95-induced apoptosis by chlamydial infection at a mitochondrial step. Infect. Immun. 2004, 72:1107-1115.
17. Foligne B., Nutten S., Grangette C., Dennin V., Goudercourt D., Poiret S., Dewulf J., Brassart D., Mercenier A., Pot B. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J. Gastroenterol. 2007, 13:236-243.
18. Fredricks D.N., Fiedler T.L., Thomas K.K., Oakley B.B., Marrazzo J.M. Targeted PCR for detection of vaginal bacteria associated with bacterial vaginosis. J. Clin. Microbiol. 2007, 45:3270-3276.
19. 2. PLoS ONE 2014, 9(9):e107758.
20. Hillier S.L. The vaginal microbial ecosystem and resistance to HIV. AIDS Res. Hum. Retroviruses 1998, 14:17-21.
21. Kim S.O., Sheikh H.I., Ha S.D., Martins A., Reid G. G-CSF-mediated inhibition of JNK is a key mechanism for Lactobacillus rhamnosus-induced suppression of TNF-α production in macrophages. Cell Microbiol. 2006, 8:1958-1971.
22. Kotzamanidis C., Kourelis A., Litopoulou-Tzanetaki E., Tzanetakis N., Yiangou M. Evaluation of adhesion capacity, cell surface traits and immunomodulatory activity of presumptive probiotic Lactobacillus strains. Int. J. Food Microbiol. 2010, 140:154-163.
23. Lamont R.F., Sobel J.D., Akins R.A., Hassan S.S., Chaiworapongsa T., Kusanovic J.P., Romero R. The vaginal microbiome: new information about genital tract flora using molecular based techniques. BJOG 2011, 118:533-549.
24. Macklaim J., Fernandes A., Di Bella J., Hammond J., Reid G., Gloor G. Comparative meta-RNA-seq of the vaginal microbiota and differential expression by Lactobacillus iners in health and dysbiosis. Microbiome 2013, 1:12.
25. Madianos P.N., Bobetsis A., Kinane D.F. Generation of inflammatory stimuli: how bacteria set up inflammatory responses in the gingiva. J. Clin. Periodontol. 2005, 32:57-71.
26. Marco M.L., Kleerebezem M. Assessment of real-time RT-PCR for quantification of Lactobacillus plantarum gene expression during stationary phase and nutrient starvation. J. Appl. Microbiol. 2008, 104:587-594.
27. Mastromarino P., Di Pietro M., Schiavoni G., Nardis C., Gentile M., Sessa R. Effects of vaginal lactobacilli in Chlamydia trachomatis infection. Int. J. Med. Microbiol. 2014, 304:654-661.
28. Maudsdotter L., Jonsson H., Roos S., Jonsson1 A.N. Lactobacilli reduce cell cytotoxicity caused by Streptococcus pyogenes by producing lactic acid that degrades the toxic component lipoteichoic acid. Antimicrob. Agents Chemother. 2011, 55:1622-1628.
29. Miller W.C., Ford C.A., Morris M., Handcock M.S., Schmitz J.L., Hobbs M.M., Cohen M.S., Harris K.M., Udry J.R. Prevalence of chlamydial and gonococcal infections among young adults in the United States. JAMA 2004, 291:2229-2236.
30. Nagy I., Pivarcsi A., Koreck A., Széll M., Urbán E., Kemény L. Distinct strains of Propionibacterium acnes induce selective human β-defensin-2 and Interleukin-8 expression in human keratinocytes through Toll-Like receptors. J. Invest. Dermatol. 2005, 124:931-938.
31. Niers L.E., Timmerman H.M., Rijkers G.T., van Bleek G.M., van Uden N.O., Knol E.F., Kapsenberg M.L., Kimpen J.L., Hoekstra M.O. Identification of strong interleukin-10 inducing lactic acid bacteria which down-regulate T helper type 2 cytokines. Clin. Exp. Allergy 2005, 35:1481-1489.
32. Ohman H., Tiitinen A., Halttunen M., Lehtinen M., Paavonen J., Surcel H.M. Cytokine polymorphisms and severity of tubal damage in women with Chlamydia-associated infertility. J. Infect. Dis. 2009, 199:1353-1359.
33. Opal S.M., Wherry J.C., Grint P. Interleukin-10: potential benefits and possible risks in clinical infectious diseases. Clin. Infect. Dis. 1998, 27:1497-1507.
34. Osset J., Bartolomé R.M., García E., Andreu A. Assessment of the capacity of Lactobacillus to inhibit the growth of uropathogens and block their adhesion to vaginal epithelial cells. J. Infect. Dis. 2001, 183:485-491.
35. 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.
36. Pessi T., Sütas Y., Hurme M., Isolauri E. Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clin. Exp. Allergy 2000, 30:1804-1808.
37. Rasmussen S.J., Eckmann L., Quayle A.J., Shen L., Zhang L.Y., Anderson J.A., Fierer J., Stephens R.S., Kagnoff M.F. Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis. J. Clin. Invest. 1997, 99:77-87.
38. Ravel J., Gajer P., Abdo Z., Schneider G.M., Koenig S.S., McCulle S.L., Karlebach S., Gorle R., Russell J., Tacket C.O., Brotman R.M., Davis C.C., Ault K., Peralta L., Forney L.J. Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:4680-4687.
39. Reid G., Burton J. Use of Lactobacillus to prevent infection by pathogenic bacteria. Microb. Infect. 2002, 4:319-324.
40. Rizzo A., Domenico M.D., Carratelli C.R., Paolillo R. The role of Chlamydia and Chlamydophila infections in reactive arthritis. Intern. Med. 2012, 51:113-117.
41. Rizzo A., Losacco A., Carratelli C.R. Lactobacillus crispatus modulates epithelial cell defense against Candida albicans through Toll-like receptors 2 and 4, interleukin 8 and human β-defensins 2 and 3. Immunol. Lett. 2013, 156:102-109.
42. Rizzo A., Losacco A., Carratelli C.R., Domenico M.D., Bevilacqua N. Lactobacillus plantarum reduces Streptococcus pyogenes virulence by modulating the IL-17, IL-23 and Toll-like receptor 2/4 expressions in human epithelial cells. Int. Immunopharmacol. 2013, 17:453-461.
43. Rönnqvist P.D., Forsgren-Brusk U.B., Grahn-Håkansson E.E. Lactobacilli in the female genital tract in relation to other genital microbes and vaginal Ph. Acta Obstet. Gynecol. Scand. 2006, 85:726-735.
44. Sellami H., Said-Sadier N., Znazen A., Gdoura R., Ojcius D.M., Hammami A. 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. Mol. Cell. Probes 2014, 28:147-154.
45. Skwor T.A., Atik B., Kandel R.P., Adhikarl H.K., Sharma B., Dean D. Role of secreted conjunctival mucosal cytokine and chemokine proteins in different stages of trachomatous disease. PLoS Negl. Trop. Dis. 2008, 2:264.
46. Steele C., Fidel P.L. Cytokine and chemokine production by human oral and vaginal epithelial cells in response to Candida albicans. Infect. Immun. 2002, 70:577-583.
47. Stephens R.S. The cellular paradigm of Chlamydial pathogenesis. Trends Microbiol. 2003, 11:44-51.
48. van den Brule A.J., Munk C., Winther J.F., Kjaer S.K., Jørgensen H.O., Meijer C.J., Morré S.A. Prevalence and persistence of asymptomatic Chlamydia trachomatis infections in urine specimens from Danish male military recruits. Int. J. STD AIDS 2002, 13:19-22.
49. Vielfort K., Sjolinder H., Roos S., Jonsson H., Aro H. Adherence of clinically isolated lactobacilli to human cervical cells in competition with Neisseria gonorrhoeae. Microbes Infect. 2008, 10:1325-1334.
50. Zaga V., Estrada-Gutierrez G., Beltran-Montoya J., Maida-Claros R., Lopez-Vancell R., Vadillo-Ortega F. Secretions of interleukin-1 beta and tumor necrosis factor alpha by whole fetal membranes depend on initial interactions of amnion or choriodecidua with lipopolysaccharides or group B streptococci. Biol. Reprod. 2004, 1:1296-1302.