1887

Abstract

When presented with certain unfavourable environmental conditions, reticulate bodies (RBs) enter into a viable, yet non-cultivable state called persistence. Previously, we established an and herpes simplex virus type 2 (HSV-2) co-infection model. These data indicate that (i) viral co-infection stimulates chlamydial persistence, (ii) productive HSV replication is not required for persistence induction, and (iii) HSV-induced persistence is not mediated by any currently characterized anti-chlamydial pathway or persistence inducer. In this study we demonstrated that chlamydial infectivity, though initially suppressed, recovered within 44 h of co-infection with UV-inactivated HSV-2, demonstrating that HSV-induced persistence is reversible. Co-incubation of chemically fixed, HSV-2-infected inducer cells with viable, -infected responder cells both suppressed production of infectious chlamydial progeny and stimulated formation of swollen, aberrantly shaped RBs. In addition, pre-incubation of viral particles with viral glycoprotein D (gD)-specific neutralizing antibody prevented co-infection-induced persistence. Finally, exposure of infected cells to a soluble, recombinant HSV-2 gD : Fc fusion protein decreased production of infectious EBs to a degree similar to that observed in co-infected cultures. Thus, we conclude that interaction of HSV gD with the host cell surface is sufficient to trigger a novel host anti-chlamydial response that restricts chlamydial development.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.036566-0
2010-05-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/5/1294.html?itemId=/content/journal/micro/10.1099/mic.0.036566-0&mimeType=html&fmt=ahah

References

  1. Abdelrahman Y. M., Belland R. J. 2005; The chlamydial developmental cycle. FEMS Microbiol Rev 29:949–959
    [Google Scholar]
  2. Amici C., Rossi A., Costanzo A., Ciafre S., Marinari B., Balsamo M., Levrero M., Santoro M. G. 2006; Herpes simplex virus disrupts NF- κB regulation by blocking its recruitment on the I κB α promoter and directing the factor on viral genes. J Biol Chem 281:7110–7117
    [Google Scholar]
  3. Beatty W. L., Byrne G. I., Morrison R. P. 1993; Morphologic and antigenic characterization of interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro. Proc Natl Acad Sci U S A 90:3998–4002
    [Google Scholar]
  4. Beatty W. L., Belanger T. A., Desai A. A., Morrison R. P., Byrne G. I. 1994; Tryptophan depletion as a mechanism of gamma interferon-mediated chlamydial persistence. Infect Immun 62:3705–3711
    [Google Scholar]
  5. Bragina E. Y., Gomberg M. A., Dmitriev G. A. 2001; Electron microscopic evidence of persistent chlamydial infection following treatment. J Eur Acad Dermatol Venereol 15:405–409
    [Google Scholar]
  6. Byrne G. I., Lehmann L. K., Landry G. J. 1986; Induction of tryptophan catabolism is the mechanism for gamma-interferon-mediated inhibition of intracellular Chlamydia psittaci replication in T24 cells. Infect Immun 53:347–351
    [Google Scholar]
  7. Cheshenko N., Del Rosario B., Woda C., Marcellino D., Satlin L. M., Herold B. C. 2003; Herpes simplex virus triggers activation of calcium-signaling pathways. J Cell Biol 163:283–293
    [Google Scholar]
  8. Cocchi F., Menotti L., Mirandola P., Lopez M., Campadelli-Fiume G. 1998; The ectodomain of a novel member of the immunoglobulin subfamily related to the poliovirus receptor has the attributes of a bona fide receptor for herpes simplex virus types 1 and 2 in human cells. J Virol 72:9992–10002
    [Google Scholar]
  9. Dean D., Suchland R. J., Stamm W. E. 2000; Evidence for long-term cervical persistence of Chlamydia trachomatis by omp1 genotyping. J Infect Dis 182:909–916
    [Google Scholar]
  10. Deka S., Vanover J., Dessus-Babus S., Whittimore J., Howett M. K., Wyrick P. B., Schoborg R. V. 2006; Chlamydia trachomatis enters a viable but non-cultivable (persistent) state within herpes simplex virus type 2 (HSV-2) co-infected host cells. Cell Microbiol 8:149–162
    [Google Scholar]
  11. Deka S., Vanover J., Sun J., Kintner J., Whittimore J., Schoborg R. V. 2007; An early event in the herpes simplex virus type-2 replication cycle is sufficient to induce Chlamydia trachomatis persistence. Cell Microbiol 9:725–737
    [Google Scholar]
  12. Duff R., Rapp F. 1971; Properties of hamster embryo fibroblasts transformed in vitro after exposure to ultraviolet-irradiated herpes simplex virus type 2. J Virol 8:469–477
    [Google Scholar]
  13. Fehlner-Gardiner C., Roshick C., Carlson J. H., Hughes S., Belland R. J., Caldwell H. D., McClarty G. 2002; Molecular basis defining human Chlamydia trachomatis tissue tropism. A possible role for tryptophan synthase. J Biol Chem 277:26893–26903
    [Google Scholar]
  14. Fortenberry J. D., Brizendine E. J., Katz B. P., Wools K. K., Blythe M. J., Orr D. P. 1999; Subsequent sexually transmitted infections among adolescent women with genital infection due to Chlamydia trachomatis, Neisseria gonorrhoeae, or Trichomonas vaginalis. Sex Transm Dis 26:26–32
    [Google Scholar]
  15. Fuller A. O., Spear P. G. 1987; Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virion–cell fusion at the cell surface. Proc Natl Acad Sci U S A 84:5454–5458
    [Google Scholar]
  16. Fuller A. O., Santos R. E., Spear P. G. 1989; Neutralizing antibodies specific for glycoprotein H of herpes simplex virus permit viral attachment to cells but prevent penetration. J Virol 63:3435–3443
    [Google Scholar]
  17. Gerard H. C., Krausse-Opatz B., Wang Z., Rudy D., Rao J. P., Zeidler H., Schumacher H. R., Whittum-Hudson J. A., Kohler L., Hudson A. P. 2001; Expression of Chlamydia trachomatis genes encoding products required for DNA synthesis and cell division during active versus persistent infection. Mol Microbiol 41:731–741
    [Google Scholar]
  18. Gerard H. C., Wang Z., Whittum-Hudson J. A., El-Gabalawy H., Goldbach-Mansky R., Bardin T., Schumacher H. R., Hudson A. P. 2002; Cytokine and chemokine mRNA produced in synovial tissue chronically infected with Chlamydia trachomatis and C. pneumoniae. J Rheumatol 29:1827–1835
    [Google Scholar]
  19. Granger S. W., Rickert S. 2003; LIGHT–HVEM signaling and the regulation of T cell-mediated immunity. Cytokine Growth Factor Rev 14:289–296
    [Google Scholar]
  20. Hogan R. J., Mathews S. A., Mukhopadhyay S., Summersgill J. T., Timms P. 2004; Chlamydial persistence: beyond the biphasic paradigm. Infect Immun 72:1843–1855
    [Google Scholar]
  21. Hoppe S., Schelhaas M., Jaeger V., Liebig T., Petermann P., Knebel-Morsdorf D. 2006; Early herpes simplex virus type 1 infection is dependent on regulated Rac1/Cdc42 signalling in epithelial MDCKII cells. J Gen Virol 87:3483–3494
    [Google Scholar]
  22. Hsu H., Solovyev I., Colombero A., Elliott R., Kelley M., Boyle W. J. 1997; ATAR, a novel tumor necrosis factor receptor family member, signals through TRAF2 and TRAF5. J Biol Chem 272:13471–13474
    [Google Scholar]
  23. Johnson F. W., Hobson D. 1977; The effect of penicillin on genital strains of Chlamydia trachomatis in tissue culture. J Antimicrob Chemother 3:49–56
    [Google Scholar]
  24. Kwon H., Bai Q., Baek H. J., Felmet K., Burton E. A., Goins W. F., Cohen J. B., Glorioso J. C. 2006; Soluble V domain of nectin-1/HveC enables entry of herpes simplex virus type 1 (HSV-1) into HSV-resistant cells by binding to viral glycoprotein D. J Virol 80:138–148
    [Google Scholar]
  25. Marsters S. A., Ayres T. M., Skubatch M., Gray C. L., Rothe M., Ashkenazi A. 1997; Herpesvirus entry mediator, a member of the tumor necrosis factor receptor (TNFR) family, interacts with members of the TNFR-associated factor family and activates the transcription factors NF- κB and AP-1. J Biol Chem 272:14029–14032
    [Google Scholar]
  26. Matsumoto A., Manire G. P. 1970; Electron microscopic observations on the effects of penicillin on the morphology of Chlamydia psittaci. J Bacteriol 101:278–285
    [Google Scholar]
  27. Mauri D. N., Ebner R., Montgomery R. I., Kochel K. D., Cheung T. C., Yu G. L., Ruben S., Murphy M., Eisenberg R. J. other authors 1998; LIGHT, a new member of the TNF superfamily, and lymphotoxin alpha are ligands for herpesvirus entry mediator. Immunity 8:21–30
    [Google Scholar]
  28. Montgomery R. I., Warner M. S., Lum B. J., Spear P. G. 1996; Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87:427–436
    [Google Scholar]
  29. Moxley M. J., Block T. M., Liu H. C., Fraser N. W., Perng G. C., Wechsler S. L., Su Y. H. 2002; Herpes simplex virus type 1 infection prevents detachment of nerve growth factor-differentiated PC12 cells in culture. J Gen Virol 83:1591–1600
    [Google Scholar]
  30. Nakanishi H., Takai Y. 2004; Roles of nectins in cell adhesion, migration and polarization. Biol Chem 385:885–892
    [Google Scholar]
  31. Nanagara R., Li F., Beutler A., Hudson A. Jr R. S. H 1995; Alteration of Chlamydia trachomatis biologic behavior in synovial membranes. Suppression of surface antigen production in reactive arthritis and Reiter's syndrome. Arthritis Rheum 38:1410–1417
    [Google Scholar]
  32. Nelson D. E., Virok D. P., Wood H., Roshick C., Johnson R. M., Whitmire W. M., Crane D. D., Steele-Mortimer O., Kari L. other authors 2005; Chlamydial IFN- γ immune evasion is linked to host infection tropism. Proc Natl Acad Sci U S A 102:10658–10663
    [Google Scholar]
  33. Nicola A. V., Ponce de Leon M., Xu R., Hou W., Whitbeck J. C., Krummenacher C., Montgomery R. I., Spear P. G., Eisenberg R. J., Cohen G. H. 1998; Monoclonal antibodies to distinct sites on herpes simplex virus (HSV) glycoprotein D block HSV binding to HVEM. J Virol 72:3595–3601
    [Google Scholar]
  34. Ogita H., Takai Y. 2006; Activation of Rap1, Cdc42, and Rac by nectin adhesion system. Methods Enzymol 406:415–424
    [Google Scholar]
  35. Parry C., Bell S., Minson T., Browne H. 2005; Herpes simplex virus type 1 glycoprotein H binds to αv β3 integrins. J Gen Virol 86:7–10
    [Google Scholar]
  36. Patton D. L., Askienazy-Elbhar M., Henry-Suchet J., Campbell L. A., Cappuccio A., Tannous W., Wang S. P., Kuo C. C. 1994; Detection of Chlamydia trachomatis in fallopian tube tissue in women with postinfectious tubal infertility. Am J Obstet Gynecol 171:95–101
    [Google Scholar]
  37. Peipert J. F. 2003; Clinical practice. Genital chlamydial infections. N Engl J Med 349:2424–2430
    [Google Scholar]
  38. Roizman B., Knipe D. M. 2001 Herpes simplex viruses and their replication. Chapter 72 in Field's Virology, 4th edn. pp 2399–2459 Edited by Knipe D. M., Howley P. M. Baltimore, MD: Lippincott Williams and Wilkins;
    [Google Scholar]
  39. Satoh T., Arii J., Suenaga T., Wang J., Kogure A., Uehori J., Arase N., Shiratori I., Tanaka S. other authors 2008; PILR α is a herpes simplex virus-1 entry co-receptor that associates with glycoprotein B. Cell 132:935–944
    [Google Scholar]
  40. Savage C. O., Hughes C. C., Pepinsky R. B., Wallner B. P., Freedman A. S., Pober J. S. 1991; Endothelial cell lymphocyte function-associated antigen-3 and an unidentified ligand act in concert to provide costimulation to human peripheral blood CD4+ T cells. Cell Immunol 137:150–163
    [Google Scholar]
  41. Sciortino M. T., Medici M. A., Marino-Merlo F., Zaccaria D., Giuffre M., Venuti A., Grelli S., Mastino A. 2007; Signaling pathway used by HSV-1 to induce NF- κB activation: possible role of herpes virus entry receptor A. Ann N Y Acad Sci 1096:89–96
    [Google Scholar]
  42. Sciortino M. T., Medici M. A., Marino-Merlo F., Zaccaria D., Giuffrè-Cuculletto M., Venuti A., Grelli S., Bramanti P., Mastino A. 2008; Involvement of gD/HVEM interaction in NF- κB-dependent inhibition of apoptosis by HSV-1 gD. Biochem Pharmacol 76:1522–1532
    [Google Scholar]
  43. Shimizu K., Takai Y. 2003; Roles of the intercellular adhesion molecule nectin in intracellular signaling. J Biochem 134:631–636
    [Google Scholar]
  44. Shukla D., Liu J., Blaiklock P., Shworak N. W., Bai X., Esko J. D., Cohen G. H., Eisenberg R. J., Rosenberg R. D., Spear P. G. 1999; A novel role for 3- O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13–22
    [Google Scholar]
  45. Spear P. G. 2004; Herpes simplex virus: receptors and ligands for cell entry. Cell Microbiol 6:401–410
    [Google Scholar]
  46. Vanover J., Sun J., Deka S., Kintner J., Duffourc M. M., Schoborg R. V. 2008; Herpes simplex virus co-infection-induced Chlamydia trachomatis persistence is not mediated by any known persistence inducer or anti-chlamydial pathway. Microbiology 154:971–978
    [Google Scholar]
  47. Wyrick P. B., Choong J., Knight S. T., Goyeau D., Stuart E. S., MacDonald A. B. 1994; Chlamydia trachomatis antigens on the surface of infected human endometrial epithelial cells. Immunol Infect Dis 4:131–141
    [Google Scholar]
  48. Wyrick P. B. Jr G. G. D Knight S. T., Raulston J. E. 1996; Accelerated development of genital Chlamydia trachomatis serovar E in McCoy cells grown on microcarrier beads. Microb Pathog 20:31–40
    [Google Scholar]
  49. Yoon M., Zago A., Shukla D., Spear P. G. 2003; Mutations in the N termini of herpes simplex virus type 1 and 2 gDs alter functional interactions with the entry/fusion receptors HVEM, nectin-2, and 3- O-sulfated heparan sulfate but not with nectin-1. J Virol 77:9221–9231
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.036566-0
Loading
/content/journal/micro/10.1099/mic.0.036566-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error