Journal of Reproductive Immunology
Volume 84, Issue 1 , Pages 8-15 , January 2010

Herpes simplex virus (HSV)-specific T cells activated in the absence of IFN-gamma express alternative effector functions but are not protective against genital HSV-2 infection

  • Alison J. Johnson

      Affiliations

    • Department of Microbiology and Immunology, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555, USA
  • ,
  • Michelle H. Nelson

      Affiliations

    • Department of Microbiology and Immunology, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555, USA
  • ,
  • Melanie D. Bird

      Affiliations

    • Department of Pathology, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555, USA
    • Present address: Department of Surgery, Burn Shock Trauma Institute, Loyola Medical Center, Maywood, IL 60153, USA.
  • ,
  • Chin-Fun Chu

      Affiliations

    • Department of Pediatrics, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555, USA
  • ,
  • Gregg N. Milligan

      Affiliations

    • Department of Microbiology and Immunology, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555, USA
    • Department of Pediatrics, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555, USA
    • Sealy Center for Vaccine Development, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555, USA
    • Corresponding Author InformationCorresponding author at: Department of Pediatrics, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555-0436, USA. Tel.: +1 409 747 8145; fax: +1 409 747 8150.

Received 16 July 2009 ,Revised 3 September 2009 ,Accepted 16 September 2009.

References 

  1. Ashkar AA, Rosenthal KL. Interleukin-15 and natural killer and NKT cells play a critical role in innate protection against genital herpes simplex virus type 2 infection. J. Virol. 2003;77:10168–10171
  2. Badovinac VP, Tvinnereim AR, Harty JT. Regulation of antigen-specific CD8+ T cell homeostasis by perforin and interferon-gamma. Science. 2001;290:1354–1358
  3. Bird MD, Chu C-F, Johnson AJ, Milligan GN. Early resolution of herpes simplex virus type 2 infection of the murine genital tract involves stimulation of genital parenchymal cells by gamma interferon. J. Virol. 2007;81:423–426
  4. Bouley DM, Kanangat S, Wire W, Rouse BT. Characterization of herpes simplex virus type-1 infection and herpetic stromal keratitis development in IFNγ knockout mice. J. Immunol. 1995;155:3964–3971
  5. Chu C-F, Meador JG, Young CG, Strasser JE, Bourne N, Milligan GN. Antibody-mediated protection against genital herpes simplex virus type 2 disease in mice by Fc gamma receptor-dependent and -independent mechanisms. J. Reprod. Immunol. 2008;78:58–67
  6. Corey L, Wald S, Celum CL, Quinn TC. The effects of herpes simplex virus-2 on HIV-1 acquisition and transmission: a review of two overlapping epidemics. J. Acquir. Immune Defic. Syndr. 2004;35:435–445
  7. Dix RD, Pereira L, Baringer JR. Use of monoclonal antibody directed against herpes simplex virus glycoproteins to protect mice against acute virus-induced neurological disease. Infect. Immun. 1981;34:192–199
  8. Dobbs ME, Strasser JE, Chu C-F, Chalk C, Milligan GN. Clearance of herpes simplex virus type 2 by CD8+ T cells requires gamma interferon and either perforin- or Fas-mediated cytolytic mechanisms. J. Virol. 2005;79:14545–14554
  9. Dudley KL, Bourne N, Milligan GN. Immune protection against HSV-2 in B-cell-deficient mice. Virology. 2000;270:454–463
  10. Harandi AM, Svennerholm B, Holmgren JH, Eriksson K. Interleukin-12 (IL-12) and IL-18 are important in innate defense against genital herpes simplex virus type 2 infection in mice but are not required for the development of acquired gamma interferon-mediated protective immunity. J. Virol. 2001;75:6705–6709
  11. Harandi AM, Svennerholm B, Holmgren J, Eriksson K. Differential roles of B cells and IFNgamma-secreting CD4 (+) T cells in innate and adaptive immune control of genital herpes simplex virus type 2 infection in mice. J. Gen. Virol. 2001;82:845–853
  12. Ijima N, Linehan MM, Zamora M, Butkus D, Dunn R, Kehry MR, et al. Dendritic cells and B cells maximize mucosal Th1 memory response to herpes simplex virus. J. Exp. Med. 2008;205:3041–3052
  13. Ito M, O-Malley JA. Antiviral effects of recombinant human tumor necrosis factor. Lymphokine Res. 1987;6:309–318
  14. Johnson AJ, Chu CF, Milligan GN. Effector CD4+ T-cell involvement in clearance of infectious herpes simplex virus type 1 from sensory ganglia and spinal cords. J. Virol. 2008;82:9678–9688
  15. Kaushic C, Ashkar AA, Reid LA, Rosenthal KL. Progesterone increases susceptibility and decreases immune responses to genital herpes infection. J. Virol. 2003;77:4558–4565
  16. Koelle DM, Posavad CM, Barnum GR, Johnson ML, Frank JM, Corey L. Clearance of HSV-2 from recurrent genital lesions correlates with infiltration of HSV-specific cytotoxic T lymphocytes. J. Clin. Invest. 1998;101:1500–1508
  17. Kohl S, Strynadka NCJ, Hodges RS, Pereira L. Analysis of the role of antibody-dependent cellular cytotoxicity antibody activity in murine neonatal herpes simplex virus infection with anti bodies to synthetic peptides of glycoprotein D and monoclonal antibodies to glycoprotein B. J. Clin. Invest. 1990;86:273–278
  18. Kuklin NA, Daheshia M, Chun S, Rouse BT. Role of mucosal immunity in herpes simplex virus infection. J. Immunol. 1998;160:5998–6003
  19. Linehan MM, Richman S, Krummenacher C, Eissenberg RJ, Cohen GH, Iwasaki A. In vivo role of nectin-1 in entry of herpes simplex virus type 1 (HSV-1) and HSV-2 through the vaginal mucosa. J. Virol. 2004;78:2530–2536
  20. McDermott MR, Smiley JR, Leslie P, Brais J, Rudzroga HE, Bienenstock J. Immunity in the female genital tract after intravaginal vaccination of mice with an attenuated strain of herpes simplex virus type 2. J. Virol. 1984;51:747–753
  21. Mikloska Z, Cunningham AL. Alpha and gamma interferons inhibit herpes simplex virus type 1 infection and spread in epidermal cells after axonal transmission. J. Virol. 2001;75:11821–11826
  22. Milligan GN, Bernstein DI. Analysis of herpes simplex virus-specific T cells in the murine female genital tract following genital infection with herpes simplex virus type 2. Virology. 1995;212:481–489
  23. Milligan GN, Bernstein DI. Interferon-gamma enhances resolution of herpes simplex virus type 2 infection of the murine genital tract. Virology. 1997;229:259–268
  24. Milligan GN, Bernstein DI, Bourne N. T lymphocytes are required for protection of the vaginal mucosae and sensory ganglia of immune mice against reinfection with herpes simplex virus type 2. J. Immunol. 1998;160:6093–6100
  25. Milligan GN, Bourne N, Dudley KL. Role of polymorphonuclear leukocytes in resolution of HSV-2 infection of the mouse vagina. J. Reprod. Immunol. 2001;49:49–65
  26. Milligan GN, Dudley-McClain KL, Young CG, Chu C-F. T-cell-mediated mechanisms involved in resolution of genital herpes simplex virus type 2 (HSV-2) infection of mice. J. Reprod. Immunol. 2004;61:115–127
  27. Parr EL, Parr MB. Immunoglobulin G, plasma cells, and lymphocytes in the murine vagina after vaginal or parenteral immunization with attenuated herpes simplex virus type 2. J. Virol. 1998;72:5137–5145
  28. Parr MB, Parr EL. The role of gamma interferon in immune resistance to vaginal infection by herpes simplex virus type 2 in mice. Virology. 1999;258:282–294
  29. Pierce AT, DeSalvo J, Foster TP, Kosinski A, Weller SK, Halford WP. Beta interferon and gamma interferon synergize to block viral DNA and virion synthesis in herpes simplex virus-infected cells. J. Gen. Virol. 2005;86:2421–2432
  30. Posavad CM, Koelle DM, Shaughnessy MF, Corey L. Severe genital herpes infections in HIV-infected individuals with impaired herpes simplex virus-specific CD8+ cytotoxic T lymphocyte responses. Proc. Natl. Acad. Sci. U.S.A. 1997;94:10289–10294
  31. Rossol-Voth R, Rossol S, Schutt KH, de Cian W, Falke D. In vivo protective effect of tumour necrosis factor alpha against experimental infection with herpes simplex virus type 1. J. Gen. Virol. 1991;72:143–147
  32. Sainz B, Halford WP. Alpha/Beta interferon and gamma interferon synergize to inhibit the replication of herpes simplex virus type 1. J. Virol. 2002;76:11541–11550
  33. Smith PM, Wolcott RM, Chervenak R, Jennings SR. Control of acute cutaneous herpes simplex virus infection: T cell-mediated viral clearance is dependent upon interferon-γ. Virology. 1994;202:76–88
  34. Tsunobuchi H, Hishimura H, Goshima F, Daikoku T, Suzuki H, Nakashima I, et al. A protective role of interleukin-15 in a mouse model for systemic infection with herpes simplex virus. Virology. 2000;275:57–66
  35. Tumpey TM, Chen SH, Oakes JE, Lausch RN. Neutrophil-mediated suppression of virus replication after herpes simplex virus type 1 infection of the murine cornea. J. Virol. 1996;70:898–904
  36. Wald A, Link K. Risk of human immunodeficiency virus infection in herpes simplex virus type 2-seropositive persons: a meta-analysis. J. Infect. Dis. 2002;18:45–52
  37. Wald A, Zeh J, Selke S, Warren T, Ryncarz AJ, Ashley , et al. Reactivation of genital herpes simplex virus type 2 infection in asymptomatic seropositive persons. N. Engl. J. Med. 2000;342:844–850
  38. Yu A, Manickan E, Rouse BT. Role of interferon-γ in immunity to herpes simplex virus. J. Leuk. Biol. 1996;60:528–532
  39. Zhu J, Koelle DM, Cao J, Vazquez J, Huang ML, Hladik F, et al. Virus-specific CD8+ T cells accumulate near sensory nerve endings in genital skin during subclinical HSV-2 reactivation. J. Exp. Med. 2007;204:595–603

PII: S0165-0378(09)00498-7

doi: 10.1016/j.jri.2009.09.007

Journal of Reproductive Immunology
Volume 84, Issue 1 , Pages 8-15 , January 2010