SpringerLink
Log in

T cell receptor signaling pathways: New targets for herpes simplex virus

  • Published:
Virologica Sinica

Abstract

Herpes simplex viruses (HSV-1 and HSV-2) cause global morbidity and synergistically correlate with HIV infection. HSV exists life-long in a latent form in sensory neurons with intermittent reactivation, in despite of host immune surveillance. While abundant evidence for HSV interfering with innate immune responses so as to favor the replication and propagation of the virus, several lines of evidence declare that HSV attenuates adaptive immunity by various mechanisms, including but not limited to the ablation of antigen presentation, induction of apoptosis, and interruption of cellular signaling. In this review, we will focus on the perturbative role of HSV in T cells signaling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Abraham R T, Weiss A. 2004. Jurkat T cells and development of the T-cell receptor signalling paradigm. Nat Rev Immunol, 4: 301–308.

    Article  PubMed  CAS  Google Scholar 

  2. Alegre M L, Frauwirth K A, Thompson C B. 2001. T-cell regulation by CD28 and CTLA-4. Nat Rev Immunol, 1: 220–228.

    Article  PubMed  CAS  Google Scholar 

  3. Aubert M, Blaho J A. 2001. Modulation of apoptosis during herpes simplex virus infection in human cells. Microbes Infect, 3: 859–866.

    Article  PubMed  CAS  Google Scholar 

  4. Barcy S, Corey L. 2001. Herpes simplex inhibits the capacity of lymphoblastoid B cell lines to stimulate CD4+ T cells. J Immunol, 166: 6242–6249.

    PubMed  CAS  Google Scholar 

  5. Benetti L, Roizman B. 2004. Herpes simplex virus protein kinase US3 activates and functionally overlaps protein kinase A to block apoptosis. Proc Natl Acad Sci USA, 101: 9411–9416.

    Article  PubMed  CAS  Google Scholar 

  6. Braun R W, Teute H K, Kirchner H, et al. 1984. Replication of herpes simplex virus in human T lymphocytes: characterization of the viral target cell. J Immunol, 132: 914–919.

    PubMed  CAS  Google Scholar 

  7. Carfi A, Willis S H, Whitbeck J C, et al. 2001. Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol Cell, 8: 169–179.

    Article  PubMed  CAS  Google Scholar 

  8. Celum C L. 2004. The interaction between herpes simplex virus and human immunodeficiency virus. Herpes, Suppl 1: 36A–45A.

    Google Scholar 

  9. Chan A C, Dalton M, Johnson R, et al. 1995. Activation of ZAP-70 kinase activity by phosphorylation of tyrosine 493 is required for lymphocyte antigen receptor function. EMBO J, 14: 2499–2508.

    PubMed  CAS  Google Scholar 

  10. Cheshenko N, Liu W, Satlin L M, et al. 2007. Multiple receptor interactions trigger release of membrane and intracellular calcium stores critical for herpes simplex virus entry. Mol Biol Cell, 18: 3119–3130.

    Article  PubMed  CAS  Google Scholar 

  11. Chuang E, Fisher T S, Morgan R W, et al. 2000. The CD28 and CTLA-4 receptors associate with the serine/ threonine phosphatase PP2A. Immunity, 13: 313–322

    Article  PubMed  CAS  Google Scholar 

  12. Cheung T C, Humphreys I R, Potter K G, et al. 2005. Evolutionarily divergent herpesviruses modulate T cell activation by targeting the herpesvirus entry mediator cosignaling pathway. Proc Natl Acad Sci USA, 102: 13218–3223.

    Article  PubMed  CAS  Google Scholar 

  13. Compaan D M, Gonzalez L C, Tom I, et al. 2005. Attenuating lymphocyte activity: the crystal structure of the BTLA-HVEM complex. J Biol Chem, 280: 39553–39561.

    Article  PubMed  CAS  Google Scholar 

  14. Corey L, Wald A, Celum C L, et al. 2004. The effects of herpes simplex virus-2 on HIV-1 acquisition and transmission: a review of two overlap** epidemics. J Acquir Immune Defic Syndr, 35(5): 435–445.

    Article  PubMed  Google Scholar 

  15. Coudronniere N, Villalba M, Englund N, et al. 2000. NF-kappa B activation induced by T cell receptor/CD28 costimulation is mediated by protein kinase C-theta. Proc Natl Acad Sci USA, 97: 3394–3399.

    Article  PubMed  CAS  Google Scholar 

  16. Cowan FM, Humphrey J H, Ntozini R, et al. 2008. Maternal Herpes simplex virus type 2 infection, syphilis and risk of intra-partum transmission of HIV-1: results of a case control study. AIDS, 22(2): 193–201.

    PubMed  Google Scholar 

  17. Derijard B, Hibi M, Wu I H, et al. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell, 76: 1025–1037.

    Article  PubMed  CAS  Google Scholar 

  18. Fruh K, Ahn K, Djaballah H, et al. 1995. A viral inhibitor of peptide transporters for antigen presentation. Nature, 375: 415–418.

    Article  PubMed  CAS  Google Scholar 

  19. Gavrieli M, Watanabe N, Loftin S K, et al. 2003. Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of B and T lymphocyte attenuator required for association with protein tyrosine phosphatases SHP-1 and SHP-2. Biochem Biophys Res Commun, 312: 1236–1243.

    Article  PubMed  CAS  Google Scholar 

  20. Golembewski E K, Wales S Q, Aurelian L, et al. 2007. The HSV-2 protein ICP10PK prevents neuronal apoptosis and loss of function in an in vivo model of neurode-generation associated with glutamate excitotoxicity. Exp Neurol, 203: 381–393.

    Article  PubMed  CAS  Google Scholar 

  21. Gonzalez L C, Loyet K M, Calemine-Fenaux J, et al. 2005. A coreceptor interaction between the CD28 and TNF receptor family members B and T lymphocyte attenuator and herpesvirus entry mediator. Proc Natl Acad Sci USA, 102: 1116–1121.

    Article  PubMed  CAS  Google Scholar 

  22. Goodkin M L, Morton E R, Blaho J A. 2004. Herpes simplex virus infection and apoptosis. Int Rev Immunol, 23: 141–172.

    Article  PubMed  CAS  Google Scholar 

  23. Gupta A, Gartner J J, Sethupathy P, et al. 2006. Anti-apoptotic function of a microRNA encoded by the HSV-1 latency-associated transcript. Nature, 442: 82–85.

    PubMed  CAS  Google Scholar 

  24. Hammer S M, Carney W P, Iacoviello V R, et al. 1982. Herpes simplex virus infection of human T-cell subpopulations. Infect Immun, 38: 795–797.

    PubMed  CAS  Google Scholar 

  25. Han J Y, Sloan D D, Aubert M, et al. 2007. Apoptosis and antigen receptor function in T and B cells following exposure to herpes simplex virus. Virology, 359: 253–263.

    Article  PubMed  CAS  Google Scholar 

  26. Hargett D, McLean T, Bachenheimer S L. 2005. Herpes simplex virus ICP27 activation of stress kinases JNK and p38. J Virol, 79: 8348–8360.

    Article  PubMed  CAS  Google Scholar 

  27. Houtman J C, Houghtling R A, Barda-Saad M, et al. 2005. Early phosphorylation kinetics of proteins involved in proximal TCR-mediated signaling pathways. J Immunol, 175: 2449–2458.

    PubMed  CAS  Google Scholar 

  28. Hsu H, Solovyev I, Colombero A, et al. 1997. ATAR, a novel tumor necrosis factor receptor family member, signals through TRAF2 and TRAF5. J Biol Chem, 272: 13471–13474.

    Article  PubMed  CAS  Google Scholar 

  29. Hughes K, Edin S, Antonsson A, et al. 2001. Calmodulin-dependent kinase II mediates T cell receptor/CD3-and phorbol ester-induced activation of IkappaB kinase. J Biol Chem, 276: 36008–36013.

    Article  PubMed  CAS  Google Scholar 

  30. Hurchla M A, Sedy J R, Gavrieli M, et al. 2005. B and T lymphocyte attenuator exhibits structural and expression polymorphisms and is highly Induced in anergic CD4+ T cells. J Immunol, 174: 3377–3385.

    PubMed  CAS  Google Scholar 

  31. Hutloff A, Dittrich A M, Beier K C, et al. 1999. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature, 397: 263–266.

    Article  PubMed  CAS  Google Scholar 

  32. Ito M, Watanabe M, Kamiya H, et al. 1997. Herpes simplex virus type 1 induces apoptosis in peripheral blood T lymphocytes. J Infect Dis, 175: 1220.

    Article  PubMed  CAS  Google Scholar 

  33. Iwahori S, Shirata N, Kawaguchi Y, et al. 2007. Enhanced phosphorylation of transcription factor sp1 in response to herpes simplex virus type 1 infection is dependent on the ataxia telangiectasia-mutated protein. J Virol, 81: 9653–9664.

    Article  PubMed  CAS  Google Scholar 

  34. Kim D B, DeLuca N A. 2002. Phosphorylation of Transcription Factor Sp1 during Herpes Simplex Virus Type 1 Infection. J Virol, 76: 6473–6479.

    Article  PubMed  CAS  Google Scholar 

  35. Kwon B S, Tan K B, Ni J, et al. 1997. A newly identified member of the tumor necrosis factor receptor superfamily with a wide tissue distribution and involvement in lymphocyte activation. J Biol Chem, 272: 14272–14276.

    Article  PubMed  CAS  Google Scholar 

  36. La S, Kim J, Kwon B S, et al. 2002. Herpes simplex virus type 1 glycoprotein D inhibits T-cell proliferation. Mol Cells, 14: 398–403.

    PubMed  CAS  Google Scholar 

  37. Lilley C E, Carson C T, Muotri A R, et al. 2005. DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc Natl Acad Sci USA, 102: 5844–5849.

    Article  PubMed  CAS  Google Scholar 

  38. Lin J, Weiss A. 2001. T cell receptor signaling. J Cell Sci, 114: 243–244.

    PubMed  CAS  Google Scholar 

  39. Marsters S A, Ayres T M, Skubatch M, et al. 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-kappaB and AP-1. J Biol Chem, 272: 14029–14032.

    Article  PubMed  CAS  Google Scholar 

  40. Mauri D N, Ebner R, Montgomery R I, et al. 1998. LIGHT, a new member of the TNF superfamily, and lymphotoxin alpha are ligands for herpesvirus entry mediator. Immunity, 8: 21–30.

    Article  PubMed  CAS  Google Scholar 

  41. Montgomery R I, Warner M S, Lum B J, et al. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell, 87: 427–436.

    Article  PubMed  CAS  Google Scholar 

  42. Mulvey M, Arias C, Mohr I. 2007. Maintenance of endoplasmic reticulum (ER) homeostasis in herpes simplex virus type 1-infected cells through the association of a viral glycoprotein with PERK, a cellular ER stress sensor. J Virol, 81: 3377–3390.

    Article  PubMed  CAS  Google Scholar 

  43. Murphy K M, Nelson C A, Sedy J R. 2006. Balancing co-stimulation and inhibition with BTLA and HVEM. Nat Rev Immunol, 6: 671–681.

    Article  PubMed  CAS  Google Scholar 

  44. Mustelin T, Tasken K. 2003. Positive and negative regulation of T-cell activation through kinases and phosphatases. Biochem J, 371: 15–27.

    Article  PubMed  CAS  Google Scholar 

  45. Nel A E. 2002. T-cell activation through the antigen receptor. Part 1: signaling components, signaling pathways, and signal integration at the T-cell antigen receptor synapse. J Allergy Clin Immunol, 109: 758–770.

    Article  PubMed  CAS  Google Scholar 

  46. Neumann J, Eis-Hubinger A M, Koch N. 2003. Herpes simplex virus type 1 targets the MHC class II processing pathway for immune evasion. J Immunol, 171: 3075–3083.

    PubMed  CAS  Google Scholar 

  47. Okazaki T, Maeda A, Nishimura H, et al. 2001. PD-1 immunoreceptor inhibits B cell receptor-mediated signaling by recruiting src homology 2-domain-containing tyrosine phosphatase 2 to phosphotyrosine. Proc Natl Acad Sci USA, 98: 13866–13871.

    Article  PubMed  CAS  Google Scholar 

  48. Okkenhaug K, Bilancio A, Emery J L, et al. 2004. Phosphoinositide 3-kinase in T cell activation and survival. Biochem Soc Trans, 32: 332–335.

    Article  PubMed  CAS  Google Scholar 

  49. Parry R V, Chemnitz J M, Frauwirth K A, et al. 2005. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol, 25: 9543–9553.

    Article  PubMed  CAS  Google Scholar 

  50. Pasieka T J, Baas T, Carter V S, et al. 2006. Functional genomic analysis of herpes simplex virus type 1 counteraction of the host innate response. J Virol, 80: 7600–7612.

    Article  PubMed  CAS  Google Scholar 

  51. Prasad K V, Cai Y C, Raab M, et al. 1994. T-cell antigen CD28 interacts with the lipid kinase phosphatidylinositol 3-kinase by a cytoplasmic Tyr(P)-Met-Xaa-Met motif. Proc Natl Acad Sci USA, 91: 2834–2838.

    Article  PubMed  CAS  Google Scholar 

  52. Raab M, Pfister S, Rudd C E. 2001. CD28 signaling via VAV/SLP-76 adaptors: regulation of cytokine transcription independent of TCR ligation. Immunity, 15: 921–933.

    Article  PubMed  CAS  Google Scholar 

  53. Raftery M J, Behrens C K, Muller A, t al. 1999. Herpes simplex virus type 1 infection of activated cytotoxic T cells: Induction of fratricide as a mechanism of viral immune evasion. J Exp Med, 190: 1103–1114.

  54. Roizman B, Knipe D M, Whitley R J. 2007. Herpes Simplex Viruses. In: Fields Virology (Knipe D M, Howley P M, eds.), 5th ed. Lippincott Williams & Wilkins, p2502–2602.

  55. Salvador J M, Mittelstadt P R, Guszczynski T, et al. 2005. Alternative p38 activation pathway mediated by T cell receptor-proximal tyrosine kinases. Nat Immunol, 6: 390–395.

    Article  PubMed  CAS  Google Scholar 

  56. Sedy J R, Gavrieli M, Potter K G, et al. 2005. B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat Immunol, 6: 90–98.

    Article  PubMed  CAS  Google Scholar 

  57. Sievers E, Neumann J, Raftery M, et al. 2002. Glycoprotein B from strain 17 of herpes simplex virus type I contains an invariant chain homologous sequence that binds to MHC class II molecules. Immunology, 107: 129–135.

    Article  PubMed  CAS  Google Scholar 

  58. Sloan D D, Han J Y, Sandifer T K, et al. 2006. Inhibition of TCR signaling by herpes simplex virus. J Immunol, 176: 1825–1833.

    PubMed  CAS  Google Scholar 

  59. Sloan D D, Jerome K R. 2007. Herpes simplex virus remodels T-cell receptor signaling, resulting in p38-dependent selective synthesis of interleukin-10. J Virol, 81: 12504–12514.

    Article  PubMed  CAS  Google Scholar 

  60. Sloan D D, Zahariadis G, Posavad C M, et al. 2003. CTL are inactivated by herpes simplex virus-infected cells expressing a viral protein kinase. J Immunol, 171: 6733–6741.

    PubMed  CAS  Google Scholar 

  61. Sommers C L, Menon R K, Grinberg A, et al. 2001. Knock-in mutation of the distal four tyrosines of linker for activation of T cells blocks murine T cell development. J Exp Med, 194: 135–142.

    Article  PubMed  CAS  Google Scholar 

  62. Sprecher E, Becker Y. 1989. Langerhans cell density and activity in mouse skin and lymph nodes affect herpes simplex type 1 (HSV-1) pathogenicity. Arch Virol, 107: 191–205.

    Article  PubMed  CAS  Google Scholar 

  63. Verjans G M, Hintzen R Q, van Dun J M, et al. 2007. Selective retention of herpes simplex virus-specific T cells in latently infected human trigeminal ganglia. Proc Natl Acad Sci USA, 104: 3496–3501.

    Article  PubMed  CAS  Google Scholar 

  64. Wange R L. 2000. LAT, the linker for activation of T cells: a bridge between T cell-specific and general signaling pathways. Sci STKE, 2000: RE1.

    Article  PubMed  CAS  Google Scholar 

  65. Watanabe N, Gavrieli M, Sedy J R, et al. 2003. BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat Immunol, 4: 670–679.

    Article  PubMed  CAS  Google Scholar 

  66. York I A, Roop C, Andrews D W, et al. 1994. A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes. Cell, 77: 525–535.

    Article  PubMed  CAS  Google Scholar 

  67. Zachos G, Clements B, Conner J. 1999. Herpes simplex virus type 1 infection stimulates p38/c-Jun N-terminal mitogen-activated protein kinase pathways and activates transcription factor AP-1. J Biol Chem, 274: 5097–5103.

    Article  PubMed  CAS  Google Scholar 

  68. Zhang J, Salo** K V, Gao J X, et al. 1999. p38 mitogen-activated protein kinase mediates signal integration of TCR/CD28 costimulation in primary murine T cells. J Immunol, 162: 3819–3829.

    PubMed  CAS  Google Scholar 

  69. Zhang W, Sloan-Lancaster J, Kitchen J, et al. 1998. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell, 92: 83–92.

    Article  PubMed  CAS  Google Scholar 

  70. Zhao X, Deak E, Soderberg K, et al. 2003. Vaginal Submucosal Dendritic Cells, but Not Langerhans Cells, Induce Protective Th1 Responses to Herpes Simplex Virus-2. J Exp Med, 197: 153–162.

    Article  PubMed  CAS  Google Scholar 

  71. Zhu M, Janssen E, Zhang W. 2003. Minimal requirement of tyrosine residues of linker for activation of T cells in TCR signaling and thymocyte development. J Immunol, 170: 325–333.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Bioactive Materials of Ministry of Education, Nankai University, Tian**, 300071, China

    You-jia Cao, Ya-peng Li & Cui-zhu Zhang

  2. Tian** Key Laboratory of Protein Sciences, Nankai University, Tian**, 300071, China

    You-jia Cao, Ying-chi Zhang & Cui-zhu Zhang

  3. Department of Biochemistry and Molecular Biology, College of Life Sciences, Nankai University, Tian**, 300071, China

    You-jia Cao, Ya-peng Li & Ying-chi Zhang

Authors
  1. You-jia Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ya-peng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ying-chi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cui-zhu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to You-jia Cao.

Additional information

Foundation items: National Natural Science Foundation of China (30670080); Ministry of Science and Technology of China (2007CB914800, 2006CB910103).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cao, Yj., Li, Yp., Zhang, Yc. et al. T cell receptor signaling pathways: New targets for herpes simplex virus. Virol. Sin. 23, 429–437 (2008). https://doi.org/10.1007/s12250-008-3000-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12250-008-3000-5

Key words

CLC number

Search

Navigation