Home LiteratureArticle Details
PMID: 16352536 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

CD8+ T cells require perforin to clear West Nile virus from infected neurons.

Journal of virology ·Vol. 80 ·No. 1 ·2006-01-00 ·Pages 119-29

Shrestha B, Samuel MA, Diamond MS

Abstract

Injury to neurons after West Nile virus (WNV) infection is believed to occur because of viral and host immune-mediated effects. Previously, we demonstrated that CD8+ T cells are required for the resolution of WNV infection in the central nervous system (CNS). CD8+ T cells can control infection by producing antiviral cytokines (e.g., gamma interferon or tumor necrosis factor alpha) or by triggering death of infected cells through perforin- or Fas ligand-dependent pathways. Here, we directly evaluated the role of perforin in controlling infection of a lineage I New York isolate of WNV in mice. A genetic deficiency of perforin molecules resulted in higher viral burden in the CNS and increased mortality after WNV infection. In the few perforin-deficient mice that survived initial challenge, viral persistence was observed in the CNS for several weeks. CD8+ T cells required perforin to control WNV infection as adoptive transfer of WNV-primed wild-type but not perforin-deficient CD8+ T cells greatly reduced infection in the brain and spinal cord and enhanced survival of CD8-deficient mice. Analogous results were obtained when wild-type or perforin-deficient CD8+ T cells were added to congenic primary cortical neuron cultures. Taken together, our data suggest that despite the risk of immunopathogenesis, CD8+ T cells use a perforin-dependent mechanism to clear WNV from infected neurons.

MeSH Terms
Animals CD8-Positive T-Lymphocytes/immunology,physiology Membrane Glycoproteins/deficiency,pharmacology Mice Mice, Inbred C57BL Neurons/drug effects,virology Perforin Pore Forming Cytotoxic Proteins/deficiency,pharmacology West Nile Fever/immunology West Nile virus/drug effects,pathogenicity,physiology
Chemicals
Membrane Glycoproteins Pore Forming Cytotoxic Proteins Perforin
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Shrestha Bimmi
Departments of Medicine, Molecular Microbiology, Pathology & Immunology, Washington University School of Medicine, 660 South Euclid Ave., Box 8051, St. Louis, MO 63110, USA.
Samuel Melanie A
Diamond Michael S
References (67)
67 references, click to expand
  1. West Nile virus neuroinvasion and encephalitis induced by macrophage depletion in mice.
    Arch Virol. 1996;141(3-4):459-69 PMID: 8645088
  2. Phenotypic changes in Langerhans' cells after infection with arboviruses: a role in the immune response to epidermally acquired viral infection?
    J Virol. 1996 Jul;70(7):4761-6 PMID: 8676503
  3. Mouse hepatitis virus is cleared from the central nervous systems of mice lacking perforin-mediated cytolysis.
    J Virol. 1997 Jan;71(1):383-91 PMID: 8985361
  4. Exocytosis and Fas mediated cytolytic mechanisms exert protection from West Nile virus induced encephalitis in mice.
    Immunol Cell Biol. 2004 Apr;82(2):170-3 PMID: 15061770
  5. Critical role of CD4 T cells in an antibody-independent mechanism of vaccination against gammaherpesvirus latency.
    J Virol. 2004 Jul;78(13):6836-45 PMID: 15194759
  6. Protective effect of vitamin E against focal brain ischemia and neuronal death through induction of target genes of hypoxia-inducible factor-1.
    Neuroscience. 2004;126(2):433-40 PMID: 15207361
  7. Langerhans cells migrate to local lymph nodes following cutaneous infection with an arbovirus.
    J Invest Dermatol. 2000 Mar;114(3):560-8 PMID: 10692118
  8. In vivo natural killer cell activities revealed by natural killer cell-deficient mice.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2731-6 PMID: 10694580
  9. The West Nile Virus outbreak of 1999 in New York: the Flushing Hospital experience.
    Clin Infect Dis. 2000 Mar;30(3):413-8 PMID: 10722421
  10. Pathology of fatal West Nile virus infections in native and exotic birds during the 1999 outbreak in New York City, New York.
    Vet Pathol. 2000 May;37(3):208-24 PMID: 10810985
  11. CD8+ T cell effector mechanisms in resistance to infection.
    Annu Rev Immunol. 2000;18:275-308 PMID: 10837060
  12. The role of CD8(+) T cells and major histocompatibility complex class I expression in the central nervous system of mice infected with neurovirulent Sindbis virus.
    J Virol. 2000 Jul;74(13):6117-25 PMID: 10846095
  13. Human skin Langerhans cells are targets of dengue virus infection.
    Nat Med. 2000 Jul;6(7):816-20 PMID: 10888933
  14. Rapid detection of west nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay.
    J Clin Microbiol. 2000 Nov;38(11):4066-71 PMID: 11060069
  15. Theiler's virus infection of perforin-deficient mice.
    J Virol. 1998 May;72(5):4515-9 PMID: 9557751
  16. West Nile encephalitis epidemic in southeastern Romania.
    Lancet. 1998 Sep 5;352(9130):767-71 PMID: 9737281
  17. How do cytotoxic lymphocytes kill their targets?
    Curr Opin Immunol. 1998 Oct;10(5):581-7 PMID: 9794837
  18. Single H2Kb, H2Db and double H2KbDb knockout mice: peripheral CD8+ T cell repertoire and anti-lymphocytic choriomeningitis virus cytolytic responses.
    Eur J Immunol. 1999 Apr;29(4):1243-52 PMID: 10229092
  19. Cell surface expression of H2 antigens on primary sensory neurons in response to acute but not latent herpes simplex virus infection in vivo.
    J Virol. 1999 Aug;73(8):6484-9 PMID: 10400743
  20. West Nile fever--a reemerging mosquito-borne viral disease in Europe.
    Emerg Infect Dis. 1999 Sep-Oct;5(5):643-50 PMID: 10511520
  21. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis.
    Nat Med. 2004 Dec;10(12):1366-73 PMID: 15558055
  22. Structure and intracellular targeting of the SARS-coronavirus Orf7a accessory protein.
    Structure. 2005 Jan;13(1):75-85 PMID: 15642263
  23. Gamma interferon-dependent, noncytolytic clearance of sindbis virus infection from neurons in vitro.
    J Virol. 2005 May;79(9):5374-85 PMID: 15827152
  24. Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis.
    J Virol. 2005 Sep;79(17):11457-66 PMID: 16103196
  25. Alpha/beta interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival.
    J Virol. 2005 Nov;79(21):13350-61 PMID: 16227257
  26. Interferon-gamma-mediated site-specific clearance of alphavirus from CNS neurons.
    Science. 2001 Jul 13;293(5528):303-6 PMID: 11452126
  27. Interleukin-1beta but not tumor necrosis factor is involved in West Nile virus-induced Langerhans cell migration from the skin in C57BL/6 mice.
    J Invest Dermatol. 2001 Sep;117(3):702-9 PMID: 11564180
  28. The relationships between West Nile and Kunjin viruses.
    Emerg Infect Dis. 2001 Jul-Aug;7(4):697-705 PMID: 11585535
  29. West Nile virus infection in the golden hamster (Mesocricetus auratus): a model for West Nile encephalitis.
    Emerg Infect Dis. 2001 Jul-Aug;7(4):714-21 PMID: 11585537
  30. Lymphocyte-mediated cytotoxicity.
    Annu Rev Immunol. 2002;20:323-70 PMID: 11861606
  31. Lack of both Fas ligand and perforin protects from flavivirus-mediated encephalitis in mice.
    J Virol. 2002 Apr;76(7):3202-11 PMID: 11884544
  32. Human dendritic cells as targets of dengue virus infection.
    J Investig Dermatol Symp Proc. 2001 Dec;6(3):219-24 PMID: 11924831
  33. Influence of effector molecules on the CD8(+) T cell response to infection.
    Curr Opin Immunol. 2002 Jun;14(3):360-5 PMID: 11973135
  34. Contribution of T cells to mortality in neurovirulent Sindbis virus encephalomyelitis.
    J Neuroimmunol. 2002 Jun;127(1-2):106-14 PMID: 12044981
  35. A poliomyelitis-like syndrome from West Nile virus infection.
    N Engl J Med. 2002 Oct 17;347(16):1279-80 PMID: 12270971
  36. West Nile poliomyelitis.
    Lancet Infect Dis. 2003 Jan;3(1):9-10 PMID: 12505023
  37. B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus.
    J Virol. 2003 Feb;77(4):2578-86 PMID: 12551996
  38. Immune-mediated clearance of virus from the central nervous system.
    Microbes Infect. 2003 Apr;5(5):439-48 PMID: 12738000
  39. Evasion of innate and adaptive immunity by flaviviruses.
    Immunol Cell Biol. 2003 Jun;81(3):196-206 PMID: 12752684
  40. Interaction of flaviviruses with cells of the vertebrate host and decoy of the immune response.
    Immunol Cell Biol. 2003 Jun;81(3):207-16 PMID: 12752685
  41. IFN-gamma-producing gamma delta T cells help control murine West Nile virus infection.
    J Immunol. 2003 Sep 1;171(5):2524-31 PMID: 12928402
  42. Innate and adaptive immune responses determine protection against disseminated infection by West Nile encephalitis virus.
    Viral Immunol. 2003;16(3):259-78 PMID: 14583143
  43. Antibody prophylaxis and therapy against West Nile virus infection in wild-type and immunodeficient mice.
    J Virol. 2003 Dec;77(24):12941-9 PMID: 14645550
  44. Infection and injury of neurons by West Nile encephalitis virus.
    J Virol. 2003 Dec;77(24):13203-13 PMID: 14645577
  45. CD8+ T cells mediate recovery and immunopathology in West Nile virus encephalitis.
    J Virol. 2003 Dec;77(24):13323-34 PMID: 14645588
  46. Early activation of natural killer and B cells in response to primary dengue virus infection in A/J mice.
    Virology. 2004 Feb 20;319(2):262-73 PMID: 14980486
  47. MHC class I-restricted killing of neurons by virus-specific CD8+ T lymphocytes is effected through the Fas/FasL, but not the perforin pathway,.
    Eur J Immunol. 2000 Dec;30(12):3623-33 PMID: 11169405
  48. Infection of human dendritic cells by dengue virus causes cell maturation and cytokine production.
    J Immunol. 2001 Feb 1;166(3):1499-506 PMID: 11160189
  49. Human dendritic cells are activated by dengue virus infection: enhancement by gamma interferon and implications for disease pathogenesis.
    J Virol. 2001 Apr;75(8):3501-8 PMID: 11264339
  50. Immunity to West Nile virus.
    Curr Opin Immunol. 2004 Aug;16(4):519-23 PMID: 15245749
  51. Role of CD8+ T cells in control of West Nile virus infection.
    J Virol. 2004 Aug;78(15):8312-21 PMID: 15254203
  52. Pathogenesis of West Nile Virus encephalitis in mice and rats. 1. Influence of age and species on mortality and infection.
    Am J Epidemiol. 1967 Nov;86(3):765-75 PMID: 6081390
  53. Pathogenesis of West Nile Virus encepahlitis in mice and rats. II. Virus multiplication, evolution of immunofluorescence, and development of histological lesions in the brain.
    Am J Epidemiol. 1967 Nov;86(3):776-90 PMID: 4866286
  54. Experimental encephalitis following peripheral inoculation of West Nile virus in mice of different ages.
    J Hyg (Lond). 1970 Sep;68(3):435-46 PMID: 4917916
  55. Monoclonal antibody analysis of MHC expression in human brain biopsies: tissue ranging from "histologically normal" to that showing different levels of glial tumor involvement.
    J Immunol. 1986 Jun 1;136(11):4054-62 PMID: 2422272
  56. The primary in vivo murine cytotoxic T cell response to the flavivirus, West Nile.
    J Gen Virol. 1987 Jul;68 ( Pt 7):2001-6 PMID: 3496425
  57. MHC-specific cytotoxic T lymphocyte killing of dissociated sympathetic neuronal cultures.
    Am J Pathol. 1987 Sep;128(3):395-409 PMID: 3498368
  58. Interferon-independent increases in class I major histocompatibility complex antigen expression follow flavivirus infection.
    J Gen Virol. 1988 Oct;69 ( Pt 10):2535-43 PMID: 2844965
  59. Induction of class I major histocompatibility complex antigen expression by West Nile virus on gamma interferon-refractory early murine trophoblast cells.
    Proc Natl Acad Sci U S A. 1989 Feb;86(3):911-5 PMID: 2492666
  60. The expression of major histocompatibility complex (MHC) class I antigens in the brain differs markedly in acute and persistent infections with lymphocytic choriomeningitis virus (LCMV).
    J Neuroimmunol. 1992 Feb;36(2-3):193-8 PMID: 1732281
  61. Broad cross-reactivity with marked fine specificity in the cytotoxic T cell response to flaviviruses.
    J Gen Virol. 1992 May;73 ( Pt 5):1115-23 PMID: 1375278
  62. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice.
    Nature. 1994 May 5;369(6475):31-7 PMID: 8164737
  63. The flavivirus nonstructural protein NS3 is a dominant source of cytotoxic T cell peptide determinants.
    Virology. 1994 Jul;202(1):195-201 PMID: 7516597
  64. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity.
    Science. 1994 Jul 22;265(5171):528-30 PMID: 7518614
  65. Flavivirus West Nile (Sarafend) egress at the plasma membrane.
    Arch Virol. 1994;137(3-4):303-13 PMID: 7944952
  66. Loss of active neuroinvasiveness in attenuated strains of West Nile virus: pathogenicity in immunocompetent and SCID mice.
    Arch Virol. 1994;137(3-4):355-70 PMID: 7944955
  67. Immune function in mice lacking the perforin gene.
    Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10854-8 PMID: 7526382
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2006-01-00
Pages
119-29
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC1317548
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com