Home LiteratureArticle Details
PMID: 7604887 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Lymphocyte apoptosis during the silencing of the immune response to acute viral infections in normal, lpr, and Bcl-2-transgenic mice.

The American journal of pathology ·Vol. 147 ·No. 1 ·1995-07-00 ·Pages 79-91

Razvi ES, Jiang Z, Woda BA, Welsh RM

Abstract

This report examines the mechanisms involved in the down-regulation of the immune response in acute viral infection and documents the presence of apoptotic lymphocytes in situ in the spleens of mice during the resolution of the immune response to acute lymphocytic choriomeningitis virus infection. Apoptotic cells were detected by an in situ nucleotidyl transferase assay. Both T and B lymphocytes were shown to be dying in vivo, the latter in clusters. A biphasic occurrence of apoptosis during the course of the acute infection was observed, with elevated levels occurring at day 3 after infection and a second more pronounced peak at day 11 after infection, coincident with the decline of the cytotoxic T lymphocyte response and with the decrease in total splenic leukocyte number. Apoptosis in vivo was detected in lpr mice, suggesting that Fas expression is not imperative for lymphocyte apoptosis in the context of an acute viral infection. Apoptosis in situ and the decline of the T lymphocyte response to acute lymphocytic choriomeningitis virus infection was unaffected by the enforced lymphocyte-directed expression of Bcl-2, a protein that blocks growth factor deprivation-induced apoptosis of lymphocytes in vitro. These results argue that the silencing of the T cell response to acute infection may not be a result simply of growth factor deprivation. The susceptibility of activated T cells to apoptotic death, which has previously been associated with virus-induced immune deficiency, may therefore also explain the en masse elimination of the expanded lymphocyte pool subsequent to an acute viral infection.

Related Genes
MeSH Terms
Acute Disease Animals Apoptosis Cell Death Cells, Cultured Down-Regulation Flow Cytometry Immunohistochemistry Leukocyte Count Lymphocytes/physiology Lymphocytic Choriomeningitis/immunology,pathology Lymphocytic choriomeningitis virus/immunology Lymphoproliferative Disorders/genetics,immunology,pathology Male Mice Mice, Inbred C57BL Mice, Transgenic Proto-Oncogene Proteins/genetics,immunology Proto-Oncogene Proteins c-bcl-2 Spleen/pathology
Chemicals
Proto-Oncogene Proteins Proto-Oncogene Proteins c-bcl-2
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Razvi E S
Department of Pathology, University of Massachusetts Medical Center, Worcester 10655-0125, USA.
Jiang Z
Woda B A
Welsh R M
References (36)
36 references, click to expand
  1. T-cell-mediated immunopathology in viral infections.
    Transplant Rev. 1974;19(0):89-120 PMID: 4601807
  2. The fas antigen is involved in peripheral but not thymic deletion of T lymphocytes in T cell receptor transgenic mice.
    Immunity. 1994 Aug;1(5):365-71 PMID: 7533645
  3. The virology and immunobiology of lymphocytic choriomeningitis virus infection.
    Adv Immunol. 1980;30:275-331 PMID: 6160740
  4. In vivo effector function of influenza virus-specific cytotoxic T lymphocyte clones is highly specific.
    J Exp Med. 1984 Sep 1;160(3):814-26 PMID: 6206190
  5. T lymphocytes in infectious mononucleosis. I. T cell death in vitro.
    Clin Exp Immunol. 1985 Apr;60(1):61-9 PMID: 3874017
  6. IL-2 addiction: withdrawal of growth factor activates a suicide program in dependent T cells.
    Lymphokine Res. 1986 Fall;5(4):289-99 PMID: 2946903
  7. Identification of a monoclonal antibody specific for a murine T3 polypeptide.
    Proc Natl Acad Sci U S A. 1987 Mar;84(5):1374-8 PMID: 2950524
  8. Cyclosporin A inhibits activation-induced cell death in T-cell hybridomas and thymocytes.
    Nature. 1989 Jun 22;339(6226):625-6 PMID: 2786609
  9. Lymphocytic choriomeningitis virus-induced immunodepression: inherent defect of B and T lymphocytes.
    J Virol. 1990 Sep;64(9):4076-83 PMID: 2143539
  10. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death.
    Nature. 1990 Nov 22;348(6299):334-6 PMID: 2250705
  11. T cell receptor/CD3-signaling induces death by apoptosis in human T cell receptor gamma delta + T cells.
    J Immunol. 1991 Jan 1;146(1):35-9 PMID: 1824593
  12. Interferon gamma plays a critical role in induced cell death of effector T cell: a possible third mechanism of self-tolerance.
    J Exp Med. 1990 Dec 1;172(6):1735-9 PMID: 2147950
  13. Receptor-stimulated death pathway is opened by antigen in mature T cells.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2151-5 PMID: 1826050
  14. Detection of apoptosis of immature CD4+8+ thymocytes by flow cytometry.
    J Immunol Methods. 1991 Mar 1;137(1):79-87 PMID: 1901329
  15. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease.
    Annu Rev Immunol. 1991;9:243-69 PMID: 1910678
  16. Interleukin-2 programs mouse alpha beta T lymphocytes for apoptosis.
    Nature. 1991 Oct 31;353(6347):858-61 PMID: 1944559
  17. bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes.
    Cell. 1991 Nov 29;67(5):879-88 PMID: 1835668
  18. bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship.
    Cell. 1991 Nov 29;67(5):889-99 PMID: 1959134
  19. Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals.
    J Exp Med. 1992 Feb 1;175(2):331-40 PMID: 1346269
  20. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis.
    Nature. 1992 Mar 26;356(6367):314-7 PMID: 1372394
  21. Roles of alpha beta and gamma delta T cell subsets in viral immunity.
    Annu Rev Immunol. 1992;10:123-51 PMID: 1534240
  22. Programmed death of T cells in HIV-1 infection.
    Science. 1992 Jul 10;257(5067):217-9 PMID: 1352911
  23. CD11b (Mac-1): a marker for CD8+ cytotoxic T cell activation and memory in virus infection.
    J Immunol. 1992 Aug 15;149(4):1326-33 PMID: 1500720
  24. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
    J Cell Biol. 1992 Nov;119(3):493-501 PMID: 1400587
  25. Interleukin 4 protects chronic lymphocytic leukemic B cells from death by apoptosis and upregulates Bcl-2 expression.
    J Exp Med. 1992 Nov 1;176(5):1319-26 PMID: 1402678
  26. Differential expression of apoptosis-related Fas antigen on lymphocyte subpopulations in human peripheral blood.
    J Immunol. 1992 Dec 1;149(11):3753-8 PMID: 1385530
  27. Suppression of apoptosis in a cytotoxic T-cell line by interleukin 2-mediated gene transcription and deregulated expression of the protooncogene bcl-2.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2189-93 PMID: 8460122
  28. Transcriptional repression and differential splicing of Fas mRNA by early transposon (ETn) insertion in autoimmune lpr mice.
    Biochem Biophys Res Commun. 1993 Mar 15;191(2):617-24 PMID: 7681668
  29. Phagocyte recognition of cells undergoing apoptosis.
    Immunol Today. 1993 Mar;14(3):131-6 PMID: 8385467
  30. Programmed cell death of T lymphocytes during acute viral infection: a mechanism for virus-induced immune deficiency.
    J Virol. 1993 Oct;67(10):5754-65 PMID: 8371341
  31. Fas transduces activation signals in normal human T lymphocytes.
    J Exp Med. 1993 Dec 1;178(6):2231-5 PMID: 7504062
  32. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand.
    Cell. 1994 Mar 25;76(6):969-76 PMID: 7511063
  33. Class I-restricted cytotoxic T lymphocytes are directly cytopathic for their target cells in vivo.
    J Immunol. 1994 Apr 1;152(7):3245-53 PMID: 8144915
  34. In vivo state of antiviral CTL precursors. Characterization of a cycling cell population containing CTL precursors in immune mice.
    J Immunol. 1995 Jan 15;154(2):620-32 PMID: 7529281
  35. Fatal interactions: Fas-induced apoptosis of mature T cells.
    Immunity. 1994 Aug;1(5):347-9 PMID: 7533643
  36. H-2 compatibility requirement for virus-specific T cell-mediated effector functions in vivo. I. Specificity of T cells conferring antiviral protection against lymphocytic choriomeningitis virus is associated with H-2K and H-2D.
    J Immunol. 1976 Nov;117(5 Pt 1):1495-502 PMID: 794412
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
0002-9440
Published
1995-07-00
Pages
79-91
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC1869886
Subset
IM
Grants
NIAID NIH HHS · AI-17672 · United States
NIAMS NIH HHS · AR-35506 · United States
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