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PMID: 10430936 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A comparison of T cell memory against the same antigen induced by virus versus intracellular bacteria.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 96 ·No. 16 ·1999-08-03 ·Pages 9293-8

Ochsenbein AF, Karrer U, Klenerman P, Althage A, Ciurea A, Shen H, Miller JF, Whitton JL, Hengartner H, Zinkernagel RM

Abstract

Cytotoxic T cell (CTL) memory was analyzed after infection with lymphocytic choriomeningitis virus (LCMV) and recombinant Listeria monocytogenes (rLM) expressing the complete nucleoprotein of LCMV (rLM-NP(actA)) or only the immunodominant epitope of H-2(d) mice (rLM-NP(118-126)). Immunization with LCMV and rLM induced a long-lived increased CTL precursor (CTLp) frequency specific for the viral (NP(118-126)) and for the bacterial (LLO(91-99)) epitope, respectively. However, after infection with rLM memory, CTLs were less protective against an intravenous LCMV challenge infection than a comparable number of LCMV-induced memory T cells. LCMV, but not recombinant Listeria-induced memory T cells were able to protect against lethal choriomeningitis by LCMV or a subsequent peripheral infection with recombinant vaccinia virus expressing LCMV-NP. The protective memory after viral and after rLM immunization was paralleled by evidence of LCMV but not rLM antigen persistence on day 15 and 30 after vaccination. These results document a striking difference in protective T cell memory between viral and bacterial vaccines and indicate that rapid T cell-dependent immune protection correlates with antigen persistence.

MeSH Terms
Animals Antigens, Bacterial/immunology Antigens, Viral/immunology Bacterial Vaccines Epitopes/immunology Immunologic Memory Listeria monocytogenes/immunology Lymphocytic Choriomeningitis/immunology Lymphocytic choriomeningitis virus/immunology Mice Mice, Inbred BALB C Nucleoproteins/immunology Recombinant Proteins/immunology T-Lymphocytes, Cytotoxic/immunology Vaccines, Synthetic Viral Vaccines
Chemicals
Antigens, Bacterial Antigens, Viral Bacterial Vaccines Epitopes Nucleoproteins Recombinant Proteins Vaccines, Synthetic Viral Vaccines
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Ochsenbein A F
Institute for Experimental Immunology, University Hospital, CH-8091 Zürich, Switzerland. [email protected]
Karrer U
Klenerman P
Althage A
Ciurea A
Shen H
Miller J F
Whitton J L
Hengartner H
Zinkernagel R M
References (59)
59 references, click to expand
  1. Immune surveillance against a solid tumor fails because of immunological ignorance.
    Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2233-8 PMID: 10051624
  2. CD8+ T cells specific for a single nonamer epitope of Listeria monocytogenes are protective in vivo.
    J Exp Med. 1992 Jun 1;175(6):1531-8 PMID: 1375265
  3. The biology of lymphocytic choriomeningitis infection: virus-induced immune disease.
    Cold Spring Harb Symp Quant Biol. 1962;27:479-99 PMID: 13955006
  4. Antivirally protective cytotoxic T cell memory to lymphocytic choriomeningitis virus is governed by persisting antigen.
    J Exp Med. 1992 Nov 1;176(5):1273-81 PMID: 1402673
  5. THE IMMUNOLOGICAL BASIS OF ACQUIRED CELLULAR RESISTANCE.
    J Exp Med. 1964 Jul 1;120:105-20 PMID: 14194388
  6. Precise prediction of a dominant class I MHC-restricted epitope of Listeria monocytogenes.
    Nature. 1991 Oct 31;353(6347):852-5 PMID: 1719425
  7. Natural immunity: a T-cell-independent pathway of macrophage activation, defined in the scid mouse.
    Immunol Rev. 1991 Dec;124:5-24 PMID: 1804781
  8. T-cell memory: the connection between function, phenotype and migration pathways.
    Immunol Today. 1991 Jun;12(6):189-92 PMID: 1831615
  9. T cell memory is short-lived in the absence of antigen.
    J Exp Med. 1991 Nov 1;174(5):969-74 PMID: 1834764
  10. Neutrophil-mediated dissolution of infected host cells as a defense strategy against a facultative intracellular bacterium.
    J Exp Med. 1991 Sep 1;174(3):741-4 PMID: 1908513
  11. Roles of CD4+ and CD8+ cells, and the effect of administration of recombinant murine interferon gamma in listerial infection.
    J Exp Med. 1990 Apr 1;171(4):1141-54 PMID: 2109036
  12. Anti-viral protection and prevention of lymphocytic choriomeningitis or of the local footpad swelling reaction in mice by immunization with vaccinia-recombinant virus expressing LCMV-WE nucleoprotein or glycoprotein.
    Eur J Immunol. 1989 Mar;19(3):417-24 PMID: 2468501
  13. T cell memory. Long-term persistence of virus-specific cytotoxic T cells.
    J Exp Med. 1989 Jun 1;169(6):1993-2005 PMID: 2471771
  14. Exacerbation of murine listeriosis by a monoclonal antibody specific for the type 3 complement receptor of myelomonocytic cells. Absence of monocytes at infective foci allows Listeria to multiply in nonphagocytic cells.
    J Exp Med. 1989 Jul 1;170(1):27-37 PMID: 2501445
  15. Acquired resistance to Listeria monocytogenes is mediated by Lyt-2+ T cells independently of the influx of monocytes into granulomatous lesions.
    J Exp Med. 1989 Aug 1;170(2):589-94 PMID: 2502601
  16. The immune response of the mouse to lymphocytic choriomeningitis virus. V. High numbers of cytolytic T lymphocytes are generated in the spleen during acute infection.
    Eur J Immunol. 1987 Jul;17(7):937-42 PMID: 2886344
  17. Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements.
    J Immunol. 1987 Sep 15;139(6):2005-9 PMID: 3114382
  18. Induction of immunity with avirulent Listeria monocytogenes 19113 depends on bacterial replication.
    Infect Immun. 1988 Aug;56(8):2109-13 PMID: 3135271
  19. Cellular mediators of anti-Listeria immunity as an enlarged population of short lived, replicating T cells. Kinetics of their production.
    J Exp Med. 1973 Aug 1;138(2):342-55 PMID: 4198199
  20. Requirement of thymus (T) lymphocytes for resistance to listeriosis.
    J Exp Med. 1972 May 1;135(5):1104-12 PMID: 4623315
  21. The virology and immunobiology of lymphocytic choriomeningitis virus infection.
    Adv Immunol. 1980;30:275-331 PMID: 6160740
  22. Biology of cloned cytotoxic T lymphocytes specific for lymphocytic choriomeningitis virus. I. Generation and recognition of virus strains and H-2b mutants.
    J Immunol. 1984 Jul;133(1):433-9 PMID: 6202788
  23. Enhanced adoptive transfer of immunity to Listeria monocytogenes after in vitro culture of murine spleen cells with concanavalin A.
    Infect Immun. 1982 Feb;35(2):560-5 PMID: 6799407
  24. Prolongation of acquired cellular resistance to Listeria monocytogenes.
    Immunology. 1982 Aug;46(4):787-92 PMID: 6809603
  25. Immunological memory to Listeria monocytogenes in rodents: evidence for protective T lymphocytes outside the recirculating lymphocyte pool.
    J Reticuloendothel Soc. 1980 Oct;28(4):405-17 PMID: 6968829
  26. Cytotoxic T-cell memory without antigen.
    Nature. 1994 Jun 23;369(6482):648-52 PMID: 7516038
  27. Virus-specific CD8+ T-cell memory determined by clonal burst size.
    Nature. 1994 Jun 23;369(6482):652-4 PMID: 7516039
  28. A recombinant Listeria monocytogenes vaccine expressing a model tumour antigen protects mice against lethal tumour cell challenge and causes regression of established tumours.
    Nat Med. 1995 May;1(5):471-7 PMID: 7585097
  29. Regression of established tumors in mice mediated by the oral administration of a recombinant Listeria monocytogenes vaccine.
    Cancer Res. 1995 Nov 1;55(21):4776-9 PMID: 7585503
  30. Induction of cell-mediated immune responses to human immunodeficiency virus type 1 Gag protein by using Listeria monocytogenes as a live vaccine vector.
    J Immunol. 1995 Nov 15;155(10):4775-82 PMID: 7594479
  31. Listeriolysin is processed efficiently into an MHC class I-associated epitope in Listeria monocytogenes-infected cells.
    J Immunol. 1995 Dec 1;155(11):5227-33 PMID: 7594534
  32. Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors.
    J Virol. 1995 Aug;69(8):4792-6 PMID: 7609046
  33. Specific immunity to Listeria monocytogenes in the absence of IFN gamma.
    Immunity. 1995 Jul;3(1):109-17 PMID: 7621071
  34. Contribution of alpha/beta and gamma/delta T lymphocytes to immunity against Mycobacterium bovis bacillus Calmette Guérin: studies with T cell receptor-deficient mutant mice.
    Eur J Immunol. 1995 Mar;25(3):838-46 PMID: 7705416
  35. Recombinant Listeria monocytogenes as a live vaccine vehicle for the induction of protective anti-viral cell-mediated immunity.
    Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3987-91 PMID: 7732018
  36. CD8+ T cell-mediated protection against an intracellular bacterium by perforin-dependent cytotoxicity.
    Eur J Immunol. 1994 Dec;24(12):3068-72 PMID: 7805735
  37. 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
  38. Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody.
    J Exp Med. 1994 Jan 1;179(1):259-68 PMID: 8270870
  39. The long-term maintenance of cytotoxic T cell memory does not require persistence of antigen.
    J Exp Med. 1994 Jan 1;179(1):317-21 PMID: 8270876
  40. Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes.
    Nature. 1993 Aug 26;364(6440):798-802 PMID: 8395024
  41. T cell-dependent IFN-gamma exerts an antiviral effect in the central nervous system but not in peripheral solid organs.
    J Immunol. 1993 Mar 15;150(6):2316-21 PMID: 8450214
  42. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes.
    Science. 1993 Mar 19;259(5102):1739-42 PMID: 8456300
  43. Immune response in mice that lack the interferon-gamma receptor.
    Science. 1993 Mar 19;259(5102):1742-5 PMID: 8456301
  44. Immunology taught by viruses.
    Science. 1996 Jan 12;271(5246):173-8 PMID: 8539616
  45. A recombinant minigene vaccine containing a nonameric cytotoxic-T-lymphocyte epitope confers limited protection against Listeria monocytogenes infection.
    Infect Immun. 1996 May;64(5):1685-93 PMID: 8613379
  46. Antiviral cytotoxic T-cell memory by vaccination with recombinant Listeria monocytogenes.
    J Virol. 1996 May;70(5):2902-10 PMID: 8627765
  47. On immunological memory.
    Annu Rev Immunol. 1996;14:333-67 PMID: 8717518
  48. On T cell memory: arguments for antigen dependence.
    Immunol Rev. 1996 Apr;150:63-90 PMID: 8782702
  49. On the role of antigen in maintaining cytotoxic T-cell memory.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9716-23 PMID: 8790397
  50. Exhaustion of CTL memory and recrudescence of viremia in lymphocytic choriomeningitis virus-infected MHC class II-deficient mice and B cell-deficient mice.
    J Immunol. 1996 Oct 1;157(7):3074-80 PMID: 8816417
  51. Recombinant Listeria monocytogenes cancer vaccines.
    Curr Opin Immunol. 1996 Oct;8(5):664-9 PMID: 8902392
  52. Protection against immunopathological consequences of a viral infection by activated but not resting cytotoxic T cells: T cell memory without "memory T cells"?
    Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):640-5 PMID: 9012837
  53. Influenza-specific immunity induced by recombinant Listeria monocytogenes vaccines.
    Vaccine. 1997 Mar;15(4):433-40 PMID: 9141215
  54. A critical role for neutralizing-antibody-producing B cells, CD4(+) T cells, and interferons in persistent and acute infections of mice with lymphocytic choriomeningitis virus: implications for adoptive immunotherapy of virus carriers.
    Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6874-9 PMID: 9192659
  55. Immunological memory.
    Curr Opin Immunol. 1997 Jun;9(3):371-9 PMID: 9203411
  56. A non-retroviral RNA virus persists in DNA form.
    Nature. 1997 Nov 20;390(6657):298-301 PMID: 9384383
  57. A functional and kinetic comparison of antiviral effector and memory cytotoxic T lymphocyte populations in vivo and in vitro.
    Eur J Immunol. 1997 Dec;27(12):3404-13 PMID: 9464829
  58. Compartmentalization of bacterial antigens: differential effects on priming of CD8 T cells and protective immunity.
    Cell. 1998 Feb 20;92(4):535-45 PMID: 9491894
  59. Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes.
    J Exp Med. 1998 May 4;187(9):1383-93 PMID: 9565631
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.96.16.9293
Email
[email protected]
Published
1999-08-03
Pages
9293-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC17773
Subset
IM
Grants
NIAID NIH HHS · R01 AI027028 · United States
NIAID NIH HHS · R21 AI027028 · United States
NIAID NIH HHS · R56 AI027028 · United States
NIAID NIH HHS · AI-27028 · United States
External Links
PubMed source DOI: 10.1073/pnas.96.16.9293 PMC Full Text View journal details
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