Resistance to and recovery from lethal influenza virus infection in B lymphocyte-deficient mice - PubMed
- ️Wed Jan 01 1997
Resistance to and recovery from lethal influenza virus infection in B lymphocyte-deficient mice
M B Graham et al. J Exp Med. 1997.
Abstract
In the adaptive immune response to most viruses, both the cellular and humoral arms of the immune system play complementary roles in eliminating virus and virus-infected cells and in promoting recovery. To evaluate the relative contribution of CD4+ and CD8+ effector T lymphocytes in virus clearance and recovery, we have examined the host response to lethal type A influenza virus infection in B lymphocyte-deficient mice with a targeted disruption in the immunoglobulin mu heavy chain. Our results indicate that naive B cell-deficient mice have a 50- 100-fold greater susceptibility to lethal type A influenza virus infection than do wild type mice. However, after priming with sublethal doses of influenza, immune B cell-deficient animals show an enhanced resistance to lethal virus infection. This finding indicates that an antibody-independent immune-mediated antiviral mechanism accounts for the increased resistance to lethal virus challenge. To assess the contribution of influenza-specific CD4+ and CD8+ effector T cells in this process, defined clonal populations of influenza-specific CD4+ and CD8+ effector T cells were adoptively transferred into lethally infected B cell-deficient mice. Cloned CD8+ effectors efficiently promoted recovery from lethal infection, whereas cloned CD4+ T cells conferred only partial protection. These results suggest that memory T lymphocytes can act independently of a humoral immune response in order to confer resistance to influenza infection in immune individuals. The potential implications of these results for vaccination against human influenza infection are discussed.
Figures

B cell–deficient mice are more susceptible to influenza viral challenge. μKO (a) and C57Bl/6 (b) mice were intranasally inoculated with varying doses (♦, 10−3 dilution; ▪, 10−4 dilution; •, 10−5 dilution; ▴, 10−6 dilution; and ✖, 10−7 dilution) of mouse adapted influenza virus and watched for 21 d for morbidity and mortality.

μKO mice can initiate and maintain an influenza-specific CTL response after challenge with influenza virus. (a) Lungs were removed from μKO (shaded bars) and C57BL/6 (open bars) mice on day 12 after intranasal viral challenge with a sublethal dose of A/JAPAN/57 (attenuated strain). Cell suspensions from the lungs were obtained by processing through a sieve, and were Ficoll purified and plated for a final effector/targer (E/T) ratio of 50:1. Assay time was 6 h and spontaneous release for all targets was <20%. Results of two separate experiments with two mice per experimental group are shown. (b) Influenza specific bulks from four individual μKO (shaded bars) and from C57BL/6 (open bars) mice were tested for their ability to lyse uninfected and A/JAPAN/57 infected class II negative (EL4) and class I and II positive (LB15.13) target cells in a standard chromium release assay. Assay time = 6 h; E/T = 10:1. Spontaneous release for all targets was <15%. Experiment is representative of three separate experiments.

B cell–deficient mice are more susceptible to rechallenge with influenza. Groups of 7–12 age-matched μKO (open symbols) and C57Bl/6 (closed symbols) mice were intranasally infected with attenuated A/JAPAN/57. 28 d later the animals were rechallenged intranasally with the dilutions of mouse adapted A/JAPAN/57: ▵, 10−1 dilution; ○, 10−2 dilution; ⋄, 10−3 dilution; □, 10−4 dilution. Animals were followed for 21 d for mortality. Data is representative of two experiments.

CD8+, but not CD4+, T cell clones promote full recovery in B cell–deficient mice. B cell–deficient (μKO) mice were infected intranasally with a 10 LD50 dose of mouse-adapted A/JAPAN/57 virus followed by an intravenous injection of 107 cells. The cells transferred included 4D7 (⋄, a CD4+ clone), 11E4 (▴, a CD8+ clone), and B1.11 (•, a CD8+ clone). Mice receiving intranasal influenza, but no cell transfer, are denoted as □. C57Bl/6 mice receiving intranasal influenza without cell transfer are also shown (✖). Each group represents 5–7 animals. Adoptive transfer of these clones and media control into lethally challenged C57Bl/ 6 mice was done simultaneously as a control.
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References
-
- Askonas, B.A., A.J. McMichael, and R.G. Webster. 1982. The immune response to influenza viruses and the problem of protection against infection. In Basic and Applied Influenza Research. A.S. Beare, editor. CRC Press, Boca Raton, FL. pp. 159–188.
-
- Doherty PC, Allan W, Eichelberger M, Carding SR. Roles of alpha beta and gamma delta T cell subsets in viral immunity. [Review] Annu Rev Immunol. 1992;10:123–151. - PubMed
-
- Allan W, Tabi Z, Cleary A, Doherty PC. Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+T cells. J Immunol. 1990;144:3980–3986. - PubMed
-
- Bender BS, Bell WE, Taylor S, Small PJ. Class I major histocompatibility complex–restricted cytotoxic T lymphocytes are not necessary for heterotypic immunity to influenza. J Infect Dis. 1994;170:1195–1200. - PubMed
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