Activation-induced apoptosis in lymphocytes

https://doi.org/10.1016/0952-7915(94)90130-9Get rights and content

Abstract

Activation-induced apoptosis has been proposed as a mechanism for purging the immune repertoire of anti-self specificities, not only in development but also during the generation of somatic mutation in germinal centers. The pathways involved in driving immature and mature T and B cells to programmed cell death are reviewed with respect to two hypotheses, the pre-emptive death model, in which certain signals are obligatory for programmed cell death, and the two signal: death/survival model. Depending on the system, some data support the former pathway, in which certain signals are obligatory for programmed cell death, whereas other data are consistent with the two signal hypothesis. Moreover, recent data suggests that the c-myc protein plays a pivotal role in controlling this process. Finally conflicting roles of protein kinases, bcl-2 and p53 are reviewed and contrasted for involvement in activation-induced cell death in T and B lymphocytes.

References (110)

  • M. Debbas et al.

    Wild-type p53 Mediates Apoptosis by E1A, which is Inhibited by E1B

    Gene Dev

    (1993)
  • J.M. Lee et al.

    p53 Mutations Increase Resistance to Ionizing Radiation

  • J. Lotem et al.

    Hematopoietic Cells from Mice Deficient in Wild-Type p53 Are More Resistant to Induction of Apoptosis by Some Agents

    Blood

    (1993)
  • C.A. Smith et al.

    Antibodies to CD3/T Cell Receptor Complex Induce by Apoptosis in Immature T Cells in Thymic Cultures

    Nature

    (1989)
  • Y. Shi et al.

    Cyclosporin A Inhibits Activation-induced Cell Death in T Cell Hybridomas and in Thymocytes

    Nature

    (1979)
  • Y. Shi et al.

    In Vivo Administration of Antibodies to the CD3/T Cell Receptor Complex Induces Cell Death (Apoptosis) in Immature Thymocytes

    J Immunol

    (1991)
  • K.M. Murphy et al.

    Induction by Antigen of Intrathymic Apoptosis of CD4+CD8+ TCR lo Thymocytes in Vivo

    Science

    (1990)
  • O. Swat et al.

    Clonal Deletion of Immature CD4+8+ Thymocytes in Suspension Culture by Extrathymic Antigen-presenting Cells

    Nature

    (1991)
  • E.J. Jenkinson et al.

    Antigen-induced Apoptosis in Developing T Cells: a Mechanism for Negative Selection of the T Cell Receptor Repertoire

    Eur J Immunol

    (1989)
  • Y.S. Lin et al.

    In Vivo Induction of Apoptosis in Immature Thymocytes by Staphylococcal Enterotoxin B

    J Immunol

    (1992)
  • L. D'Adamio et al.

    Negative Selection of Thymocytes. A Novel Polymcrase Chain Reaction-based Molecular Analysis Detects Requirements for Macromolecular Synthesis

    J Immunol

    (1992)
  • H.R. MacDonald et al.

    Programmed Death of Autoreac-tive Thymocytes

    Nature

    (1990)
  • D.J. McConkey et al.

    Calcium-dependent Killing of Immature Thymocytes by Stimulation via the CD3/T Cell Receptor Complex

    J Immunol

    (1989)
  • T. Tadakuma et al.

    CD4+CD8+ Thymocytes are Susceptible to DNA Fragmentation Induced by Phorbol Ester, Cal cium Ionophorc and Anti-CD3 Antibody

    Eur J Immunol

    (1990)
  • D.R. Green et al.

    Activation-induced Apoptosis in Lymphoid Systems

    Sem Immunol

    (1992)
  • K. Nakayama et al.

    No Requirement for p56lck in the Antigen-stimulated Clonal Deletion of Thymocytes

    Science

    (1992)
  • N.J. Vasquez et al.

    In vivo and in vitro Clonal Deletion of Double-Positive Thymocytcs

    J Exp Med

    (1992)
  • T. Nakayama et al.

    In Vivo Calcium Elevations in Thymocytes with T Cell Receptors that Arc Specific for Self Ligands

    Science

    (1992)
  • D. Nemazee et al.

    Clonal Deletion of Autorcactive B Lymphocytes in Bone Marrow Chimeras

  • M. Murakami et al.

    Antigen-induced Apoptotic Death of Ly-1 B Cells Responsible for Autoimmune Disease in Transgenic Mice

    Nature

    (1992)
  • R. Carsetti et al.

    A Role for Immunoglobulin D: Interference with Tolerance Induction

    Eur J Immunol

    (1993)
  • L.B. Liou et al.

    Can Peritoneal B Cells be Rendered Unresponsive?

    Int Immunol

    (1992)
  • J.D. Ashwell et al.

    Cell Growth Cycle Block of T Cell Hybridomas upon Activation with Antigen

    J Exp Med

    (1987)
  • M. Mercep et al.

    Inhibition of Transformed T Cell Growth in Vitro by Monoclonal Antibodies Directed against Distinct Activating Molecules

    J Immunol

    (1988)
  • M. Mercep et al.

    The Cell Cycle Block and Lysis of an Activated T Cell Hybridoma Are Distinct Processes with Different Ca2+ Requirements and Sensitivity to Cyclosporinc A

    J Immunol

    (1989)
  • D.S. Ucker et al.

    Activation-driven T Cell Death. I. Requirements for de Novo Transcription and Translation and Association with Genome Fragmentation

    J Immunol

    (1989)
  • C. Odaka et al.

    T Cell Receptor-mediated DNA Fragmentation and Cell Death in T Cell Hybridomas

    J Immunol

    (1990)
  • Y. Shi et al.

    Activation Induced Cell Death in T Cell Hybridomas is Due to Apoptosis: Morphological Aspects and DNA Fragmentation

    J Immunol

    (1990)
  • R. Suto et al.

    Effect of Accessory Cells on Stimulation of Murinc T-Ccll Leukemia with Antibodies to the CD3/T Cell Antigen Receptor Complex

    Jpn J Cancer Res

    (1993)
  • L.E. Benhamou et al.

    Anti-Immunoglobulins Induce Death by Apoptosis in WEHI-231 B Lymphoma Cells

    Eur J Immunol

    (1990)
  • J. Hasbold et al.

    Anti-immunoglobulin Antibodies Induce Apoptosis in Immature B Cell Lymphomas

    Eur J Immunol

    (1990)
  • G.L. Warner et al.

    A Polyclonal Model for B Cell Tolerance. I. Fc-dependent and Fc-independent Induction of Nonresponsiveness by Pretreatment of Normal Splenic B Cells with Anti-Ig

    J Immunol

    (1991)
  • L.A. Jones et al.

    Peripheral Clonal Elimination of Functional T Cells

    Science

    (1990)
  • Y. Kawabe et al.

    Programmed Cell Death and Extrathymic Reduction of Vβ8+ CD4+ T Cells in Mice Tolerant to Staphylococcus Aureus Enterotoxin B

    Nature

    (1991)
  • J.A. Gonzalo et al.

    Expansion and Clonal Deletion of Peripheral T Cells Induced by Bacterial Superantigen is Independent of the Interleukin-2 Pathway

    Eur J Immunol

    (1992)
  • M.J. Lenardo

    Interleukin-2 Programs Mouse αβ T Lymphocytes for Apoptosis

    Nature

    (1991)
  • L.G. Radvanyi et al.

    Religation of the T Cells, Receptor after Primary Activation of Mature T Cells Inhibits Proliferation and Induces Apoptosic Cell Death

    J Immunol

    (1993)
  • S. Wesselborg et al.

    Activation-driven Death of Human T Cell Clones: Tune Course Kinetics of the Induction of Cell Shrinkage, DNA Fragmentation, and Cell Death

    Cell Immunol

    (1993)
  • S. Wesselborg et al.

    Induction of Activation-driven Death (Apoptosis) in Activated but not Resting Peripheral Blood T Cells

    J Immunol

    (1993)
  • M.K. Newell et al.

    Death of Mature T Cells by Separate Ligation of CD4 and the T-Cell Receptor for Antigen

    Nature

    (1990)
  • Cited by (250)

    • In vitro and ex vitro functional characterization of human HLA-DRB1∗04 restricted T cell receptors

      2021, Journal of Translational Autoimmunity
      Citation Excerpt :

      Supporting this observation, adding an anti-CD3 antibody to the hTCR 58 HLA/peptide cultures, thus specifically increasing the TCR signaling, lowered the activation of the hTCR 58 ​cells (Supplementary Fig. 4B). This could potentially be explained by activation-induced cell death (AICD) [43], where excessive TCR signaling results in cell death [44]. However, including Fas-Ig protein, to block Fas-FasL interactions involved in AICD, did not increase the activation (Supplementary Fig. 4C and D).

    • Intracellular RNA Sensing in Mammalian Cells: Role in Stress Response and Cancer Therapies

      2019, International Review of Cell and Molecular Biology
      Citation Excerpt :

      One possible explanation may be the ability of given cell types to respond to genotoxic stimuli by the accumulation of DNA fragments in the cytoplasm, as was previously demonstrated in early work using lymphocytes (Wyllie et al., 1984). Cells of mesenchymal and hematopoietic origin appear to be more prone to apoptotic DNA cleavage and accumulation of nucleosomal DNA in the cytoplasm as compared to solid tumors arising from exodermal and endodermal epithelial cells (Green and Scott, 1994; Rich et al., 2000). The data indicate this is due in part to the ability to activate apoptotic nucleases in different cell types (Khodarev et al., 1998, 2000).

    • Cultured circulating tumor cells and their derived xenografts for personalized oncology

      2016, Asian Journal of Urology
      Citation Excerpt :

      Though the T and B lymphocytes harbor proliferation potential, proliferation has to be triggered by specific antigen receptor ligation [97], by a Ca2+ influx together with a PKC activation [98], or by super-antigen cross-linking [99]. Moreover, the activated lymphocyte proliferation is transient, ending with a programmed activation-induced cell death [100–102]. In general, without additional stimulation, PBMCs in resting state would perish in ex vivo culture within days, each cell type dying in a programmed manner.

    • The apoptotic and proliferative fate of cytokine-induced killer cells after redirection to tumor cells with bispecific Ab

      2006, Cytotherapy
      Citation Excerpt :

      In this case, anti-CD28 did not increase proliferation, showing that CIK cells are highly activated by cross-linking their TCR with tumor cells by bsAb and can not be further stimulated. Co-stimulatory signals (CD80 and CD86) are needed to sustain T-cell activation and proliferation, and in their absence AICD occurs [34]. AICD is in part mediated through Fas/FasL interactions, which are both up-regulated on T cells upon TCR cross-linking.

    • Principles of Tumor Immunology

      2006, Nutritional Oncology, Second Edition
    View all citing articles on Scopus
    View full text