Home LiteratureArticle Details
PMID: 1357664 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Instability of assembled T-cell receptor complex that is associated with rapid degradation of zeta chains in immature CD4+CD8+ thymocytes.

Kosugi A, Weissman AM, Ogata M, Hamaoka T, Fujiwara H

Abstract

The intracellular fate of newly synthesized T-cell receptor (TCR) chains was compared in CD4+CD8+ (double positive; DP) thymocytes and in CD4+CD8- or CD4-CD8+ (single positive; SP) thymocytes. Purified DP and SP thymocytes from normal adult mice were analyzed by pulse-chase metabolic labeling and immunoprecipitation with specific anti-TCR antibodies. Biosynthesis of invariant chains (CD3 gamma, -delta, -epsilon, and zeta) was comparable between DP and SP thymocytes, whereas DP thymocytes synthesized TCR alpha and TCR beta chains at lower and higher levels than SP thymocytes, respectively. These newly synthesized TCR chains were degraded at different rates in SP thymocytes based on their sensitivities for degradation as previously reported: TCR alpha, TCR beta, CD3 gamma, and CD3 delta chains were rapidly degraded and CD3 epsilon and zeta chains were stable. Although the degradation rates of clonotypic and invariant CD3 chains were similar in DP and SP thymocytes, the zeta subunit was rapidly degraded in DP thymocytes (t1/2, approximately 1.5 hr). Degradation of zeta was inhibited by NH4Cl, implicating lysosomes as the site of degradation. Comparison of TCR subunit assembly in DP and SP thymocytes demonstrated that, despite the same relative rate of formation of TCR complexes in a pulse period (30 min), complete complexes were unstable and degraded during the subsequent 6 hr of chase in DP thymocytes. This contrasted with the stability and a progressive increase in the levels of completely assembled complexes in SP thymocytes. Thus, these results demonstrate that a unique posttranslational regulation operates in the formation of TCR complexes in DP thymocytes and that lack of stability of complete TCR complexes is a crucial mechanism that may account for the limited surface TCR expression on this thymocyte subset.

MeSH Terms
Ammonium Chloride/pharmacology Animals CD3 Complex/metabolism CD4-Positive T-Lymphocytes/metabolism Cell Differentiation Macromolecular Substances Mice Mice, Inbred C57BL Receptors, Antigen, T-Cell, alpha-beta/metabolism T-Lymphocyte Subsets/cytology,metabolism Thymus Gland/cytology
Chemicals
CD3 Complex Macromolecular Substances Receptors, Antigen, T-Cell, alpha-beta Ammonium Chloride
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Kosugi A
Biomedical Research Center, Osaka University Medical School, Japan.
Weissman A M
Ogata M
Hamaoka T
Fujiwara H
References (26)
26 references, click to expand
  1. Inverse correlation between steady-state RNA and cell surface T cell receptor levels.
    FASEB J. 1990 Oct;4(13):3131-4 PMID: 1698681
  2. Intrathymic signalling in immature CD4+CD8+ thymocytes results in tyrosine phosphorylation of the T-cell receptor zeta chain.
    Nature. 1989 Oct 19;341(6243):651-4 PMID: 2477711
  3. Role of the zeta chain in the expression of the T cell antigen receptor: genetic reconstitution studies.
    EMBO J. 1989 Dec 1;8(12):3651-6 PMID: 2583115
  4. Pre-Golgi degradation of newly synthesized T-cell antigen receptor chains: intrinsic sensitivity and the role of subunit assembly.
    J Cell Biol. 1989 Jul;109(1):73-83 PMID: 2663883
  5. Biochemical characterization of the eta chain of the T-cell receptor. A unique subunit related to zeta.
    J Biol Chem. 1989 Sep 5;264(25):14812-7 PMID: 2768241
  6. 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
  7. Thymocytes with the predicted properties of pre-T cells.
    J Exp Med. 1987 Oct 1;166(4):874-89 PMID: 2958580
  8. Characterization of an anti-peptide antibody that recognizes the murine analogue of the human T cell antigen receptor-T3 delta-chain.
    J Immunol. 1986 Nov 15;137(10):3254-8 PMID: 3095425
  9. The T cell receptor/CD3 complex: a dynamic protein ensemble.
    Annu Rev Immunol. 1988;6:629-62 PMID: 3289580
  10. Building a multichain receptor: synthesis, degradation, and assembly of the T-cell antigen receptor.
    Proc Natl Acad Sci U S A. 1987 May;84(9):2688-92 PMID: 3495001
  11. Novel post-translational regulation of TCR expression in CD4+CD8+ thymocytes influenced by CD4.
    Nature. 1990 Mar 15;344(6263):247-51 PMID: 1690353
  12. CD3 eta and CD3 zeta are alternatively spliced products of a common genetic locus and are transcriptionally and/or post-transcriptionally regulated during T-cell development.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5202-6 PMID: 1828894
  13. The gamma and epsilon subunits of the CD3 complex inhibit pre-Golgi degradation of newly synthesized T cell antigen receptors.
    J Cell Biol. 1990 Apr;110(4):973-86 PMID: 2139038
  14. Characterization of a monoclonal antibody which detects all murine alpha beta T cell receptors.
    J Immunol. 1989 Apr 15;142(8):2736-42 PMID: 2467936
  15. Engagement of CD4 and CD8 expressed on immature thymocytes induces activation of intracellular tyrosine phosphorylation pathways.
    J Exp Med. 1989 Nov 1;170(5):1671-80 PMID: 2478653
  16. T-cell antigen receptor (TCR)-alpha/beta heterodimer formation is a prerequisite for association of CD3-zeta 2 into functionally competent TCR.CD3 complexes.
    J Biol Chem. 1989 Dec 5;264(34):20760-9 PMID: 2531145
  17. The thymus has two functionally distinct populations of immature alpha beta + T cells: one population is deleted by ligation of alpha beta TCR.
    Cell. 1989 Sep 22;58(6):1047-54 PMID: 2673539
  18. Early genetic events in T cell development analyzed by in situ hybridization.
    J Exp Med. 1987 Jun 1;165(6):1624-38 PMID: 2884272
  19. Developmentally regulated rearrangement and expression of genes encoding the T cell receptor-T3 complex.
    Cell. 1986 Jul 4;46(1):75-87 PMID: 3087626
  20. Association and dissociation of the murine T cell receptor associated protein (TRAP). Early events in the biosynthesis of a multisubunit receptor.
    J Biol Chem. 1988 Jun 25;263(18):8965-71 PMID: 3259950
  21. T cell tolerance by clonal elimination in the thymus.
    Cell. 1987 Apr 24;49(2):273-80 PMID: 3494522
  22. Pairwise, cooperative and inhibitory interactions describe the assembly and probable structure of the T-cell antigen receptor.
    EMBO J. 1991 Jul;10(7):1643-51 PMID: 1828760
  23. Distinct sequence of negative or positive selection implied by thymocyte T-cell receptor densities.
    Nature. 1990 Aug 30;346(6287):861-3 PMID: 1975427
  24. Developmental biology of T cells in T cell-receptor transgenic mice.
    Annu Rev Immunol. 1990;8:531-56 PMID: 2188673
  25. The T cell antigen receptor: insights into organelle biology.
    Annu Rev Cell Biol. 1990;6:403-31 PMID: 2275818
  26. Expression of a hybrid immunoglobulin-T cell receptor protein in transgenic mice.
    Cell. 1989 Sep 8;58(5):911-21 PMID: 2528411
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
Published
1992-10-15
Pages
9494-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC50158
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: [email protected]