TCR ζ chain in T cell development and selection

Current Opinion in Immunology

Volumn 9, Issue 3, 1997, Pages 380-389

  Shores, Elizabeth W ^a   Love, Paul E ^b  

^a Center for Biologics Evaluation/Res   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR;

CELL MATURATION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE;

EID: 0030739876     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(97)80085-4     Document Type: Article

References (96)

1. Fowlkes BJ, Pardoll DM. Molecular and cellular events in T cell development. Adv Immunol. 44:1989;207-263.
2. Weiss A. T cell antigen receptor signal transduction: a tale of tails and cytoplasmic protein-tyrosine kinases. Cell. 73:1993;209-212.
3. Klausner RD, Lippincott-Schwartz J, Bonifacino JS. The T cell antigen receptor: insights into organelle biology. Annu Rev Cell Biol. 6:1990;403-431.
4. Von Boehmer H. Control of T-cell development by the pre-T and alpha beta T-cell receptor. Ann N Y Acad Sci. 766:1995;52-61.
5. Irving BA, Chan AC, Weiss A. Functional characterization of a signal transducing motif present in the T cell antigen receptor zeta chain. J Exp Med. 177:1993;1093-1103.
6. Romeo C, Amiot M, Seed B. Sequence requirements for induction of cytolysis by the T cell antigen/Fc receptor zeta chain. Cell. 68:1992;889-897.
7. Chan AC, Shaw AS. Regulation of antigen receptor signal transduction by protein tyrosine kinases. Curr Opin Immunol. 8:1996;394-401.
8. Wange RL, Samelson LE. Complex complexes: signaling at the TCR. Immunity. 5:1996;197-205.
9. Cantrell D. T cell antigen receptor signal transduction pathways. Annu Rev Immunol. 14:1996;259-274.
10. Van Oers NS, Kileen N, Weiss A. Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes. J Exp Med. 183:1996;1053-1062.
11. Kong G, Dalton M, Wardenburg JB, Straus D, Kurosaki T, Chan AC. Distinct tyrosine phosphorylation sites in ZAP-70 mediate activation and negative regulation of antigen receptor function. Mol Cell Biol. 9:1996;5026-5035.
12. Exley M, Varticovski L, Peter M, Sancho J, Terhorst C. Association of phosphatidylinositol 3-kinase with a specific sequence of the T cell receptor zeta chain is dependent on T cell activation. J Biol Chem. 269:1994;15140-15146.
13. Isakov N, Wange RL, Burgess WH, Watts JD, Aebersold R, Samelson LE. ZAP-70 binding specificity to T cell receptor tyrosine-based activation motifs: the tandem SH2 domains of ZAP-70 bind distinct tyrosine-based activation motifs with varying affinity. J Exp Med. 181:1995;375-380.
14. Osman N, Turner H, Lucas S, Reif K, Cantrell DA. The protein interactions of the immunoglobulin receptor family tyrosine-based activation motifs present in the T cell receptor subunits and the CD3γ, δ, and ε chains. Eur J Immunol. 26:1996;1063-1068.
15. Shortman K, Wu L. Early T lymphocyte progenitors. Annu Rev Immunol. 14:1996;29-47.
16. Godfrey DI, Zlotnik A. Control points in early T-cell development. Immunol Today. 14:1993;547-553.
17. Wiest DL, Kearse KP, Shores EW, Singer A. Developmentally regulated expression of CD3 components independent of clonotypic T cell antigen receptor complexes on immature thymocytes. J Exp Med. 180:1994;1375-1382.
18. Wilson A, MacDonald HR. Expression of genes encoding the pre-TCR and CD3 complex during thymus development. Int Immunol. 7:1995;1659-1664.
19. Wiest DL, Burgess WH, McKean D, Kearse KP, Singer A. The molecular chaperone calnexin is expressed on the surface of immature thymocytes in association with clonotype-independent CD3 complexes. EMBO J. 14:1995;3425-3433.
20. Levelt CN, Eichmann K. Receptors and signals in early thymic selection. Immunity. 3:1995;667-672.
21. Jacobs H, Vandeputte D, Tolkamp L, de Vries E, Borst J, Berns A. CD3 components at the surface of pro-T cells can mediate pre-T cell development in vivo. Eur J Immunol. 24:1994;934-939.
22. Wang B, Levelt C, Salio M, Zheng D, Sancho J, Liu CP, She J, Huang M, Higgins K, Sunshine MJ, et al. Over-expression of CD3 epsilon transgenes blocks T lymphocyte development. Int Immunol. 7:1995;435-448.
23. Malissen M, Gillet A, Ardouin L, Bouvier G, Trucy J, Ferrier P, Vivier E, Malissen B. Altered T cell development in mice with a targeted mutation of the CD3-ε gene. of special interest EMBO J. 14:1995;4641-4653 Reports the generation of mice with a targeted disruption of the CD3ε gene. The phenotype of these mice demonstrates that although CD3ε is important for transition of TN thymocytes to the DP stage of development, signals mediated by CDε are not required to initiate rearrangement of TCRβ.
24. - cells. Eur J Immunol. 24:1994;1903-1907.
25. Kishi H, Borgulya P, Scott B, Karjalainen K, Traunecker A, Kaufman J, von Boehmer H. Surface expression of the beta T cell receptor (TCR) chain in the absence of other TCR or CD3 proteins on immature T cells. EMBO J. 10:1991;93-100.
26. Mombaerts P, Clarke AR, Rudnicki MA, Iacomini J, Itohara S, Lafaille JJ, Wang L, Ichikawa Y, Jaenisch R, Hooper ML, et al. Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature. 360:1992;225-231.
27. Shinkai Y, Koyasu S, Nakayama K, Murphy KM, Loh DY, Reinherz EL, Alt FW. Restoration of T cell development in RAG-2-deficient mice by functional TCR transgenes. Science. 259:1993;822-825.
28. + thymocytes in RAG-deficient mice through a T cell receptor beta chain-independent pathway. J Exp Med. 181:1995;1187-1195.
29. Groettrup M, Ungewiss K, Azogui O, Palacios R, Owen MJ, Hayday AC, von Boehmer H. A novel disulfide-linked heterodimer on pre-T cells consists of the T cell receptor beta chain and a 33 kd glycoprotein. Cell. 75:1993;283-294.
30. Saint-Ruf C, Ungeweiss K, Groettrup M, Bruno L, Fehling HJ, von Boehmer H. Analysis and expression of cloned pre-T cell receptor gene. Science. 266:1994;1208-1212.
31. Rolink A, Melchers F. Molecular and cellular origins of B lymphocyte diversity. Cell. 61:1991;1081-1094.
32. Malissen B, Malissen M. Functions of TCR and pre-TCR subunits: lessons from gene ablation. Curr Opin Immunol. 8:1996;383-393.
33. Punt JA, Kubo RT, Saito T, Finkel TH, Kathiresan S, Blank KJ, Hashimoto Y. Surface expression of a T cell receptor beta (TCR-beta) chain in the absence of TCR-alpha, -delta, and -gamma proteins. J Exp Med. 174:1991;775-783.
34. Groettrup M, Baron A, Griffiths G, Palacios R, von Boehmer H. T cell receptor (TCR) beta chain homodimers on the surface of immature but not mature alpha, gamma, delta chain deficient T cell lines. EMBO J. 11:1992;2735-2745.
35. Mombaerts P, Terhorst C, Jacks T, Tonegawa S, Sancho J. Characterization of immature thymocyte lines derived from T-cell receptor or recombination activating gene 1 and p53 double mutant mice. Proc Natl Acad Sci USA. 92:1995;7420-7424.
36. Van Oers NS, von Boehmer H, Weiss A. The pre-T cell receptor (TCR) complex is functionally coupled to the TCR-zeta subunit. J Exp Med. 182:1995;1585-1590.
37. Love PE, Shores EW, Johnson MD, Tremblay ME, Lee J, Grinberg A, Huang SP, Singer A, Westphal H. T cell development in mice that lack the ζ chain of the T cell antigen receptor complex. Science. 261:1993;918-921.
38. -/- mutant mice and identification of a novel T cell population in the intestine. EMBO J. 12:1993;4863-4875.
39. Malissen M, Gillet A, Rocha B, Trucy J, Vivier E, Boyer C, Kontgen F, Brun N, Mazza G, Spanopoulou E, et al. T cell development in mice lacking the CD3-zeta/eta gene. EMBO J. 12:1993;4347-4355.
40. Ohno H, Aoe T, Taki S, Kitamura D, Ishida Y, Rajewsky K, Saito T. Development and functional impairment of T cells in mice lacking CD3ζ chains. EMBO J. 12:1993;4357-4366.
41. Boismeru R, Rhein M, Fischer WH, Havran W. A role for CD81 in early T cell development. Science. 271:1996;198-200.
42. Krimpenfort P, Ossendorp F, Borst J, Melief C, Berns A. T cell depletion in transgenic mice carrying a mutant gene for TCR-beta. Nature. 341:1989;742-746.
43. + stage.
44. Fehling HJ, Krotkova A, Saint-Ruf C, von Boehmer H. Crucial role of the pre-T-cell receptor alpha gene in development of alpha beta but not gamma delta T cells. of special interest Nature. 375:1995;795-798 This report documents the phenotype of mice with a targeted disruption of the gene encoding pTα. Thymuses from these mice are reduced in size and contain low numbers of DP and SP thymocytes. Significantly, γδ T cell development is not affected by this mutation. These findings demonstrate a crucial role for pTα and the pre-TCR in early αβTCR thymocyte development.
45. Xu Y, Davidson L, Alt FW, Baltimore D. Function of the pre-T-cell receptor alpha chain in T-cell development and allelic exclusion at the T-cell receptor beta locus. Proc Natl Acad Sci USA. 93:1996;2169-2173.
46. Del Porto P, Bruno L, Mattei MG, von Boehmer H, Saint-Ruf C. Cloning and comparative analysis of the human pre-T-cell receptor alpha-chain gene. Proc Natl Acad Sci USA. 92:1995;12105-12119.
47. + stage in the absence of TCR-beta rearrangement. J Immunol. 154:1995;5706-5714.
48. Levelt CN, Mombaerts P, Wang B, Kohler H, Tonegawa S, Eichmann K, Terhorst C. Regulation of thymocyte development through CD3: functional dissociation between p56lck and CD3 sigma in early thymic selection. Immunity. 3:1995;215-222.
49. Shores EW, Flamand V, Tran T, Grinberg A, Kinet J-P, Love PE. FcεRIγ can support T cell development and function in mice lacking endogenous TCRζ chain. J Immunol. 1997;. in press.
50. Shores EW, Huang K, Tran T, Lee E, Grinberg A, Love PE. Role of TCR zeta chain in T cell development and selection. Science. 266:1994;1047-1050.
51. + stage.
52. lck. Nature. 357:1992;161-164.
53. lck in thymopoiesis. EMBO J. 12:1993;1671-1680.
54. Groves T, Smiley P, Cooke MP, Forbush K, Perlmutter RM, Guidos CJ. Fyn Can Partially Substitute for Lck in T Lymphocyte Development. of special interest Immunity. 5:1996;417-428 This paper, along with [55], demonstrates that the Src-family kinases, Fyn and Lck, perform partially redundant functions in early thymocyte development.
55. Van Oers NSC, Lowin-Kropf B, Finlay D, Connolly K, Weiss A. αβT cell development is abolished in mice lacking both lck and fyn protein tyrosine kinases. Immunity. 5:1996;429-436 See annotation [54].
56. + thymocytes, and B cell maturation. of special interest J Exp Med. 183:1996;1707-1718 T cell development and TCR-mediated apoptosis are shown to be markedly impaired in mice lacking all isoforms of CD45, a regulator of the Src family kinase Lck.
57. Cheng AM, Rowley B, Pao W, Hayday A, Bolen JB, Pawson T. Syk tyrosine kinase required for mouse viability and B-cell development. Nature. 378:1995;303-306.
58. Turner M, Mee PJ, Costello PS, Williams O, Price AA, Duddy LP, Furlong MT, Geahlen RL, Tybulewicz VL. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature. 378:1995;298-302.
59. -/- mice demonstrates the requirement of this protein tyrosine kinase for thymocyte development and negative selection.
60. + stage.
61. + thymocytes. of special interest Proc Natl Acad Sci USA. 93:1996;4683-4687 Demonstrates a role for Ras pathway signaling in promoting pre-TCR signal transduction.
62. Robey E, Fowlkes BJ. Selective events in T cell development. Annu Rev Immunol. 12:1994;265-705.
63. Jameson SC, Hogquist KA, Bevan MJ. Positive selection of thymocytes. Annu Rev Immunol. 13:1995;93-126.
64. + thymocytes in vitro. J Immunol. 154:1995;3636-3643.
65. + thymocytes undergoing thymic selection: requirement of calcineurin activation for thymic positive selection but not negative selection. J Exp Med. 181:1995;927-941.
66. 2+ influx and signaling through the calcineurin pathway, varies in direct relation with the extent of TCR stimulation.
67. Hashimoto K, Sohn SJ, Lavin SD, Tada T, Perlmutter RM, Nakayama T. Requirement for p56lck tyrosine kinase activation in T cell receptor mediated thymic selection. J Exp Med. 184:1996;931-943.
68. O'Shea CC, Crompton T, Rosewell IR, Hayday AC, Owen MJ. Raf regulates positive selection. Eur J Immunol. 26:1996;2350-2355.
69. Swan KA, Alberola-lla J, Gross JA, Appleby MW, Forbush KA, Thomas JF, Perlmutter RM. Involvement of p21ras distinguishes positive and negative selection in thymocytes. EMBO J. 14:1995;276-285.
70. Alberola-lla J, Forbush KA, Seger R, Krebs EG, Perlmutter RM. Selective requirement for MAP kinase activation in thymocyte differentiation. Nature. 373:1995;620-623.
71. + stage was almost completely blocked but negative selection appeared intact, suggesting that the MAP Kinase pathway is selectively required for positive selection.
72. + thymocytes. Nature. 374:1995;474-477.
73. Liao XC, Littman DR. Altered T cell receptor signaling and disrupted T cell development in mice lacking itk. Immunity. 3:1995;757-769.
74. Alam SM, Travers PJ, Wung JL, Nasholds W, Redpath S, Jameson SC, Gascoigne NR. T-cell-receptor affinity and thymocyte positive selection. of special interest Nature. 381:1996;616-620 These investigators, along with the authors of [75], use surface plasmon resonance to measure the kinetics of TCR interactions with positively and negatively selecting ligands and find that affinity (especially the ligand dissociation rate) correlates with the outcome of selection, that is high affinity interactions promote negative selection and lower affinity interactions either promote positive selection or nonselection.
75. Lyons DS, Lieberman SA, Hampl J, Boniface J, Chien Y, Berg LJ, Davis MM. A TCR binds to antagonist ligands with lower affinities and faster dissociation rates than to agonists. of special interest Immunity. 5:1996;51-59 See annotation [74].
76. + T cells. Immunity. 3:1995;79-86.
77. Sebzda E, Kundig TM, Thomson CT, Aoki K, Mak SY, Mayer JP, Zamborelli T, Nathenson SG, Ohashi PS. Mature T cell reactivity altered by peptide agonist that induces positive selection. of special interest J Exp Med. 183:1996;1093-1104 This report describes an agonist peptide that can promote positive but not negative selection. Thymocytes maturing in the presence of this peptide were specifically unresponsive to it but could proliferate in response to another agonist peptide.
78. McKeithan TW. Kinetic proofreading in T-cell receptor signal transduction. of special interest Proc Natl Acad Sci USA. 92:1995;5042-5046 Proposes a model for TCR signal transduction in which the temporal lag between TCR engagement and signal transmission enables the formation of various intermediate products that could quantitatively or qualitatively influence the signaling response. See also [79].
79. Rabinowitz JD, Beeson C, Lyons DS, Davis MM, McConnell HM. Kinetic discrimination in T-cell activation. of special interest Proc Natl Acad Sci USA. 93:1996;1401-1405 See annotation [78].
80. Wegener AM, Letourneur F, Hoeveler A, Brocker T, Luton F, Malissen B. The T cell receptor/CD3 complex is composed of at least two autonomous transduction modules. Cell. 68:1992;83-95.
81. Simpson S, Hollander G, She J, Levelt C, Huang M, Terhorst C. Selection of peripheral and intestinal T lymphocytes lacking CD3 zeta. Int Immunol. 7:1995;287-293.
82. Brocker T, Karjalainen K. Signals through T cell receptor-zeta chain alone are insufficient to prime resting T lymphocytes. J Exp Med. 181:1995;1653-1659.
83. Shores EW, Tran T, Grinberg A, Sommers CL, Shen H, Love PE. Role of the multiple TCR signaling motifs in selection of the T cell repertoire. of special interest J Exp Med. 185:1997;893-900 Demonstrates an in vivo function for the multiple ζ-chain ITAMs in thymocyte positive and negative selection.
84. Tarakhovsky A, Kanner SB, Hombach J, Ledbetter JA, Muller W, Kileen N, Rajewsky K. A role for CD5 in TCR-mediated signal transduction and thymocyte selection. of special interest Science. 269:1995;535-537 Demonstrates a function for CD5 in regulating the TCR signaling response and in positive selection.
85. Vignaux F, Vivier E, Malissen B, Depraetere V, Nagata S, Golstein P. TCR/CD3 coupling to Fas-based cytotoxicity. J Exp Med. 181:1995;781-786.
86. Combadiere B, Freedman M, Chen L, Shores EW, Love P, Lenardo MJ. Qualitative and quantitative contributions of the T cell receptor zeta chain to mature T cell apoptosis. of special interest J Exp Med. 183:1996;2109-2117 This study examined the importance of ζ-chain ITAMs in promoting mature T cell apoptosis using IL-2 receptor α (Tac)-ζ chimeric molecules and transgenic mice in which the ζ-variant molecules were substituted for the endogenous ζ chain. The ζ chain, while not absolutely required, was especially effective at promoting apoptosis as compared with the CD3 chains, and the individual ζ-chain ITAMs exhibited differences in their ability to trigger apoptosis.
87. Singer GG, Abbas AK. The Fas antigen is involved in peripheral but not thymic deletion of T lymphocytes in T cell receptor transgenic mice. Immunity. 1:1994;365-371.
88. Castro JE, Listman JA, Jacobson BA, Wang Y, Lopez PA, Ju S, Finn PW, Perkins DL. Fas modulation of apoptosis during negative selection of thymocytes. of special interest Immunity. 5:1996;617-627 Using a sensitive assay for apoptosis, this study found that mutant Fas molecules in Ipr mice decrease the sensitivity of thymocytes to TCR-mediated apoptosis and that blockade of Fas-FasL interactions can block antigen-induced apoptosis of thymocytes in non-Ipr mice suggesting that Fas can modulate apoptosis during thymocyte negative selection.
89. Anderson KL, Anderson G, Michell RH, Jenkinson EJ, Owen JJ. Intracellular signaling pathways involved in the induction of apoptosis in immature thymic T lymphocytes. J Immunol. 156:1996;4083-4091.
90. Amakawa R, Hakem A, Kundig TM, Matsuyama T, Simard JJ, Timms E, Wakeham A, Mittruecker HW, Griesser H, Takimoto H, et al. Impaired negative selection of T cells in Hodgkins disease antigen CD30-deficient mice. Cell. 84:1996;551-562.
91. Ohno H, Ono S, Hirayama N, Shimada S, Saito T. Preferential usage of the Fc Receptor chain in the T cell antigen receptor complexes by γ/δ T cells localized in epithella. J Exp Med. 179:1994;365-369.
92. - NK1.1+T cells selected by specific class I MHC antigen. Immunity. 3:1995;427-438.
93. Guehler SR, Bluestone JA, Barrett TA. Immune deviation of 2C transgenic intraepithelial lymphocytes in antigen-bearing hosts. J Exp Med. 184:1996;493-503.
94. Poussier P, Teh HS, Julius M. Thymus-independent positive and negative selection of T cells expressing a major histocompatibility complex class I restricted transgenic T cell receptor alpha/beta in the intestinal epithelium. J Exp Med. 178:1993;1947-1957.
95. Rocha B, von Boehmer H, Guy-Grand D. Selection of intraepithelial lymphocytes with CD8 alpha/alpha co-receptors by self-antigen in the murine gut. Proc Natl Acad Sci USA. 89:1992;5336-5340.
96. Shores EW, Love PE. Insights into T cell development and signal transduction provided by TCR chain deficient mice. Int Rev Immunol. 13:1996;301-315.