Molecular mechanisms for the assembly of the T cell receptor-CD3 complex

Molecular Immunology

Volumn 40, Issue 18, 2004, Pages 1295-1305

  Call, Matthew E ^a,b   Wucherpfennig, Kai W ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CD3; T cell receptor; Transmembrane

Indexed keywords

CD3 ANTIGEN; DIMER; RECEPTOR SUBUNIT; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ACIDITY; ALKALINITY; AQUEOUS SOLUTION; CELL LINE; COMPLEX FORMATION; CROSS LINKING; DIMERIZATION; ELUTION; EXTRACELLULAR SPACE; HUMAN; HYDROGEN BOND; IMMUNOPRECIPITATION; LEUKEMIA CELL LINE; LIPID BILAYER; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTON TRANSPORT; REVIEW; SOLUBILIZATION; STOICHIOMETRY; T LYMPHOCYTE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD3; ENDOPLASMIC RETICULUM; HUMANS; MACROMOLECULAR SUBSTANCES; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; RECEPTOR-CD3 COMPLEX, ANTIGEN, T-CELL; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA;

EID: 1842505447     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2003.11.017     Document Type: Review

References (61)

1. Alcover A., Mariuzza R.A., Ermonval M., Acuto O. Lysine 271 in the transmembrane domain of the T-cell antigen receptor beta chain is necessary for its assembly with the CD3 complex but not for alpha/beta dimerization. J. Biol. Chem. 265:1990;4131-4135.
2. Berkhout B., Alarcon B., Terhorst C. Transfection of genes encoding the T cell receptor-associated CD3 complex into COS cells results in assembly of the macromolecular structure. J. Biol. Chem. 263:1988;8528-8536.
3. Bijlmakers M.J., Neefjes J.J., Wojcik-Jacobs E.H., Ploegh H.L. The assembly of H2-Kb class I molecules translated in vitro requires oxidized glutathione and peptide. Eur. J. Immunol. 23:1993;1305-1313.
4. Bijlmakers M.J., Benaroch P., Ploegh H.L. Assembly of HLA DR1 molecules translated in vitro: binding of peptide in the endoplasmic reticulum precludes association with invariant chain. EMBO J. 13:1994;2699-2707.
5. Blumberg R.S., Alarcon B., Sancho J., McDermott F.V., Lopez P., Breitmeyer J., Terhorst C. Assembly and function of the T cell antigen receptor. Requirement of either the lysine or arginine residues in the transmembrane region of the alpha chain. J. Biol. Chem. 265:1990;14036-14043.
6. Bonifacino J.S., Chen C., Lippincott-Schwartz J., Ashwell J.D., Klausner R.D. Subunit interactions within the T-cell antigen receptor: clues from the study of partial complexes. Proc. Natl. Acad. Sci. U.S.A. 85:1988;6929-6933.
7. Bonifacino J.S., Suzuki C.K., Lippincott-Schwartz J., Weissman A.M., Klausner R.D. Pre-Golgi degradation of newly synthesized T-cell antigen receptor chains: intrinsic sensitivity and the role of subunit assembly. J. Cell Biol. 109:1989;73-83.
8. Bonifacino J.S., Cosson P., Klausner R.D. Colocalized transmembrane determinants for ER degradation and subunit assembly explain the intracellular fate of TCR chains. Cell. 63:1990;503-513.
9. Bonifacino J.S., Cosson P., Shah N., Klausner R.D. Role of potentially charged transmembrane residues in targeting proteins for retention and degradation within the endoplasmic reticulum. EMBO J. 10:1991;2783-2793.
10. Borel A.C., Simon S.M. Biogenesis of polytopic membrane proteins: membrane segments assemble within translocation channels prior to membrane integration. Cell. 85:1996;379-389.
11. Brenner M.B., Trowbridge I.S., Strominger J.L. Cross-linking of human T cell receptor proteins: association between the T cell idiotype beta subunit and the T3 glycoprotein heavy subunit. Cell. 40:1985;183-190.
12. Call M.E., Pyrdol J., Wiedmann M., Wucherpfennig K.W. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell. 111:2002;967-979.
13. Campbell K.S., Backstrom B.T., Tiefenthaler G., Palmer E. CART: a conserved antigen receptor transmembrane motif. Semin. Immunol. 6:1994;393-410.
14. Carr P.D., Gustin S.E., Church A.P., Murphy J.M., Ford S.C., Mann D.A., Woltring D.M., Walker I., Ollis D.L., Young I.G. Structure of the complete extracellular domain of the common beta subunit of the human GM-CSF, IL-3, and IL-5 receptors reveals a novel dimer configuration. Cell. 104:2001;291-300.
15. Chen C., Bonifacino J.S., Yuan L.C., Klausner R.D. Selective degradation of T cell antigen receptor chains retained in a pre-Golgi compartment. J. Cell Biol. 107:1988;2149-2161.
16. Choma C., Gratkowski H., Lear J.D., DeGrado W.F. Asparagine-mediated self-association of a model transmembrane helix. Nat. Struct. Biol. 7:2000;161-166.
17. Cosson P., Lankford S.P., Bonifacino J.S., Klausner R.D. Membrane protein association by potential intramembrane charge pairs. Nature. 351:1991;414-416.
18. Dave V.P., Cao Z., Browne C., Alarcon B., Fernandez-Miguel G., Lafaille J., de la Hera A., Tonegawa S., Kappes D.J. CD3 delta deficiency arrests development of the alpha beta but not the gamma delta T cell lineage. EMBO J. 16:1997;1360-1370.
19. Engel I., Letourneur F., Houston J.T., Ottenhoff T.H., Klausner R.D. T cell receptor structure and function: analysis by expression of portions of isolated subunits. Adv. Exp. Med. Biol. 323:1992;1-7.
20. Engelman D.M. Electrostatic fasteners hold the T cell receptor-CD3 complex together. Mol. Cell. 11:2003;5-6.
21. Exley M., Terhorst C., Wileman T. Structure, assembly and intracellular transport of the T cell receptor for antigen. Semin. Immunol. 3:1991;283-297.
22. Exley M., Wileman T., Mueller B., Terhorst C. Evidence for multivalent structure of T-cell antigen receptor complex. Mol. Immunol. 32:1995;829-839.
23. Fernandez-Miguel G., Alarcon B., Iglesias A., Bluethmann H., Alvarez-Mon M., Sanz E., de la Hera A. Multivalent structure of an alphabeta T cell receptor. Proc. Natl. Acad. Sci. U.S.A. 96:1999;1547-1552.
24. Garboczi D.N., Ghosh P., Utz U., Fan Q.R., Biddison W.E., Wiley D.C. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature. 384:1996;134-141.
25. Garcia K.C., Degano M., Stanfield R.L., Brunmark A., Jackson M.R., Peterson P.A., Teyton L., Wilson I.A. An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science. 274:1996;209-219.
26. Geisler C. Failure to synthesize the CD3-gamma chain. Consequences for T cell antigen receptor assembly, processing, and expression. J. Immunol. 148:1992;2437-2445.
27. Geisler C., Kuhlmann J., Rubin B. Assembly, intracellular processing, and expression at the cell surface of the human alpha beta T cell receptor/CD3 complex, function of the CD3-zeta chain. J. Immunol. 143:1989;4069-4077.
28. Gorlich D., Rapoport T.A. Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell. 75:1993;615-630.
29. Gratkowski H., Lear J.D., DeGrado W.F. Polar side chains drive the association of model transmembrane peptides. Proc. Natl. Acad. Sci. U.S.A. 98:2001;880-885.
30. Hall C., Berkhout B., Alarcon B., Sancho J., Wileman T., Terhorst C. Requirements for cell surface expression of the human TCR/CD3 complex in non-T cells. Int. Immunol. 3:1991;359-368.
31. He X., Chow D., Martick M.M., Garcia K.C. Allosteric activation of a spring-loaded natriuretic peptide receptor dimer by hormone. Science. 293:2001;1657-1662.
32. Hebert D.N., Zhang J.X., Helenius A. Protein folding and maturation in a cell-free system. Biochem. Cell Biol. 76:1998;867-873.
33. Heinrich S.U., Mothes W., Brunner J., Rapoport T.A. The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell. 102:2000;233-244.
34. Huppa J.B., Ploegh H.L. In vitro translation and assembly of a complete T cell receptor-CD3 complex. J. Exp. Med. 186:1997;393-403.
35. Jacobs H. Pre-TCR/CD3 and TCR/CD3 complexes: decamers with differential signalling properties. Immunol. Today. 18:1997;565-569.
36. John S., Banting G.S., Goodfellow P.N., Owen M.J. Surface expression of the T cell receptor complex requires charged residues within the alpha chain transmembrane region. Eur. J. Immunol. 19:1989;335-339.
37. Kane L.P., Lin J., Weiss A. Signal transduction by the TCR for antigen. Curr. Opin. Immunol. 12:2000;242-249.
38. Kearse K.P., Roberts J.L., Singer A. TCR alpha-CD3 delta epsilon association is the initial step in alpha beta dimer formation in murine T cells and is limiting in immature CD4+ CD8+ thymocytes. Immunity. 2:1995;391-399.
39. Klausner R.D., Lippincott-Schwartz J., Bonifacino J.S. The T cell antigen receptor: insights into organelle biology. Annu. Rev. Cell Biol. 6:1990;403-431.
40. Koning F., Maloy W.L., Coligan J.E. The implications of subunit interactions for the structure of the T cell receptor-CD3 complex. Eur. J. Immunol. 20:1990;299-305.
41. Livnah O., Stura E.A., Middleton S.A., Johnson D.L., Jolliffe L.K., Wilson I.A. Crystallographic evidence for preformed dimers of erythropoietin receptor before ligand activation. Science. 283:1999;987-990.
42. Luecke H., Schobert B., Richter H.T., Cartailler J.P., Lanyi J.K. Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution. Science. 286:1999a;255-261.
43. Luecke H., Schobert B., Richter H.T., Cartailler J.P., Lanyi J.K. Structure of bacteriorhodopsin at 1.55 A resolution. J. Mol. Biol. 291:1999b;899-911.
44. Manolios N., Letourneur F., Bonifacino J.S., Klausner R.D. Pairwise, cooperative and inhibitory interactions describe the assembly and probable structure of the T-cell antigen receptor. EMBO J. 10:1991;1643-1651.
45. Marie-Cardine A., Schraven B. Coupling the TCR to downstream signalling pathways: the role of cytoplasmic and transmembrane adaptor proteins. Cell Signal. 11:1999;705-712.
46. Matlack K.E., Mothes W., Rapoport T.A. Protein translocation: tunnel vision. Cell. 92:1998;381-390.
47. Plemper R.K., Wolf D.H. Retrograde protein translocation: eradication of secretory proteins in health and disease. Trends Biochem. Sci. 24:1999;266-270.
48. Punt J.A., Roberts J.L., Kearse K.P., Singer A. Stoichiometry of the T cell antigen receptor (TCR) complex: each TCR/CD3 complex contains one TCR alpha, one TCR beta, and two CD3 epsilon chains. J. Exp. Med. 180:1994;587-593.
49. Remy I., Wilson I.A., Michnick S.W. Erythropoietin receptor activation by a ligand-induced conformation change. Science. 283:1999;990-993.
50. Ribaudo R.K., Margulies D.H. Independent and synergistic effects of disulfide bond formation, beta 2-microglobulin, and peptides on class I MHC folding and assembly in an in vitro translation system. J. Immunol. 149:1992;2935-2944.
51. Ribaudo R.K., Margulies D.H. Polymorphism at position nine of the MHC class I heavy chain affects the stability of association with beta 2-microglobulin and presentation of a viral peptide. J. Immunol. 155:1995;3481-3493.
52. Rutledge T., Cosson P., Manolios N., Bonifacino J.S., Klausner R.D. Transmembrane helical interactions: zeta chain dimerization and functional association with the T cell antigen receptor. EMBO J. 11:1992;3245-3254.
53. San Jose E., Sahuquillo A.G., Bragado R., Alarcon B. Assembly of the TCR/CD3 complex: CD3 epsilon/delta and CD3 epsilon/gamma dimers associate indistinctly with both TCR alpha and TCR beta chains. Evidence for a double TCR heterodimer model. Eur. J. Immunol. 28:1998;12-21.
54. Sun Z.J., Kim K.S., Wagner G., Reinherz E.L. Mechanisms contributing to T cell receptor signaling and assembly revealed by the solution structure of an ectodomain fragment of the CD3 epsilon gamma heterodimer. Cell. 105:2001;913-923.
55. Sussman J.J., Bonifacino J.S., Lippincott-Schwartz J., Weissman A.M., Saito T., Klausner R.D., Ashwell J.D. Failure to synthesize the T cell CD3-zeta chain: structure and function of a partial T cell receptor complex. Cell. 52:1988;85-95.
56. Walter P., Blobel G. Preparation of microsomal membranes for cotranslational protein translocation. Methods Enzymol. 96:1983;84-93.
57. Weissman A.M., Frank S.J., Orloff D.G., Mercep M., Ashwell J.D., Klausner R.D. Role of the zeta chain in the expression of the T cell antigen receptor: genetic reconstitution studies. EMBO J. 8:1989;3651-3656.
58. Wileman T., Carson G.R., Concino M., Ahmed A., Terhorst C. The gamma and epsilon subunits of the CD3 complex inhibit pre-Golgi degradation of newly synthesized T cell antigen receptors. J. Cell Biol. 110:1990;973-986.
59. Wilson D.S., Keefe A.D., Szostak J.W. The use of mRNA display to select high-affinity protein-binding peptides. Proc. Natl. Acad. Sci. U.S.A. 98:2001;3750-3755.
60. Zhou F.X., Cocco M.J., Russ W.P., Brunger A.T., Engelman D.M. Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nat. Struct. Biol. 7:2000;154-160.
61. Zhou F.X., Merianos H.J., Brunger A.T., Engelman D.M. Polar residues drive association of polyleucine transmembrane helices. Proc. Natl. Acad. Sci. U.S.A. 98:2001;2250-2255.