Importance of the CD3γ ectodomain terminal β-strand and membrane proximal stalk in thymic development and receptor assembly

Journal of Immunology

Volumn 178, Issue 6, 2007, Pages 3668-3679

  Touma, Maki ^a   Sun, Zhen Yu J ^a   Clayton, Linda K ^a   Marissen, Wilfred E ^b,c   Kruisbeek, Ada M ^b,d   Wagner, Gerhard ^a   Reinherz, Ellis L ^a,e  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c CRUCELL HOLLAND BV   (Netherlands)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISERUM; CD3 ANTIGEN; CD3DELTA ANTIGEN; CD3EPSILON ANTIGEN; CD3GAMMA ANTIGEN; CELL SURFACE RECEPTOR; COMPLEMENTARY DNA; CYSTEINE; HETERODIMER; HISTIDINE; IMMUNOGLOBULIN; METAL; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; CD3 ANTIGEN, GAMMA CHAIN; CD3E PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BETA SHEET; CELL STRAIN COS7; COMPARATIVE STUDY; CONTROLLED STUDY; DISULFIDE BOND; FETUS; GENE EXPRESSION; GENETIC TRANSFECTION; LYMPHOID CELL; MOUSE; NONHUMAN; ORGAN CULTURE; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MOTIF; RETROVIRUS; SIGNAL TRANSDUCTION; STEM CELL; THYMIC DEVELOPMENT; THYMOCYTE; ANIMAL; GENETIC TRANSDUCTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; MISSENSE MUTATION; MOUSE MUTANT; ORGAN CULTURE TECHNIQUE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; THYMUS;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, CD3; MICE; MICE, KNOCKOUT; MUTATION, MISSENSE; ORGAN CULTURE TECHNIQUES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANTIGEN, T-CELL; RETROVIRIDAE; SIGNAL TRANSDUCTION; THYMUS GLAND; TRANSDUCTION, GENETIC;

EID: 33947194751     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.6.3668     Document Type: Article

References (51)

1. Alarcon, B., B. Berkhout, J. Breitmeyer, and C. Terhorst. 1988. Assembly of the human T cell receptor-CD3 complex takes place in the endoplasmic reticulum and involves intermediary complexes between the CD3- γδε core and single T cell receptor α or β chains. J. Biol. Chem. 263: 2953-2961.
2. Davis, M. M., and P. J. Bjorkman. 1988. T cell antigen receptor genes and T cell recognition. Nature 334: 395-402.
3. de la Hera, A., U. Muller, C. Olsson, S. Isaaz, and A. Tunnacliffe. 1991. Structure of the T cell antigen receptor (TCR): two CD3ε subunits in a functional TCR/ CD3 complex. J. Exp. Med. 173: 7-17.
4. Ghendler, Y., A. Smolyar, H.-C. Chang, and E. L. Reinherz. 1998. One of the CD3ε subunits within a T cell receptor complex lies in close proximity to the Cβ FG loop. J. Exp. Med. 187: 1529-1536.
5. Hayes, S. M., E. W. Shores, and P. E. Love. 2003. An architectural perspective on signaling by the pre-, αβ and γδ T cell receptors. Immunol. Rev. 191: 28-37.
6. Koning, R, W. L. Maloy, and J. E. Coligan. 1990. The implications of subunit interactions for the structure of the T cell receptor-CD3 complex. Eur. J. Immunol. 20: 299-305.
7. Manolios, N., F. Letourneur, J. S. Bonifacino, and R. D. Klausner. 1991. Pair-wise, cooperative and inhibitory interactions describe the assembly and probable structure of the T cell antigen receptor. EMBO J. 10: 1643-1651.
8. Punt, J. A., J. L. Roberts, K. P. Kearse, and A. Singer. 1994. Stoichiometry of the T cell antigen receptor (TCR) complex: each TCR/CD3 complex contains one TCR α, one TCR β, and two CD3ε chains. J. Exp. Med. 180: 587-593.
9. Reinherz, E., S. C. Meuer, and S. F. Schlossman. 1983. The human T cell receptor: analysis with cytotoxic T cell clones. Immunol. Rev. 74: 83-112.
10. Irving, B. A., and A. Weiss. 1991. The cytoplasmic domain of the T cell receptor ζ chain is sufficient to couple to receptor-associated signal transduction pathways. Cell 64: 891-901.
11. Letourneur, F., and R. D. Klausner. 1992. Activation of T cells by a tyrosine kinase activation domain in the cytoplasmic tail of CD3ε. Science 255: 79-82.
12. Reth, M. 1989. Antigen receptor tail clue. Nature 338: 383-384.
13. Exley, M., L. Varticovski, M. Peter, J. Sancho, and C. Terhorst. 1994. Association of phosphatidylinositol 3-kinase with a specific sequence of the T cell receptor ζ chain is dependent on T cell activation. J. Biol. Chem. 269: 15140-15146.
14. Isakov, N., R. L. Wange, W. H. Burgess, J. D. Watts, R. Aebersold, and L. E. Samelson. 1995. 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: 375-380.
15. Ravichandran, K. S., K. K. Lee, Z. Songyang, L. C. Cantley, P. Burn, and S. J. Burakoff. 1993. Interaction of Shc with the ζ chain of the T cell receptor upon T cell activation. Science 262: 902-905.
16. Sunder-Plassmann, R., F. Lialios, M. Madsen, S. Koyasu, and E. L. Reinherz. 1997. Functional analysis of immunoreceptor tyrosine-based activation motif (ITAM)-mediated signal transduction: the two YxxL segments within a single CD3ζ-ITAM are functionally distinct. Eur. J. Immunol. 27: 2001-2009.
17. Hogquist, K. A., T. A. Baldwin, and S. C. Jameson. 2005. Central tolerance: learning self-control in the thymus. Nat. Rev. Immunol. 5: 772-782.
18. Saint-Ruf, C., K. Ungewiss, M. Groettrup, L. Bruno, H. J. Fehling, and H. von Boehmer. 1994. Analysis and expression of a cloned pre-T cell receptor gene. Science 266: 1208-1212.
19. von Boehmer, H. 2005. Unique features of the pre-T-cell receptor α-chain: not just a surrogate. Nat. Rev. Immunol. 5: 571-577.
20. Aifantis, I., J. Buer, H. von Boehmer, and O. Azogui. 1997. Essential role of the pre-T cell receptor in allelic exclusion of the T cell receptor β locus. Immunity 1: 601-607.
21. Krotkova, A., H. von Boehmer, and H. J. Fehling. 1997. Allelic exclusion in pTα-deficient mice: no evidence for cell surface expression of two T cell receptor (TCR)-β chains, but less efficient inhibition of endogeneous Vβ-> (D)Jβ rearrangements in the presence of a functional TCR-β transgene. J. Exp. Med. 186: 767-775.
22. von Boehmer, H., and H. J. Fehling. 1997. Structure and function of the pre-T cell receptor. Annu. Rev. Immunol. 15: 433-452.
23. Sun, Z.-Y. J., K. S. Kim, G. Wagner, and E. L. Reinherz. 2001. Mechanisms contributing to T cell receptor signaling and assembly revealed by the solution structure of an ectodomain fragment of the CD3εγ heterodimer. Cell 105: 913-923.
24. Sun, Z. Y., S. T. Kim, I. C. Kim, A. Fahmy, E. L. Reinherz, and G. Wagner. 2004. Solution structure of the CD3εδ ectodomain and comparison with CD3εγ as a basis for modeling T cell receptor topology and signaling. Proc. Natl. Acad. Sci. USA 101: 16867-16872.
25. Arnett, K. L., S. C. Harrison, and D. C. Wiley. 2004. Crystal structure of a human CD3-ε/δ dimer in complex with a UCHT1 single-chain antibody fragment. Proc. Natl. Acad. Sci. USA 101: 16268-16273.
26. Kjer-Nielsen, L., M. A. Dunstone, L. Kostenko, L. K. Ely, T. Beddoe, N. A. Mifsud, A. W. Purcell, A. G. Brooks, J. McCluskey, and J. Rossjohn. 2004. Crystal structure of the human T cell receptor CD3εγ heterodimer complexed to the therapeutic mAb OKT3. Proc. Natl. Acad. Sci. USA 101: 7675-7680.
27. Haks, M. C., P. Krimpenfort, J. Borst, and A. M. Kruisbeek. 1998. The CD3γ chain is essential for development of both the TCRαβ and TCRγδ lineages. EMBO J. 17: 1871-1882.
28. Jaleco, A. C., A. P. A. Stegmann, M. H. M. Heemskerk, F. Couwenberg, A. Q. Bakker, K. Weijer, and H. Spits. 1999. Genetic modification of human B-cell development is inhibited by the dominant negative helix loop helix factor Id3. Blood 94: 2637-2646.
29. Kinsella, T. M., and G. P. Nolan. 1996. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7: 1405-1413.
30. Hooijberg, E., A. Q. Bakker, J. J. Ruizendaal, and H. Spits. 2000. NFAT-controlled expression of GFP permits visualization and isolation of antigen-stimulated primary human T cells. Blood 96: 459-466.
31. Dardalhon, V., N. Noraz, M. Boyer, A. Q. Bakker, K. Pollok, C. Rebouissou, E. Spits, and N. Taylor. 1999. Green fluorescent protein as a selectable marker of fibronectin-facilitated retroviral gene transfer in primary human T lymphocytes. Hum. Gene Ther. 10: 5-14.
32. Myers, L. C., G. L. Verdine, and G. Wagner. 1993. Solution structure of the DNA methyl phosphotriester repair domain of Escherichia coli Ada. Biochemistry 32: 14089-14094.
33. Schwabe, J. W. R., D. Neuhaus, and D. Rhodes. 1990. Solution structure of the DNA-binding domain of the oestrogen receptor. Nature 348: 458-461.
34. Haks, M. C., E. Pepin, J. H. van den Brakel, S. Smeele, S. M. Belkowski, H. W. Kessels, P. Krimpenfort, and A. M. Kruisbeek. 2002. Contributions of the T cell receptor-associated CD3γ-ITAM to thymocyte selection. J. Exp. Med. 196: 1-13.
35. Hayes, S. M., and P. E. Love. 2002. Distinct structure and signaling potential of the γδ TCR complex. Immunity 16: 827-838.
36. Call, M. E., J. Pyrdol, M. Wiedmann, and K. W. Wucherpfennig. 2002. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 111: 967-979.
37. Igbalsvah, T. M., E. Moutevelis, J. Warwicker, N. Errington, and A. J. Doig. 2006. The CXXC motif at the N terminus of an α-helical peptide. Protein Sci. 15: 1945-1950.
38. Hsu, H. J., H. J. Chang, H. P. Peng, S. S. Huang, M. Y. Lin, and A. S. Yang. 2006. Assessing computational amino acid β turn propensities with a phage-displayed combinatorial library and directed evolution. Structure 14: 1499-1510.
39. Pani, G., R. Colavitti, S. Borrello, and T. Galeotti. 2000. Endogenous oxygen radicals modulate protein tyrosine phosphorylation and JNK-1 activation in lectin-stimulated thymocytes. Biochem. J. 347: 173-181.
40. Devadas, S., L. Zaritskaya, S. G. Rhee, L. Oberley, and M. S. Williams. 2002. Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J. Exp. Med. 195: 59-70.
41. Otsuji, M., Y. Kimura, T. Aoe, Y. Okamoto, and T. Saito. 1996. Oxidative stress by tumor-derived macrophages suppresses the expression of CD3 ζ chain of T-cell receptor complex and antigen-specific T cell responses. Proc. Natl. Acad. Sci. USA 93: 13119-13124.
42. Thomassen, E. A. J., E. H. A. Dekking, A. Thompson, K. L. Franken, O. OSanal, J. P. Abrahams, M. J. D. van Tol, and F. Koning. 2006. The impact of single amino acid substitutions in CD3γ on the CD3εγ interaction and T-cell receptor-CD3 complex formation. Hum. Immunol. 67: 579-588.
43. Xu, C., M. E. Call, and K. W. Wucherpfennig. 2006. A membrane-proximal tetracysteine motif contributes to assembly of CD3δε and CD3γε dimers with the T cell receptor. J. Biol. Chem. 281: 36977-36984.
44. Borroto, A., A. Mallabiabarrena, J. P. Albar, C. Martinez-A., and B. Alarcon. 1998. Characterization of the region involved in CD3 pairwise interactions within the T cell receptor complex. J. Biol. Chem. 273: 12807-12816.
45. Delgado, P., E. Fernandez, V. Dave, D. Kappes, and B. Alarcon. 2000. CD3δ couples T cell receptor signaling to ERK activation and thymocyte positive selection. Nature 406: 426-430.
46. Dave, V. P., Z. Cao, C. Browne, B. Alarcon, G. Fernandez-Miguel, J. Lafaille, A. de la Hera, S. Tonegawa, and D. J. Kappes. 1997. CD3δ deficiency arrests development of the αβ but not the γδ T cell lineage. EMBO J. 16: 1360-1370.
47. Dadi, H. K., A. J. Simon, and C. M. Roifman. 2003. Effect of CD3δ deficiency on maturation of α/β and γ/δ T-cell lineages in severe combined immunodeficiency. N. Engl. J. Med. 349: 1821-1828.
48. de Saint Basile, G., F. Geissmann, E. Flori, B. Uring-Lambert, C. Soudais, M. Cavazzana-Calvo, A. Durandy, N. Jabado, A. Fischer, and F. Le Deist. 2004. Severe combined immunodeficiency caused by deficiency in either the δ or the ε subunit of CD3. J. Clin. Invest. 114: 1512-1517.
49. Arnaiz-Villena, A., M. Timon, A. Corell, P. Perez-Aciego, J. M. Martin-Villa, and J. R. Reguerio. 1992. Brief report: primary immunodeficiency caused by mutations in the gene encoding the CD3-γ subunit of the T-lymphocyte receptor. N. Engl. J. Med. 327: 529-533.
50. Fernandez-Malave, E., N. Wang, M. Pulgar, W. W. A. Schamel, B. Alarcon, and C. Terhorst. 2006. Overlapping functions of human CD3δ and mouse CD3γ in αβ T cell development revealed in a humanized CD3γ-deficient mouse. Blood 108: 3420-3427.
51. Pan, Q., J.-F. Brodeur, K. Drbal, and V. P. Dave. 2006. Different role for mouse and human CD3δ/ε heterodimer in preT cell receptor (preTCR) function: human CD3δ/ε heterodimer restores the defective preTCR function in CD3γ- and CD3γδ-deficient mice. Mol. Immunol. 43: 1741-1750.