Masking of the CD3γ di-leucine-based motif by ζ is required for efficient T-cell receptor expression

Traffic

Volumn 5, Issue 9, 2004, Pages 672-684

  Lauritsen, Jens Peter H ^a   Bonefeld, Charlotte Menné ^a   von Essen, Marina ^a   Nielsen, Martin Weiss ^a   Rasmussen, Anette Bødker ^a   Ødum, Niels ^a   Dietrich, Jes ^b   Geisler, Carsten ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b STATENS SERUM INSTITUT   (Denmark)

Author keywords

Degradation; Endocytosis; Sorting motifs; T lymphocytes; T cell receptors; Traffic; Truncations

Indexed keywords

CD3 ANTIGEN; LEUCINE; T LYMPHOCYTE RECEPTOR;

ARTICLE; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; MASKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD3; CELL LINE; ENDOCYTOSIS; GENE EXPRESSION REGULATION; HUMANS; MOLECULAR SEQUENCE DATA; RECEPTORS, ANTIGEN, T-CELL;

EID: 4444270185     PISSN: 13989219     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2004.00211.x     Document Type: Article

References (58)

1. Bonifacino JS, Chen C, Lippincott-Schwartz J, Ashwell JD, Klausner RD. Subunit interactions within the T-cell antigen receptor: Clues from the study of partial complexes. Proc Natl Acad Sci USA 1988;85: 6929-6933.
2. Clevers H, Alarcon B, Willeman T, Terhorst C. The T cell receptor/CD3 complex: a dynamic protein ensemble. Annu Rev Immunol 1988;6:629-662.
3. Koning F, Maloy WL, Coligan JE. The implications of subunit interactions for the structure of the T cell receptor-CD3 complex. Eur J Immunol 1990;20:299-305.
4. Manolios N, Letourneur F, Bonifacino JS, Klausner RD. Pairwise, cooperative and inhibitory interactions describe the assembly and probable structure of the T-cell antigen receptor. EMBO J 1991;10:1643-1651.
5. Hou X, Dietrich J, Kuhlmann J, Wegener A-MK, Geisler C. Structure of the T cell receptor in a TiaVβ2,aVβ8 positive cell line. Eur J Immunol 1994;24:1228-1233.
6. Call ME, Pyrdol J, Wiedmann M, Wucherpfennig KW. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 2002; 111:967-979.
7. Dembic Z, Haas W, Weiss S, McCubrey J, Kiefer H, von Boehmer H, Steinmetz M. Transfer of specificity by murine α and β T-cell receptor genes. Nature 1986;320:232-238.
8. Saito T, Weiss A, Miller J, Norcross MA, Germain RN. Specific antigenla activation of transfected human T cells expressing murine Ti α β human T3 receptor complexes. Nature 1987;325:125-130.
9. Frank SJ, Niklinska BB, Orloff DG, Mercep M, Ashwell JD, Klausner RD. Structural mutations of the T cell receptor ζ chain and its role in T cell activation. Science 1990;249:174-177.
10. Wegener A-MK, 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 1992;68:83-95.
11. Letourneur F, Klausner RD. Activation of T cells by a tyrosine kinase activation domain in the cytoplasmic tail of CD3Ε. Science 1992;255:79-82.
12. Malissen B, Schmitt-Verhulst AM. Transmembrane signalling through the T-cell-receptor-CD3 complex. Curr Opin Immunol 1993;5:324-333.
13. Geisler C. The T cell receptor. Structural and functional studies. Dan Med Bull 1995;42:342-357.
14. Sussman JJ, Bonifacino JS, Lippincott-Schwartz J, Weissman AM, Saito T, Klausner RD, Ashwell JD. Failure to synthesize the T cell CD3-ζ chain: structure and function of a partial T cell receptor complex. Cell 1988;52:85-95.
15. Geisler C. Failure to synthesize the CD3-y chain. Consequences for T cell antigen receptor assembly, processing, and expression. J Immunol 1992;148:2437-2445.
16. Bonifacino JS, Cosson P, Klausner RD. Colocalized transmembrane determinants for ER degradation and subunit assembly explain the intracellular fate of TCR chains. Cell 1990;63:503-513.
17. Letourneur F, Klausner RD. A novel di-leucine motif and a tyrosinebased motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 1992;69:1143-1157.
18. Mallabiabarrena A, Fresno M, Alarcon B. An endoplasmic reticulum retention signal in the CD3Ε chain of the T-cell receptor. Nature 1992;357:593-596.
19. Dietrich J, Hou X, Wegener AM, Geisler C. CD3y contains a phosphoserine-dependent di-leucine motif involved in down-regulation of the T cell receptor.EMBO J 1994;13:2156-2166.
20. Borroto A, Lama J, Niedergang F, Dautry-Varsat A, Alarcon B, Alcover A. The CD3Ε subunit of the TCR contains endocytosis signals. J Immunol 1999;163:25-31.
21. Torres PS, Alcover A, Zapata DA, Arnaud J, Pacheco A, Martin-Fernandez JM, Villasevil EM, Sanal O, Regueiro JR. TCR dynamics inhuman mature T lymphocytes lacking CD3Ε. J Immunol 2003;170:5947-5955.
22. Geiser C. TCR trafficking in resting and stimulated T cells. Crit Rev Immunol 2004;24:67-86.
23. Schonrich G, Kalinke U, Momburg F, Malissen M, Schmitt-Verhulst AM, Malissen B, Harnmerling GJ, Arnold B. Down-regulation of T cellreceptors on self-reactive T cells as a novel mechanism for extrathymictolerance induction. Cell 1991;65:293-304.
24. Ferber I, Schonrich G, Schenkel J, Mellor AL, Harnmerling GJ, Arnold B. Levels of peripheral T cell tolerance induced by different doses oftolerogen. Science 1994;263:674-676.
25. Valitutti S, Muller S, Dessing M, Lanzavecchia A. Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J Exp Med 1996;183:1917-1921.
26. Carballido JM, Faith A, Carballido-Perrig N, Blaser K. The intensity of T cell receptor engagement determines the cytokine pattern of human allergen-specific T helper cells. Eur J Immunol 1997;27:515-521.
27. Menne C, Lauritsen JP, Dietrich J, Kastrup J, Wegener AM, Odum N, Geisler C. Ceramide-induced TCR up-regulation. J Immunol 2000;165:3065-3072.
28. Cantrell DA, Davies AA, Crumpton MJ. Activators of protein kinase C down-regulate and phosphorylate the T3/T-cell antigen receptor complex of human T lymphocytes. Proc Natl Acad Sci U S A 1985;82:815&-8162.
29. Ando I, Hariri G, Wallace D, Beverley P. Tumor promoter phorbol esters induce unresponsiveness to antigen and expression of interleukin 2 receptor on T cells. Eur J Immunol 1985; 15:196-199.
30. Dietrich J, Hou X, Wegener AM, Pedersen LO, Odum N, Geisler C. Molecular characterization of the di-leucine-based internalization motif of the T cell receptor. J Biol Chem 1996;271:11441-11448.
31. Dietrich J, Kastrup J, Nielsen BL, Odum N, Geisler C. Regulation and function of the CD3y DLL motif. a binding site for adaptor protein-1 and adaptor protein-2 in vitro. J Cell Biol 1997;138:271-281.
32. Lamb JR, Skidmore BJ, Green N, Chiller JM, Feldmann M. Induction of tolerance in influenza virus-immune T lymphocyte clones with synthetic peptides of influenza hemagglutinin. J Exp Mad 1983; 157:1434-1447.
33. Valitutti S, Muller S, Cella M, Padovan E, Lanzavecchia A. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 1995;375:148-151.
34. + T cells. J Exp Med 1997;185:641-651.
35. Niedergang F, Hemar A, Hewitt CR, Owen MJ, Dautry-Varsat A, Alcover A. The Staphylococcus aureus enterotoxin B superantigen induces specific T cell receptor down-regulation by increasing its internalization. J Biol Chem 1995;270:12839-12845.
36. Makida R, Hofer MF, Takase K, Cambier JC, Leung DY. Bacterial superantigens induce Vβ-specific T cell receptor internalization. Mol Immunol 1996;33:891-900.
37. Telerman A, Amson RB, Romasco F, Wybran J, Galand P, Mosselmans R. Internalization of human T lymphocyte receptors. Eur J Immunol 1987;17:991-997.
38. Boyer C, Auphan N, Luton F, Malburet JM, Barad M, Bizozzero JP, Reggio H, Schmitt-Verhulst AM. T cell receptor/CD3 complex internalization following activation of a cytolytic T cell clone: evidence for a protein kinase C-independent staurosporine-sensitive step. Eur J Immunol 1991;21:1623-1634.
39. Lauritsen JP, Christensen MD, Dietrich J, Kastrup J, Odum N, Geisler C. Two distinct pathways exist for down-regulation of the TCR. J Immunol 1998;161:260-267.
40. D'Oro U, Vacchio MS, Weissman AM, Ashwell JD. Activation of the Lck tyrosine kinase targets cell surface T cell antigen receptors for lysosomal degradation. Immunity 1997;7:619-628.
41. von Essen M, Menne C, Nielsen BL, Lauritsen JP, Dietrich J, Andersen PS, Karjalainen K, Odurn N, Geisler C. The CD3y leucinebased receptor-sorting motif is required for efficient ligand-mediated TCR down-regulation. J Immunol 2002;168:4519-4523.
42. Krangel MS. Endocytosis and recycling of the T3-T cell receptor complex. The role of T3 phosphorylation. J Exp Med 1987;165: 1141-1159.
43. Minami Y, Samelson LE, Klausner RD. Internalization and cycling of the T cell antigen receptor. Role of protein kinase C. J Biol Chem 1987;262:13342-13347.
44. Menne C, Moller ST Siersma V, von Essen M, Odum N, Geisler C. Endo- and exocytic rate constants for spontaneous and protein kinase C-activated T cell receptor cycling. Eur J Immunol 2002;32: 616-626.
45. Liu H, Rhodes M, Wiest DL, Vignali DA. On the dynamics of TCR. CD3 complex cell surface expression and downmodulation. Immunity 2000;13:665-675.
46. Dietrich J, Menne C, Lauritsen JP, von Essen M, Rasmussen AB, Odum N, Geisler C. Ligand-induced TCR down-regulation is not dependent on constitutive TCR cycling. J Immunol 2002,168: 5434-5440.
47. Dietrich J, Geisler C. T cell receptor ζ allows stable expression of receptors containing the CD3y leucine-based receptor-sorting motif. J Biol Chem 1998;273:26281-26284.
48. D'Oro U, Munitic I, Chacko G, Karpova T, McNally J, Ashwell JD. Regulation of constitutive TCR internalization by the ζ-chain. J Immunol 2002; 169:6269-6278.
49. Gastman BR, Johnson DE, Whiteside TL, Rabinowich H. Caspase-mediated degradation of T-cell receptor ζ-chain. Cancer Res 1999;59:1422-1427.
50. MenneC, LauritsenJP, DietrichJ, Kastrup J, Wegener AK, Andersen PS, Odum N, Geisler C. T-cell receptor downregulation by ceramide-induced caspase activation and cleavage of the ζ chain. Scand J Immunol 2001;53:176-183.
51. von Essen M, Bonefeld CM, Siersma V, Rasmussen AB, Lauritsen JPH, Nielsen BL, Geisler C. Constitutive and ligand-induced TCR degradation. J Immunol 2004,173:384-393.
52. Dietrich J, Kastrup J, Lauritsen JP, Menne C, von Bulow F, Geisler C. TCRζ is transported to and retained in the Golgi apparatus independently of other TCR chains: implications for TCR assembly. Eur J Immunol 1999;29:1719-1728.
53. Dietrich J, Backstrorn T, Lauritsen JPH, Kastrup J, Christensen MD, von Bulow F, Palmer E, Geisler C. The phosphorylation state of CD3y influences T cell responsiveness and controls T cell receptor cycling. J Biol Chem 1998;273:24232-24238.
54. Finke JH, Zea AH, Stanley J, Longo DL, Mizoguchi H, Tubbs RR, Wiltrout RH, O'Shea JJ, Kudoh S, Klein E. Loss of T-cell receptor ζ chain and p561ck in T-cells infiltrating human renal cell carcinoma. Cancer Res 1993;53:5613-5616.
55. Ishigami S, Natsugoe S, Tokuda K, Nakajo A, Higashi H, Iwashige H, Aridome K, Hokita S, Aikou T. CD3-ζ chain expression of intraturnoral lymphocytes is closely related to survival in gastric carcinoma patients. Cancer 2002;94:1437-1442.
56. Zea AH, Ochoa MT, Ghosh P, Longo DL, Alvord WG, Valderrama L, Falabella R, Harvey LK, Saravia N, Moreno LH, Ochoa AC. Changes in expression of signal transduction proteins in T lymphocytes of patients with leprosy. Infect Immun 1998;66:499-504.
57. Liossis SN, Ding XZ, Dennis GJ, Tsokos GC. Altered pattern of TCR/ CD3-mediated protein-tyrosyl phosphorylation in T cells from patients with systemic lupus erythematosus. Deficient expression of the T cell receptor ζ chain. J Clin Invest 1998;101:1448-1457.
58. Tsuzaka K, Fukuhara I, Setoyama Y, Yoshimoto K, Suzuki K, Abe T, Takeuchi T. TCRζ mRNA with an alternatively spliced 3'-untranslated region detected in systemic lupus erythematosus patients leads to the down-regulation of TCRζ and TCR/CD3 complex. J Immunol 2003;171: 2496-2503.