Cytolytic T lymphocyte-associated antigen-4 and the TCRζ/CD3 complex, but not CD28, interact with clathrin adaptor complexes AP-1 and AP-2

Journal of Immunology

Volumn 163, Issue 4, 1999, Pages 1868-1879

  Schneider, Helga ^a,c   Martin, Margarita ^a,c   Agarraberes, Fernando A ^b   Yin, Li ^a,c   Rapoport, Iris ^c   Kirchhausen, Tomas ^c   Rudd, Christopher E ^a,c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b TUFTS UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CD28 ANTIGEN; CD3 ANTIGEN; CLATHRIN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR AP 2;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GOLGI COMPLEX; HUMAN; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ADAPTOR PROTEIN COMPLEX ALPHA SUBUNITS; ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD; ANTIGENS, CD28; ANTIGENS, DIFFERENTIATION; BINDING SITES; CALCIUM; CLATHRIN; HUMANS; HYBRIDOMAS; IMMUNOCONJUGATES; INTRACELLULAR FLUID; LYSOSOMES; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; RECEPTOR-CD3 COMPLEX, ANTIGEN, T-CELL; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES, CYTOTOXIC;

EID: 0033567050     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Linsley, P. S. 1995. Distinct roles for CD28 and cytotoxic T lymphocyte-associated molecule 4 receptor during T-cell activation. J. Exp. Med. 182:289.
2. Thompson, C. B. 1995. Distinct roles for the costimulatory ligands B7-1 and B7-2 in T helper cell differentiation? Cell 81:979.
3. Bluestone, J. 1995. New perspectives of CD28-B7 mediated T cell costimulation. Immunity 2:555.
4. Brunet, J. F., F. Denizot, M.-F. Luciani, M. Roux-Dosseto, M.-F. Suzan, M.-G. Mattei, and P. Golstein. 1987. A new member of the immunoglobulin superfamily-CTLA-4. Nature 328:267.
5. Lindsten, T., K. P. Lee, E. S. Harris, B. Petryniak, N. Craighead, P. J. Reynolds, D. B. Lombard, G. J. Freeman, L. M. Nadler, G. S. Gray, et al. 1993. Characterization of CTLA-4 structure and expression on human T cells. J. Immunol. 151:3489.
6. Schwartz, R. H. 1992. Costimulation of T lymphocytes: the role of CD28, CTLA-4, and B7/BB1 in interleukin-2 production and immunotherapy. Cell 71: 1065.
7. Jenkins, M. K. 1994. The ups and downs of T cell costimulation. Immunity 1:443.
8. Thompson, C. B., and J. P. Allison. 1997. The emerging role of CTLA-4 as an immune attenuator. Immunity 7:445.
9. Walunas, T. L., D. J. Lenschow, C. Y. Bakker, P. S. Linsley, G. J. Freeman, J. M. Green, C. B. Thompson, and J. A. Bluestone. 1994. CTLA-4 can function as a negative regulator of T cell activation. Immunity 1:405.
10. Krummel, M. F., and J. P. Allison. 1995. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J. Exp. Med. 182:459.
11. Waterhouse, P., J. M. Penninger, E. Timms, A. Wakeham, A. Shahinian, K. P. Lee, C. B. Thompson, H. Griesser, and T. W. Mak. 1995. Lymphoproliferative disorders with early lethality in mice deficient in CTLA-4. Science 270: 985.
12. Tivol, E. A., F. Borriello, A. N. Schweitzer, W. P. Lynch, J. A. Bluestone, and A. H. Sharpe. 1995. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3:541.
13. Marengere, L. E. M., P. Waterhouse, G. S. Duncan, H.-W. Mittrucker, G.-S. Feng, and T. W. Mak. 1996. Regulation of T cell receptor signaling by tyrosine phosphatase Syp association with CTLA-4. Science 272:1170.
14. Lee, K. M., E. Chuang, M. Griffin, R. Khattri, D. K. Hong, W. Zhang, D. Straus, L. E. Samelson, C. B. Thompson, and J. A. Bluestone. 1998. Molecular basis of T cell inactivation by CTLA-4. Science 282:2263.
15. Lin, H., J. C. Rathmell, G. S. Gray, C. B. Thompson, J. M. Leiden, and M.-L. Alegre. 1998. Cytotoxic T lymphocyte antigen 4 (CTLA4) blockade accelerates the acute rejection of cardiac allografts in CD28-deficient mice: CTLA4 can function independently of CD28. J. Exp. Med 188:199.
16. Fallarino, F., P. E. Fields, and T. F. Gajewski. 1998. B7-1 engagement of cytotoxic T lymphocyte antigen 4 inhibits T cell activation in the absence of CD28. J. Exp. Med. 188:205.
17. Krummel, M. F., and J. P. Allison. 1996. CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J. Exp. Med. 183:2533.
18. Tivol, E. A., S. D. Boyd, S. McKeon, F. Borriello, P. Nickerson, T. B. Strom, and A. H. Sharpe. 1997. CTLA4Ig prevents lymphoproliferation and fatal tissue destruction in CTLA-4 deficient mice. J. Immunol. 158:5091.
19. Leung, H. T., J. Bradshaw, J. S. Cleaveland, and P. S. Linsley. 1995. Cytotoxic T lymphocyte-associated molecule-4, a high avidity receptor for CD80 and CD86, contains an intracellular localization motif in its cytoplasmic tail. J. Biol. Chem. 270:25107.
20. Alegre, M.-L., P. J. Noel, B. J. Eisfelder, E. Chuang, M. R. Clark, S. L. Reiner, and C. B. Thompson. 1996. Regulation of surface and intracellular expression of CTLA4 on mouse T cells. J. Immunol. 157:4762.
21. Linsley, P. S., J. Bradshaw, J. Greene, R. Peach, K. L. Bennet, and R. S. Mittler. 1996. Intracellular trafficking of CTLA-4 and focal localization towards sites of TCR engagement. Immunity 4:535.
22. Kirchhausen, T., J. S. Bonifacino, and H. Riezman. 1997. Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr. Opin. Cell Biol. 9:488.
23. Hirst, J., and M. Robinson. 1998. Clathrin and adaptors. Biochim. Biophys. Acta 1404:173.
24. Pearse, B. M., and M. S. Robinson. 1990. Clathrin, adaptors, and sorting. Annu. Rev. Cell Biol. 6:151.
25. Robinson, M. S. 1992. Adaptins. Trends Cell Biol. 2:293.
26. Kirchhausen, T. 1993. Coated pits and coated vesicles: sorting it all out. Curr. Opin. Struct. Biol. 3:182.
27. Cowles, C. R., G. Odorizzi, G. S. Payne, and S. D. Emr. 1997. The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91: 109.
28. Panek, H. R., J. D. Stepp, H. M. Engle, K. M. Marks, P. K. Tan, S. K. Lemmon, and L. C. Robinson. 1997. Suppressors of YCK-encoded yeast casein kinase I deficiency define the four subunits of a novel clathrin AP-like complex. EMBO J. 16:4194.
29. Dell'Angelica, E. C., C. E. Ooi, and J. S. Bonifacino. 1997. Beta3A-adaptin, a subunit of the adaptor-like complex AP-3. J. Biol. Chem. 272:15078.
30. Ahle, S., A. Mann, U. Eichelsbacher, and E. Ungewickell. 1988. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J. 7:919.
31. Virshup, D. M., and V. Bennett. 1988. Clathrin-coated vesicle assembly polypeptides: physical properties and reconstruction studies with brain membranes. J. Cell Biol. 106:39.
32. Matsui, W., and T. Kirchhausen. 1999. Stabilization of clathrin coats by the core of the clathrin-associated protein complex AP-2. Biochemistry 29:10791.
33. Traub, L. M., S. Kornfeld, and E. Ungewickell. 1995. Different domains of the AP-1 adaptor complex are required for Golgi membrane binding and clathrin recruitment. J. Biol. Chem. 270:4933.
34. Gallusser, A., and T. Kirchhausen. 1993. The β1 and β2 subunits of the AP complexes are the clathrin coat assembly components. EMBO J. 12:5237.
35. Stamnes, M. A., and J. E. Rothman. 1993. The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein. Cell 73:999.
36. Zhu, Y., L. M. Traub, and S. Kornfeld. 1998. ADP-ribosylation factor 1 transiently activates high-affinity adaptor protein complex AP-1 binding sites on Golgi membranes. Mol. Biol. Cell 9:1323.
37. Traub, L. M., J. A. Ostrom, and S. Kornfeld. 1993. Biochemical dissection of AP-1 recruitment onto the Golgi membranes. J. Cell Biol. 123:561.
38. Shih, W., A. Gallusser, and T. Kirchhausen. 1995. A clathrin-binding site in the hinge of the β2 chain of mammalian AP-2 complexes. J. Biol. Chem. 270:31083.
39. Ohno, H., J. Stewart, M.-C. Fournier, H. Bosshart, I. Rhee, S. Miyatake, T. Saito, A. Gallusser, T. Kirchhausen, and J. S. Bonifacino. 1995. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269:1872.
40. Boll, W., A. Gallusser, and T. Kirchhausen. 1995. Role of the regulatory domain of the EGF-receptor cytoplasmic tail in selective binding of the clathrin-associated complex AP-2. Curr. Biol. 5:1168.
41. Trowbridge, I. S., J. F. Collawn, and C. R. Hopkins. 1993. Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol. 9:129.
42. Rapoport, I., M. Miyazaki, W. Boll, B. Duckworth, L. C. Cantley, S. Shoelson, and T. Kirchhausen. 1997. Regulatory interactions in the recognition of endocytic sorting signals by AP-2 complexes. EMBO J. 16:2240.
43. Shiratori, T., S. Miyatake, H. Ohno, C. Nakaseko, K. Isono, J. S. Bonifacino, and T. Saito. 1997. Tyrosine phosphorylation controls internalization of CTLA-4 by regulating its interaction with clathrin-associated adaptor complex AP-2. Immunity 6:583.
44. Chuang, E., M.-L. Alegre, C. S. Duckett, P. J. Noel, M. G. Vander Heiden, and C. B. Thompson. 1997. Interaction of CTLA-4 with the clathrin-associated protein AP50 results in ligand-independent endocytosis that limits cell surface expression. J. Immunol. 159:144.
45. Zhang, Y., and J. P. Allison. 1997. Interaction of CTLA-4 with AP-50, a clathrin-coated pit adaptor protein. Proc. Natl. Acad. Sci. USA 94:9273.
46. Bradshaw, J. D., P. Lu, G. Leytze, J. Rodgers, G. L. Schieven, K. L. Bennett, P. S. Linsley, and S. E. Kurtz. 1997. Interaction of the cytoplasmic tail of CTLA-4 (CD152) with a clathrin-associated protein is negatively regulated by tyrosine phosphorylation. Biochemistry 36:15975.
47. Linsley, P. S., J. A. L. Greene, P. Tan, J. Bradshaw, J. A. Ledbetter, C. Anasettei, and N. K. Damle. 1992. Compression and functional cooperation of CTLA-4 and CD28 on activated T lymphocytes. J. Exp. Med. 176:1595.
48. Takebe, Y., M. Seiki, J.-I. Fujisawa, P. Hoy, K.-I. Arai, M. Yoshida, and N. Arai. 1988. SRα promoter: an efficient and versatile mammalian cDNA expression system composed of the simian virus 40 early promoter and the R-U5 segment of human T cell leukemia virus type 1 long terminal repeat. Mol. Cell. Biol. 8:466.
49. Cefai, D., Y.-C. Cai, H. Hu, and C. E. Rudd. 1996. CD28 costimulatory regimes differ in their dependence on PI-3 kinase: common cosignals induced by CD80 and CD86. Int. Immunol. 8:1609.
50. Storrie, B., and E. A. Madden. 1990. Isolation of subcellular organelles. Methods Enzymol. 182:203.
51. Ohsumi, Y., T. Ishikawa, and K. Kato. 1983. A rapid and simplified method for the preparation of lysosomal membranes from rat liver. J. Biochem. 13:547.
52. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Rondall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265.
53. Rapoport, I., Y. C. Chen, P. Cupers, S. E. Shoelson, and T. Kirchhausen. 1998. Dileucine-based sorting signals bind to the β chain of AP-1 at a site distinct and regulated differently from the tyrosine-based motif-binding site. EMBO J. 17: 2148.
54. Cai, Y.-C., D. Cefai, H. Schneider, M. Raab, N. Nabavi, and C. E. Rudd. 1995. Selective CD28pYMNM mutations implicate phosphatidylinositol 3-kinase in CD86-CD28-mediated costimulation. Immunity 3:417.
55. Johnson, K. F., and S. Kornfeld. 1992a. The cytoplasmic tail of the mannose 6-phosphate/insulin-like growth factor-II receptor has 2 signals for lysosomal enzyme sorting in the Golgi. J. Cell Biol. 119:249.
56. LeBorgne, R., G. Griffiths, and B. Holflack. 1996. Mannose 6-phosphate receptors and ADP-ribosylation factors cooperate for high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J. Biol. Chem. 271:2162.
57. Prasad, K. V. S., Y.-C. Cai, M. Raab, B. Duckworth, L. Cantley, S. E. Shoelson, and C. E. Rudd. 1994. T-cell antigen CD28 interacts with the lipid kinase phosphatidylinositol 3-kinase by a cytoplasmic Tyr(P)-Met-Xaa-Met motif. Proc. Natl. Acad. Sci. USA 91:2834.
58. Schneider, H., K. V. S. Prasad, S. E. Shoelson, and C. E. Rudd. 1995. CTLA-4 binding to the lipid kinase phosphatidylinositol 3-kinase in T cells. J. Exp. Med. 181:351.
59. Glickman, J. A., E. Conibear, and B. M. F. Pearse. 1989. Specificity of binding of clathrin adaptors to signals on the mannose-6-phosphate/insulin like growth factor II receptor. EMBO J. 8:1041.
60. Johnson, K. F., and S. Kornfeld. 1992. A His-Leu-Leu sequence near the carboxyl terminus of the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor is necessary for the lysosomal enzyme sorting function. J. Biol. Chem. 267:17110.
61. Chen, H. J., J. Remmler, J. C. Delaney, D. J. Messner, and P. Lobel. 1993. Mutational analysis of the cation-independent mannose-6-phosphate insulin-like growth factor II receptor: a consensus casein kinase II site followed by 2 leucines near the carboxyl terminus is important for intracellular targeting of lysosomal enzymes. J. Biol. Chem. 268:22338.
62. Sosa, M. A., B. Schmidt, K. von Figura, and A. Hille-Rehfeld. 1993. In vitro binding of plasma membrane-coated vesicle adaptors to the cytoplasmic domain of lysosomal acid phosphatase. J. Biol. Chem. 268:12537.
63. Chiang, H.-L., and J. F. Dice. 1988. Peptide sequences that target proteins for enhanced degradation during serum withdrawal. J. Biol. Chem. 263:6797.
64. D'Oro, U., M. S. Vacchio, A. M. Weissman, and J. D. Ashwell. 1997. Activation of the lck tyrosine kinase targets cell surface T cell antigen receptors for lysosomal degradation. Immunity 7:619.
65. Harris, V. K., E. D. E. Liaudet-Coopman, B. J. Boyle, A. Wellstein, and A. T. Riegel. 1998. Phorbol-ester-induced transcription of a fibroblast growth factor-binding protein is modulated by a complex interplay of positive and negative regulatory promoter elements. J. Biol. Chem. 273:19130.
66. Sorkin, A., T. McKinsey, W. Shih, and T. Kirchhausen. 1995. Stoichiometric interaction of the epidermal growth factor receptor with the clathrin-associated protein complex AP-2. J. Biol. Chem. 270:619.
67. Chuang, E., K.-M. Lee, M. D. Robbins, J. M. Duerr, M.-L. Alegre, J. E. Hambor, M. J. Neveu. J. A. Bluestone, and C. B. Thompson. 1999. Regulation of cytotoxic T lymphocyte-associated molecule-4 by Src kinases. J. Immunol. 162:1270.
68. Beck, K. A., and J. H. Keen. 1991b. Self-association of the plasma membrane-associated clathrin assembly protein AP-2. J. Biol. Chem. 266:4437.