Tonic ubiquitylation controls T-cell receptor: CD3 complex expression during T-cell development

EMBO Journal

Volumn 29, Issue 7, 2010, Pages 1285-1298

  Wang, Haopeng ^a,b,h   Holst, Jeff ^a,i   Woo, Seng Ryong ^a   Guy, Cliff ^a   Bettini, Matt ^a   Wang, Yao ^a   Shafer, Aaron ^a   Naramura, Mayumi ^c   Mingueneau, Michaël ^d,k   Dragone, Leonard L ^e   Hayes, Sandra M ^f   Malissen, Bernard ^d   Band, Hamid ^c,g   Vignali, Dario A A ^a,b,j  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^d CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^e CHILDREN S HOSPITAL   (United States)

^f State University of New York Upstate Medical University: College of Medicine   (United States)

^g UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ UNIVERSITY OF SYDNEY   (Australia)

^j Children's GMP LLC   (United States)

^k HARVARD MEDICAL SCHOOL   (United States)

more..

Author keywords

C Cbl; Signalling; T cell development; T cell receptor:CD3; Ubiquitylation

Indexed keywords

AMMONIUM CHLORIDE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CONCANAVALIN A; DYNAMIN; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; MONOCLONAL ANTIBODY; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; UBIQUITIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; COMPLEX FORMATION; CONTROLLED STUDY; FLOW CYTOMETRY; INTERNALIZATION; LYSOSOME; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SPLEEN CELL; T LYMPHOCYTE; THYMOCYTE; UBIQUITINATION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; DYNAMINS; GENE EXPRESSION REGULATION; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); LYSINE; LYSOSOMES; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; ORGAN CULTURE TECHNIQUES; PROTO-ONCOGENE PROTEINS C-CBL; RECEPTOR-CD3 COMPLEX, ANTIGEN, T-CELL; T-LYMPHOCYTES; UBIQUITINATION;

EID: 77950532705     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.10     Document Type: Article

References (65)

1. Aguado E, Richelme S, Nunez-Cruz S, Miazek A, Mura AM, Richelme M, Guo XJ, Sainty D, He HT, Malissen B, Malissen M (2002) Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science 296: 2036-2040 (Pubitemid 34627528)
2. Aivazian D, Stern LJ (2000) Phosphorylation of Tcell receptor zeta is regulated by a lipid dependent folding transition. Nat Struct Biol 7: 1023-1026
3. Bluestone JA, Pardoll D, Sharrow SO, Fowlkes BJ (1987) Characterization of murine thymocytes with CD3-associated T-cell receptor structures. Nature 326: 82-84 (Pubitemid 17059408)
4. Brodeur JF, Li S, Martins MS, Larose L, Dave VP (2009) Critical and multiple roles for the CD3epsilon intracytoplasmic tail in double negative to double positive thymocyte differentiation. J Immunol 182: 4844-4853
5. Cadwell K, Coscoy L (2005) Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309: 127-130 (Pubitemid 40934990)
6. Cenciarelli C, Hou D, Hsu KC, Rellahan BL, Wiest DL, Smith HT, Fried VA, Weissman AM (1992) Activation-induced ubiquitina-tion of the T cell antigen receptor. Science 257: 795-797
7. Clevers H, Alarcon B, Wileman T, Terhorst C (1988) The T cell receptor/CD3 complex: a dynamic protein ensemble. Annu Rev Immunol 6: 629-662 (Pubitemid 19141599)
8. Daniels MA, Teixeiro E, Gill J, Hausmann B, Roubaty D, Holmberg K, Werlen G, Hollander GA, Gascoigne NR, Palmer E (2006) Thymic selection threshold defined by compartmentalization of Ras/MAPK signalling. Nature 444: 724-729 (Pubitemid 44949596)
9. Ebert PJ, Ehrlich LI, Davis MM (2008) Low ligand requirement for deletion and lack of synapses in positive selection enforce the gauntlet of thymic T cell maturation. Immunity 29: 734-745
10. Fujimuro M, Yokosawa H (2005) Production of antipolyubiquitin monoclonal antibodies and their use for characterization and isolation of polyubiquitinated proteins. Methods Enzymol 399: 75-86 (Pubitemid 41772723)
11. Gil D, Schamel WW, Montoya M, Sanchez-Madrid F, Alarcon B (2002) Recruitment of Nck by CD3 epsilon reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell 109: 901-912 (Pubitemid 34786004)
12. Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82: 373-428 (Pubitemid 34654457)
13. Goldberg AL (2003) Protein degradation and protection against misfolded or damaged proteins. Nature 426: 895-899
14. Haglund K, Di Fiore PP, Dikic I (2003a) Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem Sci 28: 598-603 (Pubitemid 38352806)
15. Haglund K, Sigismund S, Polo S, Szymkiewicz I, Di Fiore PP, Dikic I (2003b) Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 5: 461-466 (Pubitemid 36592270)
16. Hailman E, Burack WR, Shaw AS, Dustin ML, Allen PM (2002) Immature CD4(+)CD8(+) thymocytes form a multifocal immu-nological synapse with sustained tyrosine phosphorylation. Immunity 16: 839-848 (Pubitemid 34786482)
17. Hochstrasser M (2006) Lingering mysteries of ubiquitin-chain a ssembly. Cell 124: 27-34
18. Holst J, Szymczak-Workman AL, Vignali KM, Burton AR, Workman CJ, Vignali DA (2006a) Generation of T-cell receptor retrogenic mice. Nat Protoc 1: 406-417
19. Holst J, Vignali KM, Burton AR, Vignali DA (2006b) Rapid analysis of T-cell selection in vivo using T cell-receptor retrogenic mice. Nat Methods 3: 191-197
20. Holst J, Wang H, Eder KD, Workman CJ, Boyd KL, Baquet Z, Singh H, Forbes K, Chruscinski A, Smeyne R, van Oers NS, Utz PJ, Vignali DA (2008) Scalable signaling mediated by T cell antigen receptor-CD3 ITAMs ensures effective negative selection and prevents autoimmunity. Nat Immunol 9: 658-666 (Pubitemid 351712636)
21. Hou D, Cenciarelli C, Jensen JP, Nguygen HB, Weissman AM (1994) Activation-dependent ubiquitination of a T cell antigen receptor subunit on multiple intracellular lysines. J Biol Chem 269: 14244-14247 (Pubitemid 24191185)
22. Jameson SC, Hogquist KA, Bevan MJ (1995) Positive selection of thymocytes. Annu Rev Immunol 13: 93-126
23. Kearse KP, Roberts JL, Munitz TI, Wiest DL, Nakayama T, Singer A (1994) Developmental regulation of alpha beta T cell antigen receptor expression results from differential stability of nascent TCR alpha proteins within the endoplasmic reticulum of immature and mature T cells. EMBO J 13: 4504-4514 (Pubitemid 2137419)
24. Kearse KP, Takahama Y, Punt JA, Sharrow SO, Singer A (1995) Early molecular events induced by T cell receptor (TCR) signaling in immature CD4+ CD8+ thymocytes: increased synthesis of TCR-alpha protein is an early response to TCR signaling that compensates for TCR-alpha instability, improves TCR assembly, and parallels other indicators of positive selection. J Exp Med 181: 193-202
25. Klausner RD, Lippincott-Schwartz J, Bonifacino JS (1990) The Tcell antigen receptor: insights into organelle biology. Annu Rev Cell Biol 6: 403-431
26. Kosugi A, Weissman AM, Ogata M, Hamaoka T, Fujiwara H (1992) Instability of assembled T-cell receptor complex that is associated with rapid degradation of zeta chains in immature CD4+CD8+ thymocytes. Proc Natl Acad Sci USA 89: 9494-9498
27. Lacorazza HD, Nikolich-Zugich J (2004) Exclusion and inclusion of TCR alpha proteins during T cell development in TCR-transgenic and normal mice. J Immunol 173: 5591-5600 (Pubitemid 39392146)
28. Li N, Wang Y, Forbes K, Vignali KM, Heale BS, Saftig P, Hartmann D, Black RA, Rossi JJ, Blobel CP, Dempsey PJ, Workman CJ, Vignali DA (2007a) Metalloproteases regulate T-cell proliferation and effector function via LAG-3. EMBO J 26: 494-504 (Pubitemid 46160949)
29. Li QJ, Chau J, Ebert PJ, Sylvester G, Min H, Liu G, Braich R, Manoharan M, Soutschek J, Skare P, Klein LO, Davis MM, Chen CZ (2007b) miR-181a is an intrinsic modulator of Tcell sensitivity and selection. Cell 129: 147-161 (Pubitemid 46507589)
30. Liu HY, Rhodes M, Wiest DL, Vignali DAA (2000) On the dynamics of TCR:CD3 complex cell surface expression and downmodula-tion. Immunity 13: 665-675
31. Maguire JE, McCarthy SA, Singer A, Singer DS (1990) Inverse correlation between steady-state RNA and cell surface T cell receptor levels. FASEB J 4: 3131-3134 (Pubitemid 20385511)
32. Marmor MD, Yarden Y (2004) Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23: 2057-2070 (Pubitemid 38496735)
33. Mingueneau M, Sansoni A, Gregoire C, Roncagalli R, Aguado E, Weiss A, Malissen M, Malissen B (2008) The proline-rich sequence of CD3epsilon controls T cell antigen receptor expression on and signaling potency in preselection CD4+CD8+ thymocytes. Nat Immunol 9: 522-532 (Pubitemid 351560521)
34. Molero JC, Jensen TE, Withers PC, Couzens M, Herzog H, Thien CB, Langdon WY, Walder K, Murphy MA, Bowtell DD, James DE, Cooney GJ (2004) c-Cbl-deficient mice have reduced adiposity, higher energy expenditure, and improved peripheral insulin action. J Clin Invest 114: 1326-1333 (Pubitemid 40385304)
35. Molina TJ, Kishihara K, Siderovski DP, van EW, Narendran A, Timms E, Wakeham A, Paige CJ, Hartmann KU, Veillette A (1992) Profound block in thymocyte development in mice lacking p56lck. Nature 357: 161-164
36. Mukhopadhyay D, Riezman H (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315: 201-205 (Pubitemid 46166358)
37. Murphy MA, Schnall RG, Venter DJ, Barnett L, Bertoncello I, Thien CB, Langdon WY, Bowtell DD (1998) Tissue hyperplasia and enhanced T-cell signalling via ZAP-70 in c-Cbl-deficient mice. Mol Cell Biol 18: 4872-4882 (Pubitemid 28343071)
38. Myers MD, Sosinowski T, Dragone LL, White C, Band H, Gu H, Weiss A (2006) Src-like adaptor protein regulates TCR expression on thymocytes by linking the ubiquitin ligase c-Cbl to the TCR complex. Nat Immunol 7: 57-66 (Pubitemid 41823869)
39. Nakayama T, Singer A, Hsi ED, Samelson LE (1989) Intrathymic signalling in immature CD4+CD8+ thymocytes results in tyro-sine phosphorylation of the T-cell receptor zeta chain. Nature 341: 651-654 (Pubitemid 19257315)
40. Naramura M, Jang IK, Kole H, Huang F, Haines D, Gu H (2002) c-Cbl and Cbl-b regulate T cell responsiveness by promoting ligand-induced TCR down-modulation. Nat Immunol 3: 1192-1199 (Pubitemid 35469704)
41. Naramura M, Kole HK, Hu RJ, Gu H (1998) Altered thymic positive selection and intracellular signals in Cbl-deficient mice. Proc Natl Acad Sci USA 95: 15547-15552 (Pubitemid 29018736)
42. Ouchida R, Yamasaki S, Hikida M, Masuda K, Kawamura K, Wada A, Mochizuki S, Tagawa M, Sakamoto A, Hatano M, Tokuhisa T, Koseki H, Saito T, Kurosaki T, Wang JY (2008) A lysosomal protein negatively regulates surface T cell antigen receptor expression by promoting CD3zeta-chain degradation. Immunity 29: 33-43
43. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, Marsischky G, Roelofs J, Finley D, Gygi SP (2003) A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 21: 921-926 (Pubitemid 36936199)
44. Praefcke GJ, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5: 133-147
45. Rao N, Miyake S, Reddi AL, Douillard P, Ghosh AK, Dodge IL, Zhou P, Fernandes ND, Band H (2002) Negative regulation of Lck by Cbl ubiquitin ligase. Proc Natl Acad Sci USA 99: 3794-3799 (Pubitemid 34252185)
46. Richie LI, Ebert PJ, Wu LC, Krummel MF, Owen JJ, Davis MM (2002) Imaging synapse formation during thymocyte selection: inability of CD3zeta to form a stable central accumulation during negative selection. Immunity 16: 595-606
47. Shih SC, Sloper-Mould KE, Hicke L (2000) Monoubiquitin carries a novel internalization signal that is appended to activated receptors. EMBO J 19: 187-198 (Pubitemid 30042701)
48. Sigalov AB, Aivazian DA, Uversky VN, Stern LJ (2006) Lipid-binding activity of intrinsically unstructured cytoplasmic domains of multichain immune recognition receptor signaling sub-units. Biochem 45: 15731-15739
49. Sommers CL, Park CS, Lee J, Feng C, Fuller CL, Grinberg A, Hildebrand JA, Lacana E, Menon RK, Shores EW, Samelson LE, Love PE (2002) A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science 296: 2040-2043 (Pubitemid 34627529)
50. Sosinowski T, Killeen N, Weiss A (2001) The Src-like adaptor protein downregulates the T cell receptor on CD4+CD8+ thy-mocytes and regulates positive selection. Immunity 15: 457-466 (Pubitemid 32907392)
51. Szymczak A, Vignali DAA (2005) Plasticity and rigidity in AP-2-mediated internalization of the T cell receptor:CD3 complex. J Immunol 174: 4153-4160 (Pubitemid 40395993)
52. Szymczak AL, Workman CJ, Gil D, Dilioglou S, Vignali KM, Palmer E, Vignali DA (2005) The CD3epsilon proline-rich sequence, and its interaction with Nck, is not required for T cell development and function. J Immunol 175: 270-275 (Pubitemid 40884328)
53. Szymczak AL, Workman CJ, Wang Y, Vignali KM, Dilioglou S, Vanin EF, Vignali DA (2004) Correction of multi-gene deficiency in vivo using a single 'self-cleaving' 2A peptide-based retroviral vector. Nat Biotechnol 22: 589-594 (Pubitemid 38585911)
54. Tailor P, Tsai S, Shameli A, Serra P, Wang J, Robbins S, Nagata M, Szymczak-Workman AL, Vignali DA, Santamaria P (2008) The proline-rich sequence of CD3epsilon as an amplifier of low-avidity TCR signaling. J Immunol 181: 243-255
55. Tang J, Sawasdikosol S, Chang JH, Burakoff SJ (1999) SLAP, a dimeric adapter protein, plays a functional role in T cell receptor signaling. Proc Natl Acad Sci USA 96: 9775-9780 (Pubitemid 29398808)
56. Tarakhovsky A, Kanner SB, Hombach J, Ledbetter JA, Muller W, Killeen N, Rajewsky K (1995) A role for CD5 in TCR-mediated signal transduction and thymocyte selection. Science 269: 535-537
57. Thien CB, Langdon WY (2001) Cbl: many adaptations to regulate protein tyrosine kinases. Nat Rev Mol Cell Biol 2: 294-307
58. Thien CB, Scaife RM, Papadimitriou JM, Murphy MA, Bowtell DD, Langdon WY (2003) A mouse with a loss-of-function mutation in the c-Cbl TKB domain shows perturbed thymocyte signaling without enhancing the activity of the ZAP-70 tyrosine kinase. J Exp Med 197: 503-513
59. Valujskikh A, Lantz O, Celli S, Matzinger P, Heeger PS (2002) Cross-primed CD8(+) T cells mediate graft rejection via a distinct effector pathway. Nat Immunol 3: 844-851
60. Wang B, Wang N, Whitehurst CE, She J, Chen J, Terhorst C (1999) T lymphocyte development in the absence of CD3 epsilon or CD3 gamma delta epsilon zeta. J Immunol 162: 88-94
61. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, Chen ZJ (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412: 346-351 (Pubitemid 32694385)
62. Wang H, Matsuzawa A, Brown SA, Zhou J, Guy CS, Tseng PH, Forbes K, Nicholson TP, Sheppard PW, Hacker H, Karin M, Vignali DA (2008) Analysis of nondegradative protein ubiquityla-tion with a monoclonal antibody specific for lysine-63-linked polyubiquitin. Proc Natl Acad Sci USA 105: 20197-20202
63. Wang Y, Becker D, Vass T, White J, Marrack P, Kappler JW (2009) A conserved CXXC motif in CD3epsilon is critical for T cell development and TCR signaling. PLoS Biol 7: e1000253
64. Xu C, Gagnon E, Call ME, Schnell JR, Schwieters CD, Carman CV, Chou JJ, Wucherpfennig KW (2008) Regulation of T cell receptor activation by dynamic membrane binding of the CD3epsilon cytoplasmic tyrosine-based motif. Cell 135: 702-713
65. Xu P, Peng J (2008) Characterization of polyubiquitin chain structure by middle-down mass spectrometry. Anal Chem 80: 3438-3444 (Pubitemid 351620732)