T Cell Receptor Internalization from the Immunological Synapse Is Mediated by TC21 and RhoG GTPase-Dependent Phagocytosis

Immunity

Volumn 35, Issue 2, 2011, Pages 208-222

  Martínez Martín, Nuria ^a   Fernández Arenas, Elena ^a   Cemerski, Saso ^b   Delgado, Pilar ^a   Turner, Martin ^c   Heuser, John ^b   Irvine, Darrell J ^d   Huang, Bonnie ^d   Bustelo, Xosé R ^e   Shaw, Andrey ^b   Alarcón, Balbino ^a  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BABRAHAM INSTITUTE   (United Kingdom)

^d USA   (United States)

^e UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PROTEIN RHOG; PROTEIN TC21; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CONTROLLED STUDY; ENZYME ANALYSIS; HUMAN; HUMAN CELL; IMMUNOLOGICAL SYNAPSE; INTERNALIZATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN TRANSPORT; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS; CELL COMMUNICATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNOLOGICAL SYNAPSES; JURKAT CELLS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MONOMERIC GTP-BINDING PROTEINS; PEPTIDE FRAGMENTS; PHAGOCYTOSIS; PROTEIN TRANSPORT; RECEPTORS, ANTIGEN, T-CELL; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 80051875965     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2011.06.003     Document Type: Article

References (58)

1. Ahmed K.A., Munegowda M.A., Xie Y., Xiang J. Intercellular trogocytosis plays an important role in modulation of immune responses. Cell. Mol. Immunol. 2008, 5:261-269.
2. Alcover A., Alarcón B. Internalization and intracellular fate of TCR-CD3 complexes. Crit. Rev. Immunol. 2000, 20:325-346.
3. André P., Boretto J., Hueber A.O., Régnier-Vigouroux A., Gorvel J.P., Ferrier P., Chavrier P. A dominant-negative mutant of the Rab5 GTPase enhances T cell signaling by interfering with TCR down-modulation in transgenic mice. J. Immunol. 1997, 159:5253-5263.
4. Arora S., Matta A., Shukla N.K., Deo S.V., Ralhan R. Identification of differentially expressed genes in oral squamous cell carcinoma. Mol. Carcinog. 2005, 42:97-108.
5. Balagopalan L., Barr V.A., Samelson L.E. Endocytic events in TCR signaling: Focus on adapters in microclusters. Immunol. Rev. 2009, 232:84-98.
6. Barda-Saad M., Braiman A., Titerence R., Bunnell S.C., Barr V.A., Samelson L.E. Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat. Immunol. 2005, 6:80-89.
7. Batista A., Millán J., Mittelbrunn M., Sánchez-Madrid F., Alonso M.A. Recruitment of transferrin receptor to immunological synapse in response to TCR engagement. J. Immunol. 2004, 172:6709-6714.
8. Cemerski S., Das J., Giurisato E., Markiewicz M.A., Allen P.M., Chakraborty A.K., Shaw A.S. The balance between T cell receptor signaling and degradation at the center of the immunological synapse is determined by antigen quality. Immunity 2008, 29:414-422.
9. Chan A.M., Miki T., Meyers K.A., Aaronson S.A. A human oncogene of the RAS superfamily unmasked by expression cDNA cloning. Proc. Natl. Acad. Sci. USA 1994, 91:7558-7562.
10. Clark G.J., Kinch M.S., Gilmer T.M., Burridge K., Der C.J. Overexpression of the Ras-related TC21/R-Ras2 protein may contribute to the development of human breast cancers. Oncogene 1996, 12:169-176.
11. Cox D., Greenberg S. Phagocytic signaling strategies: Fc(gamma)receptor-mediated phagocytosis as a model system. Semin. Immunol. 2001, 13:339-345.
12. Das V., Nal B., Dujeancourt A., Thoulouze M.I., Galli T., Roux P., Dautry-Varsat A., Alcover A. Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse; involvement of SNARE complexes. Immunity 2004, 20:577-588.
13. Daubeuf S., Puaux A.L., Joly E., Hudrisier D. A simple trogocytosis-based method to detect, quantify, characterize and purify antigen-specific live lymphocytes by flow cytometry, via their capture of membrane fragments from antigen-presenting cells. Nat. Protoc. 2006, 1:2536-2542.
14. Davis D.M. Intercellular transfer of cell-surface proteins is common and can affect many stages of an immune response. Nat. Rev. Immunol. 2007, 7:238-243.
15. deBakker C.D., Haney L.B., Kinchen J.M., Grimsley C., Lu M., Klingele D., Hsu P.K., Chou B.K., Cheng L.C., Blangy A., et al. Phagocytosis of apoptotic cells is regulated by a UNC-73/TRIO-MIG-2/RhoG signaling module and armadillo repeats of CED-12/ELMO. Curr. Biol. 2004, 14:2208-2216.
16. Delgado P., Cubelos B., Calleja E., Martínez-Martín N., Ciprés A., Mérida I., Bellas C., Bustelo X.R., Alarcón B. Essential function for the GTPase TC21 in homeostatic antigen receptor signaling. Nat. Immunol. 2009, 10:880-888.
17. Dietrich J., Hou X., Wegener A.M., Geisler C. CD3 gamma contains a phosphoserine-dependent di-leucine motif involved in down-regulation of the T cell receptor. EMBO J. 1994, 13:2156-2166.
18. Doh J., Irvine D.J. Immunological synapse arrays: Patterned protein surfaces that modulate immunological synapse structure formation in T cells. Proc. Natl. Acad. Sci. USA 2006, 103:5700-5705.
19. Dragone L.L., Shaw L.A., Myers M.D., Weiss A. SLAP, a regulator of immunoreceptor ubiquitination, signaling, and trafficking. Immunol. Rev. 2009, 232:218-228.
20. Fernández-Miguel G., Alarcón B., Iglesias A., Bluethmann H., Alvarez-Mon M., Sanz E., de la Hera A. Multivalent structure of an alphabetaT cell receptor. Proc. Natl. Acad. Sci. USA 1999, 96:1547-1552.
21. Fooksman D.R., Vardhana S., Vasiliver-Shamis G., Liese J., Blair D.A., Waite J., Sacristán C., Victora G.D., Zanin-Zhorov A., Dustin M.L. Functional anatomy of T cell activation and synapse formation. Annu. Rev. Immunol. 2010, 28:79-105.
22. Gerisch G., Ecke M., Schroth-Diez B., Gerwig S., Engel U., Maddera L., Clarke M. Self-organizing actin waves as planar phagocytic cup structures. Cell Adh Migr 2009, 3:373-382.
23. Glebov O.O., Nichols B.J. Lipid raft proteins have a random distribution during localized activation of the T-cell receptor. Nat. Cell Biol. 2004, 6:238-243.
24. Graham S.M., Cox A.D., Drivas G., Rush M.G., D'Eustachio P., Der C.J. Aberrant function of the Ras-related protein TC21/R-Ras2 triggers malignant transformation. Mol. Cell. Biol. 1994, 14:4108-4115.
25. Groves E., Dart A.E., Covarelli V., Caron E. Molecular mechanisms of phagocytic uptake in mammalian cells. Cell. Mol. Life Sci. 2008, 65:1957-1976.
26. Henson P.M. Engulfment: Ingestion and migration with Rac, Rho and TRIO. Curr. Biol. 2005, 15:R29-R30.
27. Hogquist K.A., Jameson S.C., Heath W.R., Howard J.L., Bevan M.J., Carbone F.R. T cell receptor antagonist peptides induce positive selection. Cell 1994, 76:17-27.
28. Huang J.F., Yang Y., Sepulveda H., Shi W., Hwang I., Peterson P.A., Jackson M.R., Sprent J., Cai Z. TCR-mediated internalization of peptide-MHC complexes acquired by T cells. Science 1999, 286:952-954.
29. Hwang I., Huang J.F., Kishimoto H., Brunmark A., Peterson P.A., Jackson M.R., Surh C.D., Cai Z., Sprent J. T cells can use either T cell receptor or CD28 receptors to absorb and internalize cell surface molecules derived from antigen-presenting cells. J. Exp. Med. 2000, 191:1137-1148.
30. Joly E., Hudrisier D. What is trogocytosis and what is its purpose?. Nat. Immunol. 2003, 4:815.
31. Kaye J., Hsu M.L., Sauron M.E., Jameson S.C., Gascoigne N.R., Hedrick S.M. Selective development of CD4+ T cells in transgenic mice expressing a class II MHC-restricted antigen receptor. Nature 1989, 341:746-749.
32. Lee K.H., Holdorf A.D., Dustin M.L., Chan A.C., Allen P.M., Shaw A.S. T cell receptor signaling precedes immunological synapse formation. Science 2002, 295:1539-1542.
33. Lee K.H., Dinner A.R., Tu C., Campi G., Raychaudhuri S., Varma R., Sims T.N., Burack W.R., Wu H., Wang J., et al. The immunological synapse balances T cell receptor signaling and degradation. Science 2003, 302:1218-1222.
34. Li Q., Lau A., Morris T.J., Guo L., Fordyce C.B., Stanley E.F. A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J. Neurosci. 2004, 24:4070-4081.
35. Monjas A., Alcover A., Alarcón B. Engaged and bystander T cell receptors are down-modulated by different endocytotic pathways. J. Biol. Chem. 2004, 279:55376-55384.
36. Monks C.R., Freiberg B.A., Kupfer H., Sciaky N., Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 1998, 395:82-86.
37. Murphy G.A., Graham S.M., Morita S., Reks S.E., Rogers-Graham K., Vojtek A., Kelley G.G., Der C.J. Involvement of phosphatidylinositol 3-kinase, but not RalGDS, in TC21/R-Ras2-mediated transformation. J. Biol. Chem. 2002, 277:9966-9975.
38. Niedergang F., Chavrier P. Regulation of phagocytosis by Rho GTPases. Curr. Top. Microbiol. Immunol. 2005, 291:43-60.
39. Niedergang F., Dautry-Varsat A., Alcover A. Peptide antigen or superantigen-induced down-regulation of TCRs involves both stimulated and unstimulated receptors. J. Immunol. 1997, 159:1703-1710.
40. Prieto-Sánchez R.M., Berenjeno I.M., Bustelo X.R. Involvement of the Rho/Rac family member RhoG in caveolar endocytosis. Oncogene 2006, 25:2961-2973.
41. Rodriguez-Viciana P., Sabatier C., McCormick F. Signaling specificity by Ras family GTPases is determined by the full spectrum of effectors they regulate. Mol. Cell. Biol. 2004, 24:4943-4954.
42. Rong R., He Q., Liu Y., Sheikh M.S., Huang Y. TC21 mediates transformation and cell survival via activation of phosphatidylinositol 3-kinase/Akt and NF-kappaB signaling pathway. Oncogene 2002, 21:1062-1070.
43. Rosário M., Paterson H.F., Marshall C.J. Activation of the Ral and phosphatidylinositol 3' kinase signaling pathways by the ras-related protein TC21. Mol. Cell. Biol. 2001, 21:3750-3762.
44. Saksena S., Sun J., Chu T., Emr S.D. ESCRTing proteins in the endocytic pathway. Trends Biochem. Sci. 2007, 32:561-573.
45. San José E., Borroto A., Niedergang F., Alcover A., Alarcón B. Triggering the TCR complex causes the downregulation of nonengaged receptors by a signal transduction-dependent mechanism. Immunity 2000, 12:161-170.
46. Seminario M.C., Bunnell S.C. Signal initiation in T-cell receptor microclusters. Immunol. Rev. 2008, 221:90-106.
47. Sharma R., Sud N., Chattopadhyay T.K., Ralhan R. TC21/R-Ras2 upregulation in esophageal tumorigenesis: Potential diagnostic implications. Oncology 2005, 69:10-18.
48. Singleton K., Parvaze N., Dama K.R., Chen K.S., Jennings P., Purtic B., Sjaastad M.D., Gilpin C., Davis M.M., Wülfing C. A large T cell invagination with CD2 enrichment resets receptor engagement in the immunological synapse. J. Immunol. 2006, 177:4402-4413.
49. Smyth L.A., Afzali B., Tsang J., Lombardi G., Lechler R.I. Intercellular transfer of MHC and immunological molecules: Molecular mechanisms and biological significance. Am. J. Transplant. 2007, 7:1442-1449.
50. Swanson J.A. Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 2008, 9:639-649.
51. Umeshappa C.S., Huang H., Xie Y., Wei Y., Mulligan S.J., Deng Y., Xiang J. CD4+ Th-APC with acquired peptide/MHC class I and II complexes stimulate type 1 helper CD4+ and central memory CD8+ T cell responses. J. Immunol. 2009, 182:193-206.
52. Vardhana S., Choudhuri K., Varma R., Dustin M.L. Essential role of ubiquitin and TSG101 protein in formation and function of the central supramolecular activation cluster. Immunity 2010, 32:531-540.
53. Vigorito E., Bell S., Hebeis B.J., Reynolds H., McAdam S., Emson P.C., McKenzie A., Turner M. Immunological function in mice lacking the Rac-related GTPase RhoG. Mol. Cell. Biol. 2004, 24:719-729.
54. von Essen M., Nielsen M.W., Bonefeld C.M., Boding L., Larsen J.M., Leitges M., Baier G., Odum N., Geisler C. Protein kinase C (PKC) alpha and PKC theta are the major PKC isotypes involved in TCR down-regulation. J. Immunol. 2006, 176:7502-7510.
55. Wetzel S.A., Parker D.C. MHC transfer from APC to T cells following antigen recognition. Crit. Rev. Immunol. 2006, 26:1-21.
56. Yeung T., Grinstein S. Lipid signaling and the modulation of surface charge during phagocytosis. Immunol. Rev. 2007, 219:17-36.
57. Yokosuka T., Saito T. The immunological synapse, TCR microclusters, and T cell activation. Curr. Top. Microbiol. Immunol. 2010, 340:81-107.
58. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2001, 2:107-117.