Trogocytosis results in sustained intracellular signaling in CD4 + T cells

Journal of Immunology

Volumn 189, Issue 10, 2012, Pages 4728-4739

  Osborne, Douglas G ^a   Wetzel, Scott A ^a,b  

^a UNIVERSITY OF MONTANA   (United States)

^b UNIVERSITY OF MONTANA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; CYTOCHROME C103; CYTOCHROME C88; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE ZAP 70; T LYMPHOCYTE RECEPTOR; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN DETECTION; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL PHAGOCYTOSIS; CELL SURFACE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; COVALENT BOND; ENZYME PHOSPHORYLATION; FIBROBLAST; FLOW CYTOMETRY; IMMUNE RESPONSE; INTRACELLULAR SIGNALING; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROSCOPY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TROGOCYTOSIS;

ANIMALS; ANTIGEN PRESENTATION; CD4-POSITIVE T-LYMPHOCYTES; FIBROBLASTS; HISTOCOMPATIBILITY ANTIGENS CLASS II; MAP KINASE SIGNALING SYSTEM; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; PYRIMIDINES; RECEPTORS, ANTIGEN, T-CELL; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 84868543217     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201507     Document Type: Article

References (84)

1. Hudrisier, D., J. Riond, H. Mazarguil, J. E. Gairin, and E. Joly. 2001. Cutting edge: CTLs rapidly capture membrane fragments from target cells in a TCR signaling-dependent manner. J. Immunol. 166: 3645-3649.
2. + T cells directly from the immu-nological synapse upon cellular dissociation. J. Immunol. 174: 80-89.
3. Joly, E., and D. Hudrisier. 2003. What is trogocytosis and what is its purpose? Nat. Immunol. 4: 815.
4. Hudson, L., J. Sprent, J. F. Miller, and J. H. Playfair. 1974. B cell-derived im-munoglobulin on activated mouse T lymphocytes. Nature 251: 60-62.
5. Lorber, M. I., M. R. Loken, A. M. Stall, and F. W. Fitch. 1982. I-A antigens on cloned alloreactive murine T lymphocytes are acquired passively. J. Immunol. 128: 2798-2803.
6. Nepom, J. T., B. Benacerraf, and R. N. Germain. 1981. Acquisition of syngeneic I-A determinants by T cells proliferating in response to poly (Glu60Ala30-Tyr10). J. Immunol. 127: 888-892.
7. Sharrow, S. O., B. J. Mathieson, and A. Singer. 1981. Cell surface appearance of unexpected host MHC determinants on thymocytes from radiation bone marrow chimeras. J. Immunol. 126: 1327-1335.
8. Mannie, M. D., S. K. Rendall, P. Y. Arnold, J. P. Nardella, and G. A. White. 1996. Anergy-associated T cell antigen presentation: a mechanism of infectious tolerance in experimental autoimmune encephalomyelitis. J. Immunol. 157: 1062-1070.
9. Arnold, P. Y., D. K. Davidian, and M. D. Mannie. 1997. Antigen presentation by T cells: T cell receptor ligation promotes antigen acquisition from professional antigen-presenting cells. Eur. J. Immunol. 27: 3198-3205.
10. + T cells. Eur. J. Immunol. 29: 1363-1373.
11. Patel, D. M., P. Y. Arnold, G. A. White, J. P. Nardella, and M. D. Mannie. 1999. Class II MHC/peptide complexes are released from APC and are acquired by T cell responders during specific antigen recognition. J. Immunol. 163: 5201-5210.
12. Patel, D. M., R. W. Dudek, and M. D. Mannie. 2001. Intercellular exchange of class II MHC complexes: ultrastructural localization and functional presentation of adsorbed I-A/peptide complexes. Cell. Immunol. 214: 21-34.
13. Patel, D. M., and M. D. Mannie. 2001. Intercellular exchange of class II major histocompatibility complex/peptide complexes is a conserved process that requires activation of T cells but is constitutive in other types of antigen presenting cell. Cell. Immunol. 214: 165-172.
14. Walker, M. R., and M. D. Mannie. 2002. Acquisition of functional MHC class II/peptide complexes by T cells during thymic development and CNS-directed pathogenesis. Cell. Immunol. 218: 13-25.
15. Huang, J. F., Y. Yang, H. Sepulveda, W. Shi, I. Hwang, P. A. Peterson, M. R. Jackson, J. Sprent, and Z. Cai. 1999. TCR-Mediated internalization of peptide-MHC complexes acquired by T cells. Science 286: 952-954.
16. Hwang, I., J. F. Huang, H. Kishimoto, A. Brunmark, P. A. Peterson, M. R. Jackson, C. D. Surh, Z. Cai, and J. Sprent. 2000. 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. 191: 1137-1148.
17. Hwang, I., and J. Sprent. 2001. Role of the actin cytoskeleton in T cell absorption and internalization of ligands from APC. J. Immunol. 166: 5099-5107.
18. Espinosa, E., J. Tabiasco, D. Hudrisier, and J. J. Fournié. 2002. Synaptic transfer by human gd T cells stimulated with soluble or cellular antigens. J. Immunol. 168: 6336-6343.
19. Hudrisier, D., and P. Bongrand. 2002. Intercellular transfer of antigen-presenting cell determinants onto T cells: molecular mechanisms and biological significance. FASEB J. 16: 477-486.
20. Hudrisier, D., J. Riond, L. Garidou, C. Duthoit, and E. Joly. 2005. T cell activation correlates with an increased proportion of antigen among the materials acquired from target cells. Eur. J. Immunol. 35: 2284-2294.
21. Hudrisier, D., A. Aucher, A. L. Puaux, C. Bordier, and E. Joly. 2007. Capture of target cell membrane components via trogocytosis is triggered by a selected set of surface molecules on T or B cells. J. Immunol. 178: 3637-3647.
22. + T cells. Scand. J. Immunol. 66: 441-450.
23. Aucher, A., E. Magdeleine, E. Joly, and D. Hudrisier. 2008. Capture of plasma membrane fragments from target cells by trogocytosis requires signaling in T cells but not in B cells. Blood 111: 5621-5628.
24. Daubeuf, S., A. Aucher, C. Bordier, A. Salles, L. Serre, G. Gaibelet, J. C. Faye, G. Favre, E. Joly, and D. Hudrisier. 2010. Preferential transfer of certain plasma membrane proteins onto T and B cells by trogocytosis. PLoS ONE 5: e8716.
25. Daubeuf, S., M. A. Lindorfer, R. P. Taylor, E. Joly, and D. Hudrisier. 2010. The direction of plasma membrane exchange between lymphocytes and accessory cells by trogocytosis is influenced by the nature of the accessory cell. J. Immunol. 184: 1897-1908.
26. Stinchcombe, J. C., G. Bossi, S. Booth, and G. M. Griffiths. 2001. The immu-nological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15: 751-761.
27. Monks, C. R., B. A. Freiberg, H. Kupfer, N. Sciaky, and A. Kupfer. 1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395: 82-86.
28. Grakoui, A., S. K. Bromley, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285: 221-227.
29. Thauland, T. J., Y. Koguchi, S. A. Wetzel, M. L. Dustin, and D. C. Parker. 2008. Th1 and Th2 cells form morphologically distinct immunological synapses. J. Immunol. 181: 393-399.
30. Kupfer, A., and S. J. Singer. 1989. Cell biology of cytotoxic and helper T cell functions: immunofluorescence microscopic studies of single cells and cell couples. Annu. Rev. Immunol. 7: 309-337.
31. Huse, M., B. F. Lillemeier, M. S. Kuhns, D. S. Chen, and M. M. Davis. 2006. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7: 247-255.
32. Lee, K. H., A. R. Dinner, C. Tu, G. Campi, S. Raychaudhuri, R. Varma, T. N. Sims, W. R. Burack, H. Wu, J. Wang, et al. 2003. The immunological synapse balances T cell receptor signaling and degradation. Science 302: 1218-1222.
33. Batista, F. D., and M. S. Neuberger. 2000. B cells extract and present immobilized antigen: implications for affinity discrimination. EMBO J. 19: 513-520.
34. Batista, F. D., D. Iber, and M. S. Neuberger. 2001. B cells acquire antigen from target cells after synapse formation. Nature 411: 489-494.
35. Carlin, L. M., K. Eleme, F. E. McCann, and D. M. Davis. 2001. Intercellular transfer and supramolecular organization of human leukocyte antigen C at inhibitory natural killer cell immune synapses. J. Exp. Med. 194: 1507-1517.
36. Sjöström, A., M. Eriksson, C. Cerboni, M. H. Johansson, C. L. Sentman, K. Kärre, and P. Höglund. 2001. Acquisition of external major histocompatibility complex class I molecules by natural killer cells expressing inhibitory Ly49 receptors. J. Exp. Med. 194: 1519-1530.
37. Tabiasco, J., E. Espinosa, D. Hudrisier, E. Joly, J. J. Fournié, and A. Vercellone. 2002. Active trans-synaptic capture of membrane fragments by natural killer cells. Eur. J. Immunol. 32: 1502-1508.
38. Davis, D. M., I. Chiu, M. Fassett, G. B. Cohen, O. Mandelboim, and J. L. Strominger. 1999. The human natural killer cell immune synapse. Proc. Natl. Acad. Sci. USA 96: 15062-15067.
39. Sabzevari, H., J. Kantor, A. Jaigirdar, Y. Tagaya, M. Naramura, J. Hodge, J. Bernon, and J. Schlom. 2001. Acquisition of CD80 (B7-1) by T cells. J. Immunol. 166: 2505-2513.
40. Tatari-Calderone, Z., R. T. Semnani, T. B. Nutman, J. Schlom, and H. Sabzevari. 2002. Acquisition of CD80 by human T cells at early stages of activation: functional involvement of CD80 acquisition in T cell to T cell interaction. J. Immunol. 169: 6162-6169.
41. Baba, E., Y. Takahashi, J. Lichtenfeld, R. Tanaka, A. Yoshida, K. Sugamura, N. Yamamoto, and Y. Tanaka. 2001. Functional CD4 T cells after intercellular molecular transfer of 0X40 ligand. J. Immunol. 167: 875-883.
42. + T cells via trogocytosis. J. Immunol. 188: 744-752.
43. + T helper-antigen-presenting cells. J. Immunol. 174: 7497-7505.
44. + T cell expansion via acquired pMHC I complexes and costimulatory molecules, and IL-2 secretion. J. Leukoc. Biol. 80: 1354-1363.
45. Umeshappa, C. S., and J. Xiang. 2010. Tumor-derived HLA-G1 acquisition by monocytes through trogocytosis: possible functional consequences. Cell. Mol. Life Sci. 67: 4107-4108.
46. + T cells involving acquired MHC class II:peptide complexes: another mechanism to limit clonal expansion? Blood 101: 2704-2710.
47. Helft, J., A. Jacquet, N. T. Joncker, I. Grandjean, G. Dorothée, A. Kissenpfennig, B. Malissen, P. Matzinger, and O. Lantz. 2008. Antigen-specific T-T interactions regulate CD4 T-cell expansion. Blood 112: 1249-1258.
48. + T cell response. J. Immunol. 186: 2148-2155.
49. Choi, E. Y., K. C. Jung, H. J. Park, D. H. Chung, J. S. Song, S. D. Yang, E. Simpson, and S. H. Park. 2005. Thymocyte-thymocyte interaction for efficient positive selection and maturation of CD4 T cells. Immunity 23: 387-396.
50. Martínez-Martín, N., E. Fernández-Arenas, S. Cemerski, P. Delgado, M. Turner, J. Heuser, D. J. Irvine, B. Huang, X. R. Bustelo, A. Shaw, and B. Alarcón. 2011. T cell receptor internalization from the immunological synapse is mediated by TC21 and RhoG GTPase-dependent phagocytosis. Immunity 35: 208-222.
51. Dopfer, E. P., S. Minguet, and W. W. Schamel. 2011. A new vampire saga: the molecular mechanism of T cell trogocytosis. Immunity 35: 151-153.
52. Rachmilewitz, J., and A. Lanzavecchia. 2002. A temporal and spatial summation model for T-cell activation: signal integration and antigen decoding. Trends Immunol. 23: 592-595.
53. Gunzer, M., A. Schäfer, S. Borgmann, S. Grabbe, K. S. Zänker, E. B. Bröcker, E. Kämpgen, and P. Friedl. 2000. Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity 13: 323-332.
54. Underhill, D. M., M. Bassetti, A. Rudensky, and A. Aderem. 1999. Dynamic interactions of macrophages with T cells during antigen presentation. J. Exp. Med. 190: 1909-1914.
55. Kaye, J., N. J. Vasquez, and S. M. Hedrick. 1992. Involvement of the same region of the T cell antigen receptor in thymic selection and foreign peptide recognition. J. Immunol. 148: 3342-3353.
56. Wetzel, S. A., T. W. McKeithan, and D. C. Parker. 2002. Live-cell dynamics and the role of costimulation in immunological synapse formation. J. Immunol. 169: 6092-6101.
57. Chow, S., D. Hedley, P. Grom, R. Magari, J. W. Jacobberger, and T. V. Shankey. 2005. Whole blood fixation and permeabilization protocol with red blood cell lysis for flow cytometry of intracellular phosphorylated epitopes in leukocyte subpopulations. Cytometry A 67: 4-17.
58. Bolte, S., and F. P. Cordelières. 2006. A guided tour into subcellular colocali-zation analysis in light microscopy. J. Microsc. 224: 213-232.
59. Rasband, W. S. 1997-2009. ImageJ. National Institues of Health:http://rsb.info. nih.gov/ij/.
60. Faroudi, M., R. Zaru, P. Paulet, S. Müller, and S. Valitutti. 2003. Cutting edge: T lymphocyte activation by repeated immunological synapse formation and intermittent signaling. J. Immunol. 171: 1128-1132.
61. Hanke, J. H., J. P. Gardner, R. L. Dow, P. S. Changelian, W. H. Brissette, E. J. Weringer, B. A. Pollok, and P. A. Connelly. 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor: study of Lck-and FynT-dependent T cell activation. J. Biol. Chem. 271: 695-701.
62. Lathrop, S. K., C. A. Huddleston, P. A. Dullforce, M. J. Montfort, A. D. Weinberg, and D. C. Parker. 2004. A signal through OX40 (CD134) allows anergic, autoreactive T cells to acquire effector cell functions. J. Immunol. 172: 6735-6743.
63. Perez, O. D., and G. P. Nolan. 2006. Phospho-proteomic immune analysis by flow cytometry: from mechanism to translational medicine at the single-cell level. Immunol. Rev. 210: 208-228.
64. Huppa, J. B., and M. M. Davis. 2003. T-cell-antigen recognition and the im-munological synapse. Nat. Rev. Immunol. 3: 973-983.
65. Huppa, J. B., M. Gleimer, C. Sumen, and M. M. Davis. 2003. Continuous T cell receptor signaling required for synapse maintenance and full effector potential. Nat. Immunol. 4: 749-755.
66. Lee, K. H., A. D. Holdorf, M. L. Dustin, A. C. Chan, P. M. Allen, and A. S. Shaw. 2002. T cell receptor signaling precedes immunological synapse formation. Science 295: 1539-1542.
67. + T cells form mature immunological synapses with enhanced accumulation of c-Cbl and Cbl-b. J. Immunol. 184: 3598-3608.
68. Hwang, I., X. Shen, and J. Sprent. 2003. Direct stimulation of naive T cells by membrane vesicles from antigen-presenting cells: distinct roles for CD54 and B7 molecules. Proc. Natl. Acad. Sci. USA 100: 6670-6675.
69. Sprent, J., and C. D. Surh. 2003. Cytokines and T cell homeostasis. Immunol. Lett. 85: 145-149.
70. Sprent, J. 2005. Direct stimulation of näive T cells by antigen-presenting cell vesicles. Blood Cells Mol. Dis. 35: 17-20.
71. Kovar, M., O. Boyman, X. Shen, I. Hwang, R. Kohler, and J. Sprent. 2006. Direct stimulation of T cells by membrane vesicles from antigen-presenting cells. Proc. Natl. Acad. Sci. USA 103: 11671-11676.
72. + T cells in the absence of APCs. Blood 105: 3238-3246.
73. Rechavi, O., I. Goldstein, H. Vernitsky, B. Rotblat, and Y. Kloog. 2007. Intercellular transfer of oncogenic H-Ras at the immunological synapse. PLoS ONE 2: e1204.
74. HoWangYin, K. Y., J. Caumartin, B. Favier, M. Daouya, L. Yaghi, E. D. Carosella, and J. LeMaoult. 2011. Proper regrafting of Ig-like transcript 2 after trogocytosis allows a functional cell-cell transfer of sensitivity. J. Immunol. 186: 2210-2218.
75. Benoist, C., and D. Mathis. 1990. Regulation of major histocompatibility complex class-II genes: X, Y and other letters of the alphabet. Annu. Rev. Immunol. 8: 681-715.
76. HoWangYin, K. Y., E. Alegre, M. Daouya, B. Favier, E. D. Carosella, and J. LeMaoult. 2010. Different functional outcomes of intercellular membrane transfers to monocytes and T cells. Cell. Mol. Life Sci. 67: 1133-1145.
77. Rosenits, K., S. J. Keppler, S. Vucikuja, and P. Aichele. 2010. T cells acquire cell surface determinants of APC via in vivo trogocytosis during viral infections. Eur. J. Immunol. 40: 3450-3457.
78. Cullinan, P., A. I. Sperling, and J. K. Burkhardt. 2002. The distal pole complex: a novel membrane domain distal to the immunological synapse. Immunol. Rev. 189: 111-122.
79. Allenspach, E. J., P. Cullinan, J. Tong, Q. Tang, A. G. Tesciuba, J. L. Cannon, S. M. Takahashi, R. Morgan, J. K. Burkhardt, and A. I. Sperling. 2001. ERM-dependent movement of CD43 defines a novel protein complex distal to the immunological synapse. Immunity 15: 739-750.
80. Chang, J. T., V. R. Palanivel, I. Kinjyo, F. Schambach, A. M. Intlekofer, A. Banerjee, S. A. Longworth, K. E. Vinup, P. Mrass, J. Oliaro, et al. 2007. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315: 1687-1691.
81. Iezzi, G., K. Karjalainen, and A. Lanzavecchia. 1998. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8: 89-95.
82. Mempel, T. R., S. E. Henrickson, and U. H. Von Andrian. 2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427: 154-159.
83. Madrenas, J., R. L. Wange, J. L. Wang, N. Isakov, L. E. Samelson, and R. N. Germain. 1995. Zeta phosphorylation without ZAP-70 activation induced by TCR antagonists or partial agonists. Science 267: 515-518.
84. Kersh, E. N., G. J. Kersh, and P. M. Allen. 1999. Partially phosphorylated T cell receptor zeta molecules can inhibit T cell activation. J. Exp. Med. 190: 1627-1636.