Trogocytosis is a gateway to characterize functional diversity in melanoma-specific CD8 + T cell clones

Journal of Immunology

Volumn 188, Issue 2, 2012, Pages 632-640

  Uzana, Ronny ^a   Eisenberg, Galit ^a   Sagi, Yael ^b   Frankenburg, Shoshana ^a   Merims, Sharon ^a   Amariglio, Ninette ^c   Yefenof, Eitan ^d   Peretz, Tamar ^a   Machlenkin, Arthur ^a   Lotem, Michal ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SHEBA MEDICAL CENTER   (Israel)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CD150 ANTIGEN; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN; NATURAL KILLER T AND B CELL ANTIGEN; PROTEIN S6; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CELL ASSAY; CELL STIMULATION; CELL TRANSPORT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGRANULATION; DOWN REGULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LYMPHOCYTE FUNCTION; LYSOSOME; MELANOMA; MOLECULAR CLONING; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; TROGOCYTOSIS;

ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CLONE CELLS; CYTOTOXICITY TESTS, IMMUNOLOGIC; EPITOPES; EPITOPES, T-LYMPHOCYTE; HLA-A2 ANTIGEN; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA, EXPERIMENTAL; NEOPLASM PROTEINS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84855986634     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101429     Document Type: Article

References (50)

1. Johnson, L. A., B. Heemskerk, D. J. Powell, Jr., C. J. Cohen, R. A. Morgan, M. E. Dudley, P. F. Robbins, and S. A. Rosenberg. 2006. Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J. Immunol. 177: 6548-6559. (Pubitemid 44628874)
2. Zeh, H. J., III, D. Perry-Lalley, M. E. Dudley, S. A. Rosenberg, and J. C. Yang. 1999. High avidity CTLs for two self-antigens demonstrate superior in vitro and in vivo antitumor efficacy. J. Immunol. 162: 989-994. (Pubitemid 29035425)
3. + T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
4. Nembrini, C., B. Abel, M. Kopf, and B. J. Marsland. 2006. Strong TCR signaling, TLR ligands, and cytokine redundancies ensure robust development of type 1 effector T cells. J. Immunol. 176: 7180-7188. (Pubitemid 43849019)
5. + T cells: a story of survival. Adv. Exp. Med. Biol. 590: 149-170.
6. + T cell responses in lymph nodes. Immunity 33: 412-423.
7. Alexander-Miller, M. A., G. R. Leggatt, and J. A. Berzofsky. 1996. Selective expansion of high- or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl. Acad. Sci. USA 93: 4102-4107. (Pubitemid 26144250)
8. 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. (Pubitemid 28420234)
9. Bromley, S. K., W. R. Burack, K. G. Johnson, K. Somersalo, T. N. Sims, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 2001. The immunological synapse. Annu. Rev. Immunol. 19: 375-396. (Pubitemid 32368040)
10. Joly, E., and D. Hudrisier. 2003. What is trogocytosis and what is its purpose? Nat. Immunol. 4: 815. (Pubitemid 37098646)
11. 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.
12. 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.
13. Daubeuf, S., A. L. Puaux, E. Joly, and D. Hudrisier. 2006. 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. 1: 2536-2542.
14. Machlenkin, A., R. Uzana, S. Frankenburg, G. Eisenberg, L. Eisenbach, J. Pitcovski, R. Gorodetsky, A. Nissan, T. Peretz, and M. Lotem. 2008. Capture of tumor cell membranes by trogocytosis facilitates detection and isolation of tumor-specific functional CTLs. Cancer Res. 68: 2006-2013. (Pubitemid 351416588)
15. Lotem, M., A. Machlenkin, T. Hamburger, A. Nissan, L. Kadouri, S. Frankenburg, Z. Gimmon, O. Elias, I. B. David, A. Kuznetz, et al. 2009. Autologous melanoma vaccine induces antitumor and self-reactive immune responses that affect patient survival and depend on MHC class II expression on vaccine cells. Clin. Cancer Res. 15: 4968-4977.
16. Dudley, M. E., J. R. Wunderlich, T. E. Shelton, J. Even, and S. A. Rosenberg. 2003. Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients. J. Immunother. 26: 332-342. (Pubitemid 36858717)
17. Machlenkin, A., A. Paz, E. Bar Haim, O. Goldberger, E. Finkel, B. Tirosh, I. Volovitz, E. Vadai, G. Lugassy, S. Cytron, et al. 2005. Human CTL epitopes prostatic acid phosphatase-3 and six-transmembrane epithelial antigen of prostate-3 as candidates for prostate cancer immunotherapy. Cancer Res. 65: 6435-6442. (Pubitemid 40994432)
18. Akatsuka, Y., E. G. Martin, A. Madonik, A. A. Barsoukov, and J. A. Hansen. 1999. Rapid screening of T-cell receptor (TCR) variable gene usage by multiplex PCR: application for assessment of clonal composition. Tissue Antigens 53: 122-134. (Pubitemid 29089942)
19. Rubio, V., T. B. Stuge, N. Singh, M. R. Betts, J. S. Weber, M. Roederer, and P. P. Lee. 2003. Ex vivo identification, isolation and analysis of tumor-cytolytic T cells. Nat. Med. 9: 1377-1382. (Pubitemid 37466186)
20. + T cells responding to antigen without requiring knowledge of epitope specificities. Blood 110: 201-210.
21. Qin, Z., C. Harders, X. Cao, C. Huber, T. Blankenstein, and B. Seliger. 2002. Increased tumorigenicity, but unchanged immunogenicity, of transporter for antigen presentation 1-deficient tumors. Cancer Res. 62: 2856-2860. (Pubitemid 34525771)
22. Garcia, K. C., C. A. Scott, A. Brunmark, F. R. Carbone, P. A. Peterson, I. A. Wilson, and L. Teyton. 1996. CD8 enhances formation of stable T-cell receptor/MHC class I molecule complexes. Nature 384: 577-581. (Pubitemid 26415937)
23. Bodinier, M., M. A. Peyrat, C. Tournay, F. Davodeau, F. Romagne, M. Bonneville, and F. Lang. 2000. Efficient detection and immunomagnetic sorting of specific T cells using multimers of MHC class I and peptide with reduced CD8 binding. Nat. Med. 6: 707-710. (Pubitemid 30398798)
24. Billadeau, D. D., and P. J. Leibson. 2002. ITAMs versus ITIMs: striking a balance during cell regulation. J. Clin. Invest. 109: 161-168. (Pubitemid 34083734)
25. Flaig, R. M., S. Stark, and C. Watzl. 2004. Cutting edge: NTB-A activates NK cells via homophilic interaction. J. Immunol. 172: 6524-6527. (Pubitemid 38669084)
26. Ward, J., M. Bonaparte, J. Sacks, J. Guterman, M. Fogli, D. Mavilio, and E. Barker. 2007. HIV modulates the expression of ligands important in triggering natural killer cell cytotoxic responses on infected primary T-cell blasts. Blood 110: 1207-1214. (Pubitemid 47281418)
27. Riond, J., J. Elhmouzi, D. Hudrisier, and J. E. Gairin. 2007. Capture of membrane components via trogocytosis occurs in vivo during both dendritic cells and target cells encounter by CD8+ T cells. Scand. J. Immunol. 66: 441-450. (Pubitemid 47394565)
28. Puaux, A. L., J. Campanaud, A. Salles, X. Préville, B. Timmerman, E. Joly, and D. Hudrisier. 2006. Avery rapid and simple assay based on trogocytosis to detect and measure specific T and B cell reactivity by flow cytometry. Eur. J. Immunol. 36: 779-788.
29. Kedzierska, K., N. L. La Gruta, M. P. Davenport, S. J. Turner, and P. C. Doherty. 2005. Contribution of T cell receptor affinity to overall avidity for virus-specific CD8+ T cell responses. Proc. Natl. Acad. Sci. USA 102: 11432-11437. (Pubitemid 41153837)
30. + severe combined immunodeficiency caused by complete deficiency of the CD3ζ subunit of the T-cell antigen receptor complex. Blood 109: 3198-3206.
31. Pang, D. J., A. C. Hayday, and M. J. Bijlmakers. 2007. CD8 raft localization is induced by its assembly into CD8αβ heterodimers, not CD8αα homodimers. J. Biol. Chem. 282: 13884-13894.
32. Laugel, B., H. A. van den Berg, E. Gostick, D. K. Cole, L. Wooldridge, J. Boulter, A. Milicic, D. A. Price, and A. K. Sewell. 2007. Different T cell receptor affinity thresholds and CD8 coreceptor dependence govern cytotoxic T lymphocyte activation and tetramer binding properties. J. Biol. Chem. 282: 23799-23810. (Pubitemid 47328005)
33. 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. (Pubitemid 46417631)
34. Arechiga, A. F., B. D. Bell, S. Leverrier, B. M. Weist, M. Porter, Z. Wu, Y. Kanno, S. J. Ramos, S. T. Ong, R. Siegel, and C. M. Walsh. 2007. A Fasassociated death domain protein/caspase-8-signaling axis promotes S-phase entry and maintains S6 kinase activity in T cells responding to IL-2. J. Immunol. 179: 5291-5300.
35. Lockyer, H. M., E. Tran, and B. H. Nelson. 2007. STAT5 is essential for Akt/p70S6 kinase activity during IL-2-induced lymphocyte proliferation. J. Immunol. 179: 5301-5308.
36. Xie, C., R. Patel, T. Wu, J. Zhu, T. Henry, M. Bhaskarabhatla, R. Samudrala, K. Tus, Y. Gong, H. Zhou, et al. 2007. PI3K/AKT/mTOR hypersignaling in autoimmune lymphoproliferative disease engendered by the epistatic interplay of Sle1b and FASlpr. Int. Immunol. 19: 509-522. (Pubitemid 46523398)
37. Jenkins, M. R., A. Tsun, J. C. Stinchcombe, and G. M. Griffiths. 2009. The strength of T cell receptor signal controls the polarization of cytotoxic machinery to the immunological synapse. Immunity 31: 621-631.
38. Veillette, A. 2006. Immune regulation by SLAM family receptors and SAP-related adaptors. Nat. Rev. Immunol. 6: 56-66. (Pubitemid 43279753)
39. Veillette, A., and S. Latour. 2003. The SLAM family of immune-cell receptors. Curr. Opin. Immunol. 15: 277-285. (Pubitemid 36645103)
40. Green, J. M., V. Karpitskiy, S. L. Kimzey, and A. S. Shaw. 2000. Coordinate regulation of T cell activation by CD2 and CD28. J. Immunol. 164: 3591-3595. (Pubitemid 30169811)
41. Valdez, P. A., H. Wang, D. Seshasayee, M. van Lookeren Campagne, A. Gurney, W. P. Lee, and I. S. Grewal. 2004. NTB-A, a new activating receptor in T cells that regulates autoimmune disease. J. Biol. Chem. 279: 18662-18669. (Pubitemid 38623289)
42. Veillette, A., Z. Dong, and S. Latour. 2007. Consequence of the SLAM-SAP signaling pathway in innate-like and conventional lymphocytes. Immunity 27: 698-710. (Pubitemid 350102266)
43. Chan, B., A. Lanyi, H. K. Song, J. Griesbach, M. Simarro-Grande, F. Poy, D. Howie, J. Sumegi, C. Terhorst, and M. J. Eck. 2003. SAP couples Fyn to SLAM immune receptors. Nat. Cell Biol. 5: 155-160. (Pubitemid 36204198)
44. Howie, D., F. S. Laroux, M. Morra, A. R. Satoskar, L. E. Rosas, W. A. Faubion, A. Julien, S. Rietdijk, A. J. Coyle, C. Fraser, and C. Terhorst. 2005. Cutting edge: the SLAM family receptor Ly108 controls T cell and neutrophil functions. J. Immunol. 174: 5931-5935. (Pubitemid 40663778)
45. Chatterjee, M., K. Kis-Toth, T. H. Thai, C. Terhorst, and G. C. Tsokos. 2011. SLAMF6-driven co-stimulation of human peripheral T cells is defective in SLE T cells. Autoimmunity 44: 211-218.
46. Greenwald, R. J., G. J. Freeman, and A. H. Sharpe. 2005. The B7 family revisited. Annu. Rev. Immunol. 23: 515-548. (Pubitemid 40563179)
47. + T-cells during CD28 costimulation: implications for immune cell-based therapies and studies related to the expansion of double-positive T-cells during aging. Clin. Immunol. 96: 187-197.
48. +cytotoxic lymphocytes for adoptive immunotherapy. J. Immunol. 179: 4910-4918.
49. Suntharalingam, G., M. R. Perry, S. Ward, S. J. Brett, A. Castello-Cortes, M. D. Brunner, and N. Panoskaltsis. 2006. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N. Engl. J. Med. 355: 1018-1028. (Pubitemid 44343545)
50. Machlenkin, A., O. Goldberger, B. Tirosh, A. Paz, I. Volovitz, E. Bar-Haim, S. H. Lee, E. Vadai, E. Tzehoval, and L. Eisenbach. 2005. Combined dendritic cell cryotherapy of tumor induces systemic antimetastatic immunity. Clin. Cancer Res. 11: 4955-4961. (Pubitemid 41557217)