Ras oncoproteins transfer from melanoma cells to T cells and modulate their effector functions

Journal of Immunology

Volumn 189, Issue 9, 2012, Pages 4361-4370

  Vernitsky, Helly ^a   Rechavi, Oded ^a,b   Rainy, Nir ^a   Besser, Michal J ^a   Nagar, Meital ^a   Schachter, Jacob ^a   Lerenthal, Yaniv ^a   Ehrlich, Marcelo ^a   Kloog, Yoel ^a   Goldstein, Itamar ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; RAS PROTEIN; T LYMPHOCYTE RECEPTOR;

ANTIGEN SPECIFICITY; ARTICLE; CELL CONTACT; CELL MEMBRANE; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE FUNCTION; MELANOMA CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE;

CELL LINE; COCULTURE TECHNIQUES; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS P21(RAS); T-LYMPHOCYTES; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 84867908849     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200019     Document Type: Article

References (40)

1. 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. (Pubitemid 29329988)
2. Stinchcombe, J. C., G. Bossi, S. Booth, and G. M. Griffiths. 2001. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15: 751-761. (Pubitemid 34008503)
3. Bopp, T., C. Becker, M. Klein, S. Klein-Hessling, A. Palmetshofer, E. Serfling, V. Heib, M. Becker, J. Kubach, S. Schmitt, et al. 2007. Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression. J. Exp. Med. 204: 1303-1310. (Pubitemid 46919868)
4. Rustom, A., R. Saffrich, I. Markovic, P. Walther, and H. H. Gerdes. 2004. Nanotubular highways for intercellular organelle transport. Science 303: 1007-1010. (Pubitemid 38209703)
5. Joly, E., and D. Hudrisier. 2003. What is trogocytosis and what is its purpose? Nat. Immunol. 4: 815. (Pubitemid 37098646)
6. Davis, D. M. 2007. Intercellular transfer of cell-surface proteins is common and can affect many stages of an immune response. Nat. Rev. Immunol. 7: 238-243.
7. Sprent, J. 2005. Swapping molecules during cell-cell interactions. Sci. STKE 2005: pe8.
8. 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.
9. Rechavi, O., I. Goldstein, and Y. Kloog. 2009. Intercellular exchange of proteins: the immune cell habit of sharing. FEBS Lett. 583: 1792-1799.
10. Rechavi, O., M. Kalman, Y. Fang, H. Vernitsky, J. Jacob-Hirsch, L. J. Foster, Y. Kloog, and I. Goldstein. 2010. Trans-SILAC: sorting out the non-cellautonomous proteome. Nat. Methods 7: 923-927.
11. Bos, J. L. 1989. ras oncogenes in human cancer: a review. Cancer Res. 49: 4682-4689. (Pubitemid 19213607)
12. Shields, J. M., K. Pruitt, A. McFall, A. Shaub, and C. J. Der. 2000. Understanding Ras: 'it ain't over 'til it's over.' Trends Cell Biol. 10: 147-154. (Pubitemid 30171309)
13. Haluska, F. G., H. Tsao, H. Wu, F. S. Haluska, A. Lazar, and V. Goel. 2006. Genetic alterations in signaling pathways in melanoma. Clin. Cancer Res. 12: 2301s-2307s.
14. Schreiber, R. D., L. J. Old, and M. J. Smyth. 2011. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331: 1565-1570.
15. Rosenberg, S. A., and M. E. Dudley. 2004. Cancer regression in patients with metastatic melanoma after the transfer of autologous antitumor lymphocytes. Proc. Natl. Acad. Sci. USA 101(Suppl 2): 14639-14645. (Pubitemid 39346736)
16. Rosenberg, S. A., N. P. Restifo, J. C. Yang, R. A. Morgan, and M. E. Dudley. 2008. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat. Rev. Cancer 8: 299-308. (Pubitemid 351430867)
17. Goldstein, I., S. Ben-Horin, A. Koltakov, H. Chermoshnuk, V. Polevoy, Y. Berkun, N. Amariglio, and I. Bank. 2007. a1b1 Integrin+ and regulatory Foxp3+ T cells constitute two functionally distinct human CD4+ T cell subsets oppositely modulated by TNFalpha blockade. J. Immunol. 178: 201-210. (Pubitemid 46033602)
18. Besser, M. J., R. Shapira-Frommer, A. J. Treves, D. Zippel, O. Itzhaki, E. Schallmach, A. Kubi, B. Shalmon, I. Hardan, R. Catane, et al. 2009. Minimally cultured or selected autologous tumor-infiltrating lymphocytes after a lympho-depleting chemotherapy regimen in metastatic melanoma patients. J. Immunother. 32: 415-423.
19. 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)
20. Uzana, R., G. Eisenberg, Y. Sagi, S. Frankenburg, S. Merims, N. Amariglio, E. Yefenof, T. Peretz, A. Machlenkin, and M. Lotem. 2012. Trogocytosis is a gateway to characterize functional diversity in melanoma-specific CD8+ T cell clones. J. Immunol. 188: 632-640.
21. Rechavi, O., Y. Erlich, H. Amram, L. Flomenblit, F. V. Karginov, I. Goldstein, G. J. Hannon, and Y. Kloog. 2009. Cell contact-dependent acquisition of cellular and viral nonautonomously encoded small RNAs. Genes Dev. 23: 1971-1979.
22. Daubeuf, S., C. Bordier, D. Hudrisier, and E. Joly. 2009. Suitability of various membrane lipophilic probes for the detection of trogocytosis by flow cytometry. Cytometry A 75: 380-389.
23. Krutzik, P. O., and G. P. Nolan. 2003. Intracellular phospho-protein staining techniques for flow cytometry: monitoring single cell signaling events. Cytometry A 55: 61-70. (Pubitemid 37522508)
24. Betts, M. R., J. M. Brenchley, D. A. Price, S. C. De Rosa, D. C. Douek, M. Roederer, and R. A. Koup. 2003. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281: 65-78. (Pubitemid 37324571)
25. McCann, F. E., P. Eissmann, B. Onfelt, R. Leung, and D. M. Davis. 2007. The activating NKG2D ligand MHC class I-related chain A transfers from target cells to NK cells in a manner that allows functional consequences. J. Immunol. 178: 3418-3426. (Pubitemid 46417606)
26. Roose, J. P., M. Mollenauer, V. A. Gupta, J. Stone, and A. Weiss. 2005. A diacylglycerol-protein kinase C-RasGRP1 pathway directs Ras activation upon antigen receptor stimulation of T cells. Mol. Cell. Biol. 25: 4426-4441. (Pubitemid 40705750)
27. Mor, A., and M. R. Philips. 2006. Compartmentalized Ras/MAPK signaling. Annu. Rev. Immunol. 24: 771-800.
28. Mainiero, F., A. Gismondi, A. Soriani, M. Cippitelli, G. Palmieri, J. Jacobelli, M. Piccoli, L. Frati, and A. Santoni. 1998. Integrin-mediated ras-extracellular regulated kinase (ERK) signaling regulates interferon g production in human natural killer cells. J. Exp. Med. 188: 1267-1275. (Pubitemid 28478015)
29. Prinz, P. U., A. N. Mendler, I. Masouris, L. Durner, R. Oberneder, and E. Noessner. 2012. High DGK-a and disabled MAPK pathways cause dysfunction of human tumor-infiltrating CD8+ T cells that is reversible by pharmacologic intervention. J. Immunol. 188: 5990-6000.
30. Roy, S., S. Plowman, B. Rotblat, I. A. Prior, C. Muncke, S. Grainger, R. G. Parton, Y. I. Henis, Y. Kloog, and J. F. Hancock. 2005. Individual palmitoyl residues serve distinct roles in H-ras trafficking, microlocalization, and signaling. Mol. Cell. Biol. 25: 6722-6733. (Pubitemid 41023244)
31. Radoja, S., A. B. Frey, and S. Vukmanovic. 2006. T-cell receptor signaling events triggering granule exocytosis. Crit. Rev. Immunol. 26: 265-290. (Pubitemid 44079774)
32. 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. (Pubitemid 33081525)
33. Koebel, C. M., W. Vermi, J. B. Swann, N. Zerafa, S. J. Rodig, L. J. Old, M. J. Smyth, and R. D. Schreiber. 2007. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450: 903-907. (Pubitemid 350231320)
34. Dunn, G. P., L. J. Old, and R. D. Schreiber. 2004. The three Es of cancer immunoediting. Annu. Rev. Immunol. 22: 329-360. (Pubitemid 38680426)
35. Delon, J., and R. N. Germain. 2000. Information transfer at the immunological synapse. Curr. Biol. 10: R923-R933. (Pubitemid 32062654)
36. 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.
37. Daniels, M. A., E. Teixeiro, J. Gill, B. Hausmann, D. Roubaty, K. Holmberg, G. Werlen, G. A. Holländer, N. R. Gascoigne, and E. Palmer. 2006. Thymic selection threshold defined by compartmentalization of Ras/MAPK signalling. Nature 444: 724-729. (Pubitemid 44949596)
38. Smith-Garvin, J. E., G. A. Koretzky, and M. S. Jordan. 2009. T cell activation. Annu. Rev. Immunol. 27: 591-619.
39. Zha, Y., R. Marks, A. W. Ho, A. C. Peterson, S. Janardhan, I. Brown, K. Praveen, S. Stang, J. C. Stone, and T. F. Gajewski. 2006. T cell anergy is reversed by active Ras and is regulated by diacylglycerol kinase-alpha. Nat. Immunol. 7: 1166-1173. (Pubitemid 44594312)
40. Janardhan, S. V., K. Praveen, R. Marks, and T. F. Gajewski. 2011. Evidence implicating the Ras pathway in multiple CD28 costimulatory functions in CD4+ T cells. PLoS ONE 6: e24931.