H-Ras transfers from B to T cells via tunneling nanotubes

Cell Death and Disease

Volumn 4, Issue 7, 2013, Pages

  Rainy, N ^a   Chetrit, D ^a   Rouger, V ^b,c   Vernitsky, H ^d   Rechavi, O ^a   Marguet, D ^b,c   Goldstein, I ^a,d   Ehrlich, M ^a   Kloog, Y ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^c INSERM   (France)

^d SHEBA MEDICAL CENTER   (Israel)

Author keywords

Cell cell interactions; Cellular immunology; Intercellular transfer

Indexed keywords

CD86 ANTIGEN; GREEN FLUORESCENT PROTEIN; NANOTUBE; RAS PROTEIN;

ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; BLEACHING; CELL INTERACTION; CELL MEMBRANE; COCULTURE; CONFOCAL MICROSCOPY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TRANSPORT; T LYMPHOCYTE;

EID: 84881041895     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.245     Document Type: Article

References (29)

1. Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS, Allen PM et al. The immunological synapse: a molecular machine controlling T cell activation. Science 1999; 285: 221-227.
2. Carlin LM, Eleme K, McCann FE, Davis DM. Intercellular transfer and supramolecular organization of human leukocyte antigen C at inhibitory natural killer cell immune synapses. J Exp Med 2001; 194: 1507-1517.
3. Stinchcombe JC, Bossi G, Booth S, Griffiths GM. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 2001; 15: 751-761.
4. Davis DM, Sowinski S. Membrane nanotubes: dynamic long-distance connections between animal cells. Nat Rev Mol Cell Biol 2008; 9: 431-436.
5. Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A, Kohler K et al. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol 2008; 10: 211-219.
6. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science 2004; 303: 1007-1010.
7. Gousset K, Schiff E, Langevin C, Marijanovic Z, Caputo A, Browman DT et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat Cell Biol 2009; 11: 328-336.
8. Onfelt B, Nedvetzki S, Benninger RK, Purbhoo MA, Sowinski S, Hume AN et al. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. J Immunol 2006; 177: 8476-8483.
9. Watkins SC, Salter RD. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 2005; 23: 309-318.
10. Joly E, Hudrisier D. What is trogocytosis and what is its purpose? Nat Immunol 2003; 4: 815.
11. Rechavi O, Goldstein I, Kloog Y. Intercellular exchange of proteins: the immune cell habit of sharing. FEBS Lett 2009; 583: 1792-1799.
12. Rechavi O, Goldstein I, Vernitsky H, Rotblat B, Kloog Y. Intercellular transfer of oncogenic H-Ras at the immunological synapse. PLoS One 2007; 2: e1204.
13. Rechavi O, Kalman M, Fang Y, Vernitsky H, Jacob-Hirsch J, Foster LJ et al. Trans-SILAC: sorting out the non-cell-autonomous proteome. Nat Methods 2010; 7: 923-927.
14. Daubeuf S, Aucher A, Bordier C, Salles A, Serre L, Gaibelet G et al. Preferential transfer of certain plasma membrane proteins onto T and B cells by trogocytosis. PLoS One 2010; 5: e8716.
15. Chauveau A, Aucher A, Eissmann P, Vivier E, Davis DM. Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells. Proc Natl Acad Sci USA 2010; 107: 5545-5550.
16. Monneret S, Belloni F, Marguet D. Practical lab tool for living cells based on microstereolithography and multiple dynamic holographic optical tweezers. Proceedings of SPIE 6088, Imaging, Manipulation, and Analysis of Biomolecules, Cells, and Tissues IV 2006; 60880Z.
17. Niv H, Gutman O, Kloog Y, Henis YI. Activated K-Ras and H-Ras display different interactions with saturable nonraft sites at the surface of live cells. J Cell Biol 2002; 157: 865-872.
18. Shields JM, Pruitt K, McFall A, Shaub A, Der CJ. Understanding Ras: 'it ain't over 'til it's over'. Trends Cell Biol 2000; 10: 147-154.
19. Cox AD, Der CJ. Ras history: the saga continues. Small GTPases 2010; 1: 2-27.
20. Choy E, Chiu VK, Silletti J, Feoktistov M, Morimoto T, Michaelson D et al. Endomembrane trafficking of ras: the CAAX motif targets proteins to the ER and Golgi. Cell 1999; 98: 69-80.
21. Hancock JF. Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 2003; 4: 373-384.
22. Roy S, Plowman S, Rotblat B, Prior IA, Muncke C, Grainger S et al. Individual palmitoyl residues serve distinct roles in h-ras trafficking, microlocalization, and signaling. Mol Cell Biol 2005; 25: 6722-6733.
23. Davis DM. Intercellular transfer of cell-surface proteins is common and can affect many stages of an immune response. Nat Rev Immunol 2007; 7: 238-243.
24. Arkwright PD, Luchetti F, Tour J, Roberts C, Ayub R, Morales AP et al. Fas stimulation of T lymphocytes promotes rapid intercellular exchange of death signals via membrane nanotubes. Cell Res 2010; 20: 72-88.
25. McCann FE, Eissmann P, Onfelt B, Leung R, Davis DM. 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 2007; 178: 3418-3426.
26. Qureshi OS, Zheng Y, Nakamura K, Attridge K, Manzotti C, Schmidt EM et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 2010; 332: 600-603.
27. Vernitsky H, Rechavi O, Rainy N, Besser MJ, Nagar M, Schachter J et al. Ras oncoproteins transfer from melanoma cells to T cells and modulate their effector functions. J Immunol 2012; 189: 4361-4370.
28. Mandelboim O, Reyburn HT, Vales-Gomez M, Pazmany L, Colonna M, Borsellino G et al. Protection from lysis by natural killer cells of group 1 and 2 specificity is mediated by residue 80 in human histocompatibility leukocyte antigen C alleles and also occurs with empty major histocompatibility complex molecules. J Exp Med 1996; 184: 913-922.
29. Eisenberg S, Beckett AJ, Prior IA, Dekker FJ, Hedberg C, Waldmann H et al. Raft protein clustering alters N-Ras membrane interactions and activation pattern. Mol Cell Biol 2011; 31: 3938-3952.