Fas stimulation of T lymphocytes promotes rapid intercellular exchange of death signals via membrane nanotubes

Cell Research

Volumn 20, Issue 1, 2010, Pages 72-88

  Arkwright, Peter D ^a   Luchetti, Francesca ^a,b   Tour, Julien ^a   Roberts, Charlotte ^a   Ayub, Rahna ^a   Morales, Ana P ^a   Rodríguez, José J ^a   Gilmore, Andrew ^a   Canonico, Barbara ^b   Papa, Stefano ^b   Esposti, Mauro Degli ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF URBINO   (Italy)

Author keywords

Fas; Intercellular communication; Membrane nanotubes; T cells

Indexed keywords

EID: 73849142314     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2009.112     Document Type: Article

References (39)

1. Green DR, Droin N, Pinkoski M. Activation-induced cell death in T cells. Immunol Rev 2003; 193:70-81.
2. Siegel RM, Muppidi JR, Sarker M, Lobito A, Jen M, Martin D et al.. SPOTS: signaling protein oligomeric transduction structures are early mediators of death receptor-induced apoptosis at the plasma membrane. J Cell Biol 2004; 167:735-744.
3. Peter ME, Krammer PH. The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ 2003; 10:26-35.
4. Algeciras-Schimnich A, Shen L, Barnhart BC, Murmann AE, Burkhardt JK, Peter ME. Molecular ordering of the initial signaling events of CD95. Mol Cell Biol 2002; 22:207-220.
5. Rao VK, Straus SE. Causes and consequences of the autoimmune lymphoproliferative syndrome. Hematology 2006; 11:15-23.
6. Martin DA, Zheng L, Siegel RM, Huang B, Fisher GH, Wang J, et al.. Defective CD95/APO-1/Fas signal complex formation in the human autoimmune lymphoproliferative syndrome, type Ia. Proc Natl Acad Sci USA 1999; 96:4552-4557.
7. Rieux-Laucat F, Blachere S, Danielan S, De Villartay JP, Oleastro M, Solary E, et al.. Lymphoproliferative syndrome with autoimmunity: a possible genetic basis for dominant expression of the clinical manifestations. Blood 1999; 94:2575-2582.
8. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science 2004; 303:1007-1010.
9. 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.
10. Gerdes HH, Carvalho RN. Intercellular transfer mediated by tunneling nanotubes. Curr Opin Cell Biol 2008; 20:470-475.
11. Blanchard N, Di Bartolo V, Hivroz C. In the immune synapse, ZAP-70 controls T cell polarization and recruitment of signaling proteins but not formation of the synaptic pattern. Immunity 2000; 17:389-399.
12. Degli Esposti M. Organelle intermixing and membrane scrambling in cell death. Methods Enzymol 2008; 422:421-438.
13. Degli Esposti M, Tour J, Ouasti S, Ivanova S, Matarrese P, Malorni W, et al.. Fas death receptor enhances endocytic membrane traffic converging into the golgiregion. Mol Biol Cell 2009; 20:600-615.
14. 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.
15. Gurke S, Barroso JF, Hodneland E, Bukoreshtliev NV, Schlicker O, Gerdes HH. Tunneling nanotube (TNT)-like structures facilitate a constitutive, actomyosin-dependent exchange of endocytic organelles between normal rat kidney cells. Exp Cell Res 2008; 314:3669-3683.
16. Wherlock M, Mellor H. The Rho GTPase family: a Racs to Wrchs story. J Cell Sci 2002; 115:239-240.
17. Pelish HE, Peterson JR, Salvarezza SB, Rodriguez-Boulan E, Chen JL, Stamnes M, et al.. Secramine inhibits Cdc42- dependent functions in cells and Cdc42 activation in vitro. Nat Chem Biol 2006; 2:39-46.
18. Joly E, Hudrisier D. What is trogocytosis and what is its purpose? Nat Immunol 2003; 4:815.
19. Daubeuf S, Puaux AL, 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.
20. Aucher A, Magdeleine E, Joly E, Hudrisier D. Capture of plasma membrane fragments from target cells by trogocytosis requires signaling in T cells but not in B cells. Blood 2008; 111:5621-5628.
21. Veranic P, Lokar M, Schütz GJ, Weghuber J, Wieser S, Hägerstrand H, et al.. Different types of cell-to-cell connections mediated by nanotubular structures. Biophys J 2008; 95:4416-4425.
22. Poupot M, Fournié JJ. Spontaneous membrane transfer through homotypic synapses between lymphoma cells. J Immunol 2003; 171:2517-2523.
23. Blott E J, Bossi G, Clark R, Zvelebil M, Griffiths GM. Fas ligand is targeted to secretory lysosomesvia a proline-rich domain in its cytoplasmic tail. J Cell Sci 2001; 114:2405-2416.
24. Herr I, Posovszky C, Di Marzio LD, Cifone MG, Boehler T, Debatin KM. Autoamplification of apoptosis following ligation of CD95-L, TRAIL and TNF-alpha. Oncogene 2000; 19:4255-4262.
25. Muppidi JR, Lobito AA, Ramaswamy M, Yang JK, Wang L, Siegel RM. Homotypic FADD interactions through a conserved RXDLL motif are required for death receptor-induced apoptosis. Cell Death Differ 2006; 13:641-1650.
26. Subauste MC, Von Herrath M, Benard V, Chamberlain CE, Chuang TH, Chu K, Bokoch, et al.. Rho family proteins modulate rapid apoptosis induced by cytotoxic T lymphocytes and Fas. J Biol Chem 2000; 275:9725-9733.
27. Parlato S, Giammarioli AM, Logozzi M, Lozupone F, Matarrese P, Luciani F, et al.. CD95 (APO-1/Fas) linkage to the actin cytoskeleton through ezrin in human T lymphocytes: a novel regulatory mechanism of the CD95 apoptotic pathway. EMBO J 2000; 19:5123-5134.
28. Hébert M, Potin S, Sebbagh M, Bertoglio J, Bréard J, Hamelin J. Rho-ROCK-dependent ezrin-radixin-moesin phosphorylation regulates Fas-mediated apoptosis in Jurkat cells. J Immunol 2008; 181:5963-5973
29. Callard RE, Stark J, Yates AJ. Fratricide: a mechanism for T memory-cell homeostasis. Trends Immunol 2003; 24:370-375.
30. Arnold R, Brenner D, Becker M, Frey CR, Krammer PH. How T lymphocytes switch between life and death. Eur J Immunol 2006; 36:1654-1658.
31. Kischkel FC, Lawrence DA, Tinel A, Le Blanc H, Virmani A, Schow P, et al.. Death receptor recruitment of endogenous caspase- and apoptosis initiation in the absence of caspase-8. J Biol Chem 2001; 276:46639-46646.
32. Legembre P, Daburon S, Moreau P, Moreau JF, Taupin JL. Modulation of Fas-mediated apoptosis by lipid rafts in T lymphocytes. J Immunol 2006; 176:716-720.
33. Upton JP, Valentijn AJ, Zhang L, Gilmore AP. The N-terminal conformation of Bax regulates cell commitment to apoptosis. Cell Death Differ 2007; 14:932-942.
34. Ouasti S, Matarrese P, Paddon R, Khosravi-Far R, Sorice M, Tinari A, et al.. Death receptor ligation triggers membrane scrambling between Golgi and mitochondria. Cell Death Differ 2007; 14:453-461.
35. Horner H, Frank C, Dechant C, Repp R, Glennie M, Herrmann M, et al.. Intimate cell conjugate formation and exchange of membrane lipids precede apoptosis induction in target cells during antibody-dependent, granulocyte-mediated cytotoxicity. J Immunol 2007; 179:337-345.
36. 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.
37. Packard BZ, Komoriya A, Brotz TM, Henkart PA. Caspase 8 activity in membrane blebs after anti-Fas ligation. J Immunol 2001; 167:5061-5066.
38. Conover WJ. Pratical Nonparametric Statistics. 3rd Edition, New York: John Wiley & Sons, 1998.
39. Muppidi JR, Siegel RM. Ligand-independent redistribution of Fas (CD95) into lipid rafts mediates clonotypic T cell death. Nat Immunol 2004; 5:182-189.