Rapid and unidirectional perforin pore delivery at the cytotoxic immune synapse

Journal of Immunology

Volumn 191, Issue 5, 2013, Pages 2328-2334

  Lopez, Jamie A ^a,b   Jenkins, Misty R ^a,b   Rudd Schmidt, Jesse A ^a   Brennan, Amelia J ^a,b   Danne, Jillian C ^a   Mannering, Stuart I ^b,c   Trapani, Joseph A ^a,b   Voskoboinik, Ilia ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PERFORIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CD8+ T LYMPHOCYTE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXIC LYMPHOCYTE; DEGRANULATION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOLOGICAL SYNAPSE; LYMPHOCYTE FUNCTION; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; TARGET CELL DESTRUCTION;

ANIMALS; CELL DEGRANULATION; CELLS, CULTURED; HUMANS; IMMUNOLOGICAL SYNAPSES; KILLER CELLS, NATURAL; MICE; MICROSCOPY, CONFOCAL; PERFORIN; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84883343650     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301205     Document Type: Article

References (27)

1. Lopez, J. A., A. J. Brennan, J. C. Whisstock, I. Voskoboinik, and J. A. Trapani. 2012. Protecting a serial killer: pathways for perforin trafficking and self-defence ensure sequential target cell death. Trends Immunol. 33: 406-412.
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.
3. Jenkins, M. R., and G. M. Griffiths. 2010. The synapse and cytolytic machinery of cytotoxic T cells. Curr. Opin. Immunol. 22: 308-313.
4. Dustin, M. L., and E. O. Long. 2010. Cytotoxic immunological synapses. Immunol. Rev. 235: 24-34.
5. Lopez, J. A., O. Susanto, M. R. Jenkins, N. Lukoyanova, V. R. Sutton, R. H. Law, A. Johnston, C. H. Bird, P. I. Bird, J. C. Whisstock, et al. 2013. Perforin forms transient pores on the target cell plasma membrane to facilitate rapid access of granzymes during killer cell attack. Blood 121: 2659-2668.
6. Sutton, V. R., J. E. Davis, M. Cancilla, R. W. Johnstone, A. A. Ruefli, K. Sedelies, K. A. Browne, and J. A. Trapani. 2000. Initiation of apoptosis by granzyme B requires direct cleavage of bid, but not direct granzyme B-mediated caspase activation. J. Exp. Med. 192: 1403-1414.
7. Pores-Fernando, A. T., and A. Zweifach. 2009. Calcium influx and signaling in cytotoxic T-lymphocyte lytic granule exocytosis. Immunol. Rev. 231: 160-173.
8. Maul-Pavicic, A., S. C. C. Chiang, A. Rensing-Ehl, B. Jessen, C. Fauriat, S. M. Wood, S. Sjöqvist, M. Hufnagel, I. Schulze, T. Bass, et al. 2011. ORAI1-mediated calcium influx is required for human cytotoxic lymphocyte degranulation and target cell lysis. Proc. Natl. Acad. Sci. USA 108: 3324-3329.
9. Andzelm, M. M., X. Chen, K. Krzewski, J. S. Orange, and J. L. Strominger. 2007. Myosin IIA is required for cytolytic granule exocytosis in human NK cells. J. Exp. Med. 204: 2285-2291.
10. Fowler, K. T., N. W. Andrews, and J. W. Huleatt. 2007. Expression and function of synaptotagmin VII in CTLs. J. Immunol. 178: 1498-1504.
11. Feldmann, J., I. Callebaut, G. Raposo, S. Certain, D. Bacq, C. Dumont, N. Lambert, M. Ouachée-Chardin, G. Chedeville, H. Tamary, et al. 2003. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 115: 461-473.
12. Ménager, M. M., G. Ménasché, M. Romao, P. Knapnougel, C.-H. Ho, M. Garfa, G. Raposo, J. Feldmann, A. Fischer, and G. de Saint Basile. 2007. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat. Immunol. 8: 257-267.
13. Groffen, A. J., S. Martens, R. Díez Arazola, L. N. Cornelisse, N. Lozovaya, A. P. de Jong, N. A. Goriounova, R. L. Habets, Y. Takai, J. G. Borst, et al. 2010. Doc2b is a high-affinity Ca2+ sensor for spontaneous neurotransmitter release. Science 327: 1614-1618.
14. Topham, N. J., and E. W. Hewitt. 2009. Natural killer cell cytotoxicity: how do they pull the trigger? Immunology 128: 7-15.
15. Deguine, J., B. Breart, F. Lemaître, J. P. Di Santo, and P. Bousso. 2010. Intravital imaging reveals distinct dynamics for natural killer and CD8(+) T cells during tumor regression. Immunity 33: 632-644.
16. Campbell, P. D., E. Estella, N. L. Dudek, G. Jhala, H. E. Thomas, T. W. Kay, and S. I. Mannering. 2008. Cytotoxic T-lymphocyte-mediated killing of human pancreatic islet cells in vitro. Hum. Immunol. 69: 543-551.
17. Mannering, S. I., J. A. Dromey, J. S. Morris, D. J. Thearle, K. P. Jensen, and L. C. Harrison. 2005. An efficient method for cloning human autoantigenspecific T cells. J. Immunol. Methods 298: 83-92.
18. 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.
19. Vanherberghen, B., P. E. Olofsson, E. Forslund, M. Sternberg-Simon, M. A. Khorshidi, S. Pacouret, K. Guldevall, M. Enqvist, K. J. Malmberg, R. Mehr, and B. Önfelt. 2013. Classification of human natural killer cells based on migration behavior and cytotoxic response. Blood 121: 1326-1334.
20. Opferman, J. T., B. T. Ober, R. Narayanan, and P. G. Ashton-Rickardt. 2001. Suicide induced by cytolytic activity controls the differentiation of memory CD8 (+) T lymphocytes. Int. Immunol. 13: 411-419.
21. Kupfer, A., S. J. Singer, and G. Dennert. 1986. On the mechanism of unidirectional killing in mixtures of two cytotoxic T lymphocytes: unidirectional polarization of cytoplasmic organelles and the membrane-associated cytoskeleton in the effector cell. J. Exp. Med. 163: 489-498.
22. Wiedemann, A., D. Depoil, M. Faroudi, and S. Valitutti. 2006. Cytotoxic T lymphocytes kill multiple targets simultaneously via spatiotemporal uncoupling of lytic and stimulatory synapses. Proc. Natl. Acad. Sci. USA 103: 10985-10990.
23. Kuhn, J. R., and M. Poenie. 2002. Dynamic polarization of the microtubule cytoskeleton during CTL-mediated killing. Immunity 16: 111-121.
24. Bertrand, F., S. Müller, K. H. Roh, C. Laurent, L. Dupré, and S. Valitutti. 2013. An initial and rapid step of lytic granule secretion precedes microtubule organizing center polarization at the cytotoxic T lymphocyte/target cell synapse. Proc. Natl. Acad. Sci. USA 110: 6073-6078.
25. Choi, P. J., and T. J. Mitchison. 2013. Imaging burst kinetics and spatial coordination during serial killing by single natural killer cells. Proc. Natl. Acad. Sci. USA 110: 6488-6493.
26. Balaji, K. N., N. Schaschke, W. Machleidt, M. Catalfamo, and P. A. Henkart. 2002. Surface cathepsin B protects cytotoxic lymphocytes from self-destruction after degranulation. J. Exp. Med. 196: 493-503.
27. Baran, K., A. Ciccone, C. Peters, H. Yagita, P. I. Bird, J. A. Villadangos, and J. A. Trapani. 2006. Cytotoxic T lymphocytes from cathepsin B-deficient mice survive normally in vitro and in vivo after encountering and killing target cells. J. Biol. Chem. 281: 30485-30491.