Cytotoxic T lymphocyte effector function is independent of nucleus-centrosome dissociation

European Journal of Immunology

Volumn 42, Issue 8, 2012, Pages 2132-2141

  Lui Roberts, Winnie W Y ^a   Stinchcombe, Jane C ^a   Ritter, Alex T ^a   Akhmanova, Anna ^b   Karakesisoglou, Iakowos ^c   Griffiths, Gillian M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UTRECHT UNIVERSITY   (Netherlands)

^c DURHAM UNIVERSITY   (United Kingdom)

Author keywords

Centrosome; Cytotoxic T lymphocytes; Immunological synapse; Nucleus; Polarization

Indexed keywords

CELL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; NESPRIN 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL KILLING; CELL MIGRATION; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL POLARITY; CELL TYPE; CENTRAL SUPRAMOLECULAR ACTIVATION COMPLEX; CENTROSOME; COMPLEX FORMATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; GENETIC TRANSFECTION; GRANULE CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOLOGICAL SYNAPSE; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE;

ANIMALS; CELL NUCLEUS; CELL POLARITY; CELLS, CULTURED; CENTROSOME; CYTOPLASMIC GRANULES; GENE TRANSFER TECHNIQUES; IMMUNOLOGICAL SYNAPSES; MEMBRANE PROTEINS; MICE; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84864740473     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242525     Document Type: Article

References (35)

1. Monks, C. R., Freiberg, B. A., Kupfer, H., Sciaky, N. and Kupfer, A., Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 1998. 395: 82-86.
2. Freiberg, B. A., Kupfer, H., Maslanik, W., Delli, J., Kappler, J., Zaller, D. M. and Kupfer, A., Staging and resetting T-cell activation in SMACs. Nat. Immunol. 2002. 3: 911-917.
3. Stinchcombe, J. C. and Griffiths, G. M., Normal and abnormal secretion by haemopoietic cells. Immunology 2001. 103: 10-16.
4. Stinchcombe, J. C., Majorovits, E., Bossi, G., Fuller, S. and Griffiths, G. M., Centrosome polarization delivers secretory granules to the immunological synapse. Nature 2006. 443: 462-465.
5. Kuhn, J. R. and Poenie, M., Dynamic polarization of the microtubule cytoskeleton during CTL-mediated killing. Immunity 2002. 16: 111-121.
6. Geiger, B., Rosen, D. and Berke, G., Spatial relationships of microtubule-organizing centers and the contact area of cytotoxic T lymphocytes and target cells. J. Cell Biol. 1982. 95: 137-143.
7. Kupfer, A., Singer, S. J. and Dennert, G., 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. 1986. 163: 489-498.
8. Tsun, A., Qureshi, I., Stinchcombe, J. C., Jenkins, M. R., de la Roche, M., Kleczkowska, J., Zamoyska, R. et al., Centrosome docking at the immunological synapse is controlled by Lck signaling. J. Cell Biol. 2011. 192: 663-674.
9. Tamm, S. and Tamm, S. L., Development of macrociliary cells in Beroe. I. Actin bundles and centriole migration. J. Cell Sci. 1988. 89(Pt 1): 67-80.
10. Boisvieux-Ulrich, E., Laine, M. C. and Sandoz, D., In vitro effects of benzodiazepines on ciliogenesis in the quail oviduct. Cell Motil. Cytoskeleton 1987. 8: 333-344.
11. Boisvieux-Ulrich, E., Laine, M. C. and Sandoz, D., Cytochalasin D inhibits basal body migration and ciliary elongation in quail oviduct epithelium. Cell Tissue Res. 1990. 259: 443-454.
12. McGee, M. D., Rillo, R., Anderson, A. S. and Starr, D. A., UNC-83 is a KASH protein required for nuclear migration and is recruited to the outer nuclear membrane by a physical interaction with the SUN protein UNC-84. Mol. Biol. Cell 2006. 17: 1790-1801.
13. Zhang, X., Lei, K., Yuan, X., Wu, X., Zhuang, Y., Xu, T., Xu, R. et al., SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 2009. 64: 173-187.
14. Razafsky, D. and Hodzic, D., Bringing KASH under the SUN: the many faces of nucleocytoskeletal connections. J. Cell Biol. 2009. 186: 461-472.
15. Hoogenraad, C. C., Wulf, P., Schiefermeier, N., Stepanova, T., Galjart, N., Small, J. V., Grosveld, F. et al., Bicaudal D induces selective dynein-mediated microtubule minus end-directed transport. Embo. J. 2003. 22: 6004-6015.
16. Splinter, D., Tanenbaum, M. E., Lindqvist, A., Jaarsma, D., Flotho, A., Yu, K. L., Grigoriev, I. et al., Bicaudal D2, dynein, and kinesin-1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLoS Biol. 2010. 8: e1000350.
17. Dustin, M. L., Bromley, S. K., Kan, Z., Peterson, D. A. and Unanue, E. R., Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc. Natl. Acad. Sci. USA 1997. 94: 3909-3913.
18. Ratner, S., Sherrod, W. S. and Lichlyter, D., Microtubule retraction into the uropod and its role in T-cell polarization and motility. J. Immunol. 1997. 159: 1063-1067.
19. Hogquist, K. A., Jameson, S. C., Heath, W. R., Howard, J. L., Bevan, M. J. and Carbone, F. R., T-cell receptor antagonist peptides induce positive selection. Cell 1994. 76: 17-27.
20. Stinchcombe, J. C. and Griffiths, G. M., Secretory mechanisms in cell-mediated cytotoxicity. Annu. Rev. Cell Dev. Biol. 2007. 23: 495-517.
21. Gillingham, A. K. and Munro, S., The PACT domain, a conserved centrosomal targeting motif in the coiled-coil proteins AKAP450 and pericentrin. EMBO Rep. 2000. 1: 524-529.
22. Feldmann, J., Callebaut, I., Raposo, G., Certain, S., Bacq, D., Dumont, C., Lambert, N. et al., Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 2003. 115: 461-473.
23. Schneider, M., Lu, W., Neumann, S., Brachner, A., Gotzmann, J., Noegel, A. A. and Karakesisoglou, I., Molecular mechanisms of centrosome and cytoskeleton anchorage at the nuclear envelope. Cell Mol. Life Sci. 2011. 68: 1593-1610.
24. Jenkins, M. R., Tsun, A., Stinchcombe, J. C. and Griffiths, G. M., The strength of T-cell receptor signal controls the polarization of cytotoxic machinery to the immunological synapse. Immunity 2009. 31: 621-631.
25. Clark, R. H., Stinchcombe, J. C., Day, A., Blott, E., Booth, S., Bossi, G., Hamblin, T. et al., Adaptor protein 3-dependent microtubule-mediated movement of lytic granules to the immunological synapse. Nat. Immunol. 2003. 4: 1111-1120.
26. Daniele, T., Hackmann, Y., Ritter, A. T., Wenham, M., Booth, S., Bossi, G., Schintler, M. et al., A role for Rab7 in the movement of secretory granules in cytotoxic T lymphocytes. Traffic 2011. 12: 902-911.
27. Haddad, E. K., Wu, X., Hammer, J. A., 3rd and Henkart, P. A., Defective granule exocytosis in Rab27a-deficient lymphocytes from Ashen mice. J. Cell Biol. 2001. 152: 835-842.
28. Menasche, G., Pastural, E., Feldmann, J., Certain, S., Ersoy, F., Dupuis, S., Wulffraat, N. et al., Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nat. Genet. 2000. 25: 173-176.
29. Stinchcombe, J. C., Barral, D. C., Mules, E. H., Booth, S., Hume, A. N., Machesky, L. M., Seabra, M. C. et al., Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J. Cell Biol. 2001. 152: 825-834.
30. Arneson, L. N., Brickshawana, A., Segovis, C. M., Schoon, R. A., Dick, C. J. and Leibson, P. J., Cutting edge: syntaxin 11 regulates lymphocyte-mediated secretion and cytotoxicity. J. Immunol. 2007. 179: 3397-3401.
31. Bryceson, Y. T., Rudd, E., Zheng, C., Edner, J., Ma, D., Wood, S. M., Bechensteen, A. G. et al., Defective cytotoxic lymphocyte degranulation in syntaxin-11 deficient familial hemophagocytic lymphohistiocytosis 4 (FHL4) patients. Blood 2007. 110: 1906-1915.
32. Cote, M., Menager, M. M., Burgess, A., Mahlaoui, N., Picard, C., Schaffner, C., Al-Manjomi, F. et al., Munc18-2 deficiency causes familial hemophagocytic lymphohistiocytosis type 5 and impairs cytotoxic granule exocytosis in patient NK cells. J. Clin. Invest. 2009. 119: 3765-3773.
33. zur Stadt, U., Rohr, J., Seifert, W., Koch, F., Grieve, S., Pagel, J., Strauss, J. et al., Familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) is caused by mutations in Munc18-2 and impaired binding to syntaxin 11. Am. J. Hum. Genet. 2009. 85: 482-492.
34. Malone, C. J., Misner, L., Le Bot, N., Tsai, M. C., Campbell, J. M., Ahringer, J. and White, J. G., The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 2003. 115: 825-836.
35. Friedl, P. and Weigelin, B., Interstitial leukocyte migration and immune function. Nat. Immunol. 2008. 9: 960-969.