The actin cytoskeleton controls the efficiency of killer Ig-like receptor accumulation at inhibitory NK cell immune synapses

Journal of Immunology

Volumn 173, Issue 9, 2004, Pages 5617-5625

  Standeven, Leah J ^a   Carlin, Leo M ^b   Borszcz, Peter ^a   Davis, Daniel M ^b   Burshtyn, Deborah N ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CYTOCHALASIN D; GREEN FLUORESCENT PROTEIN; HLA C ANTIGEN; IMMUNOGLOBULIN RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; RECEPTOR PROTEIN; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ARTICLE; CHIMERA; CONJUGATION; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; EFFECTOR CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPSE; T LYMPHOCYTE; TARGET CELL;

EID: 6344275804     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.9.5617     Document Type: Article

References (47)

1. Cerwenka, A., and L. L. Lanier. 2001. Natural killer cells, viruses and cancer. Nat. Rev. Immunol. 1:41.
2. Lanier, L. L. 2001. On guard: activating NK cell receptors, Nat. Immunol. 2:23.
3. Moretta, A., C. Bottino, M. Vitale, D. Pende, C. Cantoni, M. C. Mingari, R. Biassoni, and L. Moretta. 2001. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 19:197.
4. Long, E. O., D. F. Barber, D. N. Burshtyn, M. Faure, M. Peterson, S. Rajagopalan, V. Renard, M. Sandusky, C. C. Stebbins, N. Wagtmann, and C. Watzl. 2001. Inhibition of natural killer cell activation signals by killer cell immunoglobulin-like receptors (CD158). Immunol. Rev. 181:223.
5. Long, E. O., D. N. Burshtyn, W. P. Clark, M. Peruzzi, S. Rajagopalan, S. Rojo, N. Wagtmann, and C. C. Winter. 1997. Killer cell inhibitory receptors: diversity, specificity, and function. Immunol. Rev. 155:135.
6. Ravetch, J. V., and L. L. Lanier. 2000. Immune inhibitory receptors. Science 290:84.
7. Bromley, S. K., W. R. Burack, K. G. Johnson, K. Somersalo, T. N. Sims, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 2001. The immunological synapse. Annu. Rev. Immunol. 19:375.
8. Dustin, M. L., and J. A. Cooper. 2000. The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling. Nat. Immunol. 1:23.
9. Vyas, Y. M., H. Maniar, and B. DuPont. 2002. Visualization of signaling pathways and cortical cytoskeleton in cytolytic and noncytolytic natural killer cell immune synapses. Immunol. Rev. 189:161.
10. Davis, D. M. 2002. Assembly of the immunological synapse for T cells and NK cells. Trends Immunol. 23:356.
11. Vyas, Y. M., K. M. Mehta, M. Morgan, H. Maniar, L. Butros, S. Jung, J. K. Burkhardt, and B. DuPont. 2001. Spatial organization of signal transduction molecules in the NK cell immune synapses during MHC class I-regulated non-cytolytic and cytolytic interactions. J. Immunol. 167:4358.
12. Davis, D. M., I. Chiu, M. Fassett, G. B. Cohen, O. Mandelboim, and J. L. Strominger. 1999. The human natural killer cell immune synapse. Proc. Natl. Acad. Sci. USA 96:15062.
13. McCann, F. E., B. Vanherberghen, K. Eleme, L. M. Carlin, R. J. Newsam, D. Goulding, and D. M. Davis. 2003. The size of the synaptic cleft and distinct distributions of filamentous actin, ezrin, CD43, and CD45 at activating and inhibitory human NK cell immune synapses. J. Immunol. 170:2862.
14. Borszcz, P. D., M. Peterson, L. Standeven, S. Kirwan, M. Sandusky, A. Shaw, E. O. Long, and D. N. Burshtyn. 2003. KIR enrichment at the effector-target cell interface is more sensitive than signaling to the strength of ligand binding. Eur. J. Immunol. 33:1084.
15. 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.
16. Fassett, M. S., D. M. Davis, M. M. Valter, G. B. Cohen, and J. L. Strominger. 2001. Signaling at the inhibitory natural killer cell immune synapse regulates lipid raft polarization but not class I MHC clustering. Proc. Natl. Acad. Sci. USA 98:14547.
17. Vyas, Y. M., H. Maniar, C. E. Lyddane, M. Sadelain, and B. DuPont. 2004. Ligand binding to inhibitory killer cell Ig-like receptors induce colocalization with SRC homology domain 2-containing protein tyrosine phosphatase 1 and interruption of ongoing activation signals. J. Immunol. 173:1571.
18. Vyas, Y. M., H. Maniar, and B. DuPont. 2002. Cutting edge: differential segregation of the SRC homology 2-containing protein tyrosine phosphatase-1 within the early NK cell immune synapse distinguishes noncytolytic from cytolytic interactions. J. Immunol. 168:3150.
19. Burshtyn, D. N., J. Shin, C. Stebbins, and E. O. Long. 2000. Adhesion to target cells is disrupted by the killer cell inhibitory receptor. Curr. Biol. 10:777.
20. Nakamura, M. C., E. C. Niemi, M. J. Fisher, L. D. Shultz, W. E. Seaman, and J. C. Ryan. 1997. Mouse Ly-49A interrupts early signaling events in natural killer cell cytotoxicity and functionally associates with the SHP-1 tyrosine phosphatase. J. Exp. Med 185:673.
21. Litwin, V., J. Gumperz, P. Parham, J. H. Phillips, and L. L. Lanier. 1993. Specificity of HLA class I antigen recognition by human NK clones: evidence for clonal heterogeneity, protection by self and non-self alleles, and influence of the target cell type. J. Exp. Med. 178:1321.
22. Cohen, G. B., R. T. Gandhi, D. M. Davis, O. Mandelboim, B. K. Chen, J. L. Strominger, and D. Baltimore. 1999. The selective down-regulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10:661.
23. Quan, P. C., T. Ishizaka, and B. R. Bloom. 1982. Studies on the mechanism of NK cell lysis. J. Immunol. 128:1786.
24. Katz, P., A. M. Zaytoun, and J. H. Lee, Jr. 1982. Mechanisms of human cell-mediated cytotoxicity. III. Dependence of natural killing on microtubule and microfilament integrity. J. Immunol. 129:2816.
25. Orange, J. S., N. Ramesh, E. Remold-O'Donnell, Y. Sasahara, L. Koopman, M. Byrne, F. A. Bonilla, F. S. Rosen, R. S. Geha, and J. L. Strominger. 2002. Wiskott-Aldrich syndrome protein is required for NK cell cytotoxicity and colocalizes with actin to NK cell-activating immunologic synapses. Proc. Natl. Acad. Sci. USA 99:11351.
26. Wulfing, C., B. Purtic, J. Klem, and J. D. Schatzte. 2003. Stepwise cytoskeletal polarization as a series of checkpoints in innate but not adaptive cytolytic killing. Proc. Natl. Acad. Sci. USA 100:7767.
27. Kucik, D. F., M. L. Dustin, J. M. Miller, and E. J. Brown. 1996. Adhesion-activating phorbol ester increases the mobility of leukocyte integrin LFA-1 in cultured lymphocytes. J. Clin. Invest. 97:2139.
28. Yauch, R. L., D. P. Felsenfeld, S. K. Kraeft, L. B. Chen, M. P. Sheetz, and M. E. Hemler. 1997. Mutational evidence for control of cell adhesion through integrin diffusion/clustering, independent of ligand binding. J. Exp. Med. 186:1347.
29. Wakatsuki, T., B. Schwab, N. C. Thompson, and E. L. Elson. 2001. Effects of cytochalasin D and latrunculin B on mechanical properties of cells. J. Cell Sci. 114:1025.
30. Verkhovsky, A. B., T. M. Svitkina, and G. G. Borisy. 1997. Polarity sorting of actin filaments in cytochalasin-treated fibroblasts. J. Cell Sci. 110:1693.
31. Dietrich, J., M. Cella, and M. Colonna. 2001. Ig-like transcript 2 (ILT2)/leukocyte Ig-like receptor 1 (LIR1) inhibits TCR signaling and actin cytoskeleton reorganization. J. Immunol. 166:2514.
32. Stebbins, C. C., C. Watzl, D. D. Billadeau, P. J. Leibson, D. N. Burshtyn, and E. O. Long. 2003. Vav1 dephosphorylation by the tyrosine phosphatase SHP-1 as a mechanism for inhibition of cellular cytotoxicity. Mol. Cell. Biol. 23:6291.
33. Wulfing, C., and M. M. Davis. 1998. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282:2266.
34. 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.
35. Matter, A. 1979. Microcinematographic and electron microscopic analysis of target cell lysis induced by cytotoxic T lymphocytes. Immunology 36:179.
36. Rothstein, T. L., M. Mage, G. Jones, and L. L. McHugh. 1978. Cytotoxic T lymphocyte sequential killing of immobilized allogeneic tumor target cells measured by time-lapse microcinematography. J. Immunol. 121:1652.
37. Sanderson, C. J. 1976. The mechanism of T cell mediated cytotoxicity. II. Morphological studies of cell death by time-lapse microcinematography. Proc. R. Soc. Land. B Biol. Sci. 192:241.
38. Samstag, Y., S. M. Eibert, M. Klemke, and G. H. Wabnitz. 2003. Actin cytoskeletal dynamics in T lymphocyte activation and migration. J. Leukocyte Biol. 73:30.
39. Bustelo, X. R. 2000. Regulatory and signaling properties of the Vav family. Mol. Cell. Biol. 20:1461.
40. Higgs, H. N., and T. D. Pollard. 2001. Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70:649.
41. Maekawa, M., T. Ishizaki, S. Boku, N. Watanabe, A. Fujita, A. Iwamatsu, T. Obinata, K. Ohashi, K. Mizuno, and S. Narumiya. 1999. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285:895.
42. Edwards, D. C., L. C. Sanders, G. M. Bokoch, and G. N. Gill. 1999. Activation of LIM-kinase by Pak 1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell Biol. 1:253.
43. Khurana, D., and P. J. Leibson. 2003. Regulation of lymphocyte-mediated killing by GTP-binding proteins. J. Leukocyte Biol. 73:333.
44. 2 integrin engagement on natural killer cells upstream of actin cytoskeleton and lipid raft reorganization. J. Exp. Med. 198:469.
45. Badour, K., J. Zhang, F. Shi, M. K. McGavin, V. Rampersad, L. A. Hardy, D. Field, and K. A. Siminovitch. 2003. The Wiskott-Aldrich syndrome protein acts downstream of CD2 and the CD2AP and PSTPIP1 adaptors to promote formation of the immunological synapse. Immunity 18:141.
46. Maki, G., H. G. Klingemann, J. A. Martinson, and Y. K. Tam. 2001. Factors regulating the cytotoxic activity of the human natural killer cell line, NK-92. J. Hematother. Stem Cell Res. 10:369.
47. Faure, M., D. F. Barber, S. M. Takahashi, T. Jin, and E. O. Long. 2003. Spontaneous clustering and tyrosine phosphorylation of NK cell inhibitory receptor induced by ligand binding. J. Immunol. 170:6107.