The immune synapse clears and excludes molecules above a size threshold

Nature Communications

Volumn 5, Issue , 2014, Pages

  Cartwright, Adam N R ^a,b   Griggs, Jeremy ^c   Davis, Daniel M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN; F ACTIN; LOW DENSITY LIPOPROTEIN; NANOBODY; ACTIN; MONOCLONAL ANTIBODY;

ANTIBODY; BRAIN; DRUG; IMMUNE SYSTEM; POLYMERIZATION; POLYSACCHARIDE; PROTEIN; THRESHOLD;

ARTICLE; CELL ACTIVATION; CELL FUNCTION; CELL SPREADING; CONFOCAL MICROSCOPY; CONJUGATE; CONTROLLED STUDY; DEPOLYMERIZATION; EFFECTOR CELL; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOLOGICAL SYNAPSE; MOLECULAR WEIGHT; NATURAL KILLER CELL; TARGET CELL; IMMUNOLOGY; METABOLISM; SECRETION (PROCESS); SIGNAL TRANSDUCTION;

ACTINS; ANTIBODIES, MONOCLONAL; DEXTRANS; HUMANS; IMMUNOLOGICAL SYNAPSES; KILLER CELLS, NATURAL; MICROSCOPY, FLUORESCENCE; SIGNAL TRANSDUCTION; SINGLE-DOMAIN ANTIBODIES;

EID: 84923284407     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6479     Document Type: Article

References (39)

1. Lanier, L. L. NK cell recognition. Annu. Rev. Immunol. 23, 225-274 (2005).
2. Biron, C. A., Nguyen, K. B., Pien, G. C., Cousens, L. P. & Salazar-Mather, T. P. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17, 189-220 (1999).
3. Davis, D. M. & Dustin, M. L. What is the importance of the immunological synapse? Trends Immunol. 25, 323-327 (2004).
4. Orange, J. S. Formation and function of the lytic NK-cell immunological synapse. Nat. Rev. Immunol. 8, 713-725 (2008).
5. Pipkin, M. E. & Lieberman, J. Delivering the kiss of death: progress on understanding how perforin works. Curr. Opin. Immunol. 19, 301-308 (2007).
6. Long, E. O., Kim, H. S., Liu, D., Peterson, M. E. & Rajagopalan, S. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu. Rev. Immunol. 31, 227-258 (2013).
7. Culley, F. J. et al. Natural killer cell signal integration balances synapse symmetry and migration. PLoS Biol. 7, e1000159 (2009).
8. Davis, D. M. Mechanisms and functions for the duration of intercellular contacts made by lymphocytes. Nat. Rev. Immunol. 9, 543-555 (2009).
9. Schlesinger, B. C. & Cheng, L. Characterization of a novel monoclonal antibody against human perforin using transfected cell lines. Immunology 81, 291-295 (1994).
10. Armstrong, J. K., Wenby, R. B., Meiselman, H. J. & Fisher, T. C. The hydrodynamic radii of macromolecules and their effect on red blood cell aggregation. Biophys. J. 87, 4259-4270 (2004).
11. Thorne, R. G. & Nicholson, C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc. Natl Acad. Sci. USA 103, 5567-5572 (2006).
12. Shimizu, Y. & DeMars, R. Production of human cells expressing individual transferred HLA-A,-B,-C genes using an HLA-A,-B,-C null human cell line. J. Immunol. 142, 3320-3328 (1989).
13. McCann, F. E. et al. 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, 2862-2870 (2003).
14. Davis, D. M. et al. The human natural killer cell immune synapse. Proc. Natl Acad. Sci. USA 96, 15062-15067 (1999).
15. Davis, D. M. et al. The transmembrane sequence of human histocompatibility leukocyte antigen (HLA)-C as a determinant in inhibition of a subset of natural killer cells. J. Exp. Med. 189, 1265-1274 (1999).
16. Grakoui, A. et al. The immunological synapse: a molecular machine controlling T cell activation. Science 285, 221-227 (1999).
17. James, J. R. & Vale, R. D. Biophysical mechanism of T-cell receptor triggering in a reconstituted system. Nature 487, 64-69 (2012).
18. Davis, S. J. et al. The nature of molecular recognition by T cells. Nat. Immunol. 4, 217-224 (2003).
19. Brown, A. C. et al. Remodelling of cortical actin where lytic granules dock at natural killer cell immune synapses revealed by super-resolution microscopy. PLoS Biol. 9, e1001152 (2011).
20. Vyas, Y. M. et al. Spatial organization of signal transduction molecules in the NK cell immune synapses during MHC class I-regulated noncytolytic and cytolytic interactions. J. Immunol. 167, 4358-4367 (2001).
21. Orange, J. S. et al. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc. Natl Acad. Sci. USA 100, 14151-14156 (2003).
22. Rak, G. D., Mace, E. M., Banerjee, P. P., Svitkina, T. & Orange, J. S. Natural killer cell lytic granule secretion occurs through a pervasive actin network at the immune synapse. PLoS Biol. 9, e1001151 (2011).
23. Yarmola, E. G., Somasundaram, T., Boring, T. A., Spector, I. & Bubb, M. R. Actin-latrunculin A structure and function. Differential modulation of actinbinding protein function by latrunculin A. J. Biol. Chem. 275, 28120-28127 (2000).
24. Visegrady, B., Lorinczy, D., Hild, G., Somogyi, B. & Nyitrai, M. The effect of phalloidin and jasplakinolide on the flexibility and thermal stability of actin filaments. FEBS Lett. 565, 163-166 (2004).
25. Harris, L. J., Larson, S. B., Hasel, K. W. & McPherson, A. Refined structure of an intact IgG2a monoclonal antibody. Biochemistry 36, 1581-1597 (1997).
26. Vranken, W. et al. Solution structure of a llama single-domain antibody with hydrophobic residues typical of the VH/VL interface. Biochemistry 41, 8570-8579 (2002).
27. Tschopp, J., Masson, D. & Schafer, S. Inhibition of the lytic activity of perforin by lipoproteins. J. Immunol. 137, 1950-1953 (1986).
28. Rajman, I., Eacho, P. I., Chowienczyk, P. J. & Ritter, J. M. LDL particle size: an important drug target? Br. J. Clin. Pharmacol. 48, 125-133 (1999).
29. Burroughs, N. J. et al. Boltzmann energy-based image analysis demonstrates that extracellular domain size differences explain protein segregation at immune synapses. PLoS Comput. Biol. 7, e1002076 (2011).
30. Yin, Y., Wang, X. X. & Mariuzza, R. A. Crystal structure of a complete ternary complex of T-cell receptor, peptide-MHC, and CD4. Proc. Natl Acad. Sci. USA 109, 5405-5410 (2012).
31. Alakoskela, J. M. et al. Mechanisms for size-dependent protein segregation at immune synapses assessed with molecular rulers. Biophys. J. 100, 2865-2874 (2011).
32. Qi, S. Y., Groves, J. T. & Chakraborty, A. K. Synaptic pattern formation during cellular recognition. Proc. Natl Acad. Sci. USA 98, 6548-6553 (2001).
33. Davis, S. J. & van der Merwe, P. A. The kinetic-segregation model: TCR triggering and beyond. Nat. Immunol. 7, 803-809 (2006).
34. Kohler, K. et al. Matched sizes of activating and inhibitory receptor/ligand pairs are required for optimal signal integration by human natural killer cells. PLoS ONE 5, e15374 (2010).
35. Metkar, S. S. et al. Cytotoxic cell granule-mediated apoptosis: perforin delivers granzyme B-serglycin complexes into target cells without plasma membrane pore formation. Immunity 16, 417-428 (2002).
36. Sanderson, N. S. et al. Cytotoxic immunological synapses do not restrict the action of interferon-gamma to antigenic target cells. Proc. Natl Acad. Sci. USA 109, 7835-7840 (2012).
37. Ealick, S. E. et al. Three-dimensional structure of recombinant human interferon-gamma. Science 252, 698-702 (1991).
38. Young, J. D., Damiano, A., DiNome, M. A., Leong, L. G. & Cohn, Z. A. Dissociation of membrane binding and lytic activities of the lymphocyte poreforming protein (perforin). J. Exp. Med. 165, 1371-1382 (1987).
39. Walker, A. et al. Single domain antibodies against the collagen signalling receptor glycoprotein VI are inhibitors of collagen induced thrombus formation. Platelets 20, 268-276 (2009).