Controversy and consensus regarding myosin II function at the immunological synapse

Current Opinion in Immunology

Volumn 25, Issue 3, 2013, Pages 300-306

  Hammer, John A ^a   Burkhardt, Janis K ^b  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CD4 ANTIGEN; CD8 ANTIGEN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; SMALL INTERFERING RNA; T LYMPHOCYTE RECEPTOR;

CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL TRANSPORT; HUMAN; IMMUNOLOGICAL SYNAPSE; INTRACELLULAR SIGNALING; LAMELLAR BODY; LYMPHOCYTE MIGRATION; MECHANOTRANSDUCTION; MESENCHYME CELL; NONHUMAN; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; T LYMPHOCYTE ACTIVATION;

ANIMALS; HUMANS; IMMUNOLOGICAL SYNAPSES; LYMPHOCYTE ACTIVATION; MYOSIN TYPE II; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84879233655     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2013.03.010     Document Type: Review

References (53)

1. Dustin M.L., Chakraborty A.K., Shaw A.S. Understanding the structure and function of the immunological synapse. Cold Spring Harb Perspect Biol 2010, 2:a002311.
2. Grakoui A., Bromley S.K., Sumen C., Davis M.M., Shaw A.S., Allen P.M., Dustin M.L. The immunological synapse: a molecular machine controlling T cell activation. Science 1999, 285:221-227.
3. Bunnell S.C., Kapoor V., Trible R.P., Zhang W., Samelson L.E. Dynamic actin polymerization drives T cell receptor-induced spreading: a role for the signal transduction adaptor LAT. Immunity 2001, 14:315-329.
4. Burkhardt J.K., Carrizosa E., Shaffer M.H. The actin cytoskeleton in T cell activation. Annu Rev Immunol 2008, 26:233-259.
5. Dustin M.L., Groves J.T. Receptor signaling clusters in the immune synapse. Annu Rev Biophys 2012, 41:543-556.
6. Yokosuka T., Saito T. The immunological synapse, TCR microclusters, and T cell activation. Curr Top Microbiol Immunol 2010, 340:81-107.
7. Yokosuka T., Sakata-Sogawa K., Kobayashi W., Hiroshima M., Hashimoto-Tane A., Tokunaga M., Dustin M.L., Saito T. Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat Immunol 2005, 6:1253-1262.
8. Monks C.R., Freiberg B.A., Kupfer H., Sciaky N., Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 1998, 395:82-86.
9. Varma R., Campi G., Yokosuka T., Saito T., Dustin M.L. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 2006, 25:117-127.
10. Ponti A., Machacek M., Gupton S.L., Waterman-Storer C.M., Danuser G. Two distinct actin networks drive the protrusion of migrating cells. Science 2004, 305:1782-1786.
11. Yam P.T., Wilson C.A., Ji L., Hebert B., Barnhart E.L., Dye N.A., Wiseman P.W., Danuser G., Theriot J.A. Actin-myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility. J Cell Biol 2007, 178:1207-1221.
12. Wilson C.A., Tsuchida M.A., Allen G.M., Barnhart E.L., Applegate K.T., Yam P.T., Ji L., Keren K., Danuser G., Theriot J.A. Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature 2010, 465:373-377.
13. Tojkander S., Gateva G., Schevzov G., Hotulainen P., Naumanen P., Martin C., Gunning P.W., Lappalainen P. A molecular pathway for myosin II recruitment to stress fibers. Curr Biol 2011, 21:539-550.
14. Higgs H.N., Pollard T.D. Regulation of actin polymerization by Arp2/3 complex and WASp/Scar proteins. J Biol Chem 1999, 274:32531-32534.
15. Pollard T.D., Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003, 112:453-465.
16. Lim J.I., Sabouri-Ghomi M., Machacek M., Waterman C.M., Danuser G. Protrusion and actin assembly are coupled to the organization of lamellar contractile structures. Exp Cell Res 2010, 316:2027-2041.
17. Anderson T.W., Vaughan A.N., Cramer L.P. Retrograde flow and myosin II activity within the leading cell edge deliver F-actin to the lamella to seed the formation of graded polarity actomyosin II filament bundles in migrating fibroblasts. Mol Biol Cell 2008, 19:5006-5018.
18. Tojkander S., Gateva G., Lappalainen P. Actin stress fibers-assembly, dynamics and biological roles. J Cell Sci 2012, 125:1855-1864.
19. Gomez T.S., Kumar K., Medeiros R.B., Shimizu Y., Leibson P.J., Billadeau D.D. Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse. Immunity 2007, 26:177-190.
20. Kaizuka Y., Douglass A.D., Varma R., Dustin M.L., Vale R.D. Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells. Proc Natl Acad Sci U S A 2007, 104:20296-20301.
21. Gomez T.S., McCarney S.D., Carrizosa E., Labno C.M., Comiskey E.O., Nolz J.C., Zhu P., Freedman B.D., Clark M.R., Rawlings D.J., et al. HS1 functions as an essential actin-regulatory adaptor protein at the immune synapse. Immunity 2006, 24:741-752.
22. Nolz J.C., Gomez T.S., Zhu P., Li S., Medeiros R.B., Shimizu Y., Burkhardt J.K., Freedman B.D., Billadeau D.D. The WAVE2 complex regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation. Curr Biol 2006, 16:24-34.
23. Dustin M.L. Cell adhesion molecules and actin cytoskeleton at immune synapses and kinapses. Curr Opin Cell Biol 2007, 19:529-533.
24. Dustin M.L. The cellular context of T cell signaling. Immunity 2009, 30:482-492.
25. 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 2011, 9:e1001151.
26. Brown A.C., Oddos S., Dobbie I.M., Alakoskela J.M., Parton R.M., Eissmann P., Neil M.A., Dunsby C., French P.M., Davis I., et al. Remodelling of cortical actin where lytic granules dock at natural killer cell immune synapses revealed by super-resolution microscopy. PLoS Biol 2011, 9:e1001152.
27. Yi J., Wu X.S., Crites T., Hammer J.A. Actin retrograde flow and acto-myosin II arc contraction drive receptor cluster dynamics at the immunological synapse in Jurkat T-cells. Mol Biol Cell 2012, 23:834-852.
28. Babich A., Li S., O'Connor R.S., Milone M.C., Freedman B.D., Burkhardt J.K. F-actin polymerization and retrograde flow drive sustained PLCgamma1 signaling during T cell activation. J Cell Biol 2012, 197:775-787.
29. Yu Y., Fay N.C., Smoligovets A.A., Wu H.J., Groves J.T. Myosin IIA modulates T cell receptor transport and CasL phosphorylation during early immunological synapse formation. PLoS ONE 2012, 7:e30704.
30. Sims T.N., Soos T.J., Xenias H.S., Dubin-Thaler B., Hofman J.M., Waite J.C., Cameron T.O., Thomas V.K., Varma R., Wiggins C.H., et al. Opposing effects of PKCtheta and WASp on symmetry breaking and relocation of the immunological synapse. Cell 2007, 129:773-785.
31. Jacobelli J., Chmura S.A., Buxton D.B., Davis M.M., Krummel M.F. A single class II myosin modulates T cell motility and stopping, but not synapse formation. Nat Immunol 2004, 5:531-538.
32. Barda-Saad M., Braiman A., Titerence R., Bunnell S.C., Barr V.A., Samelson L.E. Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat Immunol 2005, 6:80-89.
33. Bunnell S.C., Hong D.I., Kardon J.R., Yamazaki T., McGlade C.J., Barr V.A., Samelson L.E. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J Cell Biol 2002, 158:1263-1275.
34. Cai Y., Biais N., Giannone G., Tanase M., Jiang G., Hofman J.M., Wiggins C.H., Silberzan P., Buguin A., Ladoux B., et al. Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys J 2006, 91:3907-3920.
35. Giannone G., Dubin-Thaler B.J., Dobereiner H.G., Kieffer N., Bresnick A.R., Sheetz M.P. Periodic lamellipodial contractions correlate with rearward actin waves. Cell 2004, 116:431-443.
36. Kuo J.C., Han X., Hsiao C.T., Yates J.R., Waterman C.M. Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for beta-Pix in negative regulation of focal adhesion maturation. Nat Cell Biol 2011, 13:383-393.
37. Henson J.H., Svitkina T.M., Burns A.R., Hughes H.E., MacPartland K.J., Nazarian R., Borisy G.G. Two components of actin-based retrograde flow in sea urchin coelomocytes. Mol Biol Cell 1999, 10:4075-4090.
38. Hartman N.C., Nye J.A., Groves J.T. Cluster size regulates protein sorting in the immunological synapse. Proc Natl Acad Sci U S A 2009, 106:12729-12734.
39. DeMond A.L., Mossman K.D., Starr T., Dustin M.L., Groves J.T. T cell receptor microcluster transport through molecular mazes reveals mechanism of translocation. Biophys J 2008, 94:3286-3292.
40. Yu C.H., Wu H.J., Kaizuka Y., Vale R.D., Groves J.T. Altered actin centripetal retrograde flow in physically restricted immunological synapses. PLoS ONE 2010, 5:e11878.
41. Hashimoto-Tane A., Yokosuka T., Sakata-Sogawa K., Sakuma M., Ishihara C., Tokunaga M., Saito T. Dynein-driven transport of T cell receptor microclusters regulates immune synapse formation and T cell activation. Immunity 2011, 34:919-931.
42. Ilani T., Vasiliver-Shamis G., Vardhana S., Bretscher A., Dustin M.L. T cell antigen receptor signaling and immunological synapse stability require myosin IIA. Nat Immunol 2009, 10:531-539.
43. Jacobelli J., Bennett F.C., Pandurangi P., Tooley A.J., Krummel M.F. Myosin-IIA and ICAM-1 regulate the interchange between two distinct modes of T cell migration. J Immunol 2009, 182:2041-2050.
44. Beemiller P., Jacobelli J., Krummel M.F. Integration of the movement of signaling microclusters with cellular motility in immunological synapses. Nat Immunol 2012, 13:787-795.
45. Kumari S., Vardhana S., Cammer M., Curado S., Santos L., Sheetz M.P., Dustin M.L. T lymphocyte myosin IIA is required for maturation of the immunological synapse. Front Immunol 2012, 3:230.
46. Kolega J. Phototoxicity and photoinactivation of blebbistatin in UV and visible light. Biochem Biophys Res Commun 2004, 320:1020-1025.
47. Smyth J.T., Dehaven W.I., Bird G.S., Putney J.W. Ca2+-store-dependent and -independent reversal of Stim1 localization and function. J Cell Sci 2008, 121:762-772.
48. Dobereiner H.G., Dubin-Thaler B.J., Giannone G., Sheetz M.P. Force sensing and generation in cell phases: analyses of complex functions. J Appl Physiol 2005, 98:1542-1546.
49. Parsons J.T., Horwitz A.R., Schwartz M.A. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 2010, 11:633-643.
50. Morin N.A., Oakes P.W., Hyun Y.M., Lee D., Chin Y.E., King M.R., Springer T.A., Shimaoka M., Tang J.X., Reichner J.S., et al. Nonmuscle myosin heavy chain IIA mediates integrin LFA-1 de-adhesion during T lymphocyte migration. J Exp Med 2008, 205:195-205.
51. Judokusumo E., Tabdanov E., Kumari S., Dustin M.L., Kam L.C. Mechanosensing in T lymphocyte activation. Biophys J 2012, 102:L5-L7.
52. Straight A.F., Cheung A., Limouze J., Chen I., Westwood N.J., Sellers J.R., Mitchison T.J. Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 2003, 299:1743-1747.
53. Chen Q., Nag S., Pollard T.D. Formins filter modified actin subunits during processive elongation. J Struct Biol 2012, 177:32-39.