F-actin polymerization and retrograde flow drive sustained PLCγ1 signaling during T cell activation

Journal of Cell Biology

Volumn 197, Issue 6, 2012, Pages 775-787

  Babich, Alexander ^a,b   Li, Shuixing ^a   O'Connor, Roddy S ^a,b   Milone, Michael C ^a,b   Freedman, Bruce D ^c   Burkhardt, Janis K ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; F ACTIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN IIA; PHOSPHOLIPASE C GAMMA1;

ACTIN POLYMERIZATION; ACTIN RETROGRADE FLOW; ARTICLE; CELL ACTIVATION; CENTRALIZATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME PHOSPHORYLATION; FLOW KINETICS; HUMAN; HUMAN CELL; IMMUNOLOGICAL SYNAPSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ACTINS; CELL MOVEMENT; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; NONMUSCLE MYOSIN TYPE IIA; PHOSPHOLIPASE C GAMMA; POLYMERIZATION; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSFECTION; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 84863992208     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201201018     Document Type: Article

References (53)

1. Alon, R., and M.L. Dustin. 2007. Force as a facilitator of integrin conformational changes during leukocyte arrest on blood vessels and antigen-presenting cells. Immunity. 26:17-27. http://dx.doi.org/10.1016/j.immuni.2007.01.002
2. Baker, R.G., C.J. Hsu, D. Lee, M.S. Jordan, J.S. Maltzman, D.A. Hammer, T. Baumgart, and G.A. Koretzky. 2009. The adapter protein SLP-76 mediates "outside-in" integrin signaling and function in T cells. Mol. Cell. Biol. 29:5578-5589. http://dx.doi.org/10.1128/MCB.00283-09
3. Beemiller, P., and M.F. Krummel. 2010. Mediation of T-cell activation by actin meshworks. Cold Spring Harb. Perspect. Biol. 2:a002444. http://dx.doi.org/10.1101/cshperspect.a002444
4. Bubb, M.R., A.M. Senderowicz, E.A. Sausville, K.L. Duncan, and E.D. Korn. 1994. Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J. Biol. Chem. 269:14869-14871.
5. Bunnell, S.C., V. Kapoor, R.P. Trible, W. Zhang, and L.E. Samelson. 2001. Dynamic actin polymerization drives T cell receptor-induced spreading: A role for the signal transduction adaptor LAT. Immunity. 14:315-329. http://dx.doi.org/10.1016/S1074-7613(01)00112-1
6. Bunnell, S.C., D.I. Hong, J.R. Kardon, T. Yamazaki, C.J. McGlade, V.A. Barr, and L.E. Samelson. 2002. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 158:1263-1275. http://dx.doi.org/10.1083/jcb.200203043
7. Bunnell, S.C., V.A. Barr, C.L. Fuller, and L.E. Samelson. 2003. High-resolution multicolor imaging of dynamic signaling complexes in T cells stimulated by planar substrates. Sci. STKE. 2003:PL8. http://dx.doi.org/10.1126/stke.2003.177.pl8
8. Bunnell, S.C., A.L. Singer, D.I. Hong, B.H. Jacque, M.S. Jordan, M.C. Seminario, V.A. Barr, G.A. Koretzky, and L.E. Samelson. 2006. Persistence of cooperatively stabilized signaling clusters drives T-cell activation. Mol. Cell. Biol. 26:7155-7166. http://dx.doi.org/10.1128/MCB.00507-06
9. Burkhardt, J.K., E. Carrizosa, and M.H. Shaffer. 2008. The actin cytoskeleton in T cell activation. Annu. Rev. Immunol. 26:233-259. http://dx.doi.org/10.1146/annurev.immunol.26.021607.090347
10. Cai, Y., N. Biais, G. Giannone, M. Tanase, G. Jiang, J.M. Hofman, C.H. Wiggins, P. Silberzan, A. Buguin, B. Ladoux, and M.P. Sheetz. 2006. Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys. J. 91:3907-3920. http://dx.doi.org/10.1529/biophysj.106.084806
11. Campi, G., R. Varma, and M.L. Dustin. 2005. Actin and agonist MHC-peptide complex-dependent T cell receptor microclusters as scaffolds for signaling. J. Exp. Med. 202:1031-1036. http://dx.doi.org/10.1084/jem.20051182
12. Carrizosa, E., T.S. Gomez, C.M. Labno, D.A. Klos Dehring, X. Liu, B.D. Freedman, D.D. Billadeau, and J.K. Burkhardt. 2009. Hematopoietic lineage cell-specific protein 1 is recruited to the immunological synapse by IL-2-inducible T cell kinase and regulates phospholipase Cgamma1 Microcluster dynamics during T cell spreading. J. Immunol. 183:7352-7361. http://dx.doi.org/10.4049/jimmunol.0900973
13. Dehring, D.A., F. Clarke, B.G. Ricart, Y. Huang, T.S. Gomez, E.K. Williamson, D.A. Hammer, D.D. Billadeau, Y. Argon, and J.K. Burkhardt. 2011. Hematopoietic lineage cell-specific protein 1 functions in concert with the Wiskott-Aldrich syndrome protein to promote podosome array organization and chemotaxis in dendritic cells. J. Immunol. 186:4805-4818. http://dx.doi.org/10.4049/jimmunol.1003102
14. Gomez, T.S., S.D. McCarney, E. Carrizosa, C.M. Labno, E.O. Comiskey, J.C. Nolz, P. Zhu, B.D. Freedman, M.R. Clark, D.J. Rawlings, et al. 2006. HS1 functions as an essential actin-regulatory adaptor protein at the immune synapse. Immunity. 24:741-752. http://dx.doi.org/10.1016/j.immuni.2006.03.022
15. Gomez, T.S., K. Kumar, R.B. Medeiros, Y. Shimizu, P.J. Leibson, and D.D. Billadeau. 2007. Formins regulate the actin-related protein 2/3 complexindependent polarization of the centrosome to the immunological synapse. Immunity. 26:177-190. http://dx.doi.org/10.1016/j.immuni.2007.01.008
16. Grakoui, A., S.K. Bromley, C. Sumen, M.M. Davis, A.S. Shaw, P.M. Allen, and M.L. Dustin. 1999. The immunological synapse: A molecular machine controlling T cell activation. Science. 285:221-227. http://dx.doi.org/10.1126/science.285.5425.221
17. Hashimoto-Tane, A., T. Yokosuka, K. Sakata-Sogawa, M. Sakuma, C. Ishihara, M. Tokunaga, and T. Saito. 2011. Dynein-driven transport of T cell receptor microclusters regulates immune synapse formation and T cell activation. Immunity. 34:919-931. http://dx.doi.org/10.1016/j.immuni.2011.05.012
18. Houtman, J.C., Y. Higashimoto, N. Dimasi, S. Cho, H. Yamaguchi, B. Bowden, C. Regan, E.L. Malchiodi, R. Mariuzza, P. Schuck, et al. 2004. Binding specificity of multiprotein signaling complexes is determined by both cooperative interactions and affinity preferences. Biochemistry. 43:4170-4178. http://dx.doi.org/10.1021/bi0357311
19. Hsu, C.J., W.T. Hsieh, A. Waldman, F. Clarke, E.S. Huseby, J.K. Burkhardt, and T. Baumgart. 2012. Ligand mobility modulates immunological synapse formation and T cell activation. PLoS ONE. 7:e32398. http://dx.doi .org/10.1371/journal.pone.0032398
20. Ilani, T., G. Vasiliver-Shamis, S. Vardhana, A. Bretscher, and M.L. Dustin. 2009. T cell antigen receptor signaling and immunological synapse stability require myosin IIA. Nat. Immunol. 10:531-539. http://dx.doi.org/10.1038/ni.1723
21. Jacobelli, J., S.A. Chmura, D.B. Buxton, M.M. Davis, and M.F. Krummel. 2004. A single class II myosin modulates T cell motility and stopping, but not synapse formation. Nat. Immunol. 5:531-538. http://dx.doi.org/10.1038/ni1065
22. Jbireal, J.M., C. Strell, B. Niggemann, K. Zänker, and F. Entschladen. 2010. The selective role of myosin VI in lymphoid leukemia cell migration. Leuk. Res. 34:1656-1662. http://dx.doi.org/10.1016/j.leukres.2010.04.018
23. Johnson, H.W., and M.J. Schell. 2009. Neuronal IP3 3-kinase is an F-actin-bundling protein: Role in dendritic targeting and regulation of spine morphology. Mol. Biol. Cell. 20:5166-5180. http://dx.doi.org/10.1091/mbc.E09-01-0083
24. Kaizuka, Y., A.D. Douglass, R. Varma, M.L. Dustin, and R.D. Vale. 2007. Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells. Proc. Natl. Acad. Sci. USA. 104:20296-20301. http://dx.doi.org/10.1073/pnas.0710258105
25. Kim, H.K., J.W. Kim, A. Zilberstein, B. Margolis, J.G. Kim, J. Schlessinger, and S.G. Rhee. 1991. PDGF stimulation of inositol phospholipid hydrolysis requires PLC-gamma 1 phosphorylation on tyrosine residues 783 and 1254. Cell. 65:435-441. http://dx.doi.org/10.1016/0092-8674(91)90461-7
26. Kim, S.T., K. Takeuchi, Z.Y. Sun, M. Touma, C.E. Castro, A. Fahmy, M.J. Lang, G. Wagner, and E.L. Reinherz. 2009. The alphabeta T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 284:31028-31037. http://dx.doi.org/10.1074/jbc.M109.052712
27. Lasserre, R., and A. Alcover. 2010. Cytoskeletal cross-talk in the control of T cell antigen receptor signaling. FEBS Lett. 584:4845-4850. http://dx.doi.org/10.1016/j.febslet.2010.09.001
28. Lasserre, R., S. Charrin, C. Cuche, A. Danckaert, M.I. Thoulouze, F. de Chaumont, T. Duong, N. Perrault, N. Varin-Blank, J.C. Olivo-Marin, et al. 2010. Ezrin tunes T-cell activation by controlling Dlg1 and microtubule positioning at the immunological synapse. EMBO J. 29:2301-2314. http://dx.doi.org/10.1038/emboj.2010.127
29. Lee, K.H., A.D. Holdorf, M.L. Dustin, A.C. Chan, P.M. Allen, and A.S. Shaw. 2002. T cell receptor signaling precedes immunological synapse formation. Science. 295:1539-1542. http://dx.doi.org/10.1126/science.1067710
30. Li, Y.C., B.M. Chen, P.C. Wu, T.L. Cheng, L.S. Kao, M.H. Tao, A. Lieber, and S.R. Roffler. 2010. Cutting Edge: Mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling. J. Immunol. 184: 5959-5963. http://dx.doi.org/10.4049/jimmunol.0900775
31. Mossman, K.D., G. Campi, J.T. Groves, and M.L. Dustin. 2005. Altered TCR signaling from geometrically repatterned immunological synapses. Science. 310:1191-1193. http://dx.doi.org/10.1126/science.1119238
32. Mueller, P., A. Quintana, D. Griesemer, M. Hoth, and J. Pieters. 2007. Disruption of the cortical actin cytoskeleton does not affect store operated Ca2+ channels in human T-cells. FEBS Lett. 581:3557-3562. http://dx.doi.org/10.1016/j.febslet.2007.06.068
33. Negulescu, P.A., N. Shastri, and M.D. Cahalan. 1994. Intracellular calcium dependence of gene expression in single T lymphocytes. Proc. Natl. Acad. Sci. USA. 91:2873-2877. http://dx.doi.org/10.1073/pnas.91.7.2873
34. Nguyen, K., N.R. Sylvain, and S.C. Bunnell. 2008. T cell costimulation via the integrin VLA-4 inhibits the actin-dependent centralization of signaling microclusters containing the adaptor SLP-76. Immunity. 28:810-821. http://dx.doi.org/10.1016/j.immuni.2008.04.019
35. Nolz, J.C., T.S. Gomez, P. Zhu, S. Li, R.B. Medeiros, Y. Shimizu, J.K. Burkhardt, B.D. Freedman, and D.D. Billadeau. 2006. The WAVE2 complex regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation. Curr. Biol. 16:24-34. http://dx.doi.org/10.1016/j.cub.2005.11.036
36. Oh-hora, M. 2009. Calcium signaling in the development and function of T-lineage cells. Immunol. Rev. 231:210-224. http://dx.doi.org/10.1111/j.1600-065X .2009.00819.x Pollard, T.D., and J. Berro. 2009. Mathematical models and simulations of cellular processes based on actin filaments. J. Biol. Chem. 284:5433-5437. http://dx.doi.org/10.1074/jbc.R800043200
37. Pollard, T.D., and J. Berro. 2009. Mathematical models and simulations of cellular processes based on actin filaments. J. Biol. Chem. 284:5433-5437. http://dx.doi.org/10.1074/jbc.R800043200
38. Ponti, A., M. Machacek, S.L. Gupton, C.M. Waterman-Storer, and G. Danuser. 2004. Two distinct actin networks drive the protrusion of migrating cells. Science. 305:1782-1786. http://dx.doi.org/10.1126/science.1100533
39. Schnyder, T., A. Castello, C. Feest, N.E. Harwood, T. Oellerich, H. Urlaub, M. Engelke, J. Wienands, A. Bruckbauer, and F.D. Batista. 2011. B cell receptor-mediated antigen gathering requires ubiquitin ligase Cbl and adaptors Grb2 and Dok-3 to recruit dynein to the signaling microcluster. Immunity. 34:905-918. http://dx.doi.org/10.1016/j.immuni.2011.06.001
40. Sherman, E., V. Barr, S. Manley, G. Patterson, L. Balagopalan, I. Akpan, C.K. Regan, R.K. Merrill, C.L. Sommers, J. Lippincott-Schwartz, and L.E. Samelson. 2011. Functional nanoscale organization of signaling molecules downstream of the T cell antigen receptor. Immunity. 35:705-720. http://dx.doi.org/10.1016/j.immuni.2011.10.004
41. Straight, A.F., A. Cheung, J. Limouze, I. Chen, N.J. Westwood, J.R. Sellers, and T.J. Mitchison. 2003. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science. 299:1743-1747. http://dx.doi.org/10.1126/science.1081412
42. Ueda, K., M. Murata-Hori, M. Tatsuka, and H. Hosoya. 2002. Rho-kinase contributes to diphosphorylation of myosin II regulatory light chain in nonmuscle cells. Oncogene. 21:5852-5860. http://dx.doi.org/10.1038/sj.onc.1205747
43. Valitutti, S., D. Coombs, and L. Dupré. 2010. The space and time frames of T cell activation at the immunological synapse. FEBS Lett. 584:4851-4857. http://dx.doi.org/10.1016/j.febslet.2010.10.010
44. Varma, R., G. Campi, T. Yokosuka, T. Saito, and M.L. Dustin. 2006. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity. 25:117-127. http://dx.doi.org/10.1016/j.immuni.2006.04.010
45. Wei, Q., and R.S. Adelstein. 2000. Conditional expression of a truncated fragment of nonmuscle myosin II-A alters cell shape but not cytokinesis in HeLa cells. Mol. Biol. Cell. 11:3617-3627.
46. Wilson, C.A., M.A. Tsuchida, G.M. Allen, E.L. Barnhart, K.T. Applegate, P.T. Yam, L. Ji, K. Keren, G. Danuser, and J.A. Theriot. 2010. Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature. 465:373-377. http://dx.doi.org/10.1038/nature08994
47. Wülfing, C., and M.M. Davis. 1998. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science. 282:2266-2269. http:// dx.doi.org/10.1126/science.282.5397.2266
48. Yam, P.T., C.A. Wilson, L. Ji, B. Hebert, E.L. Barnhart, N.A. Dye, P.W. Wiseman, G. Danuser, and J.A. Theriot. 2007. Actin-myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility. J. Cell Biol. 178:1207-1221. http://dx.doi.org/10.1083/jcb.200706012
49. Yi, J., X.S. Wu, T. Crites, and J.A. Hammer III. 2012. Actin retrograde flow and actomyosin II arc contraction drive receptor cluster dynamics at the immunological synapse in Jurkat T cells. Mol. Biol. Cell. 23:834-852. http://dx.doi.org/10.1091/mbc.E11-08-0731
50. Yokosuka, T., K. Sakata-Sogawa, W. Kobayashi, M. Hiroshima, A. Hashimoto-Tane, M. Tokunaga, M.L. Dustin, and T. Saito. 2005. Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat. Immunol. 6:1253-1262. http://dx.doi.org/10.1038/ni1272
51. Yu, C.H., H.J. Wu, Y. Kaizuka, R.D. Vale, and J.T. Groves. 2010. Altered actin centripetal retrograde flow in physically restricted immunological synapses. PLoS ONE. 5:e11878. http://dx.doi.org/10.1371/journal.pone.0011878
52. Zhang, J., A. Shehabeldin, L.A. da Cruz, J. Butler, A.K. Somani, M. McGavin, I. Kozieradzki, A.O. dos Santos, A. Nagy, S. Grinstein, et al. 1999. Antigen receptor-induced activation and cytoskeletal rearrangement are impaired in Wiskott-Aldrich syndrome protein-deficient lymphocytes. J. Exp. Med. 190:1329-1342. http://dx.doi.org/10.1084/jem.190.9.1329
53. Zhao, Y., Z. Zheng, C.J. Cohen, L. Gattinoni, D.C. Palmer, N.P. Restifo, S.A. Rosenberg, and R.A. Morgan. 2006. High-efficiency transfection of primary human and mouse T lymphocytes using RNA electroporation. Mol. Ther. 13:151-159. http://dx.doi.org/10.1016/j.ymthe.2005.07.688