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Annual Review of Immunology

Volume 37, 2019

Origin, Organization, Dynamics, and Function of Actin and Actomyosin Networks at the T Cell Immunological Synapse

Abstract

The engagement of a T cell with an antigen-presenting cell (APC) or activating surface results in the formation within the T cell of several distinct actin and actomyosin networks. These networks reside largely within a narrow zone immediately under the T cell's plasma membrane at its site of contact with the APC or activating surface, i.e., at the immunological synapse. Here we review the origin, organization, dynamics, and function of these synapse-associated actin and actomyosin networks. Importantly, recent insights into the nature of these actin-based cytoskeletal structures were made possible in several cases by advances in light microscopy.

Keyword(s): actin, formin, immunological synapse, lytic granule, myosin, T cell

[Erratum, Closure]

An erratum has been published for this article:
Erratum: Origin, Organization, Dynamics, and Function of Actin and Actomyosin Networks at the T Cell Immunological Synapse
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/content/journals/10.1146/annurev-immunol-042718-041341
2019-04-26
2024-04-19
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Literature Cited

  1. 1.
    Cannon JL, Burkhardt JK 2002. The regulation of actin remodeling during T-cell-APC conjugate formation. Immunol. Rev. 186:190–99
     [Google Scholar]
  2. 2.
    Huang Y, Burkhardt JK 2007. T-cell-receptor-dependent actin regulatory mechanisms. J. Cell Sci. 120:5723–30
     [Google Scholar]
  3. 3.
    Billadeau DD, Nolz JC, Gomez TS 2007. Regulation of T-cell activation by the cytoskeleton. Nat. Rev. Immunol. 7:2131–43
     [Google Scholar]
  4. 4.
    Burkhardt JK, Carrizosa E, Shaffer MH 2008. The actin cytoskeleton in T cell activation. Annu. Rev. Immunol. 26:1233–59
     [Google Scholar]
  5. 5.
    Hammer JA, Burkhardt JK 2013. Controversy and consensus regarding myosin II function at the immunological synapse. Curr. Opin. Immunol. 25:3300–6
     [Google Scholar]
  6. 6.
    Burkhardt JK 2013. Cytoskeletal function in the immune system. Immunol. Rev. 256:15–9
     [Google Scholar]
  7. 7.
    Kumari S, Curado S, Mayya V, Dustin ML 2014. T cell antigen receptor activation and actin cytoskeleton remodeling. Biochim. Biophys. Acta Biomembr. 1838:2546–56
     [Google Scholar]
  8. 8.
    Le Floc'h A, Huse M 2015. Molecular mechanisms and functional implications of polarized actin remodeling at the T cell immunological synapse. Cell. Mol. Life Sci. 72:3537–56
     [Google Scholar]
  9. 9.
    Jankowska KI, Burkhardt JK 2017. Analyzing actin dynamics at the immunological synapse. Methods Mol. Biol. 1584:7–29
     [Google Scholar]
  10. 10.
    Ritter AT, Angus KL, Griffiths GM 2013. The role of the cytoskeleton at the immunological synapse. Immunol. Rev. 256:1107–17
     [Google Scholar]
  11. 11.
    Dustin ML, Baldari CT 2017. The immune synapse: past, present, and future. Methods Mol. Biol. 1584:1–5
     [Google Scholar]
  12. 12.
    Xie J, Tato CM, Davis MM 2013. How the immune system talks to itself: the varied role of synapses. Immunol. Rev. 251:165–79
     [Google Scholar]
  13. 13.
    Dustin ML, Starr T, Varma R, Thomas VK 2007. Supported planar bilayers for study of the immunological synapse. Curr. Protoc. Immunol. 76:1 18.13 1–35
     [Google Scholar]
  14. 14.
    Welch MD, Mullins RD 2002. Cellular control of actin nucleation. Annu. Rev. Cell Dev. Biol. 18:1247–88
     [Google Scholar]
  15. 15.
    Pollard TD, Borisy GG 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:4453–65
     [Google Scholar]
  16. 16.
    Pollard TD 2016. What we know and do not know about actin. The Actin Cytoskeleton: Handbook of Experimental Pharmacology BM Jockusch 331–47 Cham, Switz.: Springer
     [Google Scholar]
  17. 17.
    Kovar DR 2006. Molecular details of formin-mediated actin assembly. Curr. Opin. Cell Biol. 18:111–17
     [Google Scholar]
  18. 18.
    Chhabra ES, Higgs HN 2007. The many faces of actin: matching assembly factors with cellular structures. Nat. Cell Biol. 9:101110–21
     [Google Scholar]
  19. 19.
    Pollard TD 2007. Regulation of actin filament assembly by Arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36:1451–77
     [Google Scholar]
  20. 20.
    Kühn S, Geyer M 2014. Formins as effector proteins of Rho GTPases. Small GTPases 5:3e983876
     [Google Scholar]
  21. 21.
    Chesarone MA, Goode BL 2009. Actin nucleation and elongation factors: mechanisms and interplay. Curr. Opin. Cell Biol. 21:128–37
     [Google Scholar]
  22. 22.
    Swaney KF, Li R 2016. Function and regulation of the Arp2/3 complex during cell migration in diverse environments. Curr. Opin. Cell Biol. 42:63–72
     [Google Scholar]
  23. 23.
    Goode BL, Eck MJ 2007. Mechanism and function of formins in the control of actin assembly. Annu. Rev. Biochem. 76:593–627
     [Google Scholar]
  24. 24.
    Breitsprecher D, Goode BL 2013. Formins at a glance. J. Cell Sci. 126:11–7
     [Google Scholar]
  25. 25.
    Gomez TS, Kumar K, Medeiros RB, Shimizu Y, Leibson PJ, Billadeau DD 2007. Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse. Immunity 26:2177–90
     [Google Scholar]
  26. 26.
    Matalon O, Reicher B, Barda-Saad M 2013. Wiskott-Aldrich syndrome protein—dynamic regulation of actin homeostasis: from activation through function and signal termination in T lymphocytes. Immunol. Rev. 256:110–29
     [Google Scholar]
  27. 27.
    Alekhina O, Burstein E, Billadeau DD 2017. Cellular functions of WASP family proteins at a glance. J. Cell Sci. 130:142235–41
     [Google Scholar]
  28. 28.
    Chen Z, Borek D, Padrick SB, Gomez TS, Metlagel Z et al. 2010. Structure and control of the actin regulatory WAVE complex. Nature 468:7323533–38
     [Google Scholar]
  29. 29.
    Chen B, Chou H-T, Brautigam CA, Xing W, Yang S et al. 2017. Rac1 GTPase activates the WAVE regulatory complex through two distinct binding sites. eLife 6:1–22
     [Google Scholar]
  30. 30.
    Burke TA, Christensen JR, Barone E, Suarez C, Sirotkin V, Kovar DR 2014. Homeostatic actin cytoskeleton networks are regulated by assembly factor competition for monomers. Curr. Biol. 24:5579–85
     [Google Scholar]
  31. 31.
    Fritzsche M, Erlenkämper C, Moeendarbary E, Charras G, Kruse K 2016. Actin kinetics shapes cortical network structure and mechanics. Sci. Adv. 2:4e1501337
     [Google Scholar]
  32. 32.
    Rotty JD, Wu C, Haynes EM, Suarez C, Winkelman JD et al. 2015. Profilin-1 serves as a gatekeeper for actin assembly by Arp2/3-dependent and -independent pathways. Dev. Cell. 32:154–67
     [Google Scholar]
  33. 33.
    Lomakin AJ, Lee K, Han SJ, Bui DA, Davidson M et al. 2015. Competition for actin between two distinct F-actin networks defines a bistable switch for cell polarization. Nat. Cell Biol. 17:111435–45
     [Google Scholar]
  34. 34.
    Kanellos G, Frame MC 2016. Cellular functions of the ADF/cofilin family at a glance. J. Cell Sci. 129:173211–18
     [Google Scholar]
  35. 35.
    Roybal KT, Buck TE, Ruan X, Cho BH, Clark DJ et al. 2016. Computational spatiotemporal analysis identifies WAVE2 and cofilin as joint regulators of costimulation-mediated T cell actin dynamics. Sci. Signal. 9:424rs3
     [Google Scholar]
  36. 36.
    Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR 2009. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10:11778–90
     [Google Scholar]
  37. 37.
    Beach JR, Hammer JA 2015. Myosin II isoform co-assembly and differential regulation in mammalian systems. Exp. Cell Res. 334:12–9
     [Google Scholar]
  38. 38.
    Shutova MS, Svitkina TM 2018. Mammalian nonmuscle myosin II comes in three flavors. Biochem. Biophys. Res. Commun. 506:394402
     [Google Scholar]
  39. 39.
    Hammer JA, Sellers JR 2012. Walking to work: roles for class V myosins as cargo transporters. Nat. Rev. Mol. Cell Biol. 13:113–26
     [Google Scholar]
  40. 40.
    Sakamoto T, Limouze J, Combs CA, Straight AF, Sellers JR 2005. Blebbistatin, a myosin II inhibitor, is photoinactivated by blue light. Biochemistry 44:2584–88
     [Google Scholar]
  41. 41.
    Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ et al. 2003. Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299:56131743–47
     [Google Scholar]
  42. 42.
    Képiró M, Várkuti BH, Végner L, Vörös G, Hegyi G et al. 2014. para-Nitroblebbistatin, the non-cytotoxic and photostable myosin II inhibitor. Angew. Chemie Int. Ed. 53:318211–15
     [Google Scholar]
  43. 43.
    Parsey MV, Lewis GK 1993. Actin polymerization and pseudopod reorganization accompany anti-CD3-induced growth arrest in Jurkat T cells. J. Immunol. 151:41881–93
     [Google Scholar]
  44. 44.
    Bunnell SC, Kapoor V, Trible RP, Zhang W, Samelson LE 2001. Dynamic actin polymerization drives T cell receptor-induced spreading. Immunity 14:3315–29
     [Google Scholar]
  45. 45.
    Bunnell SC, Hong DI, Kardon JR, Yamazaki T, McGlade CJ et al. 2002. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 158:71263–75
     [Google Scholar]
  46. 46.
    Kaizuka Y, Douglass AD, Varma R, Dustin ML, Vale RD 2007. Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells. PNAS 104:5120296–301
     [Google Scholar]
  47. 47.
    Yi J, Wu XS, Crites T, Hammer JA 2012. Actin retrograde flow and actomyosin II arc contraction drive receptor cluster dynamics at the immunological synapse in Jurkat T cells. Mol. Biol. Cell. 23:5834–52
     [Google Scholar]
  48. 48.
    Murugesan S, Hong J, Yi J, Li D, Beach JR et al. 2016. Formin-generated actomyosin arcs propel T cell receptor microcluster movement at the immune synapse. J. Cell Biol. 215:3383–99
     [Google Scholar]
  49. 49.
    Hong J, Murugesan S, Betzig E, Hammer JA 2017. Contractile actomyosin arcs promote the activation of primary mouse T cells in a ligand-dependent manner. PLOS ONE 12:8e0183174
     [Google Scholar]
  50. 50.
    Fritzsche M, Fernandes RA, Chang VT, Colin-York H, Clausen MP et al. 2017. Cytoskeletal actin dynamics shape a ramifying actin network underpinning immunological synapse formation. Sci. Adv. 3:6e1603032
     [Google Scholar]
  51. 51.
    Ashdown GW, Burn GL, Williamson DJ, Pandžić E, Peters R et al. 2017. Live-cell super-resolution reveals F-actin and plasma membrane dynamics at the T cell synapse. Biophys. J. 112:81703–13
     [Google Scholar]
  52. 52.
    Babich A, Li S, O'Connor RS, Milone MC, Freedman BD, Burkhardt JK 2012. F-actin polymerization and retrograde flow drive sustained PLCγ1 signaling during T cell activation. J. Cell Biol. 197:6775–87
     [Google Scholar]
  53. 53.
    Yu Y, Fay NC, Smoligovets AA, Wu H-J, Groves JT 2012. Myosin IIA modulates T cell receptor transport and CasL phosphorylation during early immunological synapse formation. PLOS ONE 7:2e30704
     [Google Scholar]
  54. 54.
    Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G 2004. Two distinct actin networks drive the protrusion of migrating cells. Science 305:56911782–86
     [Google Scholar]
  55. 55.
    Hetrick B, Han MS, Helgeson LA, Nolen BJ 2013. Small molecules CK-666 and CK-869 inhibit actin-related protein 2/3 complex by blocking an activating conformational change. Chem. Biol. 20:5701–12
     [Google Scholar]
  56. 56.
    Le Floc'h A, Tanaka Y, Bantilan NS, Voisinne G, Altan-Bonnet G et al. 2013. Annular PIP3 accumulation controls actin architecture and modulates cytotoxicity at the immunological synapse. J. Exp. Med 210:122721–37 Correction. 2013 J. Exp. Med 210:122721–37
     [Google Scholar]
  57. 57.
    Sanui T, Inayoshi A, Noda M, Iwata E, Oike M et al. 2003. DOCK2 is essential for antigen-induced translocation of TCR and lipid rafts, but not PKC-θ and LFA-1, in T cells. Immunity 19:1119–29
     [Google Scholar]
  58. 58.
    Nishikimi A, Kukimoto-Niino M, Yokoyama S, Fukui Y 2013. Immune regulatory functions of DOCK family proteins in health and disease. Exp. Cell Res. 319:152343–49
     [Google Scholar]
  59. 59.
    Nolz JC, Gomez TS, Zhu P, Li S, Medeiros RB et al. 2006. The WAVE2 complex regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation. Curr. Biol. 16:124–34
     [Google Scholar]
  60. 60.
    Zipfel PA, Bunnell SC, Witherow DS, Gu JJ, Chislock EM et al. 2006. Role for the Abi/Wave protein complex in T cell receptor-mediated proliferation and cytoskeletal remodeling. Curr. Biol. 16:135–46
     [Google Scholar]
  61. 61.
    Rizvi SA, Neidt EM, Cui J, Feiger Z, Skau CT et al. 2009. Identification and characterization of a small molecule inhibitor of formin-mediated actin assembly. Chem. Biol. 16:111158–68
     [Google Scholar]
  62. 62.
    Ilani T, Vasiliver-Shamis G, Vardhana S, Bretscher A, Dustin ML 2009. T cell antigen receptor signaling and immunological synapse stability require myosin IIA. Nat. Immunol. 10:5531–39
     [Google Scholar]
  63. 63.
    Chen Q, Nag S, Pollard TD 2012. Formins filter modified actin subunits during processive elongation. J. Struct. Biol. 177:132–39
     [Google Scholar]
  64. 64.
    Rak GD, Mace EM, Banerjee PP, Svitkina T, Orange JS 2011. Natural killer cell lytic granule secretion occurs through a pervasive actin network at the immune synapse. PLOS Biol 9:9e1001151
     [Google Scholar]
  65. 65.
    Brown ACN, Oddos S, Dobbie IM, Alakoskela J-M, Parton RM et al. 2011. Remodelling of cortical actin where lytic granules dock at natural killer cell immune synapses revealed by super-resolution microscopy. PLOS Biol 9:9e1001152
     [Google Scholar]
  66. 66.
    Carisey AF, Mace EM, Saeed MB, Davis DM, Orange JS 2018. Nanoscale dynamism of actin enables secretory function in cytolytic cells. Curr. Biol. 28:4489–502.e9
     [Google Scholar]
  67. 67.
    Ritter AT, Kapnick SM, Murugesan S, Schwartzberg PL, Griffiths GM, Lippincott-Schwartz J 2017. Cortical actin recovery at the immunological synapse leads to termination of lytic granule secretion in cytotoxic T lymphocytes. PNAS 114:32E6585–94
     [Google Scholar]
  68. 68.
    Kumari S, Depoil D, Martinelli R, Judokusumo E, Carmona G et al. 2015. Actin foci facilitate activation of the phospholipase C-γ in primary T lymphocytes via the WASP pathway. eLife 4:41–31
     [Google Scholar]
  69. 69.
    Cannon JL, Burkhardt JK 2004. Differential roles for Wiskott-aldrich syndrome protein in immune synapse formation and IL-2 production. J. Immunol. 173:31658–62
     [Google Scholar]
  70. 70.
    Eddy RJ, Weidmann MD, Sharma VP, Condeelis JS 2017. Tumor cell invadopodia: invasive protrusions that orchestrate metastasis. Trends Cell Biol 27:8595–607
     [Google Scholar]
  71. 71.
    Fuller CL, Braciale VL, Samelson LE 2003. All roads lead to actin: the intimate relationship between TCR signaling and the cytoskeleton. Immunol. Rev. 191:1220–36
     [Google Scholar]
  72. 72.
    Courtney AH, Lo W-L, Weiss A 2018. TCR signaling: mechanisms of initiation and propagation. Trends Biochem. Sci. 43:2108–23
     [Google Scholar]
  73. 73.
    Tybulewicz VL 2005. Vav-family proteins in T-cell signalling. Curr. Opin. Immunol. 17:3267–74
     [Google Scholar]
  74. 74.
    Razidlo GL, Schroeder B, Chen J, Billadeau DD, McNiven MA 2014. Vav1 as a central regulator of invadopodia assembly. Curr. Biol. 24:186–93
     [Google Scholar]
  75. 75.
    Varma R, Campi G, Yokosuka T, Saito T, Dustin ML 2006. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 25:1117–27
     [Google Scholar]
  76. 76.
    Nguyen K, Sylvain NR, Bunnell SC 2008. T cell costimulation via the integrin VLA-4 inhibits the actin-dependent centralization of signaling microclusters containing the adaptor SLP-76. Immunity 28:6810–21
     [Google Scholar]
  77. 77.
    Jankowska KI, Williamson EK, Roy NH, Blumenthal D, Chandra V et al. 2018. Integrins modulate T cell receptor signaling by constraining actin flow at the immunological synapse. Front. Immunol. 9:25
     [Google Scholar]
  78. 78.
    Hashimoto-Tane A, Yokosuka T, Sakata-Sogawa K, Sakuma M, Ishihara C et al. 2011. Dynein-driven transport of T cell receptor microclusters regulates immune synapse formation and T cell activation. Immunity 34:6919–31
     [Google Scholar]
  79. 79.
    DeMond AL, Mossman KD, Starr T, Dustin ML, Groves JT 2008. T cell receptor microcluster transport through molecular mazes reveals mechanism of translocation. Biophys. J. 94:83286–92
     [Google Scholar]
  80. 80.
    Yu C, Wu H-J, Kaizuka Y, Vale RD, Groves JT 2010. Altered actin centripetal retrograde flow in physically restricted immunological synapses. PLOS ONE 5:7e11878
     [Google Scholar]
  81. 81.
    Smoligovets AA, Smith AW, Wu H-J, Petit RS, Groves JT 2012. Characterization of dynamic actin associations with T-cell receptor microclusters in primary T cells. J. Cell Sci. 125:3735–42
     [Google Scholar]
  82. 82.
    Ditlev JA, Vega AR, Köster DV, Su X, Lakoduk A et al. 2018. A composition-dependent molecular clutch between T cell signaling clusters and actin. bioRxiv316414
  83. 83.
    Janssen E, Tohme M, Hedayat M, Leick M, Kumari S et al. 2016. A DOCK8-WIP-WASp complex links T cell receptors to the actin cytoskeleton. J. Clin. Investig. 126:103837–51
     [Google Scholar]
  84. 84.
    Springer TA, Dustin ML 2012. Integrin inside-out signaling and the immunological synapse. Curr. Opin. Cell Biol. 24:1107–15
     [Google Scholar]
  85. 85.
    Comrie WA, Burkhardt JK 2016. Action and traction: cytoskeletal control of receptor triggering at the immunological synapse. Front. Immunol. 7:68
     [Google Scholar]
  86. 86.
    Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM 2006. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443:7110462–65
     [Google Scholar]
  87. 87.
    de la Roche M, Asano Y, Griffiths GM 2016. Origins of the cytolytic synapse. Nat. Rev. Immunol. 16:7421–32
     [Google Scholar]
  88. 88.
    Raaijmakers JH, Bos JL 2009. Specificity in Ras and Rap signaling. J. Biol. Chem. 284:1710995–99
     [Google Scholar]
  89. 89.
    Lagarrigue F, Kim C, Ginsberg MH 2016. The Rap1-RIAM-talin axis of integrin activation and blood cell function. Blood 128:4479–87
     [Google Scholar]
  90. 90.
    Comrie WA, Babich A, Burkhardt JK 2015. F-actin flow drives affinity maturation and spatial organization of LFA-1 at the immunological synapse. J. Cell Biol. 208:4475–91
     [Google Scholar]
  91. 91.
    Nolz JC, Medeiros RB, Mitchell JS, Zhu P, Freedman BD et al. 2007. WAVE2 regulates high-affinity integrin binding by recruiting vinculin and talin to the immunological synapse. Mol. Cell. Biol. 27:175986–6000
     [Google Scholar]
  92. 92.
    Nolz JC, Nacusi LP, Segovis CM, Medeiros RB, Mitchell JS et al. 2008. The WAVE2 complex regulates T cell receptor signaling to integrins via Abl- and CrkL-C3G-mediated activation of Rap1. J. Cell Biol. 182:61231–44
     [Google Scholar]
  93. 93.
    Gardel ML, Schneider IC, Aratyn-Schaus Y, Waterman CM 2010. Mechanical integration of actin and adhesion dynamics in cell migration. Annu. Rev. Cell Dev. Biol. 26:315–33
     [Google Scholar]
  94. 94.
    Case LB, Waterman CM 2015. Integration of actin dynamics and cell adhesion by a three-dimensional, mechanosensitive molecular clutch. Nat. Cell Biol. 17:8955–63
     [Google Scholar]
  95. 95.
    Galbraith CG, Yamada KM, Sheetz MP 2002. The relationship between force and focal complex development. J. Cell Biol. 159:4695–705
     [Google Scholar]
  96. 96.
    Klapholz B, Brown NH 2017. Talin—the master of integrin adhesions. J. Cell Sci. 130:152435–46
     [Google Scholar]
  97. 97.
    Sun Z, Guo SS, Fässler R 2016. Integrin-mediated mechanotransduction. J. Cell Biol. 215:4445–56
     [Google Scholar]
  98. 98.
    Comrie WA, Li S, Boyle S, Burkhardt JK 2015. The dendritic cell cytoskeleton promotes T cell adhesion and activation by constraining ICAM-1 mobility. J. Cell Biol. 208:4457–73
     [Google Scholar]
  99. 99.
    Hartman NC, Nye JA, Groves JT 2009. Cluster size regulates protein sorting in the immunological synapse. PNAS 106:3112729–34
     [Google Scholar]
  100. 100.
    Wilson CA, Tsuchida MA, Allen GM, Barnhart EL, Applegate KT et al. 2010. Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature 465:7296373–77
     [Google Scholar]
  101. 101.
    Gutiérrez LM, Villanueva J 2018. The role of F-actin in the transport and secretion of chromaffin granules: an historic perspective. Pflügers Arch. Eur. J. Physiol. 470:1181–86
     [Google Scholar]
  102. 102.
    Ritter AT, Asano Y, Stinchcombe JC, Dieckmann NMG, Chen B-C et al. 2015. Actin depletion initiates events leading to granule secretion at the immunological synapse. Immunity 42:5864–76
     [Google Scholar]
  103. 103.
    Hammer JA 2018. Immunology: Is actin at the lytic synapse a friend or a foe?. Curr. Biol. 28:4R155–57
     [Google Scholar]
  104. 104.
    Čemerski S, Das J, Giurisato E, Markiewicz MA, Allen PM et al. 2008. The balance between T cell receptor signaling and degradation at the center of the immunological synapse is determined by antigen quality. Immunity 29:3414–22
     [Google Scholar]
  105. 105.
    Choudhuri K, Llodrá J, Roth EW, Tsai J, Gordo S et al. 2014. Polarized release of T-cell-receptor-enriched microvesicles at the immunological synapse. Nature 507:7490118–23
     [Google Scholar]
  106. 106.
    Dustin ML, Choudhuri K 2016. Signaling and polarized communication across the T cell immunological synapse. Annu. Rev. Cell Dev. Biol. 32:303–25
     [Google Scholar]
  107. 107.
    Basu R, Whitlock BM, Husson J, Le Floc'h A, Jin W et al. 2016. Cytotoxic T cells use mechanical force to potentiate target cell killing. Cell 165:1100–10
     [Google Scholar]
  108. 108.
    Basu R, Huse M 2017. Mechanical communication at the immunological synapse. Trends Cell Biol 27:4241–54
     [Google Scholar]
  109. 109.
    Huse M 2017. Mechanical forces in the immune system. Nat. Rev. Immunol. 17:11679–90
     [Google Scholar]
  110. 110.
    Hui KL, Balagopalan L, Samelson LE, Upadhyaya A 2015. Cytoskeletal forces during signaling activation in Jurkat T-cells. Mol. Biol. Cell. 26:4685–95
     [Google Scholar]
  111. 111.
    Upadhyaya A 2017. Mechanosensing in the immune response. Semin. Cell Dev. Biol. 71:137–45
     [Google Scholar]
  112. 112.
    Chen W, Zhu C 2013. Mechanical regulation of T-cell functions. Immunol. Rev. 256:1160–76
     [Google Scholar]
  113. 113.
    Depoil D, Dustin ML 2014. Force and affinity in ligand discrimination by the TCR. Trends Immunol 35:12597–603
     [Google Scholar]
  114. 114.
    Santos LC, Blair DA, Kumari S, Cammer M, Iskratsch T et al. 2016. Actin polymerization-dependent activation of Cas-L promotes immunological synapse stability. Immunol. Cell Biol. 94:10981–93
     [Google Scholar]
  115. 115.
    Kubow KE, Horwitz AR 2011. Reducing background fluorescence reveals adhesions in 3D matrices. Nat. Cell Biol. 13:15–7
     [Google Scholar]
  116. 116.
    Chen B, Legant WR, Wang K, Shao L, Milkie DE et al. 2014. Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. Science 346:62081257998
     [Google Scholar]
  117. 117.
    Wang JC, Bolger-Munro M, Gold MR 2018. Imaging the interactions between B cells and antigen-presenting cells. Methods Mol. Biol 1707:131–61
     [Google Scholar]
  118. 118.
    Singleton K, Parvaze N, Dama KR, Chen KS, Jennings P et al. 2006. A large T cell invagination with CD2 enrichment resets receptor engagement in the immunological synapse. J. Immunol. 177:74402–13
     [Google Scholar]
  119. 119.
    Roybal KT, Mace EM, Mantell JM, Verkade P, Orange JS, Wülfing C 2015. Early signaling in primary T cells activated by antigen presenting cells is associated with a deep and transient lamellal actin network. PLOS ONE 10:8e0133299
     [Google Scholar]
  120. 120.
    Roybal KT, Mace EM, Clark DJ, Leard AD, Herman A et al. 2015. Modest interference with actin dynamics in primary T cell activation by antigen presenting cells preferentially affects lamellal signaling. PLOS ONE 10:8e0133231
     [Google Scholar]
  121. 121.
    Bertrand F, Muller S, Roh K-H, Laurent C, Dupre L, Valitutti S 2013. An initial and rapid step of lytic granule secretion precedes microtubule organizing center polarization at the cytotoxic T lymphocyte/target cell synapse. PNAS 110:156073–78
     [Google Scholar]
  122. 122.
    Clausen MP, Colin-York H, Schneider F, Eggeling C, Fritzsche M 2017. Dissecting the actin cortex density and membrane-cortex distance in living cells by super-resolution microscopy. J. Phys. D. Appl. Phys. 50:664002
     [Google Scholar]
  123. 123.
    Gomez TS, McCarney SD, Carrizosa E, Labno CM, Comiskey EO et al. 2006. HS1 functions as an essential actin-regulatory adaptor protein at the immune synapse. Immunity 24:6741–52
     [Google Scholar]
  124. 124.
    Gorman JA, Babich A, Dick CJ, Schoon RA, Koenig A et al. 2012. The cytoskeletal adaptor protein IQGAP1 regulates TCR-mediated signaling and filamentous actin dynamics. J. Immunol. 188:126135–44
     [Google Scholar]
  125. 125.
    Liang Y, Cucchetti M, Roncagalli R, Yokosuka T, Malzac A et al. 2013. The lymphoid lineage-specific actin-uncapping protein Rltpr is essential for costimulation via CD28 and the development of regulatory T cells. Nat. Immunol. 14:8858–66
     [Google Scholar]
  126. 126.
    Roncagalli R, Cucchetti M, Jarmuzynski N, Grégoire C, Bergot E et al. 2016. The scaffolding function of the RLTPR protein explains its essential role for CD28 co-stimulation in mouse and human T cells. J. Exp. Med. 213:112437–57
     [Google Scholar]
  127. 127.
    Schober T, Magg T, Laschinger M, Rohlfs M, Linhares ND et al. 2017. A human immunodeficiency syndrome caused by mutations in CARMIL2. Nat. . Commun 8:14209
     [Google Scholar]
  128. 128.
    Goode BL, Sweeney MO, Eskin JA 2018. GMF as an actin network remodeling factor. Trends Cell Biol 28:749–60
     [Google Scholar]
  129. 129.
    Morley SC 2013. The actin-bundling protein L-plastin supports T-cell motility and activation. Immunol. Rev. 256:148–62
     [Google Scholar]
  130. 130.
    Mace EM, Orange JS 2014. Lytic immune synapse function requires filamentous actin deconstruction by Coronin 1A. PNAS 111:186708–13
     [Google Scholar]
  131. 131.
    Shaffer MH, Dupree RS, Zhu P, Saotome I, Schmidt RF et al. 2009. Ezrin and moesin function together to promote T cell activation. J. Immunol. 182:21021–32
     [Google Scholar]
/content/journals/10.1146/annurev-immunol-042718-041341
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Origin, Organization, Dynamics, and Function of Actin and Actomyosin Networks at the T Cell Immunological Synapse
Annual Review of Immunology 37, 201 (2019); https://doi.org/10.1146/annurev-immunol-042718-041341
/content/journals/10.1146/annurev-immunol-042718-041341
/content/journals/10.1146/annurev-immunol-042718-041341
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