Cytoskeletal forces during signaling activation in Jurkat T-cells

Molecular Biology of the Cell

Volumn 26, Issue 4, 2015, Pages 685-695

  Hui, King Lam ^a   Balagopalan, Lakshmi ^b   Samelson, Lawrence E ^b   Upadhyaya, Arpita ^a,c  

^a Bldg 142   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ENHANCED GREEN FLUORESCENT PROTEIN; MYOSIN; T LYMPHOCYTE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; DEPOLYMERIZATION; FORCE; INTRACELLULAR SIGNALING; JURKAT CELL LINE; MICROSCOPY; MOLECULAR DYNAMICS; MOUSE; MUSCLE CONTRACTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RIGIDITY; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TRACTION THERAPY; ADAPTIVE IMMUNITY; HUMAN; MECHANOTRANSDUCTION; METABOLISM; PHYSIOLOGY; ULTRASTRUCTURE;

ADAPTIVE IMMUNITY; CYTOSKELETON; HUMANS; JURKAT CELLS; MECHANOTRANSDUCTION, CELLULAR; RECEPTORS, ANTIGEN, T-CELL;

EID: 84922831195     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-03-0830     Document Type: Article

References (64)

1. Alon R, Dustin ML (2007). Force as a facilitator of integrin conformational changes during leukocyte arrest on blood vessels and antigen-presenting cells. Immunity 26, 17-27.
2. Aratyn-Schaus Y, Oakes PW, Gardel ML (2011). Dynamic and structural signatures of lamellar actomyosin force generation. Mol Biol Cell 22, 1330-1339.
3. Babich A, Li S, O'Connor RS, Milone MC, Freedman BD, Burkhardt JK (2012). F-actin polymerization and retrograde flow drive sustained PLCgamma1 signaling during T cell activation. J Cell Biol 197, 775-787.
4. Bashour KT, Gondarenko A, Chen H, Shen K, Liu X, Huse M, Hone JC, Kam LC (2014). CD28 and CD3 have complementary roles in T-cell traction forces. Proc Natl Acad Sci USA 111, 2241-2246.
5. Beemiller P, Jacobelli J, Krummel MF (2012). Integration of the movement of signaling microclusters with cellular motility in immunological synapses. Nat Immunol 13, 787-795.
6. Beemiller P, Krummel MF (2010). Mediation of T-cell activation by actin meshworks. Cold Spring Harbor Perspect Biol 2, a002444.
7. Betz T, Koch D, Lu YB, Franze K, Kas JA (2011). Growth cones as soft and weak force generators. Proc Natl Acad Sci USA 108, 13420-13425.
8. Billadeau DD, Nolz JC, Gomez TS (2007). Regulation of T-cell activation by the cytoskeleton. Nat Rev Immunol 7, 131-143.
9. Bunnell SC, Hong DI, Kardon JR, Yamazaki T, McGlade CJ, Barr VA, Samelson LE (2002). T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J Cell Biol 158, 1263-1275.
10. Burkhardt JK, Carrizosa E, Shaffer MH (2008). The actin cytoskeleton in T cell activation. Annu Rev Immunol 26, 233-259.
11. Butler JP, Tolic-Norrelykke IM, Fabry B, Fredberg JJ (2002). Traction fields, moments, and strain energy that cells exert on their surroundings. Am J Physiol 282, C595-605.
12. Cai Y, Biais N, Giannone G, Tanase M, Jiang G, Hofman JM, Wiggins CH, Silberzan P, Buguin A, Ladoux B, Sheetz MP (2006). Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys J 91, 3907-3920.
13. Campi G, Varma R, Dustin ML (2005). Actin and agonist MHC-peptide complex-dependent T cell receptor microclusters as scaffolds for signaling. J Exp Med 202, 1031-1036.
14. Chan CE, Odde DJ (2008). Traction dynamics of filopodia on compliant substrates. Science 322, 1687-1691.
15. Cheung A, Dantzig JA, Hollingworth S, Baylor SM, Goldman YE, Mitchison TJ, Straight AF (2002). A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4, 83-88.
16. Choudhuri K, van der Merwe PA (2007). Molecular mechanisms involved in T cell receptor triggering. Semin Immunol 19, 255-261.
17. Del Alamo JC, Meili R, Alonso-Latorre B, Rodriguez-Rodriguez J, Aliseda A, Firtel RA, Lasheras JC (2007). Spatio-temporal analysis of eukaryotic cell motility by improved force cytometry. Proc Natl Acad Sci USA 104, 13343-13348.
18. Dembo M, Wang YL (1999). Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys J 76, 2307-2316.
19. Douglass AD, Vale RD (2005). Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121, 937-950.
20. Dustin ML, Groves JT (2012). Receptor signaling clusters in the immune synapse. Annu Rev Biophys 41, 543-556.
21. Fournier MF, Sauser R, Ambrosi D, Meister JJ, Verkhovsky AB (2010). Force transmission in migrating cells. J Cell Biol 188, 287-297.
22. Goley ED, Welch MD (2006). The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 7, 713-726.
23. 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, 177-190.
24. Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS, Allen PM, Dustin ML (1999). The immunological synapse: a molecular machine controlling T cell activation. Science 285, 221-227.
25. Hammer JA 3rd, Burkhardt JK (2013). Controversy and consensus regarding myosin II function at the immunological synapse. Curr Opin Immunol 25, 300-306.
26. Husson J, Chemin K, Bohineust A, Hivroz C, Henry N (2011). Force generation upon T cell receptor engagement. PLoS One 6, e19680.
27. 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, 531-539.
28. Jacobelli J, Chmura SA, Buxton DB, Davis MM, Krummel MF (2004). A single class II myosin modulates T cell motility and stopping, but not synapse formation. Nat Immunol 5, 531-538.
29. Janmey PA, McCulloch CA (2007). Cell mechanics: integrating cell responses to mechanical stimuli. Annu Rev Biomed Eng 9, 1-34.
30. Judokusumo E, Tabdanov E, Kumari S, Dustin ML, Kam LC (2012). Mechanosensing in T lymphocyte activation. Biophys J 102, L5-7.
31. Kandula S, Abraham C (2004). LFA-1 on CD4+ T cells is required for optimal antigen-dependent activation in vivo. J Immunol 173, 4443-4451.
32. Kim ST, Takeuchi K, Sun ZY, Touma M, Castro CE, Fahmy A, Lang MJ, Wagner G, Reinherz EL (2009). The alphabeta T cell receptor is an anisotropic mechanosensor. J Biol Chem 284, 31028-31037.
33. Koch D, Rosoff WJ, Jiang J, Geller HM, Urbach JS (2012). Strength in the periphery: growth cone biomechanics and substrate rigidity response in peripheral and central nervous system neurons. Biophys J 102, 452-460.
34. Kumari S, Vardhana S, Cammer M, Curado S, Santos L, Sheetz MP, Dustin ML (2012). T lymphocyte myosin IIA is required for maturation of the immunological synapse. Front Immunol 3, 230.
35. Lam Hui K, Wang C, Grooman B, Wayt J, Upadhyaya A (2012). Membrane dynamics correlate with formation of signaling clusters during cell spreading. Biophys J 102, 1524-1533.
36. Lee J, Leonard M, Oliver T, Ishihara A, Jacobson K (1994). Traction forces generated by locomoting keratocytes. J Cell Biol 127, 1957-1964.
37. Lee KH, Holdorf AD, Dustin ML, Chan AC, Allen PM, Shaw AS (2002). T cell receptor signaling precedes immunological synapse formation. Science 295, 1539-1542.
38. Li YC, Chen BM, Wu PC, Cheng TL, Kao LS, Tao MH, Lieber A, Roffler SR (2010). Cutting Edge: mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling. J Immunol 184, 5959-5963.
39. Lo CM, Wang HB, Dembo M, Wang YL (2000). Cell movement is guided by the rigidity of the substrate. Biophys J 79, 144-152.
40. Ma Z, Finkel TH (2010). T cell receptor triggering by force. Trends Immunol 31, 1-6.
41. Ma Z, Janmey PA, Finkel TH (2008). The receptor deformation model of TCR triggering. FASEB J 22, 1002-1008.
42. Marcq P, Yoshinaga N, Prost J (2011). Rigidity sensing explained by active matter theory. Biophys J 101, L33-35.
43. Meili R, Alonso-Latorre B, del Alamo JC, Firtel RA, Lasheras JC (2010). Myosin II is essential for the spatiotemporal organization of traction forces during cell motility. Mol Biol Cell 21, 405-417.
44. Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A (1998). Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82-86.
45. Moore SW, Roca-Cusachs P, Sheetz MP (2010). Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Dev Cell 19, 194-206.
46. Mossman KD, Campi G, Groves JT, Dustin ML (2005). Altered TCR signaling from geometrically repatterned immunological synapses. Science 310, 1191-1193.
47. 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, 810-821.
48. Nolen BJ, Tomasevic N, Russell A, Pierce DW, Jia Z, Mc Cormick CD, Hartman J, Sakowicz R, Pollard TD (2009). Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460, 1031-1034.
49. Oakes PW, Patel DC, Morin NA, Zitterbart DP, Fabry B, Reichner JS, Tang JX (2009). Neutrophil morphology and migration are affected by substrate elasticity. Blood 114, 1387-1395.
50. Pelham RJ Jr, Wang Y (1997). Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 94, 13661-13665.
51. Rosenbluth MJ, Lam WA, Fletcher DA (2006). Force microscopy of nonadherent cells: a comparison of leukemia cell deformability. Biophys J 90, 2994-3003.
52. Sabass B, Gardel ML, Waterman CM, Schwarz US (2008). High resolution traction force microscopy based on experimental and computational advances. Biophys J 94, 207-220.
53. Saitoh M, Ishikawa T, Matsushima S, Naka M, Hidaka H (1987). Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J Biol Chem 262, 7796-7801.
54. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R, Tanaka S, Sheetz MP (2006). Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127, 1015-1026.
55. Scholer A, Hugues S, Boissonnas A, Fetler L, Amigorena S (2008). Intercellular adhesion molecule-1-dependent stable interactions between T cells and dendritic cells determine CD8+ T cell memory. Immunity 28, 258-270.
56. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M, Narumiya S (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
57. Van Goor D, Hyland C, Schaefer AW, Forscher P (2012). The role of actin turnover in retrograde actin network flow in neuronal growth cones. PLoS One 7, e30959.
58. 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, 117-127.
59. Wulfing C, Davis MM (1998). A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282, 2266-2269.
60. Yang Q, Zhang XF, Pollard TD, Forscher P (2012). Arp2/3 complex-dependent actin networks constrain myosin II function in driving retrograde actin flow. J Cell Biol 197, 939-956.
61. Yi J, Wu XS, Crites T, Hammer JA 3rd (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.
62. Yokosuka T, Sakata-Sogawa K, Kobayashi W, Hiroshima M, Hashimoto-Tane A, Tokunaga M, Dustin ML, Saito T (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.
63. Yu Y, Fay NC, Smoligovets AA, Wu HJ, Groves JT (2012). Myosin IIA modulates T cell receptor transport and CasL phosphorylation during early immunological synapse formation. PLoS One 7, e30704.
64. Yu Y, Smoligovets AA, Groves JT (2013). Modulation of T cell signaling by the actin cytoskeleton. J Cell Sci 126, 1049-1058.