Actin retrograde flow and actomyosin II arc contraction drive receptor cluster dynamics at the immunological synapse in Jurkat T cells

Molecular Biology of the Cell

Volumn 23, Issue 5, 2012, Pages 834-852

  Yi, Jason ^a,b   Wu, Xufeng S ^a   Crites, Travis ^c   Hammer III, John A ^a  

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

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BLEBBISTATIN; CYTOCHALASIN D; F ACTIN; JASPAMIDE; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN ADENOSINE TRIPHOSPHATASE II; MYOSIN HEAVY CHAIN; MYOSIN IIA; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN MYOSIN INTERACTION; ARTICLE; DISTAL SUPRAMOLECULAR ACTIVATION CLUSTER; IMMUNOLOGICAL SYNAPSE; LAMELLAR BODY; LAMELLIPODIUM; LEUKEMIA CELL LINE; PERIPHERAL SUPRAMOLECULAR ACTIVATION CLUSTER; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION;

ACTINS; ACTOMYOSIN; CYTOCHALASIN D; DEPSIPEPTIDES; GREEN FLUORESCENT PROTEINS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; IMMUNOLOGICAL SYNAPSES; JURKAT CELLS; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; NONMUSCLE MYOSIN TYPE IIA; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 84863229197     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-08-0731     Document Type: Article

References (52)

1. Aizawa H, Sameshima M, Yahara I (1997). A green fluorescent protein-actin fusion protein dominantly inhibits cytokinesis, cell spreading, and locomotion in Dictyostelium. Cell Struct Funct 22, 335-345. (Pubitemid 27365904)
2. Allingham JS, Smith R, Rayment I (2005). The structural basis of blebbistatin inhibition and specificity for myosin II. Nat Struct Mol Biol 12, 378-379. (Pubitemid 43093094)
3. Babich A, Burkhardt JK (2011). Lymphocyte signaling converges on microtubules. Immunity 34, 825-827.
4. Billadeau DD, Nolz JC, Gomez TS (2007). Regulation of T-cell activation by the cytoskeleton. Nat Rev Immunol 7, 131-143. (Pubitemid 46174860)
5. Bunnell SC, Barr VA, Fuller CL, Samelson LE (2003). High-resolution multicolor imaging of dynamic signaling complexes in T cells stimulated by planar substrates. Sci STKE 2003, PL8.
6. Bunnell SC, Kapoor V, Trible RP, Zhang W, Samelson LE (2001). Dynamic actin polymerization drives T cell receptor-induced spreading: a role for the signal transduction adaptor LAT. Immunity 14, 315-329. (Pubitemid 32289295)
7. 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.
8. Carlier MF, Criquet P, Pantaloni D, Korn ED (1986). Interaction of cytochalasin D with actin filaments in the presence of ADP and ATP. J Biol Chem 261, 2041-2050. (Pubitemid 17205125)
9. Carrasco YR, Fleire SJ, Cameron T, Dustin ML, Batista FD (2004). LFA-1/ ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity 20, 589-599. (Pubitemid 38638128)
10. Cramer LP (1999). Role of actin-filament disassembly in lamellipodium protrusion in motile cells revealed using the drug jasplakinolide. Curr Biol 9, 1095-1105.
11. 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, 3286-3292.
12. Doyle T, Botstein D (1996). Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc Natl Acad Sci USA 93, 3886-3891. (Pubitemid 26144217)
13. Dustin ML (2007). Cell adhesion molecules and actin cytoskeleton at immune synapses and kinapses. Curr Opin Cell Biol 19, 529-533.
14. Dustin ML (2009). Supported bilayers at the vanguard of immune cell activation studies. J Struct Biol 168, 152-160.
15. Fooksman DR, Vardhana S, Vasiliver-Shamis G, Liese J, Blair DA, Waite J, Sacristan C, Victora GD, Zanin-Zhorov A, Dustin ML (2010). Functional anatomy of T cell activation and synapse formation. Annu Rev Immunol 28, 79-105.
16. Forscher P, Smith SJ (1988). Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J Cell Biol 107, 1505-1516.
17. Freiberg BA, Kupfer H, Maslanik W, Delli J, Kappler J, Zaller DM, Kupfer A (2002). Staging and resetting T cell activation in SMACs. Nat Immunol 3, 911-917. (Pubitemid 35154003)
18. 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, 315-333.
19. Giannone G et al. (2007). Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128, 561-575. (Pubitemid 46198897)
20. 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. (Pubitemid 29329988)
21. Gupton SL, Waterman-Storer CM (2006). Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125, 1361-1374. (Pubitemid 43929092)
22. Hartman NC, Groves JT (2011). Signaling clusters in the cell membrane. Curr Opin Cell Biol 23, 370-376.
23. Hartman NC, Nye JA, Groves JT (2009). Cluster size regulates protein sorting in the immunological synapse. Proc Natl Acad Sci USA 106, 12729-12734.
24. Hashimoto-Tane A, Yokosuka T, Sakata-Sogawa K, Sakuma M, Ishihara C, Tokunaga M, Saito T (2011). Dynein-driven transport of T cell receptor microclusters regulates immune synapse formation and T cell activation. Immunity 34, 919-931.
25. Henson JH, Svitkina TM, Burns AR, Hughes HE, MacPartland KJ, Nazarian R, Borisy GG (1999). Two components of actin-based retrograde flow in sea urchin coelomocytes. Mol Biol Cell 10, 4075-4090.
26. 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.
27. 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. (Pubitemid 38660466)
28. Johnson HW, Schell MJ (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.
29. 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. Proc Natl Acad Sci USA 104, 20296-20301.
30. Lin CH, Espreafico EM, Mooseker MS, Forscher P (1996). Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16, 769-782. (Pubitemid 26124054)
31. Medeiros NA, Burnette DT, Forscher P (2006). Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat Cell Biol 8, 215-226. (Pubitemid 43336063)
32. 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. (Pubitemid 28420234)
33. 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. (Pubitemid 351778409)
34. Pasapera AM, Schneider IC, Rericha E, Schlaepfer DD, Waterman CM (2010). Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J Cell Biol 188, 877-890.
35. Pollard TD, Borisy GG (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465. (Pubitemid 36263079)
36. Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G (2004). Two distinct actin networks drive the protrusion of migrating cells. Science 305, 1782-1786. (Pubitemid 39249647)
37. Rogers SL, Wiedemann U, Stuurman N, Vale RD (2003). Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J Cell Biol 162, 1079-1088. (Pubitemid 37174190)
38. Sakamoto T, Limouze J, Combs CA, Straight AF, Sellers JR (2005). Blebbistatin, a myosin II inhibitor, is photoinactivated by blue light. Biochemistry 44, 584-588. (Pubitemid 40105489)
39. Schnyder T, Castello A, Feest C, Harwood NE, Oellerich T, Urlaub H, Engelke M, Wienands J, Bruckbauer A, Batista FD (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.
40. Sims TN et al. (2007). Opposing effects of PKCtheta and WASp on symmetry breaking and relocation of the immunological synapse. Cell 129, 773-785. (Pubitemid 46802378)
41. Tojkander S, Gateva G, Schevzov G, Hotulainen P, Naumanen P, Martin C, Gunning PW, Lappalainen P (2011). A molecular pathway for myosin II recruitment to stress fibers. Curr Biol 21, 539-550.
42. Vardhana S, Choudhuri K, Varma R, Dustin ML (2010). Essential role of ubiquitin and TSG101 protein in formation and function of the central supramolecular activation cluster. Immunity 32, 531-540.
43. 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. (Pubitemid 44066825)
44. 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, 778-790.
45. Wagner W, Brenowitz SD, Hammer JA 3rd (2011). Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons. Nat Cell Biol 13, 40-48.
46. Westphal M, Jungbluth A, Heidecker M, Muhlbauer B, Heizer C, Schwartz JM, Marriott G, Gerisch G (1997). Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein. Curr Biol 7, 176-183. (Pubitemid 27164723)
47. Wilson CA, Tsuchida MA, Allen GM, Barnhart EL, Applegate KT, Yam PT, Ji L, Keren K, Danuser G, Theriot JA (2010). Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature 465, 373-377.
48. Wu JQ, Pollard TD (2005). Counting cytokinesis proteins globally and locally in fission yeast. Science 310, 310-314.
49. Wu JQ, Sirotkin V, Kovar DR, Lord M, Beltzner CC, Kuhn JR, Pollard TD (2006). Assembly of the cytokinetic contractile ring from a broad band of nodes in fission yeast. J Cell Biol 174, 391-402. (Pubitemid 44156769)
50. 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. (Pubitemid 43045637)
51. Yu CH, Wu HJ, Kaizuka Y, Vale RD, Groves JT (2010). Altered actin centripetal retrograde flow in physically restricted immunological synapses. PLoS One 5, e11878.
52. Zhang XF, Schaefer AW, Burnette DT, Schoonderwoert VT, Forscher P (2003). Rho-dependent contractile responses in the neuronal growth cone are independent of classical peripheral retrograde actin flow. Neuron 40, 931-944. (Pubitemid 37522051)