Myosin IIA modulates T cell receptor transport and CasL phosphorylation during early immunological synapse formation

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Yu, Yan ^a,b   Fay, Nicole C ^a,b   Smoligovets, Alexander A ^a,b   Wu, Hung Jen ^a,b   Groves, Jay T ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CRK ASSOCIATED SUBSTRATE PROTEIN; CRK ASSOCIATED SUBSTRATE THE LYMPHOCYTE TYPE; CYTOCHROME C; CYTOCHROME C 88 103; MYOSIN IIA; PEPTIDE; PROTEIN KINASE ZAP 70; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; CAS L PROTEIN, MOUSE; CAS-L PROTEIN, MOUSE; CYTOCHROME; LYMPHOCYTE ANTIGEN RECEPTOR; PEPTIDE FRAGMENT; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; IMMUNOLOGICAL SYNAPSE; LIPID MEMBRANE; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; T LYMPHOCYTE; ANIMAL; IMMUNOLOGY; METABOLISM; MOTH; PHOSPHORYLATION; PHYSIOLOGY; TRANSGENIC MOUSE; TRANSPORT AT THE CELLULAR LEVEL;

LEPIDOPTERA; MUS MUSCULUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BIOLOGICAL TRANSPORT; CRK-ASSOCIATED SUBSTRATE PROTEIN; CYTOCHROMES; IMMUNOLOGICAL SYNAPSES; MICE; MICE, TRANSGENIC; MOTHS; NONMUSCLE MYOSIN TYPE IIA; PEPTIDE FRAGMENTS; PHOSPHORYLATION; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84863040809     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030704     Document Type: Article

References (63)

1. Grecco HE, Schmick M, Bastiaens PIH, (2011) Signaling from the Living Plasma Membrane. Cell 6: 897-909.
2. Salaita K, Nair PM, Petit RS, Neve RM, Das D, et al. (2010) Restriction of receptor movement alters cellular response: Physical force sensing by EphA2. Science 327: 1380-85.
3. Groves JT, Kuriyan J, (2010) Molecular mechanisms in signal transduction at the membrane. Nat Struct Mol Biol 17: 659-65.
4. Scott JD, Pawson T, (2009) Cell signaling in space and time: Where proteins come together and when they're apart. Science 326: 1220-24.
5. Loose M, Fischer-Friedrich E, Ries J, Kruse K, Schwille P, (2008) Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science 320: 789-92.
6. Monks CRF, Freiberg BA, Kupfer H, Sciaky N, Kupfer A, (1998) Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395: 82-86.
7. Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS, et al. (1999) The immunological synapse: A molecular machine controlling T cell activation. Science 285: 221-27.
8. Lee KH, Dinner AR, Tu C, Campi G, Raychaudhuri S, et al. (2003) The immunological synapse balances T cell receptor signaling and degradation. Science 302: 1218-22.
9. 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: 117-27.
10. 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: 1031-36.
11. Irvine DJ, Purbhoo MA, Krogsgaard M, Davis MM, (2002) Direct observation of ligand recognition by T cells. Nature 419: 845-49.
12. Mossman KD, Campi G, Groves JT, Dustin ML, (2005) Altered TCR signaling from geometrically repatterned immunological synapses. Science 310: 1191-93.
13. Doh J, Irvine DJ, (2006) Immunological synapse arrays: Patterned protein surfaces that modulate immunological synapse structure formation in T cells. Proc Natl Acad Sci USA 103: 5700-705.
14. Manz BN, Jackson BL, Petit RS, Dustin ML, Groves JT, (2010) T-cell triggering thresholds are modulated by the number of antigen within individual T-cell receptor clusters. Proc Natl Acad Sci USA 108: 9089-94.
15. Wulfing C, Davis MM, (1998) A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282: 2266-69.
16. 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 Soc USA 104: 20296-301.
17. 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: 3286-92.
18. 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.
19. Hartman NC, Nye JA, Groves JT, (2009) Cluster size regulates protein sorting in the immunological synapse. Proc Natl Acad Sci USA 106: 12729-34.
20. Smoligovets AA, Smith AW, Wu H-J, Petit RS, Groves JT, (2011) Characterization of Dynamic Actin Associations with T-cell Receptor Microclusters in Primary T-cells. J Cell Sci In press.
21. Barda-Saad M, Braiman A, Titerence R, Bunnell SC, Barr VA, et al. (2005) Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat Immunol 6: 80-89.
22. 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: 919-31.
23. 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: 531-38.
24. 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: 531-39.
25. Groves JT, Parthasarathy R, Forstner MB, (2008) Fluorescence imaging of membrane dynamics. Annu Rev Biomed Eng 10: 311-38.
26. Burkel BM, von Dassow G, Bement WM, (2007) Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil Cytoskeleton 64: 822-32.
27. Cai Y, Biais N, Giannone G, Tanase M, Jiang G, et al. (2006) Nonmuscle Myosin IIA-Dependent Force Inhibits Cell Spreading and Drives F-Actin Flow. Biophys J 91: 3907-02.
28. Giannone G, Dubin-Thaler BJ, Döbereiner HG, Kieffer N, Bresnick AR, et al. (2004) Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116: 431-43.
29. 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: 778-90.
30. Aratyn-Schaus Y, Gardel ML, (2010) Transient frictional slip between integrin and the ECM in focal adhesions under myosin II tension. Curr Biol 20: 1145-53.
31. Sakamoto T, Limouze J, Combs CA, Straight AF, Sellers JR, (2004) Blebbistatin, a myosin II inhibitor, is photoinactivated by blue light. Biochemistry 44: 584-88.
32. Groves JT, Ulman N, Boxer SG, (1999) Micropatterning fluid lipid bilayers on solid supports. Science 275: 651-53.
33. Kovács M, Thirumurugan K, Knight PJ, Sellers JR, (2007) Load-dependent mechanism of nonmuscle myosin 2. Proc Natl Acad Sci USA 104: 9994-9.
34. Lewis RS, (2001) Calcium signaling mechanisms in T lymphocytes. Annu Rev Immunol 19: 497-521.
35. 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: 1263-75.
36. Lee KH, Holdorf AD, Dustin ML, Chan AC, Allen PM, et al. (2002) T cell receptor signaling precedes immunological synapse formation. Science 295: 1539-42.
37. Bolte S, Cordelieres FP, (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213-32.
38. Ohashi Y, Tachibana K, Kamiguchi K, Fujita H, Morimoto C, (1998) T cell receptor-mediated tyrosine phosphorylation of Cas-L, a 105-kDa Crk-associated substrate-related protein, and its association of Crk and C3G. J Biol Chem 273: 6446-51.
39. Ohashi Y, Iwata S, Kamiguchi K, Morimoto C, (1999) Tyrosine Phosphorylation of Crk-associated substrate lymphocyte-type is a critical element in TCR- and β-integrin-induced T lymphocyte migration. J Immunol 163: 3727-34.
40. Minegishi M, Tachibana K, Sato T, Iwata S, Nojima Y, et al. (1996) Structure and function of Cas-L, a 105-kD Crk-associated substrate-related protein that is involved in beta 1 integrin-mediated signaling in lymphocytes. J Exp Med 184: 1365-75.
41. Kanda H, Mimura T, Hamasaki K, Yamamoto K, Yazaki Y, et al. (1999) Fyn and Lck tyrosine kinases regulate tyrosine phosphorylation of p105CasL, a member of the p130Cas docking protein family, in T-cell receptor-mediated signaling. Immunology 97: 56-61.
42. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R, et al. (2006) Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127: 1015-26.
43. Alexander NR, Branch KM, Parekh A, Clark ES, Iwueke IC, et al. (2008) Extracellular matrix rigidity promotes invadopodia activity. Curr Biol 18: 12951299.
44. Zheng M, McKeown-Longo PJ, (2006) Cell adhesion regulates Ser/Thr phosphorylation and proteasomal degradation of HEF1/NEDD9/Cas-L. J Cell Sci 119: 96-103.
45. Liu X, Elia AEH, Law SF, Golemis EA, Farley J, et al. (2000) A novel ability of Smad3 to regulate proteasomal degradation of a Cas family member, HEF1/NEDD9/Cas-L. EMBO J 19: 6759-6769.
46. Huppa JB, Axmann M, Mortelmaier MA, Lillemeier BF, Newell EW, et al. (2010) TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 463: 963-7.
47. Ingber DE, (2003) Mechanobiology and diseases of mechanotransduction. Ann Med 35: 1-14.
48. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, et al. (2009) Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling. Cell 139: 891-906.
49. Vogel V, Sheetz M, (2006) Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7: 265-75.
50. Engler AJ, Sen S, Sweeney HL, Discher DE, (2006) Matrix Elasticity Directs Stem Cell Lineage Specification. Cell 126: 677-89.
51. Li YC, Chen BM, Wu PC, Cheng TL, Kao LS, et al. (2010) Cutting edge: Mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling. J Immunol 184: 5959-63.
52. Kim ST, Takeuchi K, Sun ZY, Touma M, Castro CE, et al. (2009) The alphabeta T cell receptor is an anisotropic mechanosensor. J Biol Chem 284: 31028-37.
53. Husson J, Chemin K, Bohineust A, Hivroz C, Henry N, (2011) Force generation upon T cell receptor engagement. PLoS ONE 6: e19680.
54. Reedquist KA, Fukazawa T, Panchamoorthy G, Langdon WY, Shoelson SE, et al. (1996) Stimulation through the T cell receptor induces Cbl association with Crk proteins and the guanine nucleotide exchange protein C3G. J Biol Chem 271: 8435-42.
55. Gelkop S, Babichev Y, Isakov N, (2001) T cell activation induces direct binding of the Crk adapter protein to the regulatory subunit of phosphatidylinositol 3-kinase (p85) via a complex mechanism involving the Cbl protein. J Biol Chem 276: 36174-82.
56. Kaye J, Hsu ML, Sauron ME, Jameson SC, Gascoigne NR, et al. (1989) Selective development of CD4+ T cells in transgenic mice expressing a class II MHC-restricted antigen receptor. Nature 341: 746-49.
57. Wei Q, Adelstein RS, (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: 3617-27.
58. Nye JA, Groves JT, (2008) Kinetic control of histidine-tagged protein surface density on supported lipid bilayers. Langmuir 24: 4145-49.
59. Smith AW, Smoligovets AA, Groves JT, (2011) Patterned two-photon photoactivation illuminates spatial reorganization in live cells. J Phys Chem A 115: 3867-75.
60. Takács B, Billington N, Gyimesi M, Kintses B, Málnási-Csizmadia A, et al. (2010) Myosin complexed with ADP and blebbistatin reversibly adopts a conformation resembling the start point of the working stroke. Proc Natl Acad Sci USA 107: 6799-804.
61. Smith A, Bracke M, Leitinger B, Porter JC, Hogg N, (2003) LFA-1-induced T cell migration on ICAM-1 involves regulation of MLCK-mediated attachment and ROCK-dependent detachment. J Cell Sci 116: 3123-33.
62. Bubb MR, Spector I, Beyer BB, Fosen KM, (2000) Effects of jasplakinolide on the kinetics of actin polymerization. An explanation for certain in vivo observations. J Biol Chem 275: 5163-70.
63. Otsu N, (1979) A threshold selection method from gray-level histograms. IEEE Trans Sys Man Cyber 9: 62-66.