Hybrid Live Cell–Supported Membrane Interfaces for Signaling Studies

Literature Cited

1. 1.

   Andreasson-Ochsner M, Romano G, Hakanson M, Smith ML, Leckband DE et al. 2011. Single cell 3-D platform to study ligand mobility in cell–cell contact. Lab Chip 11:2876–83
   [Google Scholar]
2. 2.

   Artavanis-Tsakonas S, Rand MD, Lake RJ 1999. Notch signaling: cell fate control and signal integration in development. Science 284:770–76
   [Google Scholar]
3. 3.

   Atapattu L, Saha N, Llerena C, Vail ME, Scott AM et al. 2012. Antibodies binding the ADAM10 substrate recognition domain inhibit Eph function. J. Cell Sci. 125:6084–93
   [Google Scholar]
4. 4.

   Axelrod D, Koppel DE, Schlessinger J, Elson E, Webb WW 1976. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16:1055–69
   [Google Scholar]
5. 5.

   Baksh MM, Dean C, Pautot S, DeMaria S, Isacoff E, Groves JT 2005. Neuronal activation by GPI-linked neuroligin-1 displayed in synthetic lipid bilayer membranes. Langmuir 21:10693–98
   [Google Scholar]
6. 6.

   Bashaw GJ, Klein R 2010. Signaling from axon guidance receptors. Cold Spring Harb. Perspect. Biol. 2:a001941
   [Google Scholar]
7. 7.

   Biswas KH, Cho NJ, Groves JT 2018. Fabrication of multicomponent, spatially segregated DNA and protein functionalized supported membrane microarray. Langmuir 34:9781–88
   [Google Scholar]
8. 8.

   Biswas KH, Groves JT 2016. A microbead supported membrane-based fluorescence imaging assay reveals intermembrane receptor-ligand complex dimension with nanometer precision. Langmuir 32:6775–80
   [Google Scholar]
9. 9.

   Biswas KH, Hartman KL, Yu CH, Harrison OJ, Song H et al. 2015. E-cadherin junction formation involves an active kinetic nucleation process. PNAS 112:10932–37
   [Google Scholar]
10. 10.

    Biswas KH, Hartman KL, Zaidel-Bar R, Groves JT 2016. Sustained α-catenin activation at E-cadherin junctions in the absence of mechanical force. Biophys. J. 111:1044–52
    [Google Scholar]
11. 11.

    Biswas KH, Jackman JA, Park JH, Groves JT, Cho NJ 2018. Interfacial forces dictate the pathway of phospholipid vesicle adsorption onto silicon dioxide surfaces. Langmuir 34:1775–82
    [Google Scholar]
12. 12.

    Biswas KH, Zaidel-Bar R 2017. Early events in the assembly of E-cadherin adhesions. Exp. Cell Res. 358:14–19
    [Google Scholar]
13. 13.

    Biswas KH, Zhongwen C, Dubey AK, Oh D, Groves JT 2018. Multicomponent supported membrane microarray for monitoring spatially resolved cellular signaling reactions. Adv. Biosyst. 2:1800015
    [Google Scholar]
14. 14.

    Brasch J, Harrison OJ, Honig B, Shapiro L 2012. Thinking outside the cell: how cadherins drive adhesion. Trends Cell Biol 22:299–310
    [Google Scholar]
15. 15.

    Brian AA, McConnell HM 1984. Allogeneic stimulation of cytotoxic T cells by supported planar membranes. PNAS 81:6159–63
    [Google Scholar]
16. 16.

    Buckley CD, Tan J, Anderson KL, Hanein D, Volkmann N et al. 2014. Cell adhesion. The minimal cadherin-catenin complex binds to actin filaments under force. Science 346:1254211
    [Google Scholar]
17. 17.

    Caculitan NG, Kai H, Liu EY, Fay N, Yu Y et al. 2014. Size-based chromatography of signaling clusters in a living cell membrane. Nano Lett 14:2293–98
    [Google Scholar]
18. 18.

    Caplan S, Zeliger S, Wang L, Baniyash M 1995. Cell-surface-expressed T-cell antigen-receptor zeta chain is associated with the cytoskeleton. PNAS 92:4768–72
    [Google Scholar]
19. 19.

    Carter N, Nakamoto T, Hirai H, Hunter T 2002. EphrinA1-induced cytoskeletal re-organization requires FAK and p130^cas. Nat. Cell Biol. 4:565–73
    [Google Scholar]
20. 20.

    Changede R, Xu X, Margadant F, Sheetz MP 2015. Nascent integrin adhesions form on all matrix rigidities after integrin activation. Dev. Cell 35:614–21
    [Google Scholar]
21. 21.

    Charnley M, Kroschewski R, Textor M 2012. The study of polarisation in single cells using model cell membranes. Integr. Biol. 4:1059–71
    [Google Scholar]
22. 22.

    Chen CS 2008. Mechanotransduction—a field pulling together. ? J. Cell Sci. 121:3285–92
    [Google Scholar]
23. 23.

    Chen Y, Muller JD, So PT, Gratton E 1999. The photon counting histogram in fluorescence fluctuation spectroscopy. Biophys. J. 77:553–67
    [Google Scholar]
24. 24.

    Chen Z, Oh D, Biswas KH, Yu CH, Zaidel-Bar R, Groves JT 2018. Spatially modulated ephrinA1:EphA2 signaling increases local contractility and global focal adhesion dynamics to promote cell motility. PNAS 115:E5696–705
    [Google Scholar]
25. 25.

    Choudhuri K, Llodra J, Roth EW, Tsai J, Gordo S et al. 2014. Polarized release of T-cell-receptor-enriched microvesicles at the immunological synapse. Nature 507:118–23
    [Google Scholar]
26. 26.

    Choudhuri K, Wiseman D, Brown MH, Gould K, van der Merwe PA 2005. T-cell receptor triggering is critically dependent on the dimensions of its peptide-MHC ligand. Nature 436:578–82
    [Google Scholar]
27. 27.

    Cordoba SP, Choudhuri K, Zhang H, Bridge M, Basat AB et al. 2013. The large ectodomains of CD45 and CD148 regulate their segregation from and inhibition of ligated T-cell receptor. Blood 121:4295–302
    [Google Scholar]
28. 28.

    Coyle MP, Xu Q, Chiang S, Francis MB, Groves JT 2013. DNA-mediated assembly of protein heterodimers on membrane surfaces. J. Am. Chem. Soc. 135:5012–16
    [Google Scholar]
29. 29.

    Cremer PS, Boxer SG 1999. Formation and spreading of lipid bilayers on planar glass supports. J. Phys. Chem. B 103:2554–59
    [Google Scholar]
30. 30.

    Davis MM, Boniface JJ, Reich Z, Lyons D, Hampl J et al. 1998. Ligand recognition by αβ T cell receptors. Annu. Rev. Immunol. 16:523–44
    [Google Scholar]
31. 31.

    Davis S, Gale NW, Aldrich TH, Maisonpierre PC, Lhotak V et al. 1994. Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266:816–19
    [Google Scholar]
32. 32.

    del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP 2009. Stretching single talin rod molecules activates vinculin binding. Science 323:638–41
    [Google Scholar]
33. 33.

    DeMond AL, Groves JT 2007. Interrogating the T cell synapse with patterned surfaces and photoactivated proteins. Curr. Opin. Immunol. 19:722–27
    [Google Scholar]
34. 34.

    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
    [Google Scholar]
35. 35.

    DeMond AL, Starr T, Dustin ML, Groves JT 2006. Control of antigen presentation with a photoreleasable agonist peptide. J. Am. Chem. Soc. 128:15354–55
    [Google Scholar]
36. 36.

    Engler AJ, Sen S, Sweeney HL, Discher DE 2006. Matrix elasticity directs stem cell lineage specification. Cell 126:677–89
    [Google Scholar]
37. 37.

    Fierro-Gonzalez JC, White MD, Silva JC, Plachta N 2013. Cadherin-dependent filopodia control preimplantation embryo compaction. Nat. Cell Biol. 15:1424–33
    [Google Scholar]
38. 38.

    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
    [Google Scholar]
39. 39.

    Greene AC, Lord SJ, Tian A, Rhodes C, Kai H, Groves JT 2014. Spatial organization of EphA2 at the cell-cell interface modulates trans-endocytosis of ephrinA1. Biophys. J. 106:2196–205
    [Google Scholar]
40. 40.

    Groves JT 2005. Learning the chemical language of cell-surface interactions. Sci. STKE 2005:pe45
    [Google Scholar]
41. 41.

    Groves JT 2006. Spatial mutation of the T cell immunological synapse. Curr. Opin. Chem. Biol. 10:544–50
    [Google Scholar]
42. 42.

    Groves JT 2007. Bending mechanics and molecular organization in biological membranes. Annu. Rev. Phys. Chem. 58:697–717
    [Google Scholar]
43. 43.

    Groves JT, Dustin ML 2003. Supported planar bilayers in studies on immune cell adhesion and communication. J. Immunol. Methods 278:19–32
    [Google Scholar]
44. 44.

    Groves JT, Kuriyan J 2010. Molecular mechanisms in signal transduction at the membrane. Nat. Struct. Mol. Biol. 17:659–65
    [Google Scholar]
45. 45.

    Groves JT, Mahal LK, Bertozzi CR 2001. Control of cell adhesion and growth with micropatterned supported lipid membranes. Langmuir 17:5129–33
    [Google Scholar]
46. 46.

    Groves JT, Parthasarathy R, Forstner MB 2008. Fluorescence imaging of membrane dynamics. Annu. Rev. Biomed. Eng. 10:311–38
    [Google Scholar]
47. 47.

    Groves JT, Ulman N, Boxer SG 1997. Micropatterning fluid lipid bilayers on solid supports. Science 275:651–53
    [Google Scholar]
48. 48.

    Guo Z, Neilson LJ, Zhong H, Murray PS, Zanivan S, Zaidel-Bar R 2014. E-cadherin interactome complexity and robustness resolved by quantitative proteomics. Sci. Signal. 7:rs7
    [Google Scholar]
49. 49.

    Harrison OJ, Bahna F, Katsamba PS, Jin X, Brasch J et al. 2010. Two-step adhesive binding by classical cadherins. Nat. Struct. Mol. Biol. 17:348–57
    [Google Scholar]
50. 50.

    Harrison OJ, Jin X, Hong S, Bahna F, Ahlsen G et al. 2011. The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. Structure 19:244–56
    [Google Scholar]
51. 51.

    Hartman NC, Nye JA, Groves JT 2009. Cluster size regulates protein sorting in the immunological synapse. PNAS 106:12729–34
    [Google Scholar]
52. 52.

    Himanen JP, Yermekbayeva L, Janes PW, Walker JR, Xu K et al. 2010. Architecture of Eph receptor clusters. PNAS 107:10860–65
    [Google Scholar]
53. 53.

    Hori K, Sen A, Artavanis-Tsakonas S 2013. Notch signaling at a glance. J. Cell Sci. 126:2135–40
    [Google Scholar]
54. 54.

    Horton ER, Humphries JD, James J, Jones MC, Askari JA, Humphries MJ 2016. The integrin adhesome network at a glance. J. Cell Sci. 129:4159–63
    [Google Scholar]
55. 55.

    Hsu CJ, Hsieh WT, Waldman A, Clarke F, Huseby ES et al. 2012. Ligand mobility modulates immunological synapse formation and T cell activation. PLOS ONE 7:e32398
    [Google Scholar]
56. 56.

    Humpolickova J, Gielen E, Benda A, Fagulova V, Vercammen J et al. 2006. Probing diffusion laws within cellular membranes by Z-scan fluorescence correlation spectroscopy. Biophys. J. 91:L23–25
    [Google Scholar]
57. 57.

    Iino R, Koyama I, Kusumi A 2001. Single molecule imaging of green fluorescent proteins in living cells: E-cadherin forms oligomers on the free cell surface. Biophys. J. 80:2667–77
    [Google Scholar]
58. 58.

    Jackson BL, Groves JT 2004. Scanning probe lithography on fluid lipid membranes. J. Am. Chem. Soc. 126:13878–79
    [Google Scholar]
59. 59.

    James JR, Vale RD 2012. Biophysical mechanism of T-cell receptor triggering in a reconstituted system. Nature 487:64–69
    [Google Scholar]
60. 60.

    Kaizuka Y, Groves JT 2004. Structure and dynamics of supported intermembrane junctions. Biophys. J. 86:905–12
    [Google Scholar]
61. 61.

    Kaizuka Y, Groves JT 2010. Bending-mediated superstructural organizations in phase-separated lipid membranes. New J. Phys. 12:095001
    [Google Scholar]
62. 62.

    Ketchum C, Miller H, Song W, Upadhyaya A 2014. Ligand mobility regulates B cell receptor clustering and signaling activation. Biophys. J. 106:26–36
    [Google Scholar]
63. 63.

    Klein R 2012. Eph/ephrin signalling during development. Development 139:4105–9
    [Google Scholar]
64. 64.

    Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K et al. 2005. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 34:351–78
    [Google Scholar]
65. 65.

    le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N et al. 2010. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J. Cell Biol. 189:1107–15
    [Google Scholar]
66. 66.

    Leckband DE, de Rooij J 2014. Cadherin adhesion and mechanotransduction. Annu. Rev. Cell Dev. Biol. 30:291–315
    [Google Scholar]
67. 67.

    Lee IH, Kai H, Carlson LA, Groves JT, Hurley JH 2015. Negative membrane curvature catalyzes nucleation of endosomal sorting complex required for transport (ESCRT)-III assembly. PNAS 112:15892–97
    [Google Scholar]
68. 68.

    Lillemeier BF, Mortelmaier MA, Forstner MB, Huppa JB, Groves JT, Davis MM 2010. TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat. Immunol. 11:90–96
    [Google Scholar]
69. 69.

    Lin WC, Yu CH, Triffo S, Groves JT 2010. Supported membrane formation, characterization, functionalization, and patterning for application in biological science and technology. Curr. Protoc. Chem. Biol. 2:235–69
    [Google Scholar]
70. 70.

    Liu J, Qi S, Groves JT, Chakraborty AK 2005. Phase segregation on different length scales in a model cell membrane system. J. Phys. Chem. B 109:19960–69
    [Google Scholar]
71. 71.

    Liu W, Won Sohn H, Tolar P, Meckel T, Pierce SK 2010. Antigen-induced oligomerization of the B cell receptor is an early target of Fcγ RIIB inhibition. J. Immunol. 184:1977–89
    [Google Scholar]
72. 72.

    Lohmuller T, Iversen L, Schmidt M, Rhodes C, Tu HL et al. 2012. Single molecule tracking on supported membranes with arrays of optical nanoantennas. Nano Lett 12:1717–21
    [Google Scholar]
73. 73.

    Lohmuller T, Triffo S, O'Donoghue GP, Xu Q, Coyle MP, Groves JT 2011. Supported membranes embedded with fixed arrays of gold nanoparticles. Nano Lett 11:4912–18
    [Google Scholar]
74. 74.

    Lohmuller T, Xu Q, Groves JT 2013. Nanoscale obstacle arrays frustrate transport of EphA2-Ephrin-A1 clusters in cancer cell lines. Nano Lett 13:3059–64
    [Google Scholar]
75. 75.

    Manz BN, Groves JT 2010. Spatial organization and signal transduction at intercellular junctions. Nat. Rev. Mol. Cell Biol. 11:342–52
    [Google Scholar]
76. 76.

    Manz BN, Jackson BL, Petit RS, Dustin ML, Groves J 2011. T-cell triggering thresholds are modulated by the number of antigen within individual T-cell receptor clusters. PNAS 108:9089–94
    [Google Scholar]
77. 77.

    McMahon HT, Gallop JL 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:590–96
    [Google Scholar]
78. 78.

    Miao H, Burnett E, Kinch M, Simon E, Wang B 2000. Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat. Cell Biol. 2:62–69
    [Google Scholar]
79. 79.

    Milstein O, Tseng SY, Starr T, Llodra J, Nans A et al. 2008. Nanoscale increases in CD2-CD48-mediated intermembrane spacing decrease adhesion and reorganize the immunological synapse. J. Biol. Chem. 283:34414–22
    [Google Scholar]
80. 80.

    Miura K, Nam JM, Kojima C, Mochizuki N, Sabe H 2009. EphA2 engages Git1 to suppress Arf6 activity modulating epithelial cell-cell contacts. Mol. Biol. Cell 20:1949–59
    [Google Scholar]
81. 81.

    Mosch B, Reissenweber B, Neuber C, Pietzsch J 2010. Eph receptors and ephrin ligands: important players in angiogenesis and tumor angiogenesis. J. Oncol. 2010:135285
    [Google Scholar]
82. 82.

    Mossman KD, Campi G, Groves JT, Dustin ML 2005. Altered TCR signaling from geometrically repatterned immunological synapses. Science 310:1191–93
    [Google Scholar]
83. 83.

    Murai KK, Pasquale EB 2003. ‘Eph'ective signaling: forward, reverse and crosstalk. J. Cell Sci. 116:2823–32
    [Google Scholar]
84. 84.

    Murphy DA, Courtneidge SA 2011. The ‘ins’ and ‘outs’ of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12:413–26
    [Google Scholar]
85. 85.

    Nair PM, Salaita K, Petit RS, Groves JT 2011. Using patterned supported lipid membranes to investigate the role of receptor organization in intercellular signaling. Nat. Protoc. 6:523–39
    [Google Scholar]
86. 86.

    Nam JM, Nair PM, Neve RM, Gray JW, Groves JT 2006. A fluid membrane-based soluble ligand-display system for live-cell assays. ChemBioChem 7:436–40
    [Google Scholar]
87. 87.

    Natkanski E, Lee WY, Mistry B, Casal A, Molloy JE, Tolar P 2013. B cells use mechanical energy to discriminate antigen affinities. Science 340:1587–90
    [Google Scholar]
88. 88.

    O'Donoghue GP, Pielak RM, Smoligovets AA, Lin JJ, Groves JT 2013. Direct single molecule measurement of TCR triggering by agonist pMHC in living primary T cells. eLife 2:e00778
    [Google Scholar]
89. 89.

    Ozono K, Komiya S, Shimamura K, Ito T, Nagafuchi A 2011. Defining the roles of α-catenin in cell adhesion and cytoskeleton organization: isolation of F9 cells completely lacking cadherin-catenin complex. Cell Struct. Funct. 36:131–43
    [Google Scholar]
90. 90.

    Parthasarathy R, Groves JT 2004. Optical techniques for imaging membrane topography. Cell Biochem. Biophys. 41:391–414
    [Google Scholar]
91. 91.

    Parthasarathy R, Groves JT 2004. Protein patterns at lipid bilayer junctions. PNAS 101:12798–803
    [Google Scholar]
92. 92.

    Parthasarathy R, Groves JT 2007. Curvature and spatial organization in biological membranes. Soft Matter 3:24–33
    [Google Scholar]
93. 93.

    Parthasarathy R, Yu CH, Groves JT 2006. Curvature-modulated phase separation in lipid bilayer membranes. Langmuir 22:5095–99
    [Google Scholar]
94. 94.

    Pasquale EB 2008. Eph-ephrin bidirectional signaling in physiology and disease. Cell 133:38–52
    [Google Scholar]
95. 95.

    Pautot S, Lee H, Isacoff EY, Groves JT 2005. Neuronal synapse interaction reconstituted between live cells and supported lipid bilayers. Nat. Chem. Biol. 1:283–89
    [Google Scholar]
96. 96.

    Perez TD, Nelson WJ, Boxer SG, Kam L 2005. E-cadherin tethered to micropatterned supported lipid bilayers as a model for cell adhesion. Langmuir 21:11963–68
    [Google Scholar]
97. 97.

    Pielak RM, O'Donoghue GP, Lin JJ, Alfieri KN, Fay NC et al. 2017. Early T cell receptor signals globally modulate ligand:receptor affinities during antigen discrimination. PNAS 114:12190–95
    [Google Scholar]
98. 98.

    Qi SY, Groves JT, Chakraborty AK 2001. Synaptic pattern formation during cellular recognition. PNAS 98:6548–53
    [Google Scholar]
99. 99.

    Ruoslahti E 1996. RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12:697–715
    [Google Scholar]
100. 100.

     Sackmann E 1996. Supported membranes: scientific and practical applications. Science 271:43–48
     [Google Scholar]
101. 101.

     Salaita K, Groves JT 2010. Roles of the cytoskeleton in regulating EphA2 signals. Commun. Integr. Biol. 3:454–57
     [Google Scholar]
102. 102.

     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
     [Google Scholar]
103. 103.

     Sanchez MF, Levi V, Weidemann T, Carrer DC 2015. Agonist mobility on supported lipid bilayers affects Fas mediated death response. FEBS Lett 589:3527–33
     [Google Scholar]
104. 104.

     Sapuri AR, Baksh MM, Groves JT 2003. Electrostatically targeted intermembrane lipid exchange with micropatterned supported membranes. Langmuir 19:1606–10
     [Google Scholar]
105. 105.

     Schmid EM, Bakalar MH, Choudhuri K, Weichsel J, Ann H et al. 2016. Size-dependent protein segregation at membrane interfaces. Nat. Phys. 12:704–11
     [Google Scholar]
106. 106.

     Seguin L, Desgrosellier JS, Weis SM, Cheresh DA 2015. Integrins and cancer: regulators of cancer stemness, metastasis, and drug resistance. Trends Cell Biol 25:234–40
     [Google Scholar]
107. 107.

     Seiradake E, Harlos K, Sutton G, Aricescu AR, Jones EY 2010. An extracellular steric seeding mechanism for Eph-ephrin signaling platform assembly. Nat. Struct. Mol. Biol. 17:398–402
     [Google Scholar]
108. 108.

     Seiradake E, Schaupp A, del Toro Ruiz D, Kaufmann R, Mitakidis N et al. 2013. Structurally encoded intraclass differences in EphA clusters drive distinct cell responses. Nat. Struct. Mol. Biol. 20:958–64
     [Google Scholar]
109. 109.

     Shen B, Delaney MK, Du X 2012. Inside-out, outside-in, and inside-outside-in: G protein signaling in integrin-mediated cell adhesion, spreading, and retraction. Curr. Opin. Cell Biol. 24:600–6
     [Google Scholar]
110. 110.

     Singer SJ, Nicolson GL 1972. The fluid mosaic model of the structure of cell membranes. Science 175:720–31
     [Google Scholar]
111. 111.

     Smith AW, Smoligovets AA, Groves JT 2011. Patterned two-photon photoactivation illuminates spatial reorganization in live cells. J. Phys. Chem. A 115:3867–75
     [Google Scholar]
112. 112.

     Smoligovets AA, Smith AW, Groves JT 2013. Ratiometric imaging of the T-cell actin cytoskeleton reveals the nature of receptor-induced cytoskeletal enrichment. Biophys. J. 105:L11–13
     [Google Scholar]
113. 113.

     Smoligovets AA, Smith AW, Wu HJ, Petit RS, Groves JT 2012. Characterization of dynamic actin associations with T-cell receptor microclusters in primary T cells. J. Cell Sci. 125:735–42
     [Google Scholar]
114. 114.

     Tanaka M, Sackmann E 2005. Polymer-supported membranes as models of the cell surface. Nature 437:656–63
     [Google Scholar]
115. 115.

     Taylor MJ, Husain K, Gartner ZJ, Mayor S, Vale RD 2017. A DNA-based T cell receptor reveals a role for receptor clustering in ligand discrimination. Cell 169:108–19.e20
     [Google Scholar]
116. 116.

     Treanor B, Harwood NE, Batista FD 2009. Microsignalosomes: spatially resolved receptor signalling. Biochem. Soc. Trans. 37:1014–18
     [Google Scholar]
117. 117.

     Vafaei S, Tabaei SR, Biswas KH, Groves JT, Cho N-J 2017. Dynamic cellular interactions with extracellular matrix triggered by biomechanical tuning of low-rigidity, supported lipid membranes. Adv. Healthc. Mater. 6:1700243
     [Google Scholar]
118. 118.

     Vasioukhin V 2012. Adherens junctions and cancer. Subcell. Biochem. 60:379–414
     [Google Scholar]
119. 119.

     Vasioukhin V, Bauer C, Yin M, Fuchs E 2000. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100:209–19
     [Google Scholar]
120. 120.

     Vogel V, Sheetz M 2006. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7:265–75
     [Google Scholar]
121. 121.

     Wang W, Gulden PH, Pierce RA, Shabanowitz J, Man ST et al. 1997. A naturally processed peptide presented by HLA-A*0201 is expressed at low abundance and recognized by an alloreactive CD8+ cytotoxic T cell with apparent high affinity. J. Immunol. 158:5797–804
     [Google Scholar]
122. 122.

     Weikl TR, Groves JT, Lipowsky R 2002. Pattern formation during adhesion of multicomponent membranes. Europhys. Lett. 59:916–22
     [Google Scholar]
123. 123.

     Wise AR, Nye JA, Groves JT 2008. Discrete arrays of liquid-crystal-supported proteolipid monolayers as phantom cell surfaces. ChemPhysChem 9:1688–92
     [Google Scholar]
124. 124.

     Wong AP, Groves JT 2002. Molecular topography imaging by intermembrane fluorescence resonance energy transfer. PNAS 99:14147–52
     [Google Scholar]
125. 125.

     Wu SK, Yap AS 2013. Patterns in space: coordinating adhesion and actomyosin contractility at E-cadherin junctions. Cell Commun. Adhes. 20:201–12
     [Google Scholar]
126. 126.

     Wu Y, Jin X, Harrison O, Shapiro L, Honig BH, Ben-Shaul A 2010. Cooperativity between trans and cis interactions in cadherin-mediated junction formation. PNAS 107:17592–97
     [Google Scholar]
127. 127.

     Wu Y, Kanchanawong P, Zaidel-Bar R 2015. Actin-delimited adhesion-independent clustering of E-cadherin forms the nanoscale building blocks of adherens junctions. Dev. Cell 32:139–54
     [Google Scholar]
128. 128.

     Wu Y, Vendome J, Shapiro L, Ben-Shaul A, Honig B 2011. Transforming binding affinities from three dimensions to two with application to cadherin clustering. Nature 475:510–13
     [Google Scholar]
129. 129.

     Xu Q, Lin WC, Petit RS, Groves JT 2011. EphA2 receptor activation by monomeric Ephrin-A1 on supported membranes. Biophys. J. 101:2731–39
     [Google Scholar]
130. 130.

     Yang B, Lieu ZZ, Wolfenson H, Hameed FM, Bershadsky AD, Sheetz MP 2016. Mechanosensing controlled directly by tyrosine kinases. Nano Lett 16:5951–61
     [Google Scholar]
131. 131.

     Yao M, Qiu W, Liu R, Efremov AK, Cong P et al. 2014. Force-dependent conformational switch of α-catenin controls vinculin binding. Nat. Commun. 5:4525
     [Google Scholar]
132. 132.

     Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M 2010. α-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12:533–42
     [Google Scholar]
133. 133.

     Yu CH, Groves JT 2010. Engineering supported membranes for cell biology. Med. Biol. Eng. Comput. 48:955–63
     [Google Scholar]
134. 134.

     Yu CH, Law JB, Suryana M, Low HY, Sheetz MP 2011. Early integrin binding to Arg-Gly-Asp peptide activates actin polymerization and contractile movement that stimulates outward translocation. PNAS 108:20585–90
     [Google Scholar]
135. 135.

     Yu CH, Rafiq NB, Cao F, Zhou Y, Krishnasamy A et al. 2015. Integrin-β3 clusters recruit clathrin-mediated endocytic machinery in the absence of traction force. Nat. Commun. 6:8672
     [Google Scholar]
136. 136.

     Yu CH, Rafiq NB, Krishnasamy A, Hartman KL, Jones GE et al. 2013. Integrin-matrix clusters form podosome-like adhesions in the absence of traction forces. Cell Rep 5:1456–68
     [Google Scholar]
137. 137.

     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
     [Google Scholar]
138. 138.

     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
     [Google Scholar]
139. 139.

     Yu Y, Smoligovets AA, Groves JT 2013. Modulation of T cell signaling by the actin cytoskeleton. J. Cell Sci. 126:1049–58
     [Google Scholar]