Spatial organization of epha2 at the cell-cell interface modulates trans-endocytosis of ephrina1

Biophysical Journal

Volumn 106, Issue 10, 2014, Pages 2196-2205

  Greene, Adrienne C ^a   Lord, Samuel J ^a   Tian, Aiwei ^a   Rhodes, Christopher ^a,b   Kai, Hiroyuki ^a   Groves, Jay T ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; ADAM10 PROTEIN, HUMAN; CLATHRIN; DYNAMIN; EPHRIN A1; EPHRIN RECEPTOR A2; LIGAND; MEMBRANE PROTEIN; SECRETASE;

ANIMAL; BIOMECHANICS; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; ENDOCYTOSIS; HUMAN; METABOLISM; PROTEIN CONFORMATION; SF9 CELL LINE; SPODOPTERA; TUMOR CELL LINE;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BIOMECHANICAL PHENOMENA; CELL LINE, TUMOR; CELL MEMBRANE; CLATHRIN; DYNAMINS; ENDOCYTOSIS; EPHRIN-A1; HUMANS; LIGANDS; MEMBRANE PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; RECEPTOR, EPHA2; SF9 CELLS; SPODOPTERA;

EID: 84901259701     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.03.043     Document Type: Article

References (72)

1. M. Lackmann, and A.W. Boyd Eph, a protein family coming of age: more confusion, insight, or complexity? Sci. Signal. 1 2008 re2
2. R.H. Adams, and R. Klein Eph receptors and ephrin ligands: essential mediators of vascular development Trends Cardiovasc. Med. 10 2000 183 188
3. R.H. Adams, and G.A. Wilkinson R. Klein Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis Genes Dev. 13 1999 295 306
4. A.M. Mohamed, and I.D. Chin-Sang Characterization of loss-of-function and gain-of-function Eph receptor tyrosine kinase signaling in C. elegans axon targeting and cell migration Dev. Biol. 290 2006 164 176
5. H. Miao, and K. Strebhardt B. Wang Inhibition of integrin-mediated cell adhesion but not directional cell migration requires catalytic activity of EphB3 receptor tyrosine kinase. Role of Rho family small GTPases J. Biol. Chem. 280 2005 923 932
6. Eph Nomenclature Committee Unified nomenclature for Eph family receptors and their ligands, the ephrins Cell 90 1997 403 404
7. H. Miao, and B. Wang EphA receptor signaling - complexity and emerging themes Semin. Cell Dev. Biol. 23 2012 16 25
8. J. Wykosky, and W. Debinski The EphA2 receptor and ephrinA1 ligand in solid tumors: function and therapeutic targeting Mol. Cancer Res. 6 2008 1795 1806
9. D.N. Arvanitis, and A. Davy Regulation and misregulation of Eph/ephrin expression Cell Adhes. Migr. 6 2012 131 137
10. D.P. Zelinski, and N.D. Zantek M.S. Kinch EphA2 overexpression causes tumorigenesis of mammary epithelial cells Cancer Res. 61 2001 2301 2306
11. K. Ogawa, and R. Pasqualini E.B. Pasquale The ephrin-A1 ligand and its receptor, EphA2, are expressed during tumor neovascularization Oncogene 19 2000 6043 6052
12. M. Macrae, and R.M. Neve F. McCormick A conditional feedback loop regulates Ras activity through EphA2 Cancer Cell 8 2005 111 118
13. D. Vaught, D.M. Brantley-Sieders, and J. Chen Eph receptors in breast cancer: roles in tumor promotion and tumor suppression Breast Cancer Res. 10 2008 217 224
14. M. Pan Overexpression of EphA2 gene in invasive human breast cancer and its association with hormone receptor status J. Clin. Oncol. 23 2005 9583 9584
15. G. Zhuang, and D.M. Brantley-Sieders J. Chen Elevation of receptor tyrosine kinase EphA2 mediates resistance to trastuzumab therapy Cancer Res. 70 2010 299 308
16. P. Kaenel, M. Mosimann, and A.-C. Andres The multifaceted roles of Eph/ephrin signaling in breast cancer Cell Adhes. Migr. 6 2012 138 147
17. H. Miao, and D.-Q. Li B. Wang EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt Cancer Cell 16 2009 9 20
18. M.J. Bissell, and D. Radisky Putting tumours in context Nat. Rev. Cancer 1 2001 46 54
19. C.M. Nelson, and M.M. Vanduijn M.J. Bissell Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures Science 314 2006 298 300
20. K. Salaita, and P.M. Nair J.T. Groves Restriction of receptor movement alters cellular response: physical force sensing by EphA2 Science 327 2010 1380 1385
21. Q. Xu, and W.-C. Lin J.T. Groves EphA2 receptor activation by monomeric Ephrin-A1 on supported membranes Biophys. J. 101 2011 2731 2739
22. T. Lohmüller, Q. Xu, and J.T. Groves Nanoscale obstacle arrays frustrate transport of EphA2-Ephrin-A1 clusters in cancer cell lines Nano Lett. 13 2013 3059 3064
23. S. Polo, and P.P. Di Fiore Endocytosis conducts the cell signaling orchestra Cell 124 2006 897 900
24. J. Liu, and Y. Sun D.G. Drubin Mechanochemical crosstalk during endocytic vesicle formation Curr. Opin. Cell Biol. 22 2010 36 43
25. H.T. McMahon, and E. Boucrot Molecular mechanism and physiological functions of clathrin-mediated endocytosis Nat. Rev. Mol. Cell Biol. 12 2011 517 533
26. C.A. Parachoniak, and M. Park Dynamics of receptor trafficking in tumorigenicity Trends Cell Biol. 22 2012 231 240
27. H.S. Wiley, and P.M. Burke Regulation of receptor tyrosine kinase signaling by endocytic trafficking Traffic 2 2001 12 18
28. L. Sadowski, I. Pilecka, and M. Miaczynska Signaling from endosomes: location makes a difference Exp. Cell Res. 315 2009 1601 1609
29. D.J. Marston, S. Dickinson, and C.D. Nobes Rac-dependent trans-endocytosis of ephrinBs regulates Eph-ephrin contact repulsion Nat. Cell Biol. 5 2003 879 888
30. M. Zimmer, and A. Palmer R. Klein EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion Nat. Cell Biol. 5 2003 869 878
31. M.E. Pitulescu, and R.H. Adams Eph/ephrin molecules - a hub for signaling and endocytosis Genes Dev. 24 2010 2480 2492
32. G. Zhuang, and S. Hunter J. Chen Regulation of EphA2 receptor endocytosis by SHIP2 lipid phosphatase via phosphatidylinositol 3-Kinase-dependent Rac1 activation J. Biol. Chem. 282 2007 2683 2694
33. F. Irie, and M. Okuno Y. Yamaguchi EphrinB-EphB signalling regulates clathrin-mediated endocytosis through tyrosine phosphorylation of synaptojanin 1 Nat. Cell Biol. 7 2005 501 509
34. J.T. Groves, and S.G. Boxer Electric field-induced concentration gradients in planar supported bilayers Biophys. J. 69 1995 1972 1975
35. J.T. Groves, C. Wülfing, and S.G. Boxer Electrical manipulation of glycan-phosphatidyl inositol-tethered proteins in planar supported bilayers Biophys. J. 71 1996 2716 2723
36. J. Wykosky, and E. Palma W. Debinski Soluble monomeric EphrinA1 is released from tumor cells and is a functional ligand for the EphA2 receptor Oncogene 27 2008 7260 7273
37. C.M. Lema Tomé, and E. Palma W. Debinski Structural and functional characterization of monomeric EphrinA1 binding site to EphA2 receptor J. Biol. Chem. 287 2012 14012 14022
38. A. Beauchamp, and M.O. Lively W. Debinski EphrinA1 is released in three forms from cancer cells by matrix metalloproteases Mol. Cell. Biol. 32 2012 3253 3264
39. J.T. Groves, N. Ulman, and S.G. Boxer Micropatterning fluid lipid bilayers on solid supports Science 275 1997 651 653
40. A.L. DeMond, and K.D. Mossman J.T. Groves T cell receptor microcluster transport through molecular mazes reveals mechanism of translocation Biophys. J. 94 2008 3286 3292
41. K.D. Mossman, and G. Campi M.L. Dustin Altered TCR signaling from geometrically repatterned immunological synapses Science 310 2005 1191 1193
42. P.W. Janes, and N. Saha D.B. Nikolov Adam meets Eph: an ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans Cell 123 2005 291 304
43. L. Atapattu, and N. Saha P.W. Janes Antibodies binding the ADAM10 substrate recognition domain inhibit Eph function J. Cell Sci. 125 2012 6084 6093
44. W.-C. Lin, and C.H. Yu J.T. Groves Supported membrane formation, characterization, functionalization, and patterning for application in biological science and technology Curr. Protoc. Chem. Biol 2 2010 235 269
45. J.A. Nye, and J.T. Groves Kinetic control of histidine-tagged protein surface density on supported lipid bilayers Langmuir 24 2008 4145 4149
46. J.B. Doyon, and B. Zeitler D.G. Drubin Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells Nat. Cell Biol. 13 2011 331 337
47. S.B. Triffo, and H.H. Huang J.T. Groves Monitoring lipid anchor organization in cell membranes by PIE-FCCS J. Am. Chem. Soc. 134 2012 10833 10842
48. T.P. Stauffer, S. Ahn, and T. Meyer Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells Curr. Biol. 8 1998 343 346
49. B.M. Burkel, G. von Dassow, and W.M. Bement Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin Cell Motil. Cytoskeleton 64 2007 822 832
50. A. Edelstein, and N. Amodaj N. Stuurman Computer control of microscopes using μManager Curr. Protoc. Mol. Biol. 92 2010 1 22
51. J. Schindelin, and I. Arganda-Carreras A. Cardona Fiji: an open-source platform for biological-image analysis Nat. Methods 9 2012 676 682
52. S. Bolte, and F.P. Cordelières A guided tour into subcellular colocalization analysis in light microscopy J. Microsc. 224 2006 213 232
53. E.F. Pettersen, and T.D. Goddard T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
54. A. Fotin, and Y. Cheng T. Walz Molecular model for a complete clathrin lattice from electron cryomicroscopy Nature 432 2004 573 579
55. E. Seiradake, and K. Harlos E.Y. Jones An extracellular steric seeding mechanism for Eph-ephrin signaling platform assembly Nat. Struct. Mol. Biol. 17 2010 398 402
56. O. Berger, O. Edholm, and F. Jähnig Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72 1997 2002 2013
57. J. Domański, and P.J. Stansfeld O. Beckstein Lipidbook: a public repository for force-field parameters used in membrane simulations J. Membr. Biol. 236 2010 255 258
58. L. von Kleist, and W. Stahlschmidt V. Haucke Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition Cell 146 2011 471 484
59. D. Dutta, and C.D. Williamson J.G. Donaldson Pitstop 2 is a potent inhibitor of clathrin-independent endocytosis PLoS ONE 7 2012 e45799
60. J.S. Fridman, and E. Caulder K. Vaddi Selective inhibition of ADAM metalloproteases as a novel approach for modulating ErbB pathways in cancer Clin. Cancer Res. 13 2007 1892 1902
61. B.-B.S. Zhou, and M. Peyton P.A. Scherle Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer Cancer Cell 10 2006 39 50
62. C. Le Roy, and J.L. Wrana Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling Nat. Rev. Mol. Cell Biol. 6 2005 112 126
63. J. Heuser, and T. Kirchhausen Deep-etch views of clathrin assemblies J. Ultrastruct. Res. 92 1985 1 27
64. S. Boulant, and C. Kural T. Kirchhausen Actin dynamics counteract membrane tension during clathrin-mediated endocytosis Nat. Cell Biol. 13 2011 1124 1131
65. J.C. Stachowiak, and E.M. Schmid C.C. Hayden Membrane bending by protein-protein crowding Nat. Cell Biol. 14 2012 944 949
66. R. Parthasarathy, and J.T. Groves Curvature and spatial organization in biological membranes Soft Matter 3 2007 24 33
67. R. Parthasarathy, C.H. Yu, and J.T. Groves Curvature-modulated phase separation in lipid bilayer membranes Langmuir 22 2006 5095 5099
68. P. Rangamani, and A. Agrawal D.J. Steigmann Interaction between surface shape and intra-surface viscous flow on lipid membranes Biomech. Model. Mechanobiol. 12 2013 833 845
69. S. Sigismund, and E. Argenzio P.P. Di Fiore Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation Dev. Cell 15 2008 209 219
70. A. Carroll-Portillo, and K. Spendier J.A. Timlin Formation of a mast cell synapse: Fc epsilon RI membrane dynamics upon binding mobile or immobilized ligands on surfaces J. Immunol. 184 2010 1328 1338
71. N.C. Hartman, J.A. Nye, and J.T. Groves Cluster size regulates protein sorting in the immunological synapse Proc. Natl. Acad. Sci. USA 106 2009 12729 12734
72. H.-Q. Xi, and X.-S. Wu L. Chen Eph receptors and ephrins as targets for cancer therapy J. Cell. Mol. Med. 16 2012 2894 2909