The FRET signatures of noninteracting proteins in membranes: Simulations and experiments

Biophysical Journal

Volumn 106, Issue 6, 2014, Pages 1309-1317

  King, Christopher ^a   Sarabipour, Sarvenaz ^a   Byrne, Patrick ^a   Leahy, Daniel J ^a,b   Hristova, Kalina ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR RECEPTOR 1; GREEN FLUORESCENT PROTEIN; PROTEIN BINDING;

ANIMAL; CELL MEMBRANE; CHO CELL LINE; COMPUTER SIMULATION; CRICETULUS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; HAMSTER; HEK293 CELL LINE; HUMAN; METABOLISM; PROCEDURES; PROTEIN MULTIMERIZATION;

ANIMALS; CELL MEMBRANE; CHO CELLS; COMPUTER SIMULATION; CRICETINAE; CRICETULUS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECEPTOR, ERBB-2; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1;

EID: 84896501967     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.01.039     Document Type: Article

References (50)

1. J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 103 2000 211 225
2. L. He, and K. Hristova Physical-chemical principles underlying RTK activation, and their implications for human disease Biochim. Biophys. Acta 1818 2012 995 1005
3. M.A. Lemmon, and J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 141 2010 1117 1134
4. 8 on calcium transport and molecular dynamics in cardiac sarcoplasmic reticulum Biochemistry 35 1996 13393 13399 (Pubitemid 26349434)
5. 2+-ATPase by cryoelectron microscopy Biophys. J. 81 2001 884 894 (Pubitemid 32721459)
6. A.K. Kenworthy, and M. Edidin Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100 Å using imaging fluorescence resonance energy transfer J. Cell Biol. 142 1998 69 84 (Pubitemid 28341141)
7. A.K. Kenworthy, N. Petranova, and M. Edidin High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes Mol. Biol. Cell 11 2000 1645 1655 (Pubitemid 30307902)
8. D.R. Singh, and M.M. Mohammad V. Raicu Determination of the quaternary structure of a bacterial ATP-binding cassette (ABC) transporter in living cells Integr Biol (Camb) 5 2013 312 323
9. V. Raicu, and M.R. Stoneman D.K. Saldin Determination of supramolecular structure and spatial distribution of protein complexes in living cells Nat. Photonics 3 2009 107 113
10. H.M. Chen, H.L. Puhl 3rd, and S.R. Ikeda Estimating protein-protein interaction affinity in living cells using quantitative Förster resonance energy transfer measurements J. Biomed. Opt. 12 2007 054011
11. T. Förster Intermolecular energy migration and fluorescence Ann. Phys. 2 1948 55 75
12. N.C. Shaner, P.A. Steinbach, and R.Y. Tsien A guide to choosing fluorescent proteins Nat. Methods 2 2005 905 909 (Pubitemid 43108726)
13. M.A. Rizzo, and G.H. Springer D.W. Piston An improved cyan fluorescent protein variant useful for FRET Nat. Biotechnol. 22 2004 445 449 (Pubitemid 38451376)
14. D.W. Piston, and G.J. Kremers Fluorescent protein FRET: the good, the bad and the ugly Trends Biochem. Sci. 32 2007 407 414 (Pubitemid 47369164)
15. P.K. Wolber, and B.S. Hudson An analytic solution to the Förster energy transfer problem in two dimensions Biophys. J. 28 1979 197 210 (Pubitemid 10196482)
16. W.C. Wimley, and S.H. White Determining the membrane topology of peptides by fluorescence quenching Biochemistry 39 2000 161 170 (Pubitemid 30033331)
17. Y.O. Posokhov, and M. Merzlyakov A.S. Ladokhin A simple "proximity" correction for Förster resonance energy transfer efficiency determination in membranes using lifetime measurements Anal. Biochem. 380 2008 134 136
18. M. You, and E. Li K. Hristova Förster resonance energy transfer in liposomes: measurements of transmembrane helix dimerization in the native bilayer environment Anal. Biochem. 340 2005 154 164 (Pubitemid 40404111)
19. B. Snyder, and E. Freire Fluorescence energy transfer in two dimensions. A numeric solution for random and nonrandom distributions Biophys. J. 40 1982 137 148
20. E. Freire, and B. Snyder Quantitative characterization of the lateral distribution of membrane proteins within the lipid bilayer Biophys. J. 37 1982 617 624
21. E. Li, and J. Placone K. Hristova Quantitative measurements of protein interactions in a crowded cellular environment Anal. Chem. 80 2008 5976 5985
22. L. Chen, and L. Novicky K. Hristova Measuring the energetics of membrane protein dimerization in mammalian membranes J. Am. Chem. Soc. 132 2010 3628 3635
23. R.E. Scott Plasma membrane vesiculation: a new technique for isolation of plasma membranes Science 194 1976 743 745
24. N. Del Piccolo, and J. Placone K. Hristova Production of plasma membrane vesicles with chloride salts and their utility as a cell membrane mimetic for biophysical characterization of membrane protein interactions Anal. Chem. 84 2012 8650 8655
25. S. Sarabipour, and K. Hristova Glycophorin A transmembrane domain dimerization in plasma membrane vesicles derived from CHO, HEK 293T, and A431 cells Biochim. Biophys. Acta 1828 2013 1829 1833
26. S. Sarabipour, C. King, and K. Hristova Uninduced high-yield bacterial expression of fluorescent proteins Anal. Biochem. 449C 2013 155 157
27. J. Placone, and K. Hristova Direct assessment of the effect of the Gly380Arg achondroplasia mutation on FGFR3 dimerization using quantitative imaging FRET PLoS ONE 7 2012 e46678
28. S. Sarabipour, and K. Hristova FGFR3 transmembrane domain interactions persist in the presence of its extracellular domain Biophys. J. 105 2013 165 171
29. J.U. Bowie Membrane protein folding: how important are hydrogen bonds? Curr. Opin. Struct. Biol. 21 2011 42 49
30. W.C. Wimley, and S.H. White Designing transmembrane α-helices that insert spontaneously Biochemistry 39 2000 4432 4442 (Pubitemid 30212660)
31. M. Kim, C.V. Carman, and T.A. Springer Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins Science 301 2003 1720 1725 (Pubitemid 37174365)
32. A.K. Kenworthy Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy Methods 24 2001 289 296 (Pubitemid 32846434)
33. L. Chen, and J. Placone K. Hristova The extracellular domain of fibroblast growth factor receptor 3 inhibits ligand-independent dimerization Sci. Signal. 3 2010 ra86
34. W.P. Russ, and D.M. Engelman TOXCAT: a measure of transmembrane helix association in a biological membrane Proc. Natl. Acad. Sci. USA 96 1999 863 868 (Pubitemid 29072149)
35. H. Hong, and J.U. Bowie Dramatic destabilization of transmembrane helix interactions by features of natural membrane environments J. Am. Chem. Soc. 133 2011 11389 11398
36. S.T. Low-Nam, and K.A. Lidke D.S. Lidke ErbB1 dimerization is promoted by domain co-confinement and stabilized by ligand binding Nat. Struct. Mol. Biol. 18 2011 1244 1249
37. T.W.J. Gadella Jr., and T.M. Jovin Oligomerization of epidermal growth factor receptors on A431 cells studied by time-resolved fluorescence imaging microscopy. A stereochemical model for tyrosine kinase receptor activation J. Cell Biol. 129 1995 1543 1558
38. M. Martin-Fernandez, and D.T. Clarke G.R. Jones Preformed oligomeric epidermal growth factor receptors undergo an ectodomain structure change during signaling Biophys. J. 82 2002 2415 2427 (Pubitemid 34441281)
39. Y. Sako, S. Minoghchi, and T. Yanagida Single-molecule imaging of EGFR signalling on the surface of living cells Nat. Cell Biol. 2 2000 168 172
40. P. Nagy, and J. Claus D.J. Arndt-Jovin Distribution of resting and ligand-bound ErbB1 and ErbB2 receptor tyrosine kinases in living cells using number and brightness analysis Proc. Natl. Acad. Sci. USA 107 2010 16524 16529
41. M.J. Van de Vijver, R. Kumar, and J. Mendelsohn Ligand-induced activation of A431 cell epidermal growth factor receptors occurs primarily by an autocrine pathway that acts upon receptors on the surface rather than intracellularly J. Biol. Chem. 266 1991 7503 7508 (Pubitemid 21906393)
42. A.H. Clayton, and S.G. Orchard A.W. Burgess Predominance of activated EGFR higher-order oligomers on the cell surface Growth Factors 26 2008 316 324 (Pubitemid 352781844)
43. N. Jura, and N.F. Endres J. Kuriyan Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment Cell 137 2009 1293 1307
44. K.W. Thiel, and G. Carpenter Epidermal growth factor receptor juxtamembrane region regulates allosteric tyrosine kinase activation Proc. Natl. Acad. Sci. USA 104 2007 19238 19243
45. M.A. Lemmon, and Z.M. Bu J. Schlessinger Two EGF molecules contribute additively to stabilization of the EGFR dimer EMBO J. 16 1997 281 294 (Pubitemid 27049386)
46. K.M. Ferguson, and M.B. Berger M.A. Lemmon EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization Mol. Cell 11 2003 507 517 (Pubitemid 36297057)
47. H.S. Cho, and D.J. Leahy Structure of the extracellular region of HER3 reveals an interdomain tether Science 297 2002 1330 1333 (Pubitemid 34913167)
48. A.W. Burgess, and H.S. Cho S. Yokoyama An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors Mol. Cell 12 2003 541 552 (Pubitemid 37222478)
49. H.S. Cho, and K. Mason D.J. Leahy Structure of the extracellular region of HER2 alone and in complex with the Herceptin Fab Nature 421 2003 756 760 (Pubitemid 36227628)
50. I. Chung, and R. Akita I. Mellman Spatial control of EGF receptor activation by reversible dimerization on living cells Nature 464 2010 783 787