Detection and quantification of biomolecular association in living cells using single-molecule microscopy

Methods in Enzymology

Volumn 505, Issue , 2012, Pages 159-186

  Brameshuber, Mario ^a,b   Schütz, Gerhard J ^a,b  

^a JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

^b VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

brightness; diffusion; lipid membranes; photobleaching; plasma membrane; protein interactions; rafts; stoichiometry; two color co localization

Indexed keywords

CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; FLUORESCENT DYE; NANOPARTICLE; PROTEIN KINASE LCK;

BLEACHING; CELL COMPOSITION; CELL LABELING; CELL MEMBRANE; CELL MOTILITY; CYTOSOL; DIFFUSION; EXCITATION; MEMBRANE; MICROSCOPY; MOLECULAR BIOLOGY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVIEW; SINGLE MOLECULE MICROSCOPY; STOICHIOMETRY;

EID: 84856458463     PISSN: 00766879     EISSN: 15577988     Source Type: Book Series    
DOI: 10.1016/B978-0-12-388448-0.00017-6     Document Type: Chapter

References (87)

1. B. Alberts The cell as a collection of protein machines: Preparing the next generation of molecular biologists Cell 92 1998 291 294 (Pubitemid 28093007)
2. S.R. Arumugam, T.H. Lee, and S.J. Benkovic Investigation of stoichiometry of T4 bacteriophage helicase loader protein (gp59) J. Biol. Chem. 284 2009 29283 29289
3. D. Axelrod, D.E. Koppel, J. Schlessinger, E. Elson, and W.W. Webb Mobility measurement by analysis of fluorescence photobleaching recovery kinetics Biophys. J. 16 1976 1055 1069
4. D. Axelrod, T.P. Burghardt, and N.L. Thompson Total internal reflection fluorescence Annu. Rev. Biophys. Bioeng. 13 1984 247 268
5. T. Bernas, M. Zarebski, P.R. Cook, and J.W. Dobrucki Minimizing photobleaching during confocal microscopy of fluorescent probes bound to chromatin: Role of anoxia and photon flux J. Microsc. 215 2004 281 296 (Pubitemid 39233716)
6. M. Bossi, J. Folling, V.N. Belov, V.P. Boyarskiy, R. Medda, A. Egner, C. Eggeling, A. Schonle, and S.W. Hell Multicolor far-field fluorescence nanoscopy through isolated detection of distinct molecular species Nano Lett. 8 2008 2463 2468
7. M. Brameshuber, J. Weghuber, V. Ruprecht, I. Gombos, I. Horvath, L. Vigh, P. Eckerstorfer, E. Kiss, H. Stockinger, and G.J. Schutz Imaging of mobile long-lived nanoplatforms in the live cell plasma membrane J. Biol. Chem. 285 2010 41765 41771
8. D.A. Brown, and J.K. Rose Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface Cell 68 1992 533 544
9. Y. Chen, J.D. Muller, P.T. So, and E. Gratton The photon counting histogram in fluorescence fluctuation spectroscopy Biophys. J. 77 1999 553 567 (Pubitemid 29305251)
10. D.E. Clapham TRP channels as cellular sensors Nature 426 2003 517 524 (Pubitemid 37522633)
11. S.K. Das, M. Darshi, S. Cheley, M.I. Wallace, and H. Bayley Membrane protein stoichiometry determined from the step-wise photobleaching of dye-labelled subunits Chembiochem 8 2007 994 999 (Pubitemid 47183616)
12. C. Dietrich, Z.N. Volovyk, M. Levi, N.L. Thompson, and K. Jacobson Partitioning of Thy-1, GM1, and cross-linked phospholipid analogs into lipid rafts reconstituted in supported model membrane monolayers Proc. Natl. Acad. Sci. USA 98 2001 10642 10647 (Pubitemid 32878674)
13. M.A. Digman, R. Dalal, A.F. Horwitz, and E. Gratton Mapping the number of molecules and brightness in the laser scanning microscope Biophys. J. 94 2008 2320 2332
14. M.A. Digman, P.W. Wiseman, C. Choi, A.R. Horwitz, and E. Gratton Stoichiometry of molecular complexes at adhesions in living cells Proc. Natl. Acad. Sci. USA 106 2009 2170 2175
15. A.D. Douglass, and R.D. Vale Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells Cell 121 2005 937 950 (Pubitemid 40806424)
16. K. Drbal, M. Moertelmaier, C. Holzhauser, A. Muhammad, E. Fuertbauer, S. Howorka, M. Hinterberger, H. Stockinger, and G.J. Schütz Single-molecule microscopy reveals heterogeneous dynamics of lipid raft components upon TCR engagement Int. Immunol. 19 2007 675 684 (Pubitemid 47072210)
17. M.J. Eck, S.K. Atwell, S.E. Shoelson, and S.C. Harrison Structure of the regulatory domains of the Src-family tyrosine kinase Lck Nature 368 1994 764 769 (Pubitemid 24153420)
18. M. Edidin Translational diffusion of membrane proteins P. Yeagle, The Structure of Biological Membranes 1992 CRC Press Boca Raton, FL 539 572
19. C. Eggeling, J. Widengren, R. Rigler, and C.A.M. Seidel Photobleaching of fluorescent dyes under conditions used for single-molecule detection: Evidence of two-step photolysis Anal. Chem. 70 1998 2651 2659
20. C. Espenel, E. Margeat, P. Dosset, C. Arduise, C. Le Grimellec, C.A. Royer, C. Boucheix, E. Rubinstein, and P.E. Milhiet Single-molecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web J. Cell Biol. 182 2008 765 776
21. S. Feske, Y. Gwack, M. Prakriya, S. Srikanth, S.H. Puppel, B. Tanasa, P.G. Hogan, R.S. Lewis, M. Daly, and A. Rao A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function Nature 441 2006 179 185
22. L.J. Foster, C.L. De Hoog, and M. Mann Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors Proc. Natl. Acad. Sci. USA 100 2003 5813 5818 (Pubitemid 36576890)
23. M.F. Garcia-Parajo, G.M. Segers-Nolten, J.A. Veerman, J. Greve, and N.F. van Hulst Real-time light-driven dynamics of the fluorescence emission in single green fluorescent protein molecules Proc. Natl. Acad. Sci. USA 97 2000 7237 7242 (Pubitemid 30431447)
24. G.R. Hammond, Y. Sim, L. Lagnado, and R.F. Irvine Reversible binding and rapid diffusion of proteins in complex with inositol lipids serves to coordinate free movement with spatial information J. Cell Biol. 184 2009 297 308
25. T. Harder, P. Scheiffele, P. Verkade, and K. Simons Lipid domain structure of the plasma membrane revealed by patching of membrane components J. Cell Biol. 141 1998 929 942 (Pubitemid 28243961)
26. G.S. Harms, L. Cognet, P.H. Lommerse, G.A. Blab, H. Kahr, R. Gamsjager, H.P. Spaink, N.M. Soldatov, C. Romanin, and T. Schmidt Single-molecule imaging of l-type Ca(2 +) channels in live cells Biophys. J. 81 2001 2639 2646 (Pubitemid 33020051)
27. R.P. Haugland Handbook of Fluorescent Probes and Research Chemicals 1992 Molecular Probes Inc. Eugene, Oregon, USA
28. P.N. Hedde, J. Fuchs, F. Oswald, J. Wiedenmann, and G.U. Nienhaus Online image analysis software for photoactivation localization microscopy Nat. Methods 6 2009 689 690
29. R. Henriques, M. Lelek, E.F. Fornasiero, F. Valtorta, C. Zimmer, and M.M. Mhlanga QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ Nat. Methods 7 2010 339 340
30. J.A. Hern, A.H. Baig, G.I. Mashanov, B. Birdsall, J.E. Corrie, S. Lazareno, J.E. Molloy, and N.J. Birdsall Formation and dissociation of M1 muscarinic receptor dimers seen by total internal reflection fluorescence imaging of single molecules Proc. Natl. Acad. Sci. USA 107 2010 2693 2698
31. E.A. Jares-Erijman, and T.M. Jovin FRET imaging Nat. Biotechnol. 21 2003 1387 1395 (Pubitemid 37356626)
32. W. Ji, P. Xu, Z. Li, J. Lu, L. Liu, Y. Zhan, Y. Chen, B. Hille, T. Xu, and L. Chen Functional stoichiometry of the unitary calcium-release-activated calcium channel Proc. Natl. Acad. Sci. USA 105 2008 13668 13673
33. H.-J. Kaiser, D. Lingwood, I. Levental, J.L. Sampaio, L. Kalvodova, L. Rajendran, and K. Simons Order of lipid phases in model and plasma membranes Proc. Natl. Acad. Sci. USA 106 2009 16645 16650
34. R.S. Kasai, K.G.N. Suzuki, E.R. Prossnitz, I. Koyama-Honda, C. Nakada, T.K. Fujiwara, and A. Kusumi Full characterization of GPCR monomer-dimer dynamic equilibrium by single molecule imaging J. Cell Biol. 192 2011 463 480
35. P. Kask, K. Palo, D. Ullmann, and K. Gall Fluorescence-intensity distribution analysis and its application in biomolecular detection technology Proc. Natl. Acad. Sci. USA 96 1999 13756 13761
36. A.K. Kenworthy, B.J. Nichols, C.L. Remmert, G.M. Hendrix, M. Kumar, J. Zimmerberg, and J. Lippincott-Schwartz Dynamics of putative raft-associated proteins at the cell surface J. Cell Biol. 165 2004 735 746 (Pubitemid 38765774)
37. C.A. Konopka, and S.Y. Bednarek Variable-angle epifluorescence microscopy: A new way to look at protein dynamics in the plant cell cortex Plant J. 53 2008 186 196 (Pubitemid 350265236)
38. I. Koyama-Honda, K. Ritchie, T. Fujiwara, R. Iino, H. Murakoshi, R.S. Kasai, and A. Kusumi Fluorescence imaging for monitoring the colocalization of two single molecules in living cells Biophys. J. 88 2005 2126 2136 (Pubitemid 40976221)
39. A. Kusumi, I. Koyama-Honda, and K. Suzuki Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts Traffic 5 2004 213 230 (Pubitemid 38455745)
40. M.C. Leake, J.H. Chandler, G.H. Wadhams, F. Bai, R.M. Berry, and J.P. Armitage Stoichiometry and turnover in single, functioning membrane protein complexes Nature 443 2006 355 358 (Pubitemid 44435156)
41. M.C. Leake, N.P. Greene, R.M. Godun, T. Granjon, G. Buchanan, S. Chen, R.M. Berry, T. Palmer, and B.C. Berks Variable stoichiometry of the TatA component of the twin-arginine protein transport system observed by in vivo single-molecule imaging Proc. Natl. Acad. Sci. USA 105 2008 15376 15381
42. J. Madl, J. Weghuber, R. Fritsch, I. Derler, M. Fahrner, I. Frischauf, B. Lackner, C. Romanin, and G.J. Schutz Resting state orai1 diffuses as homotetramer in the plasma membrane of live mammalian cells J. Biol. Chem. 285 2010 41135 41142
43. S. Manley, J.M. Gillette, G.H. Patterson, H. Shroff, H.F. Hess, E. Betzig, and J. Lippincott-Schwartz High-density mapping of single-molecule trajectories with photoactivated localization microscopy Nat. Methods 5 2008 155 157 (Pubitemid 351181741)
44. O. Mignen, J.L. Thompson, and T.J. Shuttleworth Orai1 subunit stoichiometry of the mammalian CRAC channel pore J. Physiol. 586 2008 419 425
45. G. Milligan G protein-coupled receptor dimerization: Function and ligand pharmacology Mol. Pharmacol. 66 2004 1 7 (Pubitemid 38822080)
46. M. Mittelbrunn, M. Yanez-Mo, D. Sancho, A. Ursa, and F. Sanchez-Madrid Cutting edge: Dynamic redistribution of tetraspanin CD81 at the central zone of the immune synapse in both T lymphocytes and APC J. Immunol. 169 2002 6691 6695 (Pubitemid 36899253)
47. M. Moertelmaier, M. Brameshuber, M. Linimeier, G.J. Schütz, and H. Stockinger Thinning out clusters while conserving stoichiometry of labeling Appl. Phys. Lett. 87 2005 263903
48. K.I. Mortensen, L.S. Churchman, J.A. Spudich, and H. Flyvbjerg Optimized localization analysis for single-molecule tracking and super-resolution microscopy Nat. Methods 7 2010 377 381
49. S. Munro Lipid rafts: Elusive or illusive? Cell 115 2003 377 388 (Pubitemid 37456801)
50. N. Ottschytsch, A. Raes, D. Van Hoorick, and D.J. Snyders Obligatory heterotetramerization of three previously uncharacterized Kv channel alpha-subunits identified in the human genome Proc. Natl. Acad. Sci. USA 99 2002 7986 7991 (Pubitemid 34650992)
51. C.Y. Park, P.J. Hoover, F.M. Mullins, P. Bachhawat, E.D. Covington, S. Raunser, T. Walz, K.C. Garcia, R.E. Dolmetsch, and R.S. Lewis STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1 Cell 136 2009 876
52. A. Penna, A. Demuro, A.V. Yeromin, S.L. Zhang, O. Safrina, I. Parker, and M.D. Cahalan The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers Nature 456 2008 116 120
53. A. Pertsinidis, Y. Zhang, and S. Chu Subnanometre single-molecule localization, registration and distance measurements Nature 466 2010 647 651
54. L.J. Pike Rafts defined J. Lipid Res. 47 2006 1597 1598
55. T.A. Planchon, L. Gao, D.E. Milkie, M.W. Davidson, J.A. Galbraith, C.G. Galbraith, and E. Betzig Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination Nat. Methods 8 2011 417 423
56. H. Qian, and E.L. Elson Distribution of molecular aggregation by analysis of fluctuation moments Proc. Natl. Acad. Sci. USA 87 1990 5479 5483
57. J.G. Ritter, R. Veith, J.P. Siebrasse, and U. Kubitscheck High-contrast single-particle tracking by selective focal plane illumination microscopy Opt. Express 16 2008 7142 7152 (Pubitemid 351697398)
58. V. Ruprecht, M. Brameshuber, and G.J. Schütz Two-color single molecule tracking combined with photobleaching for the detection of rare molecular interactions in fluid biomembranes Soft Matter 6 2010 568 581
59. Y. Sako, and T. Uyemura Total internal reflection fluorescence microscopy for single-molecule imaging in living cells Cell Struct. Funct. 27 2002 357 365 (Pubitemid 36149990)
60. J. Schlessinger Ligand-induced, receptor-mediated dimerization and activation of EGF receptor Cell 110 2002 669 672 (Pubitemid 35283957)
61. T. Schmidt, G.J. Schütz, W. Baumgartner, H.J. Gruber, and H. Schindler Characterization of photophysics and mobility of single molecules in a fluid lipid membrane J. Phys. Chem. 99 1995 17662 17668
62. T. Schmidt, G.J. Schütz, H.J. Gruber, and H. Schindler Local stoichiometries determined by counting individual molecules Anal. Chem. 68 1996 4397 4401
63. M. Schwarzenbacher, M. Kaltenbrunner, M. Brameshuber, C. Hesch, W. Paster, J. Weghuber, B. Heise, A. Sonnleitner, H. Stockinger, and G.J. Schütz Micropatterning for quantitative analysis of protein-protein interactions in living cells Nat. Methods 5 2008 1053 1060
64. P. Sengupta, A. Hammond, D. Holowka, and B. Baird Structural determinants for partitioning of lipids and proteins between coexisting fluid phases in giant plasma membrane vesicles Biochim. Biophys. Acta 1778 2008 20 32
65. A. Serge, N. Bertaux, H. Rigneault, and D. Marguet Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes Nat. Methods 5 2008 687 694
66. P. Sharma, R. Varma, R.C. Sarasij, K. Ira, G. Gousset, M. Rao Krishnamoorthy, and S. Mayor Nanoscale organization of multiple gpi-anchored proteins in living cell membranes Cell 116 2004 577 589 (Pubitemid 38264434)
67. A.S. Shaw Lipid rafts: Now you see them, now you don't Nat. Immunol. 7 2006 1139 1142 (Pubitemid 44594308)
68. A.S. Shaw, J. Chalupny, J.A. Whitney, C. Hammond, K.E. Amrein, P. Kavathas, B.M. Sefton, and J.K. Rose Short related sequences in the cytoplasmic domains of CD4 and CD8 mediate binding to the amino-terminal domain of the p56lck tyrosine protein kinase Mol. Cell. Biol. 10 1990 1853 1862
69. D. Shu, H. Zhang, J. Jin, and P. Guo Counting of six pRNAs of phi29 DNA-packaging motor with customized single-molecule dual-view system EMBO J. 26 2007 527 537 (Pubitemid 46160952)
70. K. Simons, and M.J. Gerl Revitalizing membrane rafts: New tools and insights Nat. Rev. Mol. Cell Biol. 11 2010 688 699
71. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572 (Pubitemid 27248754)
72. P.D. Simonson, H.A. DeBerg, P. Ge, J.K. Alexander, O. Jeyifous, W.N. Green, and P.R. Selvin Counting bungarotoxin binding sites of nicotinic acetylcholine receptors in mammalian cells with high signal/noise ratios Biophys. J. 99 2010 L81 L83
73. C.S. Smith, N. Joseph, B. Rieger, and K.A. Lidke Fast, single-molecule localization that achieves theoretically minimum uncertainty Nat. Methods 7 2010 373 375
74. I. Stefanova, V. Horejsi, I.J. Ansotegui, W. Knapp, and H. Stockinger GPI-anchored cell-surface molecules complexed to protein tyrosine kinases Science 254 1991 1016 1019 (Pubitemid 21917433)
75. M. Tokunaga, N. Imamoto, and K. Sakata-Sogawa Highly inclined thin illumination enables clear single-molecule imaging in cells Nat. Methods 5 2008 159 161 (Pubitemid 351181742)
76. J.M. Turner, M.H. Brodsky, B.A. Irving, S.D. Levin, R.M. Perlmutter, and D.R. Littman Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs Cell 60 1990 755 765
77. M.H. Ulbrich, and E.Y. Isacoff Subunit counting in membrane-bound proteins Nat. Methods 4 2007 319 321 (Pubitemid 46766975)
78. A.M. van Oijen Cutting the forest to see a single tree? Nat. Chem. Biol. 4 2008 440 443 (Pubitemid 352019766)
79. P.D. von Haller, S. Donohoe, D.R. Goodlett, R. Aebersold, and J.D. Watts Mass spectrometric characterization of proteins extracted from Jurkat T cell detergent-resistant membrane domains Proteomics 1 2001 1010 1021 (Pubitemid 33699617)
80. M. Vrljic, S.Y. Nishimura, S. Brasselet, W.E. Moerner, and H.M. McConnell Translational diffusion of individual class II MHC membrane proteins in cells Biophys. J. 83 2002 2681 2692 (Pubitemid 35265760)
81. S. Wieser, and G.J. Schütz Tracking single molecules in the live cell plasma membrane-Do's and don't's Methods 46 2008 131 140
82. P.W. Wiseman, C.M. Brown, D.J. Webb, B. Hebert, N.L. Johnson, J.A. Squier, M.H. Ellisman, and A.F. Horwitz Spatial mapping of integrin interactions and dynamics during cell migration by image correlation microscopy J. Cell Sci. 117 2004 5521 5534 (Pubitemid 40012199)
83. P.J. Woolf, and J.J. Linderman Self organization of membrane proteins via dimerization Biophys. Chem. 104 2003 217 227 (Pubitemid 36794473)
84. G. Yellen The voltage-gated potassium channels and their relatives Nature 419 2002 35 42 (Pubitemid 34987863)
85. M. Yunta, and P.A. Lazo Tetraspanin proteins as organisers of membrane microdomains and signalling complexes Cell. Signal. 15 2003 559 564 (Pubitemid 36385161)
86. L. Zimmermann, W. Paster, J. Weghuber, P. Eckerstorfer, H. Stockinger, and G.J. Schütz Direct observation and quantitative analysis of Lck-exchange between plasma membrane and cytosol in living T cells J. Biol. Chem. 285 2010 6063 6070
87. W.R. Zipfel, R.M. Williams, and W.W. Webb Nonlinear magic: Multiphoton microscopy in the biosciences Nat. Biotechnol. 21 2003 1369 1377 (Pubitemid 37356624)