What can we learn from single molecule trajectories?

Current Protein and Peptide Science

Volumn 12, Issue 8, 2011, Pages 714-724

  Ruprecht, Verena ^a   Axmann, Markus ^b   Wieser, Stefan ^a   Schütz, Gerhard J ^c  

^a INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

^b MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^c VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

2D random walk; Confined diffusion; Diffusion models; Monte carlo simulation; Single molecule diffusion analysis; Single molecule microscopy; Single particle tracking; Statistical analysis of trajectories

Indexed keywords

QUANTUM DOT; TRACER;

ALGORITHM; ANALYTIC METHOD; CELL LABELING; CELL MEMBRANE; CELL TRACKING; DIFFUSION; EDITORIAL; ILLUMINATION; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MONTE CARLO METHOD; MOVEMENT (PHYSIOLOGY); PARTICLE SIZE; SINGLE MOLECULE TRAJECTORY; STATISTICAL ANALYSIS;

ALGORITHMS; CELL MEMBRANE; DIFFUSION; KINETICS; MEMBRANE PROTEINS; MONTE CARLO METHOD;

EID: 84857129581     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/138920311798841753     Document Type: Editorial

References (86)

1. Saxton, M. J.; Jacobson, K. Single-particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct., 1997, 26, 373-399.
2. Michalet, X.; Pinaud, F. F.; Bentolila, L. A.; Tsay, J. M.; Doose, S.; Li, J. J.; Sundaresan, G.; Wu, A. M.; Gambhir, S. S.; Weiss, S. Quantum dots for live cells, in vivo imaging, and diagnostics. Science, 2005, 307 (5709), 538-544.
3. Pinaud, F.; Clarke, S.; Sittner, A.; Dahan, M. Probing cellular events, one quantum dot at a time. Nat. Methods, 2010, 7 (4), 275-285.
4. Wieser, S.; Schütz, G. J. Tracking single molecules in the live cell plasma membrane-Do's and Don't's. Methods 2008, 46 (2), 131-140.
5. Jacobson, K.; Sheets, E. D.; Simson, R. Revisiting the fluid mosaic model of membranes. Science 1995, 268 (5216), 1441-1442.
6. Schermelleh, L.; Heintzmann, R.; Leonhardt, H. A guide to superresolution fluorescence microscopy. J. Cell Biol., 2010, 190 (2), 165-175.
7. Hesse, J.; Schutz, G. J. Single molecule bioanalysis. Curr. Pharm. Anal., 2007, 3 (3), 186-194.
8. Rudnick, J.; Gaspari, G. The shapes of random walks. Science, 1987, 237, 384-389.
9. Wieser, S.; Axmann, M.; Schütz, G. J. Versatile analysis of singlemolecule tracking data by comprehensive testing against Monte Carlo simulations. Biophys. J., 2008, 95 (12), 5988-6001.
10. Ghosh, R. N.; Webb, W. W. Automated detection and tracking of individual and clustered cell surface low density lipoprotein receptor molecules. Biophys. J., 1994, 66 (5), 1301-1318.
11. Anderson, C. M.; Georgiou, G. N.; Morrison, I. E.; Stevenson, G. V.; Cherry, R. J. Tracking of cell surface receptors by fluorescence digital imaging microscopy using a charge-coupled device camera. Low-density lipoprotein and influenza virus receptor mobility at 4 degrees C. J. Cell Sci., 1992, 101 (Pt 2), 415-425.
12. Lee, G. M.; Ishihara, A.; Jacobson, K. A. Direct observation of brownian motion of lipids in a membrane. Proc. Natl. Acad. Sci. U. S. A., 1991, 88 (14), 6274-6278.
13. Kusumi, A.; Sako, Y.; Yamamoto, M. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J., 1993, 65 (5), 2021-2040.
14. Tomishige, M.; Sako, Y.; Kusumi, A. Regulation mechanism of the lateral diffusion of band 3 in erythrocyte membranes by the membrane skeleton. J. Cell Biol., 1998, 142 (4), 989-1000.
15. Fujiwara, T.; Ritchie, K.; Murakoshi, H.; Jacobson, K.; Kusumi, A. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol., 2002, 157 (6), 1071-1081.
16. Howarth, M.; Liu, W.; Puthenveetil, S.; Zheng, Y.; Marshall, L. F.; Schmidt, M. M.; Wittrup, K. D.; Bawendi, M. G.; Ting, A. Y. Monovalent, reduced-size quantum dots for imaging receptors on living cells. Nat. Methods, 2008, 5 (5), 397-399.
17. Fu, C. C.; Lee, H. Y.; Chen, K.; Lim, T. S.; Wu, H. Y.; Lin, P. K.; Wei, P. K.; Tsao, P. H.; Chang, H. C.; Fann, W. Characterization and application of single fluorescent nanodiamonds as cellular biomarkers. Proc. Natl. Acad. Sci. U. S. A., 2007, 104, 727-732.
18. Rabeau, J. R.; Stacey, A.; Rabeau, A.; Prawer, S.; Jelezko, F.; Mirza, I.; Wrachtrup, J. Single nitrogen vacancy centers in chemical vapor deposited diamond nanocrystals. Nano. Letters, 2007, 7 (11), 3433-3437.
19. Zheng, J.; Zhang, C.; Dickson, R. M. Highly fluorescent, watersoluble, size-tunable gold quantum dots. Phys. Rev. Lett., 2004, 93 (7), 077402.
20. Schütz, G. J.; Kada, G.; Pastushenko, V. P.; Schindler, H. Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy. Embo. J., 2000, 19 (5), 892-901.
21. Rhode, S.; Grurl, R.; Brameshuber, M.; Hermetter, A.; Schutz, G. J. Plasma membrane fluidity affects transient immobilization of oxidized phospholipids in endocytotic sites for subsequent uptake. J. Biol. Chem., 2009, 284 (4), 2258-2265.
22. Sakon, J. J.; Weninger, K. R. Detecting the conformation of individual proteins in live cells. Nat. Methods, 2010, 7 (3), 203-205.
23. Seisenberger, G.; Ried, M. U.; Endress, T.; Buning, H.; Hallek, M.; Brauchle, C., Real-time single-molecule imaging of the infection pathway of an adeno-associated virus. Science, 2001, 294 (5548), 1929-1932.
24. Shaner, N. C.; Steinbach, P. A.; Tsien, R. Y. A guide to choosing fluorescent proteins. Nat. Methods, 2005, 2 (12), 905-909.
25. Guignet, E. G.; Segura, J. M.; Hovius, R.; Vogel, H. Repetitive reversible labeling of proteins at polyhistidine sequences for singlemolecule imaging in live cells. Chemphyschem, 2007, 8 (8), 1221-1227.
26. Gronemeyer, T.; Godin, G.; Johnsson, K. Adding value to fusion proteins through covalent labelling. Curr. Opin. Biotechnol., 2005, 16 (4), 453-458.
27. Drbal, K.; Moertelmaier, M.; Holzhauser, C.; Muhammad, A.; Fuertbauer, E.; Howorka, S.; Hinterberger, M.; Stockinger, H.; Schütz, G. J. Single-molecule microscopy reveals heterogeneous dynamics of lipid raft components upon TCR engagement. Int. Immunol., 2007, 19 (5), 675-684.
28. Wieser, S.; Moertelmaier, M.; Fuertbauer, E.; Stockinger, H.; Schütz, G. J. (Un)Confined Diffusion of CD59 in the Plasma Membrane Determined by High-Resolution Single Molecule Microscopy. Biophys. J., 2007, 92 (10), 3719-3728.
29. Huppa, J. B.; Axmann, M.; Mortelmaier, M. A.; Lillemeier, B. F.; Newell, E. W.; Brameshuber, M.; Klein, L. O.; Schütz, G. J.; Davis, M. M. TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature, 2010, 463 (7283), 963-967.
30. Freudenthaler, G.; Axmann, M.; Schindler, H.; Pragl, B.; Knaus, H. G.; Schütz, G. J. Ultrasensitive pharmacological characterisation of the voltage-gated potassium channel K(V)1.3 studied by singlemolecule fluorescence microscopy. Histochem. Cell Biol., 2002, 117 (3), 197-202.
31. Füreder-Kitzmüller, E.; Hesse, J.; Ebner, A.; Gruber, H. J.; Schütz, G. J. Non-exponential bleaching of single bioconjugated Cy5 molecules. Chem. Phys. Lett., 2005, 404, 13-18.
32. Harada, Y.; Sakurada, K.; Aoki, T.; Thomas, D. D.; Yanagida, T. Mechanochemical coupling in actomyosin energy transduction studied by in vitro movement assay. J. Mol. Biol., 1990, 216 (1), 49-68.
33. Simson, R.; Sheets, E. D.; Jacobson, K. Detection of temporary lateral confinement of membrane proteins using single-particle tracking analysis. Biophys. J., 1995, 69 (3), 989-993.
34. Daumas, F.; Destainville, N.; Millot, C.; Lopez, A.; Dean, D.; Salome, L. Confined diffusion without fences of a g-proteincoupled receptor as revealed by single particle tracking. Biophys. J., 2003, 84 (1), 356-366.
35. Sheets, E. D.; Lee, G. M.; Simson, R.; Jacobson, K. Transient confinement of a glycosylphosphatidylinositol-anchored protein in the plasma membrane. Biochemistry, 1997, 36 (41), 12449-1258.
36. Chen, Y.; Thelin, W. R.; Yang, B.; Milgram, S. L.; Jacobson, K. Transient anchorage of cross-linked glycosyl-phosphatidylinositolanchored proteins depends on cholesterol, Src family kinases, caveolin, and phosphoinositides. J. Cell Biol., 2006, 175 (1), 169-178.
37. Suzuki, K. G.; Fujiwara, T. K.; Edidin, M.; Kusumi, A. Dynamic recruitment of phospholipase Cγ at transiently immobilized GPIanchored receptor clusters induces IP3-Ca2+ signaling: singlemolecule tracking study 2. J. Cell Biol., 2007, 177 (4), 731-742.
38. Suzuki, K. G.; Fujiwara, T. K.; Sanematsu, F.; Iino, R.; Edidin, M.; Kusumi, A. GPI-anchored receptor clusters transiently recruit Lyn and G for temporary cluster immobilization and Lyn activation: single-molecule tracking study 1. J. Cell Biol., 2007, 177 (4), 717-730.
39. Kusumi, A.; Shirai, Y. M.; Koyama-Honda, I.; Suzuki, K.; Fujiwara, T. K. Hierarchical organization of the plasma membrane: Investigations by single-molecule tracking vs. fluorescence correlation spectroscopy. Febs. Lett., 2010, 584 (9), 1814-1823.
40. Andrews, N. L.; Lidke, K. A.; Pfeiffer, J. R.; Burns, A. R.; Wilson, B. S.; Oliver, J. M.; Lidke, D. S. Actin restricts FcepsilonRI diffusion and facilitates antigen-induced receptor immobilization. Nat. Cell Biol., 2008, 10 (8), 955-963.
41. Treanor, B.; Depoil, D.; Gonzalez-Granja, A.; Barral, P.; Weber, M.; Dushek, O.; Bruckbauer, A.; Batista, F. D. The membrane skeleton controls diffusion dynamics and signaling through the B cell receptor. Immunity, 2010, 32 (2), 187-199.
42. Douglass, A. D.; Vale, R. D. Single-Molecule Microscopy Reveals Plasma Membrane Microdomains Created by Protein-Protein Networks that Exclude or Trap Signaling Molecules in T Cells. Cell, 2005, 121 (6), 937-950.
43. Espenel, C.; Margeat, E.; Dosset, P.; Arduise, C.; Le Grimellec, C.; Royer, C. A.; Boucheix, C.; Rubinstein, E.; Milhiet, P. E. Singlemolecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web. J. Cell Biol., 2008, 182 (4), 765-776.
44. Pinaud, F.; Michalet, X.; Iyer, G.; Margeat, E.; Moore, H. P.; Weiss, S. Dynamic Partitioning of a Glycosyl-Phosphatidylinositol-Anchored Protein in Glycosphingolipid-Rich Microdomains Imaged by Single-Quantum Dot Tracking. Traffic, 2009, 10 (6), 691-712.
45. Segura, J. M.; Guillaume, P.; Mark, S.; Dojcinovic, D.; Johannsen, A.; Bosshard, G.; Angelov, G.; Legler, D. F.; Vogel, H.; Luescher, I. F. Increased mobility of major histocompatibility complex Ipeptide complexes decreases the sensitivity of antigen recognition. J. Biol. Chem., 2008, 283 (35), 24254-24263.
46. Jacquier, V.; Prummer, M.; Segura, J. M.; Pick, H.; Vogel, H. Visualizing odorant receptor trafficking in living cells down to the single-molecule level. Proc. Natl. Acad. Sci. USA., 2006, 103 (39), 14325-14330.
47. Felsenfeld, D. P.; Choquet, D.; Sheetz, M. P. Ligand binding regulates the directed movement of beta1 integrins on fibroblasts. Nature, 1996, 383 (6599), 438-440.
48. Bouzigues, C.; Dahan, M. Transient directed motions of GABA(A) receptors in growth cones detected by a speed correlation index. Biophys. J., 2007, 92 (2), 654-660.
49. Hecht, E., Optics. Addison-Wesley: 1987.
50. Thompson, R. E.; Larson, D. R.; Webb, W. W. Precise nanometer localization analysis for individual fluorescent probes. Biophys. J., 2002, 82 (5), 2775-2783.
51. Bobroff, N. Position measurement with a resolution and noiselimited instrument. Rev. Sci. Instrum., 1986, 57 (6), 1152-1157.
52. Mortensen, K. I.; Churchman, L. S.; Spudich, J. A.; Flyvbjerg, H. Optimized localization analysis for single-molecule tracking and super-resolution microscopy. Nat. Methods, 2010, 7 (5), 377-381.
53. Smith, C. S.; Joseph, N.; Rieger, B.; Lidke, K. A., Fast, singlemolecule localization that achieves theoretically minimum uncertainty. Nat. Methods, 2010, 7 (5), 373-375.
54. Ober, R. J.; Ram, S.; Ward, E. S. Localization accuracy in singlemolecule microscopy. Biophys. J., 2004, 86 (2), 1185-1200.
55. Ram, S.; Ward, E. S.; Ober, R. J. Beyond Rayleigh's criterion: a resolution measure with application to single-molecule microscopy. Proc. Natl. Acad. Sci. USA., 2006, 103 (12), 4457-4462.
56. Serge, A.; Bertaux, N.; Rigneault, H.; Marguet, D. Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes. Nat. Methods, 2008, 5 (8), 687-694.
57. Jaqaman, K.; Loerke, D.; Mettlen, M.; Kuwata, H.; Grinstein, S.; Schmid, S. L.; Danuser, G. Robust single-particle tracking in livecell time-lapse sequences. Nat. Methods, 2008, 5 (8), 695-702.
58. Saxton, M. J. Lateral diffusion in an archipelago. Single-particle diffusion. Biophys. J., 1993, 64 (6), 1766-1780.
59. Jin, S.; Haggie, P. M.; Verkman, A. S. Single-particle tracking of membrane protein diffusion in a potential: simulation, detection, and application to confined diffusion of CFTR Cl- channels. Biophys. J., 2007, 93 (3), 1079-1088.
60. Masson, J. B.; Casanova, D.; Turkcan, S.; Voisinne, G.; Popoff, M. R.; Vergassola, M.; Alexandrou, A. Inferring maps of forces inside cell membrane microdomains. Phys. Rev. Lett., 2009, 102 (4), 048103.
61. Goulian, M.; Simon, S. M. Tracking single proteins within cells. Biophys. J., 2000, 79 (4), 2188-2198.
62. Ritchie, K.; Shan, X. Y.; Kondo, J.; Iwasawa, K.; Fujiwara, T.; Kusumi, A. Detection of non-brownian diffusion in the cell membrane in single molecule tracking. Biophys. J., 2005, 88 (3), 2266-2277.
63. Destainville, N.; Salome, L. Quantification and correction of systematic errors due to detector time-averaging in single-molecule tracking experiments. Biophys. J., 2006, 90 (2), L17-L19.
64. Wieser, S.; Schütz, G. J.; Cooper, M. E.; Stockinger, H. Single molecule diffusion analysis on cellular nanotubules: Implications on plasma membrane structure below the diffraction limit. Appl. Phys. Lett., 2007, 91 (23), 233901.
65. Meier, J.; Vannier, C.; Serge, A.; Triller, A.; Choquet, D. Fast and reversible trapping of surface glycine receptors by gephyrin. Nat. Neurosci., 2001, 4 (3), 253-260.
66. Meilhac, N.; Le Guyader, L.; Salome, L.; Destainville, N. Detection of confinement and jumps in single-molecule membrane trajectories. Phys. Rev. E., 2006, 73 (1), 253-260.
67. Montiel, D.; Cang, H.; Yang, H. Quantitative characterization of changes in dynamical behavior for single-particle tracking studies. J. Phys. Chem. B., 2006, 110 (40), 19763-19770.
68. Huet, S.; Karatekin, E.; Tran, V. S.; Fanget, I.; Cribier, S.; Henry, J. P. Analysis of transient behavior in complex trajectories: application to secretory vesicle dynamics. Biophys. J., 2006, 91 (9), 3542-3559.
69. Schütz, G. J.; Schindler, H.; Schmidt, T. Single-molecule microscopy on model membranes reveals anomalous diffusion. Biophys. J., 1997, 73 (2), 1073-1080.
70. Deverall, M. A.; Gindl, E.; Sinner, E. K.; Besir, H.; Ruehe, J.; Saxton, M. J.; Naumann, C. A. Membrane lateral mobility obstructed by polymer-tethered lipids studied at the single molecule level. Biophys. J., 2005, 88 (3), 1875-1886.
71. Lommerse, P. H.; Blab, G. A.; Cognet, L.; Harms, G. S.; Snaar-Jagalska, B. E.; Spaink, H. P.; Schmidt, T. Single-Molecule Imaging of the H-Ras Membrane-Anchor Reveals Domains in the Cytoplasmic Leaflet of the Cell Membrane. Biophys. J., 2004, 86 (1), 609-616.
72. Sahl, S. J.; Leutenegger, M.; Hilbert, M.; Hell, S. W.; Eggeling, C. Fast molecular tracking maps nanoscale dynamics of plasma membrane lipids. Proc. Natl. Acad. Sci. USA., 2010, 107 (15), 6829-6834.
73. Matsuoka, S.; Shibata, T.; Ueda, M. Statistical analysis of lateral diffusion and multistate kinetics in single-molecule imaging. Biophys. J., 2009, 97 (4), 1115-1124.
74. Das, R.; Cairo, C. W.; Coombs, D. A hidden Markov model for single particle tracks quantifies dynamic interactions between LFA-1 and the actin cytoskeleton. PLoS Comput. Biol., 2009, 5 (11), e1000556.
75. Saxton, M. J. Single-particle tracking: the distribution of diffusion coefficients. Biophys. J., 1997, 72 (4), 1744-1753.
76. Saxton, M. J. Anomalous diffusion due to binding: a Monte Carlo study. Biophys. J., 1996, 70 (3), 1250-1262.
77. Krobath, H.; Schütz, G. J.; Lipowsky, R.; Weikl, T. R. Lateral diffusion of receptor-ligand bonds in membrane adhesion zones: Effect of thermal membrane roughness. Europhys. Lett., 2007, 78, 38003.
78. Hall, D. Analysis and interpretation of two-dimensional singleparticle tracking microscopy measurements: effect of local surface roughness. Anal. Biochem., 2008, 377 (1), 24-32.
79. Adler, J.; Shevchuk, A. I.; Novak, P.; Korchev, Y. E.; Parmryd, I. Plasma membrane topography and interpretation of single-particle tracks. Nat. Methods, 2010, 7 (3), 170-171.
80. Wawrezinieck, L.; Rigneault, H.; Marguet, D.; Lenne, P. F. Fluorescence correlation spectroscopy diffusion laws to probe the submicron cell membrane organization. Biophys. J., 2005, 89 (6), 4029-4042.
81. Saxton, M. J. Single-particle tracking: effects of corrals. Biophys. J., 1995, 69 (2), 389-398.
82. Jin, S.; Verkman, A. S. Single particle tracking of complex diffusion in membranes: simulation and detection of barrier, raft, and interaction phenomena. J. Phys. Chem. B., 2007, 111 (14), 3625-3632.
83. Pappas, P. A.; DePuy, V. An overview of non-parametric tests in SAS: when, why, and how. Proceedings of the SouthEast SAS Users Group Conference (SESUG 2004) 2004, paper TU04.
84. Krogsgaard, M.; Davis, M. M. How T cells 'see' antigen. Nat. Immunol., 2005, 6 (3), 239-245.
85. Murase, K.; Fujiwara, T.; Umemura, Y.; Suzuki, K.; Iino, R.; Yamashita, H.; Saito, M.; Murakoshi, H.; Ritchie, K.; Kusumi, A. Ultrafine Membrane Compartments for Molecular Diffusion as Revealed by Single Molecule Techniques. Biophys. J., 2004, 86 (6), 4075-4093.
86. Jacak, J.; Hesch, C.; Hesse, J.; Schutz, G. J. Identification of immobile single molecules using polarization-modulated asynchronous time delay and integration-mode scanning. Anal. Chem., 2010, 82 (10), 4288-4292.