Direct observation of mobility state transitions in RNA trajectories by sensitive single molecule feedback tracking

Nucleic Acids Research

Volumn 43, Issue 2, 2015, Pages e14-

  Spille, Jan Hendrik ^a   Kaminski, Tim P ^a   Scherer, Katharina ^a   Rinne, Jennifer S ^b   Heckel, Alexander ^b   Kubitscheck, Ulrich ^a  

^a UNIVERSITY OF BONN   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE; LIPOSOME; MESSENGER RNA; RNA; RNA 28S;

ALGORITHM; ANIMAL; CELL NUCLEUS MEMBRANE; CHEMISTRY; CHIRONOMIDAE; CHROMOSOME PUFF; FLUORESCENCE MICROSCOPY; PHOTON; PROCEDURES;

ALGORITHMS; ANIMALS; CHIRONOMIDAE; CHROMOSOMAL PUFFS; FLUORESCENT DYES; MICROSCOPY, FLUORESCENCE; NUCLEAR ENVELOPE; PHOTONS; RNA; RNA, MESSENGER; RNA, RIBOSOMAL, 28S; UNILAMELLAR LIPOSOMES;

EID: 84941122695     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1194     Document Type: Article

References (49)

1. Axelrod, D., Koppel, D., Schlessinger, J., Elson, E.L., Webb, W. (1976) Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J., 16, 1055-1069.
2. Elson, E.L., Magde, D. (1974) Fluorescence correlation spectroscopy. I. Conceptual basis and theory. Biopolymers, 13, 1-27.
3. Roy, R., Hohng, S., Ha, T. (2008) A practical guide to single-molecule FRET. Nat. Methods, 5, 507-516.
4. Schmidt, T., Schütz, G., Baumgartner, W., Gruber, H., Schindler, H. (1996) Imaging of single molecule diffusion. Proc. Natl. Acad. Sci. U.S.A., 93, 2926-2929.
5. Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., Kasai, R.S., Kondo, J., Fujiwara, T. (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, 351-378.
6. Lakadamyali, M., Rust, M.J., Babcock, H.P., Zhuang, X. (2003) Visualizing infection of individual influenza viruses. Proc. Natl. Acad. Sci. U.S.A., 100, 9280-9285.
7. Yildiz, A., Selvin, P.R. (2005) Fluorescence imaging with one nanometer accuracy: application to molecular motors. Acc. Chem. Res., 38, 574-582.
8. Persson, F., Lindén, M., Unoson, C., Elf, J. (2013) Extracting intracellular diffusive states and transition rates from single-molecule tracking data. Nat. Methods, 10, 265-269.
9. Siebrasse, J.P., Veith, R., Dobay, A., Leonhardt, H., Daneholt, B., Kubtischeck, U. (2008) Discontinuous movement of mRNP particles in nucleoplasmic regions devoid of chromatin. Proc. Natl. Acad. Sci. U.S.A., 105, 20291-20296.
10. Dupont, A., Gorelashvili, M., Wehnekamp, F., Arcizet, D., Katayama, Y., Lamb, D.C., Heinrich, D. (2013) Three-dimensional single-particle tracking in live cells: news from the third dimension. New J. Phys., 15, 075008.
11. Katayama, Y., Burbacky, O., Meyer, M., Braüchle, C., Gratton, E., Lamb, D.C. (2009) Real-time nanomicroscopy via three-dimensional single-particle tracking. Chemphyschem, 10, 2458-2464.
12. Ram, S., Prabhat, P., Chao, J., Ward, E.S., Ober, R.J. (2008) High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells. Biophys. J., 95, 6025-6043.
13. Abrahamsson, S., Chen, J., Hajj, B., Stallinga, S., Katsov, A.Y., Wisniewski, J., Mizuguchi, G., Soule, P., Mueller, F., Dugast Darzacq, C. et al. (2012) Fast multicolor 3D imaging using aberration-corrected multifocus microscopy. Nat. Methods, 10, 60-63.
14. Shtengel, G., Glabraith, J.A., Galbraith, C.G., Lippincott-Schwartz, J., Gillette, J.M., Manley, S., Sougrat, R., Waterman, C.M., Kanchanawong, P., Davidson, M.W. et al. (2009) Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc. Natl. Acad. Sci. U.S.A., 106, 3125-3130.
15. Kao, H.P., Verkman, A.S. (1994) Tracking of single fluorescent particles in three dimensions: use of cylindrical optics to encode particle position. Biophys. J., 67, 1291-1300.
16. Thompson, M.A., Casolari, J.M., Badieirostami, M., Brown, P.O., Moerner, W.E. (2010) Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function. Proc. Natl. Acad. Sci. U.S.A., 107, 17864-17871.
17. Juette, M.F., Bewersdorf, J. (2010) Three-dimensional tracking of single fluorescent particles with submillisecond temporal resolution. Nano Lett., 10, 4657-4663.
18. Spille, J.-H., Kaminski, T., Königshoven, H.-P., Kubitscheck, U. (2012) Dynamic three-dimensional tracking of single fluorescent nanoparticles deep inside living tissue. Opt. Express, 20, 19697-19707.
19. Wang, Q., Moerner, W.E. (2014) Single-molecule motions enable direct visualization of biomolecular interactions in solution. Nat. Methods, 11, 555-558.
20. Ritter, J.G., Veith, R., Veenendaal, A., Siebrasse, J.P., Kubitscheck, U. (2010) Light sheet microscopy for single molecule tracking in living tissue. PLoS One, 5, e11639.
21. Muselli, M. (1996) Simple expressions for success run distributions in Bernoulli trials. Stat. Probab. Lett., 31, 121-128.
22. Saxton, M.J., Jacobson, K. (1997) Single-particle tracking: applications to membrane dynamics. Ann. Rev. Biophys. Biomol. Struct., 26, 373-399.
23. Moumtzi, A., Trenker, M., Flicker, K., Zenzmaier, E., Saf, R., Hermetter, A. (2007) Import and fate of fluorescent analogs of oxidized phospholipids in vascular smooth muscle cells. J. Lipid Res., 48, 565-582.
24. Dimitrov, D.S., Angelova, M.I. (1988) Lipid swelling and liposome formation mediated by electric fields. Bioelectrochem. Bioenerg., 19, 323-336.
25. Menger, F.M., Keiper, J.S. (1998) Giant vesicles: micromanipulation of membrane bilayers. Adv. Mater., 10, 888-890.
26. Ciobanasu, C., Harms, E., Tünnemann, G., Cardoso, M.C., Kubitscheck, U. (2009) Cell-penetrating HIV1 TAT peptides float on model lipid bilayers. Biochemistry, 48, 4728-4737.
27. Kaminski, T.P., Spille, J.-H., Nietzel, C., Siebrasse, J.P., Kubitscheck, U. (2013) Nuclear trafficking and export of single, native mRNPs in Chironomus tentans salivary gland cells. Methods Mol. Biol., 1042, 73-85.
28. Cheezum, M.K., Walker, W.F., Guilford, W.H. (2001) Quantitative comparison of algorithms for tracking single fluorescent particles. Biophys. J., 81, 2378-2388.
29. Huang, B., Jones, S.A., Brandenburg, B., Zhuang, X. (2008) Whole-cell 3D STORM reveals interactions between cellular structures with nanometerscale resolution. Nat. Methods, 5, 1047-1052.
30. Mlodzianoski, M.J., Juette, M.F., Beane, G.L., Bewersdorf, J. (2009) Experimental characterization of 3D localization techniques for particle-tracking and super-resolution microscopy. Opt. Express, 17, 8264-8277.
31. York, A.G., Ghitani, A., Vaziri, A., Davidson, M.W., Shroff, H. (2011) Confined activation and subdiffractive localization enables whole-cell PALM with genetically expressed probes. Nat. Methods, 8, 327-333.
32. Wachsmuth, M., Waldeck, W., Langowski, J. (2000) Anomalous diffusion of fluorescent probes inside living cell nuclei investigated by spatially-resolved fluorescence correlation spectroscopy. J. Mol. Biol., 298, 677-689.
33. Smith, P.R., Morrison, I.E.G., Wilson, K.M., Fernández, N., Cherry, R.J. (1999) Anomalous diffusion of major histocompatibility complex class I molecules on HeLa cells determined by single particle tracking. Biophys. J., 76, 3331-3344.
34. Veith, R., Sorkalla, T., Baumgart, E., Anzt, J., Häberlein, H., Tyagi, S., Siebrasse, J.P., Kubitscheck, U. (2010) Balbiani ring mRNPs diffuse through and bind to clusters of large intranuclear molecular structures. Biophys. J., 99, 2676-2685.
35. Weimann, L., Gnaziger, K.A., McColl, J., Irvine, K.L., Davis, S.J., Gay, N.J., Bryant, C.E., Klenerman, D. (2013) A quantitative comparison of single-dye tracking analysis tools using Monte Carlo simulations. PloS One, 8, e64287.
36. Saxton, M.J. (1993) Lateral diffusion in an archipelago. Biophys. J., 64, 1766-1780.
37. Grünwald, D., Singer, R.H. (2010) In vivo imaging of labelled endogenous-actin mRNA during nucleocytoplasmic transport. Nature, 467, 604-607.
38. Siebrasse, J.P., Kaminski, T., Kubitscheck, U. (2012) Nuclear export of single native mRNA molecules observed by light sheet fluorescence microscopy. Proc. Natl. Acad. Sci. U.S.A., 109, 9426-9431.
39. Griffin, B.A., Adams, S.R., Tsien, R.Y. (1998) Specific covalent labeling of recombinant protein molecules inside live cells. Science, 281, 269-272.
40. Huang, F., Hartwich, T.M.P., Rivera-Molina, F., Lin, Y., Duim, W.C., Long, J.J., Uchil, P.D., Myers, J.R., Baird, M.A., Mothes, W. et al. (2013) Video-rate nanoscopy using sCMOS camera-specific single-molecule localization algorithms. Nat. Methods, 10, 653-658.
41. Ma, H., Kawai, H., Toda, E., Zeng, S., Huang, Z.-L. (2013) Localization-based super-resolution microscopy with an sCMOS camera part III: camera embedded data processing significantly reduces the challenges of massive data handling. Opt. Lett., 38, 1769-1771.
42. Smith, C.S., Joseph, N., Rieger, B., Lidke, K.A. (2010) Fast, single-molecule localization that achieves theoretically minimum uncertainty. Nat. Methods, 7, 373-375.
43. Chao, J., Ram, S., Ward, E.S., Ober, R.J. (2013) Ultrahigh accuracy imaging modality for super-localization microscopy. Nat. Methods, 10, 335-338.
44. Izeddin, I., El Beheiry, M., Andilla, J., Ciepielewski, D., Darzacq, X., Dahen, M. (2012) PSF shaping using adaptive optics for three-dimensional singlemolecule super-resolution imaging and tracking. Opt. Express, 20, 4957-4967.
45. Tokunaga, M., Imamoto, N., Sakata-Sogawa, K. (2008) Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat. Methods, 5, 159-161.
46. Gebhardt, J.C.M., Suter, D.M., Roy, R., Zhao, Z.W., Chapman, A.R., Basu, S., Maniatis, T., Xi, S.X. (2013) Single-molecule imaging of transcription factor binding to DNA in live mammalian cells. Nat. Methods, 10, 421-426.
47. Juette, M.F., Terry, D.S., Wasserman, M.R., Zhou, Z., Altman, R.B., Zheng, Q., Blanchard, S.G. (2014) The bright future of single-molecule fluorescence imaging. Curr. Opin. Chem. Biol., 20, 103-111.
48. Juette, M.F., Rivera-Molina, F.E., Toomre, D.K., Bewersdorf, J. (2013) Adaptive optics enables three-dimensional single particle tracking at the submillisecond scale. Appl. Phys. Lett., 102, 173702-1-173702-4.
49. Brandenburg, B., Zhuang, X. (2007) Virus trafficking-learning from single-virus tracking. Nat. Rev. Microbiol., 5, 197-208.