Quantitative fluorescence loss in photobleaching for analysis of protein transport and aggregation

BMC Bioinformatics

Volumn 13, Issue 1, 2012, Pages

  Wüstner, Daniel ^a   Solanko, Lukasz M ^a   Lund, Frederik W ^a   Sage, Daniel ^b   Schroll, Hans J ^a   Lomholt, Michael A ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b EPFL   (Switzerland)

Author keywords

Crowding; Fractal kinetics; Mathematical model; Multi compartment; Neurodegeneration; Protein aggregation; Rate coefficient

Indexed keywords

CROWDING; FRACTAL KINETICS; MULTI-COMPARTMENT; NEURODEGENERATION; PROTEIN AGGREGATION; RATE COEFFICIENTS;

AGGREGATES; BLEACHING; CELLS; CLEANING; CYTOLOGY; EXPERIMENTS; FLUORESCENCE; IMAGING TECHNIQUES; ION EXCHANGE; KINETICS; MATHEMATICAL MODELS; PHOTOBLEACHING; TOPOGRAPHY;

PROTEINS;

ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; HTT PROTEIN, HUMAN; NERVE PROTEIN; PROTEIN;

ARTICLE; BLEACHING; CYTOPLASM; DEGENERATIVE DISEASE; DIFFUSION; FLUORESCENCE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; KINETICS; METABOLISM; PROTEIN TRANSPORT; STATISTICS;

CYTOPLASM; DIFFUSION; FLUORESCENCE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GREEN FLUORESCENT PROTEINS; HUMANS; KINETICS; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; PHOTOBLEACHING; PROTEIN TRANSPORT; PROTEINS;

MLCS; MLOWN;

EID: 84873417965     PISSN: None     EISSN: 14712105     Source Type: Journal    
DOI: 10.1186/1471-2105-13-296     Document Type: Article

References (66)

1. Dunn KW, McGraw TE, Maxfield FR. Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome. J Cell Biol 1989, 109:3303-3314. 10.1083/jcb.109.6.3303, 2115921, 2600137.
2. Ghosh RN, Maxfield FR. Evidence for nonvectorial, retrograde transferrin trafficking in the early endosomes of HEp2 cells. J Cell Biol 1995, 128:549-561. 10.1083/jcb.128.4.549, 2199884, 7860630.
3. Ghosh RN, Gelman DL, Maxfield FR. Quantification of low density lipoprotein and transferrin endocytic sorting in HEp2 cells using confocal microscopy. J Cell Sci 1994, 107:2177-2189.
4. Wüstner D. Quantification of polarized trafficking of transferrin and comparison with bulk membrane transport in hepatic cells. Biochem J 2006, 400:267-280. 1652827, 16879100.
5. Wüstner D. Mathematical analysis of hepatic high density lipoprotein transport based on quantitative imaging data. J Biol Chem 2005, 280:6766-6779. 10.1074/jbc.M413238200, 15613466.
6. Wüstner D. Steady state analysis and experimental validation of a model for hepatic high density lipoprotein transport. Traffic 2006, 7:699-715. 10.1111/j.1398-9219.2006.00421.x, 16637891.
7. Dunn KW, Maxfield FR. Delivery of ligands from sorting endosomes to late endosomes occurs by maturation of sorting endosomes. J Cell Biol 1992, 117:301-310. 10.1083/jcb.117.2.301, 2289412, 1560027.
8. Sheff DR, Daro EA, Hull M, Mellman I. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J Cell Biol 1999, 145:123-139. 10.1083/jcb.145.1.123, 2148223, 10189373.
9. Hirschberg K, Miller CM, Ellenberg J, Presley JF, Siggia ED, Phair RD, Lippincott-Schwartz J. Kinetic analysis of secretory protein traffic and characterization of golgi to plasma membrane transport intermediates in living cells. J Cell Biol 1998, 143:1485-1503. 10.1083/jcb.143.6.1485, 2132993, 9852146.
10. Dahm T, White J, Grill S, Füllekrug J, Stelzer EHK. Quantitative ER left-right-arrow golgi transport kinetics and protein separation upon golgi exit revealed by vesicular integral membrane protein 36 dynamics in live cells. Mol Biol Cell 2001, 12:1481-1498. 34599, 11359937.
11. White J, Keller P, Stelzer EH. Spatial partitioning of secretory cargo from Golgi resident proteins in live cells. BMC Cell Biol 2001, 2:19. 10.1186/1471-2121-2-19, 59882, 11707151.
12. Rhee SW, Starr T, Forsten-Williams K, Storrie B. The steady-state distribution of glycosyltransferases between the Golgi apparatus and the endoplasmic reticulum is approximately 90:10. Traffic 2005, 6:1-13.
13. Patterson GH, Hirschberg K, Polishchuk RS, Gerlich D, Phair RD, Lippincott-Schwartz J. Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell 2008, 133:1055-1067. 10.1016/j.cell.2008.04.044, 2481404, 18555781.
14. Peters R. Nuclear envelope permeability measured by fluorescence microphotolysis of single liver cell nuclei. J Biol Chem 1983, 258:11427-11429.
15. Peters R. Nucleo-cytoplasmic flux and intracellular mobility in single hepatocytes measured by fluorescence microphotolysis. EMBO J 1985, 3:1831-1836.
16. Wei X, Henke VG, Strübing C, Brown EB, Clapham DE. Real-time imaging of nuclear permeation by EGFP in single intact cells. Biophys J 2003, 84:1317-1327. 10.1016/S0006-3495(03)74947-9, 1302708, 12547812.
17. Lippincott-Schwartz J, Altan-Bonnet N, Patterson GH. Photobleaching and photoactivation: following protein dynamics in living cells. Nat Cell Biol 2003, Suppl 7:S7-14.
18. Peters R, Brünger A, Schulten K. Continuous fluorescence microphotolysis: a sensitive method for studying diffusion processes in single cells. Proc Natl Acad Sci U S A 1981, 78:962-966. 10.1073/pnas.78.2.962, 319925, 16592981.
19. Kubitscheck U, Wedekind P, Peters R. Three-dimensional diffusion measurements by scanning microphotolysis. J Microsc 1998, 192:126-138.
20. Wachsmuth M, Weidemann T, Müller G, Hoffmann-Rohrer UW, Knoch TA, Waldeck W, Langowski J. Analyzing intracellular binding and diffusion with continuous fluorescence photobleaching. Biophys J 2003, 84:3353-3363. 10.1016/S0006-3495(03)70059-9, 1302895, 12719264.
21. Müller F, Mazza D, Stasevich TJ, McNally JG. FRAP and kinetic modeling in the analysis of nuclear protein dynamics: what do we really know?. Curr Opin Cell Biol 2010, 22:403-411. 10.1016/j.ceb.2010.03.002, 2916960, 20413286.
22. van Gemert AMC, Jost CR, van der Laan A, Dirks R, Reiber JH, Tanke HJ, Lelieveldt BP. Identification of cellular dynamic patterns resulting from repetitive photobleaching using independent component analysis. I S Biomed Imaging 2009, 1382-1385.
23. van de Giessen M, van der Laan A, Hendriks EA, Vidorreta M, Reiber JH, Jost CR, Tanke HJ, Lelieveldt BP. Fully automated attenuation measurement and motion correction in FLIP image sequences. IEEE Trans Med Imaging 2012, 31:461-473.
24. Klafter J, Shlesinger MF. On the relationship among three theories of relaxation in disordered systems. Proc Natl Acad Sci U S A 1986, 83:848-851. 10.1073/pnas.83.4.848, 322967, 16593658.
25. Koppel DE. Analysis of macromolecular polydispersity in intensity correlation spectroscopy: the method of cumulants. J Chem Phys 1972, 57:4814-4820.
26. Koppel DE, Carlson C, Smilowitz H. Analysis of heterogeneous fluorescence photobleaching by video kinetics imaging: the method of cumulants. J Microsc 1989, 155:199-206. 10.1111/j.1365-2818.1989.tb02882.x, 2795650.
27. Berberan-Santos MN, Bodunov EN, Valeur B. Mathematical functions for the analysis of luminescence decays with underlying distributions 1. Kohlrausch decay function (stretched exponential). Chemical Physics 2005, 315:171-182.
28. Lee KC, Siegel J, Webb SE, Lévêque-Fort S, Cole MJ, Jones R, Dowling K, Lever MJ, French PM. Application of the stretched exponential function to fluorescence lifetime imaging. Biophys J 2001, 81:1265-1274. 10.1016/S0006-3495(01)75784-0, 1301608, 11509343.
29. Kohlrausch R. Theorie des elektrischen Rückstandes in der Leidner Flasche. Pogg Ann Phys Chem 1854, 91:179-213.
30. Williams G, Watts DC. Non-symmetrical dielectric relaxation behaviour arising from a simple empirical decay function. Trans Farad Soc 1970, 66:80-85.
31. Shlesinger MF, Montroll EW. On the Williams-Watts function of dielectric relaxation. Proc Natl Acad Sci U S A 1984, 81:1280-1283. 10.1073/pnas.81.4.1280, 344813, 16593426.
32. Cumbrera FL, Sanchez-Bajo F, Guiberteau F, Solier JD, Muñoz A. The Williams-Watts dependence as a common phenomenological approach to relaxation processes in condensed matter. J Mat Sci 1993, 28:5387-5396.
33. Braga J, Desterro JM, Carmo-Fonseca M. Intracellular macromolecular mobility measured by fluorescence recovery after photobleaching with confocal laser scanning microscopes. Mol Biol Cell 2004, 15:4749-4760. 10.1091/mbc.E04-06-0496, 519164, 15292455.
34. Berberan-Santos MN. Mathematical basis of the integral formalism of chemical kinetics. Compact representation of the general solution of the first-order linear differential equation. J Math Chem 2010, 47:1184-1188.
35. Modeling in Biopharmaceutics, Pharmacokinetics, and Pharmacodynamics 2006, New Yrok: Springer, Macheras P, Iliadis A.
36. Berberan-Santos MN, Martinho JMG. A linear response approach to kinetics with time-dependent rate coefficients. Chem Phys 1992, 164:259-269.
37. Lund FW, Lomholt MA, Solanko LM, Wüstner D. Two-photon time-lapse microscopy of BODIPY-cholesterol reveals anomalous sterol diffusion in chinese hamster ovary cells. 2012, In press.
38. Chen Y, Müller JD. Probing nucleocytoplasmic transport by two-photon activation of PA-GFP. Microsc Res Tech 2006, 69:220-226. 10.1002/jemt.20252, 16538629.
39. Van Oostveldt P, Verhaegen F, Messens K. Heterogeneous photobleaching in confocal microscopy caused by differences in refractive index and excitation mode. Cytometry 1998, 32:137-146. 10.1002/(SICI)1097-0320(19980601)32:2<137::AID-CYTO9>3.0.CO;2-I, 9627227.
40. Wüstner D, Landt Larsen A, Færgeman NJ, Brewer JR, Sage D. Selective visualization of fluorescent sterols in Caenorhabditis elegans by bleach-rate based image segmentation. Traffic 2010, 11:440-454. 10.1111/j.1600-0854.2010.01040.x, 20070610.
41. Li SH, Li XJ. Huntingtin-protein interactions and the pathogenesis of Huntington's disease. Trends Genet 2004, 20:146-154. 10.1016/j.tig.2004.01.008, 15036808.
42. Hatters DM. Protein misfolding inside cells: the case of Huntingtin and Huntington's disease. IUBMB Life 2008, 60:724-728. 10.1002/iub.111, 18756529.
43. Kim S, Nollen EA, Kitagawa K, Bindokas VP, Morimoto RI. Polyglutamine protein aggregates are dynamic. Nat Cell Biol 2002, 4:826-831. 10.1038/ncb863, 12360295.
44. Matsumoto G, Kim S, Morimoto RI. Huntingtin and mutant SOD1 form aggregate structures with distinct molecular properties in human cells. J Biol Chem 2006, 281:4477-4485. 10.1074/jbc.M509201200, 16371362.
45. Lajoie P, Snapp EL. Formation and toxicity of soluble polyglutamine oligomers in living cells. PloS One 2010, 5:e15245. 10.1371/journal.pone.0015245, 3011017, 21209946.
46. Ossato G, Digman MA, Aiken C, Lukacsovich T, Marsh JL, Gratton E. A two-step path to inclusion formation of huntingtin peptides revealed by number and brightness analysis. Biophys J 2010, 98:3078-3085. 10.1016/j.bpj.2010.02.058, 2884247, 20550921.
47. Sage D, Neumann FR, Hediger F, Gasser SM, Unser M. Automatic tracking of individual fluorescence particles: application to the study of chromosome dynamics. IEEE T Image Process 2005, 14:1372-1383.
48. Brandt S. Datenanalyse 1999, Heidelberg: Spektrum Verlag.
49. Brown CM, Dalal RB, Hebert B, Digman MA, Horwitz AR, Gratton E. Raster image correlation spectroscopy (RICS) for measuring fast protein dynamics and concentrations with a commercial laser scanning confocal microscope. J Microsc 2008, 229:78-91. 10.1111/j.1365-2818.2007.01871.x, 18173647.
50. Kühn T, Ihalainen TO, Hyväluoma J, Dross N, Willman SF, Langowski J, Vihinen-Ranta M, Timonen J. Protein diffusion in mammalian cell cytoplasm. PLoS One 2011, 6:e22962. 10.1371/journal.pone.0022962, 3158749, 21886771.
51. Kasza KE, Rowat AC, Liu J, Angelini TE, Brangwynne CP, Koenderink GH, Weitz DA. The cell as a material. Curr Opin Cell Biol 2007, 19:101-107. 10.1016/j.ceb.2006.12.002, 17174543.
52. Brangwynne CP, Koenderink GH, MacKintosh FC, Weitz DA. Intracellular transport by active diffusion. Trends Cell Biol 2009, 19:423-427. 10.1016/j.tcb.2009.04.004, 19699642.
53. Bancaud A, Huet S, Daigle N, Mozziconacci J, Beaudouin J, Ellenberg J. Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO J 2009, 28:3785-3798. 10.1038/emboj.2009.340, 2797059, 19927119.
54. Hinde E, Cardarelli F, Digman MA, Gratton E. In vivo pair correlation analysis of EGFP intranuclear diffusion reveals DNA-dependent molecular flow. Proc Natl Acad Sci U S A 2010, 107:16560-16565. 10.1073/pnas.1006731107, 2944750, 20823232.
55. Digman MA, Gratton E. Imaging barriers to diffusion by pair correlation functions. Biophys J 2009, 97:665-673. 10.1016/j.bpj.2009.04.048, 2711318, 19619481.
56. Cardarelli F, Gratton E. In vivo imaging of single-molecule translocation through nuclear pore complexes by pair correlation functions. PLoS One 2010, 5:e10475. 10.1371/journal.pone.0010475, 2862743, 20454622.
57. Thevenaz P, Ruttimann UE, Unser E. A pyramid approach to subpixel registration based on intensity. IEEE T Image Process 1998, 7:27-41.
58. Chai Y, Shao J, Miller VM, Williams A, Paulson HL. Live-cell imaging reveals divergent intracellular dynamics of polyglutamine disease proteins and supports a sequestration model of pathogenesis. Proc Natl Acad Sci U S A 2002, 99:9310-9315. 10.1073/pnas.152101299, 123137, 12084819.
59. Nag S, Chen J, Irudayaraj J, Maiti S. Measurement of the attachment and assembly of small amyloid-beta oligomers on live cell membranes at physiological concentrations using single-molecule tools. Biophys J 2010, 99:1969-1975. 10.1016/j.bpj.2010.07.020, 2941002, 20858443.
60. Goodwin JS, Drake KR, Remmert CL, Kenworthy AK. Ras diffusion is sensitive to plasma membrane viscosity. Biophys J 2005, 89:1398-1410. 10.1529/biophysj.104.055640, 1366624, 15923235.
61. Wang H, Hu L, Dalen K, Dorward H, Marcinkiewicz A, Russell D, Gong D, Londos C, Yamaguchi T, Holm C, et al. Activation of hormone-sensitive lipase requires two steps, protein phosphorylation and binding to the PAT-1 domain of lipid droplet coat proteins. J Biol Chem 2009, 284:32116-32125. 10.1074/jbc.M109.006726, 2797282, 19717842.
62. McNairn AJ, Gerton JL. Intersection of ChIP and FLIP, genomic methods to study the dynamics of the cohesin proteins. Chromosome Res 2009, 17:155-163. 10.1007/s10577-008-9007-9, 19308698.
63. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122:735-749. 10.1016/j.cell.2005.06.043, 16143105.
64. Cunningham CW, Mukhopadhyay A, Lushington GH, Blagg BS, Prisinzano TE, Krise JP. Uptake, distribution and diffusivity of reactive fluorophores in cells: implications toward target identification. Mol Pharm 2010, 7:1301-1310. 10.1021/mp100089k, 2916926, 20557111.
65. Yu L, Bharadwaj S, Brown JM, Ma Y, Du W, Davis MA, Michaely P, Liu P, Willingham MC, Rudel LL. Cholesterol-regulated translocation of NPC1L1 to the cell surface facilitates free cholesterol uptake. J Biol Chem 2006, 281:6616-6624. 10.1074/jbc.M511123200, 16407187.
66. Bright GR, Fisher GW, Rogowska J, Taylor DL. Fluorescence ratio imaging microscopy. Methods in Cell Biology 1989, 30:157-192.