Fluorescent detection of fluid phase endocytosis allows for in vivo estimation of endocytic vesicle sizes in plant cells with sub-diffraction accuracy

Traffic

Volumn 11, Issue 4, 2010, Pages 548-559

  Gall, Lars ^a   Stan, Razvan C ^b   Kress, Alice ^a   Hertel, Brigitte ^a   Thiel, Gerhard ^a   Meckel, Tobias ^a,c  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b LEIDEN UNIVERSITY   (Netherlands)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

AFM; Alexa 488 hydrazide; CLSM; Dynamic light scattering; Fluid phase endocytosis; Guard cells; Liposomes; Molecular brightness

Indexed keywords

FLUORESCENT DYE; LIPOSOME;

ACCURACY; ARTICLE; CONTROLLED STUDY; CYTOCHEMISTRY; DIFFRACTION; ENDOCYTOSIS; ENDOSOME; FLUORESCENCE ANALYSIS; GUARD CELL; HYDROPHILICITY; IN VIVO STUDY; NONHUMAN; PLANT CELL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION;

CELLS, CULTURED; ENDOCYTOSIS; FLUORESCENT DYES; HYDRAZINES; LIPOSOMES; MICROSCOPY, FLUORESCENCE; STAINING AND LABELING; TRANSPORT VESICLES; VICIA FABA;

EID: 77951759239     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2010.01037.x     Document Type: Article

References (48)

1. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007, 8:603-612.
2. Ungewickell EJ, Hinrichsen L. Endocytosis: clathrin-mediated membrane budding. Curr Opin Cell Biol 2007, 19:417-425.
3. Meckel T, Gall L, Semrau S, Homann U, Thiel G. Guard cells elongate: relationship of volume and surface area during stomatal movement. Biophys J 2007, 92:1072-1080.
4. Shope JC, DeWald DB, Mott KA. Changes in surface area of intact guard cells are correlated with membrane internalization. Plant Physiol 2003, 133:1314-1321.
5. Shope JC, Mott KA. Membrane trafficking and osmotically induced volume changes in guard cells. J Exp Bot 2006, 57:4123-4131.
6. Homann U, Thiel G. Unitary exocytotic and endocytotic events in guard-cell protoplasts during osmotically driven volume changes. FEBS Lett 1999, 460:495-499.
7. Hurst AC, Meckel T, Tayefeh S, Thiel G, Homann U. Trafficking of the plant potassium inward rectifier KAT1 in guard cell protoplasts of Vicia faba. Plant J 2004, 37:391-397.
8. Sutter JU, Homann U, Thiel G. Ca(2)+-stimulated exocytosis in maize coleoptile cells. Plant Cell 2000, 12:1127-1136.
9. Sutter JU, Sieben C, Hartel A, Eisenach C, Thiel G, Blatt MR. Abscisic acid triggers the endocytosis of the arabidopsis KAT1 K+ channel and its recycling to the plasma membrane. Curr Biol 2007, 17:1396-1402.
10. Meckel T, Hurst AC, Thiel G, Homann U. Endocytosis against high turgor: intact guard cells of Vicia faba constitutively endocytose fluorescently labelled plasma membrane and GFP-tagged k-channel KAT1. Plant J 2004, 39:182-193.
11. Meckel T, Hurst AC, Thiel G, Homann U. Guard cells undergo constitutive and pressure-driven membrane turnover. Protoplasma 2005, 226:23-29.
12. Franks PJ, Buckley TN, Shope JC, Mott KA. Guard cell volume and pressure measured concurrently by confocal microscopy and the cell pressure probe. Plant Physiol 2001, 125:1577-1584.
13. Wartenberg M, Hamann J, Pratsch I, Donath E. Osmotically induced fluid-phase uptake of fluorescent markers by protoplasts ofchenopodium album. Protoplasma 1992, 166:61-66.
14. Diekmann W, Hedrich R, Raschke K, Robinson DG. Osmocytosis and vacuolar fragmentation in guard cell protoplasts: their relevance to osmotically-lnduced volume changes in guard cells. J Exp Bot 1993, 44:1569-1577.
15. Oparka KJ, Cole L, Wright KM, Coleman JOD, Hawes CR, Evans DE. Fluidphase endocytosis and intracelllular compartmentation of fluorescent probes. Endocytosis, Exocytosis and Vesicle Traffic in Plants 1991, 81-102. In: Hawes CR, Coleman JOD, and Evans DE, editors., Cambridge, UK: Cambridge University Press, p.
16. Wieser S, Schütz GJ. Tracking single molecules in the live cell plasma membrane - Do's and Don't's. Methods 2008, 46:131-140.
17. Baron-Epel O, Gharyal PK, Schindler M. Pectins as mediators of wall porosity in soybean cells. Planta 1988, 175:389-395.
18. Graham FL, Smiley J, Russell WC, Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 1977, 36:59-74.
19. Nagata T, Nemoto Y, Hasezawa S. Tobacco BY-2 cells as the hela cells in the cell biology of higher plants. Int Rev Cytol 1992, 132:1-30.
20. Bangham AD, Standish MM, Watkins JC. Diffusion of univalent ions across the lamellae of swollen phospholipids. J Mol Biol 1965, 13:238-252.
21. Mayer LD, Hope MJ, Cullis PR, Janoff AS. Solute distributions and trapping efficiencies observed in freeze-thawed multilamellar vesicles. Biochim Biophys Acta 1985, 817:193-196.
22. Olson F, Hunt CA, Szoka FC, Vail WJ, Papahadjopoulos D. Preparation of liposomes of defined size distribution by extrusion through polycarbonate membranes. Biochim Biophys Acta 1979, 557:9-23.
23. Hope MJ, Bally MB, Webb G, Cullis PR. Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim Biophys Acta 1985, 812:55-65.
24. MacDonald RC, Jones FD, Qiu R. Fragmentation into small vesicles of dioleoylphosphatidylcholine bilayers during freezing and thawing. Biochim Biophys Acta 1994, 1191:362-370.
25. Hope MJ, Nayar R, Mayer LD, Cullis PR. Reduction of liposome size and preparation of unilamellar vesicles by extrusion techniques. Liposome Technology 1993, 123-139. In: Gregoriadis G, editor., New York, NY: Macmillan Publishing Co., p.
26. Aliño SF, Garcia-Sanz M, Irruarrizaga A, Alfaro J, Hernandez J. High encapsulation efficiencies in sized liposomes produced by extrusion of dehydration-rehydration vesicles. J Microencapsul 1990, 7:497-503.
27. Kölchens S, Ramaswami V, Birgenheier J, Nett L, O'Brien DF. Quasi-elastic light scattering determination of the size distribution of extruded vesicles. Chem Phys Lipids 1993, 65:1-10.
28. Venetie RV, Leunissen-Bijvelt J. Size determination of sonicated vesicles by freeze-fracture electron microscopy, using the spray-freezing method. J Microsc 1980, 118:401-408.
29. Egelhaaf SU, Wehrli E, Muller M, Adrian M, Schurtenberger P. Determination of the size distribution of lecithin liposomes: a comparative study using freeze fracture, cryoelectron microscopy and dynamic light scattering. J Microsc 1996, 184:214-228.
30. Ruozi B, Tosi G, Forni F, Fresta M, Vandelli MA. Atomic force microscopy and photon correlation spectroscopy: two techniques for rapid characterization of liposomes. Eur J Pharm Sci 2005, 25:81-89.
31. Hamann S, Kiilgaard JF, Litman T, Alvarez-Leefmans FJ, Winther BR, Zeuthen T. Measurement of cell volume changes by fluorescence self-quenching. J Fluoresc 2002, 12:139-145.
32. Cole L, Coleman J, Kearns A, Morgan G, Hawes C. The organic anion transport inhibitor, probenecid, inhibits the transport of lucifer yellow at the plasma membrane and the tonoplast in suspensioncultured plant cells. J Cell Sci 1991, 99:545-555.
33. Mui BL, Cullis PR, Evans EA, Madden TD. Osmotic properties of large unilamellar vesicles prepared by extrusion. Biophys J 1993, 64:443-453.
34. Reigada D, Díez-Pérez I, Gorostiza P, Verdaguer A, Gómez de Aranda I, Pineda O, Vilarrasa J, Marsal J, Blasi J, Aleu J, Solsona C. Control of neurotransmitter release by an internal gel matrix in synaptic vesicles. Proc Natl Acad Sci U S A. 2003, 100:3485-3490.
35. Paula S, Volkov AG, Van Hoek AN, Haines TH, Deamer DW. Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. Biophys J 1996, 70:339-348.
36. Beney L, Linares E, Ferret E, Gervais P. Influence of the shape of phospholipid vesicles on the measurement of their size by photon correlation spectroscopy. Eur Biophys J 1998, 27:567-574.
37. Pencer J, White GF, Hallett FR. Osmotically induced shape changes of large unilamellar vesicles measured by dynamic light scattering. Biophys J 2001, 81:2716-2728.
38. Barth M, Holstein SE. Identification and functional characterization of arabidopsis AP180, a binding partner of plant alphac-adaptin. J Cell Sci 2004, 117:2051-2062.
39. Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof YD, Friml J. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in arabidopsis. Curr Biol 2007, 17:520-527.
40. Doohan ME, Palevitz BA. Microtubules and coated vesicles in guard-cell protoplasts ofallium cepa L. Planta 1980, 149:389-401.
41. Robinson DG, Hinz G, Holstein SE. The molecular characterization of transport vesicles. Plant Mol Biol 1998, 38:49-76.
42. Baluska F, Samaj J, Hlavacka A, Kendrick-Jones J, Volkmann D. Actin-dependent fluid-phase endocytosis in inner cortex cells of maize root apices. J Exp Bot 2004, 55:463-473.
43. Stewart WW. Lucifer dyes - highly fluorescent dyes for biological tracing. Nature 1981, 292:17-21.
44. Stelzer EHK. Contrast, resolution, pixelation, dynamic range and signal-to-noise ratio: fundamental limits to resolution in fluorescence light microscopy. J. Microsc 1998, 189:15-24.
45. Charpilienne A, Nejmeddine M, Berois M, Parez N, Neumann E, Hewat E. Individual rotavirus-like particles containing 120 molecules of fluorescent protein are visible in living cells. J Biol Chem 2001, 276:29361-29367.
46. Mayer LD, Hope MJ, Cullis PR. Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim Biophys Acta 1986, 858:161-168.
47. Bioanalytic 1998, Lottspeich FZorbas H. editors., Heidelberg, Berlin, Spektrum Akademischer Verlag
48. Kanno T, Yamada T, Iwabuki H, Tanaka H, Kuroda S, Tanizawa K, Kawai T. Size distribution measurement of vesicles by atomic force microscopy. Anal Biochem 2002, 309:196-199.