Ultrastructural imaging of endocytic sites in saccharomyces cerevisiae by transmission electron microscopy and immunolabeling

Microscopy and Microanalysis

Volumn 19, Issue 2, 2013, Pages 381-392

  Buser, Christopher ^a   Drubin, David G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

actin filaments; anti GFP immunolabeling; electron tomography; endocytosis; freeze substitution; high pressure freezing; immunogold labeling; trafficking; transmission electron microscopy; yeast

Indexed keywords

ACTIN; CYTOSKELETON PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; ENDOCYTOSIS; EVALUATION; FREEZE DRYING; HISTOLOGY; IMMUNOELECTRON MICROSCOPY; METABOLISM; METHODOLOGY; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ACTINS; CYTOSKELETAL PROTEINS; ENDOCYTOSIS; FREEZE SUBSTITUTION; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, IMMUNOELECTRON; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TISSUE EMBEDDING;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 84875414373     PISSN: 14319276     EISSN: 14358115     Source Type: Journal    
DOI: 10.1017/S1431927612014304     Document Type: Article

References (59)

1. Adams, A.E. & Pringle, J.R.-1984!. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J Cell Biol 98, 934-945
2. Boettner, D.R., Chi, R.J. & Lemmon, S.K.-2012!. Lessons from yeast for clathrin-mediated endocytosis. Nat Cell Biol 14, 2-10
3. Boucrot, E., Saffarian, S., Massol, R., Kirchhausen, T. & Ehrlich, M.-2006!. Role of lipids and actin in the formation of clathrin-coated pits. Exp Cell Res 312, 4036-4048
4. Boulant, S., Kural, C., Zeeh, J.C., Ubelmann, F. & Kirchhausen, T.-2011!. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 13, 1124-1131
5. Buser, C. & McDonald, K.-2010!. Correlative GFPimmunoelectron microscopy in yeast. Methods Enzymol 470, 603-618
6. Buser, C. &Walther, P.-2008!. Freeze-substitution: The addition of water to polar solvents enhances the retention of structure and acts at temperatures around -60 degrees C. J Microsc 230, 268-277
7. Carlemalm, E., Garavito, R.M. & Villiger, W.-1982!. Resin development for electron-microscopy and an analysis of embedding at low-temperature. J Microsc-Oxford 126, 123-143
8. Collins, A.,Warrington, A., Taylor, K.A. & Svitkina, T.-2011!. Structural organization of the actin cytoskeleton at sites of clathrin-mediated endocytosis. Curr Biol 21, 1167-1175
9. Collins, K.M., Thorngren, N.L., Fratti, R.A. & Wickner,W.T.-2005!. Sec17p and HOPS, in distinct SNARE complexes, mediate SNARE complex disruption or assembly for fusion. EMBO J 24, 1775-1786
10. Collins, T.J.-2007!. ImageJ for microscopy. Biotechniques 43, 25-30
11. Doherty, G.J. & McMahon, H.T.-2009!. Mechanisms of endocytosis. Annu Rev Biochem 78, 857-902
12. Engqvist-Goldstein, A.E. & Drubin, D.G.-2003!. Actin assembly and endocytosis: From yeast to mammals. Annu Rev Cell Dev Biol 19, 287-332
13. Fazi, B., Cope, M.J., Douangamath, A., Ferracuti, S., Schirwitz, K., Zucconi, A., Drubin, D.G., Wilmanns, M., Cesareni, G. & Castagnoli, L.-2002!. Unusual binding properties of the SH3 domain of the yeast actin-binding protein Abp1: Structural and functional analysis. J Biol Chem 277, 5290-5298
14. Goode, B.L., Rodal, A.A., Barnes, G. & Drubin, D.G.-2001!. Activation of the Arp2/3 complex by the actin filament binding protein Abp1p. J Cell Biol 153, 627-634
15. Henne,W.M., Boucrot, E.,Meinecke, M., Evergren, E., Vallis, Y., Mittal, R. & McMahon, H.T.-2010!. FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328, 1281-1284
16. Humbel, B.M. & Mueller, M.-1985!. Freeze substitution and low temperature embedding. In Science of Biological Specimen Preparation, Mueller, M., Becker, R.P., Boyde, A. & Wolosewick, J.J.-Eds.!, pp. 175-183. Chicago, IL: SEM Inc., AMF O'Hare
17. Idrissi, F.Z., Blasco, A., Espinal, A. & Geli, M.I.-2012!. Ultrastructural dynamics of proteins involved in endocytic budding. Proc Natl Acad Sci USA 109-39!, E2589-2594
18. Idrissi, F.Z., Grotsch, H., Fernandez-Golbano, I.M., Presciatto-Baschong, C., Riezman, H. & Geli, M.I.-2008!. Distinct acto/myosin-I structures associate with endocytic profiles at the plasma membrane. J Cell Biol 180, 1219-1232
19. Kaksonen, M., Sun, Y. & Drubin, D.G.-2003!. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115, 475-487
20. Kaksonen, M., Toret, C.P. & Drubin, D.G.-2005!. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123, 305-320
21. Kaksonen, M., Toret, C.P. & Drubin, D.G.-2006!. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7, 404-414
22. Kilmartin, J.V. & Adams, A.E.-1984!. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J Cell Biol 98, 922-933
23. Kim, K., Galletta, B.J., Schmidt, K.O., Chang, F.S., Blumer, K.J. & Cooper, J.A.-2006!. Actin-based motility during endocytosis in budding yeast. Mol Biol Cell 17, 1354-1363
24. Kishimoto, T., Sun, Y., Buser, C., Liu, J.,Michelot, A. & Drubin, D.G.-2011!. Determinants of endocytic membrane geometry, stability, and scission. Proc Natl Acad Sci USA 108, E979-988
25. Koestler, S.A., Auinger, S., Vinzenz, M., Rottner, K. & Small, J.V.-2008!. Differentially oriented populations of actin filaments generated in lamellipodia collaborate in pushing and pausing at the cell front. Nat Cell Biol 10, 306-313
26. Kremer, J.R., Mastronarde, D.N. & McIntosh, J.R.-1996!. Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116, 71-76
27. Kukulski, W., Schorb, M., Kaksonen, M. & Briggs, J.A.-2012!. Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 150, 508-520
28. Kukulski, W., Schorb, M., Welsch, S., Picco, A., Kaksonen, M. & Briggs, J.A.-2011!. Correlated fluorescence and 3D electron microscopy with high sensitivity and spatial precision. J Cell Biol 192, 111-119
29. Liu, J., Kaksonen, M., Drubin, D.G. & Oster, G.-2006!. Endocytic vesicle scission by lipid phase boundary forces. Proc Natl Acad Sci USA 103, 10277-10282
30. Liu, J., Sun, Y., Drubin, D.G. & Oster, G.F.-2009!. The mechanochemistry of endocytosis. PLoS Biol 7, e1000204
31. Mastronarde, D.N.-1997!. Dual-axis tomography: An approach with alignment methods that preserve resolution. J Struct Biol 120, 343-352
32. Mastronarde, D.N.-2005!. Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152, 36-51
33. McMahon, H.T. & Boucrot, E.-2011!. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12, 517-533
34. Mercogliano, C.P. & DeRosier, D.J.-2007!. Concatenated metallothionein as a clonable gold label for electron microscopy. J Struct Biol 160, 70-82
35. Merrifield, C.J., Feldman, M.E., Wan, L. & Almers, W.-2002!. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4, 691-698
36. Moreira, K.E., Walther, T.C., Aguilar, P.S. & Walter, P.-2009!. Pil1 controls eisosome biogenesis. Mol Biol Cell 20, 809-818
37. Mulholland, J., Preuss, D., Moon, A., Wong, A., Drubin, D. & Botstein, D.-1994!. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J Cell Biol 125, 381-391
38. Murk, J.L., Posthuma, G., Koster, A.J., Geuze, H.J., Verkleij, A.J., Kleijmeer, M.J. & Humbel, B.M.-2003!. Influence of aldehyde fixation on the morphology of endosomes and lysosomes: Quantitative analysis and electron tomography. J Microsc 212, 81-90
39. Newpher, T.M., Smith, R.P., Lemmon, V. & Lemmon, S.K.-2005!. In vivo dynamics of clathrin and its adaptor-dependent recruitment to the actin-based endocytic machinery in yeast. Dev Cell 9, 87-98
40. Nixon, S.J.,Webb, R.I., Floetenmeyer, M., Schieber, N., Lo, H.P. & Parton, R.G.-2009!. A single method for cryofixation and correlative light, electron microscopy and tomography of zebrafish embryos. Traffic 10, 131-136
41. Seedorf, M., Damelin, M., Kahana, J., Taura, T. & Silver, P.A.-1999!. Interactions between a nuclear transporter and a subset of nuclear pore complex proteins depend on Ran GTPase. Mol Cell Biol 19, 1547-1557
42. Sims, P.A. & Hardin, J.D.-2007!. Fluorescence-integrated transmission electron microscopy images: Integrating fluorescence microscopy with transmission electron microscopy. Methods Mol Biol 369, 291-308
43. Smaczynska-de Rooij, I., Allwood, E.G., Aghamohammadzadeh, S., Hettema, E.H., Goldberg, M.W. & Ayscough, K.R.-2010!. A role for the dynamin-like protein Vps1 during endocytosis in yeast. J Cell Sci 123, 3496-3506
44. Smythe, E. & Ayscough, K.R.-2006!. Actin regulation in endocytosis. J Cell Sci 119, 4589-4598
45. Stefan, C.J., Padilla, S.M., Audhya, A. & Emr, S.D.-2005!. The phosphoinositide phosphatase Sjl2 is recruited to cortical actin patches in the control of vesicle formation and fission during endocytosis. Mol Cell Biol 25, 2910-2923
46. Stradalova, V., Blazikova, M., Grossmann, G., Opekarova, M., Tanner,W. & Malinsky, J.-2012!. Distribution of cortical endoplasmic reticulum determines positioning of endocytic events in yeast plasma membrane. PLoS One 7, e35132
47. Stradalova,V., Stahlschmidt,W., Grossmann, G., Blazikova, M., Rachel, R., Tanner, W. & Malinsky, J.-2009!. Furrowlike invaginations of the yeast plasma membrane correspond to membrane compartment of Can1. J Cell Sci 122, 2887-2894
48. Sun, Y.,Martin, A.C. & Drubin, D.G.-2006!. Endocytic internalization in budding yeast requires coordinated actin nucleation and myosin motor activity. Dev Cell 11, 33-46
49. Svitkina, T.M. & Borisy, G.G.-1999!. Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 145, 1009-1026
50. Takeo, K., Shigeta, M. & Takagi, Y.-1976!. Plasma membrane ultrastructural differences between the exponential and stationary phases of Saccharomyces cerevisiae as revealed by freezeetching. J Gen Microbiol 97, 323-329
51. Tokuyasu, K.T.-1973!. A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 57, 551-565
52. Toret, C.P., Lee, L., Sekiya-Kawasaki, M. & Drubin, D.G.-2008!. Multiple pathways regulate endocytic coat disassembly in Saccharomyces cerevisiae for optimal downstream trafficking. Traffic 9, 848-859
53. Walther, P.-2008!. High-resolution cryo-SEM allows direct identification of F-actin at the inner nuclear membrane of Xenopus oocytes by virtue of its structural features.JMicrosc 232, 379-385
54. Walther, P., Muller, M. & Schweingruber, M.E.-1984!. The ultrastructure of the cell-surface and plasma-membrane of exponential and stationary phase cells of Schizosaccharomyces- Pombe, grown in different media. Arch Microbiol 137, 128-134
55. Walther, P. & Ziegler, A.-2002!. Freeze substitution of highpressure frozen samples: The visibility of biological membranes is improved when the substitution medium contains water. J Microsc 208, 3-10
56. Walther, T.C., Brickner, J.H., Aguilar, P.S., Bernales, S., Pantoja, C. & Walter, P.-2006!. Eisosomes mark static sites of endocytosis. Nature 439, 998-1003
57. Wang, Q., Mercogliano, C.P. & Lowe, J.-2011!. A ferritin-based label for cellular electron cryotomography. Structure 19, 147-154
58. Weinberg, J. & Drubin, D.G.-2012!. Clathrin-mediated endocytosis in budding yeast. Trends Cell Biol 22, 1-13
59. Yarar, D., Waterman-Storer, C.M. & Schmid, S.L.-2005!. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16, 964-975