Visualizing the functional architecture of the endocytic machinery

eLife

Volumn 2015, Issue 4, 2015, Pages

  Picco, Andrea ^a   Mund, Markus ^a   Ries, Jonas ^a   Nédélec, François ^a   Kaksonen, Marko ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; COAT PROTEIN; ACTIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; CYTOARCHITECTURE; ENDOCYTOSIS; FLUORESCENCE; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; IMAGE ANALYSIS; MATHEMATICAL PARAMETERS; MEMBRANE VESICLE; PROTEIN DOMAIN; PROTEOMICS; SPATIAL ANALYSIS; WESTERN BLOTTING; CHEMISTRY; PHYSIOLOGY; POLYMERIZATION;

ACTINS; CLATHRIN; ENDOCYTOSIS; MICROSCOPY, FLUORESCENCE; POLYMERIZATION;

EID: 84965084012     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.04535     Document Type: Article

References (81)

1. Aghamohammadzadeh, S., and Ayscough, K.R. (2009). Differential requirements for actin during yeast and mammalian endocytosis. Nat Cell Biol 11, 1039-1042. doi:10.1038/ncb1918.
2. Arasada, R., Pollard, T.D. (2011). Distinct roles for F-BAR proteins Cdc15p and Bzzlp in actin polymerization at sites of endocytosis in fission yeast. Curr. Biol. 21(7), 1450-1459. doi: 10.1016/j.cub.2011.07.046.
3. Baggett, J.J., D'Aquino, K.E., and Wendland, B. (2003). The Sla2p talin domain plays a role in endocytosis in Saccharomyces cerevisiae. Genetics 165, 1661-1674.
4. Berro, J., Sirotkin, V., Pollard, T.D. (2010). Mathematical modeling of endocytic actin patch kinetics in fission yeast: disassembly requires release of actin filament fragments. MBoC 21, 2905-2915. doi: 10.1091/mboc.E10-06-0494.
5. Berro, J., and Pollard, T.D. (2014). Local and global analysis of endocytic patch dynamics in fission yeast using a new “temporal superresolution” realignment method. MBoC 25, 3501-3514. doi: 10.1091/mbc.E13-01-0004.
6. Betzig, E., Patterson, G.H., Sougrat, R., Lindwasser, O.W., Olenych, S., Bonifacino, J.S., Davidson, M.W., Lippincott-Schwartz, J., and Hess, H.F. (2006). Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642-1645. doi:10.1126/science.1127344.
7. Bénédetti, H., Raths, S., Crausaz, F., and Riezman, H. (1994). The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Mol Biol Cell 5, 1023-1037. doi:10.1091/mbc.5.9.1023.
8. Boettner, D.R., Chi, R.J., and Lemmon, S.K. (2012). Lessons from yeast for clathrin-mediated endocytosis. Nat Cell Biol 14, 2-10. doi:10.1038/ncb2403.
9. Boettner, D.R., Friesen, H., Andrews, B., and Lemmon, S.K. (2011). Clathrin light chain directs endocytosis by influencing the binding of the yeast HipIR homologue, Sla2, to F-actin. Mol Biol Cell 22, 3699-3714. doi:10.1091/mbc.E11-07-0628.
10. Boucrot, E., Pick, A., Çamdere, G., Liska, N., Evergren, E., McMahon, H.T., and Kozlov, M.M. (2012). Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149, 124-136. doi:10.1016/j.cell.2012.01.047.
11. Boulant, S., Kural, C., Zeeh, J.-C., Ubelmann, F., and Kirchhausen, T. (2011). Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 13, 1124-1131. doi:10.1038/ncb2307.
12. Brodsky, F.M., Chen, C.Y., Knuehl, C., Towler, M.C., and Wakeham, D.E. (2001). Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17, 517-568. doi:10.1146/annurev.cellbio.17.1.517.
13. Carroll, S.Y., Stimpson, H.E.M., Weinberg, J., Toret, C.P., Sun, Y., and Drubin, D.G. (2012). Analysis of yeast endocytic site formation and maturation through a regulatory transition point. Mol Biol Cell 23, 657-668. doi:10.1091/mbc.E11-02-0108.
14. Chen, Q., Pollard, T.D. (2012). Actin filament severing by cofinling dismantles actin patches and produces mother filaments for new patches. Curr. Biol., 23(13), 1154-1162. doi:10.1016/j.cub.2013.05.005.
15. Cocucci, E., Aguet, F., Boulant, S., and Kirchhausen, T. (2012). The first five seconds in the life of a clathrin-coated pit. Cell 150, 495-507. doi:10.1016/j.cell.2012.05.047.
16. Collins, A., Warrington, A., Taylor, K.A., and Svitkina, T. (2011). Structural organization of the actin cytoskeleton at sites of clathrin-mediated endocytosis. Curr Biol 21, 1167-1175. doi:10.1016/j.cub.2011.05.048.
17. Conibear, E. (2010). Converging views of endocytosis in yeast and mammals. Curr Opin Cell Biol 22, 513-518. doi:10.1016/j.ceb.2010.05.009.
18. D'Agostino, J.L., and Goode, B.L. (2005). Dissection of Arp2/3 complex actin nucleation mechanism and distinct roles for its nucleation-promoting factors in Saccharomycescerevisiae. Genetics 171, 35-47. doi:10.1534/genetics.105.040634.
19. Doherty, G.J., and McMahon, H.T. (2009). Mechanisms of endocytosis. Annu Rev Biochem 78, 857-902. doi:10.1146/annurev.biochem.78.081307.110540.
20. Doyle, T., and Botstein, D. (1996). Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc Natl Acad Sci USA 93, 3886-3891.
21. Engqvist-Goldstein, A.E., Warren, R.A., Kessels, M.M., Keen, J.H., Heuser, J., and Drubin, D.G. (2001). The actin-binding protein HipIR associates with clathrin during early stages of endocytosis and promotes clathrin assembly in vitro. J Cell Biol 154, 1209-1223.doi:10.1083/jcb.200106089.
22. Evangelista, M., Klebl, B.M., Tong, A.H., Webb, B.A., Leeuw, T., Leberer, E., Whiteway, M., Thomas, D.Y., and Boone, C. (2000). A role for myosin-l in actin assembly through interactions with Vrplp, Beelp, and the Arp2/3 complex. J Cell Biol 148, 353-362. doi:10.1083/jcb.148.2.353.
23. Fotin, A., Cheng, Y., Sliz, P., Grigorieff, N., Harrison, S.C., Kirchhausen, T., and Walz, T. (2004). Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432, 573-579. doi:10.1038/nature03078.
24. Gaidarov, I., Santini, F., Warren, R.A., and Keen, J.H. (1999). Spatial control of coated-pitdynamics in living cells. NatCell Biol 1, 1-7. doi:10.1038/8971.
25. Galletta, B.J., Chuang, D.Y., and Cooper, J.A. (2008). Distinct Roles for Arp2/3 Regulators in Actin Assembly and Endocytosis. PLoS Biol 6, e1. doi:10.1371/journal.pbio.0060001.
26. Godlee, C., and Kaksonen, M. (2013). From uncertain beginnings: Initiation mechanisms of clathrin-mediated endocytosis. J Cell Biol 203, 717-725. doi:10.1083/jcb.201307100 .
27. Hess, S. T., Girirajan, T. P. K. and Mason, M. D. (2006). Ultra-High Resolution Imaging by Fluorescence Photoactivation Localization Microscopy. Biophysical Journal 91,4258-4272. doi: 10.1529/biophysj.106.091116.
28. Holtzman, D.A., Yang, S., and Drubin, D.G. (1993). Synthetic-lethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly in Saccharomyces cerevisiae. J Cell Biol 122, 635-644. doi:10.1083/jcb.122.3.635.
29. Idrissi, F.-Z., Blasco, A., Espinal, A., and Geli, M.-l. (2012). Ultrastructural dynamics of proteins involved in endocytic budding. Proceedings of the National Academy ofSciences 109, E2587-E2594. doi:10.1073/pnas.1202789109.
30. Idrissi, F.-Z., Grõtsch, H., Fernández-Golbano, I.M., Presciatto-Baschong, C., Riezman, H., and Geli, M.-l. (2008). Distinct acto/myosin-l structures associate with endocytic profiles at the plasma membrane. J Cell Biol 180, 1219-1232. doi:10.1083/jcb.200708060.
31. Horn, B.K.P. (1987). Closed-form solution of absolute orientation using unit quaternions. J. Opt. Soc. Am. a, JOSAA 4, 629-642. doi:10.1364/JOSAA.4.000629.
32. Joglekar, A.P., Bouck, D.C., Molk, J.N., Bloom, K.S., and Salmon, E.D. (2006). Molecular architecture of a kinetochore-microtubule attachment site. Nat Cell Biol 8, 581-585. doi:10.1038/ncb1414.
33. Jonsdottir, G.A., and Li, R. (2004). Dynamics of yeast Myosin I: evidence for a possible role in scission of endocytic vesicles. Curr Biol 14, 1604-1609. doi:10.1016/j.cub.2004.08.055.
34. Kaksonen, M., Sun, Y., and Drubin, D.G. (2003). A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115, 475­-487. doi:10.1016/S0092-8674(03)00883-3
35. Kaksonen, M., Toret, C.P., and Drubin, D.G. (2005). A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123, 305-320. doi:10.1016/j.cell.2005.09.024.
36. Khmelinskii, A., Keller, P.J., Bartosik, A., Meurer, M., Barry, J.D., Mardin, B.R., Kaufmann, A., Trautmann, S., Wachsmuth, M., Pereira, G., et al. (2012). Tandem fluorescent protein timers for in vivo analysis of protein dynamics. Nat. Biotechnol. 30, 708-714. doi:10.1038/nbt.2281.
37. Khmelinskii, A., Meurer, M., Duishoev, N., Delhomme, N., and Knop, M. (2011). Seamless gene tagging by endonuclease-driven homologous recombination. PLoS ONE 6, e23794. doi:10.1371/journal.pone.0023794.
38. Kirchhausen, T. (2009). Imaging endocytic clathrin structures in living cells. Trends in Cell Biology 19, 596-605. doi:10.1016/j.tcb.2009.09.002.
39. Kishimoto, T., Sun, Y., Buser, C., Liu, J., Michelot, A., and Drubin, D.G. (2011). Determinants of endocytic membrane geometry, stability, and scission. Proceedings of the National Academy of Sciences 108, E979-E988. doi:10.1073/pnas.1113413108.
40. Kukulski, W., Schorb, M., Kaksonen, M., and Briggs, J.A.G. (2012). Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 150, 508-520. doi:10.1016/j.cell.2012.05.046.
41. Lawrimore, J., Bloom, K.S., and Salmon, E.D. (2011). Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome. J Cell Biol 195, 573-582. doi:10.1083/jcb.201106036.
42. Lechler, T., Shevchenko, A., and Li, R. (2000). Direct involvement of yeast type I myosins in Cdc42-dependent actin polymerization. J Cell Biol 148, 363-373. doi:10.1083/jcb.148.2.363.
43. Liu, J., Kaksonen, M., Drubin, D.G., and Oster, G. (2006). Endocytic vesicle scission by lipid phase boundary forces. Proc Natl Acad Sci USA 103, 10277­-10282. doi:10.1073/pnas.0601045103.
44. Loerke, D., Mettlen, M., Schmid, S.L., and Danuser, G. (2011). Measuring the Hierarchy of Molecular Events During Clathrin-Mediated Endocytosis. Traffic 12, 815-825. doi:10.1111/j.1600-0854.2011.01197.x.
45. Maeder, C.I., Hink, M.A., Kinkhabwala, A., Mayr, R., Bastiaens, P.I.H., and Knop, M. (2007). Spatial regulation of Fus3 MAP kinase activity through a reaction-diffusion mechanism in yeast pheromone signalling. Nat Cell Biol 9, 1319-1326. doi:10.1038/ncb1652.
46. Merrifield, C.J. (2004). Seeing is believing: imaging actin dynamics at single sites of endocytosis. Trends in Cell Biology 14, 352-358. doi:10.1016/j.tcb.2004.05.008.
47. Merrifield, C.J., Feldman, M.E., Wan, L., and Aimers, W. (2002). Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4, 691-698. doi:10.1038/ncb837.
48. Milosevic, I., Giovedi, S., Lou, X., Raimondi, A., Collesi, C., Shen, H., Paradise, S., O’Toole, E., Ferguson, S., Cremona, O., De Camilli, P. (2011). Recruitment of endophilinto clathrin-coated pit necks required for efficient vesicle uncoating after fission. Neuron 72(4):587-601, doi: 10.1016/j.neuron.2011.08.029.
49. Mim, C., Cui, H., Gawronski-Salerno, J.A., Frost, A., Lyman, E., Voth, G.A., and Unger, V.M. (2012). Structural Basis of Membrane Bending by the N-BAR Protein Endophilin. Cell 149, 137-145. doi:10.1016/j.cell.2012.01.048.
50. Mizuno, N., Jao, C.C., Langen, R., and Steven, A.C. (2010). Multiple modes of endophilin-mediated conversion of lipid vesicles into coated tubes: implications for synaptic endocytosis. Journal of Biological Chemistry 285, 23351-23358. doi:10.1074/jbc.M110.143776.
51. Mooren, O.L., Galletta, B.J., and Cooper, J.A. (2012). Roles for actin assembly in endocytosis. Annu Rev Biochem 81, 661-686. doi:10.1146/annurev-biochem-060910-094416.
52. Mulholland, J., Preuss, D., Moon, A., Wong, A., Drubin, D., and Botstein, D. (1994). Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J Cell Biol 125, 381-391. doi:10.1083/jcb.125.2.381.
53. Mund, M., Kaplan, C. & Ries, J. (2014). Localization microscopy in yeast. Methods Cell Biol. 123, 253-271. doi:10.1016/B978-0-12-420138-5.00014-8.
54. Newpher, T.M., Smith, R.P., Lemmon, V., and 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. doi:10.1016/j.devcel.2005.04.014.
55. Peter, B.J., Kent, H.M., Mills, I.G., Vallis, Y., Butler, P.J.G., Evans, P.R., and McMahon, H.T. (2004). BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499. doi:10.1126/science.1092586.
56. Pollard, T.D., and Borisy, G.G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465. doi:10.1016/S0092-8674(03)00120-X.
57. Ren, G., Vajjhala, P., Lee, J.S., Winsor, B., and Munn, A.L. (2006). The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol. Mol. Biol. Rev. 70, 37-120. doi:10.1128/MMBR.70.1.37-120.2006.
58. Ries, J., Kaplan, C., Platonova, E., Eghlidi, H., and Ewers, H. (2012). Asimple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat Methods 9, 582-584. doi:10.1038/nmeth.1991.
59. Rodal, A.A., Manning, A.L., Goode, B.L., and Drubin, D.G. (2003). Negative regulation of yeast WASp by two SH3 domain-containing proteins. Curr Biol 13, 1000-1008. doi:10.1016/S0960-9822(03)00383-X.
60. Rust, M.J., Bates, M., and Zhuang, X. (2006). Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3, 793­-795. doi:10.1038/nmeth929.
61. Saffarian, S., and Kirchhausen, T. (2008). Differential evanescence nanometry: live-cell fluorescence measurements with 10-nm axial resolution on the plasma membrane. 94, 2333-2342. doi:10.1529/biophysj.107.117234.
62. Sbalzarini, I.F., and Koumoutsakos, P. (2005). Feature point tracking and trajectory analysis for video imaging in cell biology. Journal of Structural Biology 151, 182-195. doi:10.1016/j.jsb.2005.06.002.
63. Sirotkin, V., Berro, J., Macmillan, K., Zhao, L., and Pollard, T.D. (2010). Quantitative analysis of the mechanism of endocytic actin patch assembly and disassembly in fission yeast. Mol Biol Cell 21, 2894-2904. doi:10.1091/mbc.E10-02-0157.
64. Skruzny, M., Brach, T., Ciuffa, R., Rybina, S., Wachsmuth, M., and Kaksonen, M. (2012). Molecular basis for coupling the plasma membrane to the actin cytoskeleton during clathrin-mediated endocytosis. Proceedings of the National Academy ofSciences 109, E2533-E2542. doi:10.1073/pnas.1207011109.
65. Smaczynska-de Rooij, I.I., Allwood, E.G., Mishra, R., Booth, W.I., Aghamohammadzadeh, S., Goldberg, M.W., and Ayscough, K.R. (2012). Yeast dynamin Vps1 and amphiphysin Rvs167 function together during endocytosis. Traffic 13, 317-328. doi:10.1111/j.1600-0854.2011.01311.x.
66. Sorre, B., Callan-Jones, A., Manzi, J., Goud, B., Prost, J., Bassereau, P., and Roux, A. (2012). Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proceedings of the National Academy of Sciences 109, 173-178. doi:10.1073/pnas.1103594108.
67. Stirling Churchman, L., Flyvbjerg, H., and Spudich, J.A. (2006). A Non- Gaussian Distribution Quantifies Distances Measured with Fluorescence Localization Techniques. Biophys J 90, 668-671. doi:10.1529/biophysj.105.065599.
68. Suetsugu, S. (2009). The direction of actin polymerization for vesicle fission suggested from membranes tubulated by the EFC/F-BAR domain protein FBP17. FEBS Lett. 583, 3401-3404. doi:10.1016/j.febslet.2009.10.019.
69. Sun, X., Zhang, A., Baker, B., Sun, L., Howard, A., Buswell, J., Maurel, D., Masharina, A., Johnsson, K., Noren, C.J., et al. (2011). Development of SNAP- tag fluorogenic probes for wash-free fluorescence imaging. Chembiochem 12, 2217-2226. doi:10.1002/cbic.201100173.
70. Sun, Y., Kaksonen, M., Madden, D.T., Schekman, R., and Drubin, D.G. (2005). Interaction of Sla2p's ANTH domain with Ptdlns(4,5)P2 is important for actin- dependent endocytic internalization. Mol Biol Cell 16, 717-730. doi:10.1091/mbc.E04-08-0740.
71. Sun, Y., Martin, A.C., and Drubin, D.G. (2006). Endocytic Internalization in Budding Yeast Requires Coordinated Actin Nucleation and Myosin Motor Activity. DevCell 11, 33-46. doi:10.1016/j.devcel.2006.05.008.
72. Takenawa, T., and Suetsugu, S. (2007). The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 8, 37-48. doi: 10.1038/nrm2069.
73. Tang, H.Y., Xu, J., and Cai, M. (2000). Panlp, End3p, and Slalp, three yeast proteins required for normal cortical actin cytoskeleton organization, associate with each other and play essential roles in cell wall morphogenesis. Mol. Cell. Biol. 20, 12-25. doi: 10.1128/MCB.20.1.12-25.2000
74. Taylor, M.J., Perrais, D., and Merrifield, C.J. (2011). A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9, e1000604. doi:10.1371/journal.pbio.1000604.
75. Tebar, F., Sorkina, T., Sorkin, A., Ericsson, M., and Kirchhausen, T. (1996). Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits. J. Biol. Chem. 271, 28727-28730. doi:10.1074/jbc.271.46.28727.
76. Vigers, G.P., Crowther, R.A., and Pearse, B.M. (1986). Location of the 100 kd- 50 kd accessory proteins in clathrin coats. Embo J 5, 2079-2085.
77. Weinberg, J., and Drubin, D.G. (2012). Clathrin-mediated endocytosis in budding yeast. Trends in Cell Biology 22, 1-13. doi:10.1016/j.tcb.2011.09.001.
78. Winter, D., Lechler, T., and Li, R. (1999). Activation of the yeastArp2/3 complex by Beelp, a WASP-family protein. Curr Biol 9, 501-504.
79. Wu, J.Q., and Pollard, T.D. (2005). Counting cytokinesis proteins globally and locally in fission yeast. Science 310, 310-314. doi:10.1126/science.1113230.
80. Youn, J.-Y., Friesen, H., Kishimoto, T., Henne, W.M., Kurat, C.F., Ye, W., Ceccarelli, D.F., Sicheri, F., Kohlwein, S.D., McMahon, H.T., et al. (2010). Dissecting BAR domain function in the yeast Amphiphysins Rvs161 and Rvs167 during endocytosis. Mol Biol Cell 21, 3054-3069. doi:10.1091/mbc.E10-03-0181.
81. Zhao, H., Michelot, A., Koskela, E.V., Tkach, V., Stamou, D., Drubin, D.G., and Lappalainen, P. (2013). Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep 4, 1213-1223. doi:10.1016/j.celrep.2013.08.024.