Coupling Between Clathrin-dependent Endocytic Budding and F-BAR-dependent Tubulation in a Cell-free System

Overview

Journal Nat Cell Biol

Specialty Cell Biology

Date 2010 Aug 24

PMID 20729836

Citations 79

Authors

Min Wu

Bo Huang

Morven Graham

Andrea Raimondi

John E Heuser

Xiaowei Zhuang

Pietro De Camilli

Affiliations

Soon will be listed here.

Abstract

Cell-free reconstitution of membrane traffic reactions and the morphological characterization of membrane intermediates that accumulate under these conditions have helped to elucidate the physical and molecular mechanisms involved in membrane transport. To gain a better understanding of endocytosis, we have reconstituted vesicle budding and fission from isolated plasma membrane sheets and imaged these events. Electron and fluorescence microscopy, including subdiffraction-limit imaging by stochastic optical reconstruction microscopy (STORM), revealed F-BAR (FBP17) domain coated tubules nucleated by clathrin-coated buds when fission was blocked by GTPgammaS. Triggering fission by replacing GTPgammaS with GTP led not only to separation of clathrin-coated buds, but also to vesicle formation by fragmentation of the tubules. These results suggest a functional link between FBP17-dependent membrane tubulation and clathrin-dependent budding. They also show that clathrin spatially directs plasma membrane invaginations that lead to the generation of endocytic vesicles larger than those enclosed by the coat.

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References

Itoh T, Erdmann K, Roux A, Habermann B, Werner H, De Camilli P . Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell. 2005; 9(6):791-804. DOI: 10.1016/j.devcel.2005.11.005. View

Giuliani C, Troglio F, Bai Z, Patel F, Zucconi A, Malabarba M . Requirements for F-BAR proteins TOCA-1 and TOCA-2 in actin dynamics and membrane trafficking during Caenorhabditis elegans oocyte growth and embryonic epidermal morphogenesis. PLoS Genet. 2009; 5(10):e1000675. PMC: 2744924. DOI: 10.1371/journal.pgen.1000675. View

Heuser J . Effects of cytoplasmic acidification on clathrin lattice morphology. J Cell Biol. 1989; 108(2):401-11. PMC: 2115436. DOI: 10.1083/jcb.108.2.401. View

Zimmerberg J, Kozlov M . How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol. 2005; 7(1):9-19. DOI: 10.1038/nrm1784. View

Huang B, Jones S, Brandenburg B, Zhuang X . Whole-cell 3D STORM reveals interactions between cellular structures with nanometer-scale resolution. Nat Methods. 2008; 5(12):1047-52. PMC: 2596623. DOI: 10.1038/nmeth.1274. View

Henne W, Boucrot E, Meinecke M, Evergren E, Vallis Y, Mittal R . FCHo proteins are nucleators of clathrin-mediated endocytosis. Science. 2010; 328(5983):1281-4. PMC: 2883440. DOI: 10.1126/science.1188462. View

Shimada A, Niwa H, Tsujita K, Suetsugu S, Nitta K, Hanawa-Suetsugu K . Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell. 2007; 129(4):761-72. DOI: 10.1016/j.cell.2007.03.040. View

Butler M, David C, Ochoa G, Freyberg Z, Daniell L, Grabs D . Amphiphysin II (SH3P9; BIN1), a member of the amphiphysin/Rvs family, is concentrated in the cortical cytomatrix of axon initial segments and nodes of ranvier in brain and around T tubules in skeletal muscle. J Cell Biol. 1997; 137(6):1355-67. PMC: 2132527. DOI: 10.1083/jcb.137.6.1355. View

Rust M, Bates M, Zhuang X . Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods. 2006; 3(10):793-5. PMC: 2700296. DOI: 10.1038/nmeth929. View

10.

Smythe E, Pypaert M, Lucocq J, Warren G . Formation of coated vesicles from coated pits in broken A431 cells. J Cell Biol. 1989; 108(3):843-53. PMC: 2115393. DOI: 10.1083/jcb.108.3.843. View

11.

Farsad K, Ringstad N, Takei K, Floyd S, Rose K, De Camilli P . Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol. 2001; 155(2):193-200. PMC: 2198845. DOI: 10.1083/jcb.200107075. View

12.

Henry Ho H, Rohatgi R, Lebensohn A, Ma L, Li J, Gygi S . Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell. 2004; 118(2):203-16. DOI: 10.1016/j.cell.2004.06.027. View

13.

Soulet F, Yarar D, Leonard M, Schmid S . SNX9 regulates dynamin assembly and is required for efficient clathrin-mediated endocytosis. Mol Biol Cell. 2005; 16(4):2058-67. PMC: 1073683. DOI: 10.1091/mbc.e04-11-1016. View

14.

Moore M, Mahaffey D, Brodsky F, Anderson R . Assembly of clathrin-coated pits onto purified plasma membranes. Science. 1987; 236(4801):558-63. DOI: 10.1126/science.2883727. View

15.

Schmid S, Smythe E . Stage-specific assays for coated pit formation and coated vesicle budding in vitro. J Cell Biol. 1991; 114(5):869-80. PMC: 2289107. DOI: 10.1083/jcb.114.5.869. View

16.

Takano K, Takano K, Toyooka K, Suetsugu S . EFC/F-BAR proteins and the N-WASP-WIP complex induce membrane curvature-dependent actin polymerization. EMBO J. 2008; 27(21):2817-28. PMC: 2580791. DOI: 10.1038/emboj.2008.216. View

17.

Merrifield C, Perrais D, Zenisek D . Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell. 2005; 121(4):593-606. DOI: 10.1016/j.cell.2005.03.015. View

18.

Heuser J . The production of 'cell cortices' for light and electron microscopy. Traffic. 2001; 1(7):545-52. DOI: 10.1034/j.1600-0854.2000.010704.x. View

19.

Ringstad N, Gad H, Low P, Di Paolo G, Brodin L, Shupliakov O . Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron. 2000; 24(1):143-54. DOI: 10.1016/s0896-6273(00)80828-4. View

20.

Hinshaw J . Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol. 2000; 16:483-519. PMC: 4781412. DOI: 10.1146/annurev.cellbio.16.1.483. View