A role for the dynamin-like protein Vps1 during endocytosis in yeast

Journal of Cell Science

Volumn 123, Issue 20, 2010, Pages 3496-3506

  Smaczynska de Rooij, Iwona I ^a   Allwood, Ellen G ^a   Aghamohammadzadeh, Soheil ^a   Hettema, Ewald H ^a   Goldberg, Martin W ^b   Ayscough, Kathryn R ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

Author keywords

Amphiphysin; Dynamin; Endocytosis; Rvs167; Saccharomyces cerevisiae

Indexed keywords

DYNAMIN; DYNAMIN I; MUTANT PROTEIN; PROTEIN VP1;

ARTICLE; CARBOXY TERMINAL SEQUENCE; ELECTRON MICROSCOPY; ENDOCYTOSIS; FUNGAL GENE; MAMMAL CELL; MEMBRANE FUSION; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN LOCALIZATION; VPS1 GENE; YEAST;

DYNAMINS; ENDOCYTOSIS; GTP-BINDING PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; NERVE TISSUE PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VESICULAR TRANSPORT PROTEINS;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 77957867271     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.070508     Document Type: Article

References (56)

1. Ayscough, K. R., Stryker, J., Pokala, N., Sanders, M., Crews, P. and Drubin, D. G. (1997). High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J. Cell Biol. 137, 399-416.
2. Burston, H. E., Maldonado-Baez, L., Davey, M., Montpetit, B., Schluter, C., Wendland, B. and Conibear, E. (2009). Regulators of yeast endocytosis identified by systematic quantitative analysis. J. Cell Biol. 185, 1097-1110.
3. Cao, H., Orth, J. D., Chen, J., Weller, S. G., Heuser, J. E. and McNiven, M. A. (2003). Cortactin is a component of clathrin-coated pits and participates in receptor-mediated endocytosis. Mol. Cell. Biol. 23, 2162-2170.
4. Cao, H., Weller, S., Orth, J. D., Chen, J., Huang, B., Chen, J. L., Stamnes, M. and McNiven, M. A. (2005). Actin and Arf1-dependent recruitment of a cortactin-dynamin complex to the Golgi regulates post-Golgi transport. Nat. Cell Biol. 7, 483-492.
5. Cerveny, K. L., Tamura, Y., Zhang, Z., Jensen, R. E. and Sesaki, H. (2007). Regulation of mitochondrial fusion and division. Trends Cell Biol. 17, 563-569.
6. Chen, M. S., Obar, R. A., Schroeder, C. C., Austin, T. W., Poodry, C. A., Wadsworth, S. C. and Vallee, R. B. (1991). Multiple forms of dynamin are encoded by shibire, a drosophila gene involved in endocytosis. Nature 351, 583-586.
7. Damke, H., Baba, T., Warnock, D. E. and Schmid, S. L. (1994). Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934.
8. Damke, H., Baba, T., Vanderbliek, A. M. and Schmid, S. L. (1995). Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J. Cell Biol. 131, 69-80.
9. Dawson, J. C., Legg, J. A. and Machesky, L. M. (2006). Bar domain proteins: a role in tubulation, scission and actin assembly in clathrin-mediated endocytosis. Trends Cell Biol. 16, 493-498.
10. Doyle, T. and Botstein, D. (1996). Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc. Natl Acad. Sci. USA 93, 3886-3891. (Pubitemid 26144217)
11. Ferguson, S., Raimondi, A., Paradise, S., Shen, H. Y., Mesaki, K., Ferguson, A., Destaing, O., Ko, G., Takasaki, J., Cremona, O. et al. (2009). Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev. Cell 17, 811-822.
12. Gammie, A. E., Kurihara, L. J., Vallee, R. B. and Rose, M. D. (1995). Dnm1, a dynamin-related gene, participates in endosomal trafficking in yeast. J. Cell Biol. 130, 553-566.
13. Geli, M. I. and Riezman, H. (1998). Endocytic internalization in yeast and animal cells: similar and different. J. Cell Sci. 111, 1031-1037.
14. Gheorghe, D. M., Aghamohammadzadeh, S., Rooij, L., Allwood, E. G., Winder, S. J. and Ayscough, K. R. (2008). Interactions between the yeast SM22 homologue Scp1 and actin demonstrate the importance of actin bundling in endocytosis. J. Biol. Chem. 283, 15037-15046.
15. Herskovits, J. S., Burgess, C. C., Obar, R. A. and Vallee, R. B. (1993). Effects of mutant rat dynamin on endocytosis. J. Cell Biol. 122, 565-578.
16. Hinshaw, J. E. and Schmid, S. L. (1995). Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374, 190-192.
17. Hoepfner, D., van den Berg, M., Philippsen, P., Tabak, H. F. and Hettema, E. H. (2001). A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 155, 979-990.
18. Huang, K. M., D'Hondt, K., Riezman, H. and Lemmon, S. K. (1999). Clathrin functions in the absence of heterotetrameric adaptors and AP180-related proteins in yeast. EMBO J. 18, 3897-3908.
19. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S. and O'Shea, E. K. (2003). Global analysis of protein localization in budding yeast. Nature 425, 686-691.
20. Itoh, T., Erdmann, K. S., Roux, A., Habermann, B., Werner, H. and De Camilli, P. (2005). Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 9, 791-804. (Pubitemid 41724107)
21. 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.
22. Kaiser, C., Michaelis, S. and Mitchell, A. (1994). Methods in Yeast Genetics: a Laboratory Course Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
23. 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.
24. 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.
25. Koenig, J. H. and Ikeda, K. (1989). Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9, 3844-3860.
26. Kruchten, A. E. and McNiven, M. A. (2006). Dynamin as a mover and pincher during cell migration and invasion. J. Cell Sci. 119, 1683-1690.
27. Kuravi, K., Nagotu, S., Krikken, A. M., Sjollema, K., Deckers, M., Erdmann, R., Veenhuis, M. and van der Klei, I. J. (2006). Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae. J. Cell Sci. 119, 3994-4001. (Pubitemid 44650872)
28. Liu, J., Sun, Y. D., Drubin, D. G. and Oster, G. F. (2009). The mechanochemistry of endocytosis. PLoS Biol. 7, e1000204.
29. Longtine, M. S., McKenzie, A., Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
30. Maldonado-Baez, L., Dores, M. R., Perkins, E. M., Drivas, T. G., Hicke, L. and Wendland, B. (2008). Interaction between epsin/Yap180 adaptors and the scaffolds Ede1/Pan1 is required for endocytosis. Mol. Biol. Cell 19, 2936-2948.
31. Marks, B., Stowell, M. H. B., Vallis, Y., Mills, I. G., Gibson, A., Hopkins, C. R. and McMahon, H. T. (2001). GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231-235.
32. Merrifield, C. J., Feldman, M. E., Wan, L. and Almers, W. (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat. Cell Biol. 4, 691-698. (Pubitemid 34993705)
33. Morton, W. M., Ayscough, K. R. and McLaughlin, P. J. (2000). Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat. Cell Biol. 2, 376-378.
34. Motley, A. M. and Hettema, E. H. (2007). Yeast peroxisomes multiply by growth and division. J. Cell Biol. 178, 399-410.
35. Nannapaneni, S., Wang, D., Jain, S., Schroeder, B., Highfill, C., Reustle, L., Pittsley, D., Maysent, A., Moulder, S., McDowell, R. et al. (2010). The yeast dynamin-like protein Vps1:vps1 mutations perturb the internalization and the motility of endocytic vesicles and endosomes via disorganization of the actin cytoskeleton. Eur. J. Cell Biol. 89, 499-508.
36. Narayanan, R., Leonard, M., Song, B. D., Schmid, S. L. and Ramaswami, M. (2005). An internal GAP domain negatively regulates presynaptic dynamin in vivo: a two-step model for dynamin function. J. Cell Biol. 169, 117-126. (Pubitemid 40562919)
37. Nothwehr, S. F., Conibear, E. and Stevens, T. H. (1995). Golgi and vacuolar membrane-proteins reach the vacuole in Vps1 mutant yeast cells via the plasma membrane. J. Cell Biol. 129, 35-46.
38. Ochoa, G. C., Slepnev, V. I., Neff, L., Ringstad, N., Takei, K., Daniell, L., Kim, W., Cao, H., McNiven, M., Baron, R. et al. (2000). A functional link between dynamin and the actin cytoskeleton at podosomes. J. Cell Biol. 150, 377-389.
39. Peters, C., Baars, T. L., Buhler, S. and Mayer, A. (2004). Mutual control of membrane fission and fusion proteins. Cell 119, 667-678. (Pubitemid 39535754)
40. Raymond, C. K., Howald-Stevenson, I., Vater, C. A. and Stevens, T. H. (1992). Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3, 1389-1402.
41. Robertson, A. S., Smythe, E. and Ayscough, K. R. (2009). Functions of actin in endocytosis. Cell. Mol. Life Sci. 66, 2049-2065.
42. Rothlisberger, S., Jourdain, I., Johnson, C., Takegawa, K. and Hyams, J. S. (2009). The dynamin-related protein Vps1 regulates vacuole fission, fusion and tubulation in the fission yeast, Schizosaccharomyces pombe. Fungal Genet. Biol. 46, 927-935.
43. Sever, S., Muhlberg, A. B. and Schmid, S. L. (1999). Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398, 481-486.
44. Shin, H. W., Takatsu, H., Mukai, H., Munekata, E., Murakami, K. and Nakayama, K. (1999). Intermolecular and interdomain interactions of a dynamin-related GTP-binding protein, Dnm1p/Vps1p-like protein. J. Biol. Chem. 274, 2780-2785. (Pubitemid 29075359)
45. Shpetner, H. S. and Vallee, R. B. (1989). Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell 59, 421-432.
46. Song, B. D. and Schmid, S. L. (2003). A molecular motor or a regulator? Dynamin's in a class of its own. Biochemistry 42, 1369-1376.
47. Song, B. D., Leonard, M. and Schmid, S. L. (2004a). Dynamin GTPase domain mutants that differentially affect GTP binding, GTP hydrolysis, and clathrin-mediated endocytosis. J. Biol. Chem. 279, 40431-40436.
48. Song, B. D., Yarar, D. and Schmid, S. L. (2004b). An assembly-incompetent mutant establishes a requirement for dynamin self-assembly in clathrin-mediated endocytosis in vivo. Mol. Biol. Cell 15, 2243-2252.
49. Stamenova, S. D., Dunn, R., Adler, A. S. and Hicke, L. (2004). The Rsp5 ubiquitin ligase binds to and ubiquitinates members of the yeast CIN85-endophilin complex, Sla1-Rvs167. J. Biol. Chem. 279, 16017-16025.
50. Tong, A. H. Y., Evangelista, M., Parsons, A. B., Xu, H., Bader, G. D., Page, N., Robinson, M., Raghibizadeh, S., Hogue, C. W. V., Bussey, H. et al. (2001). Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368.
51. Toshima, J. Y., Nakanishi, J.-I., Mizuno, K., Toshima, J. and Drubin, D. G. (2009). Requirements for recruitment of a G protein-coupled receptor to clathrin-coated pits in budding yeast. Mol. Biol. Cell 20, 5039-5050.
52. Van Der Bliek, A. M. and Meyerowitz, E. M. (1991). Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351, 411-414.
53. Vater, C. A., Raymond, C. K., Ekena, K., Howaldstevenson, I. and Stevens, T. H. (1992). The Vps1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevisiae, is a gtpase with 2 functionally separable domains. J. Cell Biol. 119, 773-786.
54. Yamada, H., Padilla-Parra, S., Park, S. J., Itoh, T., Chaineau, M., Monaldi, I., Cremona, O., Benfenati, F., De Camilli, P., Coppey-Moisan, M. et al. (2009). Dynamic interaction of amphiphysin with N-WASP regulates actin assembly. J. Biol. Chem. 284, 34244-34256.
55. Yoon, Y., Pitts, K. R. and McNiven, M. A. (2001). Mammalian dynamin-like protein DLP1 tubulates membranes. Mol. Biol. Cell 12, 2894-2905.
56. Yu, X. W. and Cai, M. J. (2004). The yeast dynamin-related GTPase Vps1p functions in the organization of the actin cytoskeleton via interaction with Sla1p. J. Cell Sci. 117, 3839-3853.