The yeast actin cytoskeleton and its function in endocytosis

Fungal Biology Reviews

Volumn 24, Issue 1-2, 2010, Pages 37-46

  Aghamohammadzadeh, Soheil ^a   Ayscough, Kathryn R ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Actin binding proteins; Cytoskeleton; Endocytosis; Saccharomyces cerevisiae; Yeast

Indexed keywords

SACCHAROMYCES CEREVISIAE;

EID: 77957787882     PISSN: 17494613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fbr.2010.01.003     Document Type: Review

References (86)

1. Adams A.E.M., Botstein D., Drubin D.G. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature 1991, 354:404-408.
2. Adams A.E.M., Pringle J.R. Relationship to actin and tubulin distribution to bud growth in wild type and morphogenetic mutant Saccharomyces cerevisiae. Journal of Cell Biology 1984, 98:934-945.
3. Aghamohammadzadeh S., Ayscough K.R. Differential requirements for actin during yeast and mammalian endocytosis. Nature Cell Biology 2009, 11:1039-1042.
4. Amann K.J., Pollard T.D. The Arp2/3 complex nucleates actin filament branches from the sides of pre-existing filaments. Nature Cell Biology 2001, 3:306-310.
5. Ayscough K.R. Endocytosis and the development of cell polarity in yeast require a dynamic F-actin cytoskeleton. Current Biology 2000, 10:1587-1590.
6. Ayscough K.R., Stryker J., Pokala N., Sanders M., Crews P., Drubin D.G. 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. Journal of Cell Biology 1997, 137:399-416.
7. Baggett J.J., D'Aquino K.E., Wendland B. The Sla2p talin domain plays a role in endocytosis in Saccharomyces cerevisiae. Genetics 2003, 165:1661-1674.
8. Balcer H.I., Goodman A.L., Rodal A.A., Smith E., Kugler J., Heuser J.E., Goode B.L. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1. Current Biology 2003, 13:2159-2169.
9. Balguerie A., Sivadon P., Bonneu M., Aigle M. Rvs167p, the budding yeast homolog of amphiphysin, colocalizes with actin patches. Journal of Cell Science 1999, 112:2529-2537.
10. Banuett F., Herskowitz I. Bud morphogenesis and the actin and microtubule cytoskeletons during budding in the corn smut fungus, Ustilago maydis. Fungal Genetics and Biology 2002, 37:149-170.
11. Benedetti H., Raths S., Crausaz F., Riezman H. The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Molecular Biology of the Cell 1994, 5:1023-1037.
12. Bertling E., Quintero-Monzon O., Mattila P.K., Goode B.L., Lappalainen P. Mechanism and biological role of profilin-Srv2/CAP interaction. Journal of Cell Science 2007, 120:1225-1234.
13. Chesarone M.A., Goode B.L. Actin nucleation and elongation factors: mechanisms and interplay. Current Opinion in Cell Biology 2009, 21:28-37.
14. Colwill K., Field D., Moore L., Friesen J., Andrews B. In vivo analysis of the domains of yeast Rvs167p suggests Rvs167p function is mediated through multiple protein interactions. Genetics 1999, 152:881-893.
15. Crouzet M., Urdaci M., Dulau L., Aigle M. Yeast mutant affected for viability upon nutrient starvation - characterization and cloning of the Rvs161 gene. Yeast 1991, 7:727-743.
16. D'Agostino J.L., Goode B.L. Dissection of Arp2/3 complex actin nucleation mechanism and distinct roles for its nucleation-promoting factors in Saccharomyces cerevisiae. Genetics 2005, 171:35-47.
17. Daugherty K.M., Goode B.L. Functional surfaces on the p35/ARPC2 subunit of Arp2/3 complex required for cell growth, actin nucleation, and endocytosis. Journal of Biological Chemistry 2008, 283:16950-16959.
18. Doyle T., Botstein D. Movement of yeast cortical actin cytoskeleton visualized in vivo. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:3886-3891.
19. Drees B., Brown C., Barrell B.G., Bretscher A. Tropomyosin is essential in yeast, yet the Tpm1 and Tpm2 products perform distinct functions. Journal of Cell Biology 1995, 128:383-392.
20. Duncan M.C., Cope M., Goode B.L., Wendland B., Drubin D.G. Yeast Eps15-like endocytic protein, Pan1p, activates the Arp2/3 complex. Nature Cell Biology 2001, 3:687-690.
21. Evangelista M., Klebl B.M., Tong A.H.Y., Webb B.A., Leeuw T., Leberer E., Whiteway M., Thomas D.Y., Boone C. A role for myosin-I in actin assembly through interactions with Vrp1p, Bee1p, and the Arp2/3 complex. Journal of Cell Biology 2000, 148:353-362.
22. Evangelista M., Pruyne D., Amberg D.C., Boone C., Bretscher A. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nature Cell Biology 2002, 4:32-41.
23. Fazi B., Cope M., Douangamath A., Ferracuti S., Schirwitz K., Zucconi A., Drubin D.G., Wilmanns M., Cesareni G., Castagnoli L. Unusual binding properties of the SH3 domain of the yeast actin-binding protein Abp1 - structural and functional analysis. Journal of Biological Chemistry 2002, 277:5290-5298.
24. Friesen H., Humphries C., Ho Y., Schub O., Colwill K., Andrews B. Characterization of the yeast amphiphysins Rvs161p and Rvs167p reveals roles for the Rvs heterodimer in vivo. Molecular Biology of the Cell 2006, 17:1306-1321.
25. Galletta B.J., Chuang D.Y., Cooper J.A. Distinct roles for Arp2/3 regulators in actin assembly and endocytosis. PLoS Biology 2008, 6:72-85.
26. Gandhi M., Achard V., Blanchoin L., Goode B.L. Coronin switches roles in actin disassembly depending on the nucleotide state of actin. Molecular Cell 2009, 34:364-374.
27. Geli M.I., Lombardi R., Schmelzl B., Riezman H. An intact SH3 domain is required for myosin I-induced actin polymerization. EMBO Journal 2000, 19:4281-4291.
28. Geli M.I., Riezman H. Role of type I myosins in receptor-mediated endocytosis in yeast. Science 1996, 272:533-535.
29. Gheorghe D.M., Aghamohammadzadeh S., Rooij L., Allwood E.G., Winder S.J., Ayscough K.R. Interactions between the yeast SM22 homologue Scp1 and actin demonstrate the importance of actin bundling in endocytosis. Journal of Biological Chemistry 2008, 283:15037-15046.
30. Goode B.L., Drubin D.G., Lappalainen P. Regulation of the cortical actin cytoskeleton in budding yeast by twinfilin, a ubiquitous actin monomer-sequestering protein. Journal of Cell Biology 1998, 142:723-733.
31. Gourlay C.W., Ayscough K.R. The actin cytoskeleton: a key regulator of apoptosis and ageing?. Nature Reviews Molecular Cell Biology 2005, 6:583-589.
32. Gourlay C.W., Ayscough K.R. Actin-induced hyperactivation of the Ras signaling pathway leads to apoptosis in Saccharomyces cerevisiae. Molecular and Cellular Biology 2006, 26:6487-6501.
33. Haarer B.K., Lillie S.H., Adams A.E.M., Magdolen V., Bandlow W., Brown S.S. Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells. Journal of Cell Biology 1990, 110:105-114.
34. Huckaba T.M., Gay A.C., Pantalena L.F., Yang H.C., Pon L.A. Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae. Journal of Cell Biology 2004, 167:519-530.
35. Idrissi F.Z., Grotsch H., Fernandez-Golbano I.M., Presciatto-Baschong C., Riezman H., Geli M.I. Distinct acto/myosin-I structures associate with endocytic profiles at the plasma membrane. Journal of Cell Biology 2008, 180:1219-1232.
36. Imamura H., Tanaka K., Hihara T., Umikawa M., Kamei T., Takahashi K., Sasaki T., Takai Y. Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO Journal 1997, 16:2745-2755.
37. Johnston G.C., Prendergast J.A., Singer R.A. The Saccharomyces cerevisiae Myo2 gene encodes an essential myosin for vectorial transport of vesicles. Journal of Cell Biology 1991, 113:539-551.
38. Jonsdottir G.A., Li R. Dynamics of yeast myosin I: evidence for a possible role in scission of endocytic vesicles. Current Biology 2004, 14:1604-1609.
39. Kaksonen M., Sun Y., Drubin D.G. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 2003, 115:475-487.
40. Kaksonen M., Toret C.P., Drubin D.G. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 2005, 123:305-320.
41. Kim K., Galletta B.J., Schmidt K.O., Chang F.S., Blumer K.J., Cooper J.A. Actin-based motility during endocytosis in budding yeast. Molecular Biology of the Cell 2006, 17:1354-1363.
42. Kübler E., Riezman H. Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO Journal 1993, 12:2855-2862.
43. Lappalainen P., Drubin D.G. Cofilin promotes rapid actin filament turnover in vivo. Nature 1997, 388:78-82.
44. Lappalainen P., Fedorov E.V., Fedorov A.A., Almo S.C., Drubin D.G. Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis. EMBO Journal 1997, 16:5520-5530.
45. Liu H., Bretscher A. Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell 1989, 57:233-242.
46. Machesky L.M., Atkinson S.J., Ampe C., Vandekerckhove J., Pollard T.D. Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity-chromatography on profilin-agarose. Journal of Cell Biology 1994, 127:107-115.
47. Madania A., Dumoulin P., Grava S., Kitamoto H., Scharer-Brodbeck C., Soulard A., Moreau V., Winsor B. The Saccharomyces cerevisiae homologue of human Wiskott-Aldrich syndrome protein Las17p interacts with the Arp2/3 complex. Molecular Biology of the Cell 1999, 10:3521-3538.
48. Marks J., Hyams J.S. Localization of F-actin through the cell-division cycle of Schizosaccharomyces pombe. European Journal of Cell Biology 1985, 39:27-32.
49. Moon A.L., Janmey P.A., Louie A., Drubin D.G. Cofilin is an essential component of the yeast cortical actin cytoskeleton. Journal of Cell Biology 1993, 120:421-435.
50. Moseley J.B., Goode B.L. Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6. Journal of Biological Chemistry 2005, 280:28023-28033.
51. Munn A.L., Riezman H. Endocytosis is required for the growth of vacuolar H+-ATPase-defective yeast - identification of six new end genes. Journal of Cell Biology 1994, 127:373-386.
52. Munn A.L., Stevenson B.J., Geli M.I., Riezman H. End5, end6, and end7 - mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Molecular Biology of the Cell 1995, 6:1721-1742.
53. Newpher T.M., Smith R.P., Lemmon V., Lemmon S.K. In vivo dynamics of clathrin and its adaptor-dependent recruitment to the actin-based endocytic machinery in yeast. Developmental Cell 2005, 9:87-98.
54. Okada K., Ravi H., Smith E.M., Goode B.L. Aip1 and cofilin promote rapid turnover of yeast actin patches and cables: a coordinated mechanism for severing and capping filaments. Molecular Biology of the Cell 2006, 17:2855-2868.
55. Okreglak V., Drubin D.G. Cofilin recruitment and function during actin-mediated endocytosis dictated by actin nucleotide state. Journal of Cell Biology 2007, 178:1251-1264.
56. Palmgren S., Ojala P.J., Wear M.A., Cooper J.A., Lappalainen P. Interactions with PIP2, ADP-actin monomers, and capping protein regulate the activity and localization of yeast twinfilin. Journal of Cell Biology 2001, 155:251-260.
57. Pavlov D., Muhlrad A., Cooper J., Wear M., Reisler E. Actin filament severing by cofilin. Journal of Molecular Biology 2007, 365:1350-1358.
58. Peter B.J., Kent H.M., Mills I.G., Vallis Y., Butler P.J.G., Evans P.R., McMahon H.T. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 2004, 303:495-499.
59. Pruyne D., Bretscher A. Polarization of cell growth in yeast II. The role of the cortical actin cytoskeleton. Journal of Cell Science 2000, 113:571-585.
60. Pruyne D., Evangelista M., Yang C.S., Bi E.F., Zigmond S., Bretscher A., Boone C. Role of formins in actin assembly: nucleation and barbed-end association. Science 2002, 297:612-615.
61. Pruyne D., Gao L., Bi E.F., Bretscher A. Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Molecular Biology of the Cell 2004, 15:4971-4989.
62. Raths S., Rohrer J., Crausaz F., Riezman H. end3 and end4: two mutants defective in receptor-mediated endocytosis in Saccharomyces cerevisiae. Journal of Cell Biology 1993, 120:55-65.
63. Robertson A.S., Allwood E.G., Smith A.P., Gardiner F.C., Costa R., Winder S.J., Ayscough K.R. The WASP homolog Las17 activates the novel actin-regulatory activity of Ysc84 to promote endocytosis in yeast. Molecular Biology of the Cell 2009.
64. Rodal A.A., Manning A.L., Goode B.L., Drubin D.G. Negative regulation of yeast WASp by two SH3 domain-containing proteins. Current Biology 2003, 13:1000-1008.
65. Sagot I., Rodal A.A., Moseley J., Goode B.L., Pellman D. An actin nucleation mechanism mediated by Bni1 and profilin. Nature Cell Biology 2002, 4:626-631.
66. Smythe E., Ayscough K.R. The Ark1/Prk1 family of protein kinases - regulators of endocytosis and the actin cytoskeleton. EMBO Reports 2003, 4:246-251.
67. Soulard A., Friant S., Fitterer C., Orange C., Kaneva G., Mirey G., Winsor B. The WASP/Las17p-interacting protein Bzz1p functions with Myo5p in an early stage of endocytosis. Protoplasma 2005, 226:89-101.
68. Sun Y.D., Martin A.C., Drubin D.G. Endocytic internalization in budding yeast requires coordinated actin nucleation and myosin motor activity. Developmental Cell 2006, 11:33-46.
69. Svitkina T.M., Borisy G.G. Arp2/3 complex and actin depolymerizing factor cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. Journal of Cell Biology 1999, 145:1009-1026.
70. Takizawa P.A., Sil A., Swedlow J.R., Herskowitz I., Vale R.D. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 1997, 389:90-93.
71. Thanabalu T., Rajmohan R., Meng L., Ren G., Vajjhala P.R., Munn A.L. Verprolin function in endocytosis and actin organization - roles of the Las17p (yeast WASP)-binding domain and a novel C-terminal actin-binding domain. FEBS Journal 2007, 274:4103-4125.
72. Toshima J., Toshima J.Y., Martin A.C., Drubin D.G. Phosphoregulation of Arp2/3-dependent actin assembly during receptor-mediated endocytosis. Nature Cell Biology 2005, 7:246-254.
73. Toshima J.Y., Toshima J., Kaksonen M., Martin A.C., King D.S., Drubin D.G. Spatial dynamics of receptor-mediated endocytic trafficking in budding yeast revealed by using fluorescent alpha-factor derivatives. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:5793-5798.
74. Waddle J., Karpova T., Waterson R., Cooper J. Movement of cortical actin patches in yeast. Journal of Cell Biology 1996, 132:861-870.
75. Warren D.T., Andrews P.D., Gourlay C.G., Ayscough K.R. Sla1p couples the yeast endocytic machinery to proteins regulating actin dynamics. Journal of Cell Science 2002, 115.
76. Watts F.Z., Shiels G., Orr E. The yeast Myo1 gene encoding a myosin-like protein required for cell-division. EMBO Journal 1987, 6:3499-3505.
77. Wendland B., McCaffery J.M., Xiao Q., Emr S.D. A novel fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian eps15. Journal of Cell Biology 1996, 135:1485-1500.
78. Winder S.J., Ayscough K.R. Actin-binding proteins. Journal of Cell Science 2005, 118:651-654.
79. Winder S.J., Jess T., Ayscough K.R. SCP1 encodes an actin-bundling protein in yeast. Biochemical Journal 2003, 375:287-295.
80. Winter D., Lechler T., Li R. Activation of the yeast Arp2/3 complex by Bee1p, a WASP-family protein. Current Biology 1999, 9:501-504.
81. Winter D., Podtelejnikov A.V., Mann M., Li R. The complex containing actin-related proteins Arp2 and Arp3 is required for the motility and integrity of yeast actin patches. Current Biology 1997, 7:519-529.
82. Wolven A.K., Belmont L.D., Mahoney N.M., Almo S.C., Drubin D.G. In vivo importance of actin nucleotide exchange catalyzed by profilin. Journal of Cell Biology 2000, 150:895-903.
83. Xiang X., Plamann M. Cytoskeleton and motor proteins in filamentous fungi. Current Opinion in Microbiology 2003, 6:628-633.
84. Yang S., Cope M., Drubin D.G. Sla2p is associated with the yeast cortical actin cytoskeleton via redundant localization signals. Molecular Biology of the Cell 1999, 10:2265-2283.
85. Yao X.Y., Rubenstein P.A. F-actin-like ATPase activity in a polymerization-defective mutant yeast actin (V266G/L267G). Journal of Biological Chemistry 2001, 276:25598-25604.
86. Young M.E., Cooper J.A., Bridgman P.C. Yeast actin patches are networks of branched actin filaments. Journal of Cell Biology 2004, 166:629-635.