Cell-cycle regulation of formin-mediated actin cable assembly

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 47, 2013, Pages

  Miao, Yansong ^a   Wong, Catherine C L ^b,e   Mennella, Vito ^c,d   Michelot, Alphee ^a,f   Agard, David A ^c,d   Holt, Liam J ^a   Yates, John R ^b   Drubin, David G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^f UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN CAPPING PROTEIN; COFILIN; CYCLIN DEPENDENT KINASE 1; METHENAMINE; MICROSPHERE; REGULATOR PROTEIN; TROPOMYOSIN;

ACTIN FILAMENT; ARTICLE; CELL CYCLE REGULATION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN PURIFICATION; YEAST CELL;

ACTIN NUCLEATION; CDK1; THREE-DIMENSIONAL STRUCTURED-ILLUMINATION MICROSCOPY;

ACTIN CYTOSKELETON; BLOTTING, WESTERN; CDC2 PROTEIN KINASE; CELL CYCLE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MASS SPECTROMETRY; MICROFILAMENT PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MICROSPHERES; POLYMERIZATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84888104697     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1314000110     Document Type: Article

References (117)

1. Michelot A, Drubin DG (2011) Building distinct actin filament networks in a common cytoplasm. Curr Biol 21(14-R560-R569.
2. Kaksonen M, Toret CP, Drubin DG (2006) Harnessing actin dynamics for clathrinmediated endocytosis. Nat Rev Mol Cell Biol 7(6-404-414.
3. Pollard TD (2007) Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct 36:451-477.
4. Goley ED, Welch MD (2006) The ARP2/3 complex: An actin nucleator comes of age. Nat Rev Mol Cell Biol 7(10-713-726.
5. Pruyne D, et al. (2002) Role of formins in actin assembly: Nucleation and barbed-end association. Science 297(5581-612-615.
6. Evangelista M, Pruyne D, Amberg DC, Boone C, Bretscher A (2002) Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat Cell Biol 4(1-32-41.
7. Sagot I, Klee SK, Pellman D (2002) Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat Cell Biol 4(1-42-50.
8. Kovar DR, Harris ES, Mahaffy R, Higgs HN, Pollard TD (2006) Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 124(2-423-435.
9. Wu JQ, Pollard TD (2005) Counting cytokinesis proteins globally and locally in fission yeast. Science 310(5746-310-314.
10. Wu JQ, Kuhn JR, Kovar DR, Pollard TD (2003) Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev Cell 5(5-723-734.
11. Evangelista M, et al. (1997) Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276(5309-118-122.
12. Yonetani A, Chang F (2010) Regulation of cytokinesis by the formin cdc12p. Curr Biol 20(6-561-566.
13. Basu R, Chang F (2007) Shaping the actin cytoskeleton using microtubule tips. Curr Opin Cell Biol 19(1-88-94.
14. Pelham RJ, Chang F (2002) Actin dynamics in the contractile ring during cytokinesis in fission yeast. Nature 419(6902-82-86.
15. Mooren OL, Galletta BJ, Cooper JA (2012) Roles for actin assembly in endocytosis. Annu Rev Biochem 81:661-686.
16. Akin O, Mullins RD (2008) Capping protein increases the rate of actin-based motility by promoting filament nucleation by the Arp2/3 complex. Cell 133(5-841-851.
17. Loisel TP, Boujemaa R, Pantaloni D, Carlier MF (1999) Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401(6753-613-616.
18. Upadhyaya A, van Oudenaarden A (2003) Biomimetic systems for studying actinbased motility. Curr Biol 13(18-R734-R744.
19. Wiesner S, et al. (2003) A biomimetic motility assay provides insight into the mechanism of actin-based motility. J Cell Biol 160(3-387-398.
20. Cameron LA, Footer MJ, van Oudenaarden A, Theriot JA (1999) Motility of ActA protein-coated microspheres driven by actin polymerization. Proc Natl Acad Sci USA 96(9-4908-4913.
21. Cameron LA, Robbins JR, Footer MJ, Theriot JA (2004) Biophysical parameters influence actin-based movement, trajectory, and initiation in a cell-free system. Mol Biol Cell 15(5-2312-2323.
22. Ho HY, et al. (2004) Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 118(2-203-216.
23. Ma L, Cantley LC, Janmey PA, Kirschner MW (1998) Corequirement of specific phosphoinositides and small GTP-binding protein Cdc42 in inducing actin assembly in Xenopus egg extracts. J Cell Biol 140(5-1125-1136.
24. Michelot A, et al. (2010) Reconstitution and protein composition analysis of endocytic actin patches. Curr Biol 20(21-1890-1899.
25. Yarar D, To W, Abo A, Welch MD (1999) The Wiskott-Aldrich syndrome protein directs actin-based motility by stimulating actin nucleation with the Arp2/3 complex. Curr Biol 9(10-555-558.
26. Bernheim-Groswasser A, Wiesner S, Golsteyn RM, Carlier MF, Sykes C (2002) The dynamics of actin-based motility depend on surface parameters. Nature 417(6886- 308-311.
27. McGrath JL, et al. (2003) The force-velocity relationship for the actin-based motility of Listeria monocytogenes. Curr Biol 13(4-329-332.
28. Suetsugu S, Miki H, Yamaguchi H, Takenawa T (2001) Requirement of the basic region of N-WASP/WAVE2 for actin-based motility. Biochem Biophys Res Commun 282(3-739-744.
29. Michelot A, et al. (2007) Actin-filament stochastic dynamics mediated by ADF/cofilin. Curr Biol 17(10-825-833.
30. Romero S, et al. (2004) Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119(3-419-429.
31. Alberts AS (2001) Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain. J Biol Chem 276(4-2824-2830.
32. Li F, Higgs HN (2005) Dissecting requirements for auto-inhibition of actin nucleation by the formin, mDia1. J Biol Chem 280(8-6986-6992.
33. Wallar BJ, et al. (2006) The basic region of the diaphanous- autoregulatory domain (DAD) is required for autoregulatory interactions with the diaphanous-related formin inhibitory domain. J Biol Chem 281(7-4300-4307.
34. Gould CJ, et al. (2011) The formin DAD domain plays dual roles in autoinhibition and actin nucleation. Curr Biol 21(5-384-390.
35. Copeland SJ, et al. (2007) The diaphanous inhibitory domain/diaphanous autoregulatory domain interaction is able to mediate heterodimerization between mDia1 and mDia2. J Biol Chem 282(41-30120-30130.
36. Seth A, Otomo C, Rosen MK (2006) Autoinhibition regulates cellular localization and actin assembly activity of the diaphanous-related formins FRLalpha and mDia1. J Cell Biol 174(5-701-713.
37. Lammers M, Rose R, Scrima A, Wittinghofer A (2005) The regulation of mDia1 by autoinhibition and its release by Rho GTP. EMBO J 24(23-4176-4187.
38. Otomo T, Otomo C, Tomchick DR, Machius M, Rosen MK (2005) Structural basis of Rho GTPase-mediated activation of the formin mDia1. Mol Cell 18(3-273-281.
39. Li F, Higgs HN (2003) The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr Biol 13(15-1335-1340.
40. Dong Y, Pruyne D, Bretscher A (2003) Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast. J Cell Biol 161(6-1081-1092.
41. Wang J, Neo SP, Cai M (2009) Regulation of the yeast formin Bni1p by the actinregulating kinase Prk1p. Traffic 10(5-528-535.
42. Pinot M, et al. (2012) Confinement induces actin flow in a meiotic cytoplasm. Proc Natl Acad Sci USA 109(29-11705-11710.
43. Field CM, et al. (2011) Actin behavior in bulk cytoplasm is cell cycle regulated in early vertebrate embryos. J Cell Sci 124(Pt 12-2086-2095.
44. Chew TG, Lorthongpanich C, Ang WX, Knowles BB, Solter D (2012) Symmetric cell division of the mouse zygote requires an actin network. Cytoskeleton, Hoboken 69 (12-1040-1046.
45. Mitsushima M, et al. (2010) Revolving movement of a dynamic cluster of actin filaments during mitosis. J Cell Biol 191(3-453-462.
46. Moseley JB, et al. (2004) A conserved mechanism for Bni1- and mDia1-induced actin assembly and dual regulation of Bni1 by Bud6 and profilin. Mol Biol Cell 15(2- 896-907.
47. Kamasaki T, Arai R, Osumi M, Mabuchi I (2005) Directionality of F-actin cables changes during the fission yeast cell cycle. Nat Cell Biol 7(9-916-917.
48. Bloom J, Cross FR (2007) Multiple levels of cyclin specificity in cell-cycle control. Nat Rev Mol Cell Biol 8(2-149-160.
49. Ho J, Bretscher A (2001) Ras regulates the polarity of the yeast actin cytoskeleton through the stress response pathway. Mol Biol Cell 12(6-1541-1555.
50. Moseley JB, Goode BL (2005) Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6. J Biol Chem 280(30-28023-28033.
51. Huckaba TM, Lipkin T, Pon LA (2006) Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast. J Cell Biol 175(6-957-969.
52. Yang HC, Pon LA (2002) Actin cable dynamics in budding yeast. Proc Natl Acad Sci USA 99(2-751-756.
53. Uhlmann F, Wernic D, Poupart MA, Koonin EV, Nasmyth K (2000) Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103(3- 375-386.
54. Futcher B (1999) Cell cycle synchronization. Methods Cell Sci 21(2-3-79-86.
55. Holt LJ, et al. (2009) Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325(5948-1682-1686.
56. Bishop AC, et al. (2000) A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407(6802-395-401.
57. Ubersax JA, et al. (2003) Targets of the cyclin-dependent kinase Cdk1. Nature 425(6960-859-864.
58. Liu HP, Bretscher A (1989) Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell 57(2-233-242.
59. Buttery SM, Yoshida S, Pellman D (2007) Yeast formins Bni1 and Bnr1 utilize different modes of cortical interaction during the assembly of actin cables. Mol Biol Cell 18(5-1826-1838.
60. Sagot I, Rodal AA, Moseley J, Goode BL, Pellman D (2002) An actin nucleation mechanism mediated by Bni1 and profilin. Nat Cell Biol 4(8-626-631.
61. Drees B, Brown C, Barrell BG, Bretscher A (1995) Tropomyosin is essential in yeast, yet the TPM1 and TPM2 products perform distinct functions. J Cell Biol 128(3-383-392.
62. Goode BL, Eck MJ (2007) Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem 76:593-627.
63. Karpova TS, McNally JG, Moltz SL, Cooper JA (1998) Assembly and function of the actin cytoskeleton of yeast: Relationships between cables and patches. J Cell Biol 142(6-1501-1517.
64. Harris ES, Li F, Higgs HN (2004) The mouse formin, FRLalpha, slows actin filament barbed end elongation, competes with capping protein, accelerates polymerization from monomers, and severs filaments. J Biol Chem 279(19-20076-20087.
65. Kovar DR, Wu JQ, Pollard TD (2005) Profilin-mediated competition between capping protein and formin Cdc12p during cytokinesis in fission yeast. Mol Biol Cell 16(5- 2313-2324.
66. Zigmond SH, et al. (2003) Formin leaky cap allows elongation in the presence of tight capping proteins. Curr Biol 13(20-1820-1823.
67. Okada K, Ravi H, Smith EM, Goode BL (2006) Aip1 and cofilin promote rapid turnover of yeast actin patches and cables: A coordinated mechanism for severing and capping filaments. Mol Biol Cell 17(7-2855-2868.
68. Ayscough KR, et al. (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(2-399-416.
69. Cooper JA, Schafer DA (2000) Control of actin assembly and disassembly at filament ends. Curr Opin Cell Biol 12(1-97-103.
70. Jin H, Amberg DC (2000) The secretory pathway mediates localization of the cell polarity regulator Aip3p/Bud6p. Mol Biol Cell 11(2-647-661.
71. Nishida E, et al. (1987) Cofilin is a component of intranuclear and cytoplasmic actin rods induced in cultured cells. Proc Natl Acad Sci USA 84(15-5262-5266.
72. Nolen BJ, et al. (2009) Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460(7258-1031-1034.
73. Vallen EA, Caviston J, Bi E (2000) Roles of Hof1p, Bni1p, Bnr1p, and myo1p in cytokinesis in Saccharomyces cerevisiae. Mol Biol Cell 11(2-593-611.
74. Gustafsson MG, et al. (2008) Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys J 94(12-4957-4970.
75. Enserink JM, Kolodner RD (2010) An overview of Cdk1-controlled targets and processes. Cell Div 5:11.
76. Yu JH, Crevenna AH, Bettenbühl M, Freisinger T, Wedlich-Söldner R (2011) Cortical actin dynamics driven by formins and myosin V. J Cell Sci 124(Pt 9-1533-1541.
77. Kaksonen M, Toret CP, Drubin DG (2005) A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123(2-305-320.
78. Mallavarapu A, Mitchison T (1999) Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J Cell Biol 146(5-1097-1106.
79. Yang C, et al. (2007) Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol 5(11-e317.
80. Block J, et al. (2008) Filopodia formation induced by active mDia2/Drf3. J Microsc 231(3-506-517.
81. Vassilev LT, et al. (2006) Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc Natl Acad Sci USA 103(28-10660-10665.
82. Skau CT, Kovar DR (2010) Fimbrin and tropomyosin competition regulates endocytosis and cytokinesis kinetics in fission yeast. Curr Biol 20(16-1415-1422.
83. Graziano BR, et al. (2011) Mechanism and cellular function of Bud6 as an actin nucleation- promoting factor. Mol Biol Cell 22(21-4016-4028.
84. Wear MA, Cooper JA (2004) Capping protein: New insights into mechanism and regulation. Trends Biochem Sci 29(8-418-428.
85. Wear MA, Yamashita A, Kim K, Maéda Y, Cooper JA (2003) How capping protein binds the barbed end of the actin filament. Curr Biol 13(17-1531-1537.
86. Adams AE, Botstein D, Drubin DG (1989) A yeast actin-binding protein is encoded by SAC6, a gene found by suppression of an actin mutation. Science 243(4888-231-233.
87. Adams AE, Shen W, Lin CS, Leavitt J, Matsudaira P (1995) Isoform-specific complementation of the yeast sac6 null mutation by human fimbrin. Mol Cell Biol 15(1- 69-75.
88. Chaudhry F, et al. (2013) Srv2/cyclase-associated protein forms hexameric shurikens that directly catalyze actin filament severing by cofilin. Mol Biol Cell 24(1-31-41.
89. Balcer HI, et al. (2003) Coordinated regulation of actin filament turnover by a highmolecular- weight Srv2/CAP complex, cofilin, profilin, and Aip1. Curr Biol 13(24- 2159-2169.
90. Lin MC, Galletta BJ, Sept D, Cooper JA (2010) Overlapping and distinct functions for cofilin, coronin and Aip1 in actin dynamics in vivo. J Cell Sci 123(Pt 8-1329-1342.
91. Andrianantoandro E, Pollard TD (2006) Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 24(1- 13-23.
92. Rodal AA, Tetreault JW, Lappalainen P, Drubin DG, Amberg DC (1999) Aip1p interacts with cofilin to disassemble actin filaments. J Cell Biol 145(6-1251-1264.
93. Mounier N, Arrigo AP (2002) Actin cytoskeleton and small heat shock proteins: How do they interact? Cell Stress Chaperones 7(2-167-176.
94. Aufricht C, et al. (1998) Heat-shock protein 25 induction and redistribution during actin reorganization after renal ischemia. Am J Physiol 274(1 Pt 2-F215-F222.
95. Panasenko OO, Kim MV, Marston SB, Gusev NB (2003) Interaction of the small heat shock protein with molecular mass 25 kDa (hsp25) with actin. Eur J Biochem 270(5- 892-901.
96. Miron T, Vancompernolle K, Vandekerckhove J, Wilchek M, Geiger B (1991) A 25-kD inhibitor of actin polymerization is a low molecular mass heat shock protein. J Cell Biol 114(2-255-261.
97. Lew DJ, Reed SI (1993) Morphogenesis in the yeast cell cycle: Regulation by Cdc28 and cyclins. J Cell Biol 120(6-1305-1320.
98. Yi K, et al. (2011) Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes. Nat Cell Biol 13(10-1252-1258.
99. Leader B, et al. (2002) Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat Cell Biol 4(12-921-928.
100. Pfender S, Kuznetsov V, Pleiser S, Kerkhoff E, Schuh M (2011) Spire-type actin nucleators cooperate with Formin-2 to drive asymmetric oocyte division. Curr Biol 21(11-955-960.
101. Schuh M, Ellenberg J (2008) A new model for asymmetric spindle positioning in mouse oocytes. Curr Biol 18(24-1986-1992.
102. McCusker D, Royou A, Velours C, Kellogg D (2012) Cdk1-dependent control of membrane-trafficking dynamics. Mol Biol Cell 23(17-3336-3347.
103. Loog M, Morgan DO (2005) Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 434(7029-104-108.
104. Toshima JY, et al. (2006) Spatial dynamics of receptor-mediated endocytic trafficking in budding yeast revealed by using fluorescent alpha-factor derivatives. Proc Natl Acad Sci USA 103(15-5793-5798.
105. Rodal AA, Manning AL, Goode BL, Drubin DG (2003) Negative regulation of yeast WASp by two SH3 domain-containing proteins. Curr Biol 13(12-1000-1008.
106. Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: The yeast proteome. J Proteome Res 2(1-43-50.
107. MacCoss MJ, et al. (2002) Shotgun identification of protein modifications from protein complexes and lens tissue. Proc Natl Acad Sci USA 99(12-7900-7905.
108. Lu B, Xu T, Park SK, Yates JR, 3rd (2009) Shotgun protein identification and quantification by mass spectrometry. Methods Mol Biol 564:261-288.
109. Cociorva D, Tabb D, Yates JR (2007) Validation of tandem mass spectrometry database search results using DTASelect. Current Protocols in Bioinformatics Chapter 13:Unit 13 14.
110. Tabb DL, McDonald WH, Yates JR, 3rd (2002) DTASelect and Contrast: Tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res 1(1-21-26.
111. Zybailov B, Coleman MK, Florens L, Washburn MP (2005) Correlation of relative abundance ratios derived from peptide ion chromatograms and spectrum counting for quantitative proteomic analysis using stable isotope labeling. Anal Chem 77(19- 6218-6224.
112. Liu H, Sadygov RG, Yates JR, 3rd (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76(14- 4193-4201.
113. Deutsch EW, Lam H, Aebersold R (2008) PeptideAtlas: A resource for target selection for emerging targeted proteomics workflows. EMBO Rep 9(5-429-434.
114. Breitkreutz BJ, Stark C, Tyers M (2003) Osprey: A network visualization system. Genome Biol 4(3-R22.
115. Mennella V, et al. (2012) Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat Cell Biol 14(11-1159-1168.
116. Doyon JB, et al. (2011) Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nat Cell Biol 13(3-331-337.
117. McCusker D, et al. (2007) Cdk1 coordinates cell-surface growth with the cell cycle. Nat Cell Biol 9(5-506-515.