Ligand-induced activation of a formin-NPF pair leads to collaborative actin nucleation

Journal of Cell Biology

Volumn 201, Issue 4, 2013, Pages 595-611

  Graziano, Brian R ^a   Jonasson, Erin M ^a   Pullen, Jessica G ^a   Gould, Christopher J ^a   Goodel, Bruce L ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; LIGAND; METHENAMINE; PROTEIN BNR1; PROTEIN BUD6; UNCLASSIFIED DRUG;

ALLELE; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CRYSTAL STRUCTURE; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; REGULATORY MECHANISM; REGULATORY SEQUENCE;

ACTINS; ANIMALS; CARRIER PROTEINS; CYTOSKELETAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GREEN FLUORESCENT PROTEINS; KINETICS; LIGANDS; MASS SPECTROMETRY; MICROFILAMENT PROTEINS; MUSCLE, SKELETAL; MUTATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RABBITS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84878524897     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201212059     Document Type: Article

References (72)

1. Amberg, D.C., J.E. Zahner, J.W. Mulholland, J.R. Pringle, and D. Botstein. 1997. Aip3p/Bud6p, a yeast actin-interacting protein that is involved in morphogenesis and the selection of bipolar budding sites. Mol. Biol. Cell. 8:729-753.
2. Blanchoin, L., and A. Michelot. 2012. Actin cytoskeleton: a team effort during actin assembly. Curr. Biol. 22:R643-R645. http://dx.doi.org/10.1016/ j.cub.2012.07.026
3. Block, J., D. Breitsprecher, S. Kühn, M. Winterhoff, F. Kage, R. Geffers, P. Duwe, J.L. Rohn, B. Baum, C. Brakebusch, et al. 2012. FMNL2 drives actin-based protrusion and migration downstream of Cdc42. Curr. Biol. 22:1005-1012. http://dx.doi.org/10.1016/j.cub.2012.03.064
4. Bosch, M., K.H. Le, B. Bugyi, J.J. Correia, L. Renault, and M.F. Carlier. 2007. Analysis of the function of Spire in actin assembly and its synergy with formin and profilin. Mol. Cell. 28:555-568. http://dx.doi.org/10.1016/j.molcel.2007.09.018
5. Breitsprecher, D., R. Jaiswal, J.P. Bombardier, C.J. Gould, J. Gelles, and B.L. Goode. 2012. Rocket launcher mechanism of collaborative actin assembly defined by single-molecule imaging. Science. 336:1164-1168. http://dx.doi.org/10.1126/science.1218062
6. Buttery, S.M., S. Yoshida, and D. Pellman. 2007. Yeast formins Bni1 and Bnr1 utilize different modes of cortical interaction during the assembly of actin cables. Mol. Biol. Cell. 18:1826-1838. http://dx.doi.org/10.1091/mbc.E06-09-0820
7. Chesarone, M.A., and B.L. Goode. 2009. Actin nucleation and elongation factors: mechanisms and interplay. Curr. Opin. Cell Biol. 21:28-37. http://dx.doi.org/10.1016/j.ceb.2008.12.001
8. Chesarone, M., C.J. Gould, J.B. Moseley, and B.L. Goode. 2009. Displacement of formins from growing barbed ends by bud14 is critical for actin cable architecture and function. Dev. Cell. 16:292-302. http://dx.doi .org/10.1016/j.devcel.2008.12.001
9. Courtemanche, N., and T.D. Pollard. 2012. Determinants of Formin Homology 1 (FH1) domain function in actin filament elongation by formins. J. Biol. Chem. 287:7812-7820. http://dx.doi.org/10.1074/jbc.M111.322958
10. Cristea, I.M., R. Williams, B.T. Chait, and M.P. Rout. 2005. Fluorescent proteins as proteomic probes. Mol. Cell. Proteomics. 4:1933-1941. http://dx.doi.org/10.1074/mcp.M500227-MCP200
11. Delgehyr, N., C.S. Lopes, C.A. Moir, S.M. Huisman, and M. Segal. 2008. Dissecting the involvement of formins in Bud6p-mediated cortical capture of microtubules in S. cerevisiae. J. Cell Sci. 121:3803-3814. http://dx.doi.org/10.1242/jcs.036269
12. Dominguez, R. 2009. Actin filament nucleation and elongation factors-structure-function relationships. Crit. Rev. Biochem. Mol. Biol. 44:351-366. http://dx.doi.org/10.3109/10409230903277340
13. Dominguez, R. 2010. Structural insights into de novo actin polymerization. Curr. Opin. Struct. Biol. 20:217-225. http://dx.doi.org/10.1016/j.sbi.2009.12.012
14. Evangelista, M., K. Blundell, M.S. Longtine, C.J. Chow, N. Adames, J.R. Pringle, M. Peter, and C. Boone. 1997. Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science. 276:118-122. http://dx.doi.org/10.1126/science.276.5309.118
15. Firat-Karalar, E.N., and M.D. Welch. 2011. New mechanisms and functions of actin nucleation. Curr. Opin. Cell Biol. 23:4-13. http://dx.doi.org/10.1016/j.ceb.2010.10.007
16. Gould, C.J., S. Maiti, A. Michelot, B.R. Graziano, L. Blanchoin, and B.L. Goode. 2011. The formin DAD domain plays dual roles in autoinhibition and actin nucleation. Curr. Biol. 21:384-390. http://dx.doi.org/10.1016/j.cub.2011.01.047
17. Graziano, B.R., A.G. DuPage, A. Michelot, D. Breitsprecher, J.B. Moseley, I. Sagot, L. Blanchoin, and B.L. Goode. 2011. Mechanism and cellular function of Bud6 as an actin nucleation-promoting factor. Mol. Biol. Cell. 22:4016-4028. http://dx.doi.org/10.1091/mbc.E11-05-0404
18. Heasman, S.J., and A.J. Ridley. 2008. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9:690-701. http://dx.doi.org/10.1038/nrm2476
19. Heimsath, E.G., Jr., and H.N. Higgs. 2012. The C terminus of formin FMNL3 accelerates actin polymerization and contains a WH2 domain-like sequence that binds both monomers and filament barbed ends. J. Biol. Chem. 287:3087-3098. http://dx.doi.org/10.1074/jbc.M111.312207
20. Huh, W.K., J.V. Falvo, L.C. Gerke, A.S. Carroll, R.W. Howson, J.S. Weissman, and E.K. O'Shea. 2003. Global analysis of protein localization in budding yeast. Nature. 425:686-691. http://dx.doi.org/10.1038/nature02026
21. Jin, H., and D.C. Amberg. 2000. The secretory pathway mediates localization of the cell polarity regulator Aip3p/Bud6p. Mol. Biol. Cell. 11:647-661.
22. Kamei, T., K. Tanaka, T. Hihara, M. Umikawa, H. Imamura, M. Kikyo, K. Ozaki, and Y. Takai. 1998. Interaction of Bnr1p with a novel Src homology 3 domaincontaining Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae. J. Biol. Chem. 273:28341-28345. http://dx.doi.org/10.1074/jbc.273.43.28341
23. Kikyo, M., K. Tanaka, T. Kamei, K. Ozaki, T. Fujiwara, E. Inoue, Y. Takita, Y. Ohya, and Y. Takai. 1999. An FH domain-containing Bnr1p is a multifunctional protein interacting with a variety of cytoskeletal proteins in Saccharomyces cerevisiae. Oncogene. 18:7046-7054. http://dx.doi.org/10.1038/sj.onc.1203184
24. Kita, K., T. Wittmann, I.S. Näthke, and C.M. Waterman-Storer. 2006. Adenomatous polyposis coli on microtubule plus ends in cell extensions can promote microtubule net growth with or without EB1. Mol. Biol. Cell. 17:2331-2345. http://dx.doi.org/10.1091/mbc.E05-06-0498
25. Kono, K., Y. Saeki, S. Yoshida, K. Tanaka, and D. Pellman. 2012. Proteasomal degradation resolves competition between cell polarization and cellular wound healing. Cell. 150:151-164. http://dx.doi.org/10.1016/j.cell.2012.05.030
26. Kovar, D.R., and T.D. Pollard. 2004. Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces. Proc. Natl. Acad. Sci. USA. 101:14725-14730. http://dx.doi.org/10.1073/pnas.0405902101
27. Kovar, D.R., E.S. Harris, R. Mahaffy, H.N. Higgs, and T.D. Pollard. 2006. Control of the assembly of ATP-and ADP-actin by formins and profilin. Cell. 124:423-435. http://dx.doi.org/10.1016/j.cell.2005.11.038
28. Krogan, N.J., G. Cagney, H. Yu, G. Zhong, X. Guo, A. Ignatchenko, J. Li, S. Pu, N. Datta, A.P. Tikuisis, et al. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature. 440:637-643. http://dx.doi.org/10.1038/nature04670
29. Kuhn, J.R., and T.D. Pollard. 2005. Real-time measurements of actin filament polymerization by total internal reflection fluorescence microscopy. Biophys. J. 88:1387-1402. http://dx.doi.org/10.1529/biophysj.104.047399
30. Li, F., and H.N. Higgs. 2003. The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr. Biol. 13:1335-1340. http://dx.doi.org/10.1016/S0960-9822(03)00540-2
31. Longtine, M.S., A. McKenzie III, D.J. Demarini, N.G. Shah, A. Wach, A. Brachat, P. Philippsen, and J.R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 14:953-961. http://dx.doi.org/10.1002/(SICI)1097-0061(199807)14:10953::AID-YEA2933.0.CO;2-U
32. Moseley, J.B., and B.L. Goode. 2005. Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6. J. Biol. Chem. 280:28023-28033. http://dx.doi.org/10.1074/jbc.M503094200
33. Moseley, J.B., I. Sagot, A.L. Manning, Y. Xu, M.J. Eck, D. Pellman, and B.L. Goode. 2004. A conserved mechanism for Bni1-and mDia1-induced actin assembly and dual regulation of Bni1 by Bud6 and profilin. Mol. Biol. Cell. 15:896-907. http://dx.doi.org/10.1091/mbc.E03-08-0621
34. Moseley, J.B., S. Maiti, and B.L. Goode. 2006. Formin proteins: purification and measurement of effects on actin assembly. Methods Enzymol. 406:215-234. http://dx.doi.org/10.1016/S0076-6879(06)06016-2
35. Narayanaswamy, R., E.K. Moradi, W. Niu, G.T. Hart, M. Davis, K.L. McGary, A.D. Ellington, and E.M. Marcotte. 2009. Systematic definition of protein constituents along the major polarization axis reveals an adaptive reuse of the polarization machinery in pheromone-treated budding yeast. J. Proteome Res. 8:6-19. http://dx.doi.org/10.1021/pr800524g
36. Okada, K., F. Bartolini, A.M. Deaconescu, J.B. Moseley, Z. Dogic, N. Grigorieff, G.G. Gundersen, and B.L. Goode. 2010. Adenomatous polyposis coli protein nucleates actin assembly and synergizes with the formin mDia1. J. Cell Biol. 189:1087-1096. http://dx.doi.org/10.1083/jcb.201001016
37. Otomo, T., D.R. Tomchick, C. Otomo, S.C. Panchal, M. Machius, and M.K. Rosen. 2005. Structural basis of actin filament nucleation and processive capping by a formin homology 2 domain. Nature. 433:488-494. http://dx.doi.org/10.1038/nature03251
38. Ozaki-Kuroda, K., Y. Yamamoto, H. Nohara, M. Kinoshita, T. Fujiwara, K. Irie, and Y. Takai. 2001. Dynamic localization and function of Bni1p at the sites of directed growth in Saccharomyces cerevisiae. Mol. Cell. Biol. 21:827-839. http://dx.doi.org/10.1128/MCB.21.3.827-839.2001
39. Padrick, S.B., and M.K. Rosen. 2010. Physical mechanisms of signal integration by WASP family proteins. Annu. Rev. Biochem. 79:707-735. http://dx.doi.org/10.1146/annurev.biochem.77.060407.135452
40. Paul, A.S., and T.D. Pollard. 2008. The role of the FH1 domain and profilin in formin-mediated actin-filament elongation and nucleation. Curr. Biol. 18:9-19. http://dx.doi.org/10.1016/j.cub.2007.11.062
41. Pechlivanis, M., A. Samol, and E. Kerkhoff. 2009. Identification of a short Spir interaction sequence at the C-terminal end of formin subgroup proteins. J. Biol. Chem. 284:25324-25333. http://dx.doi.org/10.1074/jbc.M109.030320
42. Pfender, S., V. Kuznetsov, S. Pleiser, E. Kerkhoff, and M. Schuh. 2011. Spire-type actin nucleators cooperate with Formin-2 to drive asymmetric oocyte division. Curr. Biol. 21:955-960. http://dx.doi.org/10.1016/j.cub.2011.04.029
43. Pollard, T.D. 2007. Regulation of actin filament assembly by Arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36:451-477. http://dx.doi.org/10.1146/annurev.biophys.35.040405.101936
44. Pollard, T.D. 2010. A guide to simple and informative binding assays. Mol. Biol. Cell. 21:4061-4067. http://dx.doi.org/10.1091/mbc.E10-08-0683
45. Pollard, T.D., and J.A. Cooper. 1984. Quantitative analysis of the effect of Acanthamoeba profilin on actin filament nucleation and elongation. Biochemistry. 23:6631-6641. http://dx.doi.org/10.1021/bi00321a054
46. Pollard, T.D., and J.A. Cooper. 2009. Actin, a central player in cell shape and movement. Science. 326:1208-1212. http://dx.doi.org/10.1126/science.1175862
47. Pruyne, D., M. Evangelista, C. Yang, E. Bi, S. Zigmond, A. Bretscher, and C. Boone. 2002. Role of formins in actin assembly: nucleation and barbed-end association. Science. 297:612-615. http://dx.doi.org/10.1126/science.1072309
48. Pruyne, D., L. Gao, E. Bi, and A. Bretscher. 2004. Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Mol. Biol. Cell. 15:4971-4989. http://dx.doi.org/10.1091/mbc.E04-04-0296
49. Quinlan, M.E., S. Hilgert, A. Bedrossian, R.D. Mullins, and E. Kerkhoff. 2007. Regulatory interactions between two actin nucleators, Spire and Cappuccino. J. Cell Biol. 179:117-128. http://dx.doi.org/10.1083/jcb.200706196
50. Romero, S., C. Le Clainche, D. Didry, C. Egile, D. Pantaloni, and M.F. Carlier. 2004. Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell. 119:419-429. http://dx.doi.org/10.1016/j.cell.2004.09.039
51. Rosales-Nieves, A.E., J.E. Johndrow, L.C. Keller, C.R. Magie, D.M. Pinto-Santini, and S.M. Parkhurst. 2006. Coordination of microtubule and microfilament dynamics by Drosophila Rho1, Spire and Cappuccino. Nat. Cell Biol. 8:367-376. http://dx.doi.org/10.1038/ncb1385
52. Rottner, K., J. Hänisch, and K.G. Campellone. 2010. WASH, WHAMM and JMY: regulation of Arp2/3 complex and beyond. Trends Cell Biol. 20:650-661. http://dx.doi.org/10.1016/j.tcb.2010.08.014
53. Sagot, I., S.K. Klee, and D. Pellman. 2002a. Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat. Cell Biol. 4:42-50.
54. Sagot, I., A.A. Rodal, J. Moseley, B.L. Goode, and D. Pellman. 2002b. An actin nucleation mechanism mediated by Bni1 and profilin. Nat. Cell Biol. 4:626-631.
55. Schuh, M. 2011. An actin-dependent mechanism for long-range vesicle transport. Nat. Cell Biol. 13:1431-1436. http://dx.doi.org/10.1038/ncb2353
56. Segal, M., K. Bloom, and S.I. Reed. 2000. Bud6 directs sequential microtubule interactions with the bud tip and bud neck during spindle morphogenesis in Saccharomyces cerevisiae. Mol. Biol. Cell. 11:3689-3702.
57. Sitar, T., J. Gallinger, A.M. Ducka, T.P. Ikonen, M. Wohlhoefler, K.M. Schmoller, A.R. Bausch, P. Joel, K.M. Trybus, A.A. Noegel, et al. 2011. Molecular architecture of the Spire-actin nucleus and its implication for actin filament assembly. Proc. Natl. Acad. Sci. USA. 108:19575-19580. http://dx.doi.org/10.1073/pnas.1115465108
58. Spudich, J.A., and S. Watt. 1971. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosintroponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246:4866-4871.
59. Su, L.K., M. Burrell, D.E. Hill, J. Gyuris, R. Brent, R. Wiltshire, J. Trent, B. Vogelstein, and K.W. Kinzler. 1995. APC binds to the novel protein EB1. Cancer Res. 55:2972-2977.
60. Ten Hoopen, R., C. Cepeda-García, R. Fernández-Arruti, M.A. Juanes, N. Delgehyr, and M. Segal. 2012. Mechanism for astral microtubule capture by cortical Bud6p priming spindle polarity in S. cerevisiae. Curr. Biol. 22:1075-1083. http://dx.doi.org/10.1016/j.cub.2012.04.059
61. Tong, A.H., M. Evangelista, A.B. Parsons, H. Xu, G.D. Bader, N. Pagé, M. Robinson, S. Raghibizadeh, C.W. Hogue, H. Bussey, et al. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science. 294:2364-2368. http://dx.doi.org/10.1126/science.1065810
62. Tu, D., B.R. Graziano, E. Park, W. Zheng, Y. Li, B.L. Goode, and M.J. Eck. 2012. Structure of the formin-interaction domain of the actin nucleationpromoting factor Bud6. Proc. Natl. Acad. Sci. USA. 109:E3424-E3433. http://dx.doi.org/10.1073/pnas.1203035109
63. Vallen, E.A., J. Caviston, and E. Bi. 2000. Roles of Hof1p, Bni1p, Bnr1p, and myo1p in cytokinesis in Saccharomyces cerevisiae. Mol. Biol. Cell. 11:593-611.
64. Vavylonis, D., D.R. Kovar, B. O'Shaughnessy, and T.D. Pollard. 2006. Model of formin-associated actin filament elongation. Mol. Cell. 21:455-466. http://dx.doi.org/10.1016/j.molcel.2006.01.016
65. Vizcarra, C.L., B. Kreutz, A.A. Rodal, A.V. Toms, J. Lu, W. Zheng, M.E. Quinlan, and M.J. Eck. 2011. Structure and function of the interacting domains of Spire and Fmn-family formins. Proc. Natl. Acad. Sci. USA. 108:11884-11889. http://dx.doi.org/10.1073/pnas.1105703108
66. Webb, R.L., M.N. Zhou, and B.M. McCartney. 2009. A novel role for an APC2-Diaphanous complex in regulating actin organization in Drosophila. Development. 136:1283-1293. http://dx.doi.org/10.1242/dev.026963
67. Wen, Y., C.H. Eng, J. Schmoranzer, N. Cabrera-Poch, E.J. Morris, M. Chen, B.J. Wallar, A.S. Alberts, and G.G. Gundersen. 2004. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat. Cell Biol. 6:820-830. http://dx.doi.org/10.1038/ncb1160
68. Xu, Y., J.B. Moseley, I. Sagot, F. Poy, D. Pellman, B.L. Goode, and M.J. Eck. 2004. Crystal structures of a Formin Homology-2 domain reveal a tethered dimer architecture. Cell. 116:711-723. http://dx.doi.org/10.1016/S0092-8674(04)00210-7
69. Yu, H., P. Braun, M.A. Yildirim, I. Lemmens, K. Venkatesan, J. Sahalie, T. Hirozane-Kishikawa, F. Gebreab, N. Li, N. Simonis, et al. 2008. Highquality binary protein interaction map of the yeast interactome network. Science. 322:104-110. http://dx.doi.org/10.1126/science.1158684
70. Yu, J.H., A.H. Crevenna, M. Bettenbühl, T. Freisinger, and R. Wedlich-Söldner. 2011. Cortical actin dynamics driven by formins and myosin V. J. Cell Sci. 124:1533-1541. http://dx.doi.org/10.1242/jcs.079038
71. Zeth, K., M. Pechlivanis, A. Samol, S. Pleiser, C. Vonrhein, and E. Kerkhoff. 2011. Molecular basis of actin nucleation factor cooperativity: crystal structure of the Spir-1 kinase non-catalytic C-lobe domain (KIND) formin-2 formin SPIR interaction motif (FSI) complex. J. Biol. Chem. 286:30732-30739. http://dx.doi.org/10.1074/jbc.M111.257782
72. Zigmond, S.H., M. Evangelista, C. Boone, C. Yang, A.C. Dar, F. Sicheri, J. Forkey, and M. Pring. 2003. Formin leaky cap allows elongation in the presence of tight capping proteins. Curr. Biol. 13:1820-1823. http://dx.doi.org/10.1016/j.cub.2003.09.057