Crystal structure of the formin mDIA1 in autoinhibited conformation

PLoS ONE

Volumn 5, Issue 9, 2010, Pages 1-13

  Otomo, Takanori ^a,c   Tomchick, Diana R ^a   Otomo, Chinatsu ^a,c   Machius, Mischa ^a,d   Rosen, Michael K ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DIAPHANOUS AUTOINHIBITORY DOMAIN; DIAPHANOUS INHIBITORY DOMAIN; DIMER; FORMIN HOMOLOGY 2; PROTEIN MDIA1; UNCLASSIFIED DRUG; ACTIN; CARRIER PROTEIN; DIAP1 PROTEIN, MOUSE;

ACTIN FILAMENT; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS; TRANS ISOMER; AMINO ACID SEQUENCE; CHEMISTRY; CONFORMATION; DIMERIZATION; GENETICS; HOMEOSTASIS; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

MAMMALIA;

ACTINS; AMINO ACID SEQUENCE; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HOMEOSTASIS; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 77958519651     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012896     Document Type: Article

References (57)

1. Pollard TD (2007) Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct 36: 451-477.
2. Chang F, Burgess D (2003) The contractile ring. Curr Biol 13: R692-R693.
3. Chesarone MA, DuPage AG, Goode BL (2010) Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat Rev Mol Cell Biol 11: 62-74.
4. Campellone KG, Welch MD (2010) A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol 11: 237-251.
5. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465.
6. Higgs HN, Pollard TD (2001) Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu Rev Biochem 70: 649-676.
7. Carlier MF, Wiesner S, Le Clainche C, Pantaloni D (2003) Actin-based motility as a self-organized system: mechanism and reconstitution in vitro. C R Biol 326: 161-170.
8. Weaver AM, Young ME, Lee WL, Cooper JA (2003) Integration of signals to the Arp2/3 complex. Curr Opin Cell Biol 15: 23-30.
9. Pruyne D, Evangelista M, Yang C, Bi E, Zigmond S, et al. (2002) Role of formins in actin assembly: nucleation and barbed-end association. Science 297: 612-615.
10. Sagot I, Rodal AA, Moseley J, Goode BL, Pellman D (2002) An actin nucleation mechanism mediated by Bni1 and profilin. Nat Cell Biol 4: 626-631.
11. 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: 423-435.
12. Romero S, Le Clainche C, Didry D, Egile C, Pantaloni D, et al. (2004) Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119: 419-429.
13. Kovar DR, Pollard TD (2004) Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces. Proc Natl Acad Sci U S A 101: 14725-14730.
14. Evangelista M, Blundell K, Longtine MS, Chow CJ, Adames N, et al. (1997) Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276: 118-122.
15. 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: 32-41.
16. 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: 2313-2324.
17. Higashida C, Miyoshi T, Fujita A, Oceguera-Yanez F, Monypenny J, et al. (2004) Actin polymerization-driven molecular movement of mDia1 in living cells. Science 303: 2007-2010.
18. Zigmond S (2004) Formin' adherens junctions. Nat Cell Biol 6: 12-14.
19. Wallar BJ, Alberts AS (2003) The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol 13: 435-446.
20. Xu Y, Moseley JB, Sagot I, Poy F, Pellman D, et al. (2004) Crystal structures of a Formin Homology-2 domain reveal a tethered dimer architecture. Cell 116: 711-723.
21. Otomo T, Tomchick DR, Otomo C, Panchal SC, Machius M, et al. (2005) Structural basis of actin filament nucleation and processive capping by a forming homology 2 domain. Nature 433: 488-494.
22. Goode BL, Eck MJ (2007) Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem 76: 593-627.
23. Vavylonis D, Kovar DR, O'Shaughnessy B, Pollard TD (2006) Model of forminassociated actin filament elongation. Mol Cell 21: 455-466.
24. Paul AS, Pollard TD (2009) Review of the mechanism of processive actin filament elongation by formins. Cell Motil Cytoskeleton 66: 606-617.
25. Shemesh T, Otomo T, Rosen MK, Bershadsky AD, Kozlov MM (2005) A novel mechanism of actin filament processive capping by formin: solution of the rotation paradox. J Cell Biol 170: 889-893.
26. Higgs HN (2005) Formin proteins: a domain-based approach. Trends Biochem Sci 30: 342-353.
27. Habas R, Kato Y, He X (2001) Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107: 843-854.
28. Narumiya S, Ishizaki T, Watanabe N (1997) Rho effectors and reorganization of actin cytoskeleton. FEBS Lett 410: 68-72.
29. Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, et al. (1997) p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 16: 3044-3056.
30. Matusek T, Djiane A, Jankovics F, Brunner D, Mlodzik M, et al. (2006) The Drosophila formin DAAM regulates the tracheal cuticle pattern through organizing the actin cytoskeleton. Development 133: 957-966.
31. Alberts AS (2001) Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain. J Biol Chem 276: 2824-2830.
32. Li F, Higgs HN (2005) Dissecting requirements for auto-inhibition of actin nucleation by the formin, mDia1. J Biol Chem 280: 6986-6992.
33. Seth A, Otomo C, Rosen MK (2006) Autoinhibition regulates cellular localization and actin assembly activity of the diaphanous-related formins FRL{alpha} and mDia1. J Cell Biol 174: 701-713.
34. 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: 273-281.
35. Rose R, Weyand M, Lammers M, Ishizaki T, Ahmadian MR, et al. (2005) Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature 435: 513-518.
36. Nezami AG, Poy F, Eck MJ (2006) Structure of the Autoinhibitory Switch in Formin mDia1. Structure 14: 257-263.
37. Kim AS, Kakalis LT, Abdul-Manan N, Liu GA, Rosen MK (2000) Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein. Nature 404: 151-158.
38. Lei M, Lu W, Meng W, Parrini MC, Eck MJ, et al. (2000) Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell 102: 387-397.
39. Pufall MA, Graves BJ (2002) Autoinhibitory domains: modular effectors of cellular regulation. Annu Rev Cell Dev Biol 18: 421-462.
40. Lammers M, Rose R, Scrima A, Wittinghofer A (2005) The regulation of mDia1 by autoinhibition and its release by Rho*GTP. EMBO J 24: 4176-4187.
41. Shimada A, Nyitrai M, Vetter IR, Kühlmann D, Bugyi B, et al. (2004) The core FH2 domain of diaphanous-related formins is an elongated actin binding protein that inhibits polymerization. Mol Cell 13: 511-522.
42. Lu J, Meng W, Poy F, Maiti S, Goode BL, et al. (2007) Structure of the FH2 domain of Daam1: implications for formin regulation of actin assembly. J Mol Biol 369: 1258-1269.
43. Wallar BJ, Stropich BN, Schoenherr JA, Holman HA, Kitchen SM, 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: 4300-4307.
44. Li F, Higgs HN (2003) The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr Biol 13: 1335-1340.
45. Gardner KH, Kay LE (1997) Production and Incorporation of 15N, 13C, 2H (1H-delta1 Methyl) Isoleucine into Proteins for Multidimensional NMR Studies. J Am Chem Soc 119: 7599-7600.
46. Spudich JA, Watt S (1971) The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complexwith actin and the proteolytic fragments of myosin. J Biol Chem 246: 4866-4871.
47. Otterbein LR, Graceffa P, Dominguez R (2001) The crystal structure of uncomplexed actin in the ADP state. Science 293: 708-711.
48. Marchand JB, Kaiser DA, Pollard TD, Higgs HN (2001) Interaction of WASP/ Scar proteins with actin and vertebrate Arp2/3 complex. Nat Cell Biol 3: 76-82.
49. Otwinowski Z, Minor W, Carter CW Jr. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology: Academic Press. Pp 307-326.
50. Navaza J (1994) AMoRe: an automated package for molecular replacement. Acta Crystallographica Section A 50: 157-163.
51. Otwinowski Z (1991) Maximum likelihood refinement of heavy atom parameters. In: Wolf W, Evans PR, Leslie AGW, eds. Isomorphous Replacement and Anomalous Scattering. Cambridge, UK: Science & Engineering Research Council. pp 80-86.
52. Cowtan K, Main P (1998) Miscellaneous algorithms for density modification. Acta Crystallogr D Biol Crystallogr 54: 487-493.
53. Jones TA, Zou JY, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallographica Section A 47: 110-119.
54. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954.
55. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383.
56. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMR Pipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
57. Johnson BA (2004) Using NMR View to visualize and analyze the NMR spectra of macromolecules. Methods Mol Biol 278: 313-352.