Structure of the ParM filament at 8.5Å resolution

Journal of Structural Biology

Volumn 184, Issue 1, 2013, Pages 33-42

  Gayathri, Pananghat ^a,c   Fujii, Takashi ^b,c   Namba, Keiichi ^b,c   Löwe, Jan ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b OSAKA UNIVERSITY   (Japan)

^c RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

Actin; Bacterial cytoskeleton; Cytomotive; Dynamic instability

Indexed keywords

ADENOSINE TRIPHOSPHATE; F ACTIN; PARM PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DENSITY; ELECTRON; ESCHERICHIA COLI; IMAGE QUALITY; IMAGE RECONSTRUCTION; MOLECULAR DYNAMICS; MOLECULAR IMAGING; NUCLEOTIDE BINDING SITE; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ACTIN; BACTERIAL CYTOSKELETON; CYTOMOTIVE; DYNAMIC INSTABILITY;

ACTIN CYTOSKELETON; ACTINS; CATALYTIC DOMAIN; ESCHERICHIA COLI PROTEINS; HYDROLYSIS; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84884816385     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2013.02.010     Document Type: Article

References (46)

1. Aylett C.H., Wang Q., Michie K.A., Amos L.A., Löwe J. Filament structure of bacterial tubulin homologue TubZ. Proc. Natl. Acad. Sci. USA 2010, 107:19766-19771.
2. Campbell C.S., Mullins R.D. In vivo visualization of type II plasmid segregation: bacterial actin filaments pushing plasmids. J. Cell Biol. 2007, 179:1059-1066.
3. Chacon P., Wriggers W. Multi-resolution contour-based fitting of macromolecular structures. J. Mol. Biol. 2002, 317:375-384.
4. Egelman E.H. A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 2000, 85:225-234.
5. Egelman E.H. The iterative helical real space reconstruction method: surmounting the problems posed by real polymers. J. Struct. Biol. 2007, 157:83-94.
6. Egerton R.F., Leapman R.D. Electron optics in imaging energy filters. Energy-Filtering Transmission Electron Microscopy 1995, 269-290. Springer, Berlin. L. Reimer (Ed.).
7. Erickson H.P. Bacterial actin homolog ParM: arguments for an apolar, antiparallel double helix. J. Mol. Biol. 2012, 422:461-463.
8. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 1996, 116:190-199.
9. Fujii T., Kato T., Namba K. Specific arrangement of alpha-helical coiled coils in the core domain of the bacterial flagellar hook for the universal joint function. Structure 2009, 17:1485-1493.
10. Fujii T., Iwane A.H., Yanagida T., Namba K. Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 2010, 467:724-728.
11. Fujii T., Cheung M., Blanco A., Kato T., Blocker A.J., et al. Structure of a type III secretion needle at 7-A resolution provides insights into its assembly and signaling mechanisms. Proc. Natl. Acad. Sci. USA 2012, 109:4461-4466.
12. Galkin V.E., Orlova A., Rivera C., Mullins R.D., Egelman E.H. Structural polymorphism of the ParM filament and dynamic instability. Structure 2009, 17:1253-1264.
13. Galkin V.E., Orlova A., Egelman E.H. Are ParM filaments polar or bipolar?. J. Mol. Biol 2012, 423:482-485.
14. Garner E.C., Campbell C.S., Mullins R.D. Dynamic instability in a DNA-segregating prokaryotic actin homolog. Science 2004, 306:1021-1025.
15. Garner E.C., Campbell C.S., Weibel D.B., Mullins R.D. Reconstitution of DNA segregation driven by assembly of a prokaryotic actin homolog. Science 2007, 315:1270-1274.
16. Gayathri P., Fujii T., Møller-Jensen J., van den Ent F., Namba K., et al. A bipolar spindle of antiparallel ParM filaments drives bacterial plasmid segregation. Science 2012, 338:1334-1337.
17. Gerdes K., Howard M., Szardenings F. Pushing and pulling in prokaryotic DNA segregation. Cell 2010, 141:927-942.
18. Hayward S., Lee R.A. Improvements in the analysis of domain motions in proteins from conformational change: DynDom version 1.50. J. Mol. Graphics Modell. 2002, 21:181-183.
19. Jensen R.B., Gerdes K. Partitioning of plasmid R1. The ParM protein exhibits ATPase activity and interacts with the centromere-like ParR-parC complex. J. Mol. Biol. 1997, 269:505-513.
20. Löwe J., Amos L.A. Evolution of cytomotive filaments: the cytoskeleton from prokaryotes to eukaryotes. Int. J. Biochem. Cell Biol. 2009, 41:323-329.
21. Ludtke S.J., Baldwin P.R., Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 1999, 128:82-97.
22. Matsui T., Yamane J., Mogi N., Yamaguchi H., Takemoto H., et al. Structural reorganization of the bacterial cell-division protein FtsZ from Staphylococcus aureus. Acta Crystallogr., D: Biol. Crystallogr. 2012, 68:1175-1188.
23. Mindell J.A., Grigorieff N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 2003, 142:334-347.
24. Møller-Jensen J., Borch J., Dam M., Jensen R.B., Roepstorff P., et al. Bacterial mitosis: ParM of plasmid R1 moves plasmid DNA by an actin-like insertional polymerization mechanism. Mol. Cell 2003, 12:1477-1487.
25. Møller-Jensen J., Ringgaard S., Mercogliano C.P., Gerdes K., Lowe J. Structural analysis of the ParR/parC plasmid partition complex. EMBO J. 2007, 26:4413-4422.
26. Narita A., Oda T., Maeda Y. Structural basis for the slow dynamics of the actin filament pointed end. EMBO J. 2011, 30:1230-1237.
27. Nogales E., Downing K.H., Amos L.A., Löwe J. Tubulin and FtsZ form a distinct family of GTPases. Nat. Struct. Biol. 1998, 5:451-458.
28. Oda T., Iwasa M., Aihara T., Maeda Y., Narita A. The nature of the globular- to fibrous-actin transition. Nature 2009, 457:441-445.
29. Oliva M.A., Cordell S.C., Löwe J. Structural insights into FtsZ protofilament formation. Nat. Struct. Mol. Biol. 2004, 11:1243-1250.
30. Oliva M.A., Trambaiolo D., Löwe J. Structural insights into the conformational variability of FtsZ. J. Mol. Biol. 2007, 373:1229-1242.
31. Orlova A., Garner E.C., Galkin V.E., Heuser J., Mullins R.D., et al. The structure of bacterial ParM filaments. Nat. Struct. Mol. Biol. 2007, 14:921-926.
32. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., et al. UCSF Chimera-a visualisation system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
33. Popp D., Narita A., Oda T., Fujisawa T., Matsuo H., et al. Molecular structure of the ParM polymer and the mechanism leading to its nucleotide-driven dynamic instability. EMBO J. 2008, 27:570-579.
34. Popp D., Xu W., Narita A., Brzoska A.J., Skurray R.A., et al. Structure and filament dynamics of the pSK41 actin-like ParM protein: implications for plasmid DNA segregation. J. Biol. Chem. 2010, 285:10130-10140.
35. Popp D., Narita A., Lee L.J., Goshdastider U., Xue B., et al. A novel actin-like filament structure from Clostridium tetani. J. Biol. Chem 2012, 287:21121-21129.
36. Rice L.M., Montabana E.A., Agard D.A. The lattice as allosteric effector: structural studies of alphabeta- and gamma-tubulin clarify the role of GTP in microtubule assembly. Proc. Natl. Acad. Sci. USA 2008, 105:5378.
37. Rivera C.R., Kollman J.M., Polka J.K., Agard D.A., Mullins R.D. Architecture and assembly of a divergent member of the ParM family of bacterial actin-like proteins. J. Biol. Chem. 2011, 286:14282-14290.
38. Salje J., Löwe J. Bacterial actin: architecture of the ParMRC plasmid DNA partitioning complex. EMBO J. 2008, 27:2230-2238.
39. Salje J., Zuber B., Löwe J. Electron cryomicroscopy of E. coli reveals filament bundles involved in plasmid DNA segregation. Science 2009, 323:509-512.
40. Salje J., Gayathri P., Löwe J. The ParMRC system: molecular mechanisms of plasmid segregation by actin-like filaments. Nat. Rev. Microbiol. 2010, 8:683-692.
41. Salje J., van den Ent F., de Boer P., Löwe J. Direct membrane binding by bacterial actin MreB. Mol. Cell 2011, 43:478-487.
42. Schumacher M.A., Glover T.C., Brzoska A.J., Jensen S.O., Dunham T.D., et al. Segrosome structure revealed by a complex of ParR with centromere DNA. Nature 2007, 450:1268-1271.
43. Szwedziak P., Wang Q., Freund S.M., Löwe J. FtsA forms actin-like protofilaments. EMBO J. 2012, 31:2249-2260.
44. van den Ent F., Amos L.A., Löwe J. Prokaryotic origin of the actin cytoskeleton. Nature 2001, 413:39-44.
45. van den Ent F., Moller-Jensen J., Amos L.A., Gerdes K., Löwe J. F-actin-like filaments formed by plasmid segregation protein ParM. EMBO J. 2002, 21:6935-6943.
46. Vorobiev S., Strokopytov B., Drubin D.G., Frieden C., Ono S., et al. The structure of nonvertebrate actin: implications for the ATP hydrolytic mechanism. Proc. Natl. Acad. Sci. USA 2003, 100:5760-5765.