The structure and assembly mechanism of a novel three-stranded tubulin filament that centers phage DNA

Structure

Volumn 22, Issue 4, 2014, Pages 539-548

  Zehr, Elena A ^a   Kraemer, James A ^a   Erb, Marcella L ^b   Coker, Joanna K C ^b   Montabana, Elizabeth A ^a,c   Pogliano, Joe ^b   Agard, David A ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGE DNA; PROTEIN PHUZ; TUBULIN; UNCLASSIFIED DRUG; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; GUANOSINE TRIPHOSPHATE DERIVATIVE; MEMBRANE PROTEIN; PHUZ FILAMENT PROTEIN; PROTEIN BINDING; RECOMBINANT PROTEIN; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; HOST CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR MODEL; MUTATION; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SUBUNIT; AMINO TERMINAL SEQUENCE; BACTERIAL CELL; CRYOELECTRON MICROSCOPY; CYTOARCHITECTURE; CYTOSKELETON; MICROTUBULE; MUTAGENESIS; NUCLEAR SIZE; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PSEUDOMONAS CHLORORAPHIS; THREE STRANDED TUBULIN FILAMENT; VIRUS REPLICATION; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; METABOLISM; PROMOTER REGION; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; PSEUDOMONAS; PSEUDOMONAS PHAGE; VIROLOGY;

CRYOELECTRON MICROSCOPY; DNA, VIRAL; ESCHERICHIA COLI; GENE EXPRESSION; MODELS, MOLECULAR; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS; PSEUDOMONAS PHAGES; RECOMBINANT PROTEINS; TUBULIN; VIRAL PROTEINS;

EID: 84898024878     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.02.006     Document Type: Article

References (31)

1. C.H. Aylett, Q. Wang, K.A. Michie, L.A. Amos, and J. Löwe Filament structure of bacterial tubulin homologue TubZ Proc. Natl. Acad. Sci. USA 107 2010 19766 19771
2. C.H. Aylett, J. Lowe, and L.A. Amos New insights into the mechanisms of cytomotive actin and tubulin filaments Int. Rev. Cell Mol. Biol. 292 2011 1 71
3. C.H. Aylett, T. Izoré, L.A. Amos, and J. Löwe Structure of the tubulin/FtsZ-like protein TubZ from Pseudomonas bacteriophage ΦKZ J. Mol. Biol. 425 2013 2164 2173
4. D. Bramhill, and C.M. Thompson GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules Proc. Natl. Acad. Sci. USA 91 1994 5813 5817
5. E.H. Egelman A robust algorithm for the reconstruction of helical filaments using single-particle methods Ultramicroscopy 85 2000 225 234
6. E.H. Egelman The iterative helical real space reconstruction method: surmounting the problems posed by real polymers J. Struct. Biol. 157 2007 83 94
7. H. Flyvbjerg, E. Jobs, and S. Leibler Kinetics of self-assembling microtubules: an "inverse problem" in biochemistry Proc. Natl. Acad. Sci. USA 93 1996 5975 5979
8. A. Fokine, A.J. Battisti, V.D. Bowman, A.V. Efimov, L.P. Kurochkina, P.R. Chipman, V.V. Mesyanzhinov, and M.G. Rossmann Cryo-EM study of the Pseudomonas bacteriophage phiKZ Structure 15 2007 1099 1104
9. J. Frank, M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116 1996 190 199
10. E.C. Garner, C.S. Campbell, D.B. Weibel, and R.D. Mullins Reconstitution of DNA segregation driven by assembly of a prokaryotic actin homolog Science 315 2007 1270 1274
11. P. Gayathri, T. Fujii, K. Namba, and J. Löwe Structure of the ParM filament at 8.5Å resolution J. Struct. Biol. 184 2013 33 42
12. G.T. Howard, R.I. Mackie, I.K. Cann, S. Ohene-Adjei, K.S. Aboudehen, B.G. Duos, and G.W. Childers Effect of insertional mutations in the pueA and pueB genes encoding two polyurethanases in Pseudomonas chlororaphis contained within a gene cluster J. Appl. Microbiol. 103 2007 2074 2083
13. J.A. Kraemer, M.L. Erb, C.A. Waddling, E.A. Montabana, E.A. Zehr, H. Wang, K. Nguyen, D.S. Pham, D.A. Agard, and J. Pogliano A phage tubulin assembles dynamic filaments by an atypical mechanism to center viral DNA within the host cell Cell 149 2012 1488 1499
14. V.N. Krylov, D.M. Dela Cruz, K. Hertveldt, and H.W. Ackermann "phiKZ-like viruses", a proposed new genus of myovirus bacteriophages Arch. Virol. 152 2007 1955 1959
15. R. Lavigne, P. Darius, E.J. Summer, D. Seto, P. Mahadevan, A.S. Nilsson, H.W. Ackermann, and A.M. Kropinski Classification of Myoviridae bacteriophages using protein sequence similarity BMC Microbiol. 9 2009 224
16. Z. Li, M.J. Trimble, Y.V. Brun, and G.J. Jensen The structure of FtsZ filaments in vivo suggests a force-generating role in cell division EMBO J. 26 2007 4694 4708
17. J. Löwe, and L.A. Amos Tubulin-like protofilaments in Ca2+-induced FtsZ sheets EMBO J. 18 1999 2364 2371
18. C. Lu, M. Reedy, and H.P. Erickson Straight and curved conformations of FtsZ are regulated by GTP hydrolysis J. Bacteriol. 182 2000 164 170
19. J.A. Mindell, and N. Grigorieff Accurate determination of local defocus and specimen tilt in electron microscopy J. Struct. Biol. 142 2003 334 347
20. E.A. Montabana, and D.A. Agard Bacterial tubulin TubZ-Bt transitions between a two-stranded intermediate and a four-stranded filament upon GTP hydrolysis Proc. Natl. Acad. Sci U S A. 2014 10.1073/pnas.1318339111 Published online February 14, 2014
21. L. Ni, W. Xu, M. Kumaraswami, and M.A. Schumacher Plasmid protein TubR uses a distinct mode of HTH-DNA binding and recruits the prokaryotic tubulin homolog TubZ to effect DNA partition Proc. Natl. Acad. Sci. USA 107 2010 11763 11768
22. E. Nogales, K.H. Downing, L.A. Amos, and J. Löwe Tubulin and FtsZ form a distinct family of GTPases Nat. Struct. Biol. 5 1998 451 458
23. E. Nogales, S.G. Wolf, and K.H. Downing Structure of the alpha beta tubulin dimer by electron crystallography Nature 391 1998 199 203
24. E. Nogales, M. Whittaker, R.A. Milligan, and K.H. Downing High-resolution model of the microtubule Cell 96 1999 79 88
25. M.A. Oliva, A.J. Martin-Galiano, Y. Sakaguchi, and J.M. Andreu Tubulin homolog TubZ in a phage-encoded partition system Proc. Natl. Acad. Sci. USA 109 2012 7711 7716
26. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
27. D. Qiu, F.H. Damron, T. Mima, H.P. Schweizer, and H.D. Yu PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria Appl. Environ. Microbiol. 74 2008 7422 7426
28. S.H. Scheres, and S. Chen Prevention of overfitting in cryo-EM structure determination Nat. Methods 9 2012 853 854
29. H. Sui, and K.H. Downing Structural basis of interprotofilament interaction and lateral deformation of microtubules Structure 18 2010 1022 1031
30. J.A. Thomas, M.R. Rolando, C.A. Carroll, P.S. Shen, D.M. Belnap, S.T. Weintraub, P. Serwer, and S.C. Hardies Characterization of Pseudomonas chlororaphis myovirus 201varphi2-1 via genomic sequencing, mass spectrometry, and electron microscopy Virology 376 2008 330 338
31. R.C. Weisenberg Microtubule formation in vitro in solutions containing low calcium concentrations Science 177 1972 1104 1105