A Conformational Switch in Bacteriophage P22 Portal Protein Primes Genome Injection

Molecular Cell

Volumn 29, Issue 3, 2008, Pages 376-383

  Zheng, Hongjin ^a   Olia, Adam S ^b   Gonen, Melissa ^a   Andrews, Simeon ^a   Cingolani, Gino ^b   Gonen, Tamir ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

MICROBIO

Indexed keywords

DOUBLE STRANDED DNA; PORTAL PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; BACTERIOPHAGE; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; GENOME ANALYSIS; HYPOTHESIS; MORPHOGENESIS; NONHUMAN; PROTEIN CONFORMATION; VIRUS CAPSID; VIRUS GENOME; VIRUS PATHOGENESIS;

BACTERIOPHAGE P22; BINDING SITES; CAPSID PROTEINS; DNA, VIRAL; GENOME; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; VIRAL TAIL PROTEINS;

DNA VIRUSES; MIRIDAE;

EID: 38949104355     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.11.034     Document Type: Article

References (49)

1. Agirrezabala X., Martin-Benito J., Valle M., Gonzalez J.M., Valencia A., Valpuesta J.M., and Carrascosa J.L. Structure of the connector of bacteriophage T7 at 8 Å resolution: structural homologies of a basic component of a DNA translocating machinery. J. Mol. Biol. 347 (2005) 895-902
2. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
3. Bazinet C., Villafane R., and King J. Novel second-site suppression of a cold-sensitive defect in phage P22 procapsid assembly. J. Mol. Biol. 216 (1990) 701-716
4. Bhardwaj A., Olia A.S., Walker-Kopp N., and Cingolani G. Domain organization and polarity of tail needle gp26 in the portal vertex structure of bacteriophage P22. J. Mol. Biol. 371 (2007) 374-387
5. Casjens S., and Huang W.M. Initiation of sequential packaging of bacteriophage P22 DNA. J. Mol. Biol. 157 (1982) 287-298
6. Chang J., Weigele P., King J., Chiu W., and Jiang W. Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 14 (2006) 1073-1082
7. Chemla Y.R., Aathavan K., Michaelis J., Grimes S., Jardine P.J., Anderson D.L., and Bustamante C. Mechanism of force generation of a viral DNA packaging motor. Cell 122 (2005) 683-692
8. Cingolani G., Petosa C., Weis K., and Muller C.W. Structure of importin-beta bound to the IBB domain of importin-alpha. Nature 399 (1999) 221-229
9. Cingolani G., Lashuel H.A., Gerace L., and Muller C.W. Nuclear import factors importin alpha and importin beta undergo mutually induced conformational changes upon association. FEBS Lett. 484 (2000) 291-298
10. Cingolani G., Moore S.D., Prevelige Jr. P.E., and Johnson J.E. Preliminary crystallographic analysis of the bacteriophage P22 portal protein. J. Struct. Biol. 139 (2002) 46-54
11. De Rosier D.J., and Klug A. Reconstruction of three dimensional structures from electron micrographs. Nature 217 (1968) 130-134
12. Earnshaw W.C., and Harrison S.C. DNA arrangement in isometric phage heads. Nature 268 (1977) 598-602
13. Earnshaw W.C., King J., Harrison S.C., and Eiserling F.A. The structural organization of DNA packaged within the heads of T4 wild-type, isometric, and giant bacteriophages. Cell 14 (1978) 559-568
14. Fotin A., Cheng Y., Sliz P., Grigorieff N., Harrison S.C., Kirchhausen T., and Walz T. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432 (2004) 573-579
15. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., and Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 (1996) 190-199
16. Frishman D., and Argos P. Incorporation of non-local interactions in protein secondary structure prediction from the amino acid sequence. Protein Eng. 9 (1996) 133-142
17. Grigorieff N. FREALIGN: high-resolution refinement of single particle structures. J. Struct. Biol. 157 (2007) 117-125
18. Guasch A., Pous J., Parraga A., Valpuesta J.M., Carrascosa J.L., and Coll M. Crystallographic analysis reveals the 12-fold symmetry of the bacteriophage phi29 connector particle. J. Mol. Biol. 281 (1998) 219-225
19. Israel V. E proteins of bacteriophage P22. I. Identification and ejection from wild-type and defective particles. J. Virol. 23 (1977) 91-97
20. Ivanovska I.L., de Pablo P.J., Ibarra B., Sgalari G., MacKintosh F.C., Carrascosa J.L., Schmidt C.F., and Wuite G.J. Bacteriophage capsids: tough nanoshells with complex elastic properties. Proc. Natl. Acad. Sci. USA 101 (2004) 7600-7605
21. Jackson E.N., Laski F., and Andres C. Bacteriophage P22 mutants that alter the specificity of DNA packaging. J. Mol. Biol. 154 (1982) 551-563
22. Jiang W., Li Z., Zhang Z., Baker M.L., Prevelige Jr. P.E., and Chiu W. Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat. Struct. Biol. 10 (2003) 131-135
23. Johnson J.E., and Chiu W. DNA packaging and delivery machines in tailed bacteriophages. Curr. Opin. Struct. Biol. 17 (2007) 237-243
24. Kleywegt G.J., and Jones T.A. xdlMAPMAN and xdlDATAMAN-programs for reformatting, analysis and manipulation of biomacromolecular electron-density maps and reflection data sets. Acta Crystallogr. D Biol. Crystallogr. 52 (1996) 826-828
25. Knopf C.W. Molecular mechanisms of replication of herpes simplex virus 1. Acta Virol. 44 (2000) 289-307
26. Kobe B. Autoinhibition by an internal nuclear localization signal revealed by the crystal structure of mammalian importin alpha. Nat. Struct. Biol. 6 (1999) 388-397
27. Lander G.C., Tang L., Casjens S.R., Gilcrease E.B., Prevelige P., Poliakov A., Potter C.S., Carragher B., and Johnson J.E. The structure of an infectious p22 virion shows the signal for headful DNA packaging. Science 312 (2006) 1791-1795
28. Lorenzen K., Olia A.S., Uetrecht C., Cingolani G., and Heck A.J.R. Structural effects of gp4 assembly to phage P22 portal protein. J. Mol. Biol. (2008) in press
29. Mettenleiter T.C., Klupp B.G., and Granzow H. Herpesvirus assembly: a tale of two membranes. Curr. Opin. Microbiol. 9 (2006) 423-429
30. Mindell J.A., and Grigorieff N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142 (2003) 334-347
31. Newcomb W.W., Juhas R.M., Thomsen D.R., Homa F.L., Burch A.D., Weller S.K., and Brown J.C. The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J. Virol. 75 (2001) 10923-10932
32. Ohi M., Li Y., Cheng Y., and Walz T. Negative staining and image classification-powerful tools in modern electron microscopy. Biol. Proced. Online 6 (2004) 23-34
33. Olia A.S., Al-Bassam J., Winn-Stapley D.A., Joss L., Casjens S.R., and Cingolani G. Binding-induced stabilization and assembly of the phage P22 tail accessory factor gp4. J. Mol. Biol. 363 (2006) 558-576
34. Orlova E.V., Gowen B., Droge A., Stiege A., Weise F., Lurz R., van Heel M., and Tavares P. Structure of a viral DNA gatekeeper at 10 Å resolution by cryo-electron microscopy. EMBO J. 22 (2003) 1255-1262
35. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
36. Poliakov A., van Duijn E., Lander G., Fu C.Y., Johnson J.E., Prevelige Jr. P.E., and Heck A.J. Macromolecular mass spectrometry and electron microscopy as complementary tools for investigation of the heterogeneity of bacteriophage portal assemblies. J. Struct. Biol. 157 (2007) 371-383
37. Rosenthal P.B., and Henderson R. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333 (2003) 721-745
38. Schiffer M., and Edmundson A.B. Use of helical wheels to represent the structures of proteins and to identify segments with helical potential. Biophys. J. 7 (1967) 121-135
39. Simpson A.A., Tao Y., Leiman P.G., Badasso M.O., He Y., Jardine P.J., Olson N.H., Morais M.C., Grimes S., Anderson D.L., et al. Structure of the bacteriophage phi29 DNA packaging motor. Nature 408 (2000) 745-750
40. Simpson A.A., Leiman P.G., Tao Y., He Y., Badasso M.O., Jardine P.J., Anderson D.L., and Rossmann M.G. Structure determination of the head-tail connector of bacteriophage phi29. Acta Crystallogr. D Biol. Crystallogr. 57 (2001) 1260-1269
41. Steven A.C., Trus B.L., Booy F.P., Cheng N., Zlotnick A., Caston J.R., and Conway J.F. The making and breaking of symmetry in virus capsid assembly: glimpses of capsid biology from cryoelectron microscopy. FASEB J. 11 (1997) 733-742
42. Stewart P.L., Chiu C.Y., Haley D.A., Kong L.B., and Schlessman J.L. Review: resolution issues in single-particle reconstruction. J. Struct. Biol. 128 (1999) 58-64
43. Strauss H., and King J. Steps in the stabilization of newly packaged DNA during phage P22 morphogenesis. J. Mol. Biol. 172 (1984) 523-543
44. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
45. Thuman-Commike P.A., Greene B., Jakana J., Prasad B.V., King J., Prevelige Jr. P.E., and Chiu W. Three-dimensional structure of scaffolding-containing phage p22 procapsids by electron cryo-microscopy. J. Mol. Biol. 260 (1996) 85-98
46. Trus B.L., Cheng N., Newcomb W.W., Homa F.L., Brown J.C., and Steven A.C. Structure and polymorphism of the UL6 portal protein of herpes simplex virus type 1. J. Virol. 78 (2004) 12668-12671
47. Ye X., Gorin A., Ellington A.D., and Patel D.J. Deep penetration of an alpha-helix into a widened RNA major groove in the HIV-1 rev peptide-RNA aptamer complex. Nat. Struct. Biol. 3 (1996) 1026-1033
48. Ye X., Gorin A., Frederick R., Hu W., Majumdar A., Xu W., McLendon G., Ellington A., and Patel D.J. RNA architecture dictates the conformations of a bound peptide. Chem. Biol. 6 (1999) 657-669
49. Zhang Z., Greene B., Thuman-Commike P.A., Jakana J., Prevelige Jr. P.E., King J., and Chiu W. Visualization of the maturation transition in bacteriophage P22 by electron cryomicroscopy. J. Mol. Biol. 297 (2000) 615-626