Cryo-electron tomography of bacteriophage φ6 procapsids shows random occupancy of the binding sites for RNA polymerase and packaging NTPase

Journal of Structural Biology

Volumn 171, Issue 3, 2010, Pages 389-396

  Nemecek, Daniel ^a   Heymann, J Bernard ^a   Qiao, Jian ^b   Mindich, Leonard ^b   Steven, Alasdair C ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Cystovirus; Electron cryo tomography; Packaging motor; Procapsid; RNA dependent RNA polymerase

Indexed keywords

RNA DIRECTED RNA POLYMERASE; DNA DIRECTED RNA POLYMERASE; NUCLEOSIDE TRIPHOSPHATASE;

ARTICLE; BACTERIOPHAGE; BINDING SITE; BINOMIAL DISTRIBUTION; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; RNA PROCESSING; STOICHIOMETRY; VIRUS CAPSID; ELECTRON TOMOGRAPHY; METABOLISM; PSEUDOMONAS PHAGE PHI6; ULTRASTRUCTURE;

CYSTOVIRUS; PSEUDOMONAS PHAGE PHI-6;

BACTERIOPHAGE PHI 6; BINDING SITES; CAPSID; CRYOELECTRON MICROSCOPY; DNA-DIRECTED RNA POLYMERASES; ELECTRON MICROSCOPE TOMOGRAPHY; NUCLEOSIDE-TRIPHOSPHATASE;

EID: 77955085566     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2010.06.005     Document Type: Article

References (27)

1. Butcher S.J., Dokland T., Ojala P.M., Bamford D.H., Fuller S.D. Intermediates in the assembly pathway of the double-stranded RNA virus phi6. EMBO J. 1997, 16:4477-4487.
2. Butcher S.J., Grimes J.M., Makeyev E.V., Bamford D.H., Stuart D.I. A mechanism for initiating RNA-dependent RNA polymerization. Nature 2001, 410:235-240.
3. Cardone G., Grunewald K., Steven A.C. A resolution criterion for electron tomography based on cross-validation. J. Struct. Biol. 2005, 151:117-129.
4. Day L.A., Mindich L. The molecular weight of bacteriophage phi6 and its nucleocapsid. Virology 1980, 103:376-385.
5. de Haas F., Paatero A.O., Mindich L., Bamford D.H., Fuller S.D. A symmetry mismatch at the site of RNA packaging in the polymerase complex of dsRNA bacteriophage phi6. J. Mol. Biol. 1999, 294:357-372.
6. Frangakis A.S., Hegerl R. Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J. Struct. Biol. 2001, 135:239-250.
7. Fu C.Y., Prevelige P.E. In vitro incorporation of the phage Phi29 connector complex. Virology 2009, 394:149-153.
8. Harris A., Cardone G., Winkler D.C., Heymann J.B., Brecher M., White J.M., Steven A.C. Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc. Natl. Acad. Sci. USA 2006, 103:19123-19127.
9. Heymann J.B., Cardone G., Winkler D.C., Steven A.C. Computational resources for cryo-electron tomography in Bsoft. J. Struct. Biol. 2008, 161:232-242.
10. Huiskonen J.T., de Haas F., Bubeck D., Bamford D.H., Fuller S.D., Butcher S.J. Structure of the bacteriophage phi6 nucleocapsid suggests a mechanism for sequential RNA packaging. Structure 2006, 14:1039-1048.
11. Huiskonen J.T., Jaalinoja H.T., Briggs J.A., Fuller S.D., Butcher S.J. Structure of a hexameric RNA packaging motor in a viral polymerase complex. J. Struct. Biol. 2007, 158:156-164.
12. Juuti J.T., Bamford D.H. RNA binding, packaging and polymerase activities of the different incomplete polymerase complex particles of dsRNA bacteriophage φ6. J. Mol. Biol. 1995, 249:545-554.
13. Juuti J.T., Bamford D.H., Tuma R., Thomas G.J. Structure and NTPase activity of the RNA-translocating protein (P4) of bacteriophage phi6. J. Mol. Biol. 1998, 279:347-359.
14. Mastronarde D.N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 2005, 152:36-51.
15. Mindich L. Precise packaging of the three genomic segments of the double-stranded-RNA bacteriophage phi6. Microbiol. Mol. Biol. Rev. 1999, 63:149-160.
16. Newcomb W.W., Homa F.L., Brown J.C. Involvement of the portal at an early step in herpes simplex virus capsid assembly. J. Virol. 2005, 79:10540-10546.
17. Olkkonen V.M., Gottlieb P., Strassman J., Qiao X.Y., Bamford D.H., Mindich L. In vitro assembly of infectious nucleocapsids of bacteriophage phi6: formation of a recombinant double-stranded RNA virus. Proc. Natl. Acad. Sci. USA 1990, 87:9173-9177.
18. Patton J.T., Spencer E. Genome replication and packaging of segmented double-stranded RNA viruses. Virology 2000, 277:217-225.
19. Pirttimaa M.J., Paatero A.O., Frilander M.J., Bamford D.H. Nonspecific nucleoside triphosphatase P4 of double-stranded RNA bacteriophage phi6 is required for single-stranded RNA packaging and transcription. J. Virol. 2002, 76:10122-10127.
20. Press W.H., Teukolsky S.A., Vetterling W.T., Flannery B.P. Confidence Limits on Estimated Model Parameters. Numerical Recipes in C: The Art of Scientific Computing 2002, Cambridge University Press, New York, pp. 689-699.
21. Press W.H., Teukolsky S.A., Vetterling W.T., Flannery B.P. Downhill Simplex Method in Multidimensions. Numerical Recipes in C: The Art of Scientific Computing 2002, Cambridge University Press, New York, pp. 408-412.
22. Qiao X., Qiao J., Mindich L. Stoichiometric packaging of the three genomic segments of double-stranded RNA bacteriophage phi6. Proc. Natl. Acad. Sci. USA 1997, 94:4074-4079.
23. Richards F.M. The interpretation of protein structures: total volume, group volume distributions and packing density. J. Mol. Biol. 1974, 82:1-14.
24. Sen A., Heymann J.B., Cheng N., Qiao J., Mindich L., Steven A.C. Initial location of the RNA-dependent RNA polymerase in the bacteriophage Phi6 procapsid determined by cryo-electron microscopy. J. Biol. Chem. 2008, 283:12227-12231.
25. Sokal R.R., Rohlf F.J. Biometry: The Principles and Practice of Statistics in Biological Research 1994, Freeman, New York. third ed.
26. Trus B.L., Newcomb W.W., Cheng N., Cardone G., Marekov L., Homa F.L., Brown J.C., Steven A.C. Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-filled HSV-1 capsids. Mol. Cell 2007, 26:479-489.
27. Wei H., Cheng R.H., Berriman J., Rice W.J., Stokes D.L., Katz A., Morgan D.G., Gottlieb P. Three-dimensional structure of the enveloped bacteriophage phi12: an incomplete T=13 lattice is superposed on an enclosed T=1 shell. PLoS One 2009, 4:e6850.