Exploiting radiation damage to map proteins in nucleoprotein complexes: The internal structure of bacteriophage T7

Journal of Structural Biology

Volumn 185, Issue 3, 2014, Pages 250-256

  Cheng, Naiqian ^a   Wu, Weimin ^a   Watts, Norman R ^a   Steven, Alasdair C ^a  

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

Author keywords

3 dimensional image reconstruction; Cryo electron microscopy; Differential mass mapping; DNA ejection; Nucleocapsid structure; Radiation biology

Indexed keywords

3-DIMENSIONAL IMAGE RECONSTRUCTION; CRYO-ELECTRON MICROSCOPY; DIFFERENTIAL MASS MAPPING; DNA EJECTION; NUCLEOCAPSID STRUCTURE; RADIATION BIOLOGY;

BACTERIOPHAGE T7; CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; NUCLEOPROTEINS;

EID: 84894484537     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2013.12.004     Document Type: Article

References (42)

1. Agirrezabala X., Martin-Benito J., Caston J.R., Miranda R., Valpuesta J.M., et al. Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J. 2005, 24:3820-3829.
2. Agirrezabala X., Martin-Benito J., Valle M., Gonzalez J.M., Valencia A., et al. Structure of the connector of bacteriophage T7 at 8Å resolution: structural homologies of a basic component of a DNA translocating machinery. J. Mol. Biol. 2005, 347:895-902.
3. Al-Bassam J., Ozer R.S., Safer D., Halpain S., Milligan R.A. MAP2 and tau bind longitudinally along the outer ridges of microtubule protofilaments. J. Cell Biol. 2002, 157:1187-1196.
4. Baker L.A., Rubinstein J.L. Radiation damage in electron cryomicroscopy. Methods Enzymol. 2010, 481:371-388.
5. Bammes B.E., Jakana J., Schmid M.F., Chiu W. Radiation damage effects at four specimen temperatures from 4 to 100K. J. Struct. Biol. 2010, 169:331-341.
6. Black L.W. DNA packaging in dsDNA bacteriophages. Annu. Rev. Microbiol. 1989, 43:267-292.
7. Black L.W., Thomas J.A. Condensed genome structure. Viral Molecular Machines 2011, 466-489. Springer, New York. M.G. Rossmann, V. Rao (Eds.).
8. Carrascosa J.L., Steven A.C. A procedure for evaluation of significant structural differences between related arrays of protein molecules. Micron 1978, 9:199-206.
9. Cerritelli M.E., Studier F.W. Assembly of T7 capsids from independently expressed and purified head protein and scaffolding protein. J. Mol. Biol. 1996, 258:286-298.
10. Cerritelli M.E., Conway J.F., Cheng N., Trus B.L., Steven A.C. Molecular mechanisms in bacteriophage T7 procapsid assembly, maturation, and DNA containment. Adv. Protein Chem. 2003, 64:301-323.
11. Cerritelli M.E., Cheng N., Rosenberg A.H., McPherson C.E., Booy F.P., et al. Encapsidated conformation of bacteriophage T7 DNA. Cell 1997, 91:271-280.
12. Cerritelli M.E., Trus B.L., Smith C.S., Cheng N., Conway J.F., et al. A second symmetry mismatch at the portal vertex of bacteriophage T7: 8-fold symmetry in the procapsid core. J. Mol. Biol. 2003, 327:1-6.
13. Cheng N., Conway J.F., Watts N.R., Hainfeld J.F., Joshi V., et al. Tetrairidium, a four-atom cluster, is readily visible as a density label in three-dimensional cryo-EM maps of proteins at 10-25Å resolution. J. Struct. Biol. 1999, 127:169-176.
14. Conway J.F., Trus B.L., Booy F.P., Newcomb W.W., Brown J.C., et al. The effects of radiation damage on the structure of frozen hydrated HSV-1 capsids. J. Struct. Biol. 1993, 111:222-233.
15. Conway J.F., Cockrell S.K., Copeland A.M., Newcomb W.W., Brown J.C., et al. Labeling and localization of the herpes simplex virus capsid protein UL25 and its interaction with the two triplexes closest to the penton. J. Mol. Biol. 2010, 397:575-586.
16. Cuervo A., Pulido-Cid M., Chagoyen M., Arranz R., Gonzalez-Garcia V.A., et al. Structural characterization of the bacteriophage T7 tail machinery. J. Biol. Chem. 2013, 288:26290-26299.
17. Dokland T. Scaffolding proteins and their role in viral assembly. Cell. Mol. Life Sci. 1999, 56:580-603.
18. Dubochet J., Adrian M., Chang J.J., Homo J.C., Lepault J., et al. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 1988, 21:129-228.
19. Fokine A., Battisti A.J., Bowman V.D., Efimov A.V., Kurochkina L.P., et al. Cryo-EM study of the Pseudomonas bacteriophage phiKZ. Structure 2007, 15:1099-1104.
20. Garman E.F., Weik M. Radiation damage to biological macromolecules: some answers and more questions. J. Synchrotron Radiat. 2013, 20:1-6.
21. Glaeser R.M. Retrospective: radiation damage and its associated "information limitations". J. Struct. Biol. 2008, 163:271-276.
22. Guo F., Liu Z., Vago F., Ren Y., Wu W., et al. Visualization of uncorrelated, tandem symmetry mismatches in the internal genome packaging apparatus of bacteriophage T7. Proc. Natl. Acad. Sci. USA 2013, 110:6811-6816.
23. Hartman P.S., Eisenstark A., Pauw P.G. Inactivation of phage T7 by near-ultraviolet radiation plus hydrogen peroxide: DNA-protein crosslinks prevent DNA injection. Proc. Natl. Acad. Sci. USA 1979, 76:3228-3232.
24. Hauser R., Blasche S., Dokland T., Haggard-Ljungquist E., von Brunn A., et al. Bacteriophage protein-protein interactions. Adv. Virus Res. 2012, 83:219-298.
25. Hu B., Margolin W., Molineux I.J., Liu J. The bacteriophage T7 virion undergoes extensive structural remodeling during infection. Science 2013, 339:576-579.
26. Iancu C.V., Wright E.R., Heymann J.B., Jensen G.J. A comparison of liquid nitrogen and liquid helium as cryogens for electron cryotomography. J. Struct. Biol. 2006, 153:231-240.
27. Ionel A., Velazquez-Muriel J.A., Luque D., Cuervo A., Caston J.R., et al. Molecular rearrangements involved in the capsid shell maturation of bacteriophage T7. J. Biol. Chem. 2011, 286:234-242.
28. Kemp P., Garcia L.R., Molineux I.J. Changes in bacteriophage T7 virion structure at the initiation of infection. Virology 2005, 340:307-317.
29. Kocsis E., Cerritelli M.E., Trus B.L., Cheng N., Steven A.C. Improved methods for determination of rotational symmetries in macromolecules. Ultramicroscopy 1995, 60:219-228.
30. Leapman R.D., Sun S. Cryo-electron energy loss spectroscopy: observations on vitrified hydrated specimens and radiation damage. Ultramicroscopy 1995, 59:71-79.
31. Ludtke S.J., Baldwin P.R., Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 1999, 128:82-97.
32. Meents A., Gutmann S., Wagner A., Schulze-Briese C. Origin and temperature dependence of radiation damage in biological samples at cryogenic temperatures. Proc. Nat. Acad. Sci. USA 2010, 107:1094-1099.
33. Newcomb W.W., Trus B.L., Booy F.P., Steven A.C., Wall J.S., et al. Structure of the herpes simplex virus capsid: molecular composition of the pentons and triplexes. J. Mol. Biol. 1993, 232:499-511.
34. Roeder G.S., Sadowski P.D. Bacteriophage T7 morphogenesis: phage-related particles in cells infected with wild-type and mutant T7 phage. Virology 1977, 76:263-285.
35. Serwer P. Internal proteins of bacteriophage T7. J. Mol. Biol. 1976, 10:271-291.
36. Steven A.C., Trus B.L. The structure of bacteriophage T7. Electron Microscopy of Proteins 1986, 1-35. Academic Press, London. J.R. Harris, R.W. Horne (Eds.).
37. Steven A.C., Conway J.F., Cheng N., Watts N.R., Belnap D.M., et al. Structure, assembly, and antigenicity of hepatitis B virus capsid proteins. Adv. Virus Res. 2005, 64:127-165.
38. Tang G., Peng L., Baldwin P.R., Mann D.S., Jiang W., et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 2007, 157:38-46.
39. Thomas J.A., Weintraub S.T., Wu W., Winkler D.C., Cheng N., et al. Extensive proteolysis of head and inner body proteins by a morphogenetic protease in the giant Pseudomonas aeruginosa phage phiKZ. Mol. Microbiol. 2012, 84:324-339.
40. Wang G.J., Porta C., Chen Z.G., Baker T.S., Johnson J.E. Identification of a Fab interaction footprint site on an icosahedral virus by cryoelectron microscopy and X-ray crystallography. Nature 1992, 355:275-278.
41. Wu W., Thomas J.A., Cheng N., Black L.W., Steven A.C. Bubblegrams reveal the inner body of bacteriophage phiKZ. Science 2012, 335:182.
42. Wu W., Chen Z., Cheng N., Watts N.R., Stahl S.J., et al. Specificity of an anti-capsid antibody associated with Hepatitis B virus-related acute liver failure. J. Struct. Biol. 2013, 181:53-60.