Maturation dynamics of a viral capsid: Visualization of transitional intermediate states

Cell

Volumn 100, Issue 2, 2000, Pages 253-263

  Lata, Ramani ^a   Conway, James F ^a,e   Cheng, Naiqian ^a   Duda, Robert L ^b   Hendrix, Roger W ^b   Wikoff, William R ^c   Johnson, John E ^c   Tsuruta, Hiro ^d   Steven, Alasdair C ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d STANFORD UNIVERSITY   (United States)

^e INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN;

ARTICLE; CELL MATURATION; CRYOELECTRON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN POLYMERIZATION; VIROGENESIS; VIRUS CAPSID; X RAY DIFFRACTION;

MIRIDAE; UNIDENTIFIED BACTERIOPHAGE;

EID: 0034695668     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81563-9     Document Type: Article

References (46)

1. Baker, T.S., and Cheng, R.H. (1996). A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J. Struct. Biol. 116, 120-130.
2. Bayer, M.E., and Bocharov, A.F. (1973). The capsid structure of bacteriophage lambda. Virology 54, 465-475.
3. Belnap, D.M., Olson, N.H., and Baker, T.S. (1997). A method for establishing the handedness of biological macromolecules. J. Struct. Biol. 120, 44-51.
4. Berriman, J., and Unwin, N. (1994). Analysis of transient structures by cryo-microscopy combined with rapid mixing of spray droplets. Ultramicroscopy 56, 241-252.
5. Butcher, S.J., Dokland, T., Ojala, P.M., Bamford, D.H., and Fuller, S.D. (1997). Intermediates in the assembly pathway of the double- Stranded RNA virus phi6. EMBO J. 16, 4477-4487.
6. Conway, J.F., and Steven, A.C. (1999). Methods for reconstructing density maps of "single particles" from cryoelectron micrographs to subnanometer resolution. J. Struct. Biol. 128, 106-118.
7. Conway, J.F., Duda, R.L., Cheng, N., Hendrix, R.W., and Steven, A.C. (1995). Proteolytic and conformational control of virus capsid maturation: The bacteriophage HK97 system. J. Mol. Biol. 253, 86-99.
8. Conway, J.F., Cheng, N., Zlotnick, A., Wingfield, P.T., Stahl, S.J., and Steven, A.C. (1997). Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy. Nature 386, 91-94.
9. Cooke, R. (1995). The actomyosin engine. FASEB J. 9, 636-642.
10. Dokland, T., and Murialdo, H. (1993). Structural transitions during maturation of bacteriophage lambda capsids. J. Mol. Biol. 233, 682-694.
11. Duda, R.L. (1998). Protein chainmail: Catenated protein in viral capsids. Cell 94, 55-60.
12. Duda, R.L., Hempel, J., Michel, H., Shabanowitz, J., Hunt, D., and Hendrix, R.W. (1995a). Structural transitions during bacteriophage HK97 head assembly. J. Mol. Biol. 247, 618-635.
13. Duda, R.L., Martincic, K., and Hendrix, R.W. (1995b). Genetic basis of bacteriophage HK97 prohead assembly. J. Mol. Biol. 247, 636-647.
14. Flynn, D.L., Abood, N.A., and Holwerda, B.C. (1997). Recent advances in antiviral research: Identification of inhibitors of the herpesvirus proteases. Curr. Opin. Chem. Biol. 1, 190-196.
15. Fuller, S.D., Butcher, S.J., Cheng, R.H., and Baker, T.S. (1996). Three-dimensional reconstruction of icosahedral particles - The uncommon line. J. Struct. Biol. 116, 48-55.
16. Fuller, S.D., Wilk, T., Gowen, B.E., Krausslich, H.G., and Vogt, V.M. (1997). Cryo-electron microscopy reveals ordered domains in the immature HIV-1 particle. Curr. Biol. 7, 729-738.
17. Galisteo, M.L., and King, J. (1993). Conformational transformations in the protein lattice of phage P22 procapsids. Biophys. J. 65, 227-235.
18. Hendrix, R.W., and Duda, R.L. (1998). Bacteriophage HK97 head assembly: A protein ballet. Adv. Virus Res. 50, 235-288.
19. Hohn, B. (1983). DNA sequences necessary for packaging of bacteriophage lambda DNA. Proc. Natl. Acad. Sci. USA 80, 7456-7460.
20. Jardine, P.J., and Coombs, D.H. (1998). Capsid expansion follows the initiation of DNA packaging in bacteriophage T4. J. Mol. Biol. 284, 661-672.
21. King, J., and Chiu, W. (1997). The procapsid-to-capsid transition in double-stranded DNA bacteriophages. In Structural Biology of Viruses, W. Chiu, R.M. Burnett, and R. Garcea, eds. (New York: Oxford University Press), pp. 288-311.
22. Müller, M., Mesyanzhinov, V., and Aebi, U. (1994). In vitro maturation of prehead-like bacteriophage T4 polyheads: Structural changes accompanying proteolytic cleavage and lattice expansion. J. Struct. Biol. 112, 199-215.
23. Nermut, M.V., Hockley, D.J., Bron, P., Thomas, D., Zhang, W.H., and Jones, I.M. (1998). Further evidence for hexagonal organization of HIV gag protein in prebudding assemblies and immature virus-like particles. J. Struct. Biol. 123, 143-149.
24. Newcomb, W.W., Homa, F.L., Booy, F.P., Thomsen, D.R., Trus, B.L., Steven, A.C., Spencer, J.V., and Brown, J.C. (1996). Assembly of the herpes simplex virus capsid: Characterization of intermediates observed during cell-free capsid formation. J. Mol. Biol. 263, 432-446.
25. Prasad, B.V.V., Prevelige, P.E., Marietta, E., Chen, R.O., Thomas, D., King, J., and Chiu, W. (1993). Three-dimensional transformation of capsids associated with genome packaging in a bacterial virus. J. Mol. Biol. 231, 65-74.
26. Saxton, W.O., and Baumeister, W. (1982). The correlation averaging of a regularly arranged bacterial cell envelope protein. J. Microsc. 127, 127-138.
27. Serwer, P., and Pichler, M.E. (1978). Electrophoresis of bacteriophage T7 and T7 capsids in agarose gels. J. Virol. 28, 917-928.
28. Shibata, H., Fujisawa, H., and Minagawa, T. (1987). Characterization of the bacteriophage T3 DNA packaging reaction in vitro in a defined system. J. Mol. Biol. 196, 845-851.
29. Steven, A.C., and Carrascosa, J.L. (1979). Proteolytic cleavage and structural transformation: Their relationship in bacteriophage T4 capsid maturation. J. Supramol. Struct. 10, 1-11.
30. Steven, A.C., Greenstone, H., Bauer, A.C., and Williams, R.W. (1990). The maturation-dependent conformational change of the major capsid protein of bacteriophage T4 involves a substantial change in secondary structure. Biochemistry 29, 5556-5561.
31. Steven, A.C., Greenstone, H.L., Booy, F.P., Black, L.W., and Ross, P.D. (1992). Conformational changes of a viral capsid protein: Thermodynamic rationale for proteolytic regulation of bacteriophage T4 capsid expansion, cooperativity, and super-stabilization by soc binding. J. Mol. Biol. 228, 870-884.
32. Tao, Y., Olson, N.H., Xu, W., Anderson, D.L., Rossmann, M.G., and Baker, T.S. (1998). Assembly of a tailed bacterial virus and its genome release studied in three dimensions. Cell 95, 431-437.
33. Trus, B.L., Booy, F.P., Newcomb, W.W., Brown, J.C., Homa, F.L., Thomsen, D.R., and Steven, A.C. (1996). The herpes simplex virus procapsid: Structure, conformational changes upon maturation, and roles of the triplex proteins VP19c and VP23 in assembly. J. Mol. Biol. 263, 447-462.
34. Trus, B.L., Roden, R.B.S., Greenstone, H.L., Schiller, J.T., and Booy, F. P. (1997). Novel structural features of bovine papillomavirus capsid revealed by a three dimensional reconstruction to 9Å resolution. Nat. Struct. Biol. 4, 413-420.
35. Tsuruta, H., Brennan, S., Rek, Z.U., Irving, T.C., Tompkins, W.H., and Hodgson, K.O. (1998). A wide-bandpass multilayer monochromator for biological small-angle scattering and fiber diffraction studies. J. Appl. Crystallogr. 31, 672-682.
36. Tuma, R., Prevelige, P.E., Jr., and Thomas, G.J., Jr. (1996). Structural transitions in the scaffolding and coat proteins of P22 virus during assembly and disassembly. Biochemistry 35, 4619-4627.
37. Tuma, R., Prevelige, P.E., Jr., and Thomas, G.J., Jr. (1998). Mechanism of capsid maturation in a double-stranded DNA virus. Proc. Natl. Acad. Sci. USA 95, 9885-9890.
38. Valpuesta, J.M., and Carrascosa, J.L. (1994). Structure of viral connectors and their function in bacteriophage assembly and DNA packaging. Q. Rev. Biophys. 27, 107-155.
39. Walker, M., Trinick, J., and White, H. (1995). Millisecond time resolution electron cryo-microscopy of the M-ATP transient kinetic state of the acto-myosin ATPase. Biophys. J. 68, 87S-91S.
40. White, H.E., Chen, S., Roseman, A.M., Yifrach, O., Horovitz, A., and Saibil, H.R. (1997). Structural basis of allosteric changes in the GroEl mutant Arg197 → Ala. Nat. Struct. Biol. 4, 690-694.
41. Wikoff, W.R., Duda, R.L., Hendrix, R.W., and Johnson, J.E. (1998). Crystallization and preliminary x-ray analysis of the dsDNA bacteriophage HK97 mature empty capsid. Virology 243, 113-118.
42. Wikoff, W.R., Duda, R.L., Hendrix, R.W., and Johnson, J.E. (1999). Crystallographic analysis of the dsDNA bacteriophage HK97 mature empty capsid. Acta Crystallogr. D 55, 763-771.
43. Wlodawer, A., and Erickson, J.W. (1993). Structure-based inhibitors of HIV-1 protease. Annu. Rev. Biochem. 62, 543-585.
44. Xie, Z., and Hendrix, R.W. (1995). Assembly in vitro of bacteriophage HK97 proheads. J. Mol. Biol. 253, 74-85.
45. Yeager, M., Wilson-Kubalek, E.M., Weiner, S.G., Brown, P.O., and Rein, A. (1998). Supramolecular organization of immature and mature murine leukemia virus revealed by electron cryo-microscopy: Implications for retroviral assembly mechanisms. Proc. Natl. Acad. Sci. USA 95, 7299-7304.
46. Zlotnick, A., Cheng, N., Conway, J.F., Booy, F.P., Steven, A.C., Stahl, S.J., and Wingfield, P.T. (1996). Dimorphism of hepatitis B virus capsids is strongly influenced by the C-terminus of the capsid protein. Biochemistry 35, 7412-7421.