Capsid Conformational Sampling in HK97 Maturation Visualized by X-Ray Crystallography and Cryo-EM

Structure

Volumn 14, Issue 11, 2006, Pages 1655-1665

  Gan, Lu ^a,f   Speir, Jeffrey A ^a   Conway, James F ^b   Lander, Gabriel ^a   Cheng, Naiqian ^c   Firek, Brian A ^d   Hendrix, Roger W ^d   Duda, Robert L ^d   Liljas, Lars ^e   Johnson, John E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

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

^d UNIVERSITY OF PITTSBURGH   (United States)

^e UPPSALA UNIVERSITY   (Sweden)

^f CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIOPHAGE; CROSS LINKING; CRYOELECTRON MICROSCOPY; MATURATION; MUTANT; NONHUMAN; PH; PRIORITY JOURNAL; VIRUS CAPSID; X RAY CRYSTALLOGRAPHY;

BACTERIOPHAGE LAMBDA; CAPSID; CROSS-LINKING REAGENTS; CRYOELECTRON MICROSCOPY; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; ELECTRONS; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR STRUCTURE; PROTEIN CONFORMATION; PROTEIN FOLDING; VIRUS ASSEMBLY;

MIRIDAE;

EID: 33846262040     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2006.09.006     Document Type: Article

References (34)

1. Alberts B. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92 (1998) 291-294
2. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
3. CCP4 (Collaborative Computational Project, Number 4). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50 (1994) 760-763
4. Conway J.F., Duda R.L., Cheng N., Hendrix R.W., and Steven A.C. Proteolytic and conformational control of virus capsid maturation: the bacteriophage HK97 system. J. Mol. Biol. 253 (1995) 86-99
5. Conway J.F., Wikoff W.R., Cheng N., Duda R.L., Hendrix R.W., Johnson J.E., and Steven A.C. Virus maturation involving large subunit rotations and local refolding. Science 292 (2001) 744-748
6. DeLano, W.L. (2002). The PyMOL Molecular Graphics System (http://www.pymol.org).
7. Duda R.L. Protein chainmail: catenated protein in viral capsids. Cell 94 (1998) 55-60
8. Duda R.L., Hempel J., Michel H., Shabanowitz J., Hunt D., and Hendrix R.W. Structural transitions during bacteriophage HK97 head assembly. J. Mol. Biol. 247 (1995) 618-635
9. Duda R.L., Martincic K., and Hendrix R.W. Genetic basis of bacteriophage HK97 prohead assembly. J. Mol. Biol. 247 (1995) 636-647
10. Fabry C.M., Rosa-Calatrava M., Conway J.F., Zubieta C., Cusack S., Ruigrok R.W., and Schoehn G. A quasi-atomic model of human adenovirus type 5 capsid. EMBO J. (2005) 1645-1654
11. Gan, L. (2006). Conformational and covalent control of bacteriophage HK97 capsid expansion. PhD thesis, The Scripps Research Institute, La Jolla, California.
12. Gan L., Conway J.F., Firek B.A., Cheng N., Hendrix R.W., Steven A.C., Johnson J.E., and Duda R.L. Control of crosslinking by quaternary structure changes during bacteriophage HK97 maturation. Mol. Cell 14 (2004) 559-569
13. Helgstrand C., Wikoff W.R., Duda R.L., Hendrix R.W., Johnson J.E., and Liljas L. The refined structure of a protein catenane: the HK97 bacteriophage capsid at 3.44 Å resolution. J. Mol. Biol. 334 (2003) 885-899
14. Jones T.A., Bergdoll M., and Kjeldgaard M. O: a macromolecular modeling environment. In: Ealick C.B.S. (Ed). Crystallographic and Modeling Methods in Molecular Design (1990), Springer-Verlag Press, New York 189-195
15. Kim M.K., Jernigan R.L., and Chirikjian G.S. An elastic network model of HK97 capsid maturation. J. Struct. Biol. 143 (2003) 107-117
16. Kleywegt G.J., and Jones T.A. Halloween. Masks and bones. In: Bailey S., Hubbard R., and Waller D. (Eds). From First Map to Final Model (1994), SERC Daresbury Laboratory, Warrington, UK 59-66
17. Korostelev A., Bertram R., and Chapman M.S. Simulated-annealing real-space refinement as a tool in model building. Acta Crystallogr. D Biol. Crystallogr. 58 (2002) 761-767
18. Laskowski R.A., Moss D.S., and Thornton J.M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231 (1993) 1049-1067
19. Lata R., Conway J.F., Cheng N., Duda R.L., Hendrix R.W., Wikoff W.R., Johnson J.E., Tsuruta H., and Steven A.C. Maturation dynamics of a viral capsid: visualization of transitional intermediate states. Cell 100 (2000) 253-263
20. Lee K.K., Gan L., Tsuruta H., Hendrix R.W., Duda R.L., and Johnson J.E. Evidence that a local refolding event triggers maturation of HK97 bacteriophage capsid. J. Mol. Biol. 340 (2004) 419-433
21. Lee K.K., Tsuruta H., Hendrix R.W., Duda R.L., and Johnson J.E. Cooperative reorganization of a 420 subunit virus capsid. J. Mol. Biol. 352 (2005) 723-735
22. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr. A 276 (1997) 307-326
23. 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
24. Rader A.J., Vlad D.H., and Bahar I. Maturation dynamics of bacteriophage HK97 capsid. Structure 13 (2005) 413-421
25. Reddy V.S., Natarajan P., Okerberg B., Li K., Damodaran K.V., Morton R.T., Brooks III C.L., and Johnson J.E. Virus Particle Explorer (VIPER), a website for virus capsid structures and their computational analyses. J. Virol. 75 (2001) 11943-11947
26. Ross P.D., Cheng N., Conway J.F., Firek B.A., Hendrix R.W., Duda R.L., and Steven A.C. Crosslinking renders bacteriophage HK97 capsid maturation irreversible and effects an essential stabilization. EMBO J. 24 (2005) 1352-1363
27. Steven A.C., Heymann J.B., Cheng N., Trus B.L., and Conway J.F. Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity. Curr. Opin. Struct. Biol. 15 (2005) 227-236
28. Tama F., and Brooks III C.L. Diversity and identity of mechanical properties of icosahedral viral capsids studied with elastic network normal mode analysis. J. Mol. Biol. 345 (2005) 299-314
29. Teschke C.M., McGough A., and Thuman-Commike P.A. Penton release from P22 heat-expanded capsids suggests importance of stabilizing penton-hexon interactions during capsid maturation. Biophys. J. 84 (2003) 2585-2592
30. Tong L., and Rossmann M.G. The locked rotation function. Acta Crystallogr. A 46 (1990) 783-792
31. Tong L., and Rossmann M.G. Rotation function calculations with GLRF program. Methods Enzymol. 276 (1997) 594-611
32. Wikoff W.R., Liljas L., Duda R.L., Tsuruta H., Hendrix R.W., and Johnson J.E. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289 (2000) 2129-2133
33. Wikoff W.R., Conway J.F., Tang J., Lee K.K., Gan L., Cheng N., Duda R.L., Hendrix R.W., Steven A.C., and Johnson J.E. Time-resolved molecular dynamics of bacteriophage HK97 capsid maturation interpreted by electron cryo-microscopy and X-ray crystallography. J. Struct. Biol. 153 (2006) 300-306
34. Xie Z., and Hendrix R.W. Assembly in vitro of bacteriophage HK97 proheads. J. Mol. Biol. 253 (1995) 74-85