P22 Coat Protein Structures Reveal a Novel Mechanism for Capsid Maturation: Stability without Auxiliary Proteins or Chemical Crosslinks

Structure

Volumn 18, Issue 3, 2010, Pages 390-401

  Parent, Kristin N ^a   Khayat, Reza ^b   Tu, Long H ^c   Suhanovsky, Margaret M ^c   Cortines, Juliana R ^c   Teschke, Carolyn M ^c   Johnson, John E ^b   Baker, Timothy S ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

MICROBIO; PROTEINS

Indexed keywords

AUXILIARY PROTEIN; CAPSID PROTEIN; COAT PROTEIN; MONOMER; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE LAMBDA; BACTERIOPHAGE MU; BACTERIOPHAGE P22; BACTERIOPHAGE T4; BIOLOGICAL MODEL; CONTROLLED STUDY; CROSS LINKING; HERPES VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; VIRUS CAPSID;

AMINO ACID SEQUENCE; BACTERIOPHAGE P22; CAPSID; CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; VIRUS ASSEMBLY;

HERPESVIRIDAE; HUMAN HERPESVIRUS 1; MIRIDAE;

EID: 77649128082     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2009.12.014     Document Type: Article

References (65)

1. Agirrezabala X., Martin-Benito J., Caston J.R., Miranda R., Valpuesta J.M., and Carrascosa J.L. Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J. 24 (2005) 3820-3829
2. Agirrezabala X., Velazquez-Muriel J.A., Gomez-Puertas P., Scheres S.H., Carazo J.M., and Carrascosa J.L. Quasi-atomic model of bacteriophage t7 procapsid shell: insights into the structure and evolution of a basic fold. Structure 15 (2007) 461-472
3. Baker T.S., Olson N.H., and Fuller S.D. Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Microbiol. Mol. Biol. Rev. 63 (1999) 862-922
4. Baker M.L., Jiang W., Rixon F.J., and Chiu W. Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 79 (2005) 14967-14970
5. Bamford D.H., Grimes J.M., and Stuart D.I. What does structure tell us about virus evolution?. Curr. Opin. Struct. Biol. 15 (2005) 655-663
6. Bazinet C., Benbaset J., King J., Carazo J.M., and Carrascosa J.L. Purification and organization of the gene 1 portal protein required for phage P22 DNA packaging. Biochemistry 27 (1988) 1849-1856
7. Bowman V.D., Chase E.S., Franz A.W., Chipman P.R., Zhang X., Perry K.L., Baker T.S., and Smith T.J. An antibody to the putative aphid recognition site on cucumber mosaic virus recognizes pentons but not hexons. J. Virol. 76 (2002) 12250-12258
8. Capen C.M., and Teschke C.M. Folding defects caused by single amino acid substitutions in a subunit are not alleviated by assembly. Biochemistry 39 (2000) 1142-1151
9. Clamp M., Cuff J., Searle S.M., and Barton G.J. The Jalview Java alignment editor. Bioinformatics 20 (2004) 426-427
10. Cole C., Barber J.D., and Barton G.J. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36 (2008) W197-W201
11. Conway J.F., Duda R.L., Cheng N., Hendrix R.W., and Steven A.C. Proteolytic and conformational control of a virus capsid maturation: the bacteriophage HK97 system. J. Mol. Biol. 253 (1995) 86-99
12. Conway J.F., Cheng N., Ross P.D., Hendrix R.W., Duda R.L., and Steven A.C. A thermally induced phase transition in a viral capsid transforms the hexamers, leaving the pentamers unchanged. J. Struct. Biol. 158 (2007) 224-232
13. 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
14. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
15. Fokine A., Leiman P.G., Shneider M.M., Ahvazi B., Boeshans K.M., Steven A.C., Black L.W., Mesyanzhinov V.V., and Rossmann M.G. Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry. Proc. Natl. Acad. Sci. USA 102 (2005) 7163-7168
16. Fraser J.S., Yu Z., Maxwell K.L., and Davidson A.R. Ig-like domains on bacteriophages: a tale of promiscuity and deceit. J. Mol. Biol. 359 (2006) 496-507
17. Frishman D., and Argos P. Knowledge-based secondary structure assignment. Proteins 23 (1995) 566-579
18. Fu C.Y., Morais M.C., Battisti A.J., Rossmann M.G., and Prevelige Jr. P.E. Molecular dissection of o29 scaffolding protein function in an in vitro assembly system. J. Mol. Biol. 366 (2007) 1161-1173
19. Galisteo M.L., Gordon C.L., and King J. Stability of wild-type and temperature-sensitive protein subunits of the phage P22 capsid. J. Biol. Chem. 270 (1995) 16595-16601
20. Gertsman I., Gan L., Guttman M., Lee K., Speir J.A., Duda R.L., Hendrix R.W., Komives E.A., and Johnson J.E. An unexpected twist in viral capsid maturation. Nature 458 (2009) 646-650
21. Goddard T.D., Huang C.C., and Ferrin T.E. Visualizing density maps with UCSF Chimera. J. Struct. Biol. 157 (2007) 281-287
22. Gordon C.L., and King J. Temperature-sensitive mutations in the phage P22 coat protein which interfere with polypeptide chain folding. J. Biol. Chem. 268 (1993) 9358-9368
23. Gordon C.L., and King J. Genetic properties of temperature-sensitive folding mutants of the coat protein of phage P22. Genetics 136 (1994) 427-438
24. Greene B., and King J. Binding of scaffolding subunits within the P22 procapsid lattice. Virology 205 (1994) 188-197
25. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environement for comparative modeling. Electrophoresis 18 (1997) 2714-2723
26. Havelka W.A., Henderson R., and Oesterhelt D. Three-dimensional structure of halorhodopsin at 7 A resolution. J. Mol. Biol. 247 (1995) 726-738
27. Hendrix R.W. Bacteriophages: evolution of the majority. Theor. Popul. Biol. 61 (2002) 471-480
28. Holden H.M., Ito M., Hartshorne D.J., and Rayment I. X-ray structure determination of telokin, the C-terminal domain of myosin light chain kinase, at 2.8Å resolution. J. Mol. Biol. 227 (1992) 840-851
29. Ishii T., Yamaguchi Y., and Yanagida M. Binding of the structural protein soc to the head shell of bacteriophage T4. J. Mol. Biol. 120 (1978) 533-544
30. Jaroszewski L., Rychlewski L., Li Z., Li W., and Godzik A. FFAS03: a server for profile-profile sequence alignments. Nucleic Acids Res. 33 (2005) W284-W288
31. Jiang W., Li Z., Zhang Z., Baker M.L., Prevelige 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
32. Jiang W., Baker M.L., Jakana J., Weigele P.R., King J., and Chiu W. Backbone structure of the infectious e15 virus capsid revealed by electron cryomicroscopy. Nature 451 (2008) 1130-1134
33. Johnson J.E. Functional implications of protein-protein interactions in icosahedral viruses. Proc. Natl. Acad. Sci. USA 93 (1996) 27-33
34. Kang S., Hawkridge A.M., Johnson K.L., Muddiman D.C., and Prevelige P.J. Identification of subunit-subunit interactions in bacteriophage P22 procapsids by chemical cross-linking and mass-spectrometry. J. Proteome Res. 5 (2006) 370-377
35. Kang S., and Prevelige Jr. P.E. Domain study of bacteriophage p22 coat protein and characterization of the capsid lattice transformation by hydrogen/deuterium exchange. J. Mol. Biol. 347 (2005) 935-948
36. King J., Botstein D., Casjens S., Earnshaw W., Harrison S., and Lenk E. Structure and assembly of the capsid of bacteriophage P22. Philos. Trans. R. Soc. Lond. B Biol. Sci. 276 (1976) 37-49
37. King J., and Chiu W. The procapsid-to-capsid transition in double-stranded DNA bacteriophages. In: Chiu W., Burnett M., and Garcea R. (Eds). Structural Biology of Viruses (1997), Oxford University Press, New York 288-311
38. Kontou M., Govindasamy L., Nam H.J., Bryant N., Llamas-Saiz A.L., Foces-Foces C., Hernando E., Rubio M.P., McKenna R., Almendral J.M., and Agbandje-McKenna M. Structural determinants of tissue tropism and in vivo pathogenicity for the parvovirus minute virus of mice. J. Virol. 79 (2005) 10931-10943
39. Lander G.C., Evilevitch A., Jeemaeva M., Potter C.S., Carragher B., and Johnson J.E. Bacteriophage lambda stabilization by auxiliary protein gpD: timing location, and mechanism of attachment determined by cryo-EM. Structure 16 (2008) 1399-1406
40. Lander G.C., Khayat R., Li R., Prevelige P.J., Potter C.S., Carragher B., and Johnson J.E. The P22 tail machine at subnanometer resolution reveals the architechture of an infectious conduit. Structure 17 (2009) 789-799
41. Lanman J., Tuma R., and Prevelige Jr. P.E. Identification and characterization of the domain structure of bacteriophage P22 coat protein. Biochemistry 38 (1999) 14614-14623
42. Montesano-Roditis L., Glitz D.G., Traut R.R., and Stewart P.L. Cryo-electron microscopic localization of protein L7/L12 within the Escherichia coli 70 S ribosome by difference mapping and Nanogold labeling. J. Biol. Chem. 276 (2001) 14117-14123
43. Morais M.C., Choi K.H., Koti J.S., Chipman P.R., Anderson D.L., and Rossmann M.G. Conservation of the capsid structure in the tailed dsDNA bacteriophages: the pseudoatomic structure of phi29. Mol. Cell 18 (2005) 149-159
44. Newcomb W.W., Homa F.L., Thomsen D.R., Booy F.P., Trus B.L., Steven A.C., Spencer J.V., and Brown J.C. Assembly of the herpes simplex virus capsid: characterization of intermediates observed during cell-free capsid formation. J. Mol. Biol. 263 (1996) 432-446
45. Newcomb W.W., Homa F.L., Thomsen D.R., Trus B.L., Cheng N., Steven A., Booy F., and Brown J.C. Assembly of the herpes simplex virus procapsid from purified components and identification of small complexes containing the major capsid and scaffolding proteins. J. Virol. 73 (1999) 4239-4250
46. Pei J., Kim B.-H., and Grishin N.V. PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res. 36 (2008) 2295-2300
47. 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
48. Prasad B.V.V., Prevelige Jr. P.E., Marieta E., Chen R.O., Thomas D., King J., and Chiu W. Three-dimensional transformation of capsids associated with genome packaging in a bacterial virus. J. Mol. Biol. 231 (1993) 65-74
49. Prevelige Jr. P.E., Thomas D., and King J. Nucleation and growth phases in the polymerization of coat and scaffolding subunits into icosahedral procapsid shells. Biophys. J. 64 (1993) 824-835
50. Ross P.D., Conway J.F., Cheng N., Dierkes L., Firek B.A., Hendrix R.W., Steven A.C., and Duda R.L. A free energy cascade with locks drives assembly and maturation of bacteriophage HK97 capsid. J. Mol. Biol. 364 (2006) 512-525
51. Stortelder A., Hendriks J., Buijs J.B., Bulthuis J., Gooijer C., van der Vies S.M., and van der Zwan G. Hexamerization of the bacteriophage T4 capsid protein gp23 and its W13V mutant studied by time-resolved tryptophan fluorescence. J. Phys. Chem. B 110 (2006) 25050-25058
52. Tang J., Olson N., Jardine P.J., Grimes S., Anderson D.L., and Baker T.S. DNA poised for release in bacteriophage phi29. Structure 16 (2008) 935-943
53. 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
54. Thuman-Commike P.A., Greene B., Malinski J.A., Burbea M., McGough A., Chiu W., and Prevelige P.E.J. Mechanism of scaffolding-directed virus assembly suggested by comparison of scaffolding-containing and scaffolding-lacking P22 procapsids. Biophys. J. 76 (1999) 3267-3277
55. Topf M., Baker M.L., John B., Chiu W., and Sali A. Structural characterization of components of protein assemblies by comparative modeling and electron cryo-microscopy. J. Struct. Biol. 149 (2005) 191-203
56. Trus B.L., Booy F.P., Newcomb W.W., Brown J.C., Homa F.L., Thomsen D.R., and Steven A.C. 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 (1996) 447-462
57. van Heel M., and Schatz M. Fourier shell correlation threshold criteria. J. Struct. Biol. 151 (2005) 250-262
58. 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
59. Yan X., Dryden K.A., Tang J., and Baker T.S. Ab initio random model method facilitates 3D reconstruction of icosahedral particles. J. Struct. Biol. 157 (2007) 211-225
60. Yan X., Sinkovits R.S., and Baker T.S. AUTO3DEM-an automated and high throughput program for image reconstruction of icosahedral particles. J. Struct. Biol. 157 (2007) 73-82
61. Yang F., Forrer P., Dauter Z., Conway J.F., Cheng N., Cerritelli M.E., Steven A.C., Pluckthun A., and Wlodawer A. Novel fold and capsid-binding properties of the lambda-phage display platform protein gpD. Nat. Struct. Biol. 7 (2000) 230-237
62. Zandi R., and Reguera D. Mechanical properties of viral capsids. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72 (2005) 021917
63. Zhang X., Walker S.B., Chipman P.R., Nibert M.L., and Baker T.S. Reovirus polymerase lambda 3 localized by cryo-electron microscopy of virions at a resolution of 7.6 A. Nat. Struct. Biol. 10 (2003) 1011-1018
64. Zhang Y., and Skolnick J. The protein structure prediction problem could be solved using the current PDB library. Proc. Natl. Acad. Sci. USA 102 (2005) 1029-1034
65. Zhou Z.H. Towards atomic resolution structural determination by single-particle cryo-electron microscopy. Curr. Opin. Struct. Biol. 18 (2008) 218-228