The role of scaffolding proteins in the assembly of the small, single-stranded DNA virus φX174

Journal of Molecular Biology

Volumn 288, Issue 4, 1999, Pages 595-608

  Dokland, Terje ^a   Bernal, Ricardo A ^a   Burch, April ^b   Pletnev, Sergei ^a   Fane, Bentley A ^b   Rossmann, Michael G ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Bacteriophage X174; Morphogenesis; Procapsid; Scaffolding proteins; Three dimensional structure

Indexed keywords

VIRUS PROTEIN;

ARTICLE; BACTERIOPHAGE PHI X 174; ELECTRON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE; VIRUS ASSEMBLY; VIRUS CAPSID; X RAY CRYSTALLOGRAPHY;

ANIMALIA; BACTERIOPHAGE PHI; DNA VIRUSES; MIRIDAE; UNIDENTIFIED BACTERIOPHAGE;

EID: 0032967636     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2699     Document Type: Article

References (57)

1. Aoyama A., Hamatake R. K., Hayashi M. Morphogenesis of φX174: in vitro synthesis of infectious phage from purified viral components. Proc. Natl Acad. Sci. USA. 78:1981;7285-7289.
2. Asakura S. Polymerization of flagellin and polymorphism of flagella. Advan. Biophys. 1:1970;99-155.
3. Bolotovsky R., Steller I., Rossmann M. G. The use of partial reflections for scaling and averaging X-ray area detector data. J. Appl. Crystallog. 31:1998;708-717.
4. Brünger A. T. X-PLOR, Version 3.1 Manual: A System for X-ray Crystallography and NMR. 1992;Yale University Press, New Haven.
5. Burch A. D., Ta J., Fane B. A. Cross-functional analysis of the Microviridae internal scaffolding protein. J. Mol. Biol. 286:1999;95-104.
6. Burgess A. B. Studies on the proteins of φX174. II. The protein composition of the φX coat. Proc. Natl Acad. Sci. USA. 64:1969;613-617.
7. Burns R. G., Symmons M. F. In vitro assembly of microtubule protein with GTP and 2′dGTP: kinetic evidence for a preassembly conformational change. Biochemistry. 34:1995;2302-2308.
8. 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 φ6. EMBO J. 16:1997;4477-4487.
9. Casjens S., Hendrix R. Control mechanisms in dsDNA bacteriophage assembly. Calendar R. The Bacteriophages. 1988;15-91 Plenum Press, New York.
10. Caspar D. L. D. Movement and self-control in protein assemblies. Quasi-equivalence revisited. Biophys. J. 32:1980;103-138.
11. Caspar D. L. D., Klug A. Physical principles in the construction of regular viruses. Cold Spring Harbor Symp. Quant. Biol. 27:1962;1-24.
12. Chretien D., Fuller S. D., Karsenti E. Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates. J. Cell Biol. 129:1995;1311-1328.
13. Dokland T., Murialdo H. Structural transitions during maturation of bacteriophage lambda capsids. J. Mol. Biol. 233:1993;682-694.
14. Dokland T., McKenna R., Ilag L. L., Bowman B. R., Incardona N. L., Fane B. A., Rossmann M. G. Structure of a viral procapsid with molecular scaffolding. Nature. 389:1997;308-313.
15. Dokland T., McKenna R., Sherman D. M., Bowman B. R., Bean W. F., Rossmann M. G. Structure determination of the φX174 closed procapsid. Acta Crystallog. sect. D. 54:1998;878-890.
16. Ekechukwu M. C., Fane B. A. Characterization of the morphogenetic defects conferred by cold-sensitive prohead accessory and scaffolding proteins of φX174. J. Bacteriol. 177:1995;829-830.
17. Ekechukwu M. C., Oberste D. J., Fane B. A. Host and φX174 mutations affecting the morphogenesis or stabilization of the 50 S complex, a single-stranded DNA synthesizing intermediate. Genetics. 140:1995;1167-1174.
18. Fane B. A., Hayashi M. Second-site suppressors of a cold-sensitive prohead assembly protein of bacteriophage φX174. Genetics. 128:1991;663-671.
19. Fane B. A., Shien S., Hayashi M. Second-site suppressors of a cold sensitive external scaffolding protein of bacteriophage φX174. Genetics. 134:1993;1003-1011.
20. Farber M. B. Purification and properties of bacteriophage φX174 gene D product. J. Virol. 17:1976;1027-1037.
21. Fujisawa H., Hayashi M. Functions of gene C and gene D products of bacteriophage φX174. J. Virol. 21:1977a;506-515.
22. Fujisawa H., Hayashi M. Two infectious forms of bacteriophage φX174. J. Virol. 23:1977b;439-442.
23. Grimes J. M., Burroughs J. N., Gouet P., Diprose J. M., Malby R., Ziéntara S., Mertens P. P. C., Stuart D. I. The atomic structure of the bluetongue virus core. Nature. 395:1998;470-478.
24. Hadfield A. T., Lee W., Zhao R., Oliveira M. A., Minor I., Rueckert R. R., Rossmann M. G. The refined structure of human rhinovirus 16 at 2.15 Å resolution: implication for the viral life cycle. Structure. 5:1997;427-441.
25. Hall C. E., Maclean E. C., Tessman I. Structure and dimensions of bacteriophage φX174 from electron microscopy. J. Mol. Biol. 1:1959;192-194.
26. Harrison S. C., Skehel J. J., Wiley D. C. Virus structure. Fields B. N., Knipe D. M., Howley P. M. Fields Virology. 1996;59-99 Lippincott-Raven, Philadelphia.
27. Hayashi M., Aoyama A., Richardson D. L. Jr, Hayashi M. N. Biology of the bacteriophage φX174. Calendar R. The Bacteriophages. 1988;1-71 Plenum Press, New York and London.
28. Ilag L. L., Olson N. H., Dokland T., Music C. L., Cheng R. H., Brown Z., McKenna R., Rossmann M. G., Baker T. S., Incardona N. L. DNA packaging intermediates of bacteriophage φX174. Structure. 3:1995;353-363.
29. Jazwinski S. M., Marco R., Kornberg A. The gene H spike protein of bacteriophage φX174 and S13. II. Relation to synthesis of the parental replicative form. Virology. 66:1975;294-305.
30. Kellenberger E. DNA viruses. Cooperativity and regulation through conformational changes as features of phage assembly. Phil. Trans. Roy. Soc. ser. B. 276:1976;3-13.
31. Kellenberger E. Form determination of the heads of bacteriophages. Eur. J. Biochem. 190:1990;233-248.
32. King J., Griffin-Shea R., Fuller M. T. Scaffolding proteins and the genetic control of virus shell assembly. Quart. Rev. Biol. 55:1980;369-393.
33. Livnah O., Stura E. A., Middleton S. A., Johnson D. L., Jolliffe L. K., Wilson I. A. Crystallographic evidence for preformed dimers of erythropoietin receptor before ligand activation. Science. 283:1999;987-990.
34. McGough A. F-actin-binding proteins. Curr. Opin. Struct. Biol. 8:1998;166-176.
35. McKenna R., Xia D., Willingmann P., Ilag L. L., Krishnaswamy S., Rossmann M. G., Olson N. H., Baker T. S., Incardona N. L. Atomic structure of single-stranded DNA bacteriophage φX174 and its functional implications. Nature. 355:1992;137-143.
36. McKenna R., Ilag L. L., Rossmann M. G. Analysis of the single-stranded DNA bacteriophage φX174, refined at a resolution of 3.0 Å J. Mol. Biol. 237:1994;517-543.
37. McKenna R., Bowman B. R., Ilag L. L., Rossmann M. G., Fane B. A. Atomic structure of the degraded procapsid particle of the bacteriophage G4: induced structural changes in the presence of calcium ions and functional implications. J. Mol. Biol. 256:1996;736-750.
38. Muckelbauer J. K., Kremer M., Minor I., Tong L., Zlotnick A., Johnson J. E., Rossmann M. G. Structure determination of coxsackievirus B3 to 3.5 Å resolution. Acta Crystallog. sect. D. 51:1995;871-887.
39. Mukai R., Hamatake R. K., Hayashi M. Isolation and identification of bacteriophage φX174 prohead. Proc. Natl Acad. Sci. USA. 76:1979;4877-4881.
40. Olson N. H., Baker T. S., Willingmann P., Incardona N. L. The three-dimensional structure of frozen-hydrated bacteriophage φX174. J. Struct. Biol. 108:1992;168-175.
41. Oosawa K., Ueno T., Aizawa S.-I. Overproduction of the bacterial flagellar switch proteins and their interactions with the MS ring complex in vitro. J. Bacteriol. 176:1994;3683-3691.
42. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276A:1997;307-326.
43. Prasad B. V. V., Prevelige P. E., Marietta E., Chen R. O., Thomas D., King J., Chiu W. Three-dimensional transformation of capsids associated with genome packaging in a bacterial virus. J. Mol. Biol. 231:1993;65-74.
44. Rossmann M. G., Johnson J. E. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58:1989;533-573.
45. Rossmann M. G., McKenna R., Tong L., Xia D., Dai J., Wu H., Choi H. K., Lynch R. E. Molecular replacement real-space averaging. J. Appl. Crystallog. 25:1992;166-180.
46. Sanger F., Coulson A. R., Friedmann T., Air G. M., Barrell B. G., Brown N. L., Fiddes J. C., Hutchison C. A. III, Slocombe P. M., Smith M. The nucleotide sequence of bacteriophage φX174. J. Mol. Biol. 125:1978;225-246.
47. Shank P. R., Hutchison C. A., III, Edgell M. H. Isolation and characterization of the four major proteins in the virion of bacteriophage φX174. Biochemistry. 16:1977;4545-4549.
48. Siden E. J., Hayashi M. Role of the gene B product in bacteriophage φX174 development. J. Mol. Biol. 89:1974;1-16.
49. Silva A. M., Rossmann M. G. Refined structure of southern bean mosaic virus at 2.9 Å resolution. J. Mol. Biol. 197:1987;69-87.
50. Sinsheimer R. L. Purification and properties of bacteriophage φX174. J. Mol. Biol. 1:1959;37-42.
51. Steven A. C. Conformational change-an alternative energy source?: exothermic phase transition in phage capsid maturation. Biophys. J. 65:1993;5-6.
52. Tessmann E. S., Peterson P. K. Bacterial rep- mutations that block development of small DNA bacteriophage late in infection. J. Virol. 20:1976;400-412.
53. Tonegawa S., Hayashi M. Intermediates in the assembly of φX174. J. Mol. Biol. 48:1970;219-242.
54. Tsao J., Chapman M. S., Agbandje M., Keller W., Smith K., Wu H., Luo M., Smith T. J., Rossmann M. G., Compans R. W., Parrish C. R. The three-dimensional structure of canine parvovirus and its functional implications. Science. 251:1991;1456-1464.
55. Weisbeek P. J., Sinsheimer R. L. A DNA- protein complex involved in bacteriophage φX174 particle formation. Proc. Natl Acad. Sci. USA. 71:1974;3054-3058.
56. Yazaki K. Electron microscopic studies of bacteriophage φX174 intact and 'eclipsing' particles, and the genome by the staining and shadowing method. J. Virol. Methods. 2:1981;159-167.
57. Zhou Z. H., Macnab S. J., Jakana J., Scott L. R., Chiu W., Rixon F. J. Identification of the sites of interaction between the scaffold and outer shell in herpes simplex virus-1 capsids by difference electron imaging. Proc. Natl Acad. Sci. USA. 95:1998;2778-2783.