Bacteriophage T5 Structure Reveals Similarities with HK97 and T4 Suggesting Evolutionary Relationships

Journal of Molecular Biology

Volumn 361, Issue 5, 2006, Pages 993-1002

  Effantin, G ^a   Boulanger, P ^b   Neumann, E ^a   Letellier, L ^b   Conway, J F ^a,c  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

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

Author keywords

assembly domain; bacteriophage; capsid; cryo electron microscopy; T5

Indexed keywords

CAPSID PROTEIN;

ARTICLE; BACTERIOPHAGE T4; BACTERIOPHAGE T5; CRYOELECTRON MICROSCOPY; EVOLUTION; GEOMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; SEQUENCE ANALYSIS; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS MORPHOLOGY;

MIRIDAE;

EID: 33746931256     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.06.081     Document Type: Article

References (48)

1. Ackermann H.-W. Bacteriophage classification. In: Kutter E., and Sulakvelidze A. (Eds). Bacteriophages: Biology and Applications (2004), CRC Press, Boca Raton
2. McCorquodale D.J., and Warner H.R. The bacteriophages. In: Calender R. (Ed). Bacteriophage T5 and related phages (1988), Plenum Press, New York
3. Letellier L., Boulanger P., Plancon L., Jacquot P., and Santamaria M. Main features on tailed phage, host recognition and DNA uptake. Front. Biosci. 9 (2004) 1228-1339
4. Saigo K. Isolation of high-density mutants and identification of nonessential structural proteins in bacteriophage T5; dispensability of L-shaped tail fibers and a secondary major head protein. Virology 85 (1978) 422-433
5. Zweig M., Rosenkranz H.S., and Morgan C. Development of coliphage T5: ultrastructural and biochemical studies. J. Virol. 9 (1972) 526-543
6. Guenebaut V., Maaloum M., Bonhivers M., Wepf R., Leonard K., and Horber J.K. TEM moire patterns explain STM images of bacteriophage T5 tails. Ultramicroscopy 69 (1997) 129-137
7. Lambert O., Plancon L., Rigaud J.L., and Letellier L. Protein-mediated DNA transfer into liposomes. Mol. Microbiol. 30 (1998) 761-765
8. Bohm J., Lambert O., Frangakis A.S., Letellier L., Baumeister W., and Rigaud J.L. FhuA-mediated phage genome transfer into liposomes: a cryo-electron tomography study. Curr. Biol. 11 (2001) 1168-1175
9. Zweig M., and Cummings D.J. Cleavage of head and tail proteins during bacteriophage T5 assembly: selective host involvement in the cleavage of a tail protein. J. Mol. Biol. 80 (1973) 505-518
10. Zweig M., and Cummings D.J. Structural proteins of bacteriophage T5. Virology 51 (1973) 443-453
11. Duda R.L., Martincic K., Xie Z., and Hendrix R.W. Bacteriophage HK97 head assembly. FEMS Microbiol. Rev. 17 (1995) 41-46
12. Wang J., Jiang Y., Vincent M., Sun Y., Yu H., Wang J., et al. Complete genome sequence of bacteriophage T5. Virology 332 (2005) 45-65
13. Bayer M.E., and Remsen C.C. Bacteriophage T2 as seen with the freeze-etching technique. Virology 40 (1970) 703-718
14. Aebi U., Bijlenga R.K., ten Heggeler B., Kistler J., Steven A.C., and Smith P.R. Comparison of the structural and chemical composition of giant T-even phage heads. J. Supramol. Struct. 5 (1976) 475-495
15. Cerritelli M.E., Cheng N., Rosenberg A.H., McPherson C.E., Booy F.P., and Steven A.C. Encapsidated conformation of bacteriophage T7 DNA. Cell 91 (1997) 271-280
16. Cerritelli M.E., Conway J.F., Cheng N., Trus B.L., and Steven A.C. Molecular mechanisms in bacteriophage T7 procapsid assembly, maturation, and DNA containment. Adv. Protein Chem. 64 (2003) 301-323
17. Olson N.H., Gingery M., Eiserling F.A., and Baker T.S. The structure of isometric capsids of bacteriophage T4. Virology 279 (2001) 385-391
18. Fokine A., Chipman P.R., Leiman P.G., Mesyanzhinov V.V., Rao V.B., and Rossmann M.G. Molecular architecture of the prolate head of bacteriophage T4. Proc. Natl Acad. Sci. USA 101 (2004) 6003-6008
19. 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
20. Ishii T., and Yanagida M. Molecular organization of the shell of the T-even bacteriophage head. J. Mol. Biol. 97 (1975) 655-660
21. 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
22. Rossmann M.G., Bernal R., and Pletnev S.V. Combining electron microscopic with x-ray crystallographic structures. J. Struct. Biol. 136 (2001) 190-200
23. Kikkawa M., Okada Y., and Hirokawa N. 15 Å resolution model of the monomeric kinesin motor, KIF1A. Cell 100 (2000) 241-252
24. 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
25. Duda R.L. Protein chainmail: catenated protein in viral capsids. Cell 94 (1998) 55-60
26. Li Y., Conway J.F., Cheng N., Steven A.C., Hendrix R.W., and Duda R.L. Control of virus assembly: HK97 "Whiffleball" mutant capsidswithout pentons. J. Mol. Biol. 348 (2005) 167-182
27. Fokine A., Leiman P.G., Shneider M.M., Ahvazi B., Boeshans K.M., Steven A.C., et al. 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
28. Iwasaki K., Trus B.L., Wingfield P.T., Cheng N., Campusano G., Rao V.B., and Steven A.C. Molecular architecture of bacteriophage T4 capsid: vertex structure and bimodal binding of the stabilizing accessory protein. Soc. Virology 271 (2000) 321-333
29. Conway J.F., Watts N.R., Belnap D.M., Cheng N., Stahl S.J., Wingfield P.T., and Steven A.C. Characterization of a conformational epitope on hepatitis B virus core antigen and quasiequivalent variations in antibody binding. J. Virol. 77 (2003) 6466-6473
30. Jiang W., Li Z., Zhang Z., Baker M.L., Prevelige Jr. P.E., and Chiu W. Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nature Struct. Biol. 10 (2003) 131-135
31. 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 tailed dsDNA bacteriophages: the pseudoatomic structure of phi29. Mol. Cell 18 (2005) 149-159
32. 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
33. Simpson A.A., Tao Y., Leiman P.G., Badasso M.O., He Y., Jardine P.J., et al. Structure of the bacteriophage phi29 DNA packaging motor. Nature 408 (2000) 745-750
34. Leonard K.R., Kleinschmidt A.K., and Lake J.A. Caulobacter crescentus bacteriophage phiCbK: structure and in vitro self-assembly of the tail. J. Mol. Biol. 81 (1973) 349-365
35. Papadopoulos S., and Smith P.R. The structure of the tail of the bacteriophage phi CbK. J. Ultrastruct. Res. 80 (1982) 62-70
36. Katsura I. Mechanism of length determination in bacteriophage lambda tails. Adv. Biophys. 26 (1990) 1-18
37. Hendrix R.W. Tail length determination in double-stranded DNA bacteriophages. Curr. Top. Microbiol. Immunol. 136 (1988) 21-29
38. Scheible P.P., Rhoades E.A., and Rhoades M. Localization of single-chain interruptions in bacteriophage T5 DNA I. Electron microscopic studies. J. Virol. 23 (1977) 725-736
39. Boulanger P., le Maire M., Bonhivers M., Dubois S., Desmadril M., and Letellier L. Purification and structural and functional characterization of FhuA, a transporter of the Escherichia coli outer membrane. Biochemistry 35 (1996) 14216-14224
40. Conway J.F., and Steven A.C. Methods for reconstructing density maps of "single" particles from cryoelectron micrographs to subnanometer resolution. J. Struct. Biol. 128 (1999) 106-118
41. Fuller S.D., Butcher S.J., Cheng R.H., and Baker T.S. Three-dimensional reconstruction of icosahedral particles-the uncommon line. J. Struct. Biol. 116 (1996) 48-55
42. Baker T.S., and Cheng R.H. A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J. Struct. Biol. 116 (1996) 120-130
43. Crowther R.A. Procedures for three-dimensional reconstruction of spherical viruses by Fourier synthesis from electron micrographs. Phil. Trans. Roy. Soc. ser. B 261 (1971) 221-230
44. Saxton W.O., and Baumeister W. The correlation averaging of a regularly arranged bacterial cell envelope protein. J. Microsc. 127 (1982) 127-138
45. Chacon P., and Wriggers W. Multi-resolution contour-based fitting of macromolecular structures. J. Mol. Biol. 317 (2002) 375-384
46. W. Humphrey, A. Dalke, K. Schulten, VMD: visual molecular dynamics. J. Mol. Graph. 14, (1996) 33-8, 27-8
47. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25 (1997) 3389-3402
48. Lupas A., Van Dyke M., and Stock J. Predicting coiled coils from protein sequences. Science 252 (1991) 1162-1164