Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host

Cell

Volumn 118, Issue 4, 2004, Pages 419-429

  Leiman, Petr G ^a   Chipman, Paul R ^a   Kostyuchenko, Victor A ^a,b   Mesyanzhinov, Vadim V ^b   Rossmann, Michael G ^a  

^a PURDUE UNIVERSITY   (United States)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIOPHAGE; CELL MEMBRANE; CELL SURFACE; CELL WALL; CRYOELECTRON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; BACTERIOPHAGE T4; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRON MICROSCOPY; METABOLISM; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

UNIDENTIFIED BACTERIOPHAGE;

DEOXYRIBONUCLEASE; DNA; UREA; VIRUS PROTEIN;

BACTERIOPHAGE T4; BACTERIOPHAGES; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; DEOXYRIBONUCLEASES; DNA; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; UREA; VIRAL PROTEINS; VIRAL TAIL PROTEINS;

EID: 4644242580     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2004.07.022     Document Type: Article

References (59)

1. Abrahams J.P., Leslie A.G., Lutter R., Walker J.E. Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature. 370:1994;621-628
2. Abuladze N.K., Gingery M., Tsai J., Eiserling F.A. Tail length determination in bacteriophage T4. Virology. 199:1994;301-310
3. Ackermann H.W. Bacteriophage observations and evolution. Res. Microbiol. 154:2003;245-251
4. Amos L.A., Klug A. Three-dimensional image reconstructions of the contractile tail of T4 bacteriophage. J. Mol. Biol. 99:1975;51-64
5. Arisaka F., Engel J., Klump H. Contraction and dissociation of the bacteriophage T4 tail sheath induced by heat and urea. Prog. Clin. Biol. Res. 64:1981;365-379
6. Arisaka F., Takeda S., Funane K., Nishijima N., Ishii S. Structural studies of the contractile tail sheath protein of bacteriophage T4. 2. Structural analyses of the tail sheath protein, Gp18, by limited proteolysis, immunoblotting, and immunoelectron microscopy. Biochemistry. 29:1990;5057-5062
7. Baker T.S., Olson N.H., 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
8. Black L.W., Showe M.K., Steven A.C. Morphogenesis of the T4 head. Karam J.D. Molecular Biology of Bacteriophage T4. 1994;218-258 American Society for Microbiology, Washington, DC
9. Caspar D.L. Movement and self-control in protein assemblies. Quasi-equivalence revisited. Biophys. J. 32:1980;103-138
10. Cerritelli M.E., Wall J.S., Simon M.N., Conway J.F., Steven A.C. Stoichiometry and domainal organization of the long tail-fiber of bacteriophage T4. a hinged viral adhesin J. Mol. Biol. 260:1996;767-780
11. Chacon P., Wriggers W. Multi-resolution contour-based fitting of macromolecular structures. J. Mol. Biol. 317:2002;375-384
12. Conway J.F., Wikoff W.R., Cheng N., Duda R.L., Hendrix R.W., Johnson J.E., Steven A.C. Virus maturation involving large subunit rotations and local refolding. Science. 292:2001;744-748
13. Coombs D.H., Eiserling F.A. Studies on the structure, protein composition and assembly of the neck of bacteriophage T4. J. Mol. Biol. 116:1977;375-405
14. Coombs D.H., Arisaka F. T4 tail structure and function. Karam J.D. Molecular Biology of Bacteriophage T4. 1994;259-281 American Society for Microbiology, Washington, DC
15. Crawford J.T., Goldberg E.B. The function of tail fibers in triggering baseplate expansion of bacteriophage T4. J. Mol. Biol. 139:1980;679-690
16. Crowther R.A., Lenk E.V., Kikuchi Y., King J. Molecular reorganization in the hexagon to star transition of the baseplate of bacteriophage T4. J. Mol. Biol. 116:1977;489-523
17. Desplats C., Krisch H.M. The diversity and evolution of the T4-type bacteriophages. Res. Microbiol. 154:2003;259-267
18. Driedonks R., Engel A., tenHeggeler A., van Driel R. Gene 20 product of bacteriophage T4 its purification and structure. J. Mol. Biol. 152:1981;641-662
19. Duda R.L., Wall J.S., Hainfeld J.F., Sweet R.M., Eiserling F.A. Mass distribution of a probable tail-length-determining protein in bacteriophage T4. Proc. Natl. Acad. Sci. USA. 82:1985;5550-5554
20. Eiserling F.A., Black L.W. Pathways in T4 morphogenesis. Karam J.D. Molecular Biology of Bacteriophage T4. 1994;209-212 American Society for Microbiology, Washington, DC
21. Fokine A., Chipman P.R., Leiman P.G., Mesyanzhinov V.V., Rao V.B., Rossmann M.G. Molecular architecture of the prolate head of bacteriophage T4. Proc. Natl. Acad. Sci. USA. in press:2004
22. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., Leith A. Spider and web. processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116:1996;190-199
23. Goldberg E., Grinius L., Letellier L. Recognition, attachment, and injection. Karam J.D. Molecular Biology of Bacteriophage T4. 1994;347-356 American Society for Microbiology, Washington, DC
24. Gowen B., Bamford J.K., Bamford D.H., Fuller S.D. The tailless icosahedral membrane virus PRD1 localizes the proteins involved in genome packaging and injection at a unique vertex. J. Virol. 77:2003;7863-7871
25. Hendrix R.W. Bacteriophages. evolution of the majority Theor. Popul. Biol. 61:2002;471-480
26. Kanamaru S., Leiman P.G., Kostyuchenko V.A., Chipman P.R., Mesyanzhinov V.V., Arisaka F., Rossmann M.G. Structure of the cell-puncturing device of bacteriophage T4. Nature. 415:2002;553-557
27. Kellenberger E., Stauffer E., Haner M., Lustig A., Karamata D. Mechanism of the long tail-fiber deployment of bacteriophages T-even and its role in adsorption, infection and sedimentation. Biophys. Chem. 59:1996;41-59
28. Kikuchi Y., King J. Assembly of the tail of bacteriophage T4. J. Supramol. Struct. 3:1975;24-38. a
29. Kikuchi Y., King J. Genetic control of bacteriophage T4 baseplate morphogenesis. I. Sequential assembly of the major precursor, in vivo and in vitro. J. Mol. Biol. 99:1975;645-672. b
30. Kikuchi Y., King J. Genetic control of bacteriophage T4 baseplate morphogenesis. II. Mutants unable to form the central part of the baseplate. J. Mol. Biol. 99:1975;673-694. c
31. Kikuchi Y., King J. Genetic control of bacteriophage T4 baseplate morphogenesis. III. Formation of the central plug and overall assembly pathway. J. Mol. Biol. 99:1975;695-716. d
32. King J. Assembly of the tail of bacteriophage T4. J. Mol. Biol. 32:1968;231-262
33. King J. Bacteriophage T4 tail assembly. four steps in core formation J. Mol. Biol. 58:1971;693-709
34. Kleywegt G.J., Jones T.A. Software for handling macromolecular envelopes. Acta Crystallogr. D. 55:1999;941-944
35. Kostyuchenko V.A., Navruzbekov G.A., Kurochkina L.P., Strelkov S.V., Mesyanzhinov V.V., Rossmann M.G. The structure of bacteriophage T4 gene product 9. the trigger for tail contraction Struct. Fold. Des. 7:1999;1213-1222
36. Kostyuchenko V.A., Leiman P.G., Chipman P.R., Kanamaru S., van Raaij M.J., Arisaka F., Mesyanzhinov V.V., Rossmann M.G. Three-dimensional structure of bacteriophage T4 baseplate. Nat. Struct. Biol. 10:2003;688-693
37. Leiman P.G., Kostyuchenko V.A., Shneider M.M., Kurochkina L.P., Mesyanzhinov V.V., Rossmann M.G. Structure of bacteriophage T4 gene product 11, the interface between the baseplate and short tail fibers. J. Mol. Biol. 301:2000;975-985
38. Leiman P.G., Kanamaru S., Mesyanzhinov V.V., Arisaka F., Rossmann M.G. Structure and morphogenesis of bacteriophage T4. Cell. Mol. Life Sci. 60:2003;2356-2370. a
39. Leiman P.G., Shneider M.M., Kostyuchenko V.A., Chipman P.R., Mesyanzhinov V.V., Rossmann M.G. Structure and location of gene product 8 in the bacteriophage T4 baseplate. J. Mol. Biol. 328:2003;821-833. b
40. Miller E.S., Kutter E., Mosig G., Arisaka F., Kunisawa T., Ruger W. Bacteriophage T4 genome. Microbiol. Mol. Biol. Rev. 67:2003;86-156
41. Monod C., Repoila F., Kutateladze M., Tetart F., Krisch H.M. The genome of the pseudo T-even bacteriophages, a diverse group that resembles T4. J. Mol. Biol. 267:1997;237-249
42. Moody M.F. Structure of the sheath of bacteriophage T4. I. Structure of the contracted sheath and polysheath. J. Mol. Biol. 25:1967;167-200
43. Moody M.F. Sheath of bacteriophage T4. 3. Contraction mechanism deduced from partially contracted sheaths. J. Mol. Biol. 80:1973;613-635
44. Moody M.F., Makowski L. X-ray diffraction study of tail-tubes from bacteriophage T2L. J. Mol. Biol. 150:1981;217-244
45. Moore S.D., Prevelige P.E. Jr. DNA packaging. a new class of molecular motors Curr. Biol. 12:2002;R96-R98
46. Newcomb W.W., Juhas R.M., Thomsen D.R., Homa F.L., Burch A.D., Weller S.K., Brown J.C. The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J. Virol. 75:2001;10923-10932
47. Orlova E.V., Gowen B., Droge A., Stiege A., Weise F., Lurz R., van Heel M., Tavares P. Structure of a viral DNA gatekeeper at 10 A resolution by cryo-electron microscopy. EMBO J. 22:2003;1255-1262
48. Rossmann M.G., Bernal R., Pletnev S.V. Combining electron microscopic with x-ray crystallographic structures. J. Struct. Biol. 136:2001;190-200
49. Simon L.D., Anderson T.F. The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. I. Attachment and penetration. Virology. 32:1967;279-297. a
50. Simon L.D., Anderson T.F. The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. II. Structure and function of the baseplate. Virology. 32:1967;298-305. b
51. Simpson A.A., Tao Y., Leiman P.G., Badasso M.O., He Y., Jardine P.J., Olson N.H., Morais M.C., Grimes S., Anderson D.L., et al. Structure of the bacteriophage phi29 DNA packaging motor. Nature. 408:2000;745-750
52. Takeda S., Arisaka F., Ishii S., Kyogoku Y. Structural studies of the contractile tail sheath protein of bacteriophage T4. 1. Conformational change of the tail sheath upon contraction as probed by differential chemical modification. Biochemistry. 29:1990;5050-5056
53. Tao Y., Strelkov S.V., Mesyanzhinov V.V., Rossmann M.G. Structure of bacteriophage T4 fibritin. a segmented coiled coil and the role of the C-terminal domain Structure. 5:1997;789-798
54. Thomassen E., Gielen G., Schutz M., Schoehn G., Abrahams J.P., Miller S., van Raaij M.J. The structure of the receptor-binding domain of the bacteriophage T4 short tail fibre reveals a knitted trimeric metal-binding fold. J. Mol. Biol. 331:2003;361-373
55. Vianelli A., Wang G.R., Gingery M., Duda R.L., Eiserling F.A., Goldberg E.B. Bacteriophage T4 self-assembly. localization of gp3 and its role in determining tail length J. Bacteriol. 182:2000;680-688
56. Watts N.R., Hainfeld J., Coombs D.H. Localization of the proteins gp7, gp8 and gp10 in the bacteriophage T4 baseplate with colloidal gold:F(ab)2 and undecagold:Fab' conjugates. J. Mol. Biol. 216:1990;315-325
57. Wommack K.E., Colwell R.R. Virioplankton. viruses in aquatic ecosystems Microbiol. Mol. Biol. Rev. 64:2000;69-114
58. Xu Z., Sigler P.B. GroEL/GroES. structure and function of a two-stroke folding machine J. Struct. Biol. 124:1998;129-141
59. Zhao L., Kanamaru S., Chaidirek C., Arisaka F. P15 and P3, the tail completion proteins of bacteriophage T4, both form hexameric rings. J. Bacteriol. 185:2003;1693-1700