Visualization of bacteriophage P1 infection by cryo-electron tomography of tiny Escherichia coli

Virology

Volumn 417, Issue 2, 2011, Pages 304-311

  Liu, Jun ^a   Chen, Cheng Yen ^a   Shiomi, Daisuke ^b   Niki, Hironori ^b   Margolin, William ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

Attachment; Bacteriophage infection; Cryo electron tomography; E. coli; P1

Indexed keywords

VIRUS DNA;

ARTICLE; BACTERIAL CELL; BACTERIOPHAGE P1; CONTROLLED STUDY; CYTOPLASM; DNA CONFORMATION; ELECTRON TOMOGRAPHY; ESCHERICHIA COLI; HOST CELL; NONHUMAN; PRIORITY JOURNAL; VIRUS CELL INTERACTION;

BACTERIOPHAGE P1; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; ESCHERICHIA COLI; IMAGING, THREE-DIMENSIONAL; VIRUS INTERNALIZATION;

ESCHERICHIA COLI;

EID: 80051941010     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.06.005     Document Type: Article

References (40)

1. Aksyuk A.A., Leiman P.G., Kurochkina L.P., Shneider M.M., Kostyuchenko V.A., Mesyanzhinov V.V., Rossmann M.G. The tail sheath structure of bacteriophage T4: a molecular machine for infecting bacteria. EMBO J. 2009, 28(7):821-829.
2. Bendezu F.O., Hale C.A., Bernhardt T.G., de Boer P.A. RodZ (YfgA) is required for proper assembly of the MreB actin cytoskeleton and cell shape in E. coli. EMBO J. 2009, 28:193-204.
3. Bohm J., Lambert O., Frangakis A.S., Letellier L., Baumeister W., Rigaud J.L. FhuA-mediated phage genome transfer into liposomes: a cryo-electron tomography study. Curr. Biol. 2001, 11(15):1168-1175.
4. Caspar D.L. Movement and self-control in protein assemblies. Quasi-equivalence revisited. Biophys. J. 1980, 32(1):103-138.
5. Crawford J.T., Goldberg E.B. The function of tail fibers in triggering baseplate expansion of bacteriophage T4. J. Mol. Biol. 1980, 139(4):679-690.
6. Fokine A., Chipman P.R., Leiman P.G., Mesyanzhinov V.V., Rao V.B., Rossmann M.G., Eisenberg D.S. Molecular architecture of the prolate head of Bacteriophage T4. Proc. Natl. Acad. Sci. U.S.A. 2004, 101(16):6003-6008.
7. Furukawa H., Kuroiwa T., Mizushima S. DNA injection during bacteriophage T4 infection of Escherichia coli. J. Bacteriol. 1983, 154(2):938-945.
8. Gelbart W.M., Knobler C.M. Virology. Pressurized viruses. Science 2009, 323(5922):1682-1683.
9. Goldberg E., Grinius L., Letellier L. Recognition, attachment, and injection. Molecular biology of bacteriophage T4 1994, American Society for Microbiology, Washington, DC. J.D. Karam, J.W. Drake (Eds.).
10. Grayson P., Molineux I.J. Is phage DNA 'injected' into cells-biologists and physicists can agree. Curr. Opin. Microbiol. 2007, 10(4):401-409.
11. Hershey A.D., Chase M. Independent functions of viral protein and nucleic acid in growth of bacteriophage. J. Gen. Physiol. 1952, 36(1):39-56.
12. 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 2002, 415(6871):553.
13. Kostyuchenko V.A., Chipman P.R., Leiman P.G., Arisaka F., Mesyanzhinov V.V., Rossmann M.G. The tail structure of bacteriophage T4 and its mechanism of contraction. Nat. Struct. Mol. Biol. 2005, 12(9):810-813.
14. 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. Mol. Biol. 2003, 10(9):688-693.
15. Kremer J.R., Mastronarde D.N., McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 1996, 116(1):71-76.
16. Labedan B., Goldberg E.B. Requirement for membrane potential in injection of phage T4 DNA. Proc. Natl. Acad. Sci. U.S.A. 1979, 76(9):4669-4673.
17. Leiman P.G., Chipman P.R., Kostyuchenko V.A., Mesyanzhinov V.V., Rossmann M.G. Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 2004, 118(4):419-429.
18. Letellier L., Boulanger P., Plancon L., Jacquot P., Santamaria M. Main features on tailed phage, host recognition and DNA uptake. Front. Biosci. 2004, 9:1228-1339.
19. Liu J., Bartesaghi A., Borgnia M.J., Sapiro G., Subramaniam S. Molecular architecture of native HIV-1 gp120 trimers. Nature 2008, 455(7209):109-113.
20. Liu J., Lin T., Botkin D.J., McCrum E., Winkler H., Norris S.J. Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C-ring assembly flexion. J. Bacteriol. 2009, 191(16):5026-5036.
21. Liu X., Zhang Q., Murata K., Baker M.L., Sullivan M.B., Fu C., Dougherty M.T., Schmid M.F., Osburne M.S., Chisholm S.W., Chiu W. Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat. Struct. Mol. Biol. 2010, 17(7):830-836.
22. Lucic V., Forster F., Baumeister W. Structural studies by electron tomography: from cells to molecules. Annu. Rev. Biochem. 2005, 74:833-865.
23. Medalia O., Weber I., Frangakis A.S., Nicastro D., Gerisch G., Baumeister W. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 2002, 298(5596):1209-1213.
24. Molineux I.J. No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. Mol. Microbiol. 2001, 40(1):1-8.
25. Molineux I.J. Fifty-three years since Hershey and Chase; much ado about pressure but which pressure is it?. Virology 2006, 344(1):221-229.
26. Panja D., Molineux I.J. Dynamics of bacteriophage genome ejection in vitro and in vivo. Phys. Biol. 2010, 7(4):045006.
27. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25(13):1605-1612.
28. Reeve J.N. Bacteriophage infection of minicells: a general method for identification of "in vivo" bacteriophage directed polypeptide biosynthesis. Mol. Gen. Genet. 1977, 158(1):73-79.
29. Riede I. Receptor specificity of the short tail fibres (gp12) of T-even type Escherichia coli phages. Mol. Gen. Genet. 1987, 206(1):110-115.
30. Rossmann M.G., Mesyanzhinov V.V., Arisaka F., Leiman P.G. The bacteriophage T4 DNA injection machine. Curr. Opin. Struct. Biol. 2004, 14(2):171-180.
31. Shiomi D., Sakai M., Niki H. Determination of bacterial rod shape by a novel cytoskeletal membrane protein. EMBO J. 2008, 27:3081-3091.
32. 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 1967, 32(2):279-297.
33. Singer M., Baker T.A., Schnitzler G., Deischel S.M., Goel M., Dove W., Jaacks K.J., Grossman A.D., Erickson J.W., Gross C.A. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol. Rev. 1989, 53(1):1-24.
34. Sun Q., Margolin W. Influence of the nucleoid on placement of FtsZ and MinE rings in Escherichia coli. J. Bacteriol. 2001, 183(4):1413-1422.
35. Wachsman G., Heidstra R. The CRE/lox system as a tool for developmental studies at the cell and tissue level. Methods Mol. Biol. 2010, 655:47-64.
36. Walker J.T., Walker D.H. Coliphage P1 morphogenesis: analysis of mutants by electron microscopy. J. Virol. 1983, 45(3):1118-1139.
37. Winkler H., Zhu P., Liu J., Ye F., Roux K.H., Taylor K.A. Tomographic subvolume alignment and subvolume classification applied to myosin V and SIV envelope spikes. J. Struct. Biol. 2009, 165(2):64-77.
38. Yarmolinsky M.B., Sternberg N. Bacteriophage P1. The Bacteriophages 1988, 1. 2 vols.. Plenum Press, New York. R. Calendar (Ed.).
39. Zhang P., Khursigara C.M., Hartnell L.M., Subramaniam S. Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(10):3777-3781.
40. Zorzopulos J., Delong S., Chapman V., Kozloff L.M. Host receptor site for the short tail fibers of bacteriophage T4D. Virology 1982, 120(1):33-41.