Structural remodeling of bacteriophage T4 and host membranes during infection initiation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 35, 2015, Pages E4919-E4928

  Hu, Bo ^a   Margolin, William ^a   Molineux, Ian J ^b   Liu, Jun ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Cryo ET; Infected cell; Membrane curvature; Phage t4; Structure

Indexed keywords

PROTEIN; PROTEIN GP29; UNCLASSIFIED DRUG; VIRUS DNA; VIRAL PROTEIN;

ADSORPTION; ARTICLE; CELL SURFACE; CYTOPLASM; ELECTRON TOMOGRAPHY; ENTEROBACTERIA PHAGE T4; ESCHERICHIA COLI; HOST; HOST CELL; INFECTION; INFORMATION; MEMBRANE; MUTANT; NONHUMAN; PRIORITY JOURNAL; VIRION; CELL MEMBRANE; CHEMISTRY; CRYOELECTRON MICROSCOPY; GENETICS; HOST PATHOGEN INTERACTION; PHYSIOLOGY; VIROLOGY; VIRUS GENE;

BACTERIOPHAGE T4; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; GENES, VIRAL; HOST-PATHOGEN INTERACTIONS; VIRAL TAIL PROTEINS; VIRION;

EID: 84941011872     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1501064112     Document Type: Article

References (90)

1. Hershey AD, Chase M (1952) Independent functions of viral protein and nucleic acid in growth of bacteriophage. J Gen Physiol 36(1):39-56.
2. Hershey AD (1955) An upper limit to the protein content of the germinal substance of bacteriophage T2. Virology 1(1):108-127.
3. Leiman PG, et al. (2010) Morphogenesis of the T4 tail and tail fibers. Virol J 7:355.
4. Cerritelli ME, Wall JS, Simon MN, Conway JF, Steven AC (1996) Stoichiometry and domainal organization of the long tail-fiber of bacteriophage T4: A hinged viral adhesin. J Mol Biol 260(5):767-780.
5. Ward S, et al. (1970) Assembly of bacteriophage T4 tail fibers. II. Isolation and characterization of tail fiber precursors. J Mol Biol 54(1):15-31.
6. Conley MP, Wood WB (1975) Bacteriophage T4 whiskers: A rudimentary environment-sensing device. Proc Natl Acad Sci USA 72(9):3701-3705.
7. Kellenberger E, Stauffer E, Häner M, Lustig A, Karamata D (1996) Mechanism of the long tail-fiber deployment of bacteriophages T-even and its role in adsorption, infection and sedimentation. Biophys Chem 59(1-2):41-59.
8. Coombs DH, Eiserling FA (1977) Studies on the structure, protein composition and aseembly of the neck of bacteriophage T4. J Mol Biol 116(3):375-405.
9. Letarov A, Manival X, Desplats C, Krisch HM (2005) gpwac of the T4-type bacteriophages: Structure, function, and evolution of a segmented coiled-coil protein that controls viral infectivity. J Bacteriol 187(3):1055-1066.
10. Efimov VP, et al. (1994) Fibritin encoded by bacteriophage T4 gene wac has a parallel triple-stranded alpha-helical coiled-coil structure. J Mol Biol 242(4):470-486.
11. Fokine A, et al. (2013) The molecular architecture of the bacteriophage T4 neck. J Mol Biol 425(10):1731-1744.
12. Yanagida M, Ahmad-Zadeh C (1970) Determination of gene product positions in bacteriophage T4 by specific antibody association. J Mol Biol 51(2):411-421.
13. Dickson RC, Barnes SL, Eiserling FA (1970) Structural proteins of bacteriophage T4. J Mol Biol 53(3):461-474.
14. Wood WB, Conley MP (1979) Attachment of tail fibers in bacteriophage T4 assembly: Role of the phage whiskers. J Mol Biol 127(1):15-29.
15. Terzaghi BE, Terzaghi E, Coombs D (1979) The role of the collar/whisker complex in bacteriophage T4D tail fiber attachment. J Mol Biol 127(1):1-14.
16. Kostyuchenko VA, et al. (2005) The tail structure of bacteriophage T4 and its mechanism of contraction. Nat Struct Mol Biol 12(9):810-813.
17. Kostyuchenko VA, et al. (2003) Three-dimensional structure of bacteriophage T4 baseplate. Nat Struct Biol 10(9):688-693.
18. Kostyuchenko VA, et al. (1999) The structure of bacteriophage T4 gene product 9: The trigger for tail contraction. Structure 7(10):1213-1222.
19. Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG (2004) Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118(4):419-429.
20. Prehm P, Jann B, Jann K, Schmidt G, Stirm S (1976) On a bacteriophage T3 and T4 receptor region within the cell wall lipopolysaccharide of Escherichia coli B. J Mol Biol 101(2):277-281.
21. Montag D, Hashemolhosseini S, Henning U (1990) Receptor-recognizing proteins of T-even type bacteriophages: The receptor-recognizing area of proteins 37 of phages T4 TuIa and TuIb. J Mol Biol 216(2):327-334.
22. Simon LD, Anderson TF (1967) The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. I. Attachment and penetration. Virology 32(2):279-297.
23. Simon LD, Anderson TF (1967) 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(2):298-305.
24. Riede I (1987) Receptor specificity of the short tail fibres (gp12) of T-even type Escherichia coli phages. Mol Gen Genet 206(1):110-115.
25. Heller K, Ölschläger T, Schwartz H (1983) Infection of LPS mutants of Escherichia coli B by phage T6. FEMS Microbiol Lett 17(1-3):1-6.
26. Amos LA, Klug A (1975) Three-dimensional image reconstructions of the contractile tail of T4 bacteriophage. J Mol Biol 99(1):51-64.
27. Coombs DH, Arisaka F (1994) T4 tail structure and function. Molecular Biology of Bacteriophage T4, ed Karam JD (American Society for Microbiology, Washington, DC), pp 259-281.
28. Aksyuk AA, et al. (2009) The tail sheath structure of bacteriophage T4: A molecular machine for infecting bacteria. EMBO J 28(7):821-829.
29. Stent GS (1963) Molecular Biology of Bacterial Viruses (Freeman, San Francisco).
30. Kanamaru S, Ishiwata Y, Suzuki T, Rossmann MG, Arisaka F (2005) Control of bacteriophage T4 tail lysozyme activity during the infection process. J Mol Biol 346(4): 1013-1020.
31. Shneider MM, et al. (2013) PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500(7462):350-353.
32. Mosig G, Lin GW, Franklin J, Fan WH (1989) Functional relationships and structural determinants of two bacteriophage T4 lysozymes: A soluble (gene e) and a baseplate-associated (gene 5) protein. New Biol 1(2):171-179.
33. Kanamaru S, Gassner NC, Ye N, Takeda S, Arisaka F (1999) The C-terminal fragment of the precursor tail lysozyme of bacteriophage T4 stays as a structural component of the baseplate after cleavage. J Bacteriol 181(9):2739-2744.
34. Nishima W, Kanamaru S, Arisaka F, Kitao A (2011) Screw motion regulates multiple functions of T4 phage protein gene product 5 during cell puncturing. J Am Chem Soc 133(34):13571-13576.
35. Kao SH, McClain WH (1980) Roles of bacteriophage T4 gene 5 and gene s products in cell lysis. J Virol 34(1):104-107.
36. Labedan B, Goldberg EB (1979) Requirement for membrane potential in injection of phage T4 DNA. Proc Natl Acad Sci USA 76(9):4669-4673.
37. Furukawa H, Yamada H, Mizushima S (1979) Interaction of bacteriophage T4 with reconstituted cell envelopes of Escherichia coli K-12. J Bacteriol 140(3): 1071-1080.
38. Kalasauskaite EV, Kadisaite DL, Daugelavicius RJ, Grinius LL, Jasaitis AA (1983) Studies on energy supply for genetic processes: Requirement for membrane potential in Escherichia coli infection by phage T4. Eur J Biochem 130(1):123-130.
39. Labedan B, Heller KB, Jasaitis AA, Wilson TH, Goldberg EB (1980) A membrane potential threshold for phage T4 DNA injection. Biochem Biophys Res Commun 93(2): 625-630.
40. Boulanger P, Letellier L (1988) Characterization of ion channels involved in the penetration of phage T4 DNA into Escherichia coli cells. J Biol Chem 263(20): 9767-9775.
41. Tarahovsky YS, Khusainov AA, Daugelavichus R, Bakene E (1995) Structural changes in Escherichia coli membranes induced by bacteriophage T4 at different temperatures. Biophys J 68(1):157-163.
42. Tarahovsky YS, Khusainov AA, Deev AA, Kim YV (1991) Membrane fusion during infection of Escherichia coli cells by phage T4. FEBS Lett 289(1):18-22.
43. Furukawa H, Kuroiwa T, Mizushima S (1983) DNA injection during bacteriophage T4 infection of Escherichia coli. J Bacteriol 154(2):938-945.
44. Lucic V, Förster F, Baumeister W (2005) Structural studies by electron tomography: From cells to molecules. Annu Rev Biochem 74:833-865.
45. Milne JLS, Subramaniam S (2009) Cryo-electron tomography of bacteria: Progress, challenges and future prospects. Nat Rev Microbiol 7(9):666-675.
46. Tocheva EI, Li Z, Jensen GJ (2010) Electron cryotomography. Cold Spring Harb Perspect Biol 2(6):a003442.
47. Böhm J, et al. (2001) FhuA-mediated phage genome transfer into liposomes: A cryo-electron tomography study. Curr Biol 11(15):1168-1175.
48. Chang JT, et al. (2010) Visualizing the structural changes of bacteriophage Epsilon15 and its Salmonella host during infection. J Mol Biol 402(4):731-740.
49. Guerrero-Ferreira RC, et al. (2011) Alternative mechanism for bacteriophage adsorption to the motile bacterium Caulobacter crescentus. Proc Natl Acad Sci USA 108(24):9963-9968.
50. Liu X, et al. (2010) Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat Struct Mol Biol 17(7):830-836.
51. Dai W, et al. (2013) Visualizing virus assembly intermediates inside marine cyanobacteria. Nature 502(7473):707-710.
52. Sun L, et al. (2014) Icosahedral bacteriophage ÖX174 forms a tail for DNA transport during infection. Nature 505(7483):432-435.
53. Hu B, Margolin W, Molineux IJ, Liu J (2013) The bacteriophage t7 virion undergoes extensive structural remodeling during infection. Science 339(6119):576-579.
54. Liu J, Chen CY, Shiomi D, Niki H, Margolin W (2011) Visualization of bacteriophage P1 infection by cryo-electron tomography of tiny Escherichia coli. Virology 417(2): 304-311.
55. Reeve JN (1977) Bacteriophage infection of minicells: A general method for identification of "in vivo" bacteriophage directed polypeptide biosynthesis. Mol Gen Genet 158(1):73-79.
56. rd (1971) Synthesis of ribonucleic acid and protein in plasmid-containing minicells of Escherichia coli K-12. J Bacteriol 107(1): 21-33.
57. Bartual SG, et al. (2010) Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc Natl Acad Sci USA 107(47):20287-20292.
58. Edgar R, et al. (2008) Bacteriophage infection is targeted to cellular poles. Mol Microbiol 68(5):1107-1116.
59. Grinius L (1987) Energy Transduction and Gene Transfer in Chemotrophic Bacteria: Macromolecules on the Move (Harwood Academic, Zurich).
60. Goldberg E, Grinius L, Letellier L (1994) Recognition, attachment, and injection. Molecular Biology of Bacteriophage T4, ed Karam JD (American Society for Microbiology, Washington, DC), pp 347-356.
61. Kanamaru S, et al. (2002) Structure of the cell-puncturing device of bacteriophage T4. Nature 415(6871):553-557.
62. Abuladze NK, Gingery M, Tsai J, Eiserling FA (1994) Tail length determination in bacteriophage T4. Virology 199(2):301-310.
63. Leiman PG, Shneider MM (2012) Contractile tail machines of bacteriophages. Adv Exp Med Biol 726:93-114.
64. Henning U, Höhn B, Sonntag I (1973) Cell envelope and shape of Escherichia coli K12: The ghost membrane. Eur J Biochem 39(1):27-36.
65. Adam G, Delbrück M (1968) Reduction of dimensionality in biological diffusion processes. Structural Chemistry and Molecular Biology, eds Rich A, Davidson N (Freeman, San Francisco), pp 198-215.
66. Rothenberg E, et al. (2011) Single-virus tracking reveals a spatial receptor-dependent search mechanism. Biophys J 100(12):2875-2882.
67. Parent KN, et al. (2014) OmpA and OmpC are critical host factors for bacteriophage Sf6 entry in Shigella. Mol Microbiol 92(1):47-60.
68. Wilson JH, Luftig RB, Wood WB (1970) Interaction of bacteriophage T4 tail fiber components with a lipopolysaccharide fraction from Escherichia coli. J Mol Biol 51(2): 423-434.
69. Wood WB, Henninger M (1969) Attachment of tail fibers in bacteriophage T4 assembly: Some properties of the reaction in vitro and its genetic control. J Mol Biol 39(3):603-618.
70. Crawford JT, Goldberg EB (1980) The function of tail fibers in triggering baseplate expansion of bacteriophage T4. J Mol Biol 139(4):679-690.
71. Crowther RA (1980) Mutants of bacteriophage T4 that produce infective fibreless particles. J Mol Biol 137(2):159-174.
72. King J (1968) Assembly of the tail of bacteriophage T4. J Mol Biol 32(2):231-262.
73. Molineux IJ, Panja D (2013) Popping the cork: Mechanisms of phage genome ejection. Nat Rev Microbiol 11(3):194-204.
74. Panja D, Molineux IJ (2010) Dynamics of bacteriophage genome ejection in vitro and in vivo. Phys Biol 7(4):045006.
75. Baumann L, Benz WC, Wright A, Goldberg EB (1970) Inactivation of urea-treated phage T4 by phosphatidylglycerol. Virology 41(2):356-364.
76. Benz WC, Goldberg EB (1973) Interactions between modified phage T4 particles and spheroplasts. Virology 53(1):225-235.
77. Kikuchi Y, King J (1975) Genetic control of bacteriophage T4 baseplate morphogenesis. III. Formation of the central plug and overall assembly pathway. J Mol Biol 99(4):695-716.
78. Vianelli A, et al. (2000) Bacteriophage T4 self-assembly: Localization of gp3 and its role in determining tail length. J Bacteriol 182(3):680-688.
79. Duckworth DH (1970) Biological activity of bacteriophage ghosts and "take-over" of host functions by bacteriophage. Bacteriol Rev 34(3):344-363.
80. Lu MJ, Stierhof YD, Henning U (1993) Location and unusual membrane topology of the immunity protein of the Escherichia coli phage T4. J Virol 67(8):4905-4913.
81. Silver S, Levine E, Spielman PM (1968) Cation fluxes and permeability changes accompanying bacteriophage infection of Escherichia coli. J Virol 2(8):763-771.
82. Lipinska B, Rao AS, Bolten BM, Balakrishnan R, Goldberg EB (1989) Cloning and identification of bacteriophage T4 gene 2 product gp2 and action of gp2 on infecting DNA in vivo. J Bacteriol 171(1):488-497.
83. Ge P, et al. (2015) Atomic structures of a bactericidal contractile nanotube in its pre-and postcontraction states. Nat Struct Mol Biol 22(5):377-382.
84. Mastronarde DN (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152(1):36-51.
85. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. JStructBiol116(1):71-76.
86. Amat F, et al. (2008) Markov random field based automatic image alignment for electron tomography. J Struct Biol 161(3):260-275.
87. Liu J, Wright ER, Winkler H (2010) 3D visualization of HIV virions by cryoelectron tomography. Methods Enzymol 483:267-290.
88. Winkler H, et al. (2009) Tomographic subvolume alignment and subvolume classification applied to myosin V and SIV envelope spikes. J Struct Biol 165(2):64-77.
89. Winkler H (2007) 3D reconstruction and processing of volumetric data in cryo-electron tomography. J Struct Biol 157(1):126-137.
90. Pettersen EF, et al. (2004) UCSF Chimera: A visualization system for exploratory research and analysis. J Comput Chem 25(13):1605-1612.