Micron-scale holes terminate the phage infection cycle

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

Volumn 107, Issue 5, 2010, Pages 2219-2223

  Dewey, Jill S ^a   Savva, Christos G ^a   White, Rebecca L ^b,c   Vitha, Stanislav ^a   Holzenburg, Andreas ^a,b   Young, Ry ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b Texas AandM University   (United States)

^c Sapphire Energy   (United States)

Author keywords

Bacteriophage; Cryoelectron tomography; Escherichia coli; Holin; Lambda

Indexed keywords

BACTERIAL PROTEIN; PROTEIN ENDOLYSIN; PROTEIN HOLIN; PROTEIN S105; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIOPHAGE LAMBDA; CELL SIZE; CONTROLLED STUDY; GROWTH RATE; IN VIVO STUDY; MEMBRANE CHANNEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

BACTERIOPHAGE LAMBDA; CRYOELECTRON MICROSCOPY; ENDOPEPTIDASES; ESCHERICHIA COLI; GENES, VIRAL; VIRAL PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 76649100791     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0914030107     Document Type: Article

References (44)

1. Young R, Wang IN (2006) Phage lysis. The Bacteriophages, ed Calendar R (Oxford Univ Press, New York), 2nd Ed, pp 104-128.
2. Wang IN, Smith DL, Young R (2000) Holins: The protein clocks of bacteriophage infections. Annu Rev Microbiol 54:799-825.
3. Gründling A, Bläsi U, Young R (2000) Biochemical and genetic evidence for three transmembrane domains in the class I holin, lambda S. J Biol Chem 275:769-776.
4. Gründling A, Manson MD, Young R (2001) Holins kill without warning. Proc Natl Acad Sci USA 98:9348-9352.
5. Summer EJ, et al. (2007) Rz/Rz1 lysis gene equivalents in phages of Gram-negative hosts. J Mol Biol 373:1098-1112.
6. Berry J,Summer EJ, StruckDK,YoungR(2008) Thefinal stepinthephageinfection cycle:The Rz and Rz1 lysis proteins link the inner and outer membranes. Mol Microbiol 70:341-351.
7. Bläsi U, Chang CY, Zagotta MT, Nam KB, Young R (1990) The lethal lambda S gene encodes its own inhibitor. EMBO J 9:981-989.
8. Gründling A, Bläsi U, Young R (2000) Genetic and biochemical analysis of dimer and oligomer interactions of the lambda S holin. J Bacteriol 182:6082-6090.
9. Savva CG, et al. (2008) The holin of bacteriophage lambda forms rings with large diameter. Mol Microbiol 69:784-793.
10. Wang IN, Deaton J, Young R (2003) Sizing the holin lesion with an endolysin-beta-galactosidase fusion. J Bacteriol 185:779-787.
11. Reader RW, Siminovitch L (1971) Lysis defective mutants of bacteriophage lambda: On the role of the S function in lysis. Virology 43:623-637.
12. Kellenberger E, et al. (1992) Artefacts and morphological changes during chemical fixation. J Microsc (Paris) 168:181-201.
13. McIntosh R, Nicastro D, Mastronarde D (2005) New views of cells in 3D: An introduction to electron tomography. Trends Cell Biol 15:43-51.
14. Dubochet J, et al. (1988) Cryo-electron microscopy of vitrified specimens. Q Rev Biophys 21:129-228.
15. Berriman J, Unwin N (1994) Analysis of transient structures by cryo-microscopy combined with rapid mixing of spray droplets. Ultramicroscopy 56:241-252.
16. Tweten RK (2005) Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect Immun 73:6199-6209.
17. Bremer H, Dennis PP (1996) Modulation of chemical composition and other parameters of the cell by growth rate. Escherichia coli and Salmonella: Cellular and Molecular Biology, ed Neidhart FC (ASM, Washington, DC), 2nd Ed.
18. Pierucci O (1978) Dimensions of Escherichia coli at various growth rates: Model for envelope growth. J Bacteriol 135:559-574.
19. Radermacher M (1992) Weighted back-projection methods. Electron Tomography, ed Frank J (Plenum, New York).
20. Ford RC, Holzenburg A (2008) Electron crystallography of biomolecules: Mysterious membranes and missing cones. Trends Biochem Sci 33:38-43.
21. Casjens S, Eppler K, Parr R, Poteete AR (1989) Nucleotide sequence of the bacteriophage P22 gene 19 to 3 region: Identification of a new gene required for lysis. Virology 171: 588-598.
22. Young R, Way J, Way S, Yin J, Syvanen M (1979) Transposition mutagenesis of bacteriophage lambda: A new gene affecting cell lysis. J Mol Biol 132:307-322.
23. Bayer ME (1968) Areas of adhesion between wall and membrane of Escherichia coli. J Gen Microbiol 53:395-404.
24. Bayer ME (1974) Ultrastructure and organization of the bacterial envelope. Ann NY Acad Sci 235:6-28.
25. Hobot JA, Carlemalm E, Villiger W, Kellenberger E (1984) Periplasmic gel: New concept resulting from the reinvestigation of bacterial cell envelope ultrastructure by new methods. J Bacteriol 160:143-152.
26. Tilley SJ, Orlova EV, Gilbert RJ, Andrew PW, Saibil HR (2005) Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 121:247-256.
27. Raab R, Neal G, Sohaskey C, Smith J, Young R (1988) Dominance in lambda S mutations and evidence for translational control. J Mol Biol 199:95-105.
28. Ramanculov E, Young R (2001) Genetic analysis of the T4 holin: Timing and topology. Gene 265:25-36.
29. Rydman PS, Bamford DH (2003) Identification and mutational analysis of bacteriophage PRD1 holin protein P35. J Bacteriol 185:3795-3803.
30. Adhya S, Sen A, Mitra S (1971) The Role of Gene S (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY).
31. Josslin R (1971) The effect of phage T4 infection on phospholipid hydrolysis in Escherichia coli. Virology 44:94-100.
32. Siegel DP, et al. (2006) Transmembrane peptides stabilize inverted cubic phases in a biphasic length-dependent manner: Implications for protein-induced membrane fusion. Biophys J 90:200-211.
33. Garrett J, Bruno C, Young R (1990) Lysis protein S of phage lambda functions in Saccharomyces cerevisiae. J Bacteriol 172:7275-7277.
34. Agu CA, et al. (2007) Bacteriophage-encoded toxins: The lambda-holin protein causes caspase-independent non-apoptotic cell death of eukaryotic cells. Cell Microbiol 9: 1753-1765.
35. Zagotta MT, Wilson DB (1990) Oligomerization of the bacteriophage lambda S protein in the inner membrane of Escherichia coli. J Bacteriol 172:912-921.
36. Chang CY, Nam K, Young R (1995) S gene expression and the timing of lysis by bacteriophage lambda. J Bacteriol 177:3283-3294.
37. Smith DL, Struck DK, Scholtz JM, Young R (1998) Purification and biochemical characterization of the lambda holin. J Bacteriol 180:2531-2540.
38. Campbell A (1961) Sensitive mutants of bacteriophage lambda. Virology 14:22-32.
39. Goldberg AR, Howe M (1969) New mutations in the S cistron of bacteriophage lambda affecting host cell lysis. Virology 38:200-202.
40. Blattner FR, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453-1462.
41. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-6645.
42. Saxton WO, Baumeister W, Hahn M (1984) Three-dimensional reconstruction of imperfect two-dimensional crystals. Ultramicroscopy 13:57-70.
43. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71-76.
44. Frangakis AS, Hegerl R (2001) Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J Struct Biol 135:239-250.