Bacteriophage P22 ejects all of its internal proteins before its genome

Virology

Volumn 485, Issue , 2015, Pages 128-134

  Jin, Yan ^a   Sdao, Sophia M ^b   Dover, John A ^b   Porcek, Natalia B ^b,c   Knobler, Charles M ^a   Gelbart, William M ^a   Parent, Kristin N ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Michigan State University   (United States)

^c Department of Microbiology and Molecular Genetics ^*  (United States)

Author keywords

Bacteriophage infectivity; Genome ejection; Internal protein ejection; Osmotic suppression; Receptors

Indexed keywords

E PROTEIN; LIPOPOLYSACCHARIDE; MACROGOL; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN A; UNCLASSIFIED DRUG; MACROGOL DERIVATIVE; OMPA OUTER MEMBRANE PROTEINS; OUTER MEMBRANE PROTEIN; VIRAL PROTEIN; VIRUS DNA;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENTEROBACTERIA PHAGE P22; IN VITRO STUDY; NONHUMAN; PODOVIRIDAE; PRIORITY JOURNAL; PROTEIN SECRETION; SALMONELLA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; VIRUS CELL INTERACTION; VIRUS STRAIN; BIOMECHANICS; CHEMISTRY; DRUG EFFECTS; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; OSMOSIS; ULTRASTRUCTURE; VIROLOGY; VIRUS CAPSID; VIRUS ENTRY; VIRUS GENOME;

MIRIDAE; PODOVIRIDAE; SALMONELLA;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIOPHAGE P22; BIOMECHANICAL PHENOMENA; CAPSID; DNA, VIRAL; GENOME, VIRAL; LIPOPOLYSACCHARIDES; OSMOSIS; POLYETHYLENE GLYCOLS; SALMONELLA TYPHIMURIUM; VIRAL PROTEINS; VIRUS INTERNALIZATION;

EID: 84939452306     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.07.006     Document Type: Article

References (46)

1. Andres D., Hanke C., Baxa U., Seul A., Barbirz S., Seckler R. Tailspike interactions with lipopolysaccharide effect DNA ejection from phage P22 particles in vitro. J. Biol. Chem. 2010, 285(47):36768-36775.
2. Andres D., Roske Y., Doering C., Heinemann U., Seckler R., Barbirz S. Tail morphology controls DNA release in two Salmonella phages with one lipopolysaccharide receptor recognition system. Mol. Microbiol. 2012, 83(6):1244-1253.
3. Bauer D.W., Huffman J.B., Homa F.L., Evilevitch A. Herpes virus genome, the pressure is on. J. Am. Chem. Soc. 2013, 135(30):11216-11221.
4. Bhardwaj A., Olia A.S., Cingolani G. Architecture of viral genome-delivery molecular machines. Curr. Opin. Struct. Biol. 2014, 25:1-8.
5. Casjens S., Huang W.M., Hayden M., Parr R. Initiation of bacteriophage P22 DNA packaging series analysis of a mutant that alters the DNA target specificity of the packaging apparatus. J. Mol. Biol. 1987, 194:411-422.
6. Casjens S., Hayden M. Analysis in vivo of the bacteriophage P22 headful nuclease. J. Mol. Biol. 1988, 199(3):467-474.
7. Casjens S.R., Thuman-Commike P.A. Evolution of mosaically related tailed bacteriophage genomes seen through the lens of phage P22 virion assembly. Virology 2011, 411(2):393-415.
8. Castelnovo M., Evilevitch A. DNA ejection from bacteriophage: towards a general behavior for osmotic-suppression experiments. Eur. Phys. J. E: Soft Matter 2007, 24(1):9-18.
9. Chang J., Weigele P., King J., Chiu W., Jiang W. Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 2006, 14(6):1073-1082.
10. Davidson A.R., Cardarelli L., Pell L.G., Radford D.R., Maxwell K.L. Long noncontractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 2012, 726:115-142.
11. Evilevitch A., Lavelle L., Knobler C.M., Raspaud E., Gelbart W.M. Osmotic pressure inhibition of DNA ejection from phage. Proc. Natl. Acad. Sci. USA 2003, 100(16):9292-9295.
12. Evilevitch A., Gober J.W., Phillips M., Knobler C.M., Gelbart W.M. Measurements of DNA lengths remaining in a viral capsid after osmotically suppressed partial ejection. Biophys. J. 2005, 88:751-756.
13. García L.R., Molineux I.J. Rate of translocation of bacteriophage T7 DNA across the membranes of Escherichia coli. J. Bacteriol. 1995, 177(14):4066-4076.
14. González-Huici V., Salas M., Hermoso J.M. Requirements for Bacillus subtilis bacteriophage phi29 DNA ejection. Gene 2006, 374:19-25.
15. Grayson P., Evilevitch A., Inamdar M.M., Purohit P.K., Gelbart W.M., Knobler C.M., Phillips R. The effect of genome length on ejection forces in bacteriophage lambda. Virology 2006, 348(2):430-436.
16. Hoffman B., Levine M. Bacteriophage P22 virion protein which performs an essential early function I. Analysis of 16-ts mutants. J. Virol. 1975, 16(6):1536-1546.
17. Hoffman B., Levine M. Bacteriophage P22 virion protein which performs an essential early function II. Characterization of the gene 16 function. J. Virol. 1975, 16(6):1547-1559.
18. Hu B., Margolin W., Molineux I.J., Liu J. The bacteriophage T7 virion undergoes extensive structural remodeling during infection. Science 2013, 339(6119):576-579.
19. Israel V., Woodworth-Gutai M., Levine M. Inhibitory effect of bacteriophage P22 infection on host cell deoxyribonuclease activity. J. Virol. 1972, 9(5):752-757.
20. Israel V. E proteins of bacetriophage P22 I. Identification and ejection from wild-type and defective particles. J. Virol. 1977, 23(1):91-97.
21. Iwashita S., Kanegasaki S. Smooth specific phage adsorption endorhamnosidase activity of tail parts of P22. Biochem. Biophys. Res. Commun. 1973, 55(2):403-409.
22. King J., Botstein D., Casjens S., Earnshaw W., Harrison S., Lenk E. Structure and assembly of the capsid of bacteriophage P22. Philos. Trans. R. Soc. Lond. B 1976, 276:37-49.
23. Koebnik R., Locher K.P., Van Gelder P. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 2000, 37(2):239-253.
24. Lander G.C., Tang L., Casjens S.R., Gilcrease E.B., Prevelige P., Poliakov A., Potter C.S., Carragher B., Johnson J.E. The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 2006, 312(5781):1791-1795.
25. Lander G.C., Khayat R., Li R., Prevelige P.E., Potter C.S., Carragher B., Johnson J.E. The P22 tail machine at subnanometer resolution reveals the architecture of an infection conduit. Structure 2009, 17(6):789-799.
26. Leavitt J.C., Gogokhia L., Gilcrease E.B., Bhardwaj A., Cingolani G., Casjens S.R. The tip of the tail needle affects the rate of DNA delivery by bacteriophage P22. PLoS One 2013, 8(8):e70936.
27. Leforestier A., Brasilès S., De Frutos M., Raspaud E., Letelier L., Tavares P., Livolant F. Bacteriophage T5 DNA ejection under pressure. J. Mol. Biol. 2008, 384(3):730-739.
28. Leiman P.G., Shneider M.M. Contractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 2012, 726:93-114.
29. Molineux I.J. No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. Mol. Microbiol. 2001, 40(1):1-8.
30. Molineux I.J., Panja D. Popping the cork: mechanisms of phage genome ejection. Nat. Rev. Microbiol. 2013, 11(3):194-204.
31. Olia A.S., Prevelige P.E., Johnson J.E., Cingolani G. Three-dimensional structure of a viral genome-delivery portal vertex. Nat. Struct. Mol. Biol. 2011, 18(5):597-603.
32. Parent K.N., Ranaghan M.J., Teschke C.M. A second-site suppressor of a folding defect functions via interactions with a chaperone network to improve folding and assembly in vivo. Mol. Microbiol. 2004, 54(4):1036-1050.
33. Parent K.N., Erb M.L., Cardone G., Nguyen K., Gilcrease E.B., Porcek N.B., Pogliano J., Baker T.S., Casjens S.R. OmpA and OmpC are critical host factors for bacteriophage Sf6 entry in Shigella. Mol. Microbiol. 2014, 92(1):47-60.
34. Patterson D.P., Prevelige P.E., Douglas T. Nanoreators by programmed enzyme encapsulation inside the capsid of the bacteriophage P22. ACS Nano 2012, 6(6):5000-5009.
35. Perez G.L., Huynh B., Slater M., Maloy S. Transport of phage P22 DNA across the cytoplasmic membrane. J. Bacteriol. 2009, 191(1):135-140.
36. Poranen M.M., Daugelavicius R., Bamford D.H. Common principles in viral entry. Annu. Rev. Microbiol. 2002, 56:521-538.
37. Porcek N.B., Parent K.N. Key residues of S. flexneri OmpA mediate infection by bacteriophage Sf6. J. Mol. Biol. 2015, 10.1016/j.jmb.2015.03.012.
38. Rau D.C., Lee B., Parsegian V.A. Measurement of the repulsive force between polyelectrolyte molecules in ionic solution hydration forces between parallel DNA doubles helices. Proc. Natl. Acad. Sci. USA 1984, 81:2621-2625.
39. Riemer S.C., Bloomfield V.A. Packaging of DNA in bacteriophage heads some considerations on energetics. Biopolymers 1978, 17:785-794.
40. Stanley C.B., Strey H.H. Measuring osmotic pressure of poly(ethylene glycol) solutions by sedimentation equilibrium ultracentrifugation. Macrolulecules 2003, 36:6888-6893.
41. Stock J.B., Rauch B., Roseman S. Periplasmic space in Salmonella typhimurium and Escherichia coli. J. Biol. Chem. 1977, 252(21):7850-7861.
42. Sun L., Young L.N., Zhang X., Boudko S.P., Fokine A., Zbornik E., Roznowski A.P., Molineux I.J., Rossmann M.G., Fane B.A. Icosahedral bacteriophage PhiX174 forms a tail for DNA transport during infection. Nature 2014, 505(7483):432-435.
43. Tang J., Lander G.C., Olia A.S., Li R., Casjens S., Prevelige P., Cingolani G., Baker T.S., Johnson J.E. Peering down the barrel of a bacteriophage portal: the genome packaging and release valve in p22. Structure 2011, 19(4):496-502.
44. 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. Stucture 1997, 5(6):789-798.
45. Tzlil S., Kindt J., Gelbart W.M., Ben-Shaul A. Forces and pressures in DNA packaging and release from viral capsids. Bioiphys. J. 2003, 84(3):1616-1627.
46. Winston F., Botstein D., Miller J.H. Characterization of amber and ochre suppressors in Salmonella typhimurium. J. Bacteriol. 1979, 137(1):433-439.