The phage tail tape measure protein, an inner membrane protein and a periplasmic chaperone play connected roles in the genome injection process of E.coli phage HK97

Molecular Microbiology

Volumn 96, Issue 3, 2015, Pages 437-447

  Cumby, Nichole ^a   Reimer, Kelly ^a   Mengin Lecreulx, Dominique ^b   Davidson, Alan R ^a   Maxwell, Karen L ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GLUCOSE TRANSPORTER; MEMBRANE PROTEIN; PERIPLASMIC PROTEIN; PHAGE TAIL TAPE MEASURE PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; ESCHERICHIA COLI PROTEIN; FKPA PROTEIN, E COLI; PEPTIDYLPROLYL ISOMERASE; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE; PHOSPHOENOLPYRUVATE-GLUCOSE PHOSPHOTRANSFERASE; VIRUS DNA;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL MEMBRANE; BACTERIOPHAGE; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI PHAGE HK97; HOST CELL; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; VIRUS GENOME; VIRUS PARTICLE; COLIPHAGE; ESCHERICHIA COLI; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS ENTRY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

COLIPHAGES; DNA, VIRAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENOME, VIRAL; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; PEPTIDYLPROLYL ISOMERASE; PERIPLASMIC PROTEINS; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; VIRAL TAIL PROTEINS; VIRUS INTERNALIZATION;

EID: 84928402372     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12918     Document Type: Article

References (46)

1. Ackermann, H.W. (2007) 5500 phages examined in the electron microscope. Arch Virol 152: 227-243.
2. Arie, J.P., Sassoon, N., and Betton, J.M. (2001) Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol Microbiol 39: 199-210.
3. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
4. Bebeacua, C., Lorenzo Fajardo, J.C., Blangy, S., Spinelli, S., Bollmann, S., Neve, H., etal. (2013) X-ray structure of a superinfection exclusion lipoprotein from phage TP-J34 and identification of the tape measure protein as its target. Mol Microbiol 89: 152-165.
5. Berkane, E., Orlik, F., Stegmeier, J.F., Charbit, A., Winterhalter, M., and Benz, R. (2006) Interaction of bacteriophage lambda with its cell surface receptor: an in vitro study of binding of the viral tail protein gpJ to LamB (Maltoporin). Biochemistry 45: 2708-2720.
6. Bohm, J., Lambert, O., Frangakis, A.S., Letellier, L., Baumeister, W., and Rigaud, J.L. (2001) FhuA-mediated phage genome transfer into liposomes: a cryo-electron tomography study. Curr Biol 11: 1168-1175.
7. Boulanger, P., and Letellier, L. (1992) Ion channels are likely to be involved in the two steps of phage T5 DNA penetration into Escherichia coli cells. J Biol Chem 267: 3168-3172.
8. Boulanger, P., Jacquot, P., Plancon, L., Chami, M., Engel, A., Parquet, C., etal. (2008) Phage T5 straight tail fiber is a multifunctional protein acting as a tape measure and carrying fusogenic and muralytic activities. J Biol Chem 283: 13556-13564.
9. Breitbart, M., Hewson, I., Felts, B., Mahaffy, J.M., Nulton, J., Salamon, P., and Rohwer, F. (2003) Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 185: 6220-6223.
10. Buhr, A., Flukiger, K., and Erni, B. (1994) The glucose transporter of Escherichia coli. Overexpression, purification, and characterization of functional domains. J Biol Chem 269: 23437-23443.
11. Cumby, N., Edwards, A.M., Davidson, A.R., and Maxwell, K.L. (2012) The Bacteriophage HK97 gp15 moron element encodes a novel superinfection exclusion protein. J Bacteriol 194: 5012-5019.
12. Davidson, A.R., and Sauer, R.T. (1994) Folded proteins occur frequently in libraries of random amino acid sequences. Proc Natl Acad Sci USA 91: 2146-2150.
13. Dhillon, E.K., Dhillon, T.S., Lai, A.N., and Linn, S. (1980a) Host range, immunity and antigenic properties of lambdoid coliphage HK97. J Gen Virol 50: 217-220.
14. Dhillon, E.K., Dhillon, T.S., Lam, Y.Y., and Tsang, A.H. (1980b) Temperate coliphages: classification and correlation with habitats. Appl Environ Microbiol 39: 1046-1053.
15. El Ghachi, M., Bouhss, A., Barreteau, H., Touze, T., Auger, G., Blanot, D., and Mengin-Lecreulx, D. (2006) Colicin M exerts its bacteriolytic effect via enzymatic degradation of undecaprenyl phosphate-linked peptidoglycan precursors. J Biol Chem 281: 22761-22772.
16. Hancock, R.W., and Braun, V. (1976) Nature of the energy requirement for the irreversible adsorption of bacteriophages T1 and phi80 to Escherichia coli. J Bacteriol 125: 409-415.
17. Hannavy, K., Barr, G.C., Dorman, C.J., Adamson, J., Mazengera, L.R., Gallagher, M.P., etal. (1990) TonB protein of Salmonella typhimurium. A model for signal transduction between membranes. J Mol Biol 216: 897-910.
18. Hofer, B., Ruge, M., and Dreiseikelmann, B. (1995) The superinfection exclusion gene (sieA) of bacteriophage P22: identification and overexpression of the gene and localization of the gene product. J Bacteriol 177: 3080-3086.
19. Horne, S.M., and Young, K.D. (1995) Escherichia coli and other species of the Enterobacteriaceae encode a protein similar to the family of Mip-like FK506-binding proteins. Arch Microbiol 163: 357-365.
20. Hu, B., Margolin, W., Molineux, I.J., and Liu, J. (2013) The bacteriophage t7 virion undergoes extensive structural remodeling during infection. Science 339: 576-579.
21. Hullmann, J., Patzer, S.I., Romer, C., Hantke, K., and Braun, V. (2008) Periplasmic chaperone FkpA is essential for imported colicin M toxicity. Mol Microbiol 69: 926-937.
22. Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G., and Gibson, T.J. (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23: 403-405.
23. Juhala, R.J., Ford, M.E., Duda, R.L., Youlton, A., Hatfull, G.F., and Hendrix, R.W. (2000) Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299: 27-51.
24. Katsura, I. (1987) Determination of bacteriophage lambda tail length by a protein ruler. Nature 327: 73-75.
25. Kimura, M., Jia, Z.-J., Nakayama, N., and Asakawa, S. (2008) Ecology of viruses in soils: past, present and future perspectives. Soil Sci Plant Nutr 54: 1-32.
26. Kliem, M., and Dreiseikelmann, B. (1989) The superimmunity gene sim of bacteriophage P1 causes superinfection exclusion. Virology 171: 350-355.
27. Labrie, S.J., Samson, J.E., and Moineau, S. (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8: 317-327.
28. Letellier, L., Plancon, L., Bonhivers, M., and Boulanger, P. (1999) Phage DNA transport across membranes. Res Microbiol 150: 499-505.
29. Likhacheva, N.A., Samsonov, V.V., and Sineoky, S.P. (1996) Genetic control of the resistance to phage C1 of Escherichia coli K-12. J Bacteriol 178: 5309-5315.
30. Lu, M.J., and Henning, U. (1994) Superinfection exclusion by T-even-type coliphages. Trends Microbiol 2: 137-139.
31. Mahony, J., McGrath, S., Fitzgerald, G.F., and van Sinderen, D. (2008) Identification and characterization of lactococcal-prophage-carried superinfection exclusion genes. Appl Environ Microbiol 74: 6206-6215.
32. Marsh, P., and Wellington, E.M.H. (1994) Phage-host interactions in soil. FEMS Microbiol Ecol 15: 99-107.
33. Marti, E., Variatza, E., and Balcazar, J.L. (2014) Bacteriophages as a reservoir of extended-spectrum beta-lactamase and fluoroquinolone resistance genes in the environment. Clin Microbiol Infect 20: O456-O459.
34. Meins, M., Jeno, P., Muller, D., Richter, W.J., Rosenbusch, J.P., and Erni, B. (1993) Cysteine phosphorylation of the glucose transporter of Escherichia coli. J Biol Chem 268: 11604-11609.
35. Mills, S., Shanahan, F., Stanton, C., Hill, C., Coffey, A., and Ross, R.P. (2013) Movers and shakers: influence of bacteriophages in shaping the mammalian gut microbiota. Gut Microbes 4: 4-16.
36. Postle, K., and Skare, J.T. (1988) Escherichia coli TonB protein is exported from the cytoplasm without proteolytic cleavage of its amino terminus. J Biol Chem 263: 11000-11007.
37. Roessner, C.A., and Ihler, G.M. (1984) Proteinase sensitivity of bacteriophage lambda tail proteins gpJ and pH in complexes with the lambda receptor. J Bacteriol 157: 165-170.
38. Roessner, C.A., and Ihler, G.M. (1986) Formation of transmembrane channels in liposomes during injection of lambda DNA. J Biol Chem 261: 386-390.
39. Roof, S.K., Allard, J.D., Bertrand, K.P., and Postle, K. (1991) Analysis of Escherichia coli TonB membrane topology by use of PhoA fusions. J Bacteriol 173: 5554-5557.
40. Samsonov, V.V., and Sineoky, S.P. (2002) DcrA and dcrB Escherichia coli genes can control DNA injection by phages specific for BtuB and FhuA receptors. Res Microbiol 153: 639-646.
41. Saul, F.A., Arie, J.P., Vulliez-le Normand, B., Kahn, R., Betton, J.M., and Bentley, G.A. (2004) Structural and functional studies of FkpA from Escherichia coli, a cis/trans peptidyl-prolyl isomerase with chaperone activity. J Mol Biol 335: 595-608.
42. Scandella, D., and Arber, W. (1976) Phage lambda DNA injection into Escherichia coli pel-mutants is restored by mutations in phage genes V or H. Virology 69: 206-215.
43. Suttle, C.A. (2007) Marine viruses - major players in the global ecosystem. Nat Rev Microbiol 5: 801-812.
44. Wang, J., Michel, V., Hofnung, M., and Charbit, A. (1998) Cloning of the J gene of bacteriophage lambda, expression and solubilization of the J protein: first in vitro studies on the interactions between J and LamB, its cell surface receptor. Res Microbiol 149: 611-624.
45. Waterhouse, A.M., Procter, J.B., Martin, D.M., Clamp, M., and Barton, G.J. (2009) Jalview version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
46. Williams, N., Fox, D.K., Shea, C., and Roseman, S. (1986) Pel, the protein that permits lambda DNA penetration of Escherichia coli, is encoded by a gene in ptsM and is required for mannose utilization by the phosphotransferase system. Proc Natl Acad Sci USA 83: 8934-8938.