Extensive proteolysis of head and inner body proteins by a morphogenetic protease in the giant Pseudomonas aeruginosa phage φKZ

Molecular Microbiology

Volumn 84, Issue 2, 2012, Pages 324-339

  Thomas, Julie A ^a   Weintraub, Susan T ^b   Wu, Weimin ^c   Winkler, Dennis C ^c   Cheng, Naiqian ^c   Steven, Alasdair C ^c   Black, Lindsay W ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HEAD PROTEIN; INNER BODY PROTEIN; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE; BIOINFORMATICS; CHEMICAL ANALYSIS; CONTROLLED STUDY; MASS SPECTROMETRY; MOLECULAR WEIGHT; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS ARUGINOSA PHAGE;

MASS SPECTROMETRY; MOLECULAR WEIGHT; MYOVIRIDAE; PEPTIDE HYDROLASES; PROTEOLYSIS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS PHAGES; VIRAL PROTEINS; VIRUS ASSEMBLY;

MIRIDAE; PSEUDOMONAS AERUGINOSA;

EID: 84862821249     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08025.x     Document Type: Article

References (46)

1. Black, L.W., and Thomas, J.A. (2012) Condensed genome structure. In Viral Molecular Machines. Rossman, M., and Rao, V.B. (eds). New York: Springer, pp. 469-488.
2. Black, L.W., Showe, M.K., and Steven, A.C. (1993) Morphogenesis of the T4 head. In Molecular Biology of Bacteriophage T4. Karam, J.D. (ed.). Washington, DC: ASM Press, pp. 218-258.
3. Briers, Y., Miroshnikov, K., Chertkov, O., Nekrasov, A., Mesyanzhinov, V., Volckaert, G., and Lavigne, R. (2008) The structural peptidoglycan hydrolase gp181 of bacteriophage φKZ. Biochem Biophys Res Commun 374: 747-751.
4. Cheng, H., Shen, N., Pei, J., and Grishin, N.V. (2004) Double-stranded DNA bacteriophage prohead protease is homologous to herpesvirus protease. Protein Sci 13: 2260-2269.
5. Cheng, N., Trus, B.L., Belnap, D.M., Newcomb, W.W., Brown, J.C., and Steven, A.C. (2002) Handedness of the Herpes Simplex Virus capsid and procapsid. J Virol 76: 7855-7859.
6. Cornelissen, A., Hardies, S.C., Shaburova, O.V., Krylov, V.N., Mattheus, W., Kropinski, A.M., and Lavigne, R. (2011) Complete genome sequence of the giant virus OBP and comparative genome analysis of the diverse φKZ-related phages. J Virol 86: 1844-1852.
7. David, N.M. (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152: 36-51.
8. Fokine, A., Kostyuchenko, V.A., Efimov, A.V., Kurochkina, L.P., Sykilinda, N.N., Robben, J., etal. (2005a) A three-dimensional cryo-electron microscopy structure of the bacteriophage φKZ head. J Mol Biol 352: 117-124.
9. Fokine, A., Leiman, P.G., Shneider, M.M., Ahvazi, B., Boeshans, K.M., Steven, A.C., etal. (2005b) Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry. Proc Natl Acad Sci USA 102: 7163-7168.
10. Fokine, A., Battisti, A., Bowman, V., Efimov, A., Kurochkina, L., Chipman, P., etal. (2007) CryoEM Study of the Pseudomonas bcacteriophage φKZ. Structure 15: 1099-1104.
11. Frangakis, A.S., and Hegerl, R. (2001) Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J Struct Biol 135: 239-250.
12. Golshahi, L., Lynch, K.H., Dennis, J.J., and Finlay, W.H. (2011) In vitro lung delivery of bacteriophages KS4-M and φKZ using dry powder inhalers for treatment of Burkholderia cepacia complex and Pseudomonas aeruginosa infections in cystic fibrosis. J Appl Microbiol 110: 106-117.
13. Grayson, P., and Molineux, I.J. (2007) Is phage DNA 'injected' into cells - biologists and physicists can agree. Curr Opin Microbiol 10: 401-409.
14. Harris, A., Cardone, G., Winkler, D.C., Heymann, J.B., Brecher, M., White, J.M., and Steven, A.C. (2006) Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc Natl Acad Sci USA 103: 19123-19127.
15. Heymann, B.J., Cardone, G., Winkler, D.C., and Steven, A.C. (2008) Computational resources for cryo-electron tomography in Bsoft. J Struct Biol 161: 232-242.
16. Hughey, R., and Krogh, A. (1996) Hidden Markov models for sequence analysis: extension and analysis of the basic method. Comput Appl Biosci 12: 95-107.
17. Karplus, K., Barrett, C., and Hughey, R. (1998) Hidden Markov models for detecting remote protein homologies. Bioinformatics 14: 846-856.
18. Keller, B., and Bickle, T.A. (1986) The nucleotide sequence of gene 21 of bacteriophage T4 coding for the prohead protease. Gene 49: 245-251.
19. Kremer, J.R., Mastronarde, D.N., and McIntosh, J.R. (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76.
20. Krylov, V.N., Smirnova, T.A., Minenkova, I.B., Plotnilova, T.G., Zhazikov, I.Z., and Khrenova, E.A. (1984) Pseudomonas bacteriophage φKZ contains an inner body in its capsid. Can J Microbiol 30: 758-762.
21. Krylov, V.N., Dela Cruz, D.M., Hertveldt, K., and Ackermann, H.W. (2007) 'KZ-like viruses', a proposed new genus of myovirus bacteriophages. Arch Virol 152: 1955-1959.
22. Lavigne, R., Darius, P., Summer, E.J., Seto, D., Mahadevan, P., Nilsson, A.S., etal. (2009) Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 9: 224.
23. Lecoutere, E., Ceyssens, P.-J., Miroshnikov, K., Mesyanzhinov, V., Krylov, V.N., Noben, J., etal. (2009) Identification and comparative analysis of the structural proteomes of φKZ and EL, two giant Pseudomonas aeruginosa bacteriophages. Proteomics 9: 3215-3219.
24. Liu, J., and Mushegian, A. (2004) Displacements of prohead protease genes in the late operons of double-stranded-DNA bacteriophages. J Bacteriol 186: 4369-4375.
25. Mangel, W.F., Baniecki, M.L., and McGrath, W.J. (2003) Specific interactions of the adenovirus proteinase with the viral DNA, an 11-amino-acid viral peptide, and the cellular protein actin. Cell Mol Life Sci 60: 2347-2355.
26. Matinkhoo, S., Lynch, K.H., Dennis, J.J., Finlay, W.H., and Vehring, R. (2011) Spray-dried respirable powders containing bacteriophages for the treatment of pulmonary infections. J Pharm Sci 100: 5197-5205.
27. Mesyanzhinov, V.V., Robben, J., Grymonprez, B., Kostyuchenko, V.A., Bourkaltseva, M.V., Sykilinda, N.N., etal. (2002) The genome of bacteriophage φKZ of Pseudomonas aeruginosa. J Mol Biol 317: 1-19.
28. Miroshnikov, K.A., Faizullina, N.M., Sykilinda, N.N., and Mesyanzhinov, V.V. (2006) Properties of the endolytic transglycosylase encoded by gene 144 of Pseudomonas aeruginosa bacteriophage φKZ. Biochemistry (Mosc) 71: 300-305.
29. Monson, R., Foulds, I., Foweraker, J., Welch, M., and Salmond, G.P.C. (2011) The Pseudomonas aeruginosa generalized transducing phage φPA3 is a new member of the φKZ-like group of 'jumbo' phages, and infects model laboratory strains and clinical isolates from cystic fibrosis patients. Microbiology 157: 859-867.
30. Mullaney, J.M., and Black, L.W. (1996) Capsid targeting sequence targets foreign proteins into bacteriophage T4 and permits proteolytic processing. J Mol Biol 261: 372-385.
31. Paradis-Bleau, C., Cloutier, I., Lemieux, L., Sanschagrin, F., Laroche, J., Auger, M., etal. (2007) Peptidoglycan lytic activity of the Pseudomonas aeruginosa phage φKZ gp144 lytic transglycosylase. FEMS Microbiol Lett 266: 201-209.
32. Plotnikova, T.G., Dzhusupova, A.B., Khrenova, E.A., and Krylov, V.N. (1982) Genetic and phenogenetic study of the ts-mutant group of Pseudomonas aeruginosa PA01 phage φKZ. Genetika 18: 1793-1798 [Russian].
33. Qiu, D., Damron, F.H., Mima, T., Schweizer, H.P., and Yu, H.D. (2008) PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl Environ Microbiol 74: 7422-7426.
34. Rasband, W.S. (19972011) ImageJ. Bethesda, MD: US National Institutes of Health [WWW document]. URL
35. Rishovd, S., Marvik, O.J., Jacobsen, E., and Lindqvist, B.H. (1994) Bacteriophage P2 and P4 morphogenesis: identification and characterization of the portal protein. Virology 200: 744-751.
36. Rishovd, S., Holzenburg, A., Johansen, B.V., and Lindqvist, B.H. (1998) Bacteriophage P2 and P4 morphogenesis: structure and function of the connector. Virology 245: 11-17.
37. Schaerli, C., Kellenberger, E. (1980) Head maturation pathway of bacteriophages T4 and T2. V. Maturable epsilon-particle accumulating an acridine-treated bacteriophage T4-infected cells. J Virol 33: 830-844.
38. Showe, M.K., Isobe, E., and Onorato, L. (1976a) Bacteriophage T4 prehead proteinase: I. Purification and properties of a bacteriophage enzyme which cleaves the capsid precursor proteins. J Mol Biol 107: 35-54.
39. Showe, M.K., Isobe, E., and Onorato, L. (1976b) Bacteriophage T4 prehead proteinase: II. Its cleavage from the product of gene 21 and regulation in phage-infected cells. J Mol Biol 107: 55-69.
40. Söding, J. (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21: 951-960.
41. Thomas, J.A., Rolando, M.R., Carroll, C.A., Shen, P.S., Belnap, D.M., Weintraub, S.T., etal. (2008) Characterization of Pseudomonas chlororaphis myovirus 201φ2-1 via genomic sequencing, mass spectrometry, and electron microscopy. Virology 376: 330-338.
42. Thomas, J.A., Weintraub, S.T., Hakala, K., Serwer, P., and Hardies, S.C. (2010) Proteome of the large Pseudomonas myovirus 201φ2-1: delineation of proteolytically processed virion proteins. Mol Cell Proteomics 9: 940-951.
43. Wainwright, M., Phoenix, D.A., Marland, J., Wareing, D.R., and Bolton, F.J. (1997) In-vitro photobactericidal activity of aminoacridines. J Antimicrob Chemother 40: 587-589.
44. Walker, J.E., Auffret, A.D., Carne, A., Gurnett, A., Hanisch, P., Hill, D., and Saraste, M. (1982) Solid-phase sequence analysis of polypeptides eluted from polyacrylamide gels. Eur J Biochem 123: 253-260.
45. Wu, W., Thomas, J.A., Cheng, N., Black, L.W., and Steven, A.C. (2012) Bubblegrams reveal the inner body structure of φKZ. Science 335: 182.
46. Zachary, A., and Black, L.W. (1991) Isolation and characterization of a portal protein-DNA complex from dsDNA bacteriophage. Intervirology 33: 6-16.