The phage φ29 membrane protein p16.7, involved in DNA replication, is required for efficient ejection of the viral genome

Journal of Bacteriology

Volumn 189, Issue 15, 2007, Pages 5542-5549

  Alcorlo, Martín ^a   González Huici, Víctor ^a,b   Hermoso, José M ^a   Meijer, Wilfried J J ^a   Salas, Margarita ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PROTEIN P16.7; PROTEIN P17; UNCLASSIFIED DRUG; VIRUS DNA; PHAGE PHI29, PROTEIN P17; PROTEIN P16.7, BACTEROPHAGE PHI29; VIRUS PROTEIN;

ARTICLE; BACILLUS SUBTILIS; BACTERIOPHAGE; CELL POLARITY; CYTOPLASM; DNA REPLICATION; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; NONHUMAN; OPEN READING FRAME; OPERON; PRIORITY JOURNAL; PROMOTER REGION; VIRUS GENOME; BACILLUS PHAGE; GENETICS; METABOLISM; PHYSIOLOGY; VIROLOGY;

BACILLUS PHAGE PHI29; BACILLUS SUBTILIS;

BACILLUS PHAGES; BACILLUS SUBTILIS; DNA REPLICATION; DNA, VIRAL; MEMBRANE PROTEINS; PROMOTER REGIONS (GENETICS); VIRAL PROTEINS;

EID: 34547620689     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00402-07     Document Type: Article

References (41)

1. Albert, A., D. Muñoz-Espín, M. Jiménez, J. L. Asensio, J. A. Hermoso, M. Salas, and W. J. J. Meijer. 2005. Structural basis for membrane anchorage of viral φ29 DNA during replication. J. Biol. Chem. 280:42486-42488.
2. Asensio, J. L., A. Albert, D. Muñoz-Espín, C. González, J. Hermoso, L. Villar, J. Jiménez-Barbero, M. Salas, and W. J. J. Meijer. 2005. Structure of the functional domain of φ29 replication organizer: insights into oligomerization and DNA binding. J. Biol. Chem. 280:20730-20739.
3. Barthelemy, I., R. P. Mellado, and M. Salas. 1989. In vitro transcription of bacteriophage φ29 DNA: inhibition of early promoters by the viral replication protein p6. J. Virol. 63:460-462.
4. Bjornsti, M. A., B. E. Reilly, and D. L. Anderson. 1983. Morphogenesis of bacteriophage φ29 of Bacillus subtilis: oriented and quantized in vitro packaging of DNA protein gp3. J. Virol. 45:383-396.
5. Bravo, A., J. M. Hermoso, and M. Salas. 1994. A genetic approach to the identification of functional amino acids in protein p6 of Bacillus subtilis phage φ29. Mol. Gen. Genet. 245:529-536.
6. Bravo, A., and M. Salas. 1997. Initiation of bacteriophage φ29 DNA replication in vivo: assembly of a membrane-associated multiprotein complex. J. Mol. Biol. 269:102-112.
7. Carrascosa, J. L., A. Camacho, F. Moreno, F. Jiménez, R. P. Mellado, E. Viñuela, and M. Salas. 1976. Bacillus subtilis phage φ29: characterization of gene products and functions. Eur. J. Biochem. 66:229-241.
8. Chang, C. N., P. Model, and G. Blobel. 1979. Membrane biogenesis: cotranslational integration of the bacteriophage f1 coat protein into an Escherichia coli membrane fraction. Proc. Natl. Acad. Sci. USA 76:1251-1255.
9. Cordes, C., R. Meima, B. Twiest, B. Kazemier, G. Venema, J. M. van Dijl, and S. Bron. 1996. The expression of a plasmid-specified exported protein causes structural plasmid instability in Bacillus subtilis. J. Bacteriol. 178:5235-5242.
10. Crucitti, P., J. M. Lázaro, V. Beneš, and M. Salas. 1998. Bacteriophage φ29 early protein p17 is conditionally required for the first rounds of viral DNA replication. Gene 223:135-142.
11. García, L. R., and I. J. Molineux. 1996. Transcription-independent DNA translocation of bacteriophage T7 DNA into Escherichia coli. J. Bacteriol. 178:6921-6929.
12. González-Huici, V., M. Alcorlo, M. Salas, and J. M. Hermoso. 2004. Bacteriophage φ29 protein p6: an architectural protein involved in genome organization, replication and control of transcription. J. Mol. Recognit. 17:390-396.
13. González-Huici, V., M. Alcorlo, M. Salas, and J. M. Hermoso. 2004. Binding of phage φ29 architectural protein p6 to the viral genome: evidence for topological restriction of the phage linear DNA. Nucleic Acids Res. 32:3493-3502.
14. González-Huici, V., M. Alcorlo, M. Salas, and J. M. Hermoso. 2004. Phage φ29 proteins p1 and p17 are required for efficient binding of architectural protein p6 to viral DNA in vivo. J. Bacteriol. 186:8401-8406.
15. González-Huici, V., M. Salas, and J. M. Hermoso. 2004. Genome wide, supercoiling-dependent, in vivo binding of a viral protein involved in DNA replication and transcriptional control. Nucleic Acids Res. 32:2306-2314.
16. González-Huici, V., M. Salas, and J. M. Hermoso. 2004. The push-pull mechanism of bacteriophage φ29 DNA injection. Mol. Microbiol. 52:529-540.
17. González-Huici, V., M. Salas, and J. M. Hermoso. 2006. Requirements for Bacillus subtilis bacteriophage φ29 DNA ejection. Gene 374:19-25.
18. Inciarte, M. R., J. M. Lázaro, M. Salas, and E. Viñuela. 1976. Physical map of bacteriophage φ29 DNA. Virology 74:314-323.
19. Ivarie, R. D., and J. J. Pène. 1973. DNA replication in bacteriophage φ29: the requirement of a viral-specific product for association of φ29 DNA with the cell membrane of Bacillus amyloliquefaciens. Virology 52:351-362.
20. Jiménez, F., A. Camacho, J. De la Torre, E. Viñuela, and M. Salas. 1977. Assembly of Bacillus subtilis phage φ29. 2. Mutants in the cistrons coding for the non-structural proteins. Eur. J. Biochem. 73:57-72.
21. Kemp, P., M. Gupta, and I. J. Molineux. 2004. Bacteriophage T7 DNA ejection into cells is initiated by an enzyme-like mechanism. Mol. Microbiol. 53:1251-1265.
22. Krawiec, S., F. Jiménez, J. A. García, N. Villanueva, J. M. Sogo, and M. Salas. 1981. The orderly, in vitro emergence of DNA from bacteriophage φ29 particles. Virology 111:440-454.
23. Lanni, Y. T. 1968. First-step-transfer deoxyribonucleic acid of bacteriophage T5. Bacteriol. Rev. 32:227-242.
24. Letellier, L., P. Boulanger, M. de Frutos, and P. Jacquot. 2003. Channeling phage DNA through membranes: from in vivo to in vitro. Res. Microbiol. 154:283-287.
25. Lin, D. C., and A. D. Grossman. 1998. Identification and characterization of a bacterial chromosome partitioning site. Cell 92:675-685.
26. Meijer, W. J. J., J. A. Horcajadas, and M. Salas. 2001. φ29 family of phages. Microbiol. Mol. Biol Rev. 65:261-287.
27. Meijer, W. J. J., P. J. Lewis, J. Errington, and M. Salas. 2000. Dynamic relocalization of phage φ29 DNA during replication and the role of the viral protein p16.7. EMBO J. 19:4182-4190.
28. Meijer, W. J. J., A. Serna-Rico, and M. Salas. 2001. Characterization of the bacteriophage φ29-encoded protein p16.7: a membrane protein involved in phage DNA replication. Mol. Microbiol. 39:731-746.
29. Molineux, I. J. 2006. Fifty-three years since Hershey and Chase: much ado about pressure but which pressure is it? Virology 344:221-229.
30. Molineux, I. J. 2001. No syringes please, ejection of phage 17 DNA from the virion is enzyme driven. Mol. Microbiol. 40:1-8.
31. Moreno, F., A. Camacho, E. Viñuela, and M. Salas. 1974. Supressor-sensitive mutants and genetic map of Bacillus subtilis bacteriophage φ29. Virology 62:1-16.
32. Muñoz-Espín, D., M. G. Mateu, L. Villar, A. Marina, M. Salas, and W. J. J. Meijer. 2004. Phage φ29 DNA replication organizer membrane protein p16.7 contains a coiled-coil and a dimeric, homeodomain-related, functional domain. J. Biol. Chem. 279:50437-50445.
33. Rossmann, M. G., V. V. Mesyanzhinov, F. Arisaka, and P. G. Leiman. 2004. The bacteriophage T4 DNA injection machine. Curr. Opin. Struct. Biol. 14:171-180.
34. Ryter, A., and A. Chang. 1975. Localization of transcribing genes in the bacterial cell by means of high resolution autoradiography. J. Mol. Biol. 98:797-810.
35. Salas, M. 1991. Protein-priming of DNA replication. Annu. Rev. Biochem. 60:37-71.
36. Serna-Rico, A., D. Muñoz-Espín, L. Villar, M. Salas, and W. J. Meijer. 2003. The integral membrane protein p16.7 organizes in vivo φ29 DNA replication through interaction with both the terminal protein and ssDNA. EMBO J. 22:2297-2306.
37. Serna-Rico, A., M. Salas, and W. J. J. Meijer. 2002. The Bacillus subtilis phage φ29 protein p16.7, involved in φ29 DNA replication, is a membrane-localized single-stranded DNA-binding protein. J. Biol. Chem. 277:6733-6742.
38. Smith, D. E., S. J. Tans, S. B. Smith, S. Grimes, D. L. Anderson, and C. Bustamante. 2001. The bacteriophage φ29 portal motor can package DNA against a large internal force. Nature 413:748-752.
39. Snyder, C. E., Jr., and R. H. Benzinger. 1981. Second-step transfer of bacteriophage T5 DNA: purification and characterization of the T5 gene A2 protein. J. Virol. 40:248-257.
40. Whiteley, H. R., W. D. Ramey, G. B. Spiegelman, and R. D. Holder. 1986. Modulation of in vivo and in vitro transcription of bacteriophage φ29 early genes. Virology 155:392-401.
41. Woldringh, C. L., P. R. Jensen, and H. V. Westerhoff. 1995. Structure and partitioning of bacterial DNA: determined by a balance of compaction and expansion forces? FEMS Microbiol. Lett. 131:235-242.