Strand and nucleotide-dependent ATPase activity of gp16 of bacterial virus phi29 DNA packaging motor

Virology

Volumn 380, Issue 1, 2008, Pages 69-74

  Lee, Tae Jin ^a   Zhang, Hui ^a   Liang, Dan ^a   Guo, Peixuan ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

ATPase; DNA packaging motor; Energy for DNA translocation; gp16; Phi 29; TIRF; Viral assembly

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GP16 PROTEIN; NUCLEOTIDE; PURINE; PYRIMIDINE; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; BACTERIOPHAGE; BINDING AFFINITY; DNA BINDING; DNA PACKAGING; DNA STRAND; DNA STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME KINETICS; FLUORESCENCE MICROSCOPY; GENE FUNCTION; MOLECULAR MECHANICS; NONHUMAN; PHI29 VIRUS; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATASES; BACILLUS PHAGES; BINDING SITES; CAPSID; DNA PACKAGING; DNA, VIRAL; DNA-BINDING PROTEINS; MICROSCOPY, FLUORESCENCE; RNA, VIRAL; VIRUS ASSEMBLY;

BACTERIA (MICROORGANISMS);

EID: 52049116701     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.07.003     Document Type: Article

References (40)

1. Alam T.I., and Rao V.B. The ATPase domain of the large terminase protein, gp17, from bacteriophage T4 binds DNA: implications to the DNA packaging mechanism. J. Mol. Biol. 376 (2008) 1272-1281
2. Baumann R.G., and Black L.W. Isolation and characterization of T4 bacteriophage gp17 terminase, a large subunit multimer with enhanced ATPase activity. J. Biol. Chem. 278 (2003) 4618-4627
3. Baumann R.G., Mullaney J., and Black L.W. Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol. Microbiol. 61 (2006) 16-32
4. Black L.W. DNA Packaging in dsDNA bacteriophages. Annual Review of Microbiology 43 (1989) 267-292
5. Brune M., Hunter J.L., Corrie J.E., and Webb M.R. Direct, real-time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment 1 ATPase. Biochemistry 33 (1994) 8262-8271
6. Brune M., Hunter J.L., Howell S.A., Martin S.R., Hazlett T.L., Corrie J.E., and Webb M.R. Mechanism of inorganic phosphate interaction with phosphate binding protein from Escherichia coli. Biochemistry 37 (1998) 10370-10380
7. Camacho A.G., Gual A., Lurz R., Tavares P., and Alonso J.C. Bacillus subtilis bacteriophage SPP1 DNA packaging motor requires terminase and portal proteins. J. Biol. Chem. 278 (2003) 23251-23259
8. Chemla Y.R., Aathavan K., Michaelis J., Grimes S., Jardine P.J., Anderson D.L., and Bustamante C. Mechanism of force generation of a viral DNA packaging motor. Cell 122 (2005) 683-692
9. Donohue T.J., Chory J., Goldsand T.E., Lynn S.P., and Kaplan S. Structure and physical map of Rhodopseudomonas sphaeroides bacteriophage RS1 DNA. Journal of Virology 55 (1985) 147-157
10. Fujisawa H., Hamada K., Shibata H., and Minagawa T. On the molecular mechanism of DNA translocation during in vitro packaging of bacteriophage T3 DNA. Virology 161 (1987) 228-233
11. Fuller D.N., Rickgauer J.P., Jardine P.J., Grimes S., Anderson D.L., and Smith D.E. Ionic effects on viral DNA packaging and portal motor function in bacteriophage phi 29. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 11245-11250
12. Grimes S., and Anderson D. The bacteriophage phi29 packaging proteins supercoil the DNA ends. J. Mol. Biol. 266 (1997) 901-914
13. Grimes S., and Anderson D. RNA dependence of the bacteriophage phi29 DNA packaging ATPase. J. Mol. Biol. 215 (1990) 559-566
14. Guasch A., Pous J., Ibarra B., Gomis-Ruth F.X., Valpuesta J.M., Sousa N., Carrascosa J.L., and Coll M. Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage phi29 connector particle. J. Mol. Biol. 315 (2002) 663-676
15. Guo P., Peterson C., and Anderson D. Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage φ{symbol}29. J. Mol. Biol. 197 (1987) 229-236
16. Guo P., Zhang C., Chen C., Trottier M., and Garver K. Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation. Molecular Cell 2 (1998) 149-155
17. Guo P., and Lee T.J. Viral nanomotors for packaging of dsDNA and dsRNA. Molecular Microbiology 64 (2007) 886-903
18. Ha T., Rasnik I., Cheng W., Babcock H.P., Gauss G.H., Lohman T.M., and Chu S. Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature 419 (2002) 638-641
19. Hayward G.S., and Smith M.G. The chromosome of bacteriophage T5. II. Arrangement of the single-stranded DNA fragments in the T5 + and T5st(O) chromosomes. J. Mol. Biol. 63 (1972) 397-407
20. He Z.H., Chillingworth R.K., Brune M., Corrie J.E., Trentham D.R., Webb M.R., and Ferenczi M.A. ATPase kinetics on activation of rabbit and frog permeabilized isometric muscle fibres: a real time phosphate assay. J. Physiol. 501 (1997) 125-148
21. Huang L.P., and Guo P. Use of acetone to attain highly active and soluble DNA packaging protein gp16 of phi29 for ATPase assay. Virology 312 2 (2003) 449-457
22. Huang L.P., and Guo P. Use of PEG to acquire highly soluble DNA-packaging enzyme gp16 of bacterial virus phi29 for stoichiometry quantification. J. Virol. Methods 109 (2003) 235-244
23. Hugel T., Michaelis J., Hetherington C.L., Jardine P.J., Grimes S., Walter J.M., Faik W., Anderson D.L., and Bustamante C. Experimental test of connector rotation during DNA packaging into bacteriophage phi 29 capsids. Plos Biology 5 (2007) 558-567
24. Hwang Y., Catalano C.E., and Feiss M. Kinetic and mutational dissection of the two ATPase activities of terminase, the DNA packaging enzyme of bacteriophage lambda. Biochemistry 35 (1996) 2796-2803
25. Ibarra B., Caston J.R., Llorca O., Valle M., Valpuesta J.M., and Carrascosa J.L. Topology of the components of the DNA packaging machinery in the phage phi29 prohead. J. Mol. Biol. 298 (2000) 807-815
26. Ibarra B., Valpuesta J.M., and Carrascosa J.L. Purification and functional characterization of p16, the ATPase of the bacteriophage phi29 packaging machinery. Nucleic Acids Research 29 21 (2001) 4264-4273
27. Khan S.A., Hayes S.J., Wright E.T., Watson R.H., and Serwer P. Specific single-stranded breaks in mature bacteriophage T7 DNA. Virology 211 (1995) 329-331
28. Lee C.S., and Guo P. In vitro assembly of infectious virions of ds-DNA phage φ{symbol}29 from cloned gene products and synthetic nucleic acids. Journal of Virology 69 (1995) 5018-5023
29. Lee T.J., and Guo P. Interaction of gp16 with pRNA and DNA for genome packaging by the motor of bacterial virus phi29. J. Mol. Biol. 356 (2006) 589-599
30. Moll D., and Guo P. Translocation of nicked but not gapped DNA by the packaging motor of bacteriophage phi29. J. Mol. Biol. 351 (2005) 100-107
31. Morita M., Tasaka M., and Fujisawa H. DNA packaging ATPase of bacteriophage T3. Virology 193 (1993) 748-752
32. Shu D., and Guo P. A Viral RNA that binds ATP and contains a motif similar to an ATP-binding aptamer from SELEX. J. Biol. Chem. 278 9 (2003) 7119-7125
33. Shu D., and Guo P. Only one pRNA hexamer but multiple copies of the DNA-packaging protein gp16 are needed for the motor to package bacterial virus phi29 genomic DNA. Virology 309 1 (2003) 108-113
34. Shu D., Zhang H., Jin J., and Guo P. Counting of six pRNAs of phi29 DNA-packaging motor with customized single molecule dual-view system. The EMBO Journal 26 (2007) 527-537
35. Simpson A.A., Leiman P.G., Tao Y., He Y., Badasso M.O., Jardine P.J., Anderson D.L., and Rossman M.G. Structure determination of the head-tail connector of bacteriophage phi29. Acta. Cryst. D57 (2001) 1260-1269
36. Simpson A.A., Tao Y., Leiman P.G., Badasso M.O., He Y., Jardine P.J., Olson N.H., Morais M.C., Grimes S., Anderson D.L., Baker T.S., and Rossmann M.G. Structure of the bacteriophage phi29 DNA packaging motor. Nature 408 (2000) 745-750
37. Smith D.E., Tans S.J., Smith S.B., Grimes S., Anderson D.L., and Bustamante C. The bacteriophage phi29 portal motor can package DNA against a large internal force. Nature 413 (2001) 748-752
38. Wei N., Hacker D.L., and Morris T.J. Characterization of an Internal Element in Turnip Crinkle Virus RNA Involved in Both Coat Protein Binding and Replication. Virology 190 (1992) 346-355
39. Zhang F., Lemieux S., Wu X., St.-Arnaud S., McMurray C.T., Major F., and Anderson D. Function of hexameric RNA in packaging of bacteriophage phi29 DNA in vitro. Molecular Cell 2 (1998) 141-147
40. Zhang H., Shu D., Huang F., and Guo P. Instrumentation and metrology for single RNA counting in biological complexes or nanoparticles by a single molecule dual-view system. RNA 13 (2007) 1793-1802