Kinetic analysis of the genome packaging reaction in bacteriophage λ

Biochemistry

Volumn 48, Issue 45, 2009, Pages 10705-10715

  Yang, Qin ^a   Catalano, Carlos E ^b   Maluf, Nasib Karl ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP HYDROLYSIS; BINARY COMPLEXES; DNA TRANSLOCATION; DNA-PACKAGING; DOUBLE STRANDED DNA; ESCHERICHIA COLI BACTERIA; GENOME PACKAGING; GENOMIC DNA; HEAD-END; KINETIC ANALYSIS; KINETIC MODELS; MECHANICAL STEPS; PROTECTION ASSAY; ROLLING CIRCLE REPLICATIONS; SINGLE-MOLECULE STUDIES; STEP SIZE; STRAND SEPARATION; VIRAL CAPSIDS;

ASSAYS; BACTERIOPHAGES; DNA; ESCHERICHIA COLI; NUCLEIC ACIDS; REACTION KINETICS;

GENES;

ADENOSINE TRIPHOSPHATE; DEOXYRIBONUCLEASE; REPETITIVE DNA;

ARTICLE; BACTERIOPHAGE LAMBDA; DNA DETERMINATION; DNA MODIFICATION; DNA PACKAGING; GENE INSERTION; GENOME; KINETICS; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; ROOM TEMPERATURE; SEQUENTIAL ANALYSIS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BACTERIOPHAGE LAMBDA; DNA PACKAGING; GENOME, VIRAL; KINETICS;

DNA VIRUSES; ENTEROBACTERIA PHAGE LAMBDA; ESCHERICHIA COLI; MIRIDAE;

EID: 70449584723     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901016n     Document Type: Article

References (32)

1. Fuller, D. N., Raymer, D. M., Rickgauer, J. P., Robertson, R. M., Catalano, C. E., Anderson, D. L., Grimes, S., and Smith, D. E. (2007) Measurements of single DNA molecule packaging dynamics in bacteriophage λ reveal high forces, high motor processivity, and capsid transformations. J. Mol. Biol. 373, 1113-1122.
2. Black, L. W. (1989) DNA packaging in dsDNA bacteriophages. Annu. Rev. Microbiol. 43, 267-292.
3. Catalano, C. E. (2000) The terminase enzyme from bacteriophage λ: A DNA-packaging machine. Cell. Mol. Life Sci. 57, 128-148.
4. McConnell, M. J., and Imperiale, M. J. (2004) Biology of adenovirus and its use as a vector for gene therapy. Hum. Gene Ther. 15, 1022-1033.
5. Rao, V. B., and Feiss, M. (2008) The bacteriophage DNA packaging motor. Annu. Rev. Genet. 42, 647-681.
6. Catalano, C. E. (2005) Viral genome packaging machines: Genetics, structure, and mechanism , Kluwer Academic/Plenum Publishers, Georgetown, TX.
7. Maluf, N. K., Gaussier, H., Bogner, E., Feiss, M., and Catalano, C. E. (2006) Assembly of bacteriophage λ terminase into a viral DNA maturation and packaging machine. Biochemistry 45, 15259-15268. (Pubitemid 46032453)
8. Maluf, N. K., Yang, Q., and Catalano, C. E. (2005) Self-association properties of the bacteriophage λ terminase holoenzyme: Implications for the DNA packaging motor. J. Mol. Biol. 347, 523-542.
9. Rice, P. A., Yang, S., Mizuuchi, K., and Nash, H. A. (1996) Crystal structure of an IHF-DNA complex: A protein-induced DNA U-turn. Cell 87, 1295-1306. (Pubitemid 27010112)
10. Chemla, Y. R., Aathavan, K., Michaelis, J., Grimes, S., Jardine, P. J., Anderson, D. L., and Bustamante, C. (2005) Mechanism of force generation of a viral DNA packaging motor. Cell 122, 683-692. (Pubitemid 41242634)
11. Fuller, D. N., Raymer, D. M., Kottadiel, V. I., Rao, V. B., and Smith, D. E. (2007) Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proc. Natl. Acad. Sci. U.S.A. 104, 16868-16873.
12. Moffitt, J. R., Chemla, Y. R., Aathavan, K., Grimes, S., Jardine, P. J., Anderson, D. L., and Bustamante, C. (2009) Intersubunit coordination in a homomeric ring ATPase. Nature 457, 446-450.
13. Smith, D. E., Tans, S. J., Smith, S. B., Grimes, S., Anderson, D. L., and Bustamante, C. (2001) The bacteriophage straight φ29 portal motor can package DNA against a large internal force. Nature 413, 748-752. (Pubitemid 33009954)
14. Yang, Q., and Catalano, C. E. (2003) Biochemical characterization of bacteriophage λ genome packaging in vitro. Virology 305, 276-287. (Pubitemid 36259662)
15. Hang, Q., Woods, L., Feiss, M., and Catalano, C. E. (1999) Cloning, expression, and biochemical characterization of hexahistidine-tagged terminase proteins. J. Biol. Chem. 274, 15305-15314.
16. Nash, H. A., Robertson, C. A., Flamm, E., Weisberg, R. A., and Miller, H. I. (1987) Overproduction of Escherichia coli integration host factor, a protein with nonidentical subunits. J. Bacteriol. 169, 4124-4127.
17. Woods, L., Terpening, C., and Catalano, C. E. (1997) Kinetic analysis of the endonuclease activity of phage λ terminase: Assembly of a catalytically competent nicking complex is rate-limiting. Biochemistry 36, 5777-5785. (Pubitemid 27214929)
18. Yang, Q., and Catalano, C. E. (2004) A minimal kinetic model for a viral DNA packaging machine. Biochemistry 43, 289-299. (Pubitemid 38082550)
19. Lucius, A. L., Maluf, N. K., Fischer, C. J., and Lohman, T. M. (2003) General methods for analysis of sequential "n-step" kinetic mechanisms: Application to single turnover kinetics of helicase-catalyzed DNA unwinding. Biophys. J. 85, 2224-2239.
20. Williams, D. J., and Hall, K. B. (2000) Monte Carlo applications to thermal and chemical denaturation experiments of nucleic acids and proteins. Methods Enzymol. 321, 330-352.
21. Grimes, S., Jardine, P. J., and Anderson, D. (2002) Bacteriophage φ29 DNA packaging. Adv. Virus Res. 58, 255-294.
22. Oliveira, L., Alonso, J. C., and Tavares, P. (2005) A defined in vitro system for DNA packaging by the bacteriophage SPP1: Insights into the headful packaging mechanism. J. Mol. Biol. 353, 529-539.
23. Gaussier, H., Yang, Q., and Catalano, C. E. (2006) Building a Virus from Scratch: Assembly of an Infectious Virus Using Purified Components in a Rigorously Defined Biochemical Assay System. J. Mol. Biol. 357, 1154-1166.
24. Guo, P., Grimes, S., and Anderson, D. (1986) A defined system for in vitro packaging of DNA-gp3 of the Bacillus subtilis bacteriophage φ29. Proc. Natl. Acad. Sci. U.S.A. 83, 3505-3509.
25. Kondabagil, K. R., Zhang, Z., and Rao, V. B. (2006) The DNA translocating ATPase of bacteriophage T4 packaging motor. J. Mol. Biol. 363, 786-799.
26. Yang, Q., Hanagan, A., and Catalano, C. E. (1997) Assembly of a nucleoprotein complex required for DNA packaging by bacteriophage φ. Biochemistry 36, 2744-2752. (Pubitemid 27138555)
27. Lohman, T. M., Tomko, E. J., and Wu, C. G. (2008) Non-hexameric DNA helicases and translocases: Mechanisms and regulation. Nat. Rev. Mol. Cell Biol. 9, 391-401.
28. Duffy, C., and Feiss, M. (2002) The large subunit of bacteriophage λ's terminase plays a role in DNA translocation and packaging termination. J. Mol. Biol. 316, 547-561.
29. Tomka, M. A., and Catalano, C. E. (1993) Kinetic characterization of the ATPase activity of the DNA packaging enzyme from bacteriophage λ. Biochemistry 32, 11992-11997. (Pubitemid 23353636)
30. Higgins, R. R., Lucko, H. J., and Becker, A. (1988) Mechanism of cos DNA cleavage by bacteriophage λ terminase: Multiple roles of ATP. Cell 54, 765-775.
31. Yang, Q., and Catalano, C. E. (1997) Kinetic characterization of the strand separation ("helicase") activity of the DNA packaging enzyme from bacteriophage λ. Biochemistry 36, 10638-10645. (Pubitemid 27382553)
32. Ortega, M. E., Gaussier, H., and Catalano, C. E. (2007) The DNA maturation domain of gpA, the DNA packaging motor protein of bacteriophage λ, contains an ATPase site associated with endonuclease activity. J. Mol. Biol. 373, 851-865.