Sequential action of ATPase, ATP, ADP, Pi and dsDNA in procapsid-free system to enlighten mechanism in viral dsDNA packaging

Nucleic Acids Research

Volumn 40, Issue 6, 2012, Pages 2577-2586

  Schwartz, Chad ^a   Fang, Huaming ^a   Huang, Lisa ^b   Guo, Peixuan ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

^b Medical Diagnostic Laboratories LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DOUBLE STRANDED DNA; VIRUS DNA;

ARTICLE; BACTERIOPHAGE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA BINDING; DNA HELIX; DNA METABOLISM; DNA PACKAGING; DNA SEQUENCE; DNA TRANSFER; ENERGY CONVERSION; HYDROLYSIS; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; VIRUS CAPSID;

ADENOSINE DIPHOSPHATE; ADENOSINE MONOPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BACILLUS PHAGES; CAPSID; DNA, VIRAL; PHOSPHATES; VIRAL PROTEINS; VIRUS ASSEMBLY;

BACILLUS PHAGE PHI29; DNA VIRUSES;

EID: 84859298657     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr841     Document Type: Article

References (63)

1. Ammelburg, M., Frickey, T. and Lupas, A.N. (2006) Classification of AAA+proteins. J. Struct. Biol., 156, 2-11
2. Frickey, T. and Lupas, A.N. (2004) Phylogenetic analysis of AAA proteins. J. Struct. Biol., 146, 2-10 (Pubitemid 38369014)
3. Iyer, L.M., Leipe, D.D., Koonin, E.V. and Aravind, L. (2004) Evolutionary history and higher order classification of AAA plus ATPases. J. Struct. Biol., 146, 11-31 (Pubitemid 38369015)
4. Hanson, P.I. and Whiteheart, S.W. (2005) AAA+proteins: Have engine, will work. Nat. Rev. Mol. Cell Biol., 6, 519-529 (Pubitemid 40943043)
5. Singleton, M.R., Dillingham, M.S. and Wigley, D.B. (2007) Structure and mechanism of helicases and nucleic acid translocases. Ann. Rev. Biochem., 76, 23-50
6. Pyle, A.M. (2008) Translocation and unwinding mechanisms of RNA and DNA helicases. Annu. Rev. Biophys., 37, 317-336
7. Wang, J. (2004) Nucleotide-dependent domain motions within rings of the RecA/AAA(+) superfamily. J. Struct. Biol., 148, 259-267 (Pubitemid 39441363)
8. Iyer, L.M., Makarova, K.S., Koonin, E.V. and Aravind, L. (2004) Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res., 32, 5260-5279 (Pubitemid 39445514)
9. Guo, P.X. and Lee, T.J. (2007) Viral nanomotors for packaging of dsDNA and dsRNA. Mol. Microbiol., 64, 886-903 (Pubitemid 46743960)
10. Rao, V.B. and Feiss, M. (2008) The bacteriophage DNA packaging motor. Annu. Rev. Genet., 42, 647-681
11. Guo, P., Peterson, C. and Anderson, D. (1987) Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage f29. J. Mol. Biol., 197, 229-236
12. 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)
13. Hwang, Y., Catalano, C.E. and Feiss, M. (1996) Kinetic and mutational dissection of the two ATPase activities of terminase, the DNA packaging enzyme of bacteriophage lambda. Biochemistry, 35, 2796-2803 (Pubitemid 26099926)
14. Sabanayagam, C.R., Oram, M., Lakowicz, J.R. and Black, L.W. (2007) Viral DNA packaging studied by fluorescence correlation spectroscopy. Biophys. J., 93, L17-L19 (Pubitemid 47330887)
15. Guo, P., Zhang, C., Chen, C., Trottier, M. and Garver, K. (1998) Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation. Mol. Cell, 2, 149-155 (Pubitemid 128378977)
16. Guo, P., Peterson, C. and Anderson, D. (1987) Initiation events in in vitro packaging of bacteriophage f29 DNA-gp3. J. Mol. Biol., 197, 219-228
17. Huang, L.P. and Guo, P. (2003) Use of acetone to attain highly active and soluble DNA packaging protein gp16 of phi29 for ATPase assay. Virology, 312, 449-457 (Pubitemid 36960019)
18. Huang, L.P. and Guo, P. (2003) Use of PEG to acquire highly soluble DNA-packaging enzyme gp16 of bacterial virus phi29 for stoichiometry quantification. J. Virol. Methods, 109, 235-244 (Pubitemid 36507113)
19. Lee, T.J. and Guo, P. (2006) Interaction of gp16 with pRNA and DNA for genome packaging by the motor of bacterial virus phi29. J. Mol Biol., 356, 589-599 (Pubitemid 43139322)
20. Lee, T.J., Zhang, H., Liang, D. and Guo, P. (2008) Strand and nucleotide-dependent ATPase activity of gp16 of bacterial virus phi29 DNA packaging motor. Virology, 380, 69-74
21. Ibarra, B., Valpuesta, J.M. and Carrascosa, J.L. (2001) Purification and functional characterization of p16, the ATPase of the bacteriophage phi29 packaging machinary. Nucleic Acids Res., 29, 4264-4273 (Pubitemid 33064767)
22. Grimes, S. and Anderson, D. (1990) RNA dependence of the bateriophage phi29 DNA packaging ATPase. J. Mol. Biol., 215, 559-566 (Pubitemid 20361392)
23. Guo, P., Erickson, S. and Anderson, D. (1987) A small viral RNA is required for in vitro packaging of bacteriophage phi29 DNA. Science, 236, 690-694 (Pubitemid 17076855)
24. Shu, D., Zhang, H., Jin, J. and Guo, P. (2007) Counting of six pRNAs of phi29 DNA-packaging motor with customized single molecule dual-view system. EMBO J., 26, 527-537 (Pubitemid 46160952)
25. Smith, D.E., Tans, S.J., Smith, S.B., Grimes, S., Anderson, D.L. and Bustamante, C. (2001) The bacteriophage phi29 portal motor can package DNA against a large internal force. Nature, 413, 748-752 (Pubitemid 33009954)
26. Guo, P., Grimes, S. and Anderson, D. (1986) A defined system for in vitro packaging of DNA-gp3 of the Bacillus subtilis bacteriophage phi29. Proc. Natl Acad. Sci. USA, 83, 3505-3509 (Pubitemid 16051995)
27. Koti, J.S., Morais, M.C., Rajagopal, R., Owen, B.A., McMurray, C.T. and Anderson, D. (2008) DNA packaging motor assembly intermediate of bacteriophage phi29. J. Mol. Biol., 381, 1114-1132
28. Chen, C. and Guo, P. (1997) Sequential action of six virus-encoded DNA-packaging RNAs during phage phi29 genomic DNA translocation. J. Virol., 71, 3864-3871 (Pubitemid 27172400)
29. 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
30. Earnshaw, W.C. and Casjens, S.R. (1980) DNA packaging by the double-stranded DNA bacteriophages. Cell, 21, 319-331 (Pubitemid 10047085)
31. Shu, D. and Guo, P. (2003) A Viral RNA that binds ATP and contains an motif similar to an ATP-binding aptamer from SELEX. J. Biol. Chem., 278, 7119-7125 (Pubitemid 36800709)
32. Lee, T.J., Zhang, H., Chang, C.L., Savran, C. and Guo, P. (2009) Engineering of the fluorescent-energy-conversion arm of phi29 DNA packaging motor for single-molecule studies. Small, 5, 2453-2459
33. Geng, J., Fang, H., Haque, F., Zhang, L. and Guo, P. (2011) Three reversible and controllable discrete steps of channel gating of a viral DNA packaging motor. Biomaterials, 32, 8234-8242
34. Lee, C.S. and Guo, P. (1994) A highly sensitive system for the in vitro assembly of bacteriophage phi29 of Bacillus subtilis. Virology, 202, 1039-1042
35. Lee, T.J., Schwartz, C. and Guo, P. (2009) Construction of bacteriophage phi29 DNA packaging motor and its applications in nanotechnology and therapy. Ann. Biomed. Eng., 37, 2064-2081
36. Shu, D. and Guo, P. (2003) 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, 108-113 (Pubitemid 36506594)
37. Khan, S.A., Hayes, S.J., Wright, E.T., Watson, R.H. and Serwer, P. (1995) Specific single-stranded breaks in mature bacteriophage T7 DNA. Virology, 211, 329-331
38. Serwer, P. (2003) Models of bacteriophage DNA packaging motors. J. Struct. Biol., 141, 179-188 (Pubitemid 36332010)
39. Astumian, R.D. (1997) Thermodynamics and kinetics of a Brownian motor. Science, 276, 917-922 (Pubitemid 27209083)
40. Hendrix, R.W. (1978) Symmetry mismatch and DNA packaging in large bacteriophages. Proc. Natl Acad. Sci. USA, 75, 4779-4783 (Pubitemid 9048617)
41. Grimes, S. and Anderson, D. (1997) The bacteriophage phi29 packaging proteins supercoil the DNA ends. J. Mol. Biol., 266, 901-914 (Pubitemid 27122597)
42. Guasch, A., Pous, J., Ibarra, B., Gomis-Ruth, F.X., Valpuesta, J.M., Sousa, N., Carrascosa, J.L. and Coll, M. (2002) Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage phi29 connector particle. J. Mol. Biol., 315, 663-676 (Pubitemid 34729317)
43. Hou, X., Yang, F., Li, L., Song, Y., Jiang, L. and Zhu, D. (2010) A biomimetic asymmetric responsive single nanochannel. J. Am. Chem. Soc., 132, 11736-11742
44. Morita, M., Tasaka, M. and Fujisawa, H. (1995) Structural and functional domains of the large subunit of the bacteriophage T3 DNA packaging enzyme: importance of the C-terminal region in prohead binding. J. Mol. Biol., 245, 635-644
45. Oram, M., Sabanayagam, C. and Black, L.W. (2008) Modulation of the packaging reaction of bacteriophage T4 terminase by DNA structure. J. Mol. Biol., 381, 61-72
46. Lisal, J., Kainov, D.E., Bamford, D.H., Thomas, G.J. Jr and Tuma, R. (2004) Enzymatic mechanism of RNA translocation in double-stranded RNA bacteriophages. J. Biol. Chem., 279, 1343-1350 (Pubitemid 38082660)
47. Jing, P., Haque, F., Shu, D., Montemagno, C. and Guo, P. (2010) One-way traffic of a viral motor channel for double-stranded DNA translocation. Nano Lett., 10, 3620-3627
48. Ray, K., Sabanayagam, C.R., Lakowicz, J.R. and Black, L.W. (2010) DNA crunching by a viral packaging motor: Compression of a procapsid-portal stalled Y-DNA substrate. Virology, 398, 224-232
49. Ray, K., Ma, J., Oram, M., Lakowicz, J.R. and Black, L.W. (2010) Single-molecule and FRET fluorescence correlation spectroscopy analyses of phage DNA packaging: colocalization of packaged phage T4 DNA ends within the capsid. J. Mol. Biol., 395, 1102-1113
50. Dixit, A., Ray, K., Lakowicz, J.R. and Black, L.W. (2011) Dynamics of the T4 bacteriophage DNA packasome motor endonuclease VII resolvase release of arrested Y-DNA substrates. J. Biol. Chem., 286, 18878-18889
51. Hess, H. and Vogel, V. (2001) Molecular shuttles based on motor proteins: Active transport in synthetic environments. J. Biotechnol., 82, 67-85 (Pubitemid 34179617)
52. Lowe, J., Ellonen, A., Allen, M.D., Atkinson, C., Sherratt, D.J. and Grainge, I. (2008) Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol. Cell, 31, 498-509
53. Skordalakes, E. and Berger, J.M. (2006) Structural insights into RNA-dependent ring closure and ATPase activation by the Rho termination factor. Cell, 127, 553-564 (Pubitemid 44647425)
54. Matias, P.M., Gorynia, S., Donner, P. and Carrondo, M.A. (2006) Crystal structure of the human AAA+protein RuvBL1. J. Biol. Chem., 281, 38918-38929 (Pubitemid 46042018)
55. McGeoch, A.T., Trakselis, M.A., Laskey, R.A. and Bell, S.D. (2005) Organization of the archaeal MCM complex on DNA and implications for the helicase mechanism. Nat. Struct. Mol. Biol., 12, 756-762 (Pubitemid 43086249)
56. Lisal, J. and Tuma, R. (2005) Cooperative mechanism of RNA packaging motor. J. Biol. Chem., 280, 23157-23164 (Pubitemid 40853227)
57. Mancini, E.J., Kainov, D.E., Grimes, J.M., Tuma, R., Bamford, D.H. and Stuart, D.I. (2004) Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell, 118, 743-755 (Pubitemid 39221733)
58. Xiao, F., Zhang, H. and Guo, P. (2008) Novel mechanism of hexamer ring assembly in protein/RNA interactions revealed by single molecule imaging. Nucleic Acids Res., 36, 6620-6632
59. Morita, M., Tasaka, M. and Fujisawa, H. (1993) DNA packaging ATPase of bacteriophage T3. Virology, 193, 748-752
60. Sun, S., Kondabagil, K., Draper, B., Alam, T.I., Bowman, V.D., Zhang, Z., Hegde, S., Fokine, A., Rossmann, M.G. and Rao, V.B. (2008) The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell, 135, 1251-1262
61. Roos, W.H., Ivanovska, I.L., Evilevitch, A. and Wuite, G.J.L. (2007) Viral capsids: mechanical characteristics, genome packaging and delivery mechanisms. Cell. Mol. Life Sci., 64, 1484-1497 (Pubitemid 46954149)
62. Aathavan, K., Politzer, A.T., Kaplan, A., Moffitt, J.R., Chemla, Y.R., Grimes, S., Jardine, P.J., Anderson, D.L. and Bustamante, C. (2009) Substrate interactions and promiscuity in a viral DNA packaging motor. Nature, 461, 669-673
63. Yu, J., Moffitt, J., Hetherington, C.L., Bustamante, C. and Oster, G. (2010) Mechanochemistry of a viral DNA packaging motor. J. Mol. Biol., 400, 186-203.