Novel mechanism of hexamer ring assembly in protein/RNA interactions revealed by single molecule imaging

Nucleic Acids Research

Volumn 36, Issue 20, 2008, Pages 6620-6632

  Xiao, Feng ^a   Zhang, Hui ^a   Guo, Peixuan ^a  

^a University of Cincinnati   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA;

ARTICLE; BACTERIOPHAGE; BINDING AFFINITY; BLEACHING; COMPLEX FORMATION; DNA PACKAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN RNA BINDING; RNA SEQUENCE; RNA STRUCTURE; STOICHIOMETRY; VIRION;

BACILLUS PHAGES; BASE SEQUENCE; CAPSID; CAPSID PROTEINS; DNA PACKAGING; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; RNA, VIRAL; RNA-BINDING PROTEINS; TERMINOLOGY AS TOPIC; VIRION; VIRUS ASSEMBLY;

BACILLUS PHAGE PHI29;

EID: 56649091437     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn669     Document Type: Article

References (90)

1. Enemark,E.J. and Joshua-Tor,L. (2006) Mechanism of DNA translocation in a replicative hexameric helicase. Nature, 442, 270-275.
2. West,S.C. (1996) DNA helicases: New breeds of translocating motors and molecular pumps. Cell, 86, 177-180.
3. Kainov,D.E., Mancini,E.J., Telenius,J., Lisai,J., Grimes,J.M., Bamford,D.H., Stuart,D.I. and Tuma,R. (2008) Structural basis of mechanochemical coupling in a hexameric molecular motor. J. Biol. Chem., 283, 3607-3617.
4. Ciampi,M.S. (2006) Rho-dependent terminators and transcription termination. Microbiology, 152, 2515-2528.
5. Geiselmann,J., Wang,Y., Seifried,S.E. and von Hippel,P.H. (1993) A physical model for the translocation and helicase activities of Escherichia coli transcription termination protein rho. Proc. Natl Acad. Sci. USA, 90, 7754-7758.
6. Mayanagi,K., Miyata,T., Oyama,T., Ishino,Y. and Morikawa,K. (2001) Three-dimensional electron microscopy of the clamp loader small subunit from Pyrococcus furiosus. J. Struct. Biol., 134, 35-45.
7. VanLoock,M.S., Alexandrov,A., Yu,X., Cozzarelli,N.R. and Egelman,E.H. (2002) SV40 large T antigen hexamer structure: Domain organization and DNA-induced conformational changes. Curr. Biol., 12, 472-476.
8. Jeruzalmi,D., O'Donnell,M. and Kuriyan,J. (2002) Clamp loaders and sliding clamps. Curr. Opin. Struct. Biol., 12, 217-224.
9. Cramer,P., Bushnell,D.A. and Kornberg,R.D. (2001) Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science 292, 1863-1876.
10. Martin,A., Baker,T.A. and Sauer,R.T. (2005) Rebuilt AAA + motors reveal operating principles for ATP-fuelled machines. Nature, 437, 1115-1120.
11. Hanson,P.I. and Whiteheart,S.W. (2005) AAA + proteins: Have engine, will work. Nat. Rev. Mol. Cell. Biol., 6, 519-529.
12. Hishida,T., Han,Y.W., Fujimoto,S., Iwasaki,H. and Shinagawa,H. (2004) Direct evidence that a conserved arginine in RuvB AAA(+) ATPase acts as an allosteric e.ector for the ATPase activity of the adjacent subunit in a hexamer. Proc. Natl Acad. Sci. USA, 101, 9573-9577.
13. Willows,R.D., Hansson,A., Birch,D., Al-Karadaghi,S. and Hansson,M. (2004) EM single particle analysis of the ATP-dependent BchI complex of magnesium chelatase: An AAA(+) hexamer. J. Struct. Biol., 146 227-233.
14. Aker,J., Hesselink,R., Engel,R., Karlova,R., Borst,J.W., Visser,A.J.W.G. and de Vries,S.C. (2007) In vivo hexamerization and characterization of the Arabidopsis AAA ATPase CDC48A complex using forster resonance energy transfer-fluorescence lifetime imaging microscopy and fluorescence correlation spectroscopy. Plant Physiol. 145, 339-350.
15. Brion,P. and Westhof,E. (1997) Hierarchy and dynamics of RNA folding. Ann. Rev. Biophys. Biomol. Struct., 26, 113-137.
16. Pan,T., Long,D.M. and Uhlenbeck,O.C. (1993) Divalent metal ions in RNA folding and catalysis. In Gesteland,R.F. and Atkins,J.F. (eds), RNA World, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 271-302.
17. Bernacchi,S., Freisz,S., Maechling,C., Spiess,B., Marquet,R., Dumas,P. and Ennifar,E. (2007) Aminoglycoside binding to the HIV-1 RNA dimerization initiation site: Thermodynamics and effect on the kissing-loop to duplex conversion. Nucleic Acids Res., 35, 7128-7139.
18. Guerrier-Takada,C., Gardiner,K., Marsh,T., Pace,N. and Altman,S. (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell, 35, 849-857.
19. Sarver,N., Cantin,E.M., Chang,P.S., Zaia,J.A., Ladne,P.A., Stephens,D.A. and Rossi,J.J. (1990) Ribozymes as potential anti-HIV-1 therapeutic agents. Science, 247, 1222-1225.
20. Kruger,K., Grabowski,P.J., Zaug,A.J., Sands,J., Gottschling,D.E. and Cech,T.R. (1982) Self-splicing RNA: Autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell, 31 147-157.
21. Leulliot,N. and Varani,G. (2001) Current topics in RNA-protein recognition: Control of specificity and biological function through induced fit and conformational capture. Biochemistry, 40, 7947-7956.
22. Williamson,J.R. (2000) Induced fit in RNA-protein recognition. Nat. Struct. Biol., 7, 834-837.
23. Catalano,C.E., Cue,D. and Feiss,M. (1995) Virus DNA packaging: The strategy used by phage lambda. Mol. Microbiol., 16, 1075-1086.
24. Molineux,I.J. (2001) No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. Mol. Microbiol., 40, 1-8.
25. Conway,J.F., Wiko.,W.R., Cheng,N., Duda,R.L., Hendrix,R.W., Johnson,J.E. and Steven,A.C. (2001) Virus maturation involving large subunit rotations and local refolding. Science, 292, 744-748.
26. Hendrix,R.W. (1978) Symmetry mismatch and DNA packaging in large bacteriophages. Proc. Natl Acad. Sci. USA, 75, 4779-4783.
27. Johnson,J.E. and Chiu,W. (2007) DNA packaging and delivery machines in tailed bacteriophages. Curr. Opin. Struct. Biol., 17, 237-243.
28. Guo,P.X. and Lee,T.J. (2007) Viral nanomotors for packaging of dsDNA and dsRNA. Mol. Microbiol., 64, 886-903.
29. 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.
30. Simpson,A.A., Leiman,P.G., Tao,Y., He,Y., Badasso,M.O., Jardine,P.J., Anderson,D.L. and Rossman,M.G. (2001) Structure determination of the head-tail connector of bacteriophage phi29. Acta Cryst., D57 1260-1269.
31. Lander,G.C., Tang,L., Casjens,S.R., Gilcrease,E.B., Prevelige,P., Poliakov,A., Potter,C.S., Carragher,B. and Johnson,J.E. (2006) The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science, 312, 1791-1795.
32. Lebedev,A.A., Krause,M.H., Isidro,A.L., Vagin,A.A., Orlova,E.V., Turner,J., Dodson,E.J., Tavares,P. and Antson,A.A. (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J. 26, 1984-1994.
33. Baumann,R.G., Mullaney,J. and Black,L.W. (2006) Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol. Microbiol., 61, 16-32.
34. Guo,P., Peterson,C. and Anderson,D. (1987) Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi29. J. Mol. Biol., 197, 229-236.
35. Hang,J.Q., Tack,B.F. and Feiss,M. (2000) ATPase center of bacteriophage lambda terminase involved in post-cleavage stages of DNA packaging: identification of ATP-interactive amino acids. J. Mol. Biol., 302, 777-795.
36. Higgins,R.R., Lucko,H.J. and Becker,A. (1988) Mechanism of cos DNA cleavage by bacteriophage lambda terminase-multiple roles of ATP. Cell, 54, 765-775.
37. Hwang,J.S. and Bogner,E. (2002) ATPase activity of the terminase subunit pUL56 of human cytomegalovirus. J. Biol. Chem., 277 6943-6948.
38. Gual,A., Camacho,A.G. and Alonso,J.C. (2000) Functional analysis of the terminase large subunit, G2P, of Bacillus subtilis bacteriophage SPP1. J. Biol. Chem., 275, 35311-35319.
39. 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.
40. Manne,V.S., Rao,V.B. and Black,L.W. (1982) A bacteriophage T4 DNA packaging related DNA-dependent ATPase-endonuclease. J. Biol. Chem. 257, 13223-13232.
41. 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.
42. Trottier,M. and Guo,P. (1997) Approaches to determine stoichiometry of viral assembly components. J. Virol., 71, 487-494.
43. 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.
44. 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.
45. Guo,P. (2002) Structure and function of phi29 hexameric RNA that drive viral DNA packaging motor: Review. Prog. in Nucl. Acid Res. & Mole. Biol., 72, 415-472.
46. 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.
47. Reid,R.J.D., Bodley,J.W. and Anderson,D. (1994) Characterization of the prohead-pRNA interaction of bacteriophage phi29. J. Biol. Chem., 269, 5157-5162.
48. Hoeprich,S. and Guo,P. (2002) Computer modeling of three-dimensional structure of DNA-packaging RNA(pRNA) monomer, dimer, and hexamer of phi29 DNA Packaging motor. J. Biol. Chem., 277, 20794-20803.
49. Garver,K. and Guo,P. (1997) Boundary of pRNA functional domains and minimum pRNA sequence requirement for specific connector binding and DNA packaging of phage phi29. RNA, 3, 1068-1079.
50. Trottier,M., Mat-Arip,Y., Zhang,C., Chen,C., Sheng,S., Shao,Z. and Guo,P. (2000) Probing the structure of monomers and dimers of the bacterial virus phi29 hexamer RNA complex by chemical modification. RNA, 6, 1257-1266.
51. Mat-Arip,Y., Garver,K., Chen,C., Sheng,S., Shao,Z. and Guo,P. (2001) Three-dimensional interaction of phi29 pRNA dimer probed by chemical modification interference, cryo-AFM, and cross-linking. J. Biol. Chem., 276, 32575-32584.
52. Zhang,C.L., Tellinghuisen,T. and Guo,P. (1997) Use of circular permutation to assess six bulges and four loops of DNA-Packaging pRNA of bacteriophage phi29. RNA, 3, 315-322.
53. Atz,R., Ma,S., Gao,J., Anderson,D.L. and Grimes,S. (2007) Alanine Scanning and Fe-BABE Probing of the Bacteriophage phi29 Prohead RNA-Connector Interaction. J. Mol. Biol., 369, 239-248.
54. Trottier,M., Zhang,C.L. and Guo,P. (1996) Complete inhibition of virion assembly in vivo with mutant pRNA essential for phage phi29 DNA packaging. J. Virol., 70, 55-61.
55. Chen,C., Sheng,S., Shao,Z. and Guo,P. (2000) A dimer as a building block in assembling RNA: A hexamer that gears bacterial virus phi29 DNA-translocating machinery. J. Biol. Chem., 275, 17510-17516.
56. Chen,C., Zhang,C. and Guo,P. (1999) Sequence requirement for hand-in-hand interaction in formation of pRNA dimers and hexamers to gear phi29 DNA translocation motor. RNA, 5, 805-818.
57. 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.
58. Zhang,F., Lemieux,S.,Wu,X., St-Arnaud,S.,McMurray,C.T., Major,F. and Anderson,D. (1998) Function of hexameric RNA in packaging of bacteriophage phi29 DNA in vitro. Mol. Cell., 2, 141-147.
59. Reid,R.J.D., Bodley,J.W. and Anderson,D. (1994) Identification of bacteriophage phi29 prohead RNA (pRNA) domains necessary for in vitro DNA-gp3 packaging. J. Biol. Chem., 269, 9084-9089.
60. Xiao,F., Moll,D., Guo,S. and Guo,P. (2005) Binding of pRNA to the N-terminal 14 amino acids of connector protein of bacterial phage phi29. Nucleic Acids Res., 33, 2640-2649.
61. Cai,Y., Xiao,F. and Guo,P. (2008) N- or C-terminal alterations of motor protein gp10 of bacterial virus phi29 on procapsid assembly, pRNA binding and DNA packaging. Nanomedicine, 4, 8-18.
62. Reid,R.J.D., Zhang,F., Benson,S. and Anderson,D. (1994) Probing the structure of bacteriophage phi29 prohead RNA with specific mutations. J. Biol. Chem., 269, 18656-18661.
63. Zhang,C.L., Lee,C.-S. and Guo,P. (1994) The proximate 5′ and 3′ ends of the 120-base viral RNA (pRNA) are crucial for the packaging of bacteriophage φ29 DNA. Virology, 201, 77-85.
64. Wichitwechkarn,J., Darrin Johnson and Dwight Anderson. (1992) Mutant prohead RNAs in Vitro packaging of bacteriophage phi29 DNA-gp3. Mol. Biol., 223, 991-998.
65. 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.
66. Fang,Y., Shu,D., Xiao,F., Guo,P. and Qin,P.Z. (2008) Modular assembly of chimeric phi29 packaging RNAs that support DNA packaging. Biochem. Biophys. Res. Commun., 372, 589-594.
67. Morais,M.C., Tao,Y., Olson,N.H., Grimes,S., Jardine,P.J., Anderson,D.L., Baker,T.S. and Rossmann,M.G. (2001) Cryoelectron-microscopy image reconstruction of symmetry mismatches in bacteriophage phi29. J. Struct. Biol., 135, 38-46.
68. Ibarra,B., Caston,J.R., Llorca,O., Valle,M., Valpuesta,J.M. and Carrascosa,J.L. (2000) Topology of the components of the DNA packaging machinery in the phage phi29 prohead. J. Mol. Biol., 298, 807-815.
69. 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. et al. (2000) Structure of the bacteriophage phi29 DNA packaging motor. Nature, 408, 745-750.
70. Morais,M.C., Koti,J.S., Bowman,V.D., Reyes-Aldrete,E., Anderson,D and Rossman,M.G. (2008) De.ning molecular and domain boundaries in the bacteriophage phi29 DNA packaging motor. Structure, 16, 1267-1274.
71. Huang,F., Wang,G., Coleman,T. and Li,N. (2003) Synthesis of adenosine derivatives as transcription initiators and preparation of 5′ fluorescein- and biotin-labeled RNA through one-step in vitro transcription. RNA, 9, 1562-1570.
72. Zhang,H., Shu,D., Huang,F. and Guo,P. (2007) Instrumentation and metrology for single RNA counting in biological complexes or nanoparticles by a single molecule dual-view system. RNA, 13 1793-1802.
73. Milligan,J.F., Groebe,D.R., Witherell,G.W. and Uhlenbeck,O.C. (1987) Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res., 15, 8783-8798.
74. Ha,T., Rasnik,I., Cheng,W., Babcock,H.P., Gauss,G.H., Lohman,T.M. and Chu,S. (2002) Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature, 419, 638-641.
75. 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.
76. Guo,P., Rajogopal,B., Anderson,D., Erickson,S. and Lee,C.-S. (1991) sRNA of bacteriophage phi29 of B.subtilis mediates DNA packaging of phi29 proheads assembled in E. coli. Virology, 185, 395-400.
77. Moll,D. and Guo,P. (2007) Grouping of ferritin and gold nano-particles conjugated to pRNA of the phage phi29 DNA-packaging motor. J. Nanosci. Nanotech., 7, 3257-3267.
78. Shu,D., Huang,L. and Guo,P. (2003) A simple mathematical formula for stoichiometry quantitation of viral and nanobiological assemblage using slopes of log/log plot curves. J. Virol. Meth., 115, 19-30.
79. 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.
80. Burroughs,A.M., Iyer,L.M. and Aravind,L. (2007) Comparative genomics and evolutionary trajectories of viral ATP dependent DNA-packaging systems. In Volff,J.-N. (ed.), Gene and Protein Evolution. Genome Dyn., Karger, Basel, Vol. 3, pp. 48-65.
81. Song,M.S., Dallmann,H.G. and McHenry,C.S. (2001) Carboxyl-terminal Domain III of the delta ' Subunit of the DNA Polymerase III Holoenzyme Binds delta. J. Biol. Chem., 276, 40668-40679.
82. Niedenzu,T., Roleke,D., Bains,G., Scherzinger,E. and Saenger,W. (2001) Crystal structure of the hexameric replicative helicase RepA of plasmid RSF1010. J. Mol. Biol., 306, 479-487.
83. Gogol,E.P., Seifried,S.E. and von Hippel,P.H. (1991) Structure and assembly of the Escherichia coli transcription termination factor rho and its interaction with RNA. Cryoelectron microscopic studies. J. Mol. Biol., 221, 1127-1138.
84. Burgess,B.R. and Richardson,J.P. (2001) RNA passes through the hole of the protein hexamer in the complex with the Escherichia coli Rho factor. J. Biol. Chem., 276, 4182-4189.
85. Bowers,J., Tran,P.T., Joshi,A., Liskay,R.M. and Alani,E. (2001) MSH-MLH complexes formed at a DNA mismatch are disrupted by the PCNA sliding clamp. J. Mol. Biol., 306, 957-968.
86. Sedman,J. and Stenlund,A. (1998) The papillomavirus E1 protein forms a DNA-dependent hexameric complex with ATPase and DNA helicase activities. J. Virol., 72, 6893-6897.
87. Castella,S., Burgin,D. and Sanders,C.M. (2006) Role of ATP hydrolysis in the DNA translocase activity of the bovine papillomavirus (BPV-1) E1 helicase. Nucleic Acids Res., 34, 3731-3741.
88. Geiduschek,E.P. (1997) Riding the (mono)rails: The structure of catenated DNA-tracking proteins. Chem. & Biol., 2, 123-125.
89. Young,M.C., Schultz,D.E., Ring,D. and von Hippel,P.H. (1994) Kinetic parameters of the translocation of bacteriophage T4 gene 41 protein helicase on single-stranded DNA. J. Mol. Biol., 235, 1447-1458.
90. Herendeen,D.R., Kassavetis,G.A. and Geiduschek,E.P. (1992) A transcriptional enhancer whose function imposes a requirement that proteins track along DNA. Science, 256, 1298-1303.