Revolution rather than rotation of AAA+ hexameric phi29 nanomotor for viral dsDNA packaging without coiling

Virology

Volumn 443, Issue 1, 2013, Pages 28-39

  Schwartz, Chad ^a   De Donatis, Gian Marco ^a   Zhang, Hui ^a   Fang, Huaming ^a   Guo, Peixuan ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

AAA+ family; ATPase; Nanobiotechnology; Packaging mechanism; Viral DNA packaging

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; PHOSPHATE; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS DOUBLE STRANDED DNA;

ARTICLE; BACTERIOPHAGE; BASE PAIRING; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA COILING; DNA HELIX; DNA STRUCTURE; DNA SUPERCOILING; ENZYME BINDING; ENZYME CONFORMATION; ENZYME SUBUNIT; HYDROLYSIS; MOLECULAR DYNAMICS; NANOMOTOR; NONHUMAN; PRIORITY JOURNAL; STOICHIOMETRY; SURFACE CHARGE; VIRUS CAPSID;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BACILLUS PHAGES; DNA PACKAGING; DNA, VIRAL; DNA-BINDING PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION;

BACILLUS PHAGE PHI29;

EID: 84879787373     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.04.019     Document Type: Article

References (99)

1. Aathavan K., Politzer A.T., Kaplan A., Moffitt J.R., Chemla Y.R., Grimes S., Jardine P.J., Anderson D.L., Bustamante C. Substrate interactions and promiscuity in a viral DNA packaging motor. Nature 2009, 461:669-673.
2. Ammelburg M., Frickey T., Lupas A.N. Classification of AAA+ proteins. J. Struct. Biol. 2006, 156:2-11.
3. Astumian R.D. Thermodynamics and kinetics of a Brownian motor. Science. 1997, 276:917-922.
4. Badasso M.O., Leiman P.G., Tao Y., He Y., Ohlendorf D.H., Rossmann M.G., Anderson D. Purification, crystallization and initial X-ray analysis of the head- tail connector of bacteriophage phi29. Acta. Crystallogr. D. Biol. Crystallogr. 2000, 56(Pt 9):1187-1190.
5. Bath J., Wu L.J., Errington J., Wang J.C. Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science. 2000, 290:995-997.
6. Baumann R.G., Mullaney J., Black L.W. Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol. Microbiol. 2006, 61:16-32.
7. Black L.W. DNA Packaging in dsDNA bacteriophages. Annu. Rev. Microbiol. 1989, 43:267-292.
8. Casjens S.R. The DNA-packaging nanomotor of tailed bacteriophages. Nat. Rev.Microbiol. 2011, 9:647-657.
9. Chang C., Zhang H., Shu D., Guo P., Savran C. Bright-field analysis of phi29 DNA packaging motor using a magnetomechanical system. Appl. Phys. Lett. 2008, 93:153902-153902-3.
10. Chemla Y.R., Aathavan K., Michaelis J., Grimes S., Jardine P.J., Anderson D.L., Bustamante C. Mechanism of force generation of a viral DNA packaging motor. Cell 2005, 122:683-692.
11. Chen C., Guo P. Sequential action of six virus-encoded DNA-packaging RNAs during phage phi29 genomic DNA translocation. J. Virol. 1997, 71:3864-3871.
12. Chen C., Trottier M., Guo P. New approaches to stoichiometry determination and mechanism investigation on RNA involved in intermediate reactions. Nucleic Acids Symp. Ser. 1997, 36:190-193.
13. Chistol G., Liu S., Hetherington C.L., Moffitt J.R., Grimes S., Jardine P.J., Bustamante C. High Degree of Coordination and Division of Labor among Subunits in a Homomeric Ring ATPase. Cell 2012, 151:1017-1028.
14. Demarre G., Galli E., Barre F.X. The FtsK family of DNA pumps. Adv. Exp. Med. Biol. 2013, 767:245-262.
15. Ding F., Lu C., Zhao W., Rajashankar K.R., Anderson D.L., Jardine P.J., Grimes S., Ke A. Structure and assembly of the essential RNA ring component of a viral DNA packaging motor. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7357-7362.
16. Egelman H.H., Yu X., Wild R., Hingorani M.M., Patel S.S. Bacteriophage T7 helicase/primase proteins form rings around single- stranded DNA that suggest a general structure for hexameric helicases. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:3869-3873.
17. Fang H., Jing P., Haque F., Guo P. Role of channel lysines and "Push Through a One-way Valve" mechanism of viral DNA packaging motor. Biophys. J. 2012, 102:127-135.
18. Feiss M., Rao V.B. The bacteriophage DNA packaging machine. Adv. Exp. Med. Biol. 2012, 726:489-509.
19. Feiss M., Reynolds E., Schrock M., Sippy J. DNA packaging by lambda-like bacteriophages: mutations broadening the packaging specificity of terminase, the lambda-packaging enzyme 7. Genetics 2010, 184:43-52.
20. Fujisawa H., Shibata H., Kato H. Analysis of interactions among factors involved in the bacteriophage T3 DNA packaging reaction in a defined in vitro system. Virology 1991, 185:788-794.
21. Grainge I. Sporulation: SpoIIIE is the key to cell differentiation. Curr. Biol. 2008, 18:R871-R872.
22. Grainge I., Bregu M., Vazquez M., Sivanathan V., Ip S.C., Sherratt D.J. Unlinking chromosome catenanes in vivo by site-specific recombination. EMBO J. 2007, 26:4228-4238.
23. Grainge I., Lesterlin C., Sherratt D.J. Activation of XerCD-dif recombination by the FtsK DNA translocase. Nucleic Acids Res. 2011, 39:5140-5148.
24. Grimes S., Anderson D. RNA Dependence of the Bateriophage phi29 DNA Packaging ATPase. J. Mol. Biol. 1990, 215:559-566.
25. Grimes S., Anderson D. The bacteriophage phi29 packaging proteins supercoil the DNA ends. J. Mol. Biol. 1997, 266:901-914.
26. Guasch A., Pous J., Ibarra B., Gomis-Ruth F.X., Valpuesta J.M., Sousa N., Carrascosa J.L., Coll M. Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage phi29 connector particle. J. Mol. Biol. 2002, 315:663-676.
27. Guenther B., Onrust R., Sali A., O'Donnell M., Kuriyan J. Crystal structure of the delta' subunit of the clamp-loader complex of E. coli DNA polymerase III. Cell 1997, 91:335-345.
28. Guo P., Erickson S., Anderson D. A small viral RNA is required for in vitro packaging of bacteriophage phi29 DNA. Science. 1987, 236:690-694.
29. Guo P., Grimes S., Anderson D. A defined system for in vitro packaging of DNA-gp3 of the Bacillus subtilis bacteriophage phi29. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:3505-3509.
30. Guo P., Peterson C., Anderson D. Initiation events in in vitro packaging of bacteriophage φ29 DNA-gp3. J. Mol. Biol. 1987, 197:219-228.
31. Guo P., Peterson C., Anderson D. Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage φ29. J. Mol. Biol. 1987, 197:229-236.
32. Guo P., Zhang C., Chen C., Trottier M., Garver K. Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation. Mol. Cell 1998, 2:149-155.
33. Guo P.X., Lee T.J. Viral nanomotors for packaging of dsDNA and dsRNA. Mol. Microbiol. 2007, 64:886-903.
34. Harjes E., Kitamura A., Zhao W., Morais M.C., Jardine P.J., Grimes S., Matsuo H. Structure of the RNA claw of the DNA packaging motor of bacteriophage Phi29. Nucleic Acids Res. 2012, 40:9953-9963.
35. Hendrix R.W. Bacteriophage DNA packaging: RNA gears in a DNA transport machine (Minireview). Cell 1998, 94:147-150.
36. Hendrix R.W. Symmetry mismatch and DNA packaging in large bacteriophages. Proc. Natl. Acad. Sci. U. S. A. 1978, 75:4779-4783.
37. Hou X., Yang F., Li L., Song Y., Jiang L., Zhu D. A biomimetic asymmetric responsive single nanochannel. J. Am. Chem. Soc. 2010, 132:11736-11742.
38. Huang L.P., Guo P. Use of acetone to attain highly active and soluble DNA packaging protein gp16 of phi29 for ATPase assay. Virology 2003, 312:449-457.
39. Huang L.P., Guo P. Use of PEG to acquire highly soluble DNA-packaging enzyme gp16 of bacterial virus phi29 for stoichiometry quantification. J. Virol. Methods 2003, 109:235-244.
40. Hugel T., Michaelis J., Hetherington C.L., Jardine P.J., Grimes S., Walter J.M., Faik W., Anderson D.L., Bustamante C. Experimental test of connector rotation during DNA packaging into bacteriophage phi29 capsids. PLoS Biol. 2007, 5:558-567.
41. Hwang Y., Catalano C.E., Feiss M. Kinetic and mutational dissection of the two ATPase activities of terminase, the DNA packaging enzyme of bacteriophage lambda. Biochemistry 1996, 35:2796-2803.
42. Ibarra B., Valpuesta J.M., Carrascosa J.L. Purification and functional characterization of p16, the ATPase of the bacteriophage phi29 packaging machinary. Nucleic Acids Res. 2001, 29:4264-4273.
43. Iyer L.M., Leipe D.D., Koonin E.V., Aravind L. Evolutionary history and higher order classification of AAA plus ATPases. J. Struct. Biol. 2004, 146:11-31.
44. Iyer L.M., Makarova K.S., Koonin E.V., Aravind L. 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. 2004, 32:5260-5279.
45. Jimenez J., Santisteban A., Carazo J.M., Carrascosa J.L. Computer graphic display method for visualizing three-dimensional biological structures. Science 1986, 232:1113-1115.
46. Jing P., Haque F., Shu D., Montemagno C., Guo P. One-way traffic of a viral motor channel for double-stranded DNA translocation. Nano Lett. 2010, 10:3620-3627.
47. Kad N.M., Wang H., Kennedy G.G., Warshaw D.M., Van H.B. Collaborative dynamic DNA scanning by nucleotide excision repair proteins investigated by single- molecule imaging of quantum-dot-labeled proteins. Mol. Cell 2010, 37:702-713.
48. Kainov D.E., Mancini E.J., Telenius J., Lisai J., Grimes J.M., Bamford D.H., Stuart D.I., Tuma R. Structural basis of mechanochemical coupling in a hexameric molecular motor. J. Biol. Chem. 2008, 283:3607-3617.
49. Koti, J.S., Morais, M.C., Rajagopal, R., Owen, B.A., McMurray, C.T., Anderson, D., 2008. DNA packaging motor assembly intermediate of bacteriophage phi29. J. Mol. Biol. 381, 1114-1132.
50. Khan S.A., Hayes S.J., Wright E.T., Watson R.H., Serwer P. Specific single-stranded breaks in mature bacteriophage T7 DNA. Virology 1995, 211:329-331.
51. Lee C.S., Guo P. A highly sensitive system for the assay of in vitro viral assembly of bacteriophage phi29 of Bacillus subtilis. Virology 1994, 202:1039-1042.
52. Lee T.J., Guo P. Interaction of gp16 with pRNA and DNA for genome packaging by the motor of bacterial virus phi29. J. Mol. Biol. 2006, 356:589-599.
53. Lee T.J., Zhang H., Chang C.L., Savran C., Guo P. Engineering of the fluorescent-energy-conversion arm of phi29 DNA packaging motor for single-molecule studies. Small 2009, 5:2453-2459.
54. Lee T.J., Zhang H., Liang D., Guo P. Strand and nucleotide-dependent ATPase activity of gp16 of bacterial virus phi29 DNA packaging motor. Virology 2008, 380:69-74.
55. Lowe J., Ellonen A., Allen M.D., Atkinson C., Sherratt D.J., Grainge I. Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol. Cell 2008, 31:498-509.
56. Maluf N.K., Feiss M. Virus DNA translocation: progress towards a first ascent of mount pretty difficult. Mol. Microbiol. 2006, 61:1-4.
57. Maluf N.K., Gaussier H., Bogner E., Feiss M., Catalano C.E. Assembly of bacteriophage lambda terminase into a viral DNA maturation and packaging machine. Biochemistry 2006, 45:15259-15268.
58. Martin A., Baker T.A., Sauer R.T. Rebuilt AAA+motors reveal operating principles for ATP-fuelled machines. Nature 2005, 437:1115-1120.
59. Massey T.H., Mercogliano C.P., Yates J., Sherratt D.J., Lowe J. Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol. Cell 2006, 23:457-469.
60. Mastrangelo I.A., Hough P.V., Wall J.S., Dodson M., Dean F.B., Hurwitz J. ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication. Nature 1989, 338:658-662.
61. McNally R., Bowman G.D., Goedken E.R., O'Donnell M., Kuriyan J. Analysis of the role of PCNA-DNA contacts during clamp loading. BMC Struct. Biol. 2010, 10:3.
62. Moffitt J.R., Chemla Y.R., Aathavan K., Grimes S., Jardine P.J., Anderson D.L., Bustamante C. Intersubunit coordination in a homomeric ring ATPase. Nature 2009, 457:446-450.
63. Moll D., Guo P. Grouping of Ferritin and Gold Nanoparticles Conjugated to pRNA of the Phage phi29 DNA-packaging motor. J. Nanosci. Nanotechnol. 2007, 7:3257-3267.
64. Morais M.C., Koti J.S., Bowman V.D., Reyes-Aldrete E., Anderson D, Rossman M.G. Defining molecular and domain boundaries in the bacteriophage phi29 DNA packaging motor. Structure 2008, 16:1267-1274.
65. Morais M.C., Tao Y, Olsen N.H., Grimes S., Jardine P.J., Anderson D., Baker TS, Rossmann M.G. Cryoelectron-Microscopy Image Reconstruction of Symmetry Mismatches in Bacteriophage phi29. J. Struct. Biol. 2001, 135:38-46.
66. Morita M., Tasaka M., Fujisawa H. 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. 1995, 245:635-644.
67. Morita M., Tasaka M., Fujisawa H. DNA packaging ATPase of bacteriophage T3. Virology 1993, 193:748-752.
68. Morita M., Tasaka M., Fujisawa H. Analysis of the fine structure of the prohead binding domain of the packaging protein of bacteriophage T3 using a hexapeptide, an analog of a prohead binding site. Virology 1995, 211:516-524.
69. Mueller-Cajar O., Stotz M., Wendler P., Hartl F.U., Bracher A., Hayer-Hartl M. Structure and function of the AAA+ protein CbbX, a red-type Rubisco activase. Nature 2011, 479:194-199.
70. Niedenzu T., Roleke D., Bains G., Scherzinger E., Saenger W. Crystal structure of the hexameric replicative helicase RepA of plasmid RSF1010. J. Mol. Biol. 2001, 306:479-487.
71. Oram M., Sabanayagam C., Black L.W. Modulation of the Packaging Reaction of Bacteriophage T4 Terminase by DNA Structure. J. Mol. Biol. 2008, 381:61-72.
72. Parsons C.A., Stasiak A., Bennett R.J., West S.C. Structure of a multisubunit complex that promotes DNA branch migration. Nature 1995, 374:375-378.
73. Putnam C.D., Clancy S.B., Tsuruta H., Gonzalez S., Wetmur J.G., Tainer J.A. Structure and mechanism of the RuvB Holliday junction branch migration motor. J. Mol. Biol. 2001, 311:297-310.
74. Rao V.B., Feiss M. The Bacteriophage DNA Packaging Motor. Annu. Rev. Genet. 2008, 42:647-681.
75. Ray K., Ma J., Oram M., Lakowicz J.R., Black L.W. 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. 2010, 395:1102-1113.
76. Ray K., Sabanayagam C.R., Lakowicz J.R., Black L.W. DNA crunching by a viral packaging motor: compression of a procapsid-portal stalled Y-DNA substrate. Virology 2010, 398:224-232.
77. Roy A., Bhardwaj A., Cingolani G. Crystallization of the nonameric small terminase subunit of bacteriophage P22. Acta Crystallogr. F-Struct. Biol. Cryst. Commun. 2011, 67:104-110.
78. Sabanayagam C.R., Oram M., Lakowicz J.R., Black L.W. Viral DNA packaging studied by fluorescence correlation spectroscopy. Biophys. J. 2007, 93:L17-L19.
79. Schwartz, C., et al., The ATPase of the phi29 DNA packaging motor is a member of the hexameric AAA+ superfamily. Virology, this issue. http://dx.doi.org/10.1016/j.virol.2013.04.004i,
80. Schwartz C., Fang H., Huang L., Guo P. Sequential action of ATPase, ATP, ADP, Pi and dsDNA in procapsid-free system to enlighten mechanism in viral dsDNA packaging. Nucleic Acids Res. 2012, 40:2577-2586.
81. Serwer P. Models of bacteriophage DNA packaging motors. J. Struct. Biol. 2003, 141:179-188.
82. Serwer P. A hypothesis for bacteriophage DNA packaging motors. Viruses 2010, 2:1821-1843.
83. Shibata H., Fujisawa H., Minagawa T. Early events in a defined in vitro system for packaging of bacteriophage T3 DNA. Virology 1987, 159:250-258.
84. Shu D., Shu Y., Haque F., Abdelmawla S., Guo P. Thermodynamically stable RNA three-way junctions for constructing multifunctional nanoparticles for delivery of therapeutics. Nat. Nanotechnol. 2011, 6:658-667.
85. Shu D., Guo P. A Viral RNA that binds ATP and contains an motif similar to an ATP-binding aptamer from SELEX. J. Biol. Chem. 2003, 278(9):7119-7125.
86. Shu D., 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 2003, 309(1):108-113.
87. Shu D., Zhang H., Jin J., Guo P. Counting of six pRNAs of phi29 DNA-packaging motor with customized single molecule dual-view system. EMBO J. 2007, 26:527-537.
88. Shu, Y., Haque, F., Shu, D., Li, W., Zhu, Z., Kotb, M., Lyubchenko, Y., Guo, P., 2013. Fabrication of 14 different RNA nanoparticles for specific tumor targeting without accumulation in normal organs RNA, 19(6), 767-777, . http://dx.doi.org/10.1261/rna.037002.112.
89. 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., Rossmann M.G. Structure of the bacteriophage phi29 DNA packaging motor. Nature 2000, 408:745-750.
90. Story R.M., Steitz T.A. Structure of the rec-A protein-ADP complex. Nature 1992, 355.
91. Trottier M., Guo P. Approaches to determine stoichiometry of viral assembly components. J. Virol. 1997, 71:487-494.
92. Wang F., Mei Z., Qi Y., Yan C., Hu Q., Wang J., Shi Y. Structure and mechanism of the hexameric MecA-ClpC molecular machine. Nature 2011, 471:331-335.
93. Willows R.D., Hansson A., Birch D., Al-Karadaghi S., Hansson M. EM single particle analysis of the ATP-dependent BchI complex of magnesium chelatase: an AAA(+) hexamer. J. Struct. Biol. 2004, 146:227-233.
94. Xiao F., Zhang H., Guo P. Novel mechanism of hexamer ring assembly in protein/RNA interactions revealed by single molecule imaging. Nucleic Acids Res. 2008, 36:6620-6632.
95. Xiao F., Demeler B., Guo P. Assembly mechanism of the sixty-subunit nanoparticles via interaction of RNA with the reengineered protein connector of phi29 DNA-packaging motor. ACS Nano 2010, 4:3293-3301.
96. Yu J., Moffitt J., Hetherington C.L., Bustamante C., Oster G. Mechanochemistry of a viral DNA packaging motor. J. Mol. Biol. 2010, 400:186-203.
97. Zhang F., Lemieux S., Wu X., St.-Arnaud S., McMurray C.T., Major F., Anderson D. Function of hexameric RNA in packaging of bacteriophage phi29 DNA in vitro. Mol. Cell. 1998, 2:141-147.
98. Zhang H., Schwartz C., De Donatis G.M., Guo P. "Push Through One-Way Valve" mechanism of viral DNA packaging. Adv. Virus Res. 2012, 83:415-465.
99. Zhang, H., Endrizzi, J. A., Shu, Y., Haque, F., Guo, P., Chi, Y. I.. Crystal structure of 3WJ core revealing divalent ion-promoted thermostability and assembly of the Phi29 hexameric motor pRNA. RNA, accepted for publication.