Three reversible and controllable discrete steps of channel gating of a viral DNA packaging motor

Biomaterials

Volumn 32, Issue 32, 2011, Pages 8234-8242

  Geng, Jia ^a   Fang, Huaming ^a   Haque, Farzin ^a   Zhang, Le ^a   Guo, Peixuan ^a  

^a University of Cincinnati   (United States)

Author keywords

Bionanotechnology; DNA packaging; Nanopore; Nanotechnology; Single molecule sensing; Viral motor

Indexed keywords

AFFINITY BINDING; BACTERIOPHAGE PHI29; BIONANOTECHNOLOGY; CHANNEL GATING; CONFORMATIONAL CHANGE; DISCRETE STEP; DNA PACKAGING; DNA-PACKAGING MOTOR; INTERNAL LOOPS; NANOMACHINES; POTENTIAL APPLICATIONS; SINGLE CHANNEL RECORDING; SINGLE MOLECULE LEVEL; SINGLE-MOLECULE; SIZE REDUCTIONS; VIRAL DNA; VIRAL MOTOR;

CONFORMATIONS; MEDICAL NANOTECHNOLOGY; PACKAGING;

DNA;

VIRUS DNA;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CONTROLLED STUDY; DNA BINDING; DNA CONFORMATION; DNA STRUCTURE; ELECTRIC CURRENT; NONHUMAN; PRIORITY JOURNAL; VIRAL DNA PACKAGING MOTOR; VIRUS CAPSID;

AMINO ACIDS; BACILLUS PHAGES; DNA PACKAGING; DNA, VIRAL; GOLD; ION CHANNEL GATING; MOLECULAR MOTOR PROTEINS; MUTANT PROTEINS; NANOSTRUCTURES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; VIRAL PROTEINS; VIRUS ASSEMBLY;

BACILLUS PHAGE PHI29; MIRIDAE;

EID: 80052342523     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.07.034     Document Type: Article

References (86)

1. Guo P. Introduction: principles, perspectives, and potential applications in viral assembly. Semin Virol (Editor's Introduction) 1994, 5(1):1-3.
2. Guo P., Lee T.J. Viral nanomotors for packaging of dsDNA and dsRNA. Mol Microbiol 2007, 64:886-903.
3. Guo P., Peterson C., Anderson D. Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi29. J Mol Biol 1987, 197:229-236.
4. Chemla Y.R., Aathavan K., Michaelis J., Grimes S., Jardine P.J., Anderson D.L., et al. Mechanism of force generation of a viral DNA packaging motor. Cell 2005, 122:683-692.
5. 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.
6. 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.
7. Meifer W.J.J., Horcajadas J.A., Salas M. Phi29 family of phages. Microbiol Mol Biol Rev 2001, 65:261-287.
8. 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.
9. 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.
10. Zhang F., Lemieux S., Wu X., St.-Arnaud S., McMurray C.T., Major F., et al. Function of hexameric RNA in packaging of bacteriophage phi29 DNA in vitro. Mol Cell 1998, 2:141-147.
11. Moffitt J.R., Chemla Y.R., Aathavan K., Grimes S., Jardine P.J., Anderson D.L., et al. Intersubunit coordination in a homomeric ring ATPase. Nature 2009, 457:446-450.
12. 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.
13. Simpson A.A., Leiman P.G., Tao Y., He Y., Badasso M.O., Jardine P.J., et al. Structure determination of the head-tail connector of bacteriophage phi29. Acta Crystallogr D Biol Crystallogr 2001, 57:1260-1269.
14. Guasch A., Pous J., Ibarra B., Gomis-Ruth F.X., Valpuesta J.M., Sousa N., et al. Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage phi29 connector particle. J Mol Biol 2002, 315:663-676.
15. 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 USA 1986, 83:3505-3509.
16. Smith D.E., Tans S.J., Smith S.B., Grimes S., Anderson D.L., Bustamante C. The bacteriophage phi29 portal motor can package DNA against a large internal force. Nature 2001, 413:748-752.
17. Hess H., Vogel V. Molecular shuttles based on motor proteins: active transport in synthetic environments. J Biotechnol 2001, 82:67-85.
18. Soong R.K., Bachand G.D., Neves H.P., Olkhovets A.G., Craighead H.G., Montemagno C.D. Powering an inorganic nanodevice with a biomolecular motor. Science 2000, 290:1555-1558.
19. 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.
20. Wendell D., Jing P., Geng J., Subramaniam V., Lee T.J., Montemagno C., et al. Translocation of double-stranded DNA through membrane-adapted phi29 motor protein nanopores. Nat Nanotechnol 2009, 4:765-772.
21. 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, 93:153902-153903.
22. Valpuesta J.M., Fujisawa H., Marco S., Carazo J.M., Carrascosa J. Three-dimensional structure of T3 connector purified from overexpressing bacteria. J Mol Biol 1992, 224:103-112.
23. Olia A.S., Prevelige P.E., Johnson J.E., Cingolani G. Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 2011, 18:597-603.
24. Agirrezabala X., Martin-Benito J., Valle M., Gonzalez J.M., Valencia A., Valpuesta J.M., et al. Structure of the connector of bacteriophage T7 at 8A resolution: structural homologies of a basic component of a DNA translocating machinery. J Mol Biol 2005, 347:895-902.
25. Bazinet C., King J. The DNA translocating vertex of dsDNA bacteriophages. Annu Rev Microbiol 1985, 39:109-129.
26. Badasso M.O., Leiman P.G., Tao Y., He Y., Ohlendorf D.H., Rossmann M.G., et al. 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.
27. Dryden K., Wang G., Yeager M., Nibert M., Coombs K., Furlong D., et al. Early steps in reovirus infection are associated with dramatic changes in supramolecular structure and protein conformation: analysis of virions and subviral particles by cryoelectron microscopy and image reconstruction. J Cell Biol 1993, 122:1023-1041.
28. Jardine P., Coombs D.H. Capsid expansion follows the initiation of DNA packaging in bacteriophage T4. J Mol Biol 1998, 284(3):661-672.
29. Tang J.H., Olson N., Jardine P.J., Girimes S., Anderson D.L., Baker T.S. DNA poised for release in bacteriophage phi29. Structure 2008, 16:935-943.
30. Ray K., Oram M., Ma J., Black L.W. Portal control of viral prohead expansion and DNA packaging. Virology 2009, 391:44-50.
31. Serwer P., Wright E.T., Hakala K., Weintraub S.T., Su M., Jiang W. DNA packaging-associated hyper-capsid expansion of bacteriophage T3. J Mol Biol 2010, 397:361-374.
32. Ionel A., Velazquez-Muriel J.A., Luque D., Cuervo A., Caston J.R., Valpuesta J.M., et al. Molecular rearrangements involved in the capsid shell maturation of bacteriophage T7. J Biol Chem 2011, 286:234-242.
33. Zheng H., Olia A.S., Gonen M., Andrews S., Cingolani G., Gonen T. A conformational switch in bacteriophage P22 portal protein primes genome injection. Mol Cell 2008, 29:376-383.
34. Kemp P., Garcia L.R., Molineux I.J. Changes in bacteriophage T7 virion structure at the initiation of infection. Virology 2005, 340:307-317.
35. Guo P., Erickson S., Xu W., Olson N., Baker T.S., Anderson D. Regulation of the phage phi29 prohead shape and size by the portal vertex. Virology 1991, 183:366-373.
36. Cy Fu, Prevelige J. in vitro incorporation of the phage phi29 connector complex. Virology 2009, 394:149-153.
37. Jing P., Haque F., Vonderheide A., Montemagno C., Guo P. Robust properties of membrane-embedded connector channel of bacterial virus phi29 DNA packaging motor. Mol Biosyst 2010, 6:1844-1852.
38. 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.
39. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., Walter P. Molecular biology of the cell 2002, Garland Science, New York, pp. 615-650. 4th ed.
40. Hille B. Ion channels of excitable membranes 2001, Sinauer Associates, Sunderland, MA, p1-21. 3rd ed.
41. Agnew W.S., Simon R.L., Brabson J.S., Raftery M.A. Purification of the tetrodotoxin-binding component associated with the voltage-sensitive sodium channel from electrophorus electricus electroplax Membranes. Proc Natl Acad Sci USA 1978, 75:2606-2610.
42. Dorogi P.L., Neumann E. Theoretical implication of liganding reactions in axonal sodium channel gating. Neurochem Int 1980, 2:45-51.
43. Sokabe M., Sachs F., Jing Z.Q. Quantitative video microscopy of patch clamped membranes stress, strain, capacitance, and stretch channel activation. Biophys J 1991, 59:722-728.
44. Yameen B., Ali M., Neumann R., Ensinger W., Knoll W., Azzaroni O. Ionic transport through single solid-state nanopores controlled with thermally nanoactuated macromolecular gates. Small 2009, 5:1287-1291.
45. Lee S., Zhang Y., White H.S., Harrell C.C., Martin C.R. Electrophoretic capture and detection of nanoparticles at the opening of a membrane pore using scanning electrochemical microscopy. Anal Chem 2004, 76:6108-6115.
46. Wanunu M., Meller A. Chemically-modified solid-state nanopores. Nano Lett 2007, 7:1580-1585.
47. Hou X., Liu Y., Dong H., Yang F., Li L., Jiang L. A pH-gating ionic transport nanodevice: asymmetric chemical modification of single nanochannels. Adv Mater 2010, 22:2440-2443.
48. 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.
49. Cai Y., Xiao F., Guo P. The effect of N- or C-terminal alterations of the connector of bacteriophage phi29 DNA packaging motor on procapsid assembly, pRNA binding, and DNA packaging. Nanomedicine 2008, 4:8-18.
50. Ibanez C., Garcia J.A., Carrascosa J.L., Salas M. Overproduction and purification of the connector protein of Bacillus subtilis phage phi29. Nucleic Acids Res 1984, 12:2351-2365.
51. Guo Y., Blocker F., Xiao F., Guo P. Construction and 3-D computer modeling of connector arrays with tetragonal to decagonal transition induced by pRNA of phi29 DNA-packaging motor. J Nanosci Nanotechnol 2005, 5:856-863.
52. Robinson M.A., Wood J.P., Capaldi S.A., Baron A.J., Gell C., Smith D.A., et al. Affinity of molecular interactions in the bacteriophage phi29 DNA packaging motor. Nucleic Acids Res 2006, 34:2698-2709.
53. Wanunu M., Morrison W., Rabin Y., Grosberg A.Y., Meller A. Electrostatic focusing of unlabelled DNA into nanoscale pores using a salt gradient. Nat Nanotechnol 2010, 5:160-165.
54. Serwer P. A hypothesis for bacteriophage DNA packaging motors. Viruses 2010, 2:1821-1843.
55. 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.
56. Serwer P. The source of energy for bacteriophage DNA packaging: an osmotic pump explains the data. Biopolymers 1988, 27:165-169.
57. Fujisawa H., Morita M. Phage DNA packaging. Genes Cells 1997, 2:537-545.
58. Astumian R.D. Thermodynamics and kinetics of a Brownian motor. Science 1997, 276:917-922.
59. Hendrix R.W. Symmetry mismatch and DNA packaging in large bacteriophages. Proc Natl Acad Sci USA 1978, 75:4779-4783.
60. Grimes S., Anderson D. The bacteriophage phi29 packaging proteins supercoil the DNA ends. J Mol Biol 1997, 266:901-914.
61. 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.
62. 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.
63. 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.
64. Xiang Y., Morais M.C., Battisti A.J., Grimes S., Jardine P.J., Anderson D.L., et al. Structural changes of bacteriophage phi29 upon DNA packaging and release. EMBO J 2006, 25:5229-5239.
65. Ding F., Lu C., Zhao W., Rajashankar K.R., Anderson D.L., Jardine P.J., et al. Structure and assembly of the essential RNA ring component of a viral DNA packaging motor. Proc Natl Acad Sci USA 2011, 108:7357-7362.
66. Zhao H., Finch C.J., Sequeira R.D., Johnson B.A., Johnson J.E., Casjens S.R., et al. Crystal structure of the DNA-recognition component of the bacterial virus Sf6 genome-packaging machine. Proc Natl Acad Sci USA 2010, 107:1971-1976.
67. 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.
68. 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.
69. 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.
70. Skordalakes E., Berger J.M. Structural insights into RNA-dependent ring closure and ATPase activation by the Rho termination factor. Cell 2006, 127:553-564.
71. Matias P.M., Gorynia S., Donner P., Carrondo M.A. Crystal structure of the human AAA+ protein RuvBL1. J Biol Chem 2006, 281:38918-38929.
72. McGeoch A.T., Trakselis M.A., Laskey R.A., Bell S.D. Organization of the archaeal MCM complex on DNA and implications for the helicase mechanism. Nat Struct Mol Biol 2005, 12:756-762.
73. Fang Y., Cai Q., Qin P.Z. The procapsid binding domain of phi29 packaging RNA has a modular architecture and requires 2'-hydroxyl groups in packaging RNA interaction. Biochemistry 2005, 44:9348-9358.
74. Fang Y., Shu D., Xiao F., Guo P., Qin P.Z. Modular assembly of chimeric phi29 packaging RNAs that support DNA packaging. Biochem Biophysical Res Commun 2008, 372:589-594.
75. Gu X., Schroeder S.J. Different sequences show similar quaternary interaction stabilities in prohead viral RNA self-assembly. J Biol Chem 2011, 286:14419-14426.
76. Chen C., Sheng S., Shao Z., Guo P. A dimer as a building block in assembling RNA: a hexamer that gears bacterial virus phi29 DNA-translocating machinery. J Biol Chem 2000, 275(23):17510-17516.
77. 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.
78. Hugel T., Michaelis J., Hetherington C.L., Jardine P.J., Grimes S., Walter J.M., et al. Experimental test of connector rotation during DNA packaging into bacteriophage phi29 capsids. PLoS Biol 2007, 5:558-567.
79. 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.
80. 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.
81. Turner D.H., Sugimoto N., Freier S.M. RNA structure prediction. Annu Rev Biophys Chem 1988, 17:167-192.
82. Tao Y., Olson N.H., Xu W., Anderson D.L., Rossmann M.G., Baker T.S. Assembly of a tailed bacterial virus and its genome release studied in three dimensions. Cell 1998, 95:431-437.
83. Gonzalez-Huici V., Salas M., Hermoso J.M. The push-pull mechanism of bacteriophage phi29 DNA injection. Mol Microbiol 2004, 52:529-540.
84. Kemp P., Gupta M., Molineux I.J. Bacteriophage T7 DNA ejection into cells is initiated by an enzyme-like mechanism. Mol Microbiol 2004, 53:1251-1265.
85. Lebedev A.A., Krause M.H., Isidro A.L., Vagin A.A., Orlova E.V., Turner J., et al. Structural framework for DNA translocation via the viral portal protein. EMBO J 2007, 26:1984-1994.
86. Lhuillier S., Gallopin M., Gilquin B., Brasiles S., Lancelot N., Letellier G., et al. Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating. Proc Natl Acad Sci USA 2009, 106:8507-8512.