Mechanism of one-way traffic of hexameric Phi29 DNA packaging motor with four electropositive relaying layers facilitating antiparallel revolution

ACS Nano

Volumn 7, Issue 5, 2013, Pages 4082-4092

  Zhao, Zhengyi ^a   Khisamutdinov, Emil ^a   Schwartz, Chad ^a   Guo, Peixuan ^a  

^a University of Kentucky   (United States)

Author keywords

AAA+ ATPase superfamily; bionanomotor; bionanotechnology; DNA packaging; one way traffic mechanism; virus assembly

Indexed keywords

AAA+ ATPASE SUPERFAMILY; BIONANOMOTOR; BIONANOTECHNOLOGY; DNA-PACKAGING; VIRUS ASSEMBLY;

NANOSYSTEMS; VIRUSES;

DNA;

ADENOSINE TRIPHOSPHATASE; VIRUS DNA;

ARTICLE; BACILLUS PHAGE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DNA PACKAGING; ELECTRON; GENETICS; METABOLISM; NANOTECHNOLOGY; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE;

ADENOSINE TRIPHOSPHATASES; BACILLUS PHAGES; DNA PACKAGING; DNA, VIRAL; ELECTRONS; MODELS, MOLECULAR; NANOTECHNOLOGY; NUCLEIC ACID CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY;

EID: 84878292282     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn4002775     Document Type: Article

References (77)

1. 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
2. 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
3. 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
4. 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
5. 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
6. 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
7. 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
8. 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
9. 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
10. 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
11. Grainge, I.; Lesterlin, C.; Sherratt, D. J. Activation of XerCD-Dif Recombination by the FtsK DNA Translocase Nucleic Acids Res. 2011, 39, 5140-5148
12. Martin, A.; Baker, T. A.; Sauer, R. T. Rebuilt AAA + Motors Reveal Operating Principles for ATP-Fuelled Machines Nature 2005, 437, 1115-1120
13. Ammelburg, M.; Frickey, T.; Lupas, A. N. Classification of AAA+ Proteins J. Struct. Biol. 2006, 156, 2-11
14. Guo, P. X.; Lee, T. J. Viral Nanomotors for Packaging of DsDNA and DsRNA Mol. Microbiol. 2007, 64, 886-903
15. Rao, V. B.; Feiss, M. The Bacteriophage DNA Packaging Motor Annu. Rev. Genet. 2008, 42, 647-681
16. 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
17. Serwer, P. A Hypothesis for Bacteriophage DNA Packaging Motors Viruses 2010, 2, 1821-1843
18. 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
19. 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
20. 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
21. 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
22. 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
23. 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
24. 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
25. Guo, P.; Peterson, C.; Anderson, D. Initiation Events in In Vitro Packaging of Bacteriophage Φ29 DNA-Gp3 J. Mol. Biol. 1987, 197, 219-228
26. 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
27. 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
28. 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
29. 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
30. 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
31. Grimes, S.; Anderson, D. RNA Dependence of the Bateriophage Phi29 DNA Packaging ATPase J. Mol. Biol. 1990, 215, 559-566
32. 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
33. 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
34. Green, D. J.; Wang, J. C.; Xiao, F.; Cai, Y.; Balhorn, R.; Guo, P.; Cheng, R. H. Self-Assembly of Heptameric Nanoparticles Derived from Tag-Functionalized Phi29 Connectors ACS Nano 2010, 4, 7651-7659
35. Xiao, F.; Cai, Y.; Wang, J. C.; Green, D.; Cheng, R. H.; Demeler, B.; Guo, P. Adjustable Ellipsoid Nanoparticles Assembled from Re-engineered Connectors of the Bacteriophage Phi29 DNA Packaging Motor ACS Nano 2009, 3, 2163-2170
36. 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
37. 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
38. Carazo, J. M.; Donate, L. E.; Herranz, L.; Secilla, J. P.; Carrascosa, J. L. Three-Dimensional Reconstruction of the Connector of Bacteriophage Φ29 at 1.8 nm Resolution J. Mol. Biol. 1986, 192, 853-867
39. Xiao, F.; Sun, J.; Coban, O.; Schoen, P.; Wang, J. C.; Cheng, R. H.; Guo, P. Fabrication of Massive Sheets of Single Layer Patterned Arrays Using Lipid Directed Reengineered Phi29 Motor Dodecamer ACS Nano 2009, 3, 100-107
40. Haque, F.; Lunn, J.; Fang, H.; Smithrud, D.; Guo, P. Real-Time Sensing and Discrimination of Single Chemicals Using the Channel of Phi29 DNA Packaging Nanomotor ACS Nano 2012, 6, 3251-3261
41. Wendell, D.; Jing, P.; Geng, J.; Subramaniam, V.; Lee, T. J.; Montemagno, C.; Guo, P. Translocation of Double-Stranded DNA through Membrane-Adapted Phi29 Motor Protein Nanopores Nat. Nanotechnol. 2009, 4, 765-772
42. Hendrix, R. W. Symmetry Mismatch and DNA Packaging in Large Bacteriophages Proc. Natl. Acad. Sci. U.S.A. 1978, 75, 4779-4783
43. Doering, C.; Ermentrout, B.; Oster, G. Rotary DNA Motors Biophys. J. 1998, 69, 2256-2267
44. 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
45. 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
46. 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
47. 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
48. 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
49. 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
50. Hendrix, R. W. Bacteriophage DNA Packaging: RNA Gears in a DNA Transport Machine (Minireview) Cell 1998, 94, 147-150
51. 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
52. 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
53. 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
54. Maluf, N. K.; Feiss, M. Virus DNA Translocation: Progress towards a First Ascent of Mount Pretty Difficult Mol. Microbiol. 2006, 61, 1-4
55. Schwartz, C.; De Donatis, G. M.; Zhang, H.; Fang, H.; Guo, P. Revolution Rather than Rotation of AAA+ Hexameric Phi29 Nanomotor for Viral DsDNA Packaging without Coiling. Virology 2013, not supplied.
56. Schwartz, C.; De Donatis, G. M.; Fang, H.; Guo, P. The ATPase of the Phi29 DNA-Packaging Motor Is a Member of the Hexameric AAA+ Superfamily. Virology 2013, not supplied.
57. 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
58. 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
59. Shu, Y.; Haque, F.; Shu, D.; Li, W.; Zhu, Z.; Kotb, M.; Lyubchenko, Y.; Guo, P. Fabrication of 14 Different RNA Nanoparticles for Specific Tumor Targeting without Accumulation in Normal Organs. RNA 2013, not supplied.
60. Zhang, H.; Endrizzi, J. A.; Shu, Y.; Haque, F.; Guo, P.; Chi, Y. I. The 3WJ Core Crystal Structure Reveals Divalent Ion-Promoted Thermostability and Functional Assembly of the Phi29 Hexameric Motor PRNA. RNA 2012, not supplied.
61. 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
62. 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
63. Morita, M.; Tasaka, M.; Fujisawa, H. DNA Packaging ATPase of Bacteriophage T3 Virology 1993, 193, 748-752
64. Geng, J.; Fang, H.; Haque, F.; Zhang, L.; Guo, P. Three Reversible and Controllable Discrete Steps of Channel Gating of a Viral DNA Packaging Motor Biomaterials 2011, 32, 8234-8242
65. Grimes, S.; Ma, S.; Gao, J.; Atz, R.; Jardine, P. J. Role of Phi29 Connector Channel Loops in Late-Stage DNA Packaging J. Mol. Biol. 2011, 410, 50-59
66. Isidro, A.; Henriques, A. O.; Tavares, P. The Portal Protein Plays Essential Roles at Different Steps of the SPP1 DNA Packaging Process Virology 2004, 322, 253-263
67. Geng, J.; Huaming, F.; shaoying, W.; Peixuan, G. Channel Size Conversion of Phi29 DNA-Packaging Nanomotor for Discrimination of Single- and Double-Stranded DNA and RNA ACS Nano 2013, 10.1021/nn400020z
68. Moll, W.-D.; Guo, P. Translocation of Nicked but Not Gapped DNA by the Packaging Motor of Bacteriophage Phi29 J. Mol. Biol. 2005, 351, 100-107
69. Lee, C. S.; Guo, P. In Vitro Assembly of Infectious Virions of Ds-DNA Phage Φ29 from Cloned Gene Products and Synthetic Nucleic Acids J. Virol. 1995, 69, 5018-5023
70. 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
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. 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
73. Ibarra, B.; Caston, J. R.; Llorca, O.; Valle, M.; Valpuesta, J. M.; Carrascosa, J. L. Topology of the Components of the DNA Packaging Machinery in the Phage Phi29 Prohead J. Mol. Biol. 2000, 298, 807-815
74. 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
75. Morais, M. C.; Tao, Y.; Olsen, N. H.; Grimes, S.; Jardine, P. J.; Anderson, D.; Baker, T. S.; Rossmann, M. G. Cryoelectron-Microscopy Image Reconstruction of Symmetry Mismatches in Bacteriophage Phi29 J. Struct. Biol. 2001, 135, 38-46
76. 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
77. 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