Counting of six pRNAs of phi29 DNA-packaging motor with customized single-molecule dual-view system

EMBO Journal

Volumn 26, Issue 2, 2007, Pages 527-537

  Shu, Dan ^a   Zhang, Hui ^a   Jin, Jiashun ^b   Guo, Peixuan ^a,c  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c Purdue University   (United States)

Author keywords

Biomotor; Bionanotechnology; Nanobiotechnology; RNA nanotechnology; SMDV TIRF

Indexed keywords

DNA; FERRITIN; RNA;

ARTICLE; BACILLUS PHAGE; BLEACHING; DNA PACKAGING; ELECTRON MICROSCOPY; GENE TRANSLOCATION; HEAT TREATMENT; IMAGING SYSTEM; NANOBIOTECHNOLOGY; PRIORITY JOURNAL; PROTEIN DENATURATION; RNA ANALYSIS; RNA STRUCTURE; STOICHIOMETRY; STRUCTURE ANALYSIS;

BACILLUS PHAGES; CAPSID; DIMERIZATION; DNA PACKAGING; DNA, VIRAL; FERRITINS; HEAT; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; RNA, VIRAL;

BACILLUS PHAGE PHI29;

EID: 33846551354     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601506     Document Type: Article

References (68)

1. Adachi K, Yasuda R, Noji H, Itoh H, Harada Y, Yoshida M, Kinosita Jr K (2000) Stepping rotation of F1-ATPase visualized through angle-resolved single-fluorophore imaging. Proc Natl Acad Sci USA 97: 7243-7247
2. Bazinet C, King J (1985) The DNA translocation vertex of dsDNA bacteriophages. Annu Rev Microbiol 39: 109-129
3. Blanco L, Lazaro JM, de Vega M, Bonnin A, Salas M (1994) Terminal protein-primed DNA amplification. Proc Natl Acad Sci USA 91: 12198-12202
4. Bogner E (2002) Human cytomegalovirus terminase as a target for antiviral chemotherapy. Rev Med Virol 12: 115-127
5. Bringmann H, Skiniotis G, Spilker A, Kandels-Lewis S, Vernos I, Surrey T (2004) A kinesin-like motor inhibits microtubule dynamic instability. Science 303: 1519-1522
6. Catalano CE, Cue D, Feiss M (1995) Virus DNA packaging: the strategy used by phage lambda. Mol Microbiol 16: 1075-1086
7. Chemla YR, Aathavan K, Michaelis J, Grimes S, Jardine PJ, Anderson DL, Bustamante C (2005) Mechanism of force generation of a viral DNA packaging motor. Cell 122: 683-692
8. Chen C, Guo P (1997) Sequential action of six virus-encoded DNA-packaging RNAs during phage phi29 genomic DNA translocation. J Virol 71: 3864-3871
9. Chen C, Sheng S, Shao Z, 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
10. Cue D, Feiss M (2001) Bacteriophage lambda DNA packaging: DNA site requirements for termination and processivity. J Mol Biol 311: 233-240
11. Dohoney KM, Gelles J (2001) Chi-sequence recognition and DNA translocation by single RecBCD helicase/nuclease molecules. Nature 409: 370-374
12. Fang Y, Cai Q, Qin PZ (2005) The procapsid binding domain of phi29 packaging RNA has a modular architecture and requires 20-hydroxyl groups in packaging RNA interaction. Biochemistry 44: 9348-9358
13. Finer JT, Simmons RM, Spudich JA (1994) Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368: 113-119
14. Fletcher SP, Dumur F, Pollard MM, Feringa BL (2005) A reversible, unidirectional molecular rotary motor driven by chemical energy. Science 310: 80-82
15. Garver K, Guo P (2000) Mapping the inter-RNA interaction of phage phi29 by site-specific photoaffinity crosslinking. J Biol Chem 275: 2817-2824
16. Grimes S, Anderson D (1989) In vitro packaging of bacteriophage phi29 DNA restriction fragments and the role of the terminal protein gp3. J Mol Biol 209: 91-100
17. Guasch A, Pous J, Ibarra B, Gomis-Ruth FX, Valpuesta JM, Sousa N, Carrascosa JL, 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
18. Guo P (1994) Introduction: principles, perspectives, and potential applications in viral assembly. Semin Virol (Editor's Introduction) 5: 1-3
19. Guo P (2005) RNA Nanotechnology: engineering, assembly and applications in detection, gene delivery and therapy. J Nanosci Nanotechnol 5: 1964-1982
20. Guo P, Erickson S, Anderson D (1987a) A small viral RNA is required for in vitro packaging of bacteriophage phi29 DNA. Science 236: 690-694
21. Guo P, Grimes S, 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
22. Guo P, Peterson C, Anderson D (1987b) Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi29. J Mol Biol 197: 229-236
23. Guo P, Zhang C, Chen C, Trottier M, Garver K (1998) Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation. Mol Cell 2: 149-155
24. Guo S, Huang F, Guo P (2006) Construction of folate-conjugated pRNA of bacteriophage phi29 DNA packaging motor for delivery of chimeric siRNA to nasopharyngeal carcinoma cells. Gene Therapy 13: 814-820
25. Guo S, Shu D, Simon M, Guo P (2003) Gene cloning, purification and stoichiometry quantification of phi29 anti-receptor gp12 with potential use as special ligand for gene delivery. Gene 315: 145-152
26. Ha T (2001) Single-molecule fluorescence resonance energy transfer. Methods 25: 78-86
27. Ha T, Rasnik I, Cheng W, Babcock HP, Gauss GH, Lohman TM, Chu S (2002) Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature 419: 638-641
28. Hendrix RW (1978) Summetry mismatch and DNA packaging in large bacteriophages. Proc Natl Acad Sci USA 75: 4779-4783
29. Hess H, Howard J, Vogel V (2002) A piconewton forcemeter assembled from microtubules and kinesins. Nano Lett 2: 1113-1115
30. Hirono-Hara Y, Noji H, Nishiura M, Muneyuki E, Hara KY, Yasuda R, Kinosita Jr K, Yoshida M (2001) Pause and rotation of F(1)-ATPase during catalysis. Proc Natl Acad Sci USA 98: 13649-13654
31. Hoeprich S, ZHou Q, Guo S, Qi G, Wang Y, Guo P (2003) Bacterial virus phi29 pRNA as a hammerhead ribozyme escort to destroy hepatitis B virus. Gene Therapy 10: 1258-1267
32. Huang F (2003) Efficient incorporation of CoA, NAD and FAD into RNA by in vitro transcription. Nucleic Acids Res 31: e8
33. Ibarra B, Caston JR, Llorca O, Valle M, Valpuesta JM, Carrascosa JL (2000) Topology of the components of the DNA packaging machinery in the phage phi29 prohead. J Mol Biol 298: 807-815
34. Ishijima A, Kojima H, Funatsu T, Tokunaga M, Higuchi H, Tanaka H, Yanagida T (1998) Simultaneous observation of individual ATPase and mechanical events by a single myosin molecule during interaction with actin. Cell 92: 161-171
35. Jankowsky E (2005) Biophysics: helicase snaps back. Nature 437: 1245
36. Jimenez J, Santisteban A, Carazo JM, Carrascosa JL (1986) Computer graphic display method for visualizing three-dimensional biological structures. Science 232: 1113-1115
37. Khaled A, Guo S, Li F, Guo P (2005) Controllable self-assembly of nanoparticles for specific delivery of multiple therapeutic molecules to cancer cells using RNA nanotechnology. Nano Lett 5: 1797-1808
38. Lee CS, Guo P (1995) In vitro assembly of infectious virions of ds-DNA phage phi29 from cloned gene products and synthetic nucleic acids. J Virol 69: 5018-5023
39. Lee TJ, 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
40. Lin H, Black LW (1998) DNA requirements in vivo for phage T4 packaging. Virology 242: 118-127
41. Moll D, Guo P (2005) Translocation of nicked but not gapped DNA by the packaging motor of bacteriophage phi29. J Mol Biol 351: 100-107
42. Morais MC, Choi KH, Koti JS, Chipman PR, Anderson DL, Rossmann MG (2005) Conservation of the capsid structure in tailed dsDNA bacteriophages: the pseudoatomic structure of phi29. Mol Cell 18: 149-159
43. Morais MC, Tao Y, Olsen NH, Grimes S, Jardine PJ, Anderson D, Baker TS, Rossmann MG (2001) Cryoelectron-microscopy image reconstruction of symmetry mismatches in bacteriophage phi29. J Struct Biol 135: 38-46
44. Myong S, Rasnik I, Joo C, Lohman TM, Ha T (2005) Repetitive shuttling of a motor protein on DNA. Nature 437: 1321-1325
45. Pomerantz RT, Ramjit R, Gueroui Z, Place C, Anikin M, Leuba S, Zlatanova J, McAllister WT (2005) A tightly regulated molecular motor based upon T7 RNA polymerase. Nano Lett 5: 1698-1703
46. Purcell T, Sweeney HL, Spudich JA (2005) A force-dependent state controls the coordination of processive myosin V. Proc Natl Acad Sci USA 102: 13873-13878
47. Reid RJD, Bodley JW, Anderson D (1994) Characterization of the prohead-pRNA interaction of bacteriophage phi29. J Biol Chem 269: 5157-5162
48. Robinson MA, Wood JP, Capaldi SA, Baron AJ, Gell C, Smith DA, Stonehouse NJ (2006) Affinity of molecular interactions in the bacteriophage phi29 DNA packaging motor. Nucleic Acids Res 34: 2698-2709
49. Rondelez Y, Tresset G, Nakashima T, Kato-Yamada Y, Fujita H, Takeuchi S, Noji H (2005) Highly coupled ATP synthesis by F1-ATPase single molecules. Nature 433: 773-777
50. Rueda D, Bokinsky G, Rhodes MM, Rust MJ, Zhuang X, Walter NG (2004) Single-molecule enzymology of RNA: essential functional groups impact catalysis from a distance. Proc Natl Acad Sci USA 101: 10066-10071
51. Seidel R, Bloom JG, van NJ, Dutta CF, Dekker NH, Firman K, Szczelkun MD, Dekker C (2005) Dynamics of initiation, termination and reinitiation of DNA translocation by the motor protein EcoR124I. EMBO J 24: 4188-4197
52. Shu D, 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
53. Simpson AA, Tao Y, Leiman PG, Badasso MO, He Y, Jardine PJ, Olson NH, Morais MC, Grimes S, Anderson DL, Baker TS, Rossmann MG (2000) Structure of the bacteriophage phi29 DNA packaging motor. Nature 408: 745-750
54. Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C (2001) The bacteriophage phi29 portal motor can package DNA against a large internal force. Nature 413: 748-752
55. Soong RK, Bachand GD, Neves HP, Olkhovets AG, Craighead HG, Montemagno CD (2000) Powering an inorganic nanodevice with a biomolecular motor. Science 290: 1555-1558
56. Sun J, Cai Y, Moll WD, Guo P (2006) Controlling bacteriophage phi29 DNA-packaging motor by addition or discharge of a peptide at N-terminus of connector protein that interacts with pRNA. Nucleic Acids Res 34: 5482-5490
57. Svoboda K, Block SM (1994) Force and velocity measured for single kinesin molecules. Cell 77: 773-784
58. Tomishige M, Klopfenstein DR, Vale RD (2002) Conversion of Unc104/KIF1A kinesin into a processive motor after dimerization. Science 297: 2263-2267
59. Trottier M, Garver K, Zhang C, Guo P (1997) DNA-packaging pRNA as target for complete inhibition of viral assembly in vitro and in vivo. Nucleic Acids Symp Ser 36: 187-189
60. Vale RD, Funatsu T, Pierce DW, Romberg L, Harada Y, Yanagida T (1996) Direct observation of single kinesin molecules moving along microtubules. Nature 380: 451-453
61. Wang MD, Schnitzer MJ, Yin H, Landick R, Gelles J, Block SM (1998) Force and velocity measured for single molecules of RNA polymerase. Science 282: 902-907
62. Weiss S (1999) Fluorescence spectroscopy of single biomolecules. Science 283: 1676-1683
63. Xiao F, Moll D, Guo S, Guo P (2005) Binding of pRNA to the N-terminal 14 amino acids of connector proteinof bacterial phage phi29. Nucleic Acids Res 33: 2640-2649
64. Yasuda R, Noji H, Yoshida M, Kinosita Jr K, Itoh H (2001) Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase. Nature 410: 898-904
65. Zhang CL, Garver K, Guo P (1995) Inhibition of phage phi29 assembly by antisense oligonucleotides targeting viral pRNA essential for DNA packaging. Virology 211: 568-576
66. Zhang CL, Lee C-S, Guo P (1994) The proximate 5′ and 3′ ends of the 120-base viral RNA (pRNA) are crucial for the packaging of bacteriophage phi29 DNA. Virology 201: 77-85
67. Zhang F, Lemieux S, Wu X, St.-Arnaud S, McMurray CT, Major F, Anderson D (1998) Function of hexameric RNA in packaging of bacteriophage phi29 DNA in vitro. Mol Cell 2: 141-147
68. Zhuang X, Bartley LE, Babcock HP, Russell R, Ha T, Herschlag D, Chu S (2000) A single-molecule study of RNA catalysis and folding. Science 288: 2048-2051