Ultrastable pRNA hexameric ring gearing hexameric phi29 DNA-packaging motor by revolving without rotating and coiling

Current Opinion in Biotechnology

Volumn 24, Issue 4, 2013, Pages 581-590

  Schwartz, Chad ^a   Guo, Peixuan ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGE PHI29; DNA-PACKAGING MOTOR; NEGATIVELY CHARGED; PHOSPHATE BACKBONE; POSITIVELY CHARGED; RNA NANOTECHNOLOGIES; ROTATIONAL MOTORS; VIRUS-INFECTED CELLS;

AMINO ACIDS; RNA; VIRUSES;

DNA;

ADENOSINE TRIPHOSPHATASE; DOUBLE STRANDED DNA; GLYCOPROTEIN; GLYCOPROTEIN GP 16; LYSINE; MICRORNA; NANOCARRIER; NANOPARTICLE; PHOSPHATE; RIBOZYME; RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS DNA;

BACTERIOPHAGE; DNA HELIX; DNA PACKAGING; DRUG DELIVERY SYSTEM; DRUG TARGETING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR INTERACTION; NANOTECHNOLOGY; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA NANOTECHNOLOGY; RNA STRUCTURE; RNA TRANSLATION; STOICHIOMETRY; THERMOSTABILITY; VIRUS INFECTION;

ADENOSINE TRIPHOSPHATASES; BACILLUS PHAGES; DNA PACKAGING; MODELS, MOLECULAR; MOLECULAR MOTOR PROTEINS; NANOTECHNOLOGY; RNA, UNTRANSLATED; VIRUS ASSEMBLY;

BACILLUS PHAGE PHI29;

EID: 84880948085     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2013.03.019     Document Type: Review

References (68)

1. 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.
2. Grainge I., Lesterlin C., Sherratt D.J. Activation of XerCD-dif recombination by the FtsK DNA translocase. Nucleic Acids Res 2011, 39:5140-5148.
3. 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.
4. 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.
5. 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.
6. 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.
7. Hendrix R.W. Bacteriophage DNA packaging: RNA gears in a DNA transport machine (Minireview). Cell 1998, 94:147-150.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. Schwartz C, De Donatis GM, Zhang H, Fang H, Guo P: Revolution rather than rotation of AAA+ hexameric phi29 nanomotor for viral dsDNA packaging without coiling. Virology 2013, in press.
15. Schwartz C, De Donatis GM, Fang H, Guo P: The ATPase of the phi29 DNA-packaging motor is a member of the hexameric AAA+ superfamily. Virology 2013, in press.
16. 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.
17. 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.
18. 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.
19. Zhao Z, Khisamutdinov E, Schwartz C, Guo P: Mechanism of one-way traffic of hexameric Phi29 DNA packaging motor with four electropositive relaying layers facilitating anti-parallel revolution. ACS Nano 2013, in press, doi:10.1021/nn4002775.
20. 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.
21. Guo P. The emerging field of RNA nanotechnology. Nat Nanotechnol 2010, 5:833-842.
22. Pleij C.W., Bosch L. RNA pseudoknots: structure, detection, and prediction. Methods Enzymol 1989, 180:289-303.
23. Guo P. RNA nanotechnology: engineering, assembly and applications in detection, gene delivery and therapy. J Nanosci Nanotechnol 2005, 5:1964-1982.
24. Isambert H. The jerky and knotty dynamics of RNA. Methods 2009, 49:189-196.
25. Sugimoto N., Nakano S., Katoh M., Matsumura A., Nakamuta H., Ohmichi T., Yoneyama M., Sasaki M. Thermodynamic parameters to predict stability of RNA/DNA hybrid duplexes. Biochemistry 1995, 34:11211-11216.
26. Searle M.S., Williams D.H. On the stability of nucleic acid structures in solution: enthalpy-entropy compensations, internal rotations and reversibility. Nucleic Acids Res 1993, 21:2051-2056.
27. Leontis N.B., Lescoute A., Westhof E. The building blocks and motifs of RNA architecture. Curr Opin Struct Biol 2006, 16:279-287.
28. Schroeder K.T., McPhee S.A., Ouellet J., Lilley D.M. A structural database for k-turn motifs in RNA. RNA 2010, 16:1463-1468.
29. Li X., Horiya S., Harada K. An efficient thermally induced RNA conformational switch as a framework for the functionalization of RNA nanostructures. J Am Chem Soc 2006, 128:4035-4040.
30. Chang K.Y., Tinoco I. Characterization of a "kissing" hairpin complex derived from the human immunodeficiency virus genome. Proc Natl Acad Sci USA 1994, 91:8705-8709.
31. 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, 275:17510-17516.
32. Wagner C., Ehresmann C., Ehresmann B., Brunel C. Mechanism of dimerization of bicoid mRNA: initiation and stabilization. J Biol Chem 2004, 279:4560-4569.
33. Bindewald E., Hayes R., Yingling Y.G., Kasprzak W., Shapiro B.A. RNAJunction: a database of RNA junctions and kissing loops for three-dimensional structural analysis and nanodesign. Nucleic Acids Res 2008, 36:D392-D397.
34. 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.
35. Haque F., Shu D., Shu Y., Shlyakhtenko L., Rychahou P., Evers M., Guo P. Ultrastable synergistic tetravalent RNA nanoparticles for targeting to cancers. Nano Today 2012, 7:245-257.
36. Guo P., Bailey S., Bodley J.W., Anderson D. Characterization of the small RNA of the bacteriophage phi29 DNA packaging machine. Nucleic Acids Res 1987, 15:7081-7090.
37. 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.
38. Shu D., Huang L., Guo P. A simple mathematical formula for stoichiometry quantitation of viral and nanobiological assemblage using slopes of log/log plot curves. J Virol Methods 2003, 115:19-30.
39. Trottier M., Guo P. Approaches to determine stoichiometry of viral assembly components. J Virol 1997, 71:487-494.
40. Zhang C.L., Lee C.-S., Guo P. The proximate 5' and 3' ends of the 120-base viral RNA (pRNA) are crucial for the packaging of bacteriophage φ29 DNA. Virology 1994, 201:77-85.
41. Zhang C.L., Tellinghuisen T., Guo P. Confirmation of the helical structure of the 5'/3' termini of the essential DNA packaging pRNA of phage φ29. RNA 1995, 1:1041-1050.
42. Zhang C.L., Trottier M., Guo P.X. Circularly permuted viral pRNA active and specific in the packaging of bacteriophage Phi29 DNA. Virology 1995, 207:442-451.
43. Reid R.J.D., Bodley J.W., Anderson D. Identification of bacteriophage phi29 prohead RNA (pRNA) domains necessary for in vitro DNA-gp3 packaging. J Biol Chem 1994, 269:9084-9089.
44. Reid R.J.D., Zhang F., Benson S., Anderson D. Probing the structure of bacteriophage phi29 prohead RNA with specific mutations. J Biol Chem 1994, 269:18656-18661.
45. Reid R.J.D., Bodley J.W., Anderson D. Characterization of the prohead-pRNA interaction of bacteriophage phi29. J Biol Chem 1994, 269:5157-5162.
46. Hoeprich S., Zhou Q., Guo S., Qi G., Wang Y., Guo P. Bacterial virus phi29 pRNA as a hammerhead ribozyme escort to destroy hepatitis B virus. Gene Ther 2003, 10:1258-1267.
47. Khaled A., Guo S., Li F., Guo P. Controllable self-assembly of nanoparticles for specific delivery of multiple therapeutic molecules to cancer cells using RNA nanotechnology. Nano Lett 2005, 5:1797-1808.
48. Guo S., Tschammer N., Mohammed S., Guo P. Specific delivery of therapeutic RNAs to cancer cells via the dimerization mechanism of phi29 motor pRNA. Hum Gene Ther 2005, 16:1097-1109.
49. Guo S., Huang F., Guo P. Construction of folate-conjugated pRNA of bacteriophage phi29 DNA packaging motor for delivery of chimeric siRNA to nasopharyngeal carcinoma cells. Gene Ther 2006, 13:814-820.
50. Shu Y., Cinier M., Fox S.R., Ben-Johnathan N., Guo P. Assembly of therapeutic pRNA-siRNA nanoparticles using bipartite approach. Mol Ther 2011, 19:1304-1311.
51. Shu Y., Cinier M., Shu D., Guo P. Assembly of multifunctional phi29 pRNA nanoparticles for specific delivery of siRNA and other therapeutics to targeted cells. Methods 2011, 54:204-214.
52. Soutschek J., Akinc A., Bramlage B., Charisse K., Constien R., Donoghue M., Elbashir S., Geick A., Hadwiger P., Harborth J., John M., Kesavan V., Lavine G., Pandey R.K., Racie T., Rajeev K.G., Rohl I., Toudjarska I., Wang G., Wuschko S., Bumcrot D., Koteliansky V., Limmer S., Manoharan M., Vornlocher H.P. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 2004, 432:173-178.
53. Dassie J.P., Liu X.Y., Thomas G.S., Whitaker R.M., Thiel K.W., Stockdale K.R., Meyerholz D.K., McCaffrey A.P., McNamara J.O., Giangrande P.H. Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors. Nat Biotechnol 2009, 27:839-849.
54. Behlke M.A. Progress towards in vivo use of siRNAs. Mol Ther 2006, 13:644-670.
55. Li S.D., Chen Y.C., Hackett M.J., Huang L. Tumor-targeted delivery of siRNA by self-assembled nanoparticles. Mol Ther 2008, 16:163-169.
56. Guo P., Haque F., Hallahan B., Reif R., Li H. Uniqueness, advantages, challenges, solutions, and perspectives in therapeutics applying RNA nanotechnology. Nucleic Acid Ther 2012, 22:226-245.
57. Shu D., Moll W.D., Deng Z., Mao C., Guo P. Bottom-up assembly of RNA arrays and superstructures as potential parts in nanotechnology. Nano Lett 2004, 4:1717-1723.
58. Cayrol B., Nogues C., Dawid A., Sagi I., Silberzan P., Isambert H. A nanostructure made of a bacterial noncoding RNA. J Am Chem Soc 2009, 131:17270-17276.
59. Ohno H., Kobayashi T., Kabata R., Endo K., Iwasa T., Yoshimura S.H., Takeyasu K., Inoue T., Saito H. Synthetic RNA-protein complex shaped like an equilateral triangle. Nat Nanotechnol 2011, 6:116-120.
60. Dibrov S.M., McLean J., Parsons J., Hermann T. Self-assembling RNA square. Proc Natl Acad Sci USA 2011, 108:6405-6408.
61. Severcan I., Geary C.V.E.C.A., Jaeger L. Square-shaped RNA particles from different RNA folds. Nano Lett 2009, 9:1270-1277.
62. Huang Z., Pei W., Han Y., Jayaseelan S., Shekhtman A., Shi H., Niu L. One RNA aptamer sequence, two structures: a collaborating pair that inhibits AMPA receptors. Nucleic Acids Res 2009, 37:4022-4032.
63. Pattabiraman N., Martinez H.M., Shapiro B.A. Molecular modeling and dynamics studies of HIV-1 kissing loop structures. J Biomol Struct Dyn 2002, 20:397-411.
64. Laughrea M., Jette L. HIV-1 genome dimerization: kissing-loop hairpin dictates whether nucleotides downstream of the 5' splice junction contribute to loose and tight dimerization of human immunodeficiency virus RNA. Biochemistry 1997, 36:9501-9508.
65. Paillart J.C., Westhof E., Ehresmann C., Ehresmann B., Marquet R. Non-canonical interactions in a kissing loop complex: the dimerization initiation site of HIV-1 genomic RNA. J Mol Biol 1997, 270:36-49.
66. Chang K.Y., Tinoco I. The structure of an RNA "kissing" hairpin complex of the HIV TAR hairpin loop and its complement. J Mol Biol 1997, 269:52-66.
67. Abdelmawla S., Guo S., Zhang L., Pulukuri S., Patankar P., Conley P., Trebley J., Guo P., Li Q.X. Pharmacological characterization of chemically synthesized monomeric pRNA nanoparticles for systemic delivery. Mol Ther 2011, 19:1312-1322.
68. 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 2012, in press.