Annals of Biomedical Engineering

, Volume 37, Issue 10, pp 2064–2081 | Cite as

Construction of Bacteriophage Phi29 DNA Packaging Motor and its Applications in Nanotechnology and Therapy

  • Tae Jin Lee
  • Chad Schwartz
  • Peixuan GuoEmail author


Nanobiotechnology involves the creation, characterization, and modification of organized nanomaterials to serve as building blocks for constructing nanoscale devices in technology and medicine. Living systems contain a wide variety of nanomachines and highly ordered structures of macromolecules. The novelty and ingenious design of the bacterial virus phi29 DNA packaging motor and its parts inspired the synthesis of this motor and its components as biomimetics. This 30-nm nanomotor uses six copies of an ATP-binding pRNA to gear the motor. The structural versatility of pRNA has been utilized to construct dimers, trimers, hexamers, and patterned superstructures via the interaction of two interlocking loops. The approach, based on bottom-up assembly, has also been applied to nanomachine fabrication, pathogen detection and the delivery of drugs, siRNA, ribozymes, and genes to specific cells in vitro and in vivo. Another essential component of the motor is the connector, which contains 12 copies of a protein gp10 to form a 3.6-nm central channel as a path for DNA. This article will review current studies of the structure and function of the phi29 DNA packaging motor, as well as the mechanism of motion, the principle of in vitro construction, and its potential nanotechnological and medical applications.


Bacteriophage phi29 DNA packaging motor pRNA Nanotechnology Nanobiotechnology Bionanotechnology Gene delivery Cancer therapy 



We thank Dr. Anne Vonderheide, Linda Keller, Dr. Hui Zhang, Feng Xiao, Dr. Farzin Haque, and Mollie Johnson for their assistance in preparing this review. The work done in the author’s laboratory was supported by NIH Grants GM59944, EB03730, and the NIH Nanomedicine Development Center (NDC) of “Phi29 DNA Packaging Motor for Nanomedicine” (PN2 EY018230) through the NIH Roadmap for Medical Research. Peixuan Guo is the cofounder of Kylin Therapeutics, Inc.

Supplementary material

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Supplementary material 1 (DOC 22 kb)


  1. 1.
    Afonin, K. A., D. J. Cieply, and N. B. Leontis 2008 Specific RNA self-assembly with minimal paranemic motifs. J. Am. Chem. Soc. 130:93-102. doi: 10.1021/ja071516m PubMedCrossRefGoogle Scholar
  2. 2.
    Agirrezabala, X., J. Martin-Benito, M. Valle, J. M. Gonzalez, A. Valencia, J. M. Valpuesta, and J. L. Carrascosa 2005 Structure of the connector of bacteriophage T7 at 8A resolution: structural homologies of a basic component of a DNA translocating machinery. J. Mol Biol. 347:895-902. doi: 10.1016/j.jmb.2005.02.005 PubMedCrossRefGoogle Scholar
  3. 3.
    Aldaye, F. A., A. L. Palmer, and H. F. Sleiman 2008 Assembling materials with DNA as the guide. Science. 321:1795-1799. doi: 10.1126/science.1154533 PubMedCrossRefGoogle Scholar
  4. 4.
    Alivisatos, A. P., K. P. Johnsson, X. Peng, T. E. Wilson, C. J. Loweth, M. P. Bruchez Jr., and P. G. Schultz 1996 Organization of nanocrystal molecules using DNA. Nature. 382:609-611. doi: 10.1038/382609a0 PubMedCrossRefGoogle Scholar
  5. 5.
    Anderson, D. L.; Reilly, B. 1993 Morphogenesis of bacteriophage ϕ29. In: Sonenshein, A. L., Hoch, J. A., Losick, R. (Eds.) Bacillus subtilis and other gram-positive bacteria: Biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, D.C., pp 859-867.Google Scholar
  6. 6.
    Andres, R. P., et al. 1996 Self-assembly of a 2-dimensional superlattice of molecularly linked metal clusters. Science. 273:1690-1693. doi: 10.1126/science.273.5282.1690 CrossRefGoogle Scholar
  7. 7.
    Atz, R., S. Ma, J. Gao, D. L. Anderson, and S. Grimes 2007 Alanine Scanning and Fe-BABE Probing of the Bacteriophage phi29 Prohead RNA-Connector Interaction. J. Mol. Biol. 369:239-248. doi: 10.1016/j.jmb.2007.03.033 PubMedCrossRefGoogle Scholar
  8. 8.
    Baer, M. F., R. M. Reilly, G. M. McCorkle, T. Y. Hai, S. Altman, and U. L. RajBhandary 1988 The recognition by RNase P of precursor tRNAs. J. Biol. Chem. 263:2344-2351.PubMedGoogle Scholar
  9. 9.
    Baumann, R. G., J. Mullaney, and L. W. Black 2006 Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol Microbiol. 61:16-32. doi: 10.1111/j.1365-2958.2006.05203.x PubMedCrossRefGoogle Scholar
  10. 10.
    Black, L. W. 1989 DNA Packaging in dsDNA bacteriophages. Ann Rev Microbiol. 43:267-292. doi: 10.1146/annurev.mi.43.100189.001411 CrossRefGoogle Scholar
  11. 11.
    Bowers J., P. T. Tran, A. Joshi, R. M. Liskay, E. Alani (2001) MSH-MLH complexes formed at a DNA mismatch are disrupted by the PCNA sliding clamp. J Mol Biol 306(5):957-968. doi: 10.1006/jmbi.2001.4467 PubMedCrossRefGoogle Scholar
  12. 12.
    Brust, M., D. Bethall, D. J. Schiffrin, and C. J. Kiely 1995 Novel gold dithiol nanonetworks with non-metallic electronic properties. Adv. Mater. 7:795-797. doi: 10.1002/adma.19950070907 CrossRefGoogle Scholar
  13. 13.
    Burgess, B. R., J. P. Richardson 2001 RNA passes through the hole of the protein hexamer in the complex with the Escherichia coli Rho factor. J Biol Chem 276(6):4182-4189. doi:  10.1074/jbc.M007066200 PubMedCrossRefGoogle Scholar
  14. 14.
    Cai, Y., F. Xiao, and P. Guo 2008 N- or C- terminal alterations of motor protein gp10 of bacterial virus phi29 on procapsid assembly, pRNA binding and DNA packaging. Nanomedicine. 4:8-18.PubMedGoogle Scholar
  15. 15.
    Carrascosa, J. L., A. Camacho, F. Moreno, F. Jimenez, R. P. Mellado, E. Vinuela, and M. Salas 1976 Bacillus subtilis phage phi29. Characterization of gene products and functions. Eur. J Biochem. 66:229-241. doi: 10.1111/j.1432-1033.1976.tb10512.x PubMedCrossRefGoogle Scholar
  16. 16.
    Chan, Y. N. C., R. R. Schrock, and R. E. Cohen 1992 Synthesis of single silver nanoclusters within spherical microdomains in block copolymer films. J. Am. Chem. Soc. 114:7295-7296. doi: 10.1021/ja00044a051 CrossRefGoogle Scholar
  17. 17.
    Chang CL, Zhang H, Shu D, Guo P, and Savran CA 2008 Bright-field analysis of phi29 DNA packaging motor using a magnetomechanical system. Appl. Phys. Lett. 93:153902-1539023.Google Scholar
  18. 18.
    Channon, K., E. H. C. Bromley, and D. N. Woolfson 2008 Synthetic biology through biomolecular design and engineering. Current Opinion in Structural Biology. 18:491-498. doi: 10.1016/ PubMedCrossRefGoogle Scholar
  19. 19.
    Chemla, Y. R., K. Aathavan, J. Michaelis, S. Grimes, P. J. Jardine, D. L. Anderson, and C. Bustamante 2005 Mechanism of force generation of a viral DNA packaging motor. Cell. 122:683-692. doi: 10.1016/j.cell.2005.06.024 PubMedCrossRefGoogle Scholar
  20. 20.
    Chen, C., P. Guo 1997 Sequential action of six virus-encoded DNA-packaging RNAs during phage phi29 genomic DNA translocation. J. Virol. 71(5):3864-3871.PubMedGoogle Scholar
  21. 21.
    Chen, C., C. Zhang, and P. Guo 1999 Sequence requirement for hand-in-hand interaction in formation of pRNA dimers and hexamers to gear phi29 DNA translocation motor. RNA. 5:805-818. doi: 10.1017/S1355838299990350 PubMedCrossRefGoogle Scholar
  22. 22.
    Cohen, D. N., S. E. Erickson, Y. Xiang, M. G. Rossmann, and D. L. Anderson 2008 Multifunctional roles of a bacteriophage phi 29 morphogenetic factor in assembly and infection. J Mol Biol. 378(4):804-817. doi: 10.1016/j.jmb.2008.02.068 PubMedCrossRefGoogle Scholar
  23. 23.
    Colvin, V. L., A. N. Goldstein, and A. P. Alivisatos 1992 Semiconductor nanocrystals covalently bound to metal surfaces with self-assembled monolayers. J. Am. Chem. Soc. 114:5221-5230. doi: 10.1021/ja00039a038 CrossRefGoogle Scholar
  24. 24.
    Craighead, H. G. 2000 Nanoelectromechanical systems. Science. 290:1532-1536. doi: 10.1126/science.290.5496.1532 PubMedCrossRefGoogle Scholar
  25. 25.
    Cui, Y., C. M. Lieber 2001 Functional nanoscale electronic devices assembled using silicon nanowire building blocks. Science. 291(5505):851-853. doi: 10.1126/science.291.5505.851 PubMedCrossRefGoogle Scholar
  26. 26.
    Dabbousi, B. O., C. B. Murray, M. F. Rubner, and M. G. Bawendi 1994 Langmuir-Blodgett manipulation of size selected CdSe nanocrystals. Chem Mater. 6:216-219. doi: 10.1021/cm00038a020 CrossRefGoogle Scholar
  27. 27.
    Davis, L. I. 1995 The nuclear pore complex. Ann. Rev. Biochem. 64:865-896. doi: 10.1146/ PubMedCrossRefGoogle Scholar
  28. 28.
    Dujardin, E., C. Peet, G. Stubbs, J. N. Culver, and S. Mann 2003 Organization of Metallic Nanoparticles Using Tobacco Mosaic Virus Templates. Nano Letters. 3 (3):413-417. doi: 10.1021/nl034004o CrossRefGoogle Scholar
  29. 29.
    Earnshaw, W. C., S. R. Casjens 1980 DNA packaging by the double-stranded DNA bacteriophages. Cell. 21:319-331. doi: 10.1016/0092-8674(80)90468-7 PubMedCrossRefGoogle Scholar
  30. 30.
    Eguchi, Y., J. Tomizawa 1990 Complex formed by complementary RNA stem-loops and its stabilization by a protein: function of CoIE1 Rom protein. Cell. 60:199-209. doi: 10.1016/0092-8674(90)90736-X PubMedCrossRefGoogle Scholar
  31. 31.
    Ellison, V., B. Stillman 2001 Opening of the clamp: an intimate view of an ATP-driven biological machine. Cell. 106(6):655-660. doi: 10.1016/S0092-8674(01)00498-6 PubMedCrossRefGoogle Scholar
  32. 32.
    Fang, Y., D. Shu, F. Xiao, P. Guo, and P. Z. Qin 2008 Modular assembly of chimeric phi29 packaging RNAs that support DNA packaging. Biochemical and Biophysical Research Communications. 372:589-594. doi: 10.1016/j.bbrc.2008.05.094 PubMedCrossRefGoogle Scholar
  33. 33.
    Feldkamp, U., C. M. Niemeyer 2006 Rational design of DNA nanoarchitectures. Angewandte Chemie-International Edition. 45:1856-1876. doi: 10.1002/anie.200502358 CrossRefGoogle Scholar
  34. 34.
    Ferrandon, D., I. Koch, E. Westhof, and C. Nusslein-Volhard 1997 RNA-RNA interaction is required for the formation of specific bicoid mRNA 3’ UTR-STAUFEN ribonucleoprotein particles. EMBO J. 16:1751-1758. doi: 10.1093/emboj/16.7.1751 PubMedCrossRefGoogle Scholar
  35. 35.
    Fletcher, S. P., F. Dumur, M. M. Pollard, and B. L. Feringa 2005 A reversible, unidirectional molecular rotary motor driven by chemical energy. Science. 310:80-82. doi: 10.1126/science.1117090 PubMedCrossRefGoogle Scholar
  36. 36.
    Fuller, D. N., J. P. Rickgauer, P. J. Jardine, S. Grimes, D. L. Anderson, and D. E. Smith 2007 Ionic effects on viral DNA packaging and portal motor function in bacteriophage phi 29. Proc. Natl. Acad. Sci. U. S. A. 104:11245-11250. doi: 10.1073/pnas.0701323104 PubMedCrossRefGoogle Scholar
  37. 37.
    Gates, B. D., Q. Xu, M. Stewart, D. Ryan, C. G. Willson, and G. M. Whitesides 2005 New approaches to nanofabrication: molding, printing, and other techniques. Chem. Rev. 105:1171-1196. doi: 10.1021/cr030076o PubMedCrossRefGoogle Scholar
  38. 38.
    Gogol, E. P., S. E. Seifried, and P. H. von Hippel 1991 Structure and assembly of the Escherichia coli transcription termination factor rho and its interaction with RNA. I. Cryoelectron microscopic studies. J Mol Biol. 221:1127-1138.PubMedGoogle Scholar
  39. 39.
    Grigoriev D. N., Moll W., Hall J., Guo P. (2003) Bionanomotor. Encycl. Nanosci. Nanotechnol. 1:361–374.Google Scholar
  40. 40.
    Grimes, S., D. Anderson 1989 In Vitro Packaging of Bacteriophage ϕ29 DNA Restriction Fragments and the Role of the Terminal Protein gp3. J. Mol. Biol. 209:91-100. doi: 10.1016/0022-2836(89)90172-1 PubMedCrossRefGoogle Scholar
  41. 41.
    Grimes, S., D. Anderson 1997 The bacteriophage phi29 packaging proteins supercoil the DNA ends. J Mol Biol. 266:901-914. doi: 10.1006/jmbi.1996.0843 PubMedCrossRefGoogle Scholar
  42. 42.
    Grimes, S., D. Anderson 1990 RNA Dependence of the Bateriophage phi29 DNA Packaging ATPase. J. Mol. Biol. 215:559-566. doi: 10.1016/S0022-2836(05)80168-8 PubMedCrossRefGoogle Scholar
  43. 43.
    Guasch, A., J. Pous, B. Ibarra, F. X. Gomis-Ruth, J. M. Valpuesta, N. Sousa, J. L. Carrascosa, and M. Coll 2002 Detailed architecture of a DNA translocating machine: the high- resolution structure of the bacteriophage phi29 connector particle. J Mol Biol 315(4):663-676. doi: 10.1006/jmbi.2001.5278 PubMedCrossRefGoogle Scholar
  44. 44.
    Guerrier-Takada, C., K. Gardiner, T. Marsh, N. Pace, and S. Altman 1983 The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell. 35:849-857. doi: 10.1016/0092-8674(83)90117-4 PubMedCrossRefGoogle Scholar
  45. 45.
    Guo P. 2005 RNA Nanotechnology: Engineering, Assembly and Applications in Detection, Gene Delivery and Therapy. Journal of Nanoscience and Nanotechnology. 5(12):1964-1982. doi: 10.1166/jnn.2005.446 PubMedCrossRefGoogle Scholar
  46. 46.
    Guo Y, Blocker F, Xiao F, and Guo P. 2005 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. 5:856-863. doi: 10.1166/jnn.2005.143 PubMedCrossRefGoogle Scholar
  47. 47.
    Guo, P. (2005) Bacterial virus phi29 DNA-packaging motor and its potential applications in gene therapy and nanotechnology. Methods Mol. Biol. 300:285–324PubMedGoogle Scholar
  48. 48.
    Guo, P., S. Erickson, and D. Anderson 1987 A small viral RNA is required for in vitro packaging of bacteriophage phi29 DNA. Science. 236:690-694. doi: 10.1126/science.3107124 PubMedCrossRefGoogle Scholar
  49. 49.
    Guo, P., S. Grimes, and D. Anderson 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. doi: 10.1073/pnas.83.10.3505 PubMedCrossRefGoogle Scholar
  50. 50.
    Guo, P., C. Peterson, and D. Anderson 1987 Initiation events in in vitro packaging of bacteriophage ϕ29 DNA-gp3. J Mol Biol. 197:219-228. doi: 10.1016/0022-2836(87)90120-3 PubMedCrossRefGoogle Scholar
  51. 51.
    Guo, P., C. Peterson, and D. Anderson 1987 Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage ϕ29. J Mol Biol. 197:229-236. doi: 10.1016/0022-2836(87)90121-5 PubMedCrossRefGoogle Scholar
  52. 52.
    Guo, P., B. Rajogopal, D. Anderson, S. Erickson, and C.-S. Lee 1991 sRNA of bacteriophage phi29 of Bsubtilis mediates DNA packaging of phi29 proheads assembled in E coli. Virology 185:395-400. doi: 10.1016/0042-6822(91)90787-C PubMedCrossRefGoogle Scholar
  53. 53.
    Guo, P., M. Trottier 1994 Biological and biochemical properties of the small viral RNA (pRNA) essential for the packaging of the double-stranded DNA of phage ϕ29. Seminars in Virology. 5:27-37. doi: 10.1006/smvy.1994.1004 CrossRefGoogle Scholar
  54. 54.
    Guo, P., C. Zhang, C. Chen, M. Trottier, and K. Garver 1998 Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation. Mol. Cell. 2:149-155. doi: 10.1016/S1097-2765(00)80124-0 PubMedCrossRefGoogle Scholar
  55. 55.
    Guo, P. X., T. J. Lee 2007 Viral nanomotors for packaging of dsDNA and dsRNA. Mol. Microbiol. 64:886-903. doi: 10.1111/j.1365-2958.2007.05706.x PubMedCrossRefGoogle Scholar
  56. 56.
    Guo, S., N. Tschammer, S. Mohammed, and P. Guo 2005 Specific delivery of therapeutic RNAs to cancer cells via the dimerization mechanism of phi29 motor pRNA. Hum Gene Ther. 16:1097-1109. doi: 10.1089/hum.2005.16.1097 PubMedCrossRefGoogle Scholar
  57. 57.
    Guo, S., F. Huang, and P. Guo 2006 Construction of folate-conjugated pRNA of bacteriophage phi29 DNA packaging motor for delivery of chimeric siRNA to nasopharyngeal carcinoma cells. Gene Ther. 13(10):814-820.PubMedGoogle Scholar
  58. 58.
    Ha, T. 2001 Single-molecule fluorescence resonance energy transfer. Methods. 25(1):78-86. doi: 10.1006/meth.2001.1217 PubMedCrossRefGoogle Scholar
  59. 59.
    Ha, T., I. Rasnik, W. Cheng, H. P. Babcock, G. H. Gauss, T. M. Lohman, and S. Chu 2002 Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature. 419(6907):638-641. doi: 10.1038/nature01083 PubMedCrossRefGoogle Scholar
  60. 60.
    Hendrix, R. W. 1978 Symmetry mismatch and DNA packaging in large bacteriophages. Proc. Natl. Acad. Sci. USA. 75:4779-4783. doi: 10.1073/pnas.75.10.4779 PubMedCrossRefGoogle Scholar
  61. 61.
    Hess, H., V. Vogel 2001 Molecular shuttles based on motor proteins: Active transport in synthetic environments. J Biotechnol. 82(1):67-85.PubMedGoogle Scholar
  62. 62.
    Hingorani, M. M., M. O’Donnell 2000 Sliding Clamps: a (tail)ored fit. Curr. Biol. 10:25-29. doi: 10.1016/S0960-9822(99)00252-3 CrossRefGoogle Scholar
  63. 63.
    Hoeprich, S., P. Guo 2002 Computer modeling of three-dimensional structure of DNA-packaging RNA(pRNA) monomer, dimer, and hexamer of phi29 DNA Packaging motor. J Biol Chem 277(23):20794-20803. doi: 10.1074/jbc.M112061200 PubMedCrossRefGoogle Scholar
  64. 64.
    Hoeprich, S., Q. ZHou, S. Guo, G. Qi, Y. Wang, and P. Guo 2003 Bacterial virus phi29 pRNA as a hammerhead ribozyme escort to destroy hepatitis B virus. Gene Ther. 10:1258-1267. doi: 10.1038/ PubMedCrossRefGoogle Scholar
  65. 65.
    Huang, L. P., P. Guo 2003 Use of acetone to attain highly active and soluble DNA packaging protein gp16 of phi29 for ATPase assay. Virology. 312(2):449-457. doi: 10.1016/S0042-6822(03)00241-1 PubMedCrossRefGoogle Scholar
  66. 66.
    Huang, L. P., P. Guo 2003 Use of PEG to acquire highly soluble DNA-packaging enzyme gp16 of bacterial virus phi29 for stoichiometry quantification. J Virol Methods. 109(2):235-244. doi: 10.1016/S0166-0934(03)00077-6 PubMedCrossRefGoogle Scholar
  67. 67.
    Hugel, T., J. Michaelis, C. L. Hetherington, P. J. Jardine, S. Grimes, J. M. Walter, W. Faik, D. L. Anderson, and C. Bustamante 2007 Experimental test of connector rotation during DNA packaging into bacteriophage phi 29 capsids. Plos Biology. 5:558-567. doi: 10.1371/journal.pbio.0050059 CrossRefGoogle Scholar
  68. 68.
    Ibarra B, Caston J.R., Llorca O., Valle M, Valpuesta J.M., and Carrascosa J.L. 2000 Topology of the components of the DNA packaging machinery in the phage phi29 prohead. J. Mol. Biol. 298:807-815. doi: 10.1006/jmbi.2000.3712 PubMedCrossRefGoogle Scholar
  69. 69.
    Ibarra, B., J. M. Valpuesta, and J. L. Carrascosa 2001 Purification and functional characterization of p16, the ATPase of the bacteriophage phi29 packaging machinary. Nucleic Acids Res. 29(21):4264-4273. doi: 10.1093/nar/29.21.4264 PubMedCrossRefGoogle Scholar
  70. 70.
    Jung, G. Y., E. Johnston-Halperin, W. Wu, Z. N. Yu, S. Y. Wang, W. M. Tong, Z. Y. Li, J. E. Green, B. A. Sheriff, A. Boukai, Y. Bunimovich, J. R. Heath, and R. S. Williams 2006 Circuit fabrication at 17 nm half-pitch by nanoimprint lithography. Nano Letters. 6:351-354. doi: 10.1021/nl052110f PubMedCrossRefGoogle Scholar
  71. 71.
    Katz, E., I. Willner 2004 Integrated nanoparticle-biomolecule hybrid systems: Synthesis, properties, and applications. Angewandte Chemie-International Edition. 43:6042-6108. doi: 10.1002/anie.200400651 CrossRefGoogle Scholar
  72. 72.
    Khaled, A., S. Guo, F. Li, and P. Guo 2005 Controllable Self-Assembly of Nanoparticles for Specific Delivery of Multiple Therapeutic Molecules to Cancer Cells Using RNA Nanotechnology. Nano Letters. 5:1797-1808. doi: 10.1021/nl051264s PubMedCrossRefGoogle Scholar
  73. 73.
    Koti, J. S., M. C. Morais, R. Rajagopal, B. A. Owen, C. T. McMurray, and Anderson D. 2008 DNA packaging motor assembly intermediate of bacteriophage phi29. J Mol. Biol. 381:1114-1132. doi: 10.1016/j.jmb.2008.04.034 PubMedCrossRefGoogle Scholar
  74. 74.
    Krug, R. M. 1993 The regulation of export of mRNA from nucleus to cytoplasm. Current Opinion in Cell Biology. 5:944-949. doi: 10.1016/0955-0674(93)90074-Z PubMedCrossRefGoogle Scholar
  75. 75.
    Kruger, K., P. J. Grabowski, A. J. Zaug, J. Sands, D. E. Gottschling, and T. R. Cech 1982 Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell. 31:147-157. doi: 10.1016/0092-8674(82)90414-7 PubMedCrossRefGoogle Scholar
  76. 76.
    Lee, C. S., P. Guo 1995 In vitro assembly of infectious virions of ds-DNA phage ϕ29 from cloned gene products and synthetic nucleic acids. J. Virol. 69:5018-5023.PubMedGoogle Scholar
  77. 77.
    Lee, C. S., P. Guo 1995 Sequential interactions of structural proteins in phage phi29 procapsid assembly. J. Virol. 69:5024-5032.PubMedGoogle Scholar
  78. 78.
    Lee, S. W., C. Mao, C. E. Flynn, and A. M. Belcher 2002 Ordering of quantum dots using genetically engineered viruses. Science. 296(5569):892-895. doi: 10.1126/science.1068054 PubMedCrossRefGoogle Scholar
  79. 79.
    Lee, T. J., P. Guo 2006 Interaction of gp16 with pRNA and DNA for Genome Packaging by the Motor of Bacterial Virus phi29. J. Mol Biol. 356:589-599. doi: 10.1016/j.jmb.2005.10.045 PubMedCrossRefGoogle Scholar
  80. 80.
    Lee, T. J., H. Zhang, D. Liang, and P. Guo 2008 Strand and nucleotide-dependent ATPase activity of gp16 of bacterial virus phi29 DNA packaging motor. Virology. 380:69-74. doi: 10.1016/j.virol.2008.07.003 PubMedCrossRefGoogle Scholar
  81. 81.
    Leu, F. P., and M. O’Donnell. Interplay of a clamp loader subunits in opening the {beta} sliding clamp of E. coli DNA polymerase III holoenzyme. J. Biol. Chem. 276(50):47185–47194, 2001.PubMedCrossRefGoogle Scholar
  82. 82.
    Lin, H., M. N. Simon, and L. W. Black 1997 Purification and characterization of the small subunit of phage T4 terminase, gp16, required for DNA packaging. J Biol Chem 272(6):3495-3501. doi: 10.1074/jbc.272.6.3309 PubMedCrossRefGoogle Scholar
  83. 83.
    Liu, H., S. Guo, R. Roll, J. Li, Z. Diao, N. Shao, M. R. Riley, A. M. Cole, J. P. Robinson, N. M. Snead, G. Shen, and P. Guo 2007 Phi29 pRNA Vector for Efficient Escort of Hammerhead Ribozyme Targeting Survivin in Multiple Cancer Cells. Cancer Biol Ther 6(5):697-704.PubMedCrossRefGoogle Scholar
  84. 84.
    Lubrich, D., J. Bath, and A. J. Turberfield 2008 Templated self-assembly of wedge-shaped DNA arrays. Tetrahedron. 64:8530-8534. doi: 10.1016/j.tet.2008.05.135 CrossRefGoogle Scholar
  85. 85.
    Mancini, E. J., D. E. Kainov, J. M. Grimes, R. Tuma, D. H. Bamford, and D. I. Stuart 2004 Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell. 118:743-755. doi: 10.1016/j.cell.2004.09.007 PubMedCrossRefGoogle Scholar
  86. 86.
    Mao, C., T. H. LaBean, J. H. Relf, and N. C. Seeman 2000 Logical computation using algorithmic self-assembly of DNA triple-crossover molecules. Nature. 407:493-496. doi: 10.1038/35035038 PubMedCrossRefGoogle Scholar
  87. 87.
    Mbindyo, J. K. N., B. D. Reiss, B. R. Martin, C. D. Keating, M. J. Natan, and T. E. Mallouk 2001 DNA-directed assembly of gold nanowires on complementary surfaces. Advanced Materials. 13:249-254. doi: 10.1002/1521-4095(200102)13:4≤249::AID-ADMA249≥3.0.CO;2-9 CrossRefGoogle Scholar
  88. 88.
    Mickler, M., E. Schleiff, and T. Hugel 2008 From biological towards artificial molecular motors. Chemphyschem. 9:1503-1509. doi: 10.1002/cphc.200800216 PubMedCrossRefGoogle Scholar
  89. 89.
    Mirkin, C. A., R. L. Letsinger, R. C. Mucic, and J. J. Storhoff 1996 A DNA based method for rationally assembling nanoparticles into macroscopic materials. Nature. 382:607-609. doi: 10.1038/382607a0 PubMedCrossRefGoogle Scholar
  90. 90.
    Moffitt J. R., Y. R. Chemla, K. Aathavan, S. Grimes, P. J. Jardine, D. L. Anderson, C. Bustamante (2009). Intersubunit coordination in a homomeric ring ATPase. Nature 457(7228):446–452PubMedCrossRefGoogle Scholar
  91. 91.
    Moll, D., P. Guo 2005 Translocation of nicked but not gapped DNA by the packaging motor of bacteriophage phi29. J Mol Biol. 351:100-107. doi: 10.1016/j.jmb.2005.05.038 PubMedCrossRefGoogle Scholar
  92. 92.
    Moll, D., C. Huber, B. Schlegel, D. Pum, U. B. Sleytr, and M. Sara 2002 S-layer-streptavidin fusion proteins as template for nanopatterned molecular arrays. Proc Natl Acad Sci USA 99(23):14646-14651. doi: 10.1073/pnas.232299399 PubMedCrossRefGoogle Scholar
  93. 93.
    Morton, V. L., P. G. Stockley, N. J. Stonehouse, and A. E. Ashcroft 2008 Insights into virus capsid assembly from non-covalent mass spectrometry. Mass Spectrom. Rev. 27:575-595. doi: 10.1002/mas.20176 PubMedCrossRefGoogle Scholar
  94. 94.
    Motte, L., F. Billoudet, E. Lacaze, and M. Pileni 1996 Self-organization of size-selected nanoparticles into three dimensional superlattices. Adv. Mater. 8:1018-1020. doi: 10.1002/adma.19960081218 CrossRefGoogle Scholar
  95. 95.
    Murray, C. B., C. R. Kagan, and M. G. Bawendi 1995 Self-organization of CdSe nanocrystals into 3-dimensional quantum dot super lattices. Science. 270:1335-1338. doi: 10.1126/science.270.5240.1335 CrossRefGoogle Scholar
  96. 96.
    Niedenzu, T., D. Roleke, G. Bains, E. Scherzinger, and W. Saenger 2001 Crystal structure of the hexameric replicative helicase RepA of plasmid RSF1010. J Mol Biol 306(3):479-487. doi: 10.1006/jmbi.2000.4398 PubMedCrossRefGoogle Scholar
  97. 97.
    Nykypanchuk, D., M. M. Maye, D. van der Lelie, and O. Gang 2008 DNA-guided crystallization of colloidal nanoparticles. Nature. 451:549-552. doi: 10.1038/nature06560 PubMedCrossRefGoogle Scholar
  98. 98.
    Oh, B. K., N. R. Pace 1994 Interaction of the 3’-end of tRNA with ribonuclease P RNA. Nucleic Acids Res. 22(20):4087-4094. doi: 10.1093/nar/22.20.4087 PubMedCrossRefGoogle Scholar
  99. 99.
    Oram, M., C. Sabanayagam, and L. W. Black 2008 Modulation of the Packaging Reaction of Bacteriophage T4 Terminase by DNA Structure. J Mol Biol. 381:61-72. doi: 10.1016/j.jmb.2008.05.074 PubMedCrossRefGoogle Scholar
  100. 100.
    Orlova E. V., B. Gowen, A. Droge, A. Stiege, F. Weise, R. Lurz, M. van Heel, P. Tavares (2003). Structure of a viral DNA gatekeeper at 10 A resolution by cryo-electron microscopy. EMBO J. 22:1255–1262. doi: 10.1093/emboj/cdg123 PubMedCrossRefGoogle Scholar
  101. 101.
    Otero, R., D. Ecija, G. Fernandez, J. M. Gallego, L. Sanchez, N. Martin, and R. Miranda 2007 An organic donor/acceptor lateral superlattice at the nanoscale. Nano Letters. 7:2602-2607. doi: 10.1021/nl070897z PubMedCrossRefGoogle Scholar
  102. 102.
    Paillart, J. C., E. Skripkin, B. Ehresmann, C. Ehresmann, and R. Marquet 1996 A loop-loop “kissing” complex is the essential part of the dimer linkage of genomic HIV-1 RNA. Proc Natl Acad Sci U. S. A. 93:5572-5577. doi: 10.1073/pnas.93.11.5572 PubMedCrossRefGoogle Scholar
  103. 103.
    Peterson, C., M. Simon, J. Hodges, P. Mertens, L. Higgins, E. Egelman, and D. Anderson 2001 Composition and Mass of the Bacteriophage phi29 Prohead and Virion. J Struct Biol. 135:18-25. doi: 10.1006/jsbi.2001.4375 PubMedCrossRefGoogle Scholar
  104. 104.
    Pfeifer, K., B. E. Weiler, D. Ugarkovic, M. Bachmann, H. C. Schroder, and W. E. Muller 1991 Evidence for a direct interaction of Rev protein with nuclear envelope mRNA-translocation system. Eur. J. Biochem. 199:53-64. doi: 10.1111/j.1432-1033.1991.tb16091.x PubMedCrossRefGoogle Scholar
  105. 105.
    Rishovd, S., A. Holzenburg, B. V. Johansen, and B. H. Lindqvist 1998 Bacteriophage P2 and P4 morphogenesis: structure and function of the connector. Virology. 245:11-17. doi: 10.1006/viro.1998.9153 PubMedCrossRefGoogle Scholar
  106. 106.
    Robinson, M. A., J. P. Wood, S. A. Capaldi, A. J. Baron, C. Gell, D. A. Smith, and N. J. Stonehouse 2006 Affinity of molecular interactions in the bacteriophage phi29 DNA packaging motor. Nucleic Acids Res. 34:2698-2709. doi: 10.1093/nar/gkl318 PubMedCrossRefGoogle Scholar
  107. 107.
    Rothemund, P. W. K. 2006 Folding DNA to create nanoscale shapes and patterns. Nature. 440:297-302. doi: 10.1038/nature04586 PubMedCrossRefGoogle Scholar
  108. 108.
    Rueda, D., G. Bokinsky, M. M. Rhodes, M. J. Rust, X. Zhuang, and N. G. Walter 2004 Single-molecule enzymology of RNA: essential functional groups impact catalysis from a distance. Proc. Natl. Acad. Sci. U. S. A. 101:10066-10071. doi: 10.1073/pnas.0403575101 PubMedCrossRefGoogle Scholar
  109. 109.
    Sabanayagam, C. R., M. Oram, J. R. Lakowicz, and L. W. Black 2007 Viral DNA packaging studied by fluorescence correlation spectroscopy. Biophys J 93(4):L17-L19. doi: 10.1529/biophysj.107.111526 PubMedCrossRefGoogle Scholar
  110. 110.
    Sara, M., U. B. Sleytr 2000 S-layer proteins. J Bact. 182:859-868. doi: 10.1128/JB.182.4.859-868.2000 PubMedCrossRefGoogle Scholar
  111. 111.
    Sedman, J., A. Stenlund 1998 The papillomavirus E1 protein forms a DNA-dependent hexameric complex with ATPase and DNA helicase activities. J Virol. 72:6893-6897.PubMedGoogle Scholar
  112. 112.
    Seeman, N. C., and A. M. Belcher. Emulating biology: building nanostructures from the bottom up. Proc. Natl. Acad. Sci. USA 99(Suppl 2):6451–6455, 2002.Google Scholar
  113. 113.
    Serwer, P. 2003 Models of bacteriophage DNA packaging motors. J Struct Biol 141(3):179-188. doi: 10.1016/S1047-8477(02)00628-7 PubMedCrossRefGoogle Scholar
  114. 114.
    Shu, D., P. Guo 2003 A Viral RNA that binds ATP and contains an motif similar to an ATP-binding aptamer from SELEX. J Biol Chem 278(9):7119-7125. doi: 10.1074/jbc.M209895200 PubMedCrossRefGoogle Scholar
  115. 115.
    Shu, D., P. Guo 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(1):108-113. doi: 10.1016/S0042-6822(03)00011-4 PubMedCrossRefGoogle Scholar
  116. 116.
    Shu, D., L. Huang, and P. Guo 2003 A simple mathematical formula for stoichiometry quantitation of viral and nanobiological assemblage using slopes of log/log plot curves. J Virol Meth 115(1):19-30. doi: 10.1016/j.jviromet.2003.08.015 CrossRefGoogle Scholar
  117. 117.
    Shu, D., L. Huang, S. Hoeprich, and P. Guo 2003 Construction of phi29 DNA-packaging RNA (pRNA) monomers, dimers and trimers with variable sizes and shapes as potential parts for nano-devices. J. Nanosci. Nanotechnol. 3:295-302. doi: 10.1166/jnn.2003.160 PubMedCrossRefGoogle Scholar
  118. 118.
    Shu, D., D. Moll, Z. Deng, C. Mao, and P. Guo 2004 Bottom-up assembly of RNA arrays and superstructures as potential parts in nanotechnology. Nano Lett. 4:1717-1724. doi: 10.1021/nl0494497 CrossRefGoogle Scholar
  119. 119.
    Shu, D., H. Zhang, J. Jin, and P. Guo 2007 Counting of six pRNAs of phi29 DNA-packaging motor with customized single molecule dual-view system. EMBO J. 26:527-537. doi: 10.1038/sj.emboj.7601506 PubMedCrossRefGoogle Scholar
  120. 120.
    Simpson, A. A., P. G. Leiman, Y. Tao, Y. He, M. O. Badasso, P. J. Jardine, D. L. Anderson, and M. G. Rossman 2001 Structure determination of the head-tail connector of bacteriophage phi29. Acta Cryst. D57:1260-1269. doi: 10.1107/S0907444901010435 Google Scholar
  121. 121.
    Skripkin, E., J. C. Paillart, R. Marquet, B. Ehresmann, and C. Ehresmann 1994 Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro. Proc. Natl. Acad. Sci USA. 91:4945-4949. doi: 10.1073/pnas.91.11.4945 PubMedCrossRefGoogle Scholar
  122. 122.
    Sleytr, U. B., M. Sara 1997 Bacterial and archaeal S-layer proteins: structure-function relationships and their biotechnological applications. Trends Biotechnol. 15(1):20-26. doi: 10.1016/S0167-7799(96)10063-9 PubMedCrossRefGoogle Scholar
  123. 123.
    Smith, D. E., S. J. Tans, S. B. Smith, S. Grimes, D. L. Anderson, and C. Bustamante 2001 The bacteriophage phi29 portal motor can package DNA against a large internal force. Nature. 413:748-752. doi: 10.1038/35099581 PubMedCrossRefGoogle Scholar
  124. 124.
    Song, M. S., H. G. Dallmann, and C. S. McHenry 2001 Carboxyl-terminal Domain III of the delta ‘Subunit of the DNA Polymerase III Holoenzyme Binds delta. J Biol Chem 276(44):40668-40679. doi: 10.1074/jbc.M106373200 PubMedCrossRefGoogle Scholar
  125. 125.
    Song, Q., Y. Ding, Z. L. Wang, and Z. J. Zhang 2006 Formation of orientation-ordered superlattices of magnetite magnetic nanocrystals from shape-segregated self-assemblies. Journal of Physical Chemistry B. 110:25547-25550. doi: 10.1021/jp0652695 PubMedCrossRefGoogle Scholar
  126. 126.
    Sun, J., Y. Cai, W. D. Moll, and P. Guo 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(19):5482-5490. doi: 10.1093/nar/gkl701 PubMedCrossRefGoogle Scholar
  127. 127.
    Sun, S., K. Kondabagil, B. Draper, T. I. Alam, V. D. Bowman, Z. Zhang, S. Hegde, A. Fokine, M. G. Rossmann, and V. B. Rao 2008 The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell. 135:1251-1262. doi: 10.1016/j.cell.2008.11.015 PubMedCrossRefGoogle Scholar
  128. 128.
    Sundquist, W. I., S. Heaphy 1993 Evidence for interstand quadruplex formation in the dimerization of human immunodeficiency virus 1 genomic RNA. Proc. Natl. Acad. Sci. USA. 90:3393-3397. doi: 10.1073/pnas.90.8.3393 PubMedCrossRefGoogle Scholar
  129. 129.
    Svoboda, K., S. M. Block 1994 Force and velocity measured for single kinesin molecules. Cell. 77(5):773-784. doi: 10.1016/0092-8674(94)90060-4 PubMedCrossRefGoogle Scholar
  130. 130.
    Trottier, M., K. Garver, C. Zhang, and P. Guo 1997 DNA-packaging pRNA as target for complete inhibition of viral assembly in vitro and in vivo. Nucleic Acids Symposium Series. 36:187-189.Google Scholar
  131. 131.
    Trottier, M., P. Guo 1997 Approaches to determine stoichiometry of viral assembly components. J. Virol. 71:487-494.PubMedGoogle Scholar
  132. 132.
    Trottier, M., C. L. Zhang, and P. Guo 1996 Complete inhibition of virion assembly in vivo with mutant pRNA essential for phage phi29 DNA packaging. J. Virol. 70:55-61.PubMedGoogle Scholar
  133. 133.
    Uchida, M., M. T. Klem, M. Allen, P. Suci, M. Flenniken, E. Gillitzer, Z. Varpness, L. O. Liepold, M. Young, and T. Douglas 2007 Biological containers: Protein cages as multifunctional nanoplatforms. Advanced Materials. 19:1025-1042. doi: 10.1002/adma.200601168 CrossRefGoogle Scholar
  134. 134.
    Ulijn, R. V., A. M. Smith 2008 Designing peptide based nanomaterials. Chemical Society Reviews. 37:664-675. doi: 10.1039/b609047h PubMedCrossRefGoogle Scholar
  135. 135.
    Valpuesta, J. M., J. J. Fernandez, J. M. Carazo, and J. L. Carrascosa 1999 The three-dimensional structure of a DNA translocating machine at 10 A resolution. Structure. 7:289-296. doi: 10.1016/S0969-2126(99)80039-2 PubMedCrossRefGoogle Scholar
  136. 136.
    Valpuesta, J. M., N. Sousa, I. Barthelemy, J. J. Fernandez, H. Fujisawa, B. Ibarra, and J. L. Carrascosa 2000 Structural analysis of the bacteriophage T3 head-to-tail connector. J. Struct. Biol. 131:146-155. doi: 10.1006/jsbi.2000.4281 PubMedCrossRefGoogle Scholar
  137. 137.
    van Blaaderen, A., R. Ruel, and P. Wiltzius 1997 Template-directed colloidal crystallization. Nature. 385(6614):321-324. doi: 10.1038/385321a0 CrossRefGoogle Scholar
  138. 138.
    Vossmeyer, T., et al. 1995 A double diamond superlattice built up of Cd17S4(SCH2CH2OH)(26)clusters. Science. 267:1476-1479. doi: 10.1126/science.267.5203.1476 PubMedCrossRefGoogle Scholar
  139. 139.
    Wargacki, S. P., B. Pate, and R. A. Vaia 2008 Fabrication of 2D ordered films of tobacco mosaic virus (TMV): Processing morphology correlations for convective assembly. Langmuir. 24:5439-5444. doi: 10.1021/la7040778 PubMedCrossRefGoogle Scholar
  140. 140.
    West, S. C. 1996 DNA helicases: New breeds of translocating motors and molecular pumps. Cell. 86:177-180. doi: 10.1016/S0092-8674(00)80088-4 PubMedCrossRefGoogle Scholar
  141. 141.
    Whetten, R. L., et al. 1996 Nanocrystal gold molecules. Adv. Mater. 8:428-433. doi: 10.1002/adma.19960080513 CrossRefGoogle Scholar
  142. 142.
    Xiang, Y., M. C. Morais, D. N. Cohen, V. D. Bowman, D. L. Anderson, and M. G. Rossmann 2008 Crystal and cryoEM structural studies of a cell wall degrading enzyme in the bacteriophage phi29 tail. Proc. Natl. Acad. Sci. U. S. A. 105:9552-9557. doi: 10.1073/pnas.0803787105 PubMedCrossRefGoogle Scholar
  143. 143.
    Xiao, F., D. Moll, S. Guo, and P. Guo 2005 Binding of pRNA to the N-terminal 14 amino acids of connector protein of bacterial phage phi29. Nucleic Acids Res. 33:2640-2649. doi: 10.1093/nar/gki554 PubMedCrossRefGoogle Scholar
  144. 144.
    Xiao, F., J. Sun, O. Coban, P. Schoen, J. C. Wang, R. H. Cheng, and P. Guo 2009 Fabrication of Massive Sheets of Single Layer Patterned Arrays Using Reengineered Phi29 Motor Dodecamer. ACS Nano. 3:100-107. doi: 10.1021/nn800409a PubMedCrossRefGoogle Scholar
  145. 145.
    Xiao, F., H. Zhang, and P. Guo 2008 Novel mechanism of hexamer ring assembly in protein/RNA interactions revealed by single molecule imaging. Nucleic Acids Res. 36 (20):6620-6632. doi: 10.1093/nar/gkn669 PubMedCrossRefGoogle Scholar
  146. 146.
    Yasuda, R., H. Noji, M. Yoshida, K. Kinosita, Jr., and H. Itoh 2001 Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase. Nature. 410(6831):898-904. doi: 10.1038/35073513 PubMedCrossRefGoogle Scholar
  147. 147.
    Zhang, C., M. Su, Y. He, X. Zhao, P. A. Fang, A. E. Ribbe, W. Jiang, and C. D. Mao 2008 Conformational flexibility facilitates self-assembly of complex DNA nanostructures. Proc. Natl. Acad. Sci. USA. 105:10665-10669. doi: 10.1073/pnas.0803841105 PubMedCrossRefGoogle Scholar
  148. 148.
    Zhang, C. L., K. Garver, and P. Guo 1995 Inhibition of phage phi29 assembly by antisense oligonucleotides targeting viral pRNA essential for DNA packaging. Virology. 211:568-576. doi: 10.1006/viro.1995.1439 PubMedCrossRefGoogle Scholar
  149. 149.
    Zhang, F., S. Lemieux, X. Wu, S. St.-Arnaud, C. T. McMurray, F. Major, and D. Anderson 1998 Function of hexameric RNA in packaging of bacteriophage phi29 DNA in vitro. Mol. Cell. 2:141-147. doi: 10.1016/S1097-2765(00)80123-9 PubMedCrossRefGoogle Scholar
  150. 150.
    Zhang, H., D. Shu, F. Huang, and P. Guo 2007 Instrumentation and metrology for single RNA counting in biological complexes or nanoparticles by a single molecule dual-view system. RNA. 13:1793-1802. doi: 10.1261/rna.587607 PubMedCrossRefGoogle Scholar
  151. 151.
    Zheng, N. F., X. H. Bu, and P. Y. Feng 2002 Self-assembly of novel dye molecules and [Cd-8(SPh)(12)](4 +) cubic clusters into three-dimensional photoluminescent souperlattice. J. Am. Chem. Soc. 124:9688-9689. doi: 10.1021/ja020480p PubMedCrossRefGoogle Scholar
  152. 152.
    Zhuang, X., L. E. Bartley, H. P. Babcock, R. Russell, T. Ha, D. Herschlag, and S. Chu 2000 A single-molecule study of RNA catalysis and folding. Science. 288(5473):2048-2051. doi: 10.1126/science.288.5473.2048 PubMedCrossRefGoogle Scholar

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© Biomedical Engineering Society 2009

Authors and Affiliations

  1. 1.Department of Biomedical Engineering, The Vontz Center for Molecular StudiesCollege of Engineering and College of Medicine, University of CincinnatiCincinnatiUSA

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