A hypothesis for bacteriophage DNA packaging motors

Viruses

Volumn 2, Issue 9, 2010, Pages 1821-1843

  Serwer, Philip ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Bacteriophage structure; Biological energy transduction; Biological signal noise; Cryo electron microscopy; Single molecule analysis

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BACTERIOPHAGE DNA; CHAPERONIN; DOUBLE STRANDED DNA; GLYCOPROTEIN GP 19; MOLECULAR MOTOR; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE T3; BACTERIOPHAGE T4; BASE MISPAIRING; CRYSTALLOGRAPHY; DNA CLEAVAGE; DNA METHYLATION; DNA PACKAGING; DNA SYNTHESIS; ENERGY TRANSFER; ENZYME ACTIVITY; HIGH TEMPERATURE PROCEDURES; INTERMETHOD COMPARISON; MOLECULAR INTERACTION; NONHUMAN; PROTEIN FOLDING; PROTEIN FUNCTION; SIGNAL NOISE RATIO; THERMAL RATCHETING; THERMODYNAMICS; VIRUS CAPSID; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS MUTATION;

EID: 79952154608     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v2091821     Document Type: Article

References (93)

1. Pajunen, M.I.; Elizondo, M.R.; Skurnik, M.; Kieleczawa, J.; Molineux, I.J. Complete nucleotide sequence and likely recombinatorial origin of bacteriophage T3. J. Mol. Biol. 2002, 319, 1115-1132.
2. Fujisawa, H.; Kimura, M.; Hashimoto, C. In vitro cleavage of the concatemer joint of bacteriophage T3 DNA. Virology 1990, 174, 26-34.
3. Catalano, C.E. The terminase enzyme from bacteriophage lambda: a DNA-packaging machine. Cell Mol. Life Sci. 2000, 57, 128-148.
4. Petrov, A.S.; Harvey, S.C. Packaging double-helical DNA into viral capsids: structures, forces, and energetics. Biophys. J. 2008, 95, 497-502.
5. Rao, V.B.; Feiss, M. The bacteriophage DNA packaging motor. Annu. Rev. Genet. 2008, 42, 647-681.
6. Lee, T.J.; Schwartz, C.; Guo, P. Construction of bacteriophage phi29 DNA packaging motor and its applications in nanotechnology and therapy. Ann. Biomed. Engineering 2009, 37, 2064-2081.
7. Ponchon, L.; Boulanger, P.; Labesse, G.; Letellier, L. The endonuclease domain of bacteriophage terminases belongs to the resolvase/integrase/ribonuclease H superfamily: a bioinformatics analysis validated by a functional study on bacteriophage T5. J. Biol. Chem. 2006, 281, 5829-5836.
8. Al-Zahrani, A.S.; Kondabagil, K.; Gao, S.; Kelly, N.; Ghosh-Kumar, M.; Rao, V.B. The small terminase, gp16, of bacteriophage T4 is a regulator of the DNA packaging motor. J. Biol. Chem. 2009, 284, 24490-24500.
9. Bogner, E. Human cytomegalovirus terminase as a target for antiviral chemotherapy. Rev. Med. Virol. 2002, 12, 115-127.
10. Cardone, G.; Winkler, D.C.; Trus, B.L.; Cheng, N.; Heuser, J.E.; Newcomb, W.W.; Brown, J.C.; Steven, A.C. Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 2007, 361, 426-434.
11. Sheaffer, A.K.; Newcomb, W.W.; Gao, M.; Yu, D.; Weller, S.K.; Brown, J.C.; Tenney, D.J. Herpes simplex virus DNA cleavage and packaging proteins associate with the procapsid prior to its maturation. J. Virol. 2001, 75, 687-698.
12. Serwer, P.; Hayes, S.J.; Zaman, S.; Lieman, K.; Rolando, M.; Hardies, S.C. Improved isolation of undersampled bacteriophages: finding of distant terminase genes. Virology 2004, 329, 412-424.
13. Baker, M.L.; Jiang, W.; Rixon, F.J.; Chiu, W. Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 2005, 79, 14967-14970.
14. Kutschera, U.; Niklas, K.J. The modern theory of biological evolution: an expanded synthesis. Naturwissenschaften 2004, 91, 255-276.
15. 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.
16. 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.
17. 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.
18. Hendrix, R.W. Symmetry mismatch and DNA packaging in large bacteriophages. Proc. Natl. Acad. Sci. U. S. A. 1978, 75, 4779-4783.
19. 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.
20. Grimes, S.; D. Anderson, D. The bacteriophage phi29 packaging proteins supercoil the DNA ends. J. Mol. Biol. 1997, 266, 901-914.
21. Simpson, A.A.; Tao, Y.; Leiman, P.G.; Badasso, M.O.; He, Y.; Jardine, P.J.; Olson, N.H.; Morais, M.C.; Grimes, S.; Anderson, D.L.; Baker, T.S.; Rossmann, M.G. Structure of the bacteriophage phi29 DNA packaging motor. Nature 2000, 408, 745-750.
22. 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.
23. Hügel, T.; Michaelis, J.; Hetherington, C.L.; Jardine, P.J.; Grimes, S.; Walter, J.M.; Falk, W.; Anderson, D.L.; Bustamante, C. Experimental test of connector rotation during DNA packaging into bacteriophage phi29 capsids. PLoS Biol. 2007, 5, e59.
24. 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.
25. Serwer, P. The source of energy for bacteriophage DNA packaging: an osmotic pump explains the data. Biopolymers 1988, 27, 165-169.
26. Serwer, P. Models of bacteriophage DNA packaging motors. J. Struct. Biol. 2003, 141, 179-188.
27. Alberts, B.; Miake-Lye, R. Unscrambling the puzzle of biological machines: the importance of the details, Cell 1992, 68, 415-420.
28. Howard, J. Motor proteins as nanomachines: The roles of thermal fluctuations in generating force and motion. Séminaire Poincaré 2009, 12, 33-44.
29. Mickler, M.; Schleiff, E.; Hügel, T. From biological towards artificial molecular motors. Chemphyschem. 2008, 9, 1503-1509.
30. 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.
31. Fuller, D.N.; Raymer, D.M.; Rickgauer, J.P.; Robertson, R.M.; Catalano, C.E.; Anderson, D.L.; Grimes, S.; Smith, D.E. Measurements of single DNA molecule packaging dynamics in bacteriophage lambda reveal high forces, high motor processivity, and capsid transformations. J. Mol. Biol. 2007, 373, 1113-1122.
32. Yang, Q.; Maluf, N.K.; Catalano, C.E. Packaging of a unit-length viral genome: the role of nucleotides and the gpD decoration protein in stable nucleocapsid assembly in bacteriophage lambda. J. Mol. Biol. 2008, 383, 1037-1048.
33. JConway, J.F.; Cheng, N.; Ross, P.D.; Hendrix, R.W.; Duda, R.L.; Steven, A.C. A thermally induced phase transition in a viral capsid transforms the hexamers, leaving the pentamers unchanged. J. Struct. Biol. 2007, 158, 224-232.
34. Gertsman, I.; Komives, E.A.; Johnson, J.E. HK97 maturation studied by crystallography and H/2H exchange reveals the structural basis for exothermic particle transitions J. Mol. Biol. 2010, 397, 560-574.
35. Tuma, R.; Prevelige, P.E., Jr.; Thomas, G.J., Jr. Mechanism of capsid maturation in a double-stranded DNA virus. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 9885-9890.
36. Lander, G.C.; Evilevitch, A.; Jeembaeva, M.; Potter, C.S.; Carragher, B.; Johnson, J.E. Bacteriophage lambda stabilization by auxiliary protein gpD: timing, location, and mechanism of attachment determined by cryo-EM. Structure 2008, 16, 1399-1406.
37. Agirrezabala, X.; Martin-Benito, J.; Valle, M.; Gonzalez, J.M.; Valencia, A.; J. Valpuesta, J.M.; Carrascosa, J.L. 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.
38. Lebedev, A.A.; Krause, M.H.; Isidro, A.L.; Vagin, A.A.; Orlova, E.V.; Turner, J.; Dodson, E.J.; Tavares, P.; Antson, A.A. Structural framework for DNA translocation via the viral portal protein. EMBO J. 2007, 26, 1984-1994.
39. Hardies, S.C.; Serwer, P. Alignment and structural modeling of DNA packaging ATPases: Utilization of a steric clamp to hold the DNA. XXth Biennial Conference on Phage/Virus Assembly 2007, Toronto, Canada.
40. Grimes, S.; Jardine, P.J.; Anderson, D. Bacteriophage phi 29 DNA packaging. Adv. Virus Res. 2002, 58, 255-294.
41. Guo, P.; Peterson, C.; Anderson, D. Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi 29. J. Mol. Biol. 1987, 197, 229-236.
42. Hamada, K.; Fujisawa, H.; Minagawa, T. Characterization of ATPase activity of a defined in vitro system for packaging of bacteriophage T3 DNA. Virology 1987, 159, 244-249.
43. Yanagida, T. Fluctuation as a tool of biological molecular machines. Biosystems 2008, 93, 3-7.
44. Verbrugge, S.; Lechner, B.; Woehlke, G.; Peterman, E.J. Alternating-site mechanism of kinesin-1 characterized by single-molecule FRET using fluorescent ATP analogues. Biophys. J. 2009, 97, 173-182.
45. Petrov, A.S.; Lim-Hing, K.; Harvey, S.C. Packaging of DNA by bacteriophage epsilon15: structure, forces, and thermodynamics. Structure 2007, 15, 807-812.
46. Fang, P.A.; Wright, E.T.; Weintraub, S.T.; Hakala, K.; Wu, W.; Serwer, P.; Jiang, W. Visualization of bacteriophage T3 capsids with DNA incompletely packaged in vivo. J. Mol. Biol. 2008, 384, 1384-1399.
47. Smith, D.E.; Tans, S.J.; Smith, S.B.; Grimes, S.; Anderson, D.L.; Bustamante, C. The bacteriophage straight phi29 portal motor can package DNA against a large internal force. Nature 2001, 413, 748-752.
48. Rickgauer, J.P.; Fuller, D.N.; Grimes, S.; Jardine, P.J.; Anderson, D.L.; Smith, D.E. Portal motor velocity and internal force resisting viral DNA packaging in bacteriophage phi29. Biophys. J. 2008, 94, 159-167.
49. Fuller, D.N.; Raymer, D.M.; Kottadiel, V.I.; Rao, V.B.; Smith, D.E. Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 16868-16873.
50. Koch, A.L. Shrinkage of growing Escherichia coli cells by osmotic challenge. J. Bact. 1984, 159, 919-924.
51. 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.
52. 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.
53. 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.
54. Gope, R.; Serwer, P. Bacteriophage P22 in vitro DNA packaging monitored by agarose gel electrophoresis: rate of DNA entry into capsids. J. Virol. 1983, 47, 96-105.
55. Son, M.; Hayes, S.J.; Serwer, P. Optimization of the in vitro packaging efficiency of bacteriophage T7 DNA: effects of neutral polymers. Gene 1989, 82, 321-325.
56. Shibata, H.; Fujisawa, H.; Minagawa, T. Characterization of the bacteriophage T3 DNA packaging reaction in vitro in a defined system. J. Mol. Biol. 1987, 196, 845-851.
57. Oliveira, L.; Alonso, J.C.; Tavares, P. A defined in vitro system for DNA packaging by the bacteriophage SPP1: insights into the headful packaging mechanism. J. Mol. Biol. 2005, 353, 529-539.
58. Morais, M.C.; Koti, J.S.; Bowman, V.D.; Reyes-Aldrete, E.; Anderson, D.L.; Rossmann, M.G. Defining molecular and domain boundaries in the bacteriophage phi29 DNA packaging motor. Structure 2008, 16, 1267-1274.
59. Cuervo, A.; Vaney, M.C.; Antson, A.A.; Tavares, P.; Oliveira, L. Structural rearrangements between portal protein subunits are essential for viral DNA translocation. J. Biol. Chem. 2007, 282, 18907-18913.
60. Oliveira, L.; Henriques, A.O.; Tavares, P. Modulation of the viral ATPase activity by the portal protein correlates with DNA packaging efficiency. J. Biol. Chem. 2006, 281, 21914-21923.
61. Michaelis, J.; Muschielok, A.; Adrecka, J.; Kügel, W.; Moffitt, J.R. DNA based molecular motors. Phys. Life Rev. 2009, 6, 250-266.
62. Fink, T.M.; Ball, R.C. How many conformations can a protein remember?, Phys. Rev. Lett. 2001, 87, 198103.
63. Atz, R.; Ma, S.; Aathavan, K.; Bustamante, C.; Gao, J.; Anderson, D.L.; Grimes, S. Role of 4)29 connector channel domains in late phase DNA-gp3 packaging. XXth Biennial Conference on Phage/Virus Assembly 2007, Toronto, Canada.
64. Pearson, R.K.; Fox, M.S. Effects of DNA heterologies on bacteriophage lambda packaging. Genetics 1988, 118, 5-12.
65. Louie, D.; Serwer, P. Quantification of the effect of excluded volume on double-stranded DNA. J. Mol. Biol. 1994, 242, 547-558.
66. Higgins, C.F. Multiple molecular mechanisms for multidrug resistance transporters. Nature 2007, 446, 749-757.
67. Linton, K.J. Structure and function of ABC transporters. Physiology 2007, 22, 122-130.
68. Lin, Z.; Madan, D.; Rye, H.S. GroEL stimulates protein folding through forced unfolding. Nature Struct. Mol. Biol. 2008, 15, 303-311.
69. Horwich, A.L.; Fenton, W.A. Chaperonin-mediated protein folding: using a central cavity to kinetically assist polypeptide chain folding. Q. Rev. Biophys. 2009, 42, 83-116.
70. Jewett, A.I.; Shea, J.E. Reconciling theories of chaperonin accelerated folding with experimental evidence. Cell Mol. Life Sci. 2010, 67, 255-276.
71. Zaikin, A.; Garcia-Ojalvo, J.; Bascones, R.; Ullner, E.; Kurths, J. Doubly stochastic coherence via noise-induced symmetry in bistable neural models. Phys. Rev. Lett. 2003, 90, 030601.
72. Ray, K.; Oram, M.; Ma, J.; Black, L.W. Portal control of viral prohead expansion and DNA packaging. Virology 2009, 391, 44-50.
73. Fujisawa, H.; Kimura, M.; Hashimoto, C. In vitro cleavage of the concatemer joint of bacteriophage T3 DNA. Virology 1990, 174, 26-34.
74. Casjens, S.; Wyckoff, E.; Hayden, M.; Sampson, L.; Eppler, K.; Randall, S.; Moreno, E.T.; Serwer, P. Bacteriophage P22 portal protein is part of the gauge that regulates packing density of intravirion DNA. J. Mol. Biol. 1992, 224, 1055-1074.
75. Nemecek, D.; Lander, GC.; Johnson, J.E.; Casjens, S.R.; Thomas, G.J., Jr. Assembly architecture and DNA binding of the bacteriophage P22 terminase small subunit. J. Mol. Biol. 2008, 383, 494-501.
76. Morais, M.C.; Tao, Y.; Olson, N.H.; Grimes, S.; Jardine, P.J.; Anderson, D.L.; Baker, T.S.; Rossmann, M.G. Cryoelectron-microscopy image reconstruction of symmetry mismatches in bacteriophage phi29. J. Struct. Biol. 2001, 135, 38-46.
77. Feynmann, R.P.; Leighton, R.B.; Sands, M.L. The Feynman Lectures on Physics, 2nd ed.; Addison-Wesley, Reading, MA, USA, 1963, Volume I, Chapter 46.
78. Fujisawa, H.; Morita, M. Phage DNA packaging. Genes Cells 1997, 2, 537-545.
79. Huxley, A.F. Muscle structure and theories of contraction. Prog. Biophys. Biophys. Chem. 1957, 7, 255-318.
80. Donnan, F.G.; The mystery of Life, Smithsonian Report for 1929. 1929; pp. 309-321.
81. Ishii, Y.; Taniguchi, Y.; Iwaki, M.; Yanagida, T. Thermal fluctuations biased for directional motion in molecular motors. BioSystems 2008, 93, 34-38.
82. Iwaki, M.; Iwane, A.H.; Shimokawa, T.; Cooke, R.; Yanagida, T. Brownian search-and-catch mechanism for myosin-VI steps. Nat. Chem. Biol. 2009, 5, 403-405.
83. Sun, S.; Kondabagil, K.; Draper, B.; Alam, T.I.; Bowman, V.D.; Zhang, Z.; Hegde, S.; Fokine, A.; Rossmann, M.G.; Rao, V.B. The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell 2008, 135, 1251-1262.
84. Singh, K.P.; Ropars, G.; Brunel, M.; Le Floch, A. Lever-assisted two-noise stochastic resonance. Phys. Rev. Lett. 2003, 90, 073901.
85. Ropars, G.; Singh, K.P.; Brunel, M.; Dore, F.; Le Floch, A. The dual stochastic response of nonlinear systems. Europhys. Lett. 2004, 68, 755-761.
86. Beuron, F.; Maurizi, M.R.; Belnap, D.M.; Kocsis, E.; Booy, F.P.; Kessel, M.; Steven, A.C. At sixes and sevens: characterization of the symmetry mismatch of the ClpAP chaperone-assisted protease. J. Struct. Biol. 1998, 123. 248-259.
87. Bewley, M.C.; Graziano, V.; Griffin, K.; Flanagan, J.M. The asymmetry in the mature amino-terminus of ClpP facilitates a local symmetry match in ClpAP and ClpXP complexes. J. Struct. Biol. 2006, 153, 113-128.
88. 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.
89. Klug, A. Architectural design of spherical viruses. Nature 1983, 303, 378-379.
90. Jiang, W.; Chang, J.; Jakana, P.; Weigele, J.; King, J.A.; Chiu, W. Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 2006, 439, 612-616.
91. Johnson, J.E.; Chiu, W. DNA packaging and delivery machines in tailed bacteriophages. Curr. Opin. Struct. Biol. 2007, 17, 237-243.
92. Yu, J.; Moffitt, J.; Hetherington, C.L.; Bustamante, C.; and Oster, G. Mechanochemistry of a viral DNA packging motor. J. Mol. Biol. 2010, 400, 186-203.
93. Sun, M.; Louie, D.; Serwer, P. Single-event analysis of the packaging of bacteriophage T7 DNA concatemers in vitro. Biophys. J. 1999, 77, 1627-1637.