Thermodynamic characterization of viral procapsid expansion into a functional capsid shell

Journal of Molecular Biology

Volumn 418, Issue 3-4, 2012, Pages 167-180

  Medina, Elizabeth ^a   Nakatani, Eri ^a   Kruse, Shannon ^a   Catalano, Carlos Enrique ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

bacteriophage lambda; herpesviruses; macromolecular transitions; thermodynamics; virus assembly

Indexed keywords

MAGNESIUM; UREA;

ARTICLE; CHEMICAL PHENOMENA; CONCENTRATION (PARAMETERS); DNA VIRUS; HYDROPHOBICITY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; TEMPERATURE DEPENDENCE; THERMODYNAMICS; VIRUS CAPSID;

DNA VIRUSES; ENTEROBACTERIA PHAGE LAMBDA; MIRIDAE;

EID: 84859270120     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.02.020     Document Type: Article

References (71)

1. Calendar R., and Abedon S.T. The Bacteriophages 2006 Oxford University Press New York, NY
2. Roizman B., and Palese P. Multiplication of viruses: an overview B.N. Fields, D.M. Knipe, P.M. Howley, Fields Virology 3rd edit. 1996 Lippincott-Raven New York, NY 101 111
3. Rao V.B., and Feiss M. The bacteriophage DNA packaging motor Annu. Rev. Genet. 42 2008 647 681
4. Roizman B., Knipe D.M., and Whitley R.J. Herpes simplex viruses D.M. Knipe, P.M. Howley, Fields Virology 5th edit. 2007 Lippincott, Williams and Wilkins Philadelphia, PA 2501 2602
5. Catalano C.E. Viral genome packaging machines: an overview C.E. Catalano, Viral Genome Packaging Machines: Genetics, Structure, and Mechanism 2005 Kluwer Academic Plenum Publishers New York, NY 1 4
6. Baines J.D., and Weller S.K. Cleavage and packaging of herpes simplex virus 1 DNA C.E. Catalano, Viral Genome Packaging Machines: Genetics, Structure, and Mechanism 2005 Kluwer Academic Plenum Publishers New York, NY 135 149
7. Feiss M., and Catalano C.E. Bacteriophage lambda terminase and the mechanism of viral DNA packaging C.E. Catalano, Viral Genome Packaging Machines: Genetics, Structure, and Mechanism 2005 Kluwer Academic Plenum Publishers New York, NY 5 39
8. Jardine P.J., and Anderson D.L. DNA packaging in double-stranded DNA phages R. Calendar, S.T. Abedon, The Bacteriophages 2nd edit. 2006 Oxford University Press New York, NY 49 65
9. Baines J.D., and Duffy C. Nucloeocapsid assembly and envelopment of herpes simplex virus R.M. Sandri-Goldin, Alpha Herpesviruses: Molecular and Cellular Biology 2006 Caister Academic Press Norfolk, VA 175 204
10. Alonso J.C., Tavares P., Lurz R., and Trautner T.A. Bacteriophage SPP1 R. Calendar, S.T. Abedon, The Bacteriophages 2nd edit. 2006 Oxford University Press New York, NY 331 349
11. Hendrix R.W., and Casjens S. Bacteriophage lambda and its genetic neighborhood R. Calendar, S.T. Abedon, The Bacteriophages 2nd edit. 2006 Oxford University Press New York, NY 409 447
12. Hendrix R.W., Roberts J.W., Stahl F.W., and Weisberg R.A. Lambda II 1983 Cold Spring Harbor Laboratory Cold Spring Harbor, NY
13. Medina E., Wieczorek D.J., Medina E.M., Yang Q., Feiss M., and Catalano C.E. Assembly and maturation of the bacteriophage lambda procapsid: gpC is the viral protease J. Mol. Biol. 401 2010 813 830
14. Georgopoulos C., Tilly K., and Casjens S. Lambdoid phage head assembly R.W. Hendrix, J.W. Roberts, F.W. Stahl, R.A. Weisberg, Lambda II 1983 Cold Spring Harbor Laboratory Cold Spring Harbor, NY 279 304
15. Kochan J., and Murialdo H. Early intermediates in bacteriophage lambda prohead assembly. II. Identification of biologically active intermediates Virology 131 1983 100 115 (Pubitemid 14248602)
16. Medina E.M., Andrews B.T., Nakatani E., and Catalano C.E. The bacteriophage lambda gpNu3 scaffolding protein is an intrinsically disordered and biologically functional procapsid assembly catalyst J. Mol. Biol. 412 2011 723 736
17. Johnson J.E. Virus particle maturation: insights into elegantly programmed nanomachines Curr. Opin. Struct. Biol. 20 2010 210 216
18. Fane B.A., and Prevelige P.E. Mechanism of scaffolding-assisted viral assembly C. Wah, E.J. John, Virus Structure 64 2003 Academic Press Oxford, UK 259 299 (Pubitemid 37070658)
19. Dokland T. Scaffolding proteins and their role in viral assembly Cell. Mol. Life Sci. 56 1999 580 603
20. Fuller D.N., Raymer D.M., Rickgauer J.P., Robertson R.M., Catalano C.E., and Anderson D.L. Measurements of single DNA molecule packaging dynamics in bacteriophage lambda reveal high forces, high motor processivity, and capsid transformations J. Mol. Biol. 373 2007 1113 1122 (Pubitemid 47542509)
21. Hohn T., Wurtz M., and Hohn B. Capsid transformation during packaging of bacteriophage lambda DNA Philos. Trans. R. Soc. London 276 1976 51 61
22. Hohn T., Morimasa T., and Tsugita A. The capsid protein of bacteriophage lambda and of its prehead J. Mol. Biol. 105 1976 337 342
23. Dokland T., and Murialdo H. Structural transitions during maturation of bacteriophage lambda capsids J. Mol. Biol. 233 1993 682 694 (Pubitemid 23314779)
24. Steven A.C., Heymann J.B., Cheng N., Trus B.L., and Conway J.F. Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity Curr. Opin. Struct. Biol. 15 2005 227 236
25. Black L.W. DNA packaging in dsDNA bacteriophages Annu. Rev. Microbiol. 43 1989 267 292 (Pubitemid 19250048)
26. Duda R.L., Hempel J., Michel H., Shabanowitz J., Hunt D., and Hendrix R.W. Structural transitions during bacteriophage HK97 head assembly J. Mol. Biol. 247 1995 618 635
27. Galisteo M.L., and King J. Conformational transformations in the protein lattice of phage P22 procapsids Biophys. J. 65 1993 227 235 (Pubitemid 23206056)
28. Kunzler P., and Hohn T. Stages of bacteriophage lambda head morphogenesis: physical analysis of particles in solution J. Mol. Biol. 122 1978 191 211 (Pubitemid 8374260)
29. Imber R., Tsugita A., Wurtz M., and Hohn T. Outer surface protein of bacteriophage lambda J. Mol. Biol. 139 1980 277 295 (Pubitemid 10016712)
30. Newcomb W.W., Homa F.L., Thomsen D.R., Booy F.P., Trus B.L., and Steven A.C. Assembly of the herpes simplex virus capsid: characterization of intermediates observed during cell-free capsid formation J. Mol. Biol. 263 1996 432 446 (Pubitemid 26375527)
31. Conway J.F., Duda R.L., Cheng N., Hendrix R.W., and Steven A.C. Proteolytic and conformational control of virus capsid maturation: the bacteriophage HK97 system J. Mol. Biol. 253 1995 86 99
32. Santoro M.M., and Bolen D.W. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants Biochemistry 18 1988 8063 8068
33. Pace C.N., and Shaw K.L. Linear extrapolation method of analyzing solvent denaturation curves Proteins 4 2000 1 7
34. Santoro M.M., and Bolen D.W. A test of the linear extrapolation of unfolding free energy changes over an extended denaturant concentration range Biochemistry 31 1992 4901 4907
35. N-U values in a thermodynamic cycle Biochemistry 18 1988 8069 8074
36. Yang Q., and Catalano C.E. Biochemical characterization of bacteriophage lambda genome packaging in vitro Virology 305 2003 276 287 (Pubitemid 36259662)
37. Gaussier H., Yang Q., and Catalano C.E. Building a virus from scratch: assembly of an infectious virus using purified components in a rigorously defined biochemical assay system J. Mol. Biol. 357 2006 1154 1166 (Pubitemid 43361922)
38. Yang Q., Maluf N.K., and 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. 383 2008 1037 1048
39. Murialdo H., and Becker A. Head morphogenesis of complex double-stranded deoxyribonucleic acid bacteriophages Microbiol. Rev. 42 1978 529 576 (Pubitemid 9044053)
40. Medina, E. (2010). Growing Pains of Bacteriophage Lambda: Examination of the Maturation of Procapsids into Capsids. Ph.D., University of Washington.
41. Lander G.C., Evilevitch A., Jeembaeva M., Potter C.S., Carragher B., and Johnson J.E. Bacteriophage lambda stabilization by auxiliary protein gpD: timing, location, and mechanism of attachment determined by cryo-EM Structure 16 2008 1399 1406
42. Conway J.F., Cheng N., Ross P.D., Hendrix R.W., Duda R.L., and Steven A.C. A thermally induced phase transition in a viral capsid transforms the hexamers, leaving the pentamers unchanged J. Struct. Biol. 158 2007 224 232 (Pubitemid 46729662)
43. Jardine P.J., and Coombs D.H. Capsid expansion follows the initiation of DNA packaging in bacteriophage T4 J. Mol. Biol. 284 1998 661 672 (Pubitemid 28550013)
44. Lee K.K., Tsuruta H., Hendrix R.W., Duda R.L., and Johnson J.E. Cooperative reorganization of a 420 subunit virus capsid J. Mol. Biol. 352 2005 723 735 (Pubitemid 41225481)
45. Lata R., Conway J.F., Cheng N., Duda R.L., Hendrix R.W., and Wikoff W.R. Maturation dynamics of a viral capsid: visualization of transitional intermediate states Cell 100 2000 253 263 (Pubitemid 30064913)
46. Fuller D.N., Raymer D.M., Kottadiel V.I., Rao V.B., and Smith D.E. Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability Proc. Natl Acad. Sci. USA 104 2007 16868 16873 (Pubitemid 350210957)
47. Tsay J.M., Sippy J., Feiss M., and Smith D.E. The Q motif of a viral packaging motor governs its force generation and communicates ATP recognition to DNA interaction Proc. Natl Acad. Sci. USA 106 2009 14355 14360
48. Salunke D.M., Caspar D.L., and Garcea R.L. Polymorphism in the assembly of polyomavirus capsid protein VP1 Biophys. J. 56 1989 887 900
49. Salunke D.M., Caspar D.L.D., and Garcea R.L. Self-assembly of purified polyomavirus capsid protein VP1 Cell 46 1986 895 904 (Pubitemid 16027938)
50. Brady J.N., Winston V.D., and Consigli R.A. Dissociation of polyoma virus by the chelation of calcium ions found associated with purified virions J. Virol. 23 1977 717 724 (Pubitemid 8172791)
51. Yanagi K., and Harada S. Destabilization of herpes simplex virus type 1 virions by local anesthetics, alkaline pH, and calcium depletion Arch. Virol. 108 1989 151 159 (Pubitemid 20055725)
52. Sternberg N., and Weisberg R. Packaging of coliphage lambda DNA: II. The role of the gene D protein J. Mol. Biol. 117 1977 733 759 (Pubitemid 8256701)
53. Sternberg N., and Hoess R.H. Display of peptides and proteins on the surface of bacteriophage lambda Proc. Natl Acad. Sci. USA 92 1995 1609 1613
54. Bode V.C., and Harrison D.P. Distinct effects of diamines, polyamines, and magnesium ions on the stability of lambda phage heads Biochemistry 12 1973 3193 3196
55. Gertsman I., Gan L., Guttman M., Lee K., Speir J.A., and Duda R.L. An unexpected twist in viral capsid maturation Nature 458 2009 646 650
56. Nurmemmedov E., Castelnovo M., Medina E., Catalano C.E., and Evilevitch A. Challenging packaging limits and infectivity of phage lambda J. Mol. Biol. 415 2012 263 273
57. Fuller D.N., Rickgauer J.P., Jardine P.J., Grimes S., Anderson D.L., and Smith D.E. Ionic effects on viral DNA packaging and portal motor function in bacteriophage phi29 Proc. Natl Acad. Sci. USA 104 2007 11245 11250 (Pubitemid 47175126)
58. Yang Q., Catalano C.E., and Maluf N.K. Kinetic analysis of the genome packaging reaction in bacteriophage lambda Biochemistry 48 2009 10705 10715
59. Baldwin R.L. Temperature dependence of the hydrophobic interaction in protein folding Proc. Natl Acad. Sci. USA 83 1986 8069 8072 (Pubitemid 17182445)
60. Makhatadze G.I., and Privalov P.L. Protein interactions with urea and guanidinium chloride: a calorimetric study J. Mol. Biol. 226 1992 491 505
61. Schellman J.A. Temperature, stability, and the hydrophobic interaction Biophys. J. 73 1997 2960 2964 (Pubitemid 27525762)
62. Myers J.K., Pace C.N., and Scholtz J.M. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding Protein Sci. 4 1995 2138 2148
63. Tzlil S., Kindt J.T., Gelbart W.M., and Ben-Shaul A. Forces and pressures in DNA packaging and release from viral capsids Biophys. J. 84 2003 1616 1627 (Pubitemid 36322926)
64. Evilevitch A., Lavelle L., Knobler C.M., Raspaud E., and Gelbart W.M. Osmotic pressure inhibition of DNA ejection from phage Proc. Natl Acad. Sci. USA 100 2003 9292 9295 (Pubitemid 37033922)
65. Nurmemmedov E., Castelnovo M., Catalano C.E., and Evilevitch A. Biophysics of viral infectivity: matching genome length with capsid size Q. Rev. Biophys. 40 2007 327 356 (Pubitemid 351569385)
66. Yang F., Forrer P., Dauter Z., Conway J.F., Cheng N., and Cerritelli M.E. Novel fold and capsid-binding properties of the lambda phage display platform protein gpD Nat. Struct. Biol. 7 2000 230 237 (Pubitemid 30140770)
67. Iwai H., Forrer P., Pluckthun A., and Guntert P. NMR solution structure of the monomeric form of the bacteriophage lambda capsid stabilizing protein gpD J. Biomol. NMR 31 2005 351 356 (Pubitemid 41348911)
68. Rao V.B., and Black L.W. DNA packaging of bacteriophage T4 proheads in vitro. Evidence that prohead expansion is not coupled to DNA packaging J. Mol. Biol. 185 1985 565 578 (Pubitemid 15241165)
69. Zhang Z., Kottadiel V.I., Vafabakhsh R., Dai L., Chemla Y.R., Ha T., and Rao V.B. A promiscuous DNA packaging machine from bacteriophage T4 PLoS Biol. 9 2011 e1000592
70. Tomka M.A., and Catalano C.E. Physical and kinetic characterization of the DNA packaging enzyme from bacteriophage lambda J. Biol. Chem. 268 1993 3056 3065 (Pubitemid 23070926)
71. Filutowicz M., Grimek H., and Appekt K. Purification of the Escherichia coli integration host factor (IHF) in one chromatographic step Gene 147 1996 149 150