A Structural Model of the Genome Packaging Process in a Membrane-Containing Double Stranded DNA Virus

PLoS Biology

Volumn 12, Issue 12, 2014, Pages

  Hong, Chuan ^a   Oksanen, Hanna M ^b   Liu, Xiangan ^a   Jakana, Joanita ^a   Bamford, Dennis H ^b   Chiu, Wah ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DOUBLE STRANDED DNA; HETERODIMER; PROTEIN P20; PROTEIN P22; PROTEIN P3; PROTEIN P6; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN; DNA; MEMBRANE PROTEIN;

ARTICLE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; DNA PACKAGING; DNA VIRUS; GENE FUNCTION; GENE IDENTIFICATION; IMAGE RECONSTRUCTION; LIPID BILAYER; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOLECULAR MODEL; NONHUMAN; SIGNAL TRANSDUCTION; VIRION; VIRUS CAPSID; VIRUS ENVELOPE; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS MORPHOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; ENTEROBACTERIA PHAGE PRD1; GENETICS; IMAGE PROCESSING; MEMBRANE; MUTATION; ULTRASTRUCTURE; VIRUS ASSEMBLY;

DNA VIRUSES; MIRIDAE;

BACTERIOPHAGE PRD1; CAPSID; CRYOELECTRON MICROSCOPY; DNA; DNA, VIRAL; GENOME, VIRAL; IMAGE PROCESSING, COMPUTER-ASSISTED; MEMBRANE PROTEINS; MEMBRANES; MODELS, MOLECULAR; MUTATION; VIRAL PROTEINS; VIRION; VIRUS ASSEMBLY;

EID: 84923686122     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002024     Document Type: Article

References (82)

1. Feiss M, Rao VB, (2012) The bacteriophage DNA packaging machine. Adv Exp Med Biol 726: 489–509.
2. Lander GC, Tang L, Casjens SR, Gilcrease EB, Prevelige P, et al. (2006) The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312: 1791–1795.
3. Jiang W, Chang J, Jakana J, Weigele P, King J, et al. (2006) Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439: 612–616.
4. Rochat RH, Liu X, Murata K, Nagayama K, Rixon FJ, et al. (2011) Seeing the portal in herpes simplex virus type 1 B capsids. J Virol 85: 1871–1874.
5. Chen DH, Baker ML, Hryc CF, DiMaio F, Jakana J, et al. (2011) Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus. Proc Natl Acad Sci U S A 108: 1355–1360.
6. Guo P, Lee TJ, (2007) Viral nanomotors for packaging of dsDNA and dsRNA. Mol Microbiol 64: 886–903.
7. Strömsten NJ, Bamford DH, Bamford JK, (2005) In vitro DNA packaging of PRD1: a common mechanism for internal-membrane viruses. J Mol Biol 348: 617–629.
8. Ziedaite G, Kivela HM, Bamford JK, Bamford DH, (2009) Purified membrane-containing procapsids of bacteriophage PRD1 package the viral genome. J Mol Biol 386: 637–647.
9. Happonen LJ, Oksanen E, Liljeroos L, Goldman A, Kajander T, et al. (2013) The structure of the NTPase that powers DNA packaging into Sulfolobus turreted icosahedral virus 2. J Virol 87: 8388–8398.
10. Iyer LM, Makarova KS, Koonin EV, Aravind L, (2004) Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 32: 5260–5279.
11. Benson SD, Bamford JK, Bamford DH, Burnett RM, (1999) Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98: 825–833.
12. Benson SD, Bamford JK, Bamford DH, Burnett RM, (2004) Does common architecture reveal a viral lineage spanning all three domains of life? Mol Cell 16: 673–685.
13. Bamford DH, Burnett RM, Stuart DI, (2002) Evolution of viral structure. Theor Popul Biol 61: 461–470.
14. Bamford DH, (2003) Do viruses form lineages across different domains of life? Res Microbiol 154: 231–236.
15. Rux JJ, Kuser PR, Burnett RM, (2003) Structural and phylogenetic analysis of adenovirus hexons by use of high-resolution x-ray crystallographic, molecular modeling, and sequence-based methods. J Virol 77: 9553–9566.
16. Abrescia NG, Grimes JM, Kivelä HM, Assenberg R, Sutton GC, et al. (2008) Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Mol Cell 31: 749–761.
17. Bahar MW, Graham SC, Stuart DI, Grimes JM, (2011) Insights into the evolution of a complex virus from the crystal structure of vaccinia virus D13. Structure 19: 1011–1020.
18. Khayat R, Tang L, Larson ET, Lawrence CM, Young M, et al. (2005) Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc Natl Acad Sci U S A 102: 18944–18949.
19. Zhang X, Sun S, Xiang Y, Wong J, Klose T, et al. (2012) Structure of Sputnik, a virophage, at 3.5-Å resolution. Proc Natl Acad Sci U S A 109: 18431–18436.
20. Liu H, Jin L, Koh SB, Atanasov I, Schein S, et al. (2010) Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science 329: 1038–1043.
21. Veesler D, Ng TS, Sendamarai AK, Eilers BJ, Lawrence CM, et al. (2013) Atomic structure of the 75 MDa extremophile Sulfolobus turreted icosahedral virus determined by CryoEM and X-ray crystallography. Proc Natl Acad Sci U S A 110: 5504–5509.
22. Pawlowski A, Rissanen I, Bamford JK, Krupovic M, Jalasvuori M, (2014) Gammasphaerolipovirus, a newly proposed bacteriophage genus, unifies viruses of halophilic archaea and thermophilic bacteria within the novel family Sphaerolipoviridae. Arch Virol 159: 1541–1554.
23. Rissanen I, Grimes JM, Pawlowski A, Mantynen S, Harlos K, et al. (2013) Bacteriophage P23-77 capsid protein structures reveal the archetype of an ancient branch from a major virus lineage. Structure 21: 718–726.
24. Abrescia NG, Bamford DH, Grimes JM, Stuart DI, (2012) Structure unifies the viral universe. Annu Rev Biochem 81: 795–822.
25. Bamford DH, Grimes JM, Stuart DI, (2005) What does structure tell us about virus evolution? Curr Opin Struct Biol 15: 655–663.
26. Abrescia NG, Cockburn JJ, Grimes JM, Sutton GC, Diprose JM, et al. (2004) Insights into assembly from structural analysis of bacteriophage PRD1. Nature 432: 68–74.
27. Cockburn JJ, Abrescia NG, Grimes JM, Sutton GC, Diprose JM, et al. (2004) Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature 432: 122–125.
28. San Martin C, Huiskonen JT, Bamford JK, Butcher SJ, Fuller SD, et al. (2002) Minor proteins, mobile arms and membrane-capsid interactions in the bacteriophage PRD1 capsid. Nat Struct Biol 9: 756–763.
29. Davis TN, Muller ED, Cronan JE, Jr (1982) The virion of the lipid-containing bacteriophage PR4. Virology 120: 287–306.
30. Oksanen HM, Bamford DH (2012) Family Tectiviridae. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, editors. Virus taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses. Oxford: Elsevier. pp. 317–322.
31. Rydman PS, Bamford JK, Bamford DH, (2001) A minor capsid protein P30 is essential for bacteriophage PRD1 capsid assembly. J Mol Biol 313: 785–795.
32. Muller ED, Cronan JE, Jr (1983) The lipid-containing bacteriophage PR4. Effects of altered lipid composition on the virion. J Mol Biol 165: 109–124.
33. Laurinavicius S, Käkela R, Somerharju P, Bamford DH, (2004) Phospholipid molecular species profiles of tectiviruses infecting Gram-negative and Gram-positive hosts. Virology 322: 328–336.
34. Jaatinen ST, Viitanen SJ, Bamford DH, Bamford JK, (2004) Integral membrane protein P16 of bacteriophage PRD1 stabilizes the adsorption vertex structure. J Virol 78: 9790–9797.
35. Grahn AM, Caldentey J, Bamford JK, Bamford DH, (1999) Stable packaging of phage PRD1 DNA requires adsorption protein P2, which binds to the IncP plasmid-encoded conjugative transfer complex. J Bacteriol 181: 6689–6696.
36. Bamford JK, Bamford DH, (2000) A new mutant class, made by targeted mutagenesis, of phage PRD1 reveals that protein P5 connects the receptor binding protein to the vertex. J Virol 74: 7781–7786.
37. Huiskonen JT, Manole V, Butcher SJ, (2007) Tale of two spikes in bacteriophage PRD1. Proc Natl Acad Sci U S A 104: 6666–6671.
38. Grahn AM, Daugelavicius R, Bamford DH, (2002) Sequential model of phage PRD1 DNA delivery: active involvement of the viral membrane. Mol Microbiol 46: 1199–1209.
39. Peralta B, Gil-Carton D, Castano-Diez D, Bertin A, Boulogne C, et al. (2013) Mechanism of membranous tunnelling nanotube formation in viral genome delivery. PLoS Biol 11: e1001667.
40. Lundström KH, Bamford DH, Palva ET, Lounatmaa K, (1979) Lipid-containing bacteriophage PR4: structure and life cycle. J Gen Virol 43: 583–592.
41. Bamford D, McGraw T, MacKenzie G, Mindich L, (1983) Identification of a protein bound to the termini of bacteriophage PRD1 DNA. J Virol 47: 311–316.
42. Saren AM, Ravantti JJ, Benson SD, Burnett RM, Paulin L, et al. (2005) A snapshot of viral evolution from genome analysis of the tectiviridae family. J Mol Biol 350: 427–440.
43. Gowen B, Bamford JK, Bamford DH, Fuller SD, (2003) The tailless icosahedral membrane virus PRD1 localizes the proteins involved in genome packaging and injection at a unique vertex. J Virol 77: 7863–7871.
44. Strömsten NJ, Bamford DH, Bamford JK, (2003) The unique vertex of bacterial virus PRD1 is connected to the viral internal membrane. J Virol 77: 6314–6321.
45. Karhu NJ, Ziedaite G, Bamford DH, Bamford JK, (2007) Efficient DNA packaging of bacteriophage PRD1 requires the unique vertex protein P6. J Virol 81: 2970–2979.
46. Liu X, Jiang W, Jakana J, Chiu W, (2007) Averaging tens to hundreds of icosahedral particle images to resolve protein secondary structure elements using a Multi-Path Simulated Annealing optimization algorithm. J Struct Biol 160: 11–27.
47. Liu X, Zhang Q, Murata K, Baker ML, Sullivan MB, et al. (2010) Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat Struct Mol Biol 17: 830–836.
48. Chang J, Weigele P, King J, Chiu W, Jiang W, (2006) Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 14: 1073–1082.
49. Scheres SH, Chen S, (2012) Prevention of overfitting in cryo-EM structure determination. Nat Methods 9: 853–854.
50. Murray SC, Flanagan J, Popova OB, Chiu W, Ludtke SJ, et al. (2013) Validation of cryo-EM structure of IP(3)R1 channel. Structure 21: 900–909.
51. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037–10041.
52. Callebaut I, Labesse G, Durand P, Poupon A, Canard L, et al. (1997) Deciphering protein sequence information through hydrophobic cluster analysis (HCA): current status and perspectives. Cell Mol Life Sci 53: 621–645.
53. Jones DT, (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195–202.
54. Mindich L, Bamford D, Goldthwaite C, Laverty M, Mackenzie G, (1982) Isolation of nonsense mutants of lipid-containing bacteriophage PRD1. J Virol 44: 1013–1020.
55. Agirrezabala X, Martin-Benito J, Valle M, Gonzalez JM, Valencia A, et al. (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.
56. Erickson HP, (2009) Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy. Biol Proced Online 11: 32–51.
57. Butcher SJ, Bamford DH, Fuller SD, (1995) DNA packaging orders the membrane of bacteriophage PRD1. EMBO J 14: 6078–6086.
58. Mindich L, Bamford D, McGraw T, Mackenzie G, (1982) Assembly of bacteriophage PRD1: particle formation with wild-type and mutant viruses. J Virol 44: 1021–1030.
59. Caldentey J, Hanninen AL, Holopainen JM, Bamford JK, Kinnunen PK, et al. (1999) Purification and characterization of the assembly factor P17 of the lipid-containing bacteriophage PRD1. Eur J Biochem 260: 549–558.
60. Bamford JK, Cockburn JJ, Diprose J, Grimes JM, Sutton G, et al. (2002) Diffraction quality crystals of PRD1, a 66-MDa dsDNA virus with an internal membrane. J Struct Biol 139: 103–112.
61. Hänninen AL, Bamford DH, Bamford JK, (1997) Assembly of membrane-containing bacteriophage PRD1 is dependent on GroEL and GroES. Virology 227: 207–210.
62. San Martin C, Burnett RM, de Haas F, Heinkel R, Rutten T, et al. (2001) Combined EM/X-ray imaging yields a quasi-atomic model of the adenovirus-related bacteriophage PRD1 and shows key capsid and membrane interactions. Structure 9: 917–930.
63. Nemecek D, Lander GC, Johnson JE, Casjens SR, Thomas GJ, Jr (2008) Assembly architecture and DNA binding of the bacteriophage P22 terminase small subunit. J Mol Biol 383: 494–501.
64. Johnson JE, (2010) Virus particle maturation: insights into elegantly programmed nanomachines. Curr Opin Struct Biol 20: 210–216.
65. Morais MC, Koti JS, Bowman VD, Reyes-Aldrete E, Anderson DL, et al. (2008) Defining molecular and domain boundaries in the bacteriophage phi29 DNA packaging motor. Structure 16: 1267–1274.
66. Zheng H, Olia AS, Gonen M, Andrews S, Cingolani G, et al. (2008) A conformational switch in bacteriophage p22 portal protein primes genome injection. Mol Cell 29: 376–383.
67. Simpson AA, Tao Y, Leiman PG, Badasso MO, He Y, et al. (2000) Structure of the bacteriophage phi29 DNA packaging motor. Nature 408: 745–750.
68. Roy A, Bhardwaj A, Datta P, Lander GC, Cingolani G, (2012) Small terminase couples viral DNA binding to genome-packaging ATPase activity. Structure 20: 1403–1413.
69. Chistol G, Liu S, Hetherington CL, Moffitt JR, Grimes S, et al. (2012) High degree of coordination and division of labor among subunits in a homomeric ring ATPase. Cell 151: 1017–1028.
70. Ko SH, Chen Y, Shu D, Guo P, Mao C, (2008) Reversible switching of pRNA activity on the DNA packaging motor of bacteriophage phi29. J Am Chem Soc 130: 17684–17687.
71. Conway JF, Wikoff WR, Cheng N, Duda RL, Hendrix RW, et al. (2001) Virus maturation involving large subunit rotations and local refolding. Science 292: 744–748.
72. Atanasova NS, Senčilo A, Pietilä MK, Roine E, Oksanen HM, et al. (2015) Lipid-containing prokaryotic viruses. Editors: Maramorosch K and Murphy F. Elsevier. Adv Virus Res. In press.
73. Bamford JK, Bamford DH, (1990) Capsomer proteins of bacteriophage PRD1, a bacterial virus with a membrane. Virology 177: 445–451.
74. Mindich L, Cohen J, Weisburd M, (1976) Isolation of nonsense suppressor mutants in Pseudomonas. J Bacteriol 126: 177–182.
75. Winston F, Botstein D, Miller JH, (1979) Characterization of amber and ochre suppressors in Salmonella typhimurium. J Bacteriol 137: 433–439.
76. Bamford JK, Bamford DH, (1991) Large-scale purification of membrane-containing bacteriophage PRD1 and its subviral particles. Virology 181: 348–352.
77. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254.
78. Olkkonen VM, Bamford DH, (1989) Quantitation of the adsorption and penetration stages of bacteriophage phi 6 infection. Virology 171: 229–238.
79. Kivioja T, Ravantti J, Verkhovsky A, Ukkonen E, Bamford D, (2000) Local average intensity-based method for identifying spherical particles in electron micrographs. J Struct Biol 131: 126–134.
80. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, et al. (2007) EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol 157: 38–46.
81. Ludtke SJ, Baldwin PR, Chiu W, (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82–97.
82. Olsen RH, Siak JS, Gray RH, (1974) Characteristics of PRD1, a plasmid-dependent broad host range DNA bacteriophage. J Virol 14: 689–699.