Structure-function analysis of the DNA translocating portal of the bacteriophage T4 packaging machine

Journal of Molecular Biology

Volumn 426, Issue 5, 2014, Pages 1019-1038

  Padilla Sanchez, Victor ^a   Gao, Song ^a,b   Kim, Hyung Rae ^c   Kihara, Daisuke ^c,d   Sun, Lei ^c   Rossmann, Michael G ^c   Rao, Venigalla B ^a  

^a CATHOLIC UNIVERSITY OF AMERICA   (United States)

^b HUAIHAI INSTITUTE OF TECHNOLOGY   (China)

^c PURDUE UNIVERSITY   (United States)

^d Purdue University   (United States)

Author keywords

DNA packaging motor; head assembly; headful packaging; portal vertex; structural modeling

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO ACID; CAPSID PROTEIN; MONOMER; NUCLEASE; VIRUS DNA;

AGAR GEL ELECTROPHORESIS; AMINO ACID SEQUENCE; ARTICLE; BACTERIOPHAGE T4; COLUMN CHROMATOGRAPHY; CROSS LINKING; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DELETION MUTANT; DENSITY GRADIENT CENTRIFUGATION; DNA PACKAGING; DNA TRANSLOCATION PORTAL; HEAD; MOLECULAR WEIGHT; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; STRUCTURE ACTIVITY RELATION; VIRAL PHENOMENA AND FUNCTIONS; VIRION; VIRUS CAPSID; VIRUS GENOME; VIRUS PARTICLE; BACTERIAL TRANSLOCATION; BINDING ASSAY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA DETERMINATION; ENERGY TRANSFER; ENTEROBACTERIA PHAGE T4; MUTAGENESIS; PLASMID; PROGENY; PROTEIN STRUCTURE; VIRUS MORPHOLOGY; WESTERN BLOTTING;

ESCHERICHIA COLI; MIRIDAE;

DNA PACKAGING MOTOR; HEAD ASSEMBLY; HEADFUL PACKAGING; PORTAL VERTEX; STRUCTURAL MODELING;

BACTERIOPHAGE T4; CAPSID PROTEINS; DNA PACKAGING; DNA, VIRAL; ESCHERICHIA COLI; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; VIRION; VIRUS ASSEMBLY;

EID: 84894029950     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.10.011     Document Type: Article

References (71)

1. V.B. Rao, and M. Feiss The bacteriophage DNA packaging motor Annu Rev Genet 42 2008 647 681
2. S.R. Casjens The DNA-packaging nanomotor of tailed bacteriophages Nat Rev Microbiol 9 2011 647 657
3. L.W. Black, and V.B. Rao Structure, assembly, and DNA packaging of the bacteriophage T4 head Adv Virus Res 82 2012 119 153
4. R.A. Driedonks, A. Engel, B. tenHeggeler, and D. van Gene 20 product of bacteriophage T4 its purification and structure J Mol Biol 152 1981 641 662 (Pubitemid 12215809)
5. J.M. Valpuesta, and J.L. Carrascosa Structure of viral connectors and their function in bacteriophage assembly and DNA packaging Q Rev Biophys 27 1994 107 155 (Pubitemid 24246113)
6. P.G. Leiman, S. Kanamaru, V.V. Mesyanzhinov, F. Arisaka, and M.G. Rossmann Structure and morphogenesis of bacteriophage T4 Cell Mol Life Sci 60 2003 2356 2370 (Pubitemid 37487257)
7. V.B. Rao, and L.W. Black Structure and assembly of bacteriophage T4 head Virol J 7 2010 356
8. F.A. Eiserling, and L.W. Black Pathways in T4 morphogenesis J.D. Karam, Molecular biology of bacteriophage T4 1994 ASM Press Washington, DC
9. C.L. Hsiao, and L.W. Black Head morphogenesis of bacteriophage T4. II. The role of gene 40 in initiating prehead assembly Virology 91 1978 15 25 (Pubitemid 9065507)
10. G. Michaud, A. Zachary, V.B. Rao, and L.W. Black Membrane-associated assembly of a phage T4 DNA entrance vertex structure studied with expression vectors J Mol Biol 209 1989 667 681 (Pubitemid 20046124)
11. T.A. Quinten, and A. Kuhn Membrane interaction of the portal protein gp20 of bacteriophage T4 J Virol 86 2012 11107 11114
12. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
13. M.K. Showe, E. Isobe, and L. Onorato Bacteriophage T4 prehead proteinase. I. Purification and properties of a bacteriophage enzyme which cleaves the capsid precursor proteins J Mol Biol 107 1976 35 54
14. S. Sun, S. Gao, K. Kondabagil, Y. Xiang, M.G. Rossmann, and V.B. Rao Structure and function of the small terminase component of the DNA packaging machine in T4-like bacteriophages Proc Natl Acad Sci USA 109 2012 817 822
15. S. Hegde, V. Padilla-Sanchez, B. Draper, and V.B. Rao Portal-large terminase interactions of the bacteriophage T4 DNA packaging machine implicate a molecular lever mechanism for coupling ATPase to DNA translocation J Virol 86 2012 4046 4057
16. L. Oliveira, A. Cuervo, and P. Tavares Direct interaction of the bacteriophage SPP1 packaging ATPase with the portal protein J Biol Chem 285 2010 7366 7373
17. S. Sun, K. Kondabagil, B. Draper, T.I. Alam, V.D. Bowman, and Z. Zhang et al. The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces Cell 135 2008 1251 1262
18. G. Leffers, and V.B. Rao Biochemical characterization of an ATPase activity associated with the large packaging subunit gp17 from bacteriophage T4 J Biol Chem 275 2000 37127 37136 (Pubitemid 32002131)
19. K.R. Goetzinger, and V.B. Rao Defining the ATPase center of bacteriophage T4 DNA packaging machine: requirement for a catalytic glutamate residue in the large terminase protein gp17 J Mol Biol 331 2003 139 154 (Pubitemid 36870782)
20. V.B. Rao, and L.W. Black 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)
21. S. Sun, K. Kondabagil, P.M. Gentz, M.G. Rossmann, and V.B. Rao The structure of the ATPase that powers DNA packaging into bacteriophage T4 procapsids Mol Cell 25 2007 943 949 (Pubitemid 46436529)
22. T.I. Alam, B. Draper, K. Kondabagil, F.J. Rentas, M. Ghosh-Kumar, and S. Sun et al. The headful packaging nuclease of bacteriophage T4 Mol Microbiol 69 2008 1180 1190
23. M. Ghosh-Kumar, T.I. Alam, B. Draper, J.D. Stack, and V.B. Rao Regulation by interdomain communication of a headful packaging nuclease from bacteriophage T4 Nucleic Acids Res 39 2010 2742 2755
24. A. Fokine, Z. Zhang, S. Kanamaru, V.D. Bowman, A.A. Aksyuk, and F. Arisaka et al. The molecular architecture of the bacteriophage T4 neck J Mol Biol 425 2013 1731 1744
25. A.A. Simpson, Y. Tao, P.G. Leiman, M.O. Badasso, Y. He, and P.J. Jardine et al. Structure of the bacteriophage phi29 DNA packaging motor Nature 408 2000 745 750 (Pubitemid 32015993)
26. A.A. Lebedev, M.H. Krause, A.L. Isidro, A.A. Vagin, E.V. Orlova, and J. Turner et al. Structural framework for DNA translocation via the viral portal protein EMBO J 26 2007 1984 1994 (Pubitemid 46624054)
27. A.S. Olia, P.E. Prevelige, J.E. Johnson, and G. Cingolani Three-dimensional structure of a viral genome-delivery portal vertex Nat Struct Mol Biol 18 2011 597 603
28. Z. Zhang, V.I. Kottadiel, R. Vafabakhsh, L. Dai, Y.R. Chemla, and T. Ha et al. A promiscuous DNA packaging machine from bacteriophage T4 PLoS Biol 9 2011 e1000592
29. R.W. Hendrix Symmetry mismatch and DNA packaging in large bacteriophages Proc Natl Acad Sci USA 75 1978 4779 4783 (Pubitemid 9048617)
30. M. Oram, C. Sabanayagam, and L.W. Black Modulation of the packaging reaction of bacteriophage T4 terminase by DNA structure J Mol Biol 381 2008 61 72
31. P. Jing, F. Haque, D. Shu, C. Montemagno, and P. Guo One-way traffic of a viral motor channel for double-stranded DNA translocation Nano Lett 10 2010 3620 3627
32. H. Fang, P. Jing, F. Haque, and P. Guo Role of channel lysines and the "push through a one-way valve" mechanism of the viral DNA packaging motor Biophys J 102 2012 127 135
33. R.G. Baumann, J. Mullaney, and L.W. Black Portal fusion protein constraints on function in DNA packaging of bacteriophage T4 Mol Microbiol 61 2006 16 32
34. T. Hugel, J. Michaelis, C.L. Hetherington, P.J. Jardine, S. Grimes, and J.M. Walter et al. Experimental test of connector rotation during DNA packaging into bacteriophage phi29 capsids PLoS Biol 5 2007 e59
35. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J Mol Biol 234 1993 779 815 (Pubitemid 24007801)
36. Y. Ye, and A. Godzik Multiple flexible structure alignment using partial order graphs Bioinformatics 21 2005 2362 2369 (Pubitemid 40731591)
37. X. Agirrezabala, J. Martin-Benito, M. Valle, J.M. Gonzalez, A. Valencia, and J.M. Valpuesta et al. 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 2005 895 902 (Pubitemid 40387441)
38. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, and E.C. Meng et al. UCSF Chimera-a visualization system for exploratory research and analysis J Comput Chem 25 2004 1605 1612
39. P. Tavares, S. Zinn-Justin, and E.V. Orlova Genome gating in tailed bacteriophage capsids Adv Exp Med Biol 726 2012 585 600
40. K.R. Kondabagil, Z. Zhang, and V.B. Rao The DNA translocating ATPase of bacteriophage T4 packaging motor J Mol Biol 363 2006 786 799 (Pubitemid 44537291)
41. H. Lin, V.B. Rao, and L.W. Black Analysis of capsid portal protein and terminase functional domains: interaction sites required for DNA packaging in bacteriophage T4 J Mol Biol 289 1999 249 260 (Pubitemid 29278380)
42. A. Dixit, K. Ray, J.R. Lakowicz, and L.W. Black Dynamics of the T4 bacteriophage DNA packasome motor: endonuclease VII resolvase release of arrested Y-DNA substrates J Biol Chem 286 2011 18878 18889
43. C. Cornilleau, N. Atmane, E. Jacquet, C. Smits, J.C. Alonso, and P. Tavares et al. The nuclease domain of the SPP1 packaging motor coordinates DNA cleavage and encapsidation Nucleic Acids Res 41 2013 340 354
44. M.I. Dauden, J. Martin-Benito, J.C. Sanchez-Ferrero, M. Pulido-Cid, J.M. Valpuesta, and J.L. Carrascosa Large terminase conformational change induced by connector binding in bacteriophage T7 J Biol Chem 288 2013 16998 17007
45. M.S. Mitchell, S. Matsuzaki, S. Imai, and V.B. Rao Sequence analysis of bacteriophage T4 DNA packaging/terminase genes 16 and 17 reveals a common ATPase center in the large subunit of viral terminases Nucleic Acids Res 30 2002 4009 4021
46. M. Morita, M. Tasaka, and H. Fujisawa Structural and functional domains of the large subunit of the bacteriophage T3 DNA packaging enzyme: importance of the C-terminal region in prohead binding J Mol Biol 245 1995 635 644
47. A. Yeo, and M. Feiss Mutational analysis of the prohead binding domain of the large subunit of terminase, the bacteriophage lambda DNA packaging enzyme J Mol Biol 245 1995 126 140
48. V.I. Kottadiel, V.B. Rao, and Y.R. Chemla The dynamic pause-unpackaging state, an off-translocation recovery state of a DNA packaging motor from bacteriophage T4 Proc Natl Acad Sci USA 109 2012 20000 20005
49. A. Cuervo, M.C. Vaney, A.A. Antson, P. Tavares, and L. Oliveira Structural rearrangements between portal protein subunits are essential for viral DNA translocation J Biol Chem 282 2007 18907 18913 (Pubitemid 47100132)
50. S. Kanamaru, K. Kondabagil, M.G. Rossmann, and V.B. Rao The functional domains of bacteriophage T4 terminase J Biol Chem 279 2004 40795 40801 (Pubitemid 39287676)
51. D.N. Fuller, D.M. Raymer, V.I. Kottadiel, V.B. Rao, and D.E. Smith 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)
52. S. Grimes, S. Ma, J. Gao, R. Atz, and P.J. Jardine Role of phi29 connector channel loops in late-stage DNA packaging J Mol Biol 410 2011 50 59
53. D.E. Smith, S.J. Tans, S.B. Smith, S. Grimes, D.L. Anderson, and C. Bustamante The bacteriophage straight phi29 portal motor can package DNA against a large internal force Nature 413 2001 748 752 (Pubitemid 33009954)
54. G.C. Lander, L. Tang, S.R. Casjens, E.B. Gilcrease, P. Prevelige, and A. Poliakov et al. The structure of an infectious P22 virion shows the signal for headful DNA packaging Science 312 2006 1791 1795 (Pubitemid 43962896)
55. E.V. Orlova, P. Dube, E. Beckmann, F. Zemlin, R. Lurz, and T.A. Trautner et al. Structure of the 13-fold symmetric portal protein of bacteriophage SPP1 Nat Struct Biol 6 1999 842 846 (Pubitemid 29415176)
56. H. Zheng, A.S. Olia, M. Gonen, S. Andrews, G. Cingolani, and T. Gonen A conformational switch in bacteriophage p22 portal protein primes genome injection Mol Cell 29 2008 376 383 (Pubitemid 351215935)
57. S. Casjens, E. Wyckoff, M. Hayden, L. Sampson, K. Eppler, and S. Randall et al. Bacteriophage P22 portal protein is part of the gauge that regulates packing density of intravirion DNA J Mol Biol 224 1992 1055 1074
58. K. Ray, M. Oram, J. Ma, and L.W. Black Portal control of viral prohead expansion and DNA packaging Virology 391 2009 44 50
59. D.N. Fuller, D.M. Raymer, J.P. Rickgauer, R.M. Robertson, C.E. Catalano, and D.L. Anderson et al. 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)
60. J. Shi, T.L. Blundell, and K. Mizuguchi FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties J Mol Biol 310 2001 243 257 (Pubitemid 32619966)
61. A. Kolinski Protein modeling and structure prediction with a reduced representation Acta Biochim Pol 51 2004 349 371 (Pubitemid 38969298)
62. C. Cole, J.D. Barber, and G.J. Barton The Jpred 3 secondary structure prediction server Nucleic Acids Res 36 2008 W197 W201
63. B. Rost, G. Yachdav, and J. Liu The PredictProtein server Nucleic Acids Res 32 2004 W321 W326 (Pubitemid 39004075)
64. D.T. Jones Protein secondary structure prediction based on position-specific scoring matrices J Mol Biol 292 1999 195 202 (Pubitemid 29435759)
65. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, and E. Villa et al. Scalable molecular dynamics with NAMD J Comput Chem 26 2005 1781 1802 (Pubitemid 43078511)
66. L. Bordoli, F. Kiefer, K. Arnold, P. Benkert, J. Battey, and T. Schwede Protein structure homology modeling using SWISS-MODEL workspace Nat Protoc 4 2009 1 13
67. J. Soding, A. Biegert, and A.N. Lupas The HHpred interactive server for protein homology detection and structure prediction Nucleic Acids Res 33 2005 W244 W248 (Pubitemid 44529917)
68. G. Chopra, N. Kalisman, and M. Levitt Consistent refinement of submitted models at CASP using a knowledge-based potential Proteins 78 2010 2668 2678
69. P. Artimo, M. Jonnalagedda, K. Arnold, D. Baratin, G. Csardi, and E. de Castro et al. ExPASy: SIB bioinformatics resource portal Nucleic Acids Res 40 2012 W597 W603
70. V.B. Rao, and M.S. Mitchell The N-terminal ATPase site in the large terminase protein gp17 is critically required for DNA packaging in bacteriophage T4 J Mol Biol 314 2001 401 411 (Pubitemid 33131844)
71. R.M. Horton, H.D. Hunt, S.N. Ho, J.K. Pullen, and L.R. Pease Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension Gene 77 1989 61 68 (Pubitemid 19125654)