Structural rearrangements in the phage head-to-tail interface during assembly and infection

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 22, 2015, Pages 7009-7014

  Chaban, Yuriy ^a   Lurz, Rudi ^b   Brasilès, Sandrine ^c   Cornilleau, Charlène ^c,e   Karreman, Matthia ^a,d   Zinn Justin, Sophie ^c   Tavares, Paulo ^c   Orlova, Elena V ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^e UMR1319 MICALIS   (France)

Author keywords

Allosteric mechanism; Bacteriophage; DNA gatekeeper; Hybrid methods; Viral infection

Indexed keywords

BACTERIOPHAGE DNA; PROTEIN GP15; PROTEIN GP16; PROTEIN GP6; UNCLASSIFIED DRUG; VIRUS PROTEIN; PORTAL PROTEIN, BACTERIOPHAGE SPP1; VIRAL PROTEIN;

ARTICLE; BACTERIOPHAGE; CONTROLLED STUDY; DNA PROTEIN COMPLEX; ENTEROBACTERIA PHAGE P22; INFECTION; MOLECULAR DOCKING; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS GENOME; VIRUS PARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION; ULTRASTRUCTURE; VIRUS ENTRY;

CAUDOVIRALES; MIRIDAE; PYRONIA TITHONUS;

BACTERIOPHAGES; CRYOELECTRON MICROSCOPY; GENOME, VIRAL; MODELS, MOLECULAR; PROTEIN CONFORMATION; VIRAL PROTEINS; VIRAL TAIL PROTEINS; VIRUS ASSEMBLY; VIRUS INTERNALIZATION;

EID: 84930668333     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1504039112     Document Type: Article

References (47)

1. Bazinet C, King J (1985) The DNA translocating vertex of dsDNA bacteriophage. Annu Rev Microbiol 39:109-129.
2. Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Annu Rev Genet 42:647-681.
3. Tavares P, Zinn-Justin S, Orlova EV (2012) Genome gating in tailed bacteriophage capsids. Adv Exp Med Biol 726:585-600.
4. Orlova EV, et al. (2003) Structure of a viral DNA gatekeeper at 10 A resolution by cryoelectron microscopy. EMBO J 22(6):1255-1262.
5. Fokine A, et al. (2013) The molecular architecture of the bacteriophage T4 neck. J Mol Biol 425(10):1731-1744.
6. Veesler D, Cambillau C (2011) A common evolutionary origin for tailed-bacteriophage functional modules and bacterial machineries. Microbiol Mol Biol Rev 75(3):423-433.
7. Plisson C, et al. (2007) Structure of bacteriophage SPP1 tail reveals trigger for DNA ejection. EMBO J 26(15):3720-3728.
8. Hambly E, Suttle CA (2005) The viriosphere, diversity, and genetic exchange within phage communities. Curr Opin Microbiol 8(4):444-450.
9. Oliveira L, Tavares P, Alonso JC (2013) Headful DNA packaging: Bacteriophage SPP1 as a model system. Virus Res 173(2):247-259.
10. White HE, et al. (2012) Capsid structure and its stability at the late stages of bacteriophage SPP1 assembly. J Virol 86(12):6768-6777.
11. Lebedev AA, et al. (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J 26(7):1984-1994.
12. Oliveira L, Cuervo A, Tavares P (2010) Direct interaction of the bacteriophage SPP1 packaging ATPase with the portal protein. J Biol Chem 285(10):7366-7373.
13. Lhuillier S, et al. (2009) Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating. Proc Natl Acad Sci USA 106(21):8507-8512.
14. Chagot B, et al. (2012) Solution structure of gp17 from the Siphoviridae bacteriophage SPP1: Insights into its role in virion assembly. Proteins 80(1):319-326.
15. Auzat I, Petitpas I, Lurz R, Weise F, Tavares P (2014) A touch of glue to complete bacteriophage assembly: The tail-to-head joining protein (THJP) family. Mol Microbiol 91(6):1164-1178.
16. Auzat I, Dröge A, Weise F, Lurz R, Tavares P (2008) Origin and function of the two major tail proteins of bacteriophage SPP1. Mol Microbiol 70(3):557-569.
17. Goulet A, et al. (2011) The opening of the SPP1 bacteriophage tail, a prevalent mechanism in Gram-positive-infecting siphophages. J Biol Chem 286(28):25397-25405.
18. Vinga I, et al. (2012) Role of bacteriophage SPP1 tail spike protein gp21 on host cell receptor binding and trigger of phage DNA ejection. Mol Microbiol 83(2):289-303.
19. Langlois C, et al. (2015) Bacteriophage SPP1 tail tube protein self-assembles into β-structure-rich tubes. J Biol Chem 290(6):3836-3849.
20. Tavares P, Lurz R, Stiege A, Rückert B, Trautner TA (1996) Sequential headful packaging and fate of the cleaved DNA ends in bacteriophage SPP1. J Mol Biol 264(5):954-967.
21. Lurz R, et al. (2001) Structural organisation of the head-to-tail interface of a bacterial virus. J Mol Biol 310(5):1027-1037.
22. São-José C, et al. (2006) The ectodomain of the viral receptor YueB forms a fiber that triggers ejection of bacteriophage SPP1 DNA. J Biol Chem 281(17):11464-11470.
23. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40-49.
24. Thomas JO (1974) Chemical linkage of the tail to the right-hand end of bacteriophage lambda DNA. J Mol Biol 87(1):1-9.
25. Cuervo A, Vaney MC, Antson AA, Tavares P, Oliveira L (2007) Structural rearrangements between portal protein subunits are essential for viral DNA translocation. J Biol Chem 282(26):18907-18913.
26. Simpson AA, et al. (2000) Structure of the bacteriophage phi29 DNA packaging motor. Nature 408(6813):745-750.
27. Guasch A, et al. (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.
28. Grimes S, Ma S, Gao J, Atz R, Jardine PJ (2011) Role of ö29 connector channel loops in late-stage DNA packaging. J Mol Biol 410(1):50-59.
29. Fang H, Jing P, Haque F, Guo P (2012) Role of channel lysines and the "push through a one-way valve" mechanism of the viral DNA packaging motor. Biophys J 102(1):127-135.
30. Padilla-Sanchez V, et al. (2014) Structure-function analysis of the DNA translocating portal of the bacteriophage T4 packaging machine. J Mol Biol 426(5):1019-1038.
31. Olia AS, Prevelige PE, Jr, Johnson JE, Cingolani G (2011) Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 18(5):597-603.
32. Sun L, et al. (2014) Icosahedral bacteriophage ÖX174 forms a tail for DNA transport during infection. Nature 505(7483):432-435.
33. Isidro A, Henriques AO, Tavares P (2004) The portal protein plays essential roles at different steps of the SPP1 DNA packaging process. Virology 322(2):253-263.
34. Cardarelli L, et al. (2010) The crystal structure of bacteriophage HK97 gp6: Defining a large family of head-tail connector proteins. J Mol Biol 395(4):754-768.
35. São-José C, de Frutos M, Raspaud E, Santos MA, Tavares P (2007) Pressure built by DNA packing inside virions: Enough to drive DNA ejection in vitro, largely insufficient for delivery into the bacterial cytoplasm. J Mol Biol 374(2):346-355.
36. Petersen MTN, Jonson PH, Petersen SB (1999) Amino acid neighbours and detailed conformational analysis of cysteines in proteins. Protein Eng 12(7):535-548.
37. Kostyuchenko VA, et al. (2005) The tail structure of bacteriophage T4 and its mechanism of contraction. Nat Struct Mol Biol 12(9):810-813.
38. Riva S, Polsinelli M, Falaschi A (1968) A new phage of Bacillus subtilis with infectious DNA having separable strands. J Mol Biol 35(2):347-356.
39. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: Semiautomated software for highresolution single-particle reconstructions. JStructBiol128(1):82-97.
40. Frank J, et al. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116(1):190-199.
41. van Heel M, et al. (2000) Single-particle electron cryo-microscopy: Towards atomic resolution. Q Rev Biophys 33(4):307-369.
42. Pettersen EF, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605-1612.
43. Siebert X, Navaza J (2009) UROX 2.0: An interactive tool for fitting atomic models into electron-microscopy reconstructions. Acta Crystallogr D Biol Crystallogr 65(Pt 7):651-658.
44. Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR (2009) The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc Natl Acad Sci USA 106(11):4160-4165.
45. Mougous JD, et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312(5779):1526-1530.
46. Topf M, et al. (2008) Protein structure fitting and refinement guided by cryo-EM density. Structure 16(2):295-307.
47. DeLano WL (2002) The PyMOL Molecular Graphics System (DeLano Scientific, San Carlos, CA).