Visualizing a complete Siphoviridae member by single-particle electron microscopy: The structure of lactococcal phage TP901-1

Journal of Virology

Volumn 87, Issue 2, 2013, Pages 1061-1068

  Bebeacua, Cecilia ^a,c   Lai, Livia ^a   Vegge, Christina Skovgaard ^b   Brøndsted, Lone ^b   van Heel, Marin ^a   Veesler, David ^c,d   Cambillau, Christian ^c  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c AIX MARSEILLE UNIVERSITY   (France)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIOPHAGE; BACTERIOPHAGE TAIL; CONTROLLED STUDY; ELECTRON MICROSCOPY; EVOLUTION; IMAGE ANALYSIS; IMAGE PROCESSING; IMAGE RECONSTRUCTION; LACTOCOCCAL PHAGE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RECEPTOR BINDING; SEQUENCE ANALYSIS; STRUCTURAL BIOINFORMATICS; STRUCTURE ANALYSIS; VIRION; VIRUS ATTACHMENT; VIRUS CAPSID; VIRUS HEAD TO TAIL CONNECTING REGION; VIRUS MORPHOLOGY;

BACTERIOPHAGES; LACTOCOCCUS LACTIS; MICROSCOPY, ELECTRON; MODELS, BIOLOGICAL; MODELS, MOLECULAR; SIPHOVIRIDAE;

CAUDOVIRALES; LACTOCOCCUS LACTIS; POSIBACTERIA; SIPHOVIRIDAE;

EID: 84871999238     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02836-12     Document Type: Article

References (53)

1. Brussow H, Hendrix RW. 2002. Phage genomics: small is beautiful. Cell 108:13-16.
2. Kostyuchenko VA, Leiman PG, Chipman PR, Kanamaru S, van Raaij MJ, Arisaka F, Mesyanzhinov VV, Rossmann MG. 2003. Threedimensional structure of bacteriophage T4 baseplate. Nat. Struct. Biol. 10:688-693.
3. Lander GC, Khayat R, Li R, Prevelige PE, Potter CS, Carragher B, Johnson JE. 2009. The P22 tail machine at subnanometer resolution reveals the architecture of an infection conduit. Structure 17:789-799.
4. Lander GC, Tang L, Casjens SR, Gilcrease EB, Prevelige P, Poliakov A, Potter CS, Carragher B, Johnson JE. 2006. The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312: 1791-1795.
5. Plisson C, White HE, Auzat I, Zafarani A, Sao-Jose C, Lhuillier S, Tavares P, Orlova EV. 2007. Structure of bacteriophage SPP1 tail reveals trigger for DNA ejection. EMBO J. 26:3720-3728.
6. Bebeacua C, Bron P, Lai L, Vegge CS, Brondsted L, Spinelli S, Campanacci V, Veesler D, van Heel M, Cambillau C. 2010. Structure and molecular assignment of lactococcal phage TP901-1 baseplate. J. Biol. Chem. 285:39079-39086.
7. Campanacci V, Veesler D, Lichière J, Blangy S, Sciara G, Moineau S, van Sinderen D, Bron P, Cambillau C. 2010. Solution and electronmicroscopy characterization of lactococcal phage baseplates expressed in Escherichia coli. J. Struct. Biol. 172:75-84.
8. Sciara G, Bebeacua C, Bron P, Tremblay D, Ortiz-Lombardia M, Lichiere J, van Heel M, Campanacci V, Moineau S, Cambillau C. 2010. Structure of lactococcal phage p2 baseplate and its mechanism of activation. Proc. Natl. Acad. Sci. U. S. A. 107:6852-6857.
9. Shepherd DA, Veesler D, Lichiere J, Ashcroft AE, Cambillau C. 2011. Unraveling lactococcal phage baseplate assembly by mass spectrometry. Mol. Cell. Proteomics 10:M111.009787. doi:10.1074/ mcp.M111.009787.
10. Spinelli S, Desmyter A, Verrips CT, de Haard HJ, Moineau S, Cambillau C. 2006. Lactococcal bacteriophage p2 receptor-binding protein structure suggests a common ancestor gene with bacterial and mammalian viruses. Nat. Struct. Mol. Biol. 13:85-89.
11. Veesler D, Spinelli S, Mahony J, Lichiere J, Blangy S, Bricogne G, Legrand P, Ortiz-Lombardia M, Campanacci V, van Sinderen D, Cambillau C. 2012. Structure of the phage TP901-1 1.8MDa baseplate suggests an alternative host adhesion mechanism. Proc. Natl. Acad. Sci. U. S. A. 109:8954-8958.
12. Lhuillier S, Gallopin M, Gilquin B, Brasiles S, Lancelot N, Letellier G, Gilles M, Dethan G, Orlova EV, Couprie J, Tavares P, Zinn-Justin S. 2009. Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating. Proc. Natl. Acad. Sci. U. S. A. 106:8507-8512.
13. Vegge CS, Brondsted L, Neve H, McGrath S, van Sinderen D, Vogensen FK. 2005. Structural characterization and assembly of the distal tail structure of the temperate lactococcal bacteriophage TP901-1. J. Bacteriol. 187: 4187-4197.
14. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M. 1996. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116: 17-24.
15. Dube P, Tavares P, Lurz R, van Heel M. 1993. The portal protein of bacteriophage SPP1: a DNA pump with 13-fold symmetry. EMBO J. 12: 1303-1309.
16. van Heel M. 1984. Multivariate statistical classification of noisy images (randomly oriented biological macromolecules). Ultramicroscopy 13: 165-183.
17. Harauz G, Ottensmeyer FP. 1983. Interpolation in computing forward projections in direct three-dimensional reconstruction. Phys. Med. Biol. 28:1419-1427.
18. Egelman EH. 2007. The iterative helical real space reconstruction method: surmounting the problems posed by real polymers. J. Struct. Biol. 157:83-94.
19. Owen CH, Morgan DG, DeRosier DJ. 1996. Image analysis of helical objects: the Brandeis Helical Package. J. Struct. Biol. 116:167-175.
20. Metlagel Z, Kikkawa YS, Kikkawa M. 2007. Ruby-Helix: an implementation of helical image processing based on object-oriented scripting language. J. Struct. Biol. 157:95-105.
21. van Heel M, Schatz M. 2005. Fourier shell correlation threshold criteria. J. Struct. Biol. 151:250-262.
22. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
23. Veesler D, Johnson JE. 2012. Virus maturation. Annu. Rev. Biophys. 41:473-496.
24. Veesler D, Cambillau C. 2011. A common evolutionary origin for tailedbacteriophage functional modules and bacterial machineries. Microbiol. Mol. Biol. Rev. 75:423-433.
25. Wikoff WR, Liljas L, Duda RL, Tsuruta H, Hendrix RW, Johnson JE. 2000. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289:2129-2133.
26. Jaroszewski L, Li Z, Cai XH, Weber C, Godzik A. 2011. FFAS server: novel features and applications. Nucleic Acids Res. 39:W38-W44.
27. Lebedev AA, Krause MH, Isidro AL, Vagin AA, Orlova EV, Turner J, Dodson EJ, Tavares P, Antson AA. 2007. Structural framework for DNA translocation via the viral portal protein. EMBO J. 26:1984-1994.
28. Olia AS, Prevelige PE, Johnson JE, Cingolani G. 2011. Threedimensional structure of a viral genome-delivery portal vertex. Nat. Struct. Mol. Biol. 18:597-603.
29. Tang J, Lander GC, Olia AS, Li R, Casjens S, Prevelige P, Jr, Cingolani G, Baker TS, Johnson JE. 2011. Peering down the barrel of a bacteriophage portal: the genome packaging and release valve in p22. Structure 19:496-502.
30. Goulet A, Lai-Kee-Him J, Veesler D, Auzat I, Robin G, Shepherd DA, Ashcroft AE, Richard E, Lichiere J, Tavares P, Cambillau C, Bron P. 2011. The opening of the SPP1 bacteriophage tail, a prevalent mechanism in Gram-positive-infecting siphophages. J. Biol. Chem. 286:25397-25405.
31. Veesler D, Robin G, Lichiere J, Auzat I, Tavares P, Bron P, Campanacci V, Cambillau C. 2010. Crystal structure of bacteriophage SPP1 distal tail protein (gp19.1): a baseplate hub paradigm in Gram-positive infecting phages. J. Biol. Chem. 285:36666-36673.
32. Pedersen M, Ostergaard S, Bresciani J, Vogensen FK. 2000. Mutational analysis of two structural genes of the temperate lactococcal bacteriophage TP901-1 involved in tail length determination and baseplate assembly. Virology 276:315-328.
33. Chapot-Chartier MP, Vinogradov E, Sadovskaya I, Andre G, Mistou MY, Trieu-Cuot P, Furlan S, Bidnenko E, Courtin P, Pechoux C, Hols P, Dufrene YF, Kulakauskas S. 2010. Cell surface of Lactococcus lactis is covered by a protective polysaccharide pellicle. J. Biol. Chem. 285:10464-10471.
34. Kenny JG, McGrath S, Fitzgerald GF, van Sinderen D. 2004. Bacteriophage Tuc2009 encodes a tail-associated cell wall-degrading activity. J. Bacteriol. 186:3480-3491.
35. Greene B, King J. 1994. Binding of scaffolding subunits within the P22 procapsid lattice. Virology 205:188-197.
36. Johnsen MG, Neve H, Vogensen FK, Hammer K. 1995. Virion positions and relationships of lactococcal temperate bacteriophage TP901-1 proteins. Virology 212:595-606.
37. Sao-Jose 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. 374:346-355.
38. Letellier L, Boulanger P, Plancon L, Jacquot P, Santamaria M. 2004. Main features on tailed phage, host recognition and DNA uptake. Front. Biosci. 9:1228-1339.
39. Molineux IJ. 2001. No syringes please, ejection of phage T7DNAfrom the virion is enzyme driven. Mol. Microbiol. 40:1-8.
40. Ricagno S, Campanacci V, Blangy S, Spinelli S, Tremblay D, Moineau S, Tegoni M, Cambillau C. 2006. Crystal structure of the receptorbinding protein head domain from Lactococcus lactis phage bIL170. J. Virol. 80:9331-9335.
41. Spinelli S, Campanacci V, Blangy S, Moineau S, Tegoni M, Cambillau C. 2006. Modular structure of the receptor binding proteins of Lactococcus lactis phages. The RBP structure of the temperate phage TP901-1. J. Biol. Chem. 281:14256-14262.
42. Tremblay DM, Tegoni M, Spinelli S, Campanacci V, Blangy S, Huyghe C, Desmyter A, Labrie S, Moineau S, Cambillau C. 2006. Receptorbinding protein of Lactococcus lactis phages: identification and characterization of the saccharide receptor-binding site. J. Bacteriol. 188:2400-2410.
43. Baptista C, Santos MA, Sao-Jose C. 2008. Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB. J. Bacteriol. 190:4989-4996.
44. Geller BL, Ivey RG, Trempy JE, Hettinger-Smith B. 1993. Cloning of a chromosomal gene required for phage infection of Lactococcus lactis subsp. lactis C2. J. Bacteriol. 175:5510-5519.
45. Monteville MR, Ardestani B, Geller BL. 1994. Lactococcal bacteriophages require a host cell wall carbohydrate and a plasma membrane protein for adsorption and ejection of DNA. Appl. Environ. Microbiol. 60: 3204-3211.
46. Sao-Jose C, Baptista C, Santos MA. 2004. Bacillus subtilis operon encoding a membrane receptor for bacteriophage SPP1. J. Bacteriol. 186:8337-8346.
47. Sao-Jose C, Lhuillier S, Lurz R, Melki R, Lepault J, Santos MA, Tavares P. 2006. The ectodomain of the viral receptor YueB forms a fiber that triggers ejection of bacteriophage SPP1 DNA. J. Biol. Chem. 281:11464-11470.
48. Valyasevi R, Sandine WE, Geller BL. 1991. A membrane protein is required for bacteriophage c2 infection of Lactococcus lactis subsp. lactis C2. J. Bacteriol. 173:6095-6100.
49. Vinga I, Baptista C, Auzat I, Petipas I, Lurz R, Tavares P, Santos MA, Sao-Jose C. 2012. Role of bacteriophage SPP1 tail spike protein gp21 on host cell receptor binding and trigger of phage DNA ejection. Mol. Microbiol. 83:289-303.
50. Lortat-Jacob H, Chouin E, Cusack S, van Raaij MJ. 2001. Kinetic analysis of adenovirus fiber binding to its receptor reveals an avidity mechanism for trimeric receptor-ligand interactions. J. Biol. Chem. 276:9009-9015.
51. Veesler D, Dreier B, Blangy S, Lichiere J, Tremblay D, Moineau S, Spinelli S, Tegoni M, Pluckthun A, Campanacci V, Cambillau C. 2009. Crystal structure and function of a DARPin neutralizing inhibitor of lactococcal phage TP901-1: comparison of DARPin and camelid VHH binding mode. J. Biol. Chem. 284:30718-30726.
52. Plancon L, Janmot C, le Maire M, Desmadril M, Bonhivers M, Letellier L, Boulanger P. 2002. Characterization of a high-affinity complex between the bacterial outer membrane protein FhuA and the phage T5 protein pb5. J. Mol. Biol. 318:557-569.
53. Berkane E, Orlik F, Stegmeier JF, Charbit A, Winterhalter M, Benz R. 2006. Interaction of bacteriophage lambda with its cell surface receptor: an in vitro study of binding of the viral tail protein gpJ to LamB (Maltoporin). Biochemistry 45:2708-2720.