Bacteriophage SPP1 tail tube protein self-assembles into β-structure-rich tubes

Journal of Biological Chemistry

Volumn 290, Issue 6, 2015, Pages 3836-3849

  Langlois, Chantal ^a   Ramboarina, Stéphanie ^a   Cukkemane, Abhishek ^b,c   Auzat, Isabelle ^a   Chagot, Benjamin ^a   Gilquin, Bernard ^a   Ignatiou, Athanasios ^a   Petitpas, Isabelle ^d   Kasotakis, Emmanouil ^a   Paternostre, Maïté ^a   White, Helen E ^d   Orlova, Elena V ^d   Baldus, Marc ^b   Tavares, Paulo ^a   Zinn Justin, Sophie ^a  

^a CNRS   (France)

^b UTRECHT UNIVERSITY   (Netherlands)

^c Tuljaram Chaturchand College   (India)

^d UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; DRUG THERAPY; DYES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS; SELF ASSEMBLY;

ATOMIC MODELING; FOURIER TRANSFORM INFRA REDS; GLOBULAR STRUCTURE; HELICAL PARAMETERS; HEXAMERIC RINGS; PHAGE PARTICLES; SHEATH STRUCTURES; TARGET RECOGNITION;

TUBES (COMPONENTS);

GP17.1 PROTEIN; HEXAMER; MONOMER; OLIGOMER; TAIL TUBE PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ALPHA HELIX; ARTICLE; BACILLUS SUBTILIS; BACTERIOPHAGE; BETA SHEET; BETA STRAND; BIOINFORMATICS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON MICROSCOPY; INFRARED SPECTROSCOPY; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN STRUCTURE; TAIL TUBE; VIRION; AMINO ACID SEQUENCE; CHEMISTRY; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE;

BACTERIA (MICROORGANISMS); ENTEROBACTERIA PHAGE LAMBDA; MIRIDAE;

AMINO ACID SEQUENCE; BACTERIOPHAGES; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; VIRAL PROTEINS;

EID: 84922362496     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.613166     Document Type: Article

References (42)

1. Ackermann, H. W. (2007) 5500 phages examined in the electron microscope. Arch. Virol. 152, 227-243
2. Katsura, I. (1990) Mechanism of length determination in bacteriophage λ tails. Adv. Biophys. 26, 1-18
3. Veesler, D., and Cambillau, C. (2011) A common evolutionary origin for tailed-bacteriophage functional modules and bacterial machineries. Microbiol. Mol. Biol. Rev. 75, 423-433
4. King, J. (1971) Bacteriophage T4 tail assembly: four steps in core formation. J. Mol. Biol. 58, 693-709
5. Davidson, A. R., Cardarelli, L., Pell, L. G., Radford, D. R., and Maxwell, K. L. (2012) Long noncontractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 726, 115-142
6. Plisson, C, White, H. E., Auzat, I., Zafarani, A., São-José, C, Lhuillier, S., Tavares, P., and Orlova, E. V. (2007) Structure of bacteriophage SPP1 tail reveals trigger for DNA ejection. EMBOJ. 26, 3720-3728
7. Kostyuchenko, V. A., Chipman, P. R., Leiman, P. G., Arisaka, F., Mesyanzhinov, V. V., and Rossmann, M. G. (2005) The tail structure of bacteriophage T4 and its mechanism of contraction. Nat. Struct. Mol. Biol. 12, 810-813
8. Fokine, A., Zhang, Z., Kanamaru, S., Bowman, V. D., Aksyuk, A. A., Arisaka, F., Rao, V. B., and Rossmann, M. G. (2013) The molecular architecture of the bacteriophage T4 neck. J. Mol. Biol. 425, 1731-1744
9. Effantin, G., Hamasaki, R., Kawasaki, T., Bacia, M., Moriscot, C., Weissenhorn, W., Yamada, T., and Schoehn, G. (2013) Cryo-electron microscopy three-dimensional structure of the jumbo phage PhiRSL1 infecting the phytopathogen Ralstonia solanacearum. Structure 21, 298-305
10. Sassi, M., Bebeacua, C., Drancourt, M., and Cambillau, C. (2013) The first structure of a mycobacteriophage, the Mycobacterium abscessus subsp. bolletii phage Araucaria. J. Virol. 87, 8099-8109
11. Auzat, I., Dröge, A., Weise, F., Lurz, R., and Tavares, P. (2008) Origin and function of the two major tail proteins of bacteriophage SPP1. Mol. Microbiol. 70, 557-569
12. Fraser, J. S., Maxwell, K. L., and Davidson, A. R. (2007) Immunoglobulin-like domains on bacteriophage: weapons of modest damage? Curr. Opin. Microbiol. 10, 382-387
13. Haima, P., Bron, S., and Venema, G. (1987) The effect of restriction on shotgun cloning and plasmid stability in Bacillus subtilis Marburg. Mol. Gen. Genet. 209, 335-342
14. Le Grice, S. F. (1990) Regulated promoter for high-level expression of heterologous genes in Bacillus subtilis. Methods Enzymol. 185, 201-214
15. Heckman, K. L., and Pease, L. R. (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat. Protoc. 2, 924-932
16. Berjanskii, M. V., Neal, S., and Wishart, D. S. (2006) PREDATOR: a web server for predicting protein torsion angle restraints. Nucleic Acids Res. 34, W63-W69
17. Fung, B. M., Khitrin, A. K., and Ermolaev, K. (2000) An improved broadband decoupling sequence for liquid crystals and solids. J Magn. Reson. 142, 97-101
18. Gradmann, S., Ader, C., Heinrich, I., Nand, D., Dittmann, M., Cukkemane, A., van Dijk, M., Bonvin, A. M., Engelhard, M., and Baldus, M. (2012) Rapid prediction ofmulti-dimensional NMR data sets. J. Biomol. NMR 54, 377-387
19. Wang, Y., and Jardetzky, O. (2002) Probability-based protein secondary structure identification using combined NMR chemical-shift data. Protein Sci. 11, 852-861
20. Seidel, K., Lange, A., Becker, S., Hughes, C. E., Heise, H., and Baldus, M. (2004) Protein solid-state NMR resonance assignments from (13C,13C) correlation spectroscopy. Physical Chemistry Chemical Physics 6, 5090-5093
21. Baldus, M., Petkova, A. T., Herzfeld, J., and Griffin, R. G. (1998) Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems. Mol. Physics 95, 1197-1207
22. Mindell, J. A., and Grigorieff, N. (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347
23. Ludtke, S. J., Baldwin, P. R., and Chiu, W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97
24. van Heel, M. (2001) Do single (ribosome) molecules phase themselves? Cold Spring Harb. Symp. Quant. Biol. 66, 77-86
25. Stewart, M. (1988) Computer image processing of electron micrographs of biological structures with helical symmetry. J. Electron Microsc. Tech. 9, 325-358
26. Söding, J., Biegert, A., and Lupas, A. N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-W248
27. Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9, 40
28. Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., Pieper, U., and Sali, A. (2006) Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics 2006 Chapter 5, Unit 5.6
29. Veesler, D., Robin, G., Lichière, J., Auzat, I., Tavares, P., Bron, P., Campanacci, V., and 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
30. Behrens, B., Lüder, G., Behncke, M., Trautner, T. A., and Ganesan, A. T. (1979) The genome of B. subtilis phage SPP1: physical arrangement in phage genes. Mol. Gen. Genet. 175, 351-357
31. Chai, S., Bravo, A., Lüder, G., Nedlin, A., Trautner, T. A., and Alonso, J. C. (1992) Molecular analysis of the Bacillus subtilis bacteriophage SPP1 region encompassing genes 1 to 6. The products of gene 1 and gene 2 are required for pac cleavage. J. Mol. Biol. 224, 87-102
32. Sambrook, J., Fritsh, E. F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
33. Droge, A., and Tavares, P. (2000) In vitro packaging of DNA of the Bacillus subtilis bacteriophage SPP1. J. Mol. Biol. 296, 103-115
34. Isidro, A., Santos, M. A., Henriques, A. O., and Tavares, P. (2004) The high-resolution functional map of bacteriophage SPP1 portal protein. Mol. Microbiol. 51, 949-962
35. Pell, L. G., Kanelis, V., Donaldson, L. W., Howell, P. L., and Davidson, A. R. (2009) The phage λ major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc. Natl. Acad. Sci. U.S.A. 106, 4160-4165
36. Lopes, A., Tavares, P., Petit, M. A., Guérois, R., and Zinn-Justin, S. (2014) Automated identification of tailed bacteriophages and classification according to their neck organization. BMC Genomics 15, 1027-1043
37. Moran, C. P., Jr., Lang, N, LeGrice, S. F., Lee, G., Stephens, M., Sonenshein, A. L., Pero, J., and Losick, R. (1982) Nucleotide sequences that signal the initiation of transcription and translation in Bacillus subtilis. Mol. Gen. Genet. 186, 339-346
38. São-José, C, Lhuillier, S., Lurz, R., Melki, R., Lepault, J., Santos, M. A., and 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
39. Jobichen, C, Chakraborty, S., Li, M., Zheng, J., Joseph, L., Mok, Y. K., Leung, K. Y., and Sivaraman, J. (2010) Structural basis for the secretion of EvpC: a key type VI secretion system protein from Edwardsiella tarda. PLoS one 5, e12910
40. Douzi, B., Spinelli, S., Blangy, S., Roussel, A., Durand, E., Brunet, Y. R., Cascales, E., and Cambillau, C (2014) Crystal structure and self-interaction of the type VI secretion tail-tube protein from enteroaggregative Escherichia coli. PLoS One 9, e86918
41. Ballister, E. R., Lai, A. H., Zuckermann, R. N, Cheng, Y., and Mougous, J. D. (2008) In vitro self-assembly of tailorable nanotubes from a simple protein building block. Proc. Natl. Acad. Sci. U.S.A. 105, 3733-3738
42. Wishart, D. S., and Sykes, B. D. (1994) The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J. Biomol. NMR 4, 171-180