Structural investigations of a Podoviridae streptococcus phage C1, implicationsfor the mechanism of viral entry

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

Volumn 109, Issue 35, 2012, Pages 14025-14026

  Aksyuk, Anastasia A ^a   Bowman, Valorie D ^a   Kaufmann, Bärbel ^a   Fields, Christopher ^b   Klose, Thomas ^a   Holdaway, Heather A ^a,c   Fischetti, Vincent A ^b   Rossmann, Michael G ^a  

^a PURDUE UNIVERSITY   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Bacteriophage C1 tail; Tail knob; X ray crystallography

Indexed keywords

CAPSID PROTEIN; PEPTIDASE; STRUCTURAL PROTEIN; VIRUS PROTEIN;

ARTICLE; BACTERIOPHAGE; CELL WALL; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DNA PACKAGING; ENZYME ACTIVITY; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; STREPTOCOCCUS PHAGE; VIRUS CAPSID; VIRUS ENTRY; VIRUS GENE; VIRUS MORPHOLOGY; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; STREPTOCOCCUS; ULTRASTRUCTURE; VIROLOGY; VIRUS REPLICATION; X RAY CRYSTALLOGRAPHY;

MIRIDAE; MYOVIRIDAE; PODOVIRIDAE; SIPHOVIRIDAE; STREPTOCOCCUS;

CAPSID; CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; MYOVIRIDAE; PODOVIRIDAE; PROTEIN STRUCTURE, TERTIARY; STREPTOCOCCUS; STREPTOCOCCUS PHAGES; VIRAL STRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84865535036     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1207730109     Document Type: Article

References (60)

1. Clark PF, Clark AS (1926) A "bacteriophage" active against a hemolytic streptococcus. J Bacteriol 11:89.
2. Evans AC (1934) Streptococcus bacteriophage: A study of four serological types. Public Health Rep 49:1386-1401.
3. Diaz E, Lopez R, Garcia JL (1990) Chimeric phage-bacterial enzymes: A clue to the modular evolution of genes. Proc Natl Acad Sci USA 87:8125-8129.
4. Loeffler JM, Nelson D, Fischetti VA (2001) Rapid killing of Streptococcus pneumoniae with a bacteriophage cell wall hydrolase. Science 294:2170-2172. (Pubitemid 33150674)
5. Schuch R, Nelson D, Fischetti VA (2002) A bacteriolytic agent that detects and kills Bacillus anthracis. Nature 418:884-889. (Pubitemid 34966308)
6. Köller T, et al. (2008) PlyC, a novel bacteriophage lysin for compartment-dependent proteomics of group A streptococci. Proteomics 8:140-148.
7. Nelson D, Schuch R, Zhu S, Tscherne DM, Fischetti VA (2003) Genomic sequence of C1, the first streptococcal phage. J Bacteriol 185:3325-3332. (Pubitemid 36617744)
8. Nelson D, Schuch R, Chahales P, Zhu S, Fischetti VA (2006) PlyC: A multimeric bacteriophage lysin. Proc Natl Acad Sci USA 103:10765-10770. (Pubitemid 44078050)
9. Fischetti VA (2010) Bacteriophage endolysins: A novel anti-infective to control Gram-positive pathogens. Int J Med Microbiol 300:357-362.
10. Vybiral D, et al. (2003) Complete nucleotide sequence and molecular characterization of two lytic Staphylococcus aureus phages: 44AHJD and P68. FEMS Microbiol Lett 219:275-283. (Pubitemid 36302609)
11. Meijer WJ, Horcajadas JA, Salas M (2001) Phi29 family of phages. Microbiol Mol Biol Rev 65:261-287.
12. Jiang W, et al. (2003) Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat Struct Biol 10:131-135. (Pubitemid 36177094)
13. Fokine A, et al. (2005) Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry. Proc Natl Acad Sci USA 102:7163-7168. (Pubitemid 40696351)
14. Morais MC, et al. (2005) Conservation of the capsid structure in tailed dsDNA bacteriophages: The pseudoatomic structure of φ29. Mol Cell 18:149-159.
15. Baker ML, Jiang W, Rixon FJ, Chiu W (2005) Common ancestry of herpesviruses and tailed DNA bacteriophages. J Virol 79:14967-14970. (Pubitemid 41636294)
16. Leiman PG, et al. (2007) The structures of bacteriophages K1E and K1-5 explain processive degradation of polysaccharide capsules and evolution of new host specificities. J Mol Biol 371:836-849. (Pubitemid 47087828)
17. Dai W, et al. (2010) Three-dimensional structure of tropism-switching Bordetella bacteriophage. Proc Natl Acad Sci USA 107:4347-4352.
18. Liu X, et al. (2010) Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat Struct Mol Biol 17:830-836.
19. Cardarelli L, et al. (2010) Phages have adapted the same protein fold to fulfill multiple functions in virion assembly. Proc Natl Acad Sci USA 107:14384-14389.
20. Altschul SF, et al. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25:3389-3402. (Pubitemid 27359211)
21. Biegert A, Mayer C, Remmert M, Soding J, Lupas AN (2006) The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic Acids Res 34:W335-W339. (Pubitemid 44529789)
22. McDonnell AV, Jiang T, Keating AE, Berger B (2006) Paircoil2: Improved prediction of coiled coils from sequence. Bioinformatics 22:356-358. (Pubitemid 43205384)
23. Soding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951-960.
24. Aksyuk AA, et al. (2011) Structural conservation of the Myoviridae phage tail sheath protein fold. Structure 19:1885-1894.
25. Browning C, Shneider MM, Bowman VD, Schwarzer D, Leiman PG (2012) Phage pierces the host cell membrane with the iron-loaded spike. Structure 20:326-339.
26. Agirrezabala X, et al. (2005) Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J 24:3820-3829. (Pubitemid 41581697)
27. Wikoff WR, et al. (2000) Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289:2129-2133.
28. Jiang W, et al. (2006) Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439:612-616. (Pubitemid 43185387)
29. Choi KH, et al. (2008) Insight into DNA and protein transport in double-stranded DNA viruses: The structure of bacteriophage N4. J Mol Biol 378:726-736.
30. Tao Y, et al. (1998) Assembly of a tailed bacterial virus and its genome release studied in three dimensions. Cell 95:431-437. (Pubitemid 28507330)
31. Choi KH, Morais MC, Anderson DL, Rossmann MG (2006) Determinants of bacteriophage φ29 head morphology. Structure 14:1723-1727.
32. Dokland T, Wang S, Lindqvist BH (2002) The structure of P4 procapsids produced by coexpression of capsid and external scaffolding proteins. Virology 298:224-231. (Pubitemid 35034539)
33. Marvik OJ, et al. (1995) The capsid size-determining protein Sid forms an external scaffold on phage P4 procapsids. J Mol Biol 251:59-75.
34. Fu X, Walter MH, Paredes A, Morais MC, Liu J (2011) The mechanism of DNA ejection in the Bacillus anthracis spore-binding phage 8a revealed by cryo-electron tomography. Virology 421:141-148.
35. Rossmann MG, Bernal R, Pletnev SV (2001) Combining electron microscopic with X-ray crystallographic structures. J Struct Biol 136:190-200.
36. Chen DH, et al. (2011) Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus. Proc Natl Acad Sci USA 108:1355-1360.
37. Duda RL, et al. (1995) Structural transitions during bacteriophage KH97 head assembly. J Mol Biol 247:618-635.
38. Morais MC, et al. (2001) Cryoelectron-microscopy image reconsruction of symmetry mismatches in bacteriophage φ29. J Struct Biol 135:38-46.
39. Xiang Y, et al. (2006) Structural changes of bacteriophage φ29 upon DNA packaging and release. EMBO J 25:5229-5239. (Pubitemid 44658539)
40. Tang J, Sinkovits RS, Baker TS (2010) Three-dimensional asymmetric reconstruction of tailed bacteriophage. Methods Enzymol 482:185-210.
41. Simpson AA, et al. (2000) Structure of the bacteriophage φ29 DNA packaging motor. Nature 408:745-750. (Pubitemid 32015993)
42. Olia AS, Prevelige PE, Jr, Johnson JE, Cingolani G (2011) Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 18:597-603.
43. Tang J, et al. (2011) Peering down the barrel of a bacteriophage portal: The genome packaging and release valve in P22. Structure 19:496-502.
44. Xiang Y, et al. (2008) Crystal and cryoEM structural studies of a cell wall degrading enzyme in the bacteriophage φ29 tail. Proc Natl Acad Sci USA 105:9552-9557. (Pubitemid 352031339)
45. Xiang Y, et al. (2009) Crystallographic insights into the autocatalytic assembly mechanism of a bacteriophage tail spike. Mol Cell 34:375-386.
46. Steinbacher S, et al. (1994) Crystal structure of P22 tailspike protein: Interdigitated subunits in a thermostable trimer. Science 265:383-386. (Pubitemid 24259969)
47. Holm L, Park J (2000) DaliLite workbench for protein structure comparison. Bioinformatics 16:566-567.
48. Kanamaru S, et al. (2002) Structure of the cell-puncturing device of bacteriophage T4. Nature 415:553-557. (Pubitemid 34130613)
49. Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR (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 USA 106:4160-4165.
50. Pell LG, et al. (2009) The X-ray crystal structure of the phage λ tail terminator protein reveals the biologically relevant hexameric ring structure and demonstrates a conserved mechanism of tail termination among diverse long-tailed phages. J Mol Biol 389:938-951.
51. Maxwell KL, Yee AA, Arrowsmith CH, Gold M, Davidson AR (2002) The solution structure of the bacteriophage λ head-tail joining protein, gpFII. J Mol Biol 318:1395-1404. (Pubitemid 34754006)
52. Leiman PG, et al. (2010) Morphogenesis of the T4 tail and tail fibers. Virol J 7:355, Available at http://www.virologyj.com/content/7/1/355.
53. Bertin A, de Frutos M, Letellier L (2011) Bacteriophage-host interactions leading to genome internalization. Curr Opin Microbiol 14:492-496.
54. Lhuillier S, et al. (2009) Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating. Proc Natl Acad Sci USA 106:8507-8512.
55. Plisson C, et al. (2007) Structure of bacteriophage SPP1 tails reveals trigger for DNA ejection. EMBO J 26:3720-3728. (Pubitemid 47236871)
56. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: Semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128:82-97. (Pubitemid 30013436)
57. Frank J, et al. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116:190-199. (Pubitemid 26093143)
58. Kleywegt GJ, Zou JY, Kjeldgaard M, Jones TA (2001) Around O. International Tables for Crystallograhy, Vol F, Crystallography of Biological Macromolecules, eds MG Rossmann and E Arnold (Kluwer Academic Publishers, Dordrecht/Boston/London), pp 353-356-366-367.
59. Pettersen EF, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Computat Chem 25:1605-1612.
60. Pintilie GD, Zhang J, Goddard TD, Chiu W, Gossard DC (2010) Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions. J Struct Biol 170:427-438.