Structure and function of the small terminase component of the DNA packaging machine in T4-like bacteriophages

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

Volumn 109, Issue 3, 2012, Pages 817-822

  Suna, Siyang ^a   Gao, Song ^b   Kondabagil, Kiran ^b,c   Xiang, Ye ^a   Rossmann, Michael G ^a   Rao, Venigalla B ^b  

^a PURDUE UNIVERSITY   (United States)

^b CATHOLIC UNIVERSITY OF AMERICA   (United States)

^c INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

Author keywords

T4 like phages; X ray crystal structure

Indexed keywords

BACTERIOPHAGE DNA; MONOMER;

AEROMONAS SALMONICIDA; ARTICLE; BACTERIOPHAGE T4; CONFORMATION; CRYSTALLIZATION; DNA BINDING; DNA PACKAGING; GENE TRANSLOCATION; MOLECULAR MODEL; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; VIRUS GENOME; X RAY DIFFRACTION;

BACTERIOPHAGE T4; DNA PACKAGING; ENDODEOXYRIBONUCLEASES; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL PROTEINS;

EID: 84856402988     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1110224109     Document Type: Article

References (51)

1. Sun S, Rao VB, Rossmann MG (2010) Genome packaging in viruses. Curr Opin Struct Biol 20:114-120.
2. Newcomb WW, Homa FL, Brown JC (2005) Involvement of the portal at an early step in herpes simplex virus capsid assembly. J Virol 79:10540-10546. (Pubitemid 41098593)
3. Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Annu Rev Genet 42:647-681.
4. Smith DE, et al. (2001) The bacteriophage φ29 portal motor can package DNA against a large internal force. Nature 413:748-752. (Pubitemid 33009954)
5. Chemla YR, et al. (2005) Mechanism of force generation of a viral DNA packaging motor. Cell 122:683-692. (Pubitemid 41242634)
6. Fuller DN, Raymer DM, Kottadiel V, Rao VB, Smith DE (2007) Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proc Natl Acad Sci USA 104:16868-16873. (Pubitemid 350210957)
7. Casjens SR (2011) The DNA-packaging nanomotor of tailed bacteriophages. Nat Rev Microbiol 9:647-657.
8. Simpson AA, et al. (2000) Structure of the bacteriophage φ29 DNA packaging motor. Nature 408:745-750. (Pubitemid 32015993)
9. Lebedev AA, et al. (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J 26:1984-1994. (Pubitemid 46624054)
10. 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.
11. Orlova EV, et al. (2003) Structure of a viral DNA gatekeeper at 10 Å resolution by cryo-electron microscopy. EMBO J 22:1255-1262. (Pubitemid 36362689)
12. Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG (2004) Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118:419-429. (Pubitemid 39485662)
13. Chang J, Weigele P, King J, Chiu W, Jiang W (2006) Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 14:1073-1082. (Pubitemid 43831665)
14. Lander GC, et al. (2006) The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312:1791-1795. (Pubitemid 43962896)
15. Jiang W, et al. (2006) Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439:612-616. (Pubitemid 43185387)
16. Morais MC, et al. (2008) Defining molecular and domain boundaries in the bacteriophage φ29 DNA packaging motor. Structure 16:1267-1274.
17. Xiang Y, et al. (2006) Structural changes of bacteriophage φ29 upon DNA packaging and release. EMBO J 25:5229-5239. (Pubitemid 44658539)
18. Casjens S, et al. (1992) Bacteriophage P22 portal protein is part of the gauge that regulates packing density of intravirion DNA. J Mol Biol 224:1055-1074.
19. Tavares P, et al. (1992) Identification of a gene in Bacillus subtilis bacteriophage SPP1 determining the amount of packaged DNA. J Mol Biol 225:81-92.
20. Kanamaru S, Kondabagil K, Rossmann MG, Rao VB (2004) The functional domains of bacteriophage T4 terminase. J Biol Chem 279:40795-40801. (Pubitemid 39287676)
21. Sun S, et al. (2008) The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell 135:1251-1262.
22. Sun S, Kondabagil K, Gentz PM, Rossmann MG, Rao VB (2007) The structure of the ATPase that powers DNA packaging into bacteriophage T4 procapsids. Mol Cell 25:943-949. (Pubitemid 46436529)
23. Catalano CE, Cue D, Feiss M (1995) Virus DNA packaging: The strategy used by phage l. Mol Microbiol 16:1075-1086.
24. Chai S, Lurz R, Alonso JC (1995) The small subunit of the terminase enzyme of Bacillus subtilis bacteriophage SPP1 forms a specialized nucleoprotein complex with the packaging initiation region. J Mol Biol 252:386-398.
25. Rao VB, Black LW (2005) DNA packaging in bacteriophage T4. Viral Genome Packaging: Genetics, Structure, and Mechanism, ed CE Catalano (Kluwer Academic/Plenum, Boston), pp 40-58.
26. Lin H, Simon MN, Black LW (1997) Purification and characterization of the small subunit of phage T4 terminase, gp16, required for DNA packaging. J Biol Chem 272:3495-3501. (Pubitemid 27066850)
27. Rao VB, Black LW (1988) Cloning, overexpression and purification of the terminase proteins gp16 and gp17 of bacteriophage T4: Construction of a defined in-vitro DNA packaging system using purified terminase proteins. J Mol Biol 200:475-488.
28. Hamada K, Fujisawa H, Minagawa T (1986) A defined in vitro system for packaging of bacteriophage T3 DNA. Virology 151:119-123. (Pubitemid 16111050)
29. Rubinchik S, Parris W, Gold M (1995) The in vitro translocase activity of l terminase and its subunits: Kinetic and biochemical analysis. J Biol Chem 270:20059-20066.
30. Kondabagil KR, Zhang Z, Rao VB (2006) The DNA translocating ATPase of bacteriophage T4 packaging motor. J Mol Biol 363:786-799. (Pubitemid 44537291)
31. Black LW, Peng G (2006) Mechanistic coupling of bacteriophage T4 DNA packaging to components of the replication-dependent late transcription machinery. J Biol Chem 281:25635-25643. (Pubitemid 44401952)
32. Al-Zahrani AS, et al. (2009) The small terminase, gp16, of bacteriophage T4 is a regulator of the DNA packaging motor. J Biol Chem 284:24490-24500.
33. Gao S, Rao VB (2011) Specificity of interactions among the DNA packaging machine components of T4 related bacteriophages. J Biol Chem 286:3944-3956.
34. de Beer T, et al. (2002) Insights into specific DNA recognition during the assembly of a viral genome packaging machine. Mol Cell 9:981-991.
35. Brennan RG, Matthews BW (1989) The helix-turn-helix DNA binding motif. J Biol Chem 264:1903-1906. (Pubitemid 19057656)
36. Zhao H, et al. (2010) Crystal structure of the DNA-recognition component of the bacterial virus Sf6 genome-packaging machine. Proc Natl Acad Sci USA 107:1971-1976.
37. Büttner CR, et al. (2011) Structural basis for DNA recognition and loading into a viral packaging motor. Proc Natl Acad Sci USA, doi: 10.1073/pnas.1110270109.
38. Kondabagil KR, Rao VB (2006) A critical coiled coil motif in the small terminase, gp16, from bacteriophage T4: insights into DNA packaging initiation and assembly of packaging motor. J Mol Biol 358:67-82.
39. Karam JD, Miller ES (2010) Bacteriophage T4 and its relatives. Virol J 7:293-296.
40. Kim DE, Chivian D, Baker D (2004) Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 32(suppl 2):W526-W531. (Pubitemid 38997389)
41. Leffers G, Rao VB (2000) Biochemical characterization of an ATPase activity associated with the large packaging subunit gp17 from bacteriophage T4. J Biol Chem 275:37127-37136. (Pubitemid 32002131)
42. Ghosh-Kumar M, Alam TI, Draper B, Stack J, Rao VB (2011) Regulation by interdomain communication of a headful packaging nuclease from bacteriophage T4. Nucleic Acids Res 39:2742-2755.
43. Nemecek D, Lander GC, Johnson JE, Casjens SR, Thomas GJ, Jr (2008) Assembly architecture and DNA binding of the bacteriophage P22 terminase small subunit. J Mol Biol 383:494-501.
44. Nemecek D, et al. (2007) Subunit conformations and assembly states of a DNA-translocating motor: The terminase of bacteriophage P22. J Mol Biol 374:817-836. (Pubitemid 350018767)
45. Frackman S, Siegele DA, Feiss M (1985) The terminase of bacteriophage l. Functional domains for cosB binding and multimer assembly. J Mol Biol 183:225-238.
46. van Duijn E (2010) Current limitations in native mass spectrometry based structural biology. J Am Soc Mass Spectrom 21:971-978.
47. Sternberg N, Coulby J (1987) Recognition and cleavage of the bacteriophage P1 packaging site (pac). I. Differential processing of the cleaved ends in vivo. J Mol Biol 194:453-468.
48. Ortega ME, Catalano CE (2006) Bacteriophage lambda gpNu1 and Escherichia coli IHF proteins cooperatively bind and bend viral DNA: Implications for the assembly of a genome-packaging motor. Biochemistry 45:5180-5189.
49. Baumann RG, Black LW (2003) Isolation and characterization of T4 bacteriophage gp17 terminase, a large subunit multimer with enhanced ATPase activity. J Biol Chem 278:4618-4627. (Pubitemid 36800960)
50. Granboulan P, Sechaud J, Kellenberger E (1971) On the fragility of phage T4-related particles. Virology 46:407-425.
51. Pettersen EF, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612.