The nuclease domain of the SPP1 packaging motor coordinates DNA cleavage and encapsidation

Nucleic Acids Research

Volumn 41, Issue 1, 2013, Pages 340-354

  Cornilleau, Charlène ^a   Atmane, Noureddine ^a   Jacquet, Eric ^b   Smits, Callum ^c,e   Alonso, Juan C ^d   Tavares, Paulo ^a   Oliveira, Leonor ^a  

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

^b INSTITUT DE CHIMIE DES SUBSTANCES NATURELLES   (France)

^c UNIVERSITY OF YORK   (United Kingdom)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^e VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CARBOXY TERMINAL TELOPEPTIDE; MANGANESE; NUCLEASE; NUCLEASE GP2; OSTEOPONTIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIOPHAGE; CONTROLLED STUDY; DNA CLEAVAGE; DNA PACKAGING; ENZYME ACTIVITY; GENE MUTATION; GENE TRANSLOCATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; TRANSCRIPTION INITIATION SITE;

ADENOSINE TRIPHOSPHATASES; BACILLUS PHAGES; CAPSID; CATALYTIC DOMAIN; CATIONS, DIVALENT; DNA CLEAVAGE; DNA PACKAGING; ENDODEOXYRIBONUCLEASES; MANGANESE; METALS; MUTATION; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; VIRAL PROTEINS;

HERPESVIRIDAE;

EID: 84871763061     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks974     Document Type: Article

References (52)

1. Casjens, S. and Hendrix, R. (1988) Control mechanisms in dsDNA bacteriophage assembly. In: Calendar, R. (ed.), The Bacteriophages, Vol. 1. Plenum Press, New York, pp. 15-91.
2. Black, L.W. (1989) DNA packaging in dsDNA bacteriophages. Annu. Rev. Microbiol., 43, 267-292.
3. Lo Piano, A., Martinez-Jimenez, M., Zecchi, L. and Ayora, S. (2011) Recombination-dependent concatemeric viral DNA replication. Virus Res., 160, 1-14.
4. Rao, V.B. and Feiss, M. (2008) The bacteriophage DNA packaging motor. Ann. Rev. Genet., 42, 19.1-19.35.
5. Adams, M., Hayden, M. and Casjens, S. (1983) On the sequential packaging of bacteriophage P22 DNA. J. Virol., 46, 673-677.
6. Tavares, P., Lurz, R., Stiege, A., Ruckert, B. and Trautner, T.A. (1996) Sequential headful packaging and fate of the cleaved DNA ends in bacteriophage SPP1. J. Mol. Biol., 264, 954-967.
7. Tavares, P., Zinn-Justin, S. and Orlova, E.V. (2012) Genome gating in tailed bacteriophage capsids. Adv. Exp. Med. Biol., 726, 585-600.
8. Sun, S., Kondabagil, K., Draper, B., Alam, T.I., Bowman, V.D., Zhang, Z., Hegde, S., Fokine, A., Rossmann, M.G. and Rao, V.B. (2008) The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell, 135, 1251-1262.
9. Smits, C., Chechik, M., Kovalevskiy, O.V., Shevtsov, M.B., Foster, A.W., Alonso, J.C. and Antson, A.A. (2009) Structural basis for the nuclease activity of a bacteriophage large terminase. EMBO Reports, 10, 592-598.
10. Roy, A. and Cingolani, G. (2012) Structure of P22 headful packaging nuclease. J. Biol. Chem., 287, 28196-28205.
11. Nadal, M., Mas, P.J., Blanco, A.G., Arnan, C., Sola, M., Hart, D.J. and Coll, M. (2010) Structure and inhibition of herpesvirus DNA packaging terminase nuclease domain. Proc. Natl Acad. Sci. USA, 107, 16078-16083.
12. Chai, S., Bravo, A., Luder, G., Nedlin, A., Trautner, T.A. and Alonso, J.C. (1992) Molecular analysis of the Bacillus subtilis bacteriophage SPP1 region encompassing gene 1 to 6: the products of gene 1 and gene 2 are required for pac cleavage. J. Mol. Biol., 124, 87-102.
13. Chai, S., Lurz, R. and Alonso, J.C. (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.
14. Gual, A., Camacho, A.C. and Alonso, J.C. (2000) Functional analysis of the terminase large subunit, gp2, of Bacillus subtilis bacteriophage SPP1. J. Biol. Chem., 275, 35311-35319.
15. Camacho, A.C., Gual, A., Lurz, R., Tavares, P. and Alonso, J.C. (2003) Bacillus subtilis bacteriophage SPP1 DNA packaging motor requires terminase and portal proteins. J. Biol. Chem., 278, 23251-23259.
16. Oliveira, L., Alonso, J.C. and Tavares, P. (2005) A defined in vitro system for DNA packaging by the bacteriophage SPP1: insights into the headful packaging mechanism. J. Mol. Biol., 353, 529-539.
17. Oliveira, L., Henriques, A.O. and Tavares, P. (2006) Modulation of the viral ATPase activity by the portal protein correlates with DNA packaging efficiency. J. Biol. Chem., 281, 21914-21923.
18. Oliveira, L., Cuervo, A. and Tavares, P. (2010) Direct interaction of the bacteriophage SPP1 packaging ATPase with the portal protein. J. Biol. Chem., 285, 7366-7373.
19. Lebedev, A.A., Krause, M.H., Isidro, A.L., Vagin, A., Orlova, E.V., Turner, J., Dodson, E.J., Tavares, P. and Antson, A.A. (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J., 26, 1984-1994.
20. Cuervo, A., Vaney, M.C., Antson, A., Tavares, P. and Oliveira, L. (2007) Structural rearrangements between portal protein subunits are essential for viral DNA translocation. J. Biol. Chem., 282, 18907-18913.
21. Tavares, P., Santos, M.A., Lurz, R., Morelli, G., de Lencastre, H. and Trautner, T.A. (1992) Identification of a gene in Bacillus subtilis bacteriophage SPP1 determining the amount of packaged DNA. J. Mol. Biol., 225, 81-92.
22. Isidro, A., Henriques, A.O. and Tavares, P. (2004) The portal protein plays essential roles at different steps of the SPP1 DNA packaging process. Virology, 322, 253-263.
23. Studier, F.W. (1991) Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system. J. Mol. Biol., 219, 37-44.
24. Gual, A. and Alonso, J.C. (1998) Characterization of the small subunit of the terminase enzyme of the Bacillus subtilis bacteriophage SPP1. Virology, 242, 279-287.
25. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem., 72, 248-254.
26. Ericsson, U.B., Hallberg, B.M., Detitta, G.T., Dekker, N. and Nordlund, P. (2006) Thermofluor-based high-throughput stability optimization of proteins for structural studies. Anal. Biochem., 357, 289-298.
27. Sambrook, J., Maniatis, T. and Fritsch, E.F. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
28. Ghosh-Kumar, M., Alam, T.I., Draper, B., Stack, J.D. and Rao, V.B. (2010) Regulation by interdomain communication of a headful packaging nuclease from bacteriophage T4. Nucleic Acids Res., 397, 2742-2755.
29. Morita, M., Tasaka, M. and Fujisawa, H. (1995) Structural and functional domains of the large subunit of the bacteriophage T3 DNA packaging enzyme: importance of the C-terminal region in prohead binding. J. Mol. Biol., 245, 635-644.
30. Lin, H., Rao, V.B. and Black, L.W. (1999) Analysis of capsid portal protein and terminase functional domains: interaction sites required for DNA packaging in bacteriophage T4. J. Mol. Biol., 289, 249-260.
31. Kanamaru, S., Kondabagil, K., Rossman, M.G and Rao, V. (2004) The functional domains of bacteriophage T4 terminase. J. Biol. Chem., 279, 40795-40801.
32. Yeo, A. and Feiss, M. (1995) Specific interaction of terminase, the DNA packaging enzyme of bacteriophage X, with the portal protein of the prohead. J. Mol. Biol., 245, 141-150.
33. Yang, W., Lee, JY. and Nowotny, M. (2006) Making and breaking nucleic acids: two-Mg2+-ion catalysis and substrate specificity. Mol. Cell, 22, 5-13.
34. Bravo, A., Alonso, J.C. and Trautner, TA. (1990) Functional analysis of the Bacillus subtilis bacteriophage SPP1 pac site. Nucleic Acids Res., 18, 2881-2886.
35. Crepin, T., Dias, A., Palencia, A., Swale, C, Cusack, S. and Ruigrok, R.W. (2010) Mutational and metal binding analysis of the endonuclease domain of the influenza virus polymerase PA subunit. J. Virol., 84, 9096-9104.
36. Dias, A., Bouvier, D., Crepin, T., McCarthy, A.A., Hart, D.J., Baudin, F., Cusack, S. and Ruigrok, R.W. (2009) The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature, 458, 914-918.
37. Reguera, J., Weber, F. and Cusack, S. (2010) Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog., 6, e1001101.
38. Morin, B., Coutard, B., Lelke, M., Ferron, F., Kerber, R., Jamal, S., Frangeul, A., Baronti, C, Charrel, R., de Lamballerie, X. et al. (2010) The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog., 69, e1001038.
39. Tomka, MA. and Catalano, C.E. (1993) Physical and kinetic characterization of the DNA packaging enzyme from bacteriophage lambda. J. Biol. Chem., 268, 3056-3065.
40. Ponchon, L., Boulanger, P., Labesse, G and Letellier, L. (2006) The endonuclease domain of bacteriophage terminases belongs to the resolvase/integrase/ribonuclease H superfamily: a bioinformatics analysis validated by a functional study on bacteriophage T5. J. Biol. Chem., 281, 5829-5836.
41. Steitz, TA. and Steitz, JA. (1993) A general two-metal-ion mechanism for catalytic RNA. Proc. Natl Acad. Sci. USA, 90, 6498-6502.
42. Nowotny, M. and Yang, W. (2006) Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release. EMBO J., 259, 1924-1933.
43. Nowotny, M., Gaidamakov, S.A., Ghirlando, R., Cerritelli, S.M., Crouch, R.J. and Yang, W. (2007) Structure of human RNase H1 complexed with an RNA/DNA hybrid: insight into HIV reverse transcription. Mol. Cell, 28, 264-276.
44. Bock, C.W., Kaufman., Katz, A., Markham, G.D. and Glusker, J.P. (1999) Manganese as a Replacement for Magnesium and Zinc, Functional Comparison of the Divalent Ions. J. Am. Chem. Soc., 121, 7360-7372.
45. Glusker, J., Katz, A. and Bock, C.W. (1999) Metal ions in biological systems. Rigaku J., 16, 8-17.
46. Medicis, E.D., Paquette, J., Gauthier, J.J. and Shapcott, D. (1986) Magnesium and manganese content of halophilic bacteria. Appl. Environ. Microbiol., 52, 567-573.
47. Zhao, C., Lou, Z., Guo, Y., Ma, M., Chen, Y., Liang, S., Zhang, L., Chen, S., Li, X., Liu, Y. et al. (2009) Nucleoside monophosphate complex structures of the endonuclease domain from the influenza virus polymerase PA subunit reveal the substrate binding site inside the catalytic center. J. Virol., 83, 9024-9030.
48. Buttner, C.R., Chechik, M., Ortiz-Lombardia, M., Smits, C., Ebong, I.O., Chechik, V., Jeschke, G., Dykeman, E., Benini, S., Robinson, C.V. et al. (2012) Structural basis for DNA recognition and loading into a viral packaging motor. Proc. Natl Acad. Sci. USA, 109, 811-816.
49. Chai, S., Szepan, U. and Alonso, J.C. (1997) Bacillus subtilis bacteriophage SPP1 terminase has a dual activity: it is required for the packaging initiation and represses its own synthesis. Gene, 184, 251-256.
50. Hegde, S., Padilla-Sanchez, V., Draper, B. and Rao, V.B. (2012) Portal-large terminase interactions of the bacteriophage T4 DNA packaging machine implicate a molecular lever mechanism for coupling ATPase to DNA translocation. J. Virol., 86, 4046-4057.
51. Hang, J.Q., Tack, B.F. and Feiss, M. (2000) ATPase center of bacteriophage lambda terminase involved in post-cleavage stages of DNA packaging: identification of ATP-interactive amino acids. J. Mol. Biol., 302, 777-795.
52. Orlova, E.V., Dube, P., Beckmann, E., Zemlin, F., Lurz, R., Trautner, T.A., Tavares, P. and van Heel, M. (1999) Structure of the 13-fold symmetric portal protein of bacteriophage SPP1. Nat. Struct. Biol., 6, 842-846.