Headful DNA packaging: Bacteriophage SPP1 as a model system

Virus Research

Volumn 173, Issue 2, 2013, Pages 247-259

  Oliveira, Leonor ^a   Tavares, Paulo ^a   Alonso, Juan C ^b  

^a CNRS   (France)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

DNA packaging; DsDNA tailed bacteriophages; Herpesviruses; Portal protein; Terminase complex

Indexed keywords

BINDING PROTEIN; MOLECULAR MOTOR;

BACILLUS SUBTILIS; BACTERIOPHAGE; DNA PACKAGING; DNA VIRUS; GENE SEQUENCE; MACHINE; PORTAL VEIN; PRIORITY JOURNAL; REVIEW; VIRUS CAPSID; VIRUS GENOME;

BACILLUS PHAGES; BACILLUS SUBTILIS; DNA PACKAGING; DNA, VIRAL;

BACILLUS SUBTILIS; MIRIDAE;

EID: 84876882403     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2013.01.021     Document Type: Review

References (99)

1. Alonso J.C., Tavares P., Lurz R., Trautner T.A. Bacteriophage SPP1. The Bacteriophages 2006, 331-349. Oxford University Press, New York, USA. R. Calendar (Ed.).
2. Alonso J.C., Lüder G., Stiege A.C., Chai S., Weise F., Trautner T.A. The complete nucleotide sequence and functional organization of Bacillus subtilis bacteriophage SPP1. Gene 1997, 204:201-212.
3. Bath J., Wu L.J., Errington J., Wang J.C. Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science 2000, 290:995-997.
4. Bazinet C., King J. The DNA translocating vertex of dsDNA bacteriophage. Annual Review of Microbiology 1985, 39:109-129.
5. Becker B., de la Fuente N., Gassel M., Günther D., Tavares P., Lurz R., Trautner T.A., Alonso J. Head morphogenesis genes of the Bacillus subtilis bacteriophage SPP1. Journal of Molecular Biology 1997, 268:822-839.
6. de Beer T., Fang J., Ortega M.E., Yang Q., Maes L., Duffy C., Berton N., Sippy J., Overduin M., Feiss M., Catalano C.E. Insights into specific DNA recognition during the assembly of a viral genome packaging machine. Molecular Cell 2002, 9:981-991.
7. Black L.W. DNA packaging in dsDNA bacteriophages. Annual Review of Microbiology 1989, 43:267-292.
8. Bravo A., Alonso J.C., Trautner T.A. Functional analysis of the Bacillus subtilis bacteriophage SPP1 pac site. Nucleic Acids Research 1990, 18:2881-2886.
9. Büttner C.R., Chechik M., Ortiz-Lombardía M., Smits C., Ebong I.O., Chechik V., Jeschke G., Dykeman E., Benini S., Robinson C.V., Alonso J.C., Antson A.A. Structural basis for DNA recognition and loading into a viral packaging motor. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:811-816.
10. Camacho A.G., Gual A., Lurz R., Tavares P., Alonso J.C. Bacillus subtilis bacteriophage SPP1 DNA packaging motor requires terminase and portal proteins. Journal of Biological Chemistry 2003, 278:23251-23259.
11. Casjens S., Hendrix R. Control mechanisms in dsDNA bacteriophage assembly. The Bacteriophages 1988, vol. 1. Plenum Press, New York.
12. Casjens S. The DNA-packaging nanomotor of tailed bacteriophages. Nature Reviews Microbiology 2011, 9:647-657.
13. Catalano C.E., Cue D., Feiss M. Virus DNA packaging: the strategy used by phage lambda. Molecular Microbiology 1995, 16:1075-1086.
14. Catalano C.E. Viral Genome Packaging Machines: Genetics, Structure, and Mechanism 2005, vol. 1-4. Kluwer Academic/Plenium Publishers, NY.
15. Chai S., Bravo A., Lüder G., Nedlin A., Trautner T.A., Alonso J.C. 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. Journal of Molecular Biology 1992, 224:87-102.
16. Chai S., Kruft V., Alonso J.C. Analysis of the Bacillus subtilis bacteriophages SPP1 and SF6 gene 1 product: a protein involved in the initiation of headful packaging. Virology 1994, 202:930-939.
17. Chai S., Lurz R., Alonso J.C. The small subunit of the terminase enzyme of Bacillus subtilis bacteriophage SPP1 forms a specialized nucleoprotein complex with the packaging initiation region. Journal of Molecular Biology 1995, 252:386-398.
18. Chai S., Alonso J.C. Distamycin-induced inhibition of formation of a nucleoprotein complex between the terminase small subunit G1P and the non-encapsidated end (pacL site) of Bacillus subtilis bacteriophage SPP1. Nucleic Acids Research 1996, 24:282-288.
19. Chai S., Szepan U., Alonso J.C. Bacillus subtilis bacteriophage SPP1 terminase has a dual activity: it is required for the packaging initiation and represses its own synthesis. Gene 1997, 184:251-256.
20. Cornilleau C., Atmane N., Jacquet E., Smits C., Alonso J.C., Tavares P., Oliveira L. The nuclease domain of the SPP1 packaging motor coordinates DNA cleavage and encapsidation. Nucleic Acids Research 2013, 41:340-354.
21. Cuervo A., Vaney M.-C., Antson A.A., Tavares P., Oliveira L. Structural rearrangements between portal protein subunits are essential for viral DNA translocation. Journal of Biological Chemistry 2007, 282:18907-18913.
22. Cuervo A., Carrascosa J.L. Viral connectors for DNA encapsulation. Current Opinion in Biotechnology 2012, 23:529-536.
23. Deichelbohrer I., Messer W., Trautner T.A. Genome of Bacillus subtilis bacteriophage SPP1: structure and nucleotide sequence of pac, the origin of DNA packaging. Journal of Virology 1982, 42:83-90.
24. Dröge A., Tavares P. In vitro packaging of DNA of the Bacillus subtilis bacteriophage SPP1. Journal of Molecular Biology 2000, 296:103-115.
25. Dröge A., Santos M.A., Stiege A.C., Alonso J.C., Lurz R., Trautner T.A., Tavares P. Shape and DNA packaging activity of bacteriophage SPP1 procapsid: protein components and interactions during assembly. Journal of Molecular Biology 2000, 296:117-132.
26. Dröge A., Tavares P. Bacteriophage SPP1 DNA packaging. Viral Genome packaging 2005, 89-101. Landes Publishing, Georgetown, Texas, USA and Kluwer Academic/Plenum Publishers, New York, USA. C.E. Catalano (Ed.).
27. Dröge A., Santos M.A., Stiege A., Alonso J.C., Lurz R., Trautner T.A., Tavares P. Shape and DNA packaging activity of bacteriophage SPP1 procapsid: protein components and interactions during assembly. Journal of Molecular Biology 2000, 296:117-132.
28. Dube P., Tavares P., Lurz R., van Heel M. The portal protein of bacteriophage SPP1: a DNA pump with 13-fold symmetry. EMBO Journal 1993, 12:1303-1309.
29. Evilevitch A., Lavelle L., Knobler C.M., Raspaud E., Gelbart W.M. Osmotic pressure inhibition of DNA ejection from phage. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:9292-9295.
30. Feiss M., Rao V.B. The bacteriophage DNA packaging machine. Advances in Experimental Medicine and Biology 2012, 726:489-509.
31. Fujisawa H., Morita M. Phage DNA packaging. Genes to Cells 1997, 2:537-545.
32. Ghosh-Kumar M., Alam T.I., Draper B., Stack J.D., Rao V.B. Regulation by interdomain communication of a headful packaging nuclease from bacteriophage T4. Nucleic Acids Research 2010, 397:2742-2755.
33. Grimes S., Ma S., Gao J., Atz R., Jardine P.J. Role of φ29 connector channel loops in late-stage DNA packaging. Journal of Molecular Biology 2011, 410:50-59.
34. Gual A., Alonso J.C. Characterization of the small subunit of the terminase enzyme of the Bacillus subtilis bacteriophage SPP1. Virology 1998, 242:279-287.
35. Gual A., Camacho A.G., Alonso J.C. Functional analysis of the terminase large subunit, G2P, of Bacillus subtilis bacteriophage SPP1. Journal of Biological Chemistry 2000, 275:35311-35319.
36. Hamada K., Fujisawa H., Minagawa T. A defined in vitro system for packaging of bacteriophage T3 DNA. Virology 1986, 151:119-123.
37. Hwang Y., Catalano C.E., Feiss M. Kinetic and mutational dissection of the two ATPase activities of terminase, the DNA packaging enzyme of bacteriophage Chi. Biochemistry 1996, 35:2796-2803.
38. Humphreys G.O., Trautner T.A. Maturation of bacteriophage SPP1 DNA: limited precision in the sizing of mature bacteriophage genomes. Journal of Virology 1981, 37:832-835.
39. Isidro A., Santos M.A., Henriques A.O., Tavares P. The high-resolution functional map of bacteriophage SPP1 portal protein. Molecular Microbiology 2004, 51:949-962.
40. Isidro A., Henriques A.O., Tavares P. The portal protein plays essential roles at different steps of the SPP1 DNA packaging process. Virology 2004, 322:253-263.
41. Jekow P., Behlke J., Tichelaar W., Lurz R., Regalla M., Hinrichs W., Tavares P. Role of the ionic environment on the assembly of bacteriophage SPP1 portal protein. European Journal of Biochemistry 1999, 264:724-735.
42. Jekow P., Schaper S., Günther D., Tavares P., Hinrichs W. Crystallization and preliminary X-ray crystallographic studies of the 13-fold symmetric portal protein of bacteriophage SPP1. Acta Crystallographica Section D 1998, 54:1008-1011.
43. Kondabagil K.R., Zhang Z., Rao V.B. The DNA translocating ATPase of bacteriophage T4 packaging motor. Journal of Molecular Biology 2006, 363:86-99.
44. Koti J.C., Morais M.C., Rajagopal R., Owen B.A.L., McMurray C.T., Anderson D. DNA packaging motor assembly intermediates of bacteriophage φ29. Journal of Molecular Biology 2008, 381:1114-1132.
45. Lebedev A.A., Krause M.H., Isidro A.L., Vagin A., Orlova E.V., Turner J., Dodson E.J., Tavares P., Antson A.A. Structural framework for DNA translocation via the viral portal protein. EMBO Journal 2007, 26:1984-1994.
46. Leffers G., Rao V.B. Biochemical characterization of an ATPase activity associated with the large packaging subunit gp17 from the bacteriophage T4. Journal of Biological Chemistry 2000, 275:37127-37136.
47. Lhuillier S., Gallopin M., Gilquin B., Brasilès S., Lancelot N., Letellier G., Gilles M., Dethan G., Orlova E.V., Couprie J., Tavares P., Zinn-Justin S. Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:8507-8512.
48. Lin H., Rao V.B., Black L.W. Analysis of capsid portal protein and terminase functional domains: interaction sites required for DNA packaging in bacteriophage T4. Journal of Molecular Biology 1999, 289:249-260.
49. Lo Piano A., Martínez-Jiménez M., Zecchi L., Ayora S. Recombination-dependent concatemeric viral DNA replication. Virus Research 2011, 160:1-14.
50. Lurz R., Orlova E., Günther D., Dube P., Dröge A., Weise F., van Heel M., Tavares P. Structural organisation of the head-to-tail interface of a bacterial virus. Journal of Molecular Biology 2001, 310:1027-1037.
51. Maluf N.K., Gaussier H., Bogner E., Feiss M., Catalano C.E. Assembly of bacteriophage lambda terminase into a viral DNA maturation and packaging machine. Biochemistry 2006, 45:15259-15268.
52. McIntosh P.K., Dunker R., Mulder C., Brown N. DNA of Bacillus subtilis bacteriophage SPP1: physical mapping and localization of the origin of replication. Journal of Virology 1978, 28:865-876.
53. Morais M.C., Koti J.S., Browman V.D., Reyes-Aldrete E., Anderson D., Rossmann M. Defining molecular and domain boundaries in the bacteriophage φ29 DNA packaging motor. Structure 2008, 16:1267-1274.
54. Morelli G., Fisseau C., Behrens B., Trautner T.A., Luh J., Ratcliff S.W., Allison D.P., Ganesan A.T. The genome of Bacillus subtilis phage SPP1: the topology of DNA molecules. Molecular and General Genetics 1979, 168:153-161.
55. Morita M., Tasaka M., Fujisawa H. Structural and functional domains of the large subunit of the bacteriophage T3 DNA packaging enzyme: importance of the C-terminal region in prohead binding. Journal of Molecular Biology 1995, 245:635-644.
56. Nadal M., Mas P.J., Blanco A.G., Arnan C., Solà M., Hart D.J., Coll M. Structure and inhibition of herpesvirus DNA packaging terminase nuclease domain. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:16078-16083.
57. Nemecek D., Gilcrease E.B., Kang S., Prevelige P.E., Casjens S., Thomas G.J. Subunit conformations and assembly states of a DNA-translocating motor: the terminase of bacteriophage P22. Journal of Molecular Biology 2007, 374:817-836.
58. Nemecek D., Lander G.C., Johnson J.E., Casjens S.R., Thomas G.J. Assembly architecture and DNA binding of the bacteriophage P22 terminase small subunit. Journal of Molecular Biology 2008, 383:494-501.
59. Olia A.S., Prevelige P.E., Johnson J.E., Cingolani G. Three-dimensional structure of a viral genome-delivery portal vertex. Nature Structural & Molecular Biology 2011, 18:597-603.
60. Oliveira L., Alonso J.C., Tavares P. A defined in vitro system for DNA packaging by the bacteriophage SPP1: insights into the headful packaging mechanism. Journal of Molecular Biology 2005, 353:529-539.
61. Oliveira L., Henriques A.O., Tavares P. Modulation of the viral ATPase activity by the portal protein correlates with DNA packaging efficiency. Journal of Biological Chemistry 2006, 281:21914-21923.
62. Oliveira L., Cuervo A., Tavares P. Direct interaction of the bacteriophage SPP1 packaging ATPase with the portal protein. Journal of Biological Chemistry 2010, 285:7366-7373.
63. Orlova E., Dube P., Beckmann E., Zemlin F., Lurz R., Trautner T.A., Tavares P., van Heel M. Structure of the 13-fold symmetric portal protein of bacteriophage SPP1. Natural Structural Biology 1999, 6:842-846.
64. Orlova E.V., Gowen B., Dröge A., Stiege A., Lurz R., Weise F., van Heel M., Tavares P. Structure of a viral DNA gatekeeper at 10Å resolution by cryo-electron microscopy. EMBO Journal 2003, 22:1255-1262.
65. Pease P.J., Levy O., Cost G.J., Gore J., Ptacin J.L., Sherratt D., Bustamante C., Cozzarelli N.R. Sequence-directed DNA translocation by purified FtsK. Science 2005, 307:586-590.
66. Pedré X., Weise F., Chai S., Lüder G., Alonso J.C. Analysis of cis and trans acting elements required for the initiation of DNA replication in the Bacillus subtilis bacteriophage SPP1. Journal of Molecular Biology 1994, 236:1324-1340.
67. Plisson C., White H.E., Auzat I., Zafarani A., São-José C., Lhuillier S., Tavares P., Orlova E.V. Structure of bacteriophage SPP1 tail reveals trigger for DNA ejection. EMBO Journal 2007, 26:3720-3728.
68. Poh S.L., El Khadali F., Berrier C., Lurz R., Melki R., Tavares P. Oligomerization of the SPP1 scaffolding protein. Journal of Molecular Biology 2008, 378:551-564.
69. Prevelige P.E., Fane B.A. Building the machines: scaffolding protein functions during bacteriophage morphogenesis. Advances in Experimental Medicine and Biology 2012, 726:325-350.
70. Rao V.B., Black L. DNA packaging in bacteriophage T4. Viral Genome Packaging Machines 2005, 40-58. Landes Bioscience, Georgetown, TX. C. Catalano (Ed.).
71. Rao V.B., Feiss M. The bacteriophage DNA packaging motor. Annual Review of Genetics 2008, 42:647-681.
72. Raspaud E., Forth T., São-José C., Tavares P., De Frutos M. A kinetic analysis of DNA ejection from tailed bacteriophages revealing the prerequisite activation energy. Biophysical Journal 2007, 93:3999-4005.
73. Roy A., Cingolani G. Structure of P22 headful packaging nuclease. Journal of Biological Chemistry 2012, 287:28196-28205.
74. Roy A., Bhardwaj A., Datta P., Lander G.C., Cingolani G. Small terminase couples viral DNA binding to genome-packaging ATPase activity. Structure 2012, 20:1403-1413.
75. Saleh O.A., Perals C., Barre F.X., Allemand J.F. Fast, DNA-sequence independent translocation by FtsK in a single-molecule experiment. EMBO Journal 2004, 23:2430-2439.
76. São-José C., Baptista C., Santos M.A. Bacillus subtilis operon encoding a membrane receptor for bacteriophage SPP1. Journal of Bacteriology 2004, 186:8337-8346.
77. São-José C., Lhuillier S., Lurz R., Melki R., Lepault J., Santos M.A., Tavares P. The ectodomain of the viral receptor YueB forms a fiber that triggers ejection of bacteriophage SPP1 DNA. Journal of Biological Chemistry 2006, 281:11464-11470.
78. São-José C., De Frutos M., Raspaud E., Santos M.A., Tavares P. Pressure built by DNA packing inside virions: enough to drive DNA ejection in vitro, largely insufficient for delivery into the bacterial cytoplasm. Journal of Molecular Biology 2007, 374:346-355.
79. Simpson A.A., Tao Y., Leiman P.G., Badasso M.O., He Y., Jardine P.J., Olson N.H., Morais M.C., Grimes S., Anderson D.L., Baker T.S., Rossmann M.G. Structure of the bacteriophage phi29 DNA packaging motor. Nature 2000, 408:745-750.
80. Smits C., Chechik M., Kovalevskiy O.V., Shevtsov M.B., Foster A.W., Alonso J.C., Antson A.A. Structural basis for the nuclease activity of a bacteriophage large terminase. EMBO Reports 2009, 10:592-598.
81. Sternberg N., Coulby J. Recognition and cleavage of the bacteriophage P1 packaging site (pac). Differential processing of the cleaved ends in vivo. Journal of Molecular Biology 1987, 194:453-468.
82. Stiege A., Isidro A., Dröge A., Tavares P. Specific and stoichiometric targetting of a DNA-binding protein to the SPP1 procapsid by interaction with the portal oligomer. Molecular Microbiology 2003, 49:1201-1212.
83. Streisinger G., Emrich J., Stahl M.M. Chromosome structure in phage T4. iii. Terminal redundancy and length determination. Proceedings of the National Academy of Sciences of the United States of America 1967, 57:292-295.
84. Sun S., Kondabagil K., Draper B., Alam T.I., Bowman V.D., Zhang Z., Hegde S., Fokine A., Rossmann M.G., Rao V.B. The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell 2008, 135:1251-1262.
85. Sun S., Gao S., Kondabagil K., Xiang Y., Rossman M.G., Rao V.B. 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 2012, 109:817-822.
86. Tang J., Lander G.C., Olia A.S., Li R., Casjens S., Prevelige P., Cingolani G., Baker T.S., Johnson J.E. Peering down the barrel of a bacteriophage portal: the genome packaging and release valve in p22. Structure 2011, 19:496-502.
87. Tavares P., Santos M.A., Lurz R., Morelli G., Lencastre H., Trautner T.A. Identification of a gene in Bacillus subtilis bacteriophage SPP1 determining the amount of packaged DNA. Journal of Molecular Biology 1992, 225:81-92.
88. Tavares P., Dröge A., Lurz R., Graeber I., Orlova E., Dube P., van Heel M. The SPP1 connection. FEMS Microbiology Reviews 1995, 17:47-56.
89. Tavares P., Lurz R., Stiege A., Rückert B., Trautner T.A. Sequential headful packaging and fate of the cleaved DNA end in bacteriophage SPP1. Journal of Molecular Biology 1996, 264:954-967.
90. Tavares P., Zinn-Justin S., Orlova E.V. Genome gating in tailed bacteriophage capsids. Viral Molecular Machines, Adv. Exp. Med. Biol. 726 2012, 585-600. M.G. Rossmann, V.B. Rao (Eds.).
91. Trautner T.A., Spatz C., Behrens B., Pawlek B., Behnke M. Exchange between complementary strands of DNA?. Advances in Biosciences 1972, 8:79-87.
92. Tye B.K., Huberman J.A., Botstein D. Non-random circular permutation of phage P22 DNA. Journal of Molecular Biology 1974, 85:501-532.
93. Valpuesta J.M., Carrascosa J.L. Structure of viral connectors and their function in bacteriophage assembly and DNA packaging. Quarterly Reviews of Biophysics 1994, 27:107-155.
94. Van Heel M., Orlova E., Dube P., Tavares P. Intrinsic versus imposed curvature in cyclical oligomers: the portal protein of bacteriophage SPP1. EMBO Journal 1996, 15:4785-4788.
95. Vinga I., Dröge A., Stiege A.C., Lurz R., Santos M.A., Daugelavičius R., Tavares P. The minor capsid protein gp7 of bacteriophage SPP1 is required for efficient infection of Bacillus subtilis. Molecular Microbiology 2006, 61:1609-1621.
96. White H.E., Sherman M.B., Brasilès S., Jacquet E., Seavers P., Tavares P., Orlova E.V. Capsid structure and its stability at the late stages of bacteriophage SPP1 assembly. Journal of Virology 2012, 86:6768-6777.
97. 2+-ion catalysis and substrate specificity. Molecular Cell 2006, 22:5-13.
98. Yeo A., Feiss M. Specific interaction of terminase, the DNA packaging enzyme of bacteriophage λ, with the portal protein of the prohead. Journal of Molecular Biology 1995, 245:141-150.
99. Zhao H., Finch C.J., Sequeira R.D., Johnson B.A., Johnson J.E., Casjens S.R., Tang L. Crystal structure of the DNA-recognition component of the bacterial virus Sf6 genome-packaging machine. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:1971-1976.