Adenosine triphosphatases of thermophilic archaeal double-stranded DNA viruses

Cell and Bioscience

Volumn 4, Issue 1, 2014, Pages

  Happonen, Lotta J ^a   Erdmann, Susanne ^b   Garrett, Roger A ^b   Butcher, Sarah J ^c  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Archaeal; ATPase; Genome injection; Genome packaging; MoxR ATPase; Virus

Indexed keywords

ARCHAEA; DNA VIRUSES;

EID: 84904520306     PISSN: None     EISSN: 20453701     Source Type: Journal    
DOI: 10.1186/2045-3701-4-37     Document Type: Review

References (94)

1. Guo P, Lee TJ. Viral nanomotors for packaging of dsDNA and dsRNA. Mol Microbiol 2007, 64(4):886-903.
2. Hanson PI, Whiteheart SW. AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol 2005, 6(7):519-529.
3. Iyer LM, Makarova KS, Koonin EV, Aravind L. Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 2004, 32(17):5260-5279.
4. Walker JE, Saraste M, Runswick MJ, Gay NJ. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1982, 1(8):945-951.
5. Goetzinger KR, Rao VB. Defining the ATPase center of bacteriophage T4 DNA packaging machine: requirement for a catalytic glutamate residue in the large terminase protein gp17. J Mol Biol 2003, 331(1):139-154.
6. Iyer LM, Leipe DD, Koonin EV, Aravind L. Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol 2004, 146(1-2):11-31.
7. Happonen LJ, Oksanen E, Liljeroos L, Goldman A, Kajander T, Butcher SJ. The Structure of the NTPase That Powers DNA Packaging into Sulfolobus Turreted Icosahedral Virus 2. J Virol 2013, 87(15):8388-8398.
8. Massey TH, Mercogliano CP, Yates J, Sherratt DJ, Lowe J. Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol Cell 2006, 23(4):457-469.
9. Subramanya HS, Bird LE, Brannigan JA, Wigley DB. Crystal structure of a DExx box DNA helicase. Nature 1996, 384(6607):379-383.
10. Mancini EJ, Kainov DE, Grimes JM, Tuma R, Bamford DH, Stuart DI. Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell 2004, 118(6):743-755.
11. Nadanaciva S, Weber J, Wilke-Mounts S, Senior AE. Importance of F1-ATPase residue alpha-Arg-376 for catalytic transition state stabilization. Biochemistry 1999, 38(47):15493-15499.
12. Sun S, Kondabagil K, Gentz PM, Rossmann MG, Rao VB. The structure of the ATPase that powers DNA packaging into bacteriophage T4 procapsids. Mol Cell 2007, 25(6):943-949.
13. Guenther B, Onrust R, Sali A, O'Donnell M, Kuriyan J. Crystal structure of the delta' subunit of the clamp-loader complex of E. coli DNA polymerase III. Cell 1997, 91(3):335-345.
14. Bochtler M, Hartmann C, Song HK, Bourenkov GP, Bartunik HD, Huber R. The structures of HsIU and the ATP-dependent protease HsIU-HsIV. Nature 2000, 403(6771):800-805.
15. Liu J, Smith CL, DeRyckere D, DeAngelis K, Martin GS, Berger JM. Structure and function of Cdc6/Cdc18: implications for origin recognition and checkpoint control. Mol Cell 2000, 6(3):637-648.
16. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011, 7:539.
17. Gouet P, Courcelle E, Stuart DI, Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15(4):305-308.
18. Rao VB, Feiss M. The bacteriophage DNA packaging motor. Annu Rev Genet 2008, 42:647-681.
19. Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C. The bacteriophage straight phi29 portal motor can package DNA against a large internal force. Nature 2001, 413(6857):748-752.
20. Simpson AA, Tao Y, Leiman PG, Badasso MO, He Y, Jardine PJ, Olson NH, Morais MC, Grimes S, Anderson DL, Rossmann MG. Structure of the bacteriophage phi29 DNA packaging motor. Nature 2000, 408(6813):745-750.
21. Guo P, Peterson C, Anderson D. Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi 29. J Mol Biol 1987, 197(2):229-236.
22. Schwartz C, De Donatis GM, Fang H, Guo P. The ATPase of the phi29 DNA packaging motor is a member of the hexameric AAA+ superfamily. Virology 2013, 443(1):20-27.
23. Guo P, Schwartz C, Haak J, Zhao Z. Discovery of a new motion mechanism of biomotors similar to the earth revolving around the sun without rotation. Virology 2013, 446(1-2):133-143.
24. Schwartz C, De Donatis GM, Zhang H, Fang H, Guo P. Revolution rather than rotation of AAA+ hexameric phi29 nanomotor for viral dsDNA packaging without coiling. Virology 2013, 443(1):28-39.
25. Driedonks RA, Engel A, tenHeggeler B, van D. Gene 20 product of bacteriophage T4 its purification and structure. J Mol Biol 1981, 152(4):641-662.
26. Sun S, Kondabagil K, Draper B, Alam TI, Bowman VD, Zhang Z, Hegde S, Fokine A, Rossmann MG, Rao VB. The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell 2008, 135(7):1251-1262.
27. Sun S, Gao S, Kondabagil K, Xiang Y, Rossmann MG, Rao VB. Structure and function of the small terminase component of the DNA packaging machine in T4-like bacteriophages. Proc Natl Acad Sci U S A 2012, 109(3):817-822.
28. Fuller DN, Raymer DM, Kottadiel VI, Rao VB, Smith DE. Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proc Natl Acad Sci U S A 2007, 104(43):16868-16873.
29. Kanamaru S, Kondabagil K, Rossmann MG, Rao VB. The functional domains of bacteriophage t4 terminase. J Biol Chem 2004, 279(39):40795-40801.
30. Schwartz C, Guo P. Ultrastable pRNA hexameric ring gearing hexameric phi29 DNA-packaging motor by revolving without rotating and coiling. Curr Opin Biotechnol 2013, 24(4):581-590.
31. Zhao Z, Khisamutdinov E, Schwartz C, Guo P. Mechanism of one-way traffic of hexameric phi29 DNA packaging motor with four electropositive relaying layers facilitating antiparallel revolution. ACS Nano 2013, 7(5):4082-4092.
32. Kainov DE, Mancini EJ, Telenius J, Lisal J, Grimes JM, Bamford DH, Stuart DI, Tuma R. Structural basis of mechanochemical coupling in a hexameric molecular motor. J Biol Chem 2008, 283(6):3607-3617.
33. Lisal J, Tuma R. Cooperative mechanism of RNA packaging motor. J Biol Chem 2005, 280(24):23157-23164.
34. Stro¨msten NJ, Bamford DH, Bamford JK. In vitro DNA packaging of PRD1: a common mechanism for internal-membrane viruses. J Mol Biol 2005, 348(3):617-629.
35. Ziedaite G, Kivela¨ HM, Bamford JK, Bamford DH. Purified membrane-containing procapsids of bacteriophage PRD1 package the viral genome. J Mol Biol 2009, 386(3):637-647.
36. Stro¨msten NJ, Bamford DH, Bamford JK. The unique vertex of bacterial virus PRD1 is connected to the viral internal membrane. J Virol 2003, 77(11):6314-6321.
37. Rice G, Tang L, Stedman K, Roberto F, Spuhler J, Gillitzer E, Johnson JE, Douglas T, Young M. The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life. Proc Natl Acad Sci U S A 2004, 101(20):7716-7720.
38. Ha¨ring M, Peng X, Bru¨gger K, Rachel R, Stetter KO, Garrett RA, Prangishvili D. Morphology and genome organization of the virus PSV of the hyperthermophilic archaeal genera Pyrobaculum and Thermoproteus: a novel virus family, the Globuloviridae. Virology 2004, 323(2):233-242.
39. Ahn DG, Kim SI, Rhee JK, Kim KP, Pan JG, Oh JW. TTSV1, a new virus-like particle isolated from the hyperthermophilic crenarchaeote Thermoproteus tenax. Virology 2006, 351(2):280-290.
40. Erdmann S, Scheele U, Garrett RA. AAA ATPase p529 of Acidianus two-tailed virus ATV and host receptor recognition. Virology 2011, 421(1):61-66.
41. Scheele U, Erdmann S, Ungewickell EJ, Felisberto-Rodrigues C, Ortiz-Lombardia M, Garrett RA. Chaperone role for proteins p618 and p892 in the extracellular tail development of Acidianus two-tailed virus. J Virol 2011, 85(10):4812-4821.
42. Xiang X, Chen L, Huang X, Luo Y, She Q, Huang L. Sulfolobus tengchongensis spindle-shaped virus STSV1: virus-host interactions and genomic features. J Virol 2005, 79(14):8677-8686.
43. Erdmann S, Chen B, Huang X, Deng L, Liu C, Shah SA, Le Moine BS, Sobrino CL, Wang H, Wei Y, She Q, Garrett RA, Huang L, Lin L. A novel single-tailed fusiform Sulfolobus virus STSV2 infecting model Sulfolobus species. Extremophiles 2014, 18(1):51-60.
44. Erdmann S, Le Moine BS, Garrett RA. Inter-viral conflicts that exploit host CRISPR immune systems of Sulfolobus. Mol Microbiol 2014, 91(5):900-917.
45. Redder P, Peng X, Bru¨gger K, Shah SA, Roesch F, Greve B, She Q, Schleper C, Forterre P, Garrett RA, Prangishvili D. Four newly isolated fuselloviruses from extreme geothermal environments reveal unusual morphologies and a possible interviral recombination mechanism. Environ Microbiol 2009, 11(11):2849-2862.
46. Palm P, Schleper C, Grampp B, Yeats S, McWilliam P, Reiter WD, Zillig W. Complete nucleotide sequence of the virus SSV1 of the archaebacterium Sulfolobus shibatae. Virology 1991, 185(1):242-250.
47. Stedman KM, She Q, Phan H, Arnold HP, Holz I, Garrett RA, Zillig W. Relationships between fuselloviruses infecting the extremely thermophilic archaeon Sulfolobus: SSV1 and SSV2. Res Microbiol 2003, 154(4):295-302.
48. Peng X. Evidence for the horizontal transfer of an integrase gene from a fusellovirus to a pRN-like plasmid within a single strain of Sulfolobus and the implications for plasmid survival. Microbiology 2008, 154(Pt 2):383-391.
49. Wiedenheft B, Stedman K, Roberto F, Willits D, Gleske AK, Zoeller L, Snyder J, Douglas T, Young M. Comparative genomic analysis of hyperthermophilic archaeal Fuselloviridae viruses. J Virol 2004, 78(4):1954-1961.
50. Rice G, Stedman K, Snyder J, Wiedenheft B, Willits D, Brumfield S, McDermott T, Young MJ. Viruses from extreme thermal environments. Proc Natl Acad Sci U S A 2001, 98(23):13341-13345.
51. Servin-Garciduenas LE, Peng X, Garrett RA, Martinez-Romero E. Genome sequence of a novel archaeal fusellovirus assembled from the metagenome of a mexican hot spring. Genome Announcements 2013, 1(2):e0016413.
52. Mochizuki T, Sako Y, Prangishvili D. Provirus induction in hyperthermophilic archaea: characterization of Aeropyrum pernix spindle-shaped virus 1 and Aeropyrum pernix ovoid virus 1. J Bacteriol 2011, 193(19):5412-5419.
53. Bettstetter M, Peng X, Garrett RA, Prangishvili D. AFV1, a novel virus infecting hyperthermophilic archaea of the genus acidianus. Virology 2003, 315(1):68-79.
54. Ha¨ring M, Vestergaard G, Bru¨gger K, Rachel R, Garrett RA, Prangishvili D. Structure and genome organization of AFV2, a novel archaeal lipothrixvirus with unusual terminal and core structures. J Bacteriol 2005, 187(11):3855-3858.
55. Vestergaard G, Ha¨ring M, Peng X, Rachel R, Garrett RA, Prangishvili D. A novel rudivirus, ARV1, of the hyperthermophilic archaeal genus Acidianus. Virology 2005, 336(1):83-92.
56. Peng X, Blum H, She Q, Mallok S, Bru¨gger K, Garrett RA, Zillig W, Prangishvili D. Sequences and replication of genomes of the archaeal rudiviruses SIRV1 and SIRV2: relationships to the archaeal lipothrixvirus SIFV and some eukaryal viruses. Virology 2001, 291(2):226-234.
57. Vestergaard G, Shah SA, Bize A, Reitberger W, Reuter M, Phan H, Briegel A, Rachel R, Garrett RA, Prangishvili D. Stygiolobus rod-shaped virus and the interplay of crenarchaeal rudiviruses with the CRISPR antiviral system. J Bacteriol 2008, 190(20):6837-6845.
58. Servin-Garciduenas LE, Peng X, Garrett RA, Martinez-Romero E. Genome sequence of a novel archaeal rudivirus recovered from a mexican hot spring. Genome Announcements 2013, 1(2):e0016413.
59. Garrett RA, Prangishvili D, Shah SA, Reuter M, Stetter KO, Peng X. Metagenomic analyses of novel viruses and plasmids from a cultured environmental sample of hyperthermophilic neutrophiles. Environ Microbiol 2010, 12(11):2918-2930.
60. Gorlas A, Koonin EV, Bienvenu N, Prieur D, Geslin C. TPV1, the first virus isolated from the hyperthermophilic genus Thermococcus. Environ Microbiol 2012, 14(2):503-516.
61. Bamford DH, Ravantti JJ, Ro¨nnholm G, Laurinavicius S, Kukkaro P, Dyall-Smith M, Somerharju P, Kalkkinen N, Bamford JK. Constituents of SH1, a novel lipid-containing virus infecting the halophilic euryarchaeon Haloarcula hispanica. J Virol 2005, 79(14):9097-9107.
62. Zhang Z, Liu Y, Wang S, Yang D, Cheng Y, Hu J, Chen J, Mei Y, Shen P, Bamford DH, Chen X. Temperate membrane-containing halophilic archaeal virus SNJ1 has a circular dsDNA genome identical to that of plasmid pHH205. Virology 2012, 434(2):233-241.
63. Aalto AP, Bitto D, Ravantti JJ, Bamford DH, Huiskonen JT, Oksanen HM. Snapshot of virus evolution in hypersaline environments from the characterization of a membrane-containing Salisaeta icosahedral phage 1. Proc Natl Acad Sci U S A 2012, 109(18):7079-7084.
64. Pietila¨ MK, Laurinma¨ki P, Russell DA, Ko CC, Jacobs-Sera D, Butcher SJ, Bamford DH, Hendrix RW. Insights into head-tailed viruses infecting extremely halophilic archaea. J Virol 2013, 87(6):3248-3260.
65. Pietila¨ MK, Laurinma¨ki P, Russell DA, Ko CC, Jacobs-Sera D, Hendrix RW, Bamford DH, Butcher SJ. Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story. Proc Natl Acad Sci U S A 2013, 110(26):10604-10609.
66. Bath C, Cukalac T, Porter K, Dyall-Smith ML. His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group. Salterprovirus. Virology 2006, 350(1):228-239.
67. Pietila¨ MK, Atanasova NS, Manole V, Liljeroos L, Butcher SJ, Oksanen HM, Bamford DH. Virion architecture unifies globally distributed pleolipoviruses infecting halophilic archaea. J Virol 2012, 86(9):5067-5079.
68. Pietila¨ MK, Atanasova NS, Oksanen HM, Bamford DH. Modified coat protein forms the flexible spindle-shaped virion of haloarchaeal virus His1. Environ Microbiol 2013, 15(6):1674-1686.
69. Ha¨ring M, Vestergaard G, Rachel R, Chen L, Garrett RA, Prangishvili D. Virology: independent virus development outside a host. Nature 2005, 436(7054):1101-1102.
70. Prangishvili D, Vestergaard G, Ha¨ring M, Aramayo R, Basta T, Rachel R, Garrett RA. Structural and genomic properties of the hyperthermophilic archaeal virus ATV with an extracellular stage of the reproductive cycle. J Mol Biol 2006, 359(5):1203-1216.
71. Happonen LJ, Redder P, Peng X, Reigstad LJ, Prangishvili D, Butcher SJ. Familial relationships in hyperthermo- and acidophilic archaeal viruses. J Virol 2010, 84(9):4747-4754.
72. Lee TJ, Guo P. Interaction of gp16 with pRNA and DNA for genome packaging by the motor of bacterial virus phi29. J Mol Biol 2006, 356(3):589-599.
73. Alam TI, Rao VB. The ATPase domain of the large terminase protein, gp17, from bacteriophage T4 binds DNA: implications to the DNA packaging mechanism. J Mol Biol 2008, 376(5):1272-1281.
74. Abrescia NG, Bamford DH, Grimes JM, Stuart DI. Structure unifies the viral universe. Annu Rev Biochem 2012, 81:795-822.
75. Benson SD, Bamford JK, Bamford DH, Burnett RM. Does common architecture reveal a viral lineage spanning all three domains of life?. Mol Cell 2004, 16(5):673-685.
76. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 2004, 25(13):1605-1612.
77. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 2008, 9:40.
78. Davies JM, Brunger AT, Weis WI. Improved structures of full-length p97, an AAA ATPase: implications for mechanisms of nucleotide-dependent conformational change. Structure 2008, 16(5):715-726.
79. El Bakkouri M, Gutsche I, Kanjee U, Zhao B, Yu M, Goret G, Schoehn G, Burmeister WP, Houry WA. Structure of RavA MoxR AAA+ protein reveals the design principles of a molecular cage modulating the inducible lysine decarboxylase activity. Proc Natl Acad Sci U S A 2010, 107(52):22499-22504.
80. Butcher SJ, Manole V, Karhu NJ. Lipid-containing viruses: bacteriophage PRD1 assembly. Adv Exp Med Biol 2012, 726:365-377.
81. Veesler D, Ng TS, Sendamarai AK, Eilers BJ, Lawrence CM, Lok SM, Young MJ, Johnson JE, Fu CY. Atomic structure of the 75 MDa extremophile Sulfolobus turreted icosahedral virus determined by CryoEM and X-ray crystallography. Proc Natl Acad Sci U S A 2013, 110(14):5504-5509.
82. Zhang Y, Skolnick J. Scoring function for automated assessment of protein structure template quality. Proteins 2004, 57(4):702-710.
83. Pye VE, Dreveny I, Briggs LC, Sands C, Beuron F, Zhang X, Freemont PS. Going through the motions: the ATPase cycle of p97. J Struct Biol 2006, 156(1):12-28.
84. Larson ET, Eilers B, Menon S, Reiter D, Ortmann A, Young MJ, Lawrence CM. A winged-helix protein from Sulfolobus turreted icosahedral virus points toward stabilizing disulfide bonds in the intracellular proteins of a hyperthermophilic virus. Virology 2007, 368(2):249-261.
85. Larson ET, Eilers BJ, Reiter D, Ortmann AC, Young MJ, Lawrence CM. A new DNA binding protein highly conserved in diverse crenarchaeal viruses. Virology 2007, 363(2):387-396.
86. Maaty WS, Ortmann AC, Dlakic M, Schulstad K, Hilmer JK, Liepold L, Weidenheft B, Khayat R, Douglas T, Young MJ, Bothner B. Characterization of the archaeal thermophile Sulfolobus turreted icosahedral virus validates an evolutionary link among double-stranded DNA viruses from all domains of life. J Virol 2006, 80(15):7625-7635.
87. Hanhija¨rvi KJ, Ziedaite G, Pietila¨ MK, Haeggstrom E, Bamford DH. DNA ejection from an archaeal virus-a single-molecule approach. Biophys J 2013, 104(10):2264-2272.
88. Molineux IJ. Fifty-three years since Hershey and Chase; much ado about pressure but which pressure is it?. Virology 2006, 344(1):221-229.
89. Gonzalez-Huici V, Salas M, Hermoso JM. The push-pull mechanism of bacteriophage O29 DNA injection. Mol Microbiol 2004, 52(2):529-540.
90. Gonzalez-Huici V, Salas M, Hermoso JM. Requirements for Bacillus subtilis bacteriophage phi29 DNA ejection. Gene 2006, 374:19-25.
91. Gogliettino M, Balestrieri M, Pocsfalvi G, Fiume I, Natale L, Rossi M, Palmieri G. A highly selective oligopeptide binding protein from the archaeon Sulfolobus solfataricus. J Bacteriol 2010, 192(12):3123-3131.
92. Bauer DW, Huffman JB, Homa FL, Evilevitch A. Herpes virus genome, the pressure is on. J Am Chem Soc 2013, 135(30):11216-11221.
93. Snider J, Houry WA. MoxR AAA+ ATPases: a novel family of molecular chaperones?. J Struct Biol 2006, 156(1):200-209.
94. Wong KS, Houry WA. Novel structural and functional insights into the MoxR family of AAA+ ATPases. J Struct Biol 2012, 179(2):211-221.