Loading strategies of ring-shaped nucleic acid translocases and helicases

Current Opinion in Structural Biology

Volumn 25, Issue , 2014, Pages 16-24

  O'Shea, Valerie L ^a   Berger, James M ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CHAPERONE; DNA; HELICASE; NUCLEIC ACID; NUCLEOSIDE TRIPHOSPHATE; OLIGONUCLEOTIDE; RING SHAPED NUCLEIC ACID TRANSLOCASE; RNA; UNCLASSIFIED DRUG; DNA HELICASE;

CATALYSIS; CHROMOSOME; ENZYME LOADING; ENZYME SUBSTRATE; ENZYMOLOGY; GENE REPLICATION; GENETIC TRANSCRIPTION; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW;

DNA HELICASES; MOLECULAR CHAPERONES; NUCLEOBASE, NUCLEOSIDE, NUCLEOTIDE, AND NUCLEIC ACID TRANSPORT PROTEINS;

EID: 84890724459     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.11.006     Document Type: Review

References (90)

1. Singleton M.R., Dillingham M.S., Wigley D.B. Structure and mechanism of helicases and nucleic acid translocases. Annu Rev Biochem 2007, 76:23-50.
2. Enemark E.J., Joshua-Tor L. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 2006, 442:270-275.
3. Thomsen N.D., Berger J.M. Running in reverse: the structural basis for translocation polarity in hexameric helicases. Cell 2009, 139:523-534.
4. Itsathitphaisarn O., Wing R.A., Eliason W.K., Wang J., Steitz T.A. The hexameric helicase DnaB adopts a nonplanar conformation during translocation. Cell 2012, 151:267-277.
5. 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.
6. Davey M.J., O'Donnell M. Replicative helicase loaders: ring breakers and ring makers. Curr Biol 2003, 13:R594-R596.
7. Iyer L.M., Leipe D.D., Koonin E.V., Aravind L. Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol 2004, 146:11-31.
8. Iyer L.M., Makarova K.S., Koonin E.V., 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, 32:5260-5279.
9. Massey T.H., Mercogliano C.P., Yates J., Sherratt D.J., Lowe J. Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol Cell 2006, 23:457-469.
10. Duderstadt K.E., Berger J.M. AAA+ ATPases in the initiation of DNA replication. Crit Rev Biochem Mol Biol 2008, 43:163-187.
11. Demarre G., Galli E., Barre F.X. The FtsK family of DNA pumps. Adv Exp Med Biol 2013, 767:245-262.
12. Aussel L., Barre F.X., Aroyo M., Stasiak A., Stasiak A.Z., Sherratt D. FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 2002, 108:195-205.
13. 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.
14. Crozat E., Grainge I. FtsK DNA translocase: the fast motor that knows where it's going. Chembiochem 2010, 11:2232-2243.
15. Ben-Yehuda S., Rudner D.Z., Losick R. Assembly of the SpoIIIE DNA translocase depends on chromosome trapping in Bacillus subtilis. Curr Biol 2003, 13:2196-2200.
16. Levy O., Ptacin J.L., Pease P.J., Gore J., Eisen M.B., Bustamante C., Cozzarelli N.R. Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc Natl Acad Sci U S A 2005, 102:17618-17623.
17. Bigot S., Saleh O.A., Cornet F., Allemand J.F., Barre F.X. Oriented loading of FtsK on KOPS. Nat Struct Mol Biol 2006, 13:1026-1028.
18. Graham J.E., Sherratt D.J., Szczelkun M.D. Sequence-specific assembly of FtsK hexamers establishes directional translocation on DNA. Proc Natl Acad Sci U S A 2010, 107:20263-20268.
19. Lowe J., Ellonen A., Allen M.D., Atkinson C., Sherratt D.J., Grainge I. Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol Cell 2008, 31:498-509.
20. Hickman A.B., Dyda F. Binding and unwinding: SF3 viral helicases. Curr Opin Struct Biol 2005, 15:77-85.
21. Li D., Zhao R., Lilyestrom W., Gai D., Zhang R., DeCaprio J.A., Fanning E., Jochimiak A., Szakonyi G., Chen X.S. Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. Nature 2003, 423:512-518.
22. Gai D., Zhao R., Li D., Finkielstein C.V., Chen X.S. Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 2004, 119:47-60.
23. Bochkareva E., Martynowski D., Seitova A., Bochkarev A. Structure of the origin-binding domain of simian virus 40 large T antigen bound to DNA. Embo J 2006, 25:5961-5969.
24. Meinke G., Phelan P., Moine S., Bochkareva E., Bochkarev A., Bullock P.A., Bohm A. The crystal structure of the SV40 T-antigen origin binding domain in complex with DNA. PLoS Biol 2007, 5:e23.
25. Yardimci H., Wang X., Loveland A.B., Tappin I., Rudner D.Z., Hurwitz J., van Oijen A.M., Walter J.C. Bypass of a protein barrier by a replicative DNA helicase. Nature 2012, 492:205-209.
26. Chang Y.P., Xu M., Machado A.C., Yu X.J., Rohs R., Chen X.S. Mechanism of origin DNA recognition and assembly of an initiator-helicase complex by SV40 large tumor antigen. Cell Rep 2013, 3:1117-1127.
27. Bergvall M., Melendy T., Archambault J. The E1 proteins. Virology 2013, 445:35-56.
28. Enemark E.J., Stenlund A., Joshua-Tor L. Crystal structures of two intermediates in the assembly of the papillomavirus replication initiation complex. Embo J 2002, 21:1487-1496.
29. Abbate E.A., Berger J.M., Botchan M.R. The X-ray structure of the papillomavirus helicase in complex with its molecular matchmaker E2. Genes Dev 2004, 18:1981-1996.
30. Schuck S., Stenlund A. Assembly of a double hexameric helicase. Mol Cell 2005, 20:377-389.
31. Schuck S., Stenlund A. Mechanistic analysis of local ori melting and helicase assembly by the papillomavirus E1 protein. Mol Cell 2011, 43:776-787.
32. Peters J.M., Vangeloff A.D., Landick R. Bacterial transcription terminators: the RNA 3'-end chronicles. J Mol Biol 2011, 412:793-813.
33. Richardson J.P. Loading Rho to terminate transcription. Cell 2003, 114:157-159.
34. McSwiggen J.A., Bear D.G., von Hippel P.H. Interactions of Escherichia coli transcription termination factor rho with RNA. I. Binding stoichiometries and free energies. J Mol Biol 1988, 199:609-622.
35. Gogol E.P., Seifried S.E., von Hippel P.H. Structure and assembly of the Escherichia coli transcription termination factor rho and its interaction with RNA. I. Cryoelectron microscopic studies. J Mol Biol 1991, 221:1127-1138.
36. Yu X., Horiguchi T., Shigesada K., Egelman E.H. Three-dimensional reconstruction of transcription termination factor rho: orientation of the N-terminal domain and visualization of an RNA-binding site. J Mol Biol 2000, 299:1279-1287.
37. Skordalakes E., Berger J.M. Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading. Cell 2003, 114:135-146.
38. Kim D.E., Patel S.S. The kinetic pathway of RNA binding to the Escherichia coli transcription termination factor Rho. J Biol Chem 2001, 276:13902-13910.
39. Patel S.S., Picha K.M. Structure and function of hexameric helicases. Annu Rev Biochem 2000, 69:651-697.
40. Patel S.S., Hingorani M.M. Oligomeric structure of bacteriophage T7 DNA primase/helicase proteins. J Biol Chem 1993, 268:10668-10675.
41. Matson S.W., Richardson C.C. Nucleotide-dependent binding of the gene 4 protein of bacteriophage T7 to single-stranded DNA. J Biol Chem 1985, 260:2281-2287.
42. Egelman E.H., Yu X., Wild R., Hingorani M.M., Patel S.S. Bacteriophage T7 helicase/primase proteins form rings around single-stranded DNA that suggest a general structure for hexameric helicases. Proc Natl Acad Sci U S A 1995, 92:3869-3873.
43. Crampton D.J., Ohi M., Qimron U., Walz T., Richardson C.C. Oligomeric states of bacteriophage T7 gene 4 primase/helicase. J Mol Biol 2006, 360:667-677.
44. Singleton M.R., Sawaya M.R., Ellenberger T., Wigley D.B. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell 2000, 101:589-600.
45. Toth E.A., Li Y., Sawaya M.R., Cheng Y., Ellenberger T. The crystal structure of the bifunctional primase-helicase of bacteriophage T7. Mol Cell 2003, 12:1113-1123.
46. Guo S., Tabor S., Richardson C.C. The linker region between the helicase and primase domains of the bacteriophage T7 gene 4 protein is critical for hexamer formation. J Biol Chem 1999, 274:30303-30309.
47. Ahnert P., Picha K.M., Patel S.S. A ring-opening mechanism for DNA binding in the central channel of the T7 helicase-primase protein. Embo J 2000, 19:3418-3427.
48. Sawaya M.R., Guo S., Tabor S., Richardson C.C., Ellenberger T. Crystal structure of the helicase domain from the replicative helicase-primase of bacteriophage T7. Cell 1999, 99:167-177.
49. Robinson A., van Oijen A.M. Bacterial replication, transcription and translation: mechanistic insights from single-molecule biochemical studies. Nat Rev Microbiol 2013, 11:303-315.
50. Yu X., Jezewska M.J., Bujalowski W., Egelman E.H. The hexameric E. coli DnaB helicase can exist in different Quaternary states. J Mol Biol 1996, 259:7-14.
51. San Martin C., Radermacher M., Wolpensinger B., Engel A., Miles C.S., Dixon N.E., Carazo J.M. Three-dimensional reconstructions from cryoelectron microscopy images reveal an intimate complex between helicase DnaB and its loading partner DnaC. Structure 1998, 6:501-509.
52. San Martin M.C., Stamford N.P., Dammerova N., Dixon N.E., Carazo J.M. A structural model for the Escherichia coli DnaB helicase based on electron microscopy data. J Struct Biol 1995, 114:167-176.
53. Bailey S., Eliason W.K., Steitz T.A. Structure of hexameric DnaB helicase and its complex with a domain of DnaG primase. Science 2007, 318:459-463.
54. Wang G., Klein M.G., Tokonzaba E., Zhang Y., Holden L.G., Chen X.S. The structure of a DnaB-family replicative helicase and its interactions with primase. Nat Struct Mol Biol 2008, 15:94-100.
55. Lo Y.H., Tsai K.L., Sun Y.J., Chen W.T., Huang C.Y., Hsiao C.D. The crystal structure of a replicative hexameric helicase DnaC and its complex with single-stranded DNA. Nucleic Acids Res 2009, 37:804-814.
56. Barcena M., Martin C.S., Weise F., Ayora S., Alonso J.C., Carazo J.M. Polymorphic quaternary organization of the Bacillus subtilis bacteriophage SPP1 replicative helicase (G40 P). J Mol Biol 1998, 283:809-819.
57. Biswas T., Tsodikov O.V. Hexameric ring structure of the N-terminal domain of Mycobacterium tuberculosis DnaB helicase. FEBS J 2008, 275:3064-3071.
58. Yang S., Yu X., VanLoock M.S., Jezewska M.J., Bujalowski W., Egelman E.H. Flexibility of the rings: structural asymmetry in the DnaB hexameric helicase. J Mol Biol 2002, 321:839-849.
59. Kobori J.A., Kornberg A. The Escherichia coli dnaC gene product. III. Properties of the dnaB-dnaC protein complex. J Biol Chem 1982, 257:13770-13775.
60. Wickner S., Hurwitz J. Interaction of Escherichia coli dnaB and dnaC(D) gene products in vitro. Proc Natl Acad Sci U S A 1975, 72:921-925.
61. Davey M.J., Fang L., McInerney P., Georgescu R.E., O'Donnell M. The DnaC helicase loader is a dual ATP/ADP switch protein. Embo J 2002, 21:3148-3159.
62. Kobori J.A., Kornberg A. The Escherichia coli dnaC gene product. II. Purification, physical properties, and role in replication. J Biol Chem 1982, 257:13763-13769.
63. Bramhill D., Kornberg A. Duplex opening by dnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell 1988, 52:743-755.
64. Arias-Palomo E., O'Shea V.L., Hood I.V., Berger J.M. The bacterial DnaC helicase loader is a DnaB ring breaker. Cell 2013, 153:438-448.
65. Mott M.L., Erzberger J.P., Coons M.M., Berger J.M. Structural synergy and molecular crosstalk between bacterial helicase loaders and replication initiators. Cell 2008, 135:623-634.
66. Kelch B.A., Makino D.L., O'Donnell M., Kuriyan J. Clamp loader ATPases and the evolution of DNA replication machinery. BMC Biol 2012, 10:34.
67. Marszalek J., Kaguni J.M. DnaA protein directs the binding of DnaB protein in initiation of DNA replication in Escherichia coli. J Biol Chem 1994, 269:4883-4890.
68. Seitz H., Weigel C., Messer W. The interaction domains of the DnaA and DnaB replication proteins of Escherichia coli. Mol Microbiol 2000, 37:1270-1279.
69. Ioannou C., Schaeffer P.M., Dixon N.E., Soultanas P. Helicase binding to DnaI exposes a cryptic DNA-binding site during helicase loading in Bacillus subtilis. Nucleic Acids Res 2006, 34:5247-5258.
70. Tsai K.L., Lo Y.H., Sun Y.J., Hsiao C.D. Molecular interplay between the replicative helicase DnaC and its loader protein DnaI from Geobacillus kaustophilus. J Mol Biol 2009, 393:1056-1069.
71. Velten M., McGovern S., Marsin S., Ehrlich S.D., Noirot P., Polard P. A two-protein strategy for the functional loading of a cellular replicative DNA helicase. Mol Cell 2003, 11:1009-1020.
72. Liu B., Eliason W.K., Steitz T.A. Structure of a helicase-helicase loader complex reveals insights into the mechanism of bacterial primosome assembly. Nat Commun 2013, 4:2495.
73. Mueser T.C., Jones C.E., Nossal N.G., Hyde C.C. Bacteriophage T4 gene 59 helicase assembly protein binds replication fork DNA. The 1.45 A resolution crystal structure reveals a novel alpha-helical two-domain fold. J Mol Biol 2000, 296:597-612.
74. Bailey S., Sedelnikova S.E., Mesa P., Ayora S., Waltho J.P., Ashcroft A.E., Baron A.J., Alonso J.C., Rafferty J.B. Structural analysis of Bacillus subtilis SPP1 phage helicase loader protein G39P. J Biol Chem 2003, 278:15304-15312.
75. Stelter M., Gutsche I., Kapp U., Bazin A., Bajic G., Goret G., Jamin M., Timmins J., Terradot L. Architecture of a dodecameric bacterial replicative helicase. Structure 2012, 20:554-564.
76. Soni R.K., Mehra P., Choudhury N.R., Mukhopadhyay G., Dhar S.K. Functional characterization of Helicobacter pylori DnaB helicase. Nucleic Acids Res 2003, 31:6828-6840.
77. Boos D., Frigola J., Diffley J.F. Activation of the replicative DNA helicase: breaking up is hard to do. Curr Opin Cell Biol 2012, 24:423-430.
78. Gai D., Chang Y.P., Chen X.S. Origin DNA melting and unwinding in DNA replication. Curr Opin Struct Biol 2010, 20:756-762.
79. Costa A., Ilves I., Tamberg N., Petojevic T., Nogales E., Botchan M.R., Berger J.M. The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat Struct Mol Biol 2011, 18:471-477.
80. Lyubimov A.Y., Costa A., Bleichert F., Botchan M.R., Berger J.M. ATP-dependent conformational dynamics underlie the functional asymmetry of the replicative helicase from a minimalist eukaryote. Proc Natl Acad Sci U S A 2012, 109:11999-12004.
81. Costa A., Onesti S. Structural biology of MCM helicases. Crit Rev Biochem Mol Biol 2009, 44:326-342.
82. Remus D., Diffley J.F. Eukaryotic DNA replication control: lock and load, then fire. Curr Opin Cell Biol 2009, 21:771-777.
83. Remus D., Beuron F., Tolun G., Griffith J.D., Morris E.P., Diffley J.F. Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 2009, 139:719-730.
84. Evrin C., Clarke P., Zech J., Lurz R., Sun J., Uhle S., Li H., Stillman B., Speck C. A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc Natl Acad Sci U S A 2009, 106:20240-20245.
85. Costa A., Hood I.V., Berger J.M. Mechanisms for initiating cellular DNA replication. Annu Rev Biochem 2013, 82:25-54.
86. Yardimci H., Loveland A.B., Habuchi S., van Oijen A.M., Walter J.C. Uncoupling of sister replisomes during eukaryotic DNA replication. Mol Cell 2010, 40:834-840.
87. Fu Y.V., Yardimci H., Long D.T., Ho T.V., Guainazzi A., Bermudez V.P., Hurwitz J., van Oijen A., Scharer O.D., Walter J.C. Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 2011, 146:931-941.
88. Labib K., Tercero J.A., Diffley J.F. Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 2000, 288:1643-1647.
89. Bochman M.L., Bell S.P., Schwacha A. Subunit organization of MCM2-7 and the unequal role of active sites in ATP hydrolysis and viability. Mol Cell Biol 2008, 28:5865-5873.
90. Sun J., Evrin C., Samel S.A., Fernandez-Cid A., Riera A., Kawakami H., Stillman B., Speck C., Li H. Cryo-EM structure of a helicase loading intermediate containing ORC-Cdc6-Cdt1-MCM2-7 bound to DNA. Nat Struct Mol Biol 2013, 20:944-951.