Home LiteratureArticle Details
PMID: 18329872 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

On helicases and other motor proteins.

Current opinion in structural biology ·Vol. 18 ·No. 2 ·2008-04-00 ·Pages 243-57

Enemark EJ, Joshua-Tor L

Abstract

Helicases are molecular machines that utilize energy derived from ATP hydrolysis to move along nucleic acids and to separate base-paired nucleotides. The movement of the helicase can also be described as a stationary helicase that pumps nucleic acid. Recent structural data for the hexameric E1 helicase of papillomavirus in complex with single-stranded DNA and MgADP has provided a detailed atomic and mechanistic picture of its ATP-driven DNA translocation. The structural and mechanistic features of this helicase are compared with the hexameric helicase prototypes T7gp4 and SV40 T-antigen. The ATP-binding site architectures of these proteins are structurally similar to the sites of other prototypical ATP-driven motors such as F1-ATPase, suggesting related roles for the individual site residues in the ATPase activity.

MeSH Terms
Adenosine Triphosphate/metabolism Amino Acid Sequence Animals Binding Sites DNA/chemistry,metabolism DNA Helicases/chemistry,metabolism Molecular Motor Proteins/metabolism Molecular Sequence Data RNA Helicases/chemistry,metabolism
Chemicals
Molecular Motor Proteins Adenosine Triphosphate DNA DNA Helicases RNA Helicases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Enemark Eric J
W.M. Keck Structural Biology Laboratory, Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, United States.
Joshua-Tor Leemor
References (94)
94 references, click to expand
  1. The crystal structure of the bifunctional primase-helicase of bacteriophage T7.
    Mol Cell. 2003 Nov;12(5):1113-23 PMID: 14636571
  2. Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen.
    Nature. 2003 May 29;423(6939):512-8 PMID: 12774115
  3. The crystal structure of the Thermus aquaticus DnaB helicase monomer.
    Nucleic Acids Res. 2007;35(14):4728-36 PMID: 17606462
  4. Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation.
    Cell. 2004 Sep 17;118(6):743-55 PMID: 15369673
  5. Structure of hexameric DnaB helicase and its complex with a domain of DnaG primase.
    Science. 2007 Oct 19;318(5849):459-63 PMID: 17947583
  6. 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 Apr 25;92(9):3869-73 PMID: 7731998
  7. Identification of domains of the human papillomavirus type 11 E1 helicase involved in oligomerization and binding to the viral origin.
    J Virol. 2000 Aug;74(16):7349-61 PMID: 10906188
  8. Oligomeric structure of Escherichia coli primary replicative helicase DnaB protein.
    J Biol Chem. 1994 Dec 16;269(50):31350-8 PMID: 7989299
  9. ATP activates dnaA protein in initiating replication of plasmids bearing the origin of the E. coli chromosome.
    Cell. 1987 Jul 17;50(2):259-65 PMID: 3036372
  10. Rebuilt AAA + motors reveal operating principles for ATP-fuelled machines.
    Nature. 2005 Oct 20;437(7062):1115-20 PMID: 16237435
  11. Oligomeric structure of bacteriophage T7 DNA primase/helicase proteins.
    J Biol Chem. 1993 May 15;268(14):10668-75 PMID: 8486715
  12. The structural basis for regulated assembly and function of the transcriptional activator NtrC.
    Genes Dev. 2006 Jun 1;20(11):1485-95 PMID: 16751184
  13. Evolutionary history and higher order classification of AAA+ ATPases.
    J Struct Biol. 2004 Apr-May;146(1-2):11-31 PMID: 15037234
  14. Roles of Mcm7 and Mcm4 subunits in the DNA helicase activity of the mouse Mcm4/6/7 complex.
    J Biol Chem. 2002 Nov 8;277(45):42471-9 PMID: 12207017
  15. Crystal structure of the processivity clamp loader gamma (gamma) complex of E. coli DNA polymerase III.
    Cell. 2001 Aug 24;106(4):429-41 PMID: 11525729
  16. The hexameric E. coli DnaB helicase can exist in different Quaternary states.
    J Mol Biol. 1996 May 31;259(1):7-14 PMID: 8648650
  17. Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen.
    Cell. 2004 Oct 1;119(1):47-60 PMID: 15454080
  18. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes.
    Genome Res. 1999 Jan;9(1):27-43 PMID: 9927482
  19. Minichromosome maintenance helicase activity is controlled by N- and C-terminal motifs and requires the ATPase domain helix-2 insert.
    Proc Natl Acad Sci U S A. 2006 May 16;103(20):7613-8 PMID: 16679413
  20. Biochemical analysis of the intrinsic Mcm4-Mcm6-mcm7 DNA helicase activity.
    Mol Cell Biol. 1999 Dec;19(12):8003-15 PMID: 10567526
  21. Hexameric ring structure of the full-length archaeal MCM protein complex.
    EMBO Rep. 2003 Nov;4(11):1079-83 PMID: 14566326
  22. Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading.
    Cell. 2003 Jul 11;114(1):135-46 PMID: 12859904
  23. The papillomavirus E1 protein forms a DNA-dependent hexameric complex with ATPase and DNA helicase activities.
    J Virol. 1998 Aug;72(8):6893-7 PMID: 9658141
  24. High-resolution structure of the E.coli RecQ helicase catalytic core.
    EMBO J. 2003 Oct 1;22(19):4910-21 PMID: 14517231
  25. Reconstitution of the Mcm2-7p heterohexamer, subunit arrangement, and ATP site architecture.
    J Biol Chem. 2003 Feb 14;278(7):4491-9 PMID: 12480933
  26. Structure of the ATP-dependent oligomerization domain of N-ethylmaleimide sensitive factor complexed with ATP.
    Nat Struct Biol. 1998 Sep;5(9):803-11 PMID: 9731775
  27. A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase.
    Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1530-5 PMID: 10677495
  28. The binding change mechanism for ATP synthase--some probabilities and possibilities.
    Biochim Biophys Acta. 1993 Jan 8;1140(3):215-50 PMID: 8417777
  29. Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair.
    EMBO J. 1999 Dec 15;18(24):6899-907 PMID: 10601012
  30. A hexameric helicase encircles one DNA strand and excludes the other during DNA unwinding.
    Biochemistry. 1997 Nov 18;36(46):14080-7 PMID: 9369480
  31. Organization of the archaeal MCM complex on DNA and implications for the helicase mechanism.
    Nat Struct Mol Biol. 2005 Sep;12(9):756-62 PMID: 16116441
  32. Interactions of Escherichia coli primary replicative helicase DnaB protein with single-stranded DNA. The nucleic acid does not wrap around the protein hexamer.
    Biochemistry. 1995 Jul 11;34(27):8513-9 PMID: 7612593
  33. Mcm4,6,7 uses a "pump in ring" mechanism to unwind DNA by steric exclusion and actively translocate along a duplex.
    J Biol Chem. 2003 Dec 5;278(49):49171-82 PMID: 13679365
  34. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa.
    Cell. 2006 Apr 21;125(2):287-300 PMID: 16630817
  35. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism.
    Cell. 1999 Apr 2;97(1):75-84 PMID: 10199404
  36. Six molecules of SV40 large T antigen assemble in a propeller-shaped particle around a channel.
    J Mol Biol. 1997 Apr 25;268(1):15-20 PMID: 9149137
  37. Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex.
    Nature. 2004 Jun 17;429(6993):724-30 PMID: 15201901
  38. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps.
    Acta Crystallogr D Biol Crystallogr. 1999 Apr;55(Pt 4):938-40 PMID: 10089341
  39. The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation.
    EMBO J. 2002 Sep 16;21(18):4763-73 PMID: 12234917
  40. A structural model for the Escherichia coli DnaB helicase based on electron microscopy data.
    J Struct Biol. 1995 May-Jun;114(3):167-76 PMID: 7662485
  41. Crystal structures of two intermediates in the assembly of the papillomavirus replication initiation complex.
    EMBO J. 2002 Mar 15;21(6):1487-96 PMID: 11889054
  42. Crystal structure of the hexamerization domain of N-ethylmaleimide-sensitive fusion protein.
    Cell. 1998 Aug 21;94(4):525-36 PMID: 9727495
  43. Adjacent residues in the E1 initiator beta-hairpin define different roles of the beta-hairpin in Ori melting, helicase loading, and helicase activity.
    Mol Cell. 2007 Mar 23;25(6):825-37 PMID: 17386260
  44. A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex.
    J Biol Chem. 1997 Sep 26;272(39):24508-13 PMID: 9305914
  45. Crystal structure of the DNA nucleotide excision repair enzyme UvrB from Thermus thermophilus.
    Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):11717-22 PMID: 10518516
  46. Cooperative mechanism of RNA packaging motor.
    J Biol Chem. 2005 Jun 17;280(24):23157-64 PMID: 15840563
  47. Biochemical and electron microscopic image analysis of the hexameric E1 helicase.
    J Biol Chem. 1999 Feb 12;274(7):4447-58 PMID: 9933649
  48. Isolation and characterization of various complexes of the minichromosome maintenance proteins of Schizosaccharomyces pombe.
    J Biol Chem. 2000 Jun 23;275(25):18871-8 PMID: 10770926
  49. The structure of a DnaB-family replicative helicase and its interactions with primase.
    Nat Struct Mol Biol. 2008 Jan;15(1):94-100 PMID: 18157148
  50. DNA is bound within the central hole to one or two of the six subunits of the T7 DNA helicase.
    Nat Struct Biol. 1996 Sep;3(9):740-3 PMID: 8784344
  51. Demonstration of unidirectional single-stranded DNA translocation by PcrA helicase: measurement of step size and translocation speed.
    Biochemistry. 2000 Jan 11;39(1):205-12 PMID: 10625495
  52. Mechanisms of a ring shaped helicase.
    Nucleic Acids Res. 2006;34(15):4216-24 PMID: 16935879
  53. The arginine finger of bacteriophage T7 gene 4 helicase: role in energy coupling.
    Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4373-8 PMID: 15070725
  54. Raster3D: photorealistic molecular graphics.
    Methods Enzymol. 1997;277:505-24 PMID: 18488322
  55. The structure and function of MCM from archaeal M. Thermoautotrophicum.
    Nat Struct Biol. 2003 Mar;10(3):160-7 PMID: 12548282
  56. Structural basis for DNA recognition and processing by UvrB.
    Nat Struct Mol Biol. 2006 Apr;13(4):360-4 PMID: 16532007
  57. Functional and structural heterogeneity of the DNA binding site of the Escherichia coli primary replicative helicase DnaB protein.
    J Biol Chem. 1998 Apr 10;273(15):9058-69 PMID: 9535894
  58. The bacterial replicative helicase DnaB evolved from a RecA duplication.
    Genome Res. 2000 Jan;10(1):5-16 PMID: 10645945
  59. Assembly of a double hexameric helicase.
    Mol Cell. 2005 Nov 11;20(3):377-89 PMID: 16285920
  60. Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria.
    Nature. 1994 Aug 25;370(6491):621-8 PMID: 8065448
  61. ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication.
    Nature. 1989 Apr 20;338(6217):658-62 PMID: 2539565
  62. PcrA helicase, a prototype ATP-driven molecular motor.
    Structure. 2006 Sep;14(9):1345-53 PMID: 16962966
  63. The molecular architecture of the metalloprotease FtsH.
    Proc Natl Acad Sci U S A. 2006 Feb 28;103(9):3066-71 PMID: 16484367
  64. The roles of the residues on the channel beta-hairpin and loop structures of simian virus 40 hexameric helicase.
    Proc Natl Acad Sci U S A. 2005 Aug 9;102(32):11248-53 PMID: 16061814
  65. Differences in the single-stranded DNA binding activities of MCM2-7 and MCM467: MCM2 and MCM5 define a slow ATP-dependent step.
    J Biol Chem. 2007 Nov 16;282(46):33795-33804 PMID: 17895243
  66. ATP-dependent minor groove recognition of TA base pairs is required for template melting by the E1 initiator protein.
    J Virol. 2007 Apr;81(7):3293-302 PMID: 17202221
  67. Structural basis for DNA duplex separation by a superfamily-2 helicase.
    Nat Struct Mol Biol. 2007 Jul;14(7):647-52 PMID: 17558417
  68. Crystal structure of the helicase domain from the replicative helicase-primase of bacteriophage T7.
    Cell. 1999 Oct 15;99(2):167-77 PMID: 10535735
  69. Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP.
    Cell. 1997 Aug 22;90(4):635-47 PMID: 9288744
  70. DNA-induced switch from independent to sequential dTTP hydrolysis in the bacteriophage T7 DNA helicase.
    Mol Cell. 2006 Jan 20;21(2):165-74 PMID: 16427007
  71. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides.
    Cell. 2000 Jun 9;101(6):589-600 PMID: 10892646
  72. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA.
    Cell. 2006 Aug 25;126(4):713-25 PMID: 16923391
  73. Mechanochemistry of t7 DNA helicase.
    J Mol Biol. 2005 Jul 15;350(3):452-75 PMID: 15950239
  74. Biochemical characterization of the Methanothermobacter thermautotrophicus minichromosome maintenance (MCM) helicase N-terminal domains.
    J Biol Chem. 2004 Jul 2;279(27):28358-66 PMID: 15100218
  75. Papillomavirus E1 helicase assembly maintains an asymmetric state in the absence of DNA and nucleotide cofactors.
    Nucleic Acids Res. 2007;35(19):6451-7 PMID: 17881379
  76. An extensively modified version of MolScript that includes greatly enhanced coloring capabilities.
    J Mol Graph Model. 1997 Apr;15(2):132-4, 112-3 PMID: 9385560
  77. Simian virus 40 T-antigen DNA helicase is a hexamer which forms a binary complex during bidirectional unwinding from the viral origin of DNA replication.
    J Virol. 1992 Feb;66(2):804-15 PMID: 1309914
  78. Crystal structure of the hepatitis C virus NS3 protease domain complexed with a synthetic NS4A cofactor peptide.
    Cell. 1996 Oct 18;87(2):343-55 PMID: 8861917
  79. Mechanism of DNA translocation in a replicative hexameric helicase.
    Nature. 2006 Jul 20;442(7100):270-5 PMID: 16855583
  80. Structure and mechanism of helicases and nucleic acid translocases.
    Annu Rev Biochem. 2007;76:23-50 PMID: 17506634
  81. The dTTPase mechanism of T7 DNA helicase resembles the binding change mechanism of the F1-ATPase.
    Proc Natl Acad Sci U S A. 1997 May 13;94(10):5012-7 PMID: 9144181
  82. ATP ground- and transition states of bacterial enhancer binding AAA+ ATPases support complex formation with their target protein, sigma54.
    Structure. 2007 Apr;15(4):429-40 PMID: 17437715
  83. The DEAD-box protein family of RNA helicases.
    Gene. 2006 Feb 15;367:17-37 PMID: 16337753
  84. The structure of bovine F1-ATPase inhibited by ADP and beryllium fluoride.
    EMBO J. 2004 Jul 21;23(14):2734-44 PMID: 15229653
  85. Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13080-5 PMID: 11087862
  86. The 3'-tail of a forked-duplex sterically determines whether one or two DNA strands pass through the central channel of a replication-fork helicase.
    J Mol Biol. 2000 Aug 11;301(2):285-99 PMID: 10926510
  87. Bovine papilloma virus (BPV)-encoded E1 protein contains multiple activities required for BPV DNA replication.
    Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):702-6 PMID: 8380645
  88. Crystal structure of the human AAA+ protein RuvBL1.
    J Biol Chem. 2006 Dec 15;281(50):38918-29 PMID: 17060327
  89. Organization and evolution of bacterial and bacteriophage primase-helicase systems.
    J Mol Evol. 1992 Apr;34(4):351-7 PMID: 1569588
  90. Common determinants in DNA melting and helicase-catalysed DNA unwinding by papillomavirus replication protein E1.
    Nucleic Acids Res. 2006 May 31;34(10):3008-19 PMID: 16738139
  91. Structural basis of mechanochemical coupling in a hexameric molecular motor.
    J Biol Chem. 2008 Feb 8;283(6):3607-3617 PMID: 18057007
  92. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke.
    Cell. 2006 Dec 29;127(7):1349-60 PMID: 17190599
  93. Interplay between an AAA module and an integrin I domain may regulate the function of magnesium chelatase.
    J Mol Biol. 2001 Aug 3;311(1):111-22 PMID: 11469861
  94. DNA binding and helicase actions of mouse MCM4/6/7 helicase.
    Nucleic Acids Res. 2005 May 25;33(9):3033-47 PMID: 15917436
Article Info
Journal
Current opinion in structural biology
Abbr.
Curr Opin Struct Biol
ISSN
0959-440X
Published
2008-04-00
Epub
2008-00-10
Pages
243-57
Language
English
Region
England
NLM ID
9107784
PMCID
PMC2396192
Subset
IM
Grants
NIAID NIH HHS · R01 AI046724 · United States
NIAID NIH HHS · R01 AI046724-06A2 · United States
NIAID NIH HHS · AI146724 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]