Structure and operation of the DNA-translocating type I DNA restriction enzymes

Christopher K. Kennaway; James E. Taylor; Chun Feng Song; Wojciech Potrzebowski; William Nicholson; John H. White; Anna Swiderska; Agnieszka Obarska-Kosinska; Philip Callow; Laurie P. Cooper; Gareth A. Roberts; Jean-Baptiste Artero; Janusz M. Bujnicki; John Trinick; G. Geoff Kneale; David T.F. Dryden

doi:10.1101/gad.179085.111

Structure and operation of the DNA-translocating type I DNA restriction enzymes

Christopher K. Kennaway, James E. Taylor, Chun Feng Song, Wojciech Potrzebowski, William Nicholson, John H. White, Anna Swiderska, Agnieszka Obarska-Kosinska, Philip Callow, Laurie P. Cooper, Gareth A. Roberts, Jean-Baptiste Artero, Janusz M. Bujnicki, John Trinick, G. Geoff Kneale, David T.F. Dryden (Lead / Corresponding author)

Research output: Contribution to journal › Article › peer-review

46 Citations (Scopus)

Abstract

Type I DNA restriction/modification (RM) enzymes are molecular machines found in the majority of bacterial species. Their early discovery paved the way for the development of genetic engineering. They control (restrict) the influx of foreign DNA via horizontal gene transfer into the bacterium while maintaining sequence-specific methylation (modification) of host DNA. The endonuclease reaction of these enzymes on unmethylated DNA is preceded by bidirectional translocation of thousands of base pairs of DNA toward the enzyme. We present the structures of two type I RM enzymes, EcoKI and EcoR124I, derived using electron microscopy (EM), small-angle scattering (neutron and X-ray), and detailed molecular modeling. DNA binding triggers a large contraction of the open form of the enzyme to a compact form. The path followed by DNA through the complexes is revealed by using a DNA mimic anti-restriction protein. The structures reveal an evolutionary link between type I RM enzymes and type II RM enzymes.

Original language	English
Pages (from-to)	92-104
Number of pages	13
Journal	Genes and Development
Volume	26
DOIs	https://doi.org/10.1101/gad.179085.111
Publication status	Published - 2012

Keywords

DNA restriction enzymes
DNA TRANSLOCATION
electron microscopy
small-angle scattering
Molecular modeling
DNA translocases

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Kennaway, C. K., Taylor, J. E., Song, C. F., Potrzebowski, W., Nicholson, W., White, J. H., Swiderska, A., Obarska-Kosinska, A., Callow, P., Cooper, L. P., Roberts, G. A., Artero, J.-B., Bujnicki, J. M., Trinick, J., Kneale, G. G., & Dryden, D. T. F. (2012). Structure and operation of the DNA-translocating type I DNA restriction enzymes. Genes and Development, 26, 92-104. https://doi.org/10.1101/gad.179085.111

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title = "Structure and operation of the DNA-translocating type I DNA restriction enzymes",

abstract = "Type I DNA restriction/modification (RM) enzymes are molecular machines found in the majority of bacterial species. Their early discovery paved the way for the development of genetic engineering. They control (restrict) the influx of foreign DNA via horizontal gene transfer into the bacterium while maintaining sequence-specific methylation (modification) of host DNA. The endonuclease reaction of these enzymes on unmethylated DNA is preceded by bidirectional translocation of thousands of base pairs of DNA toward the enzyme. We present the structures of two type I RM enzymes, EcoKI and EcoR124I, derived using electron microscopy (EM), small-angle scattering (neutron and X-ray), and detailed molecular modeling. DNA binding triggers a large contraction of the open form of the enzyme to a compact form. The path followed by DNA through the complexes is revealed by using a DNA mimic anti-restriction protein. The structures reveal an evolutionary link between type I RM enzymes and type II RM enzymes. ",

keywords = "DNA restriction enzymes, DNA TRANSLOCATION, electron microscopy, small-angle scattering, Molecular modeling, DNA translocases",

author = "Kennaway, {Christopher K.} and Taylor, {James E.} and Song, {Chun Feng} and Wojciech Potrzebowski and William Nicholson and White, {John H.} and Anna Swiderska and Agnieszka Obarska-Kosinska and Philip Callow and Cooper, {Laurie P.} and Roberts, {Gareth A.} and Jean-Baptiste Artero and Bujnicki, {Janusz M.} and John Trinick and Kneale, {G. Geoff} and Dryden, {David T.F.}",

year = "2012",

doi = "10.1101/gad.179085.111",

language = "English",

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journal = "Genes and Development",

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publisher = "Cold Spring Harbor Laboratory Press",

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Kennaway, CK, Taylor, JE, Song, CF, Potrzebowski, W, Nicholson, W, White, JH, Swiderska, A, Obarska-Kosinska, A, Callow, P, Cooper, LP, Roberts, GA, Artero, J-B, Bujnicki, JM, Trinick, J, Kneale, GG & Dryden, DTF 2012, 'Structure and operation of the DNA-translocating type I DNA restriction enzymes', Genes and Development, vol. 26, pp. 92-104. https://doi.org/10.1101/gad.179085.111

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T1 - Structure and operation of the DNA-translocating type I DNA restriction enzymes

AU - Kennaway, Christopher K.

AU - Taylor, James E.

AU - Song, Chun Feng

AU - Potrzebowski, Wojciech

AU - Nicholson, William

AU - White, John H.

AU - Swiderska, Anna

AU - Obarska-Kosinska, Agnieszka

AU - Callow, Philip

AU - Cooper, Laurie P.

AU - Roberts, Gareth A.

AU - Artero, Jean-Baptiste

AU - Bujnicki, Janusz M.

AU - Trinick, John

AU - Kneale, G. Geoff

AU - Dryden, David T.F.

PY - 2012

Y1 - 2012

N2 - Type I DNA restriction/modification (RM) enzymes are molecular machines found in the majority of bacterial species. Their early discovery paved the way for the development of genetic engineering. They control (restrict) the influx of foreign DNA via horizontal gene transfer into the bacterium while maintaining sequence-specific methylation (modification) of host DNA. The endonuclease reaction of these enzymes on unmethylated DNA is preceded by bidirectional translocation of thousands of base pairs of DNA toward the enzyme. We present the structures of two type I RM enzymes, EcoKI and EcoR124I, derived using electron microscopy (EM), small-angle scattering (neutron and X-ray), and detailed molecular modeling. DNA binding triggers a large contraction of the open form of the enzyme to a compact form. The path followed by DNA through the complexes is revealed by using a DNA mimic anti-restriction protein. The structures reveal an evolutionary link between type I RM enzymes and type II RM enzymes.

AB - Type I DNA restriction/modification (RM) enzymes are molecular machines found in the majority of bacterial species. Their early discovery paved the way for the development of genetic engineering. They control (restrict) the influx of foreign DNA via horizontal gene transfer into the bacterium while maintaining sequence-specific methylation (modification) of host DNA. The endonuclease reaction of these enzymes on unmethylated DNA is preceded by bidirectional translocation of thousands of base pairs of DNA toward the enzyme. We present the structures of two type I RM enzymes, EcoKI and EcoR124I, derived using electron microscopy (EM), small-angle scattering (neutron and X-ray), and detailed molecular modeling. DNA binding triggers a large contraction of the open form of the enzyme to a compact form. The path followed by DNA through the complexes is revealed by using a DNA mimic anti-restriction protein. The structures reveal an evolutionary link between type I RM enzymes and type II RM enzymes.

KW - DNA restriction enzymes

KW - DNA TRANSLOCATION

KW - electron microscopy

KW - small-angle scattering

KW - Molecular modeling

KW - DNA translocases

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U2 - 10.1101/gad.179085.111

DO - 10.1101/gad.179085.111

M3 - Article

SN - 0890-9369

VL - 26

SP - 92

EP - 104

JO - Genes and Development

JF - Genes and Development

ER -

Structure and operation of the DNA-translocating type I DNA restriction enzymes

Abstract

Keywords

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