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Hpy188I-DNA pre- and post-cleavage complexes--snapshots of the GIY-YIG nuclease mediated catalysis.

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Sokolowska M, Czapinska H, Bochtler M
OpenAccess logo Nucleic Acids Res 39 1554-64 (2011)
Cited: 24 times
EuropePMC logo PMID: 20935048

Abstract

The GIY-YIG nuclease domain is present in all kingdoms of life and has diverse functions. It is found in the eukaryotic flap endonuclease and Holliday junction resolvase Slx1-Slx4, the prokaryotic nucleotide excision repair proteins UvrC and Cho, and in proteins of 'selfish' genetic elements. Here we present the structures of the ternary pre- and post-cleavage complexes of the type II GIY-YIG restriction endonuclease Hpy188I with DNA and a surrogate or catalytic metal ion, respectively. Our structures suggest that GIY-YIG nucleases catalyze DNA hydrolysis by a single substitution reaction. They are consistent with a previous proposal that a tyrosine residue (which we expect to occur in its phenolate form) acts as a general base for the attacking water molecule. In contrast to the earlier proposal, our data identify the general base with the GIY and not the YIG tyrosine. A conserved glutamate residue (Glu149 provided in trans in Hpy188I) anchors a single metal cation in the active site. This metal ion contacts the phosphate proS oxygen atom and the leaving group 3'-oxygen atom, presumably to facilitate its departure. Taken together, our data reveal striking analogy in the absence of homology between GIY-YIG and ββα-Me nucleases.

Articles - 3oqg mentioned but not cited (5)

  1. Hpy188I-DNA pre- and post-cleavage complexes--snapshots of the GIY-YIG nuclease mediated catalysis. Sokolowska M, Czapinska H, Bochtler M. Nucleic Acids Res. 39 1554-1564 (2011)
  2. Flexibility-rigidity index for protein-nucleic acid flexibility and fluctuation analysis. Opron K, Xia K, Burton Z, Wei GW. J Comput Chem 37 1283-1295 (2016)
  3. Divalent metal ion differentially regulates the sequential nicking reactions of the GIY-YIG homing endonuclease I-BmoI. Kleinstiver BP, Bérubé-Janzen W, Fernandes AD, Edgell DR. PLoS ONE 6 e23804 (2011)
  4. Holliday junction resolution by At-HIGLE: an SLX1 lineage endonuclease from Arabidopsis thaliana with a novel in-built regulatory mechanism. Verma P, Kumari P, Negi S, Yadav G, Gaur V. Nucleic Acids Res 50 4630-4646 (2022)
  5. Recognition and processing of branched DNA substrates by Slx1-Slx4 nuclease. Gaur V, Ziajko W, Nirwal S, Szlachcic A, Gapińska M, Nowotny M. Nucleic Acids Res. 47 11681-11690 (2019)


Reviews citing this publication (6)

  1. Type II restriction endonucleases--a historical perspective and more. Pingoud A, Wilson GG, Wende W. Nucleic Acids Res. 42 7489-7527 (2014)
  2. Homing endonucleases: from genetic anomalies to programmable genomic clippers. Belfort M, Bonocora RP. Methods Mol. Biol. 1123 1-26 (2014)
  3. Structural, functional and evolutionary relationships between homing endonucleases and proteins from their host organisms. Taylor GK, Stoddard BL. Nucleic Acids Res. 40 5189-5200 (2012)
  4. Structure and mechanism of nucleases regulated by SLX4. Nowotny M, Gaur V. Curr. Opin. Struct. Biol. 36 97-105 (2016)
  5. Holliday junction-resolving enzymes-structures and mechanisms. Lilley DMJ. FEBS Lett. 591 1073-1082 (2017)
  6. Exploring the Structures and Functions of Macromolecular SLX4-Nuclease Complexes in Genome Stability. Payliss BJ, Patel A, Sheppard AC, Wyatt HDM. Front Genet 12 784167 (2021)

Articles citing this publication (13)

  1. Highlights of the DNA cutters: a short history of the restriction enzymes. Loenen WA, Dryden DT, Raleigh EA, Wilson GG, Murray NE. Nucleic Acids Res. 42 3-19 (2014)
  2. Monomeric site-specific nucleases for genome editing. Kleinstiver BP, Wolfs JM, Kolaczyk T, Roberts AK, Hu SX, Edgell DR. Proc. Natl. Acad. Sci. U.S.A. 109 8061-8066 (2012)
  3. The endonuclease Ankle1 requires its LEM and GIY-YIG motifs for DNA cleavage in vivo. Brachner A, Braun J, Ghodgaonkar M, Castor D, Zlopasa L, Ehrlich V, Jiricny J, Gotzmann J, Knasmüller S, Foisner R. J. Cell. Sci. 125 1048-1057 (2012)
  4. Crystal structure and mechanism of action of the N6-methyladenine-dependent type IIM restriction endonuclease R.DpnI. Siwek W, Czapinska H, Bochtler M, Bujnicki JM, Skowronek K. Nucleic Acids Res. 40 7563-7572 (2012)
  5. A sequence-specific DNA glycosylase mediates restriction-modification in Pyrococcus abyssi. Miyazono K, Furuta Y, Watanabe-Matsui M, Miyakawa T, Ito T, Kobayashi I, Tanokura M. Nat Commun 5 3178 (2014)
  6. Structural and Mechanistic Analysis of the Slx1-Slx4 Endonuclease. Gaur V, Wyatt HDM, Komorowska W, Szczepanowski RH, de Sanctis D, Gorecka KM, West SC, Nowotny M. Cell Rep 10 1467-1476 (2015)
  7. The monomeric GIY-YIG homing endonuclease I-BmoI uses a molecular anchor and a flexible tether to sequentially nick DNA. Kleinstiver BP, Wolfs JM, Edgell DR. Nucleic Acids Res. 41 5413-5427 (2013)
  8. Perpetuating the homing endonuclease life cycle: identification of mutations that modulate and change I-TevI cleavage preference. Roy AC, Wilson GG, Edgell DR. Nucleic Acids Res. 44 7350-7359 (2016)
  9. Structure specific DNA recognition by the SLX1-SLX4 endonuclease complex. Xu X, Wang M, Sun J, Yu Z, Li G, Yang N, Xu RM. Nucleic Acids Res 49 7740-7752 (2021)
  10. Distortion of double-stranded DNA structure by the binding of the restriction DNA glycosylase R.PabI. Miyazono KI, Wang D, Ito T, Tanokura M. Nucleic Acids Res 48 5106-5118 (2020)
  11. Biochemical and mechanistic analysis of the cleavage of branched DNA by human ANKLE1. Freeman ADJ, Déclais AC, Wilson TJ, Lilley DMJ. Nucleic Acids Res 51 5743-5754 (2023)
  12. Crystal structure and DNA cleavage mechanism of the restriction DNA glycosylase R.CcoLI from Campylobacter coli. Miyazono KI, Wang D, Ito T, Tanokura M. Sci Rep 11 859 (2021)
  13. Tetrameric structure of the restriction DNA glycosylase R.PabI in complex with nonspecific double-stranded DNA. Wang D, Miyazono KI, Tanokura M. Sci Rep 6 35197 (2016)


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