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Atomic structures and functional implications of the archaeal RecQ-like helicase Hjm.

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Oyama T, Oka H, Mayanagi K, Shirai T, Matoba K, Fujikane R, Ishino Y, Morikawa K
OpenAccess logo BMC Struct Biol 9 2 (2009)
Related entries: 2zj2, 2zj8, 2zja

Cited: 23 times
EuropePMC logo PMID: 19159486

Abstract

Background

Pyrococcus furiosus Hjm (PfuHjm) is a structure-specific DNA helicase that was originally identified by in vitro screening for Holliday junction migration activity. It belongs to helicase superfamily 2, and shares homology with the human DNA polymerase Theta (PolTheta), HEL308, and Drosophila Mus308 proteins, which are involved in DNA repair. Previous biochemical and genetic analyses revealed that PfuHjm preferentially binds to fork-related Y-structured DNAs and unwinds their double-stranded regions, suggesting that this helicase is a functional counterpart of the bacterial RecQ helicase, which is essential for genome maintenance. Elucidation of the DNA unwinding and translocation mechanisms by PfuHjm will require its three-dimensional structure at atomic resolution.

Results

We determined the crystal structures of PfuHjm, in two apo-states and two nucleotide bound forms, at resolutions of 2.0-2.7 A. The overall structures and the local conformations around the nucleotide binding sites are almost the same, including the side-chain conformations, irrespective of the nucleotide-binding states. The architecture of Hjm was similar to that of Archaeoglobus fulgidus Hel308 complexed with DNA. An Hjm-DNA complex model, constructed by fitting the five domains of Hjm onto the corresponding Hel308 domains, indicated that the interaction of Hjm with DNA is similar to that of Hel308. Notably, sulphate ions bound to Hjm lie on the putative DNA binding surfaces. Electron microscopic analysis of an Hjm-DNA complex revealed substantial flexibility of the double stranded region of DNA, presumably due to particularly weak protein-DNA interactions. Our present structures allowed reasonable homology model building of the helicase region of human PolTheta, indicating the strong conformational conservation between archaea and eukarya.

Reviews - 2zj5 mentioned but not cited (2)

  1. Ski2-like RNA helicase structures: common themes and complex assemblies. Johnson SJ, Jackson RN. RNA Biol 10 33-43 (2013)
  2. Probing the structure and function of polymerase θ helicase-like domain. Vanson S, Li Y, Wood RD, Doublié S. DNA Repair (Amst) 116 103358 (2022)

Articles - 2zj5 mentioned but not cited (2)

  1. Prp43p contains a processive helicase structural architecture with a specific regulatory domain. Walbott H, Mouffok S, Capeyrou R, Lebaron S, Humbert O, van Tilbeurgh H, Henry Y, Leulliot N. EMBO J 29 2194-2204 (2010)
  2. Atomic structures and functional implications of the archaeal RecQ-like helicase Hjm. Oyama T, Oka H, Mayanagi K, Shirai T, Matoba K, Fujikane R, Ishino Y, Morikawa K. BMC Struct Biol 9 2 (2009)


Reviews citing this publication (6)

  1. End resection at double-strand breaks: mechanism and regulation. Symington LS. Cold Spring Harb Perspect Biol 6 a016436 (2014)
  2. XPB and XPD helicases in TFIIH orchestrate DNA duplex opening and damage verification to coordinate repair with transcription and cell cycle via CAK kinase. Fuss JO, Tainer JA. DNA Repair (Amst) 10 697-713 (2011)
  3. From keys to bulldozers: expanding roles for winged helix domains in nucleic-acid-binding proteins. Harami GM, Gyimesi M, Kovács M. Trends Biochem Sci 38 364-371 (2013)
  4. Nanobiomotors of archaeal DNA repair machineries: current research status and application potential. Han W, Shen Y, She Q. Cell Biosci 4 32 (2014)
  5. Genome Protection by DNA Polymerase θ. Wood RD, Doublié S. Annu Rev Genet 56 207-228 (2022)
  6. A deep dive into the RecQ interactome: something old and something new. Simmons RH, Rogers CM, Bochman ML. Curr Genet 67 761-767 (2021)

Articles citing this publication (13)

  1. The crystal structure of Mtr4 reveals a novel arch domain required for rRNA processing. Jackson RN, Klauer AA, Hintze BJ, Robinson H, van Hoof A, Johnson SJ. EMBO J 29 2205-2216 (2010)
  2. Structural basis for the function of DEAH helicases. He Y, Andersen GR, Nielsen KH. EMBO Rep 11 180-186 (2010)
  3. Structural evidence for consecutive Hel308-like modules in the spliceosomal ATPase Brr2. Zhang L, Xu T, Maeder C, Bud LO, Shanks J, Nix J, Guthrie C, Pleiss JA, Zhao R. Nat Struct Mol Biol 16 731-739 (2009)
  4. Ter-dependent stress response systems: novel pathways related to metal sensing, production of a nucleoside-like metabolite, and DNA-processing. Anantharaman V, Iyer LM, Aravind L. Mol Biosyst 8 3142-3165 (2012)
  5. Structure of the Helicase Domain of DNA Polymerase Theta Reveals a Possible Role in the Microhomology-Mediated End-Joining Pathway. Newman JA, Cooper CDO, Aitkenhead H, Gileadi O. Structure 23 2319-2330 (2015)
  6. Characterization of metalloproteins by high-throughput X-ray absorption spectroscopy. Shi W, Punta M, Bohon J, Sauder JM, D'Mello R, Sullivan M, Toomey J, Abel D, Lippi M, Passerini A, Frasconi P, Burley SK, Rost B, Chance MR. Genome Res 21 898-907 (2011)
  7. The Mtr4 ratchet helix and arch domain both function to promote RNA unwinding. Taylor LL, Jackson RN, Rexhepaj M, King AK, Lott LK, van Hoof A, Johnson SJ. Nucleic Acids Res 42 13861-13872 (2014)
  8. Helq acts in parallel to Fancc to suppress replication-associated genome instability. Luebben SW, Kawabata T, Akre MK, Lee WL, Johnson CS, O'Sullivan MG, Shima N. Nucleic Acids Res 41 10283-10297 (2013)
  9. DNA binding and unwinding by Hel308 helicase requires dual functions of a winged helix domain. Northall SJ, Buckley R, Jones N, Penedo JC, Soultanas P, Bolt EL. DNA Repair (Amst) 57 125-132 (2017)
  10. Genome-wide identification of SF1 and SF2 helicases from archaea. Chamieh H, Ibrahim H, Kozah J. Gene 576 214-228 (2016)
  11. Taking a molecular motor for a spin: helicase mechanism studied by spin labeling and PELDOR. Constantinescu-Aruxandei D, Petrovic-Stojanovska B, Schiemann O, Naismith JH, White MF. Nucleic Acids Res 44 954-968 (2016)
  12. Long-range allostery mediates cooperative adenine nucleotide binding by the Ski2-like RNA helicase Brr2. Absmeier E, Vester K, Ghane T, Burakovskiy D, Milon P, Imhof P, Rodnina MV, Santos KF, Wahl MC. J Biol Chem 297 100829 (2021)
  13. Archaeal Hel308 suppresses recombination through a catalytic switch that controls DNA annealing. Lever RJ, Simmons E, Gamble-Milner R, Buckley RJ, Harrison C, Parkes AJ, Mitchell L, Gausden JA, Škulj S, Bertoša B, Bolt EL, Allers T. Nucleic Acids Res 51 8563-8574 (2023)


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