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The structures of the SNM1A and SNM1B/Apollo nuclease domains reveal a potential basis for their distinct DNA processing activities.

Allerston CK, Lee SY, Newman JA, Schofield CJ, McHugh PJ, Gileadi O
Nucleic Acids Res 43 11047-60 (2015)
Cited: 27 times
EuropePMC logo PMID: 26582912

Abstract

The human SNM1A and SNM1B/Apollo proteins are members of an extended family of eukaryotic nuclease containing a motif related to the prokaryotic metallo-β-lactamase (MBL) fold. SNM1A is a key exonuclease during replication-dependent and transcription-coupled interstrand crosslink repair, while SNM1B/Apollo is required for maintaining telomeric overhangs. Here, we report the crystal structures of SNM1A and SNM1B at 2.16 Å. While both proteins contain a typical MBL-β-CASP domain, a region of positive charge surrounds the active site of SNM1A, which is absent in SNM1B and explains the greater apparent processivity of SNM1A. The structures of both proteins also reveal a putative, wide DNA-binding groove. Extensive mutagenesis of this groove, coupled with detailed biochemical analysis, identified residues that did not impact on SNM1A catalytic activity, but drastically reduced its processivity. Moreover, we identified a key role for this groove for efficient digestion past DNA interstrand crosslinks, facilitating the key DNA repair reaction catalysed by SNM1A. Together, the architecture and dimensions of this groove, coupled to the surrounding region of high positive charge, explain the remarkable ability of SNM1A to accommodate and efficiently digest highly distorted DNA substrates, such as those containing DNA lesions.

Reviews - 5aho mentioned but not cited (2)

  1. The Chemical Biology of Human Metallo-β-Lactamase Fold Proteins. Pettinati I, Brem J, Lee SY, McHugh PJ, Schofield CJ. Trends Biochem Sci 41 338-355 (2016)
  2. The SNM1A DNA repair nuclease. Baddock HT, Yosaatmadja Y, Newman JA, Schofield CJ, Gileadi O, McHugh PJ. DNA Repair (Amst) 95 102941 (2020)

Articles - 5aho mentioned but not cited (6)

  1. The structures of the SNM1A and SNM1B/Apollo nuclease domains reveal a potential basis for their distinct DNA processing activities. Allerston CK, Lee SY, Newman JA, Schofield CJ, McHugh PJ, Gileadi O. Nucleic Acids Res 43 11047-11060 (2015)
  2. Cephalosporins inhibit human metallo β-lactamase fold DNA repair nucleases SNM1A and SNM1B/apollo. Lee SY, Brem J, Pettinati I, Claridge TD, Gileadi O, Schofield CJ, McHugh PJ. Chem Commun (Camb) 52 6727-6730 (2016)
  3. Structural analysis of the catalytic domain of Artemis endonuclease/SNM1C reveals distinct structural features. Karim MF, Liu S, Laciak AR, Volk L, Koszelak-Rosenblum M, Lieber MR, Wu M, Curtis R, Huang NN, Carr G, Zhu G. J Biol Chem 295 12368-12377 (2020)
  4. Characterization of Lhr-Core DNA helicase and manganese- dependent DNA nuclease components of a bacterial gene cluster encoding nucleic acid repair enzymes. Ejaz A, Shuman S. J Biol Chem 293 17491-17504 (2018)
  5. A phosphate binding pocket is a key determinant of exo- versus endo-nucleolytic activity in the SNM1 nuclease family. Baddock HT, Newman JA, Yosaatmadja Y, Bielinski M, Schofield CJ, Gileadi O, McHugh PJ. Nucleic Acids Res 49 9294-9309 (2021)
  6. Staring at the Naked Goddess: Unraveling the Structure and Reactivity of Artemis Endonuclease Interacting with a DNA Double Strand. Hognon C, Monari A. Molecules 26 3986 (2021)


Reviews citing this publication (4)

  1. Involvement of translesion synthesis DNA polymerases in DNA interstrand crosslink repair. Roy U, Schärer OD. DNA Repair (Amst) 44 33-41 (2016)
  2. SNM1B/Apollo in the DNA damage response and telomere maintenance. Schmiester M, Demuth I. Oncotarget 8 48398-48409 (2017)
  3. Origin, Diversity, and Multiple Roles of Enzymes with Metallo-β-Lactamase Fold from Different Organisms. Diene SM, Pontarotti P, Azza S, Armstrong N, Pinault L, Chabrière E, Colson P, Rolain JM, Raoult D. Cells 12 1752 (2023)
  4. Structure and Function of SNM1 Family Nucleases. Wu HY, Zheng Y, Laciak AR, Huang NN, Koszelak-Rosenblum M, Flint AJ, Carr G, Zhu G. Adv Exp Med Biol 1414 1-26 (2023)

Articles citing this publication (15)

  1. RPA activates the XPF-ERCC1 endonuclease to initiate processing of DNA interstrand crosslinks. Abdullah UB, McGouran JF, Brolih S, Ptchelkine D, El-Sagheer AH, Brown T, McHugh PJ. EMBO J 36 2047-2060 (2017)
  2. Identification of LACTB2, a metallo-β-lactamase protein, as a human mitochondrial endoribonuclease. Levy S, Allerston CK, Liveanu V, Habib MR, Gileadi O, Schuster G. Nucleic Acids Res 44 1813-1832 (2016)
  3. Human metallo-β-lactamase enzymes degrade penicillin. Diene SM, Pinault L, Keshri V, Armstrong N, Khelaifia S, Chabrière E, Caetano-Anolles G, Colson P, La Scola B, Rolain JM, Pontarotti P, Raoult D. Sci Rep 9 12173 (2019)
  4. The structure and duplex context of DNA interstrand crosslinks affects the activity of DNA polymerase η. Roy U, Mukherjee S, Sharma A, Frank EG, Schärer OD. Nucleic Acids Res 44 7281-7291 (2016)
  5. Structural and mechanistic insights into the Artemis endonuclease and strategies for its inhibition. Yosaatmadja Y, Baddock HT, Newman JA, Bielinski M, Gavard AE, Mukhopadhyay SMM, Dannerfjord AA, Schofield CJ, McHugh PJ, Gileadi O. Nucleic Acids Res 49 9310-9326 (2021)
  6. Structure-specific endonuclease activity of SNM1A enables processing of a DNA interstrand crosslink. Buzon B, Grainger R, Huang S, Rzadki C, Junop MS. Nucleic Acids Res 46 9057-9066 (2018)
  7. Inherited human Apollo deficiency causes severe bone marrow failure and developmental defects. Kermasson L, Churikov D, Awad A, Smoom R, Lainey E, Touzot F, Audebert-Bellanger S, Haro S, Roger L, Costa E, Mouf M, Bottero A, Oleastro M, Abdo C, de Villartay JP, Géli V, Tzfati Y, Callebaut I, Danielian S, Soares G, Kannengiesser C, Revy P. Blood 139 2427-2440 (2022)
  8. Squaramide-Based 5'-Phosphate Replacements Bind to the DNA Repair Exonuclease SNM1A. Dürr EM, Doherty W, Lee SY, El-Sagheer AH, Shivalingam A, McHugh PJ, Brown T, McGouran JF. ChemistrySelect 3 12824-12829 (2018)
  9. Inflammatory factor receptor Toll-like receptor 4 controls telomeres through heterochromatin protein 1 isoforms in liver cancer stem cell. Zheng Q, Xu J, Lin Z, Lu Y, Xin X, Li X, Yang Y, Meng Q, Wang C, Xiong W, Lu D. J Cell Mol Med 22 3246-3258 (2018)
  10. A hydroxamic-acid-containing nucleoside inhibits DNA repair nuclease SNM1A. Doherty W, Dürr EM, Baddock HT, Lee SY, McHugh PJ, Brown T, Senge MO, Scanlan EM, McGouran JF. Org Biomol Chem 17 8094-8105 (2019)
  11. Probing the Binding Requirements of Modified Nucleosides with the DNA Nuclease SNM1A. Dürr EM, McGouran JF. Molecules 26 E320 (2021)
  12. Synthesis and evaluation of squaramide and thiosquaramide inhibitors of the DNA repair enzyme SNM1A. Berney M, Doherty W, Jauslin WT, T Manoj M, Dürr EM, McGouran JF. Bioorg Med Chem 46 116369 (2021)
  13. Two-Step Validation Approach for Tools To Study the DNA Repair Enzyme SNM1A. Fay EM, Newton A, Berney M, El-Sagheer AH, Brown T, McGouran JF. Chembiochem 24 e202200756 (2023)
  14. Deploying solid-phase synthesis to access thymine-containing nucleoside analogs that inhibit DNA repair nuclease SNM1A. Arbour CA, Fay EM, McGouran JF, Imperiali B. Org Biomol Chem 21 5873-5879 (2023)
  15. Evolutionary insights into the active-site structures of the metallo-β-lactamase superfamily from a classification study with support vector machine. Wang L, Yang L, Feng YL, Zhang H. J Biol Inorg Chem 25 1023-1034 (2020)


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