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Crystal structures of Escherichia coli exonuclease I in complex with single-stranded DNA provide insights into the mechanism of processive digestion.

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Korada SK, Johns TD, Smith CE, Jones ND, McCabe KA, Bell CE
OpenAccess logo Nucleic Acids Res 41 5887-97 (2013)
Related entries: 4jrq, 4js4, 4js5

Cited: 13 times
EuropePMC logo PMID: 23609540

Abstract

Escherichia coli Exonuclease I (ExoI) digests single-stranded DNA (ssDNA) in the 3'-5' direction in a highly processive manner. The crystal structure of ExoI, determined previously in the absence of DNA, revealed a C-shaped molecule with three domains that form a central positively charged groove. The active site is at the bottom of the groove, while an extended loop, proposed to encircle the DNA, crosses over the groove. Here, we present crystal structures of ExoI in complex with four different ssDNA substrates. The structures all have the ssDNA bound in essentially the predicted manner, with the 3'-end in the active site and the downstream end under the crossover loop. The central nucleotides of the DNA form a prominent bulge that contacts the SH3-like domain, while the nucleotides at the downstream end of the DNA form extensive interactions with an 'anchor' site. Seven of the complexes are similar to one another, but one has the ssDNA bound in a distinct conformation. The highest-resolution structure, determined at 1.95 Å, reveals an Mg(2+) ion bound to the scissile phosphate in a position corresponding to Mg(B) in related two-metal nucleases. The structures provide new insights into the mechanism of processive digestion that will be discussed.

Articles - 4jrp mentioned but not cited (5)

  1. Complete genome of Pieris rapae, a resilient alien, a cabbage pest, and a source of anti-cancer proteins. Shen J, Cong Q, Kinch LN, Borek D, Otwinowski Z, Grishin NV. F1000Res 5 2631 (2016)
  2. A dedicated diribonucleotidase resolves a key bottleneck for the terminal step of RNA degradation. Kim SK, Lormand JD, Weiss CA, Eger KA, Turdiev H, Turdiev A, Winkler WC, Sondermann H, Lee VT. Elife 8 e46313 (2019)
  3. Crystal structures of Escherichia coli exonuclease I in complex with single-stranded DNA provide insights into the mechanism of processive digestion. Korada SK, Johns TD, Smith CE, Jones ND, McCabe KA, Bell CE. Nucleic Acids Res 41 5887-5897 (2013)
  4. NrnC, an RNase D-Like Protein From Agrobacterium, Is a Novel Octameric Nuclease That Specifically Degrades dsDNA but Leaves dsRNA Intact. Yuan Z, Gao F, Yin K, Gu L. Front Microbiol 9 3230 (2018)
  5. Characterization of an intertidal zone metagenome oligoribonuclease and the role of the intermolecular disulfide bond for homodimer formation and nuclease activity. Piotrowski Y, Berg K, Klebl DP, Leiros I, Larsen AN. FEBS Open Bio 9 1674-1688 (2019)


Reviews citing this publication (2)

  1. Processivity in Bacterial Glycosyltransferases. Yakovlieva L, Walvoort MTC. ACS Chem Biol 15 3-16 (2020)
  2. The mechanism of action of the SSB interactome reveals it is the first OB-fold family of genome guardians in prokaryotes. Bianco PR. Protein Sci 30 1757-1775 (2021)

Articles citing this publication (6)

  1. Crystal structure of the Redβ C-terminal domain in complex with λ Exonuclease reveals an unexpected homology with λ Orf and an interaction with Escherichia coli single stranded DNA binding protein. Caldwell BJ, Zakharova E, Filsinger GT, Wannier TM, Hempfling JP, Chun-Der L, Pei D, Church GM, Bell CE. Nucleic Acids Res 47 1950-1963 (2019)
  2. Structural insights into the duplex DNA processing of TREX2. Cheng HL, Lin CT, Huang KW, Wang S, Lin YT, Toh SI, Hsiao YY. Nucleic Acids Res 46 12166-12176 (2018)
  3. Structural basis for substrate recognition and processive cleavage mechanisms of the trimeric exonuclease PhoExo I. Miyazono K, Ishino S, Tsutsumi K, Ito T, Ishino Y, Tanokura M. Nucleic Acids Res 43 7122-7136 (2015)
  4. Structural Adaptation of the Single-Stranded DNA-Binding Protein C-Terminal to DNA Metabolizing Partners Guides Inhibitor Design. Tököli A, Bodnár B, Bogár F, Paragi G, Hetényi A, Bartus É, Wéber E, Hegedüs Z, Szabó Z, Kecskeméti G, Szakonyi G, Martinek TA. Pharmaceutics 15 1032 (2023)
  5. Structural and biochemical studies of a moderately thermophilic exonuclease I from Methylocaldum szegediense. Fei L, Tian S, Moysey R, Misca M, Barker JJ, Smith MA, McEwan PA, Pilka ES, Crawley L, Evans T, Sun D. PLoS One 10 e0117470 (2015)
  6. Tn5 tagments and transposes oligos to single-stranded DNA for strand-specific RNA sequencing. Zhang Y, Tang Y, Sun Z, Jia J, Fang Y, Wan X, Fang D. Genome Res 33 412-426 (2023)


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