1w0h Citations

Crystallographic structure of the nuclease domain of 3'hExo, a DEDDh family member, bound to rAMP.

J Mol Biol 343 305-12 (2004)
Cited: 33 times
EuropePMC logo PMID: 15451662

Abstract

A human 3'-5'-exoribonuclease (3'hExo) has recently been identified and shown to be responsible for histone mRNA degradation. Functionally, 3'hExo and a stem-loop binding protein (SLBP) target opposite faces of a unique highly conserved stem-loop RNA scaffold towards the 3' end of histone mRNA, which is composed of a 6 bp stem and a 4 nt loop, followed by an ACCCA sequence. Its Caenorhabditis elegans homologue, ERI-1, has been shown to degrade small interfering RNA in vitro and to function as a negative regulator of RNA interference in neuronal cells. We have determined the structure of the nuclease domain (Nuc) of 3'hExo complexed with rAMP in the presence of Mg2+ at 1.6 A resolution. The Nuc domain adopts an alpha/beta globular fold, with four acidic residues coordinating a binuclear metal cluster within the active site, whose topology is related to DEDDh exonuclease family members, despite a very low level of primary sequence identity. The two magnesium cations in the Nuc active site are coordinated to D134, E136, D234 and D298, and together with H293, which can potentially act as a general base, provide a platform for hydrolytic cleavage of bound RNA in the 3' --> 5' direction. The bound rAMP is positioned within a deep active-site pocket, with its purine ring close-packed with the hydrophobic F185 and L189 side-chains and its sugar 2'-OH and 3'-OH groups hydrogen bonded to backbone atoms of Nuc. There are striking similarities between the active sites of Nuc and epsilon186, an Escherichia coli DNA polymerase III proofreading domain, providing a common hydrolytic cleavage mechanism for RNA degradation and DNA editing, respectively.

Articles - 1w0h mentioned but not cited (5)

  1. Crystallographic structure of the nuclease domain of 3'hExo, a DEDDh family member, bound to rAMP. Cheng Y, Patel DJ. J. Mol. Biol. 343 305-312 (2004)
  2. Crystal structure of RNase T, an exoribonuclease involved in tRNA maturation and end turnover. Zuo Y, Zheng H, Wang Y, Chruszcz M, Cymborowski M, Skarina T, Savchenko A, Malhotra A, Minor W. Structure 15 417-428 (2007)
  3. Functional insight into Maelstrom in the germline piRNA pathway: a unique domain homologous to the DnaQ-H 3'-5' exonuclease, its lineage-specific expansion/loss and evolutionarily active site switch. Zhang D, Xiong H, Shan J, Xia X, Trudeau VL. Biol. Direct 3 48 (2008)
  4. Genetic and biochemical characterization of Drosophila Snipper: A promiscuous member of the metazoan 3'hExo/ERI-1 family of 3' to 5' exonucleases. Kupsco JM, Wu MJ, Marzluff WF, Thapar R, Duronio RJ. RNA 12 2103-2117 (2006)
  5. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)


Reviews citing this publication (8)

  1. Nucleases: diversity of structure, function and mechanism. Yang W. Q. Rev. Biophys. 44 1-93 (2011)
  2. Formation of the 3' end of histone mRNA: getting closer to the end. Dominski Z, Marzluff WF. Gene 396 373-390 (2007)
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  4. Roles of metal ions in nucleases. Dupureur CM. Curr Opin Chem Biol 12 250-255 (2008)
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  6. Comparison of preribosomal RNA processing pathways in yeast, plant and human cells - focus on coordinated action of endo- and exoribonucleases. Tomecki R, Sikorski PJ, Zakrzewska-Placzek M. FEBS Lett. 591 1801-1850 (2017)
  7. Eri1: a conserved enzyme at the crossroads of multiple RNA-processing pathways. Thomas MF, L'Etoile ND, Ansel KM. Trends Genet. 30 298-307 (2014)
  8. Degradation of oligouridylated histone mRNAs: see UUUUU and goodbye. Hoefig KP, Heissmeyer V. Wiley Interdiscip Rev RNA 5 577-589 (2014)

Articles citing this publication (20)

  1. Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways. Duchaine TF, Wohlschlegel JA, Kennedy S, Bei Y, Conte D, Pang K, Brownell DR, Harding S, Mitani S, Ruvkun G, Yates JR, Mello CC. Cell 124 343-354 (2006)
  2. Discovery of an RNA virus 3'->5' exoribonuclease that is critically involved in coronavirus RNA synthesis. Minskaia E, Hertzig T, Gorbalenya AE, Campanacci V, Cambillau C, Canard B, Ziebuhr J. Proc. Natl. Acad. Sci. U.S.A. 103 5108-5113 (2006)
  3. Structure of histone mRNA stem-loop, human stem-loop binding protein, and 3'hExo ternary complex. Tan D, Marzluff WF, Dominski Z, Tong L. Science 339 318-321 (2013)
  4. Plant development. Arabidopsis NAC45/86 direct sieve element morphogenesis culminating in enucleation. Furuta KM, Yadav SR, Lehesranta S, Belevich I, Miyashima S, Heo JO, Vatén A, Lindgren O, De Rybel B, Van Isterdael G, Somervuo P, Lichtenberger R, Rocha R, Thitamadee S, Tähtiharju S, Auvinen P, Beeckman T, Jokitalo E, Helariutta Y. Science 345 933-937 (2014)
  5. Mouse Eri1 interacts with the ribosome and catalyzes 5.8S rRNA processing. Ansel KM, Pastor WA, Rath N, Lapan AD, Glasmacher E, Wolf C, Smith LC, Papadopoulou N, Lamperti ED, Tahiliani M, Ellwart JW, Shi Y, Kremmer E, Rao A, Heissmeyer V. Nat. Struct. Mol. Biol. 15 523-530 (2008)
  6. The RNase H-like superfamily: new members, comparative structural analysis and evolutionary classification. Majorek KA, Dunin-Horkawicz S, Steczkiewicz K, Muszewska A, Nowotny M, Ginalski K, Bujnicki JM. Nucleic Acids Res. 42 4160-4179 (2014)
  7. The role of deadenylation in the degradation of unstable mRNAs in trypanosomes. Schwede A, Manful T, Jha BA, Helbig C, Bercovich N, Stewart M, Clayton C. Nucleic Acids Res. 37 5511-5528 (2009)
  8. The 1.4-A crystal structure of the S. pombe Pop2p deadenylase subunit unveils the configuration of an active enzyme. Jonstrup AT, Andersen KR, Van LB, Brodersen DE. Nucleic Acids Res. 35 3153-3164 (2007)
  9. Crystal structure of the PIN domain of human telomerase-associated protein EST1A. Takeshita D, Zenno S, Lee WC, Saigo K, Tanokura M. Proteins 68 980-989 (2007)
  10. Crystal structure of CRN-4: implications for domain function in apoptotic DNA degradation. Hsiao YY, Nakagawa A, Shi Z, Mitani S, Xue D, Yuan HS. Mol. Cell. Biol. 29 448-457 (2009)
  11. Structural and biochemical studies of TREX1 inhibition by metals. Identification of a new active histidine conserved in DEDDh exonucleases. Brucet M, Querol-Audí J, Bertlik K, Lloberas J, Fita I, Celada A. Protein Sci. 17 2059-2069 (2008)
  12. Hydrolysis of the 5'-p-nitrophenyl ester of TMP by oligoribonucleases (ORN) from Escherichia coli, Mycobacterium smegmatis, and human. Young Park A, Elvin CM, Hamdan SM, Wood RJ, Liyou NE, Hamwood TE, Jennings PA, Dixon NE. Protein Expr. Purif. 57 180-187 (2008)
  13. Aromatic residues in RNase T stack with nucleobases to guide the sequence-specific recognition and cleavage of nucleic acids. Duh Y, Hsiao YY, Li CL, Huang JC, Yuan HS. Protein Sci. 24 1934-1941 (2015)
  14. Structural and molecular basis of mismatch correction and ribavirin excision from coronavirus RNA. Ferron F, Subissi L, Silveira De Morais AT, Le NTT, Sevajol M, Gluais L, Decroly E, Vonrhein C, Bricogne G, Canard B, Imbert I. Proc. Natl. Acad. Sci. U.S.A. 115 E162-E171 (2018)
  15. Deletion of the rnl gene encoding a nick-sealing RNA ligase sensitizes Deinococcus radiodurans to ionizing radiation. Schmier BJ, Chen X, Wolin S, Shuman S. Nucleic Acids Res. 45 3812-3821 (2017)
  16. Crystal structure and functional properties of the human CCR4-CAF1 deadenylase complex. Chen Y, Khazina E, Izaurralde E, Weichenrieder O. Nucleic Acids Res 49 6489-6510 (2021)
  17. Influenza A virus co-opts ERI1 exonuclease bound to histone mRNA to promote viral transcription. Declercq M, Biquand E, Karim M, Pietrosemoli N, Jacob Y, Demeret C, Barbezange C, van der Werf S. Nucleic Acids Res 48 10428-10440 (2020)
  18. Null and missense mutations of ERI1 cause a recessive phenotypic dichotomy in humans. Guo L, Salian S, Xue JY, Rath N, Rousseau J, Kim H, Ehresmann S, Moosa S, Nakagawa N, Kuroda H, Clayton-Smith J, Wang J, Wang Z, Banka S, Jackson A, Zhang YM, Wei ZJ, Hüning I, Brunet T, Ohashi H, Thomas MF, Bupp C, Miyake N, Matsumoto N, Mendoza-Londono R, Costain G, Hahn G, Di Donato N, Yigit G, Yamada T, Nishimura G, Ansel KM, Wollnik B, Hrabě de Angelis M, Mégarbané A, Rosenfeld JA, Heissmeyer V, Ikegawa S, Campeau PM. Am J Hum Genet 110 1068-1085 (2023)
  19. Letter Snipper, an Eri1 homologue, affects histone mRNA abundance and is crucial for normal Drosophila melanogaster development. Alexiadis A, Delidakis C, Kalantidis K. FEBS Lett. 591 2106-2120 (2017)
  20. Uridylation of the histone mRNA stem-loop weakens binding interactions with SLBP while maintaining interactions with 3'hExo. Shine M, Harris SE, Pellegrene KA, Kensinger AH, Mihailescu MR, Evanseck JD, Lackey PE. RNA Biol 20 469-481 (2023)