4fhp › Citations

Crystal structures of the Cid1 poly (U) polymerase reveal the mechanism for UTP selectivity.

Figure 1.
Figure 2.
Figure 3.
Lunde BM, Magler I, Meinhart A
OpenAccess logo Nucleic Acids Res 40 9815-24 (2012)
Related entries: 4fh3, 4fh5, 4fhv, 4fhw, 4fhx, 4fhy

Cited: 32 times
EuropePMC logo PMID: 22885303

Abstract

Polyuridylation is emerging as a ubiquitous post-translational modification with important roles in multiple aspects of RNA metabolism. These poly (U) tails are added by poly (U) polymerases with homology to poly (A) polymerases; nevertheless, the selection for UTP over ATP remains enigmatic. We report the structures of poly (U) polymerase Cid1 from Schizoscaccharomyces pombe alone and in complex with UTP, CTP, GTP and 3'-dATP. These structures reveal that each of the 4 nt can be accommodated at the active site; however, differences exist that suggest how the polymerase selects UTP over the other nucleotides. Furthermore, we find that Cid1 shares a number of common UTP recognition features with the kinetoplastid terminal uridyltransferases. Kinetic analysis of Cid1's activity for its preferred substrates, UTP and ATP, reveal a clear preference for UTP over ATP. Ultimately, we show that a single histidine in the active site plays a pivotal role for poly (U) activity. Notably, this residue is typically replaced by an asparagine residue in Cid1-family poly (A) polymerases. By mutating this histidine to an asparagine residue in Cid1, we diminished Cid1's activity for UTP addition and improved ATP incorporation, supporting that this residue is important for UTP selectivity.

Articles - 4fhp mentioned but not cited (3)

  1. FAM46 proteins are novel eukaryotic non-canonical poly(A) polymerases. Kuchta K, Muszewska A, Knizewski L, Steczkiewicz K, Wyrwicz LS, Pawlowski K, Rychlewski L, Ginalski K. Nucleic Acids Res 44 3534-3548 (2016)
  2. Crystal structures of the Cid1 poly (U) polymerase reveal the mechanism for UTP selectivity. Lunde BM, Magler I, Meinhart A. Nucleic Acids Res 40 9815-9824 (2012)
  3. Nucleotide specificity of the human terminal nucleotidyltransferase Gld2 (TUT2). Chung CZ, Jo DH, Heinemann IU. RNA 22 1239-1249 (2016)


Reviews citing this publication (3)

  1. Cytoplasmic RNA: a case of the tail wagging the dog. Norbury CJ. Nat Rev Mol Cell Biol 14 643-653 (2013)
  2. A tale of non-canonical tails: gene regulation by post-transcriptional RNA tailing. Yu S, Kim VN. Nat Rev Mol Cell Biol 21 542-556 (2020)
  3. Function and Regulation of Human Terminal Uridylyltransferases. Yashiro Y, Tomita K. Front Genet 9 538 (2018)

Articles citing this publication (26)

  1. TUT7 controls the fate of precursor microRNAs by using three different uridylation mechanisms. Kim B, Ha M, Loeff L, Chang H, Simanshu DK, Li S, Fareh M, Patel DJ, Joo C, Kim VN. EMBO J 34 1801-1815 (2015)
  2. Uridylation prevents 3' trimming of oligoadenylated mRNAs. Sement FM, Ferrier E, Zuber H, Merret R, Alioua M, Deragon JM, Bousquet-Antonelli C, Lange H, Gagliardi D. Nucleic Acids Res 41 7115-7127 (2013)
  3. Multi-domain utilization by TUT4 and TUT7 in control of let-7 biogenesis. Faehnle CR, Walleshauser J, Joshua-Tor L. Nat Struct Mol Biol 24 658-665 (2017)
  4. Identification of small molecule inhibitors of Zcchc11 TUTase activity. Lin S, Gregory RI. RNA Biol 12 792-800 (2015)
  5. Unbiased screen of RNA tailing activities reveals a poly(UG) polymerase. Preston MA, Porter DF, Chen F, Buter N, Lapointe CP, Keles S, Kimble J, Wickens M. Nat Methods 16 437-445 (2019)
  6. Crystal structures of U6 snRNA-specific terminal uridylyltransferase. Yamashita S, Takagi Y, Nagaike T, Tomita K. Nat Commun 8 15788 (2017)
  7. Structural basis for the activation of the C. elegans noncanonical cytoplasmic poly(A)-polymerase GLD-2 by GLD-3. Nakel K, Bonneau F, Eckmann CR, Conti E. Proc Natl Acad Sci U S A 112 8614-8619 (2015)
  8. Structural plasticity of Cid1 provides a basis for its distributive RNA terminal uridylyl transferase activity. Yates LA, Durrant BP, Fleurdépine S, Harlos K, Norbury CJ, Gilbert RJ. Nucleic Acids Res 43 2968-2979 (2015)
  9. Structure of mitochondrial poly(A) RNA polymerase reveals the structural basis for dimerization, ATP selectivity and the SPAX4 disease phenotype. Lapkouski M, Hällberg BM. Nucleic Acids Res 43 9065-9075 (2015)
  10. A critical switch in the enzymatic properties of the Cid1 protein deciphered from its product-bound crystal structure. Munoz-Tello P, Gabus C, Thore S. Nucleic Acids Res 42 3372-3380 (2014)
  11. The nucleic acid-binding domain and translational repression activity of a Xenopus terminal uridylyl transferase. Lapointe CP, Wickens M. J Biol Chem 288 20723-20733 (2013)
  12. Evolution of miRNA Tailing by 3' Terminal Uridylyl Transferases in Metazoa. Modepalli V, Moran Y. Genome Biol Evol 9 1547-1560 (2017)
  13. RNA surveillance by uridylation-dependent RNA decay in Schizosaccharomyces pombe. Chung CZ, Jaramillo JE, Ellis MJ, Bour DYN, Seidl LE, Jo DHS, Turk MA, Mann MR, Bi Y, Haniford DB, Duennwald ML, Heinemann IU. Nucleic Acids Res 47 3045-3057 (2019)
  14. Crystal structure of the Lin28-interacting module of human terminal uridylyltransferase that regulates let-7 expression. Yamashita S, Nagaike T, Tomita K. Nat Commun 10 1960 (2019)
  15. Terminal Uridylyl Transferase Mediated Site-Directed Access to Clickable Chromatin Employing CRISPR-dCas9. George JT, Azhar M, Aich M, Sinha D, Ambi UB, Maiti S, Chakraborty D, Srivatsan SG. J Am Chem Soc 142 13954-13965 (2020)
  16. Structural basis for acceptor RNA substrate selectivity of the 3' terminal uridylyl transferase Tailor. Kroupova A, Ivascu A, Reimão-Pinto MM, Ameres SL, Jinek M. Nucleic Acids Res 47 1030-1042 (2019)
  17. Synthesis of modified nucleotide polymers by the poly(U) polymerase Cid1: application to direct RNA sequencing on nanopores. Vo JM, Mulroney L, Quick-Cleveland J, Jain M, Akeson M, Ares M. RNA 27 1497-1511 (2021)
  18. Biochemical and structural bioinformatics studies of fungal CutA nucleotidyltransferases explain their unusual specificity toward CTP and increased tendency for cytidine incorporation at the 3'-terminal positions of synthesized tails. Kobyłecki K, Kuchta K, Dziembowski A, Ginalski K, Tomecki R. RNA 23 1902-1926 (2017)
  19. Gld2 activity is regulated by phosphorylation in the N-terminal domain. Chung CZ, Balasuriya N, Manni E, Liu X, Li SS, O'Donoghue P, Heinemann IU. RNA Biol 16 1022-1033 (2019)
  20. Structural insights into a unique preference for 3' terminal guanine of mirtron in Drosophila TUTase tailor. Cheng L, Li F, Jiang Y, Yu H, Xie C, Shi Y, Gong Q. Nucleic Acids Res 47 495-508 (2019)
  21. Nanocellulose Composites as Smart Devices With Chassis, Light-Directed DNA Storage, Engineered Electronic Properties, and Chip Integration. Bencurova E, Shityakov S, Schaack D, Kaltdorf M, Sarukhanyan E, Hilgarth A, Rath C, Montenegro S, Roth G, Lopez D, Dandekar T. Front Bioeng Biotechnol 10 869111 (2022)
  22. Selective inhibitors of trypanosomal uridylyl transferase RET1 establish druggability of RNA post-transcriptional modifications. Cording A, Gormally M, Bond PJ, Carrington M, Balasubramanian S, Miska EA, Thomas B. RNA Biol 14 611-619 (2017)
  23. Responsive fluorescent nucleotides serve as efficient substrates to probe terminal uridylyl transferase. George JT, Srivatsan SG. Chem Commun (Camb) 56 12319-12322 (2020)
  24. Molecular mechanism underlying the di-uridylation activity of Arabidopsis TUTase URT1. Hu Q, Yang H, Li M, Zhu L, Lv M, Li F, Zhang Z, Ren G, Gong Q. Nucleic Acids Res 50 10614-10625 (2022)
  25. Structure and mechanism of CutA, RNA nucleotidyl transferase with an unusual preference for cytosine. Malik D, Kobyłecki K, Krawczyk P, Poznański J, Jakielaszek A, Napiórkowska A, Dziembowski A, Tomecki R, Nowotny M. Nucleic Acids Res 48 9387-9405 (2020)
  26. Mechanism of U6 snRNA oligouridylation by human TUT1. Yamashita S, Tomita K. Nat Commun 14 4686 (2023)


Quick links