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The activity and selectivity of fission yeast Pop2p are affected by a high affinity for Zn2+ and Mn2+ in the active site.

Andersen KR, Jonstrup AT, Van LB, Brodersen DE
RNA 15 850-61 (2009)
Cited: 31 times
EuropePMC logo PMID: 19307292

Abstract

In eukaryotic organisms, initiation of mRNA turnover is controlled by progressive shortening of the poly-A tail, a process involving the mega-Dalton Ccr4-Not complex and its two associated 3'-5' exonucleases, Ccr4p and Pop2p (Caf1p). RNA degradation by the 3'-5' DEDDh exonuclease, Pop2p, is governed by the classical two metal ion mechanism traditionally assumed to be dependent on Mg(2+) ions bound in the active site. Here, we show biochemically and structurally that fission yeast (Schizosaccharomyces pombe) Pop2p prefers Mn(2+) and Zn(2+) over Mg(2+) at the concentrations of the ions found inside cells and that the identity of the ions in the active site affects the activity of the enzyme. Ion replacement experiments further suggest that mRNA deadenylation could be subtly regulated by local Zn(2+) levels in the cell. Finally, we use site-directed mutagenesis to propose a mechanistic model for the basis of the preference for poly-A sequences exhibited by the Pop2p-type deadenylases as well as their distributive enzymatic behavior.

Reviews - 3g0z mentioned but not cited (2)

  1. Insights into the structure and architecture of the CCR4-NOT complex. Xu K, Bai Y, Zhang A, Zhang Q, Bartlam MG. Front Genet 5 137 (2014)
  2. Structure and function of molecular machines involved in deadenylation-dependent 5'-3' mRNA degradation. Zhao Q, Pavanello L, Bartlam M, Winkler GS. Front Genet 14 1233842 (2023)

Articles - 3g0z mentioned but not cited (3)

  1. The activity and selectivity of fission yeast Pop2p are affected by a high affinity for Zn2+ and Mn2+ in the active site. Andersen KR, Jonstrup AT, Van LB, Brodersen DE. RNA 15 850-861 (2009)
  2. The intrinsic structure of poly(A) RNA determines the specificity of Pan2 and Caf1 deadenylases. Tang TTL, Stowell JAW, Hill CH, Passmore LA. Nat Struct Mol Biol 26 433-442 (2019)
  3. Recognition of Poly(A) RNA through Its Intrinsic Helical Structure. Tang TTL, Passmore LA. Cold Spring Harb Symp Quant Biol 84 21-30 (2019)


Reviews citing this publication (6)

  1. Nucleases: diversity of structure, function and mechanism. Yang W. Q Rev Biophys 44 1-93 (2011)
  2. Proteins involved in the degradation of cytoplasmic mRNA in the major eukaryotic model systems. Siwaszek A, Ukleja M, Dziembowski A. RNA Biol 11 1122-1136 (2014)
  3. Poly(A)-specific ribonuclease (PARN): an allosterically regulated, processive and mRNA cap-interacting deadenylase. Virtanen A, Henriksson N, Nilsson P, Nissbeck M. Crit Rev Biochem Mol Biol 48 192-209 (2013)
  4. The structural basis for deadenylation by the CCR4-NOT complex. Bartlam M, Yamamoto T. Protein Cell 1 443-452 (2010)
  5. Deadenylation: enzymes, regulation, and functional implications. Yan YB. Wiley Interdiscip Rev RNA 5 421-443 (2014)
  6. Heterogeneity and complexity within the nuclease module of the Ccr4-Not complex. Winkler GS, Balacco DL. Front Genet 4 296 (2013)

Articles citing this publication (20)

  1. RNA decay machines: deadenylation by the Ccr4-not and Pan2-Pan3 complexes. Wahle E, Winkler GS. Biochim Biophys Acta 1829 561-570 (2013)
  2. PDE12 removes mitochondrial RNA poly(A) tails and controls translation in human mitochondria. Rorbach J, Nicholls TJ, Minczuk M. Nucleic Acids Res 39 7750-7763 (2011)
  3. Reconstitution of Targeted Deadenylation by the Ccr4-Not Complex and the YTH Domain Protein Mmi1. Stowell JAW, Webster MW, Kögel A, Wolf J, Shelley KL, Passmore LA. Cell Rep 17 1978-1989 (2016)
  4. The architecture of the Schizosaccharomyces pombe CCR4-NOT complex. Ukleja M, Cuellar J, Siwaszek A, Kasprzak JM, Czarnocki-Cieciura M, Bujnicki JM, Dziembowski A, Valpuesta JM. Nat Commun 7 10433 (2016)
  5. Human 2'-phosphodiesterase localizes to the mitochondrial matrix with a putative function in mitochondrial RNA turnover. Poulsen JB, Andersen KR, Kjær KH, Durand F, Faou P, Vestergaard AL, Talbo GH, Hoogenraad N, Brodersen DE, Justesen J, Martensen PM. Nucleic Acids Res 39 3754-3770 (2011)
  6. Recognition of adenosine residues by the active site of poly(A)-specific ribonuclease. Henriksson N, Nilsson P, Wu M, Song H, Virtanen A. J Biol Chem 285 163-170 (2010)
  7. A fluorescence-based assay suitable for quantitative analysis of deadenylase enzyme activity. Maryati M, Kaur I, Jadhav GP, Olotu-Umoren L, Oveh B, Hashmi L, Fischer PM, Winkler GS. Nucleic Acids Res 42 e30 (2014)
  8. CCR4 and CAF1 deadenylases have an intrinsic activity to remove the post-poly(A) sequence. Niinuma S, Fukaya T, Tomari Y. RNA 22 1550-1559 (2016)
  9. Analysis of mRNA deadenylation by multi-protein complexes. Webster MW, Stowell JAW, Tang TTL, Passmore LA. Methods 126 95-104 (2017)
  10. Saccharomyces cerevisiae Ngl3p is an active 3'-5' exonuclease with a specificity towards poly-A RNA reminiscent of cellular deadenylases. Feddersen A, Dedic E, Poulsen EG, Schmid M, Van LB, Jensen TH, Brodersen DE. Nucleic Acids Res 40 837-846 (2012)
  11. The CCR4-NOT complex is implicated in the viability of aneuploid yeasts. Tange Y, Kurabayashi A, Goto B, Hoe KL, Kim DU, Park HO, Hayles J, Chikashige Y, Tsutumi C, Hiraoka Y, Yamao F, Nurse P, Niwa O. PLoS Genet 8 e1002776 (2012)
  12. 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)
  13. Hidden relationships between metalloproteins unveiled by structural comparison of their metal sites. Valasatava Y, Andreini C, Rosato A. Sci Rep 5 9486 (2015)
  14. Biochemical and biophysical characterization of the deadenylase CrCaf1 from Chlamydomonas reinhardtii. Zhang JQ, He GJ, Yan YB. PLoS One 8 e69582 (2013)
  15. ATP is dispensable for both miRNA- and Smaug-mediated deadenylation reactions. Niinuma S, Tomari Y. RNA 23 866-871 (2017)
  16. Identification of the ternary complex of ribonuclease HI:RNA/DNA hybrid:metal ions by ESI mass spectrometry. Ando T, Jongruja N, Okumura N, Morikawa K, Kanaya S, Takao T. J Biol Chem 296 100462 (2021)
  17. Letter Structural basis for inhibition of the deadenylase activity of human CNOT6L. Zhang Q, Yan D, Guo E, Ding B, Yang W, Liu R, Yamamoto T, Bartlam M. FEBS Lett 590 1270-1279 (2016)
  18. Structure of the human Ccr4-Not nuclease module using X-ray crystallography and electron paramagnetic resonance spectroscopy distance measurements. Zhang Q, Pavanello L, Potapov A, Bartlam M, Winkler GS. Protein Sci 31 758-764 (2022)
  19. Alternative RNA degradation pathways by the exonuclease Pop2p from Saccharomyces cerevisiae. Ye X, Axhemi A, Jankowsky E. RNA 27 465-476 (2021)
  20. Short PolyA RNA Homopolymers Undergo Mg2+-Mediated Kinetically Arrested Condensation. Tom JKA, Onuchic PL, Deniz AA. J Phys Chem B 126 9715-9725 (2022)


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