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RNA specificity and regulation of catalysis in the eukaryotic polynucleotide kinase Clp1.

Dikfidan A, Loll B, Zeymer C, Magler I, Clausen T, Meinhart A
Mol Cell 54 975-86 (2014)
Related entries: 4ohv, 4ohw, 4ohx, 4ohy, 4ohz, 4oi0, 4oi1, 4oi2

Cited: 16 times
EuropePMC logo PMID: 24813946

Abstract

RNA-specific polynucleotide kinases of the Clp1 subfamily are key components of various RNA maturation pathways. However, the structural basis explaining their substrate specificity and the enzymatic mechanism is elusive. Here, we report crystal structures of Clp1 from Caenorhabditis elegans (ceClp1) in a number of nucleotide- and RNA-bound states along the reaction pathway. The combined structural and biochemical analysis of ceClp1 elucidates the RNA specificity and lets us derive a general model for enzyme catalysis of RNA-specific polynucleotide kinases. We identified an RNA binding motif referred to as "clasp" as well as a conformational switch that involves the essential Walker A lysine (Lys127) and regulates the enzymatic activity of ceClp1. Structural comparison with other P loop proteins, such as kinases, adenosine triphosphatases (ATPases), and guanosine triphosphatases (GTPases), suggests that the observed conformational switch of the Walker A lysine is a broadly relevant mechanistic feature.

Articles - 4oi4 mentioned but not cited (1)

  1. Reconstitution of mammalian cleavage factor II involved in 3' processing of mRNA precursors. Schäfer P, Tüting C, Schönemann L, Kühn U, Treiber T, Treiber N, Ihling C, Graber A, Keller W, Meister G, Sinz A, Wahle E. RNA 24 1721-1737 (2018)


Reviews citing this publication (3)

  1. RNA damage in biological conflicts and the diversity of responding RNA repair systems. Burroughs AM, Aravind L. Nucleic Acids Res 44 8525-8555 (2016)
  2. CLP1 as a novel player in linking tRNA splicing to neurodegenerative disorders. Weitzer S, Hanada T, Penninger JM, Martinez J. Wiley Interdiscip Rev RNA 6 47-63 (2015)
  3. Recent insights into the structure, function, and regulation of the eukaryotic transfer RNA splicing endonuclease complex. Hayne CK, Lewis TA, Stanley RE. Wiley Interdiscip Rev RNA 13 e1717 (2022)

Articles citing this publication (12)

  1. Grc3 programs the essential endoribonuclease Las1 for specific RNA cleavage. Pillon MC, Sobhany M, Borgnia MJ, Williams JG, Stanley RE. Proc Natl Acad Sci U S A 114 E5530-E5538 (2017)
  2. Reconstitution of the human tRNA splicing endonuclease complex: insight into the regulation of pre-tRNA cleavage. Hayne CK, Schmidt CA, Haque MI, Matera AG, Stanley RE. Nucleic Acids Res 48 7609-7622 (2020)
  3. Reconstitution of 3' end processing of mammalian pre-mRNA reveals a central role of RBBP6. Schmidt M, Kluge F, Sandmeir F, Kühn U, Schäfer P, Tüting C, Ihling C, Conti E, Wahle E. Genes Dev 36 195-209 (2022)
  4. Characterization of the molecular crosstalk within the essential Grc3/Las1 pre-rRNA processing complex. Pillon MC, Sobhany M, Stanley RE. RNA 24 721-738 (2018)
  5. Cryo-EM reveals active site coordination within a multienzyme pre-rRNA processing complex. Pillon MC, Hsu AL, Krahn JM, Williams JG, Goslen KH, Sobhany M, Borgnia MJ, Stanley RE. Nat Struct Mol Biol 26 830-839 (2019)
  6. Nol9 Is a Spatial Regulator for the Human ITS2 Pre-rRNA Endonuclease-Kinase Complex. Gordon J, Pillon MC, Stanley RE. J Mol Biol 431 3771-3786 (2019)
  7. Large-Scale Molecular Evolutionary Analysis Uncovers a Variety of Polynucleotide Kinase Clp1 Family Proteins in the Three Domains of Life. Saito M, Sato A, Nagata S, Tamaki S, Tomita M, Suzuki H, Kanai A. Genome Biol Evol 11 2713-2726 (2019)
  8. Structures of Drosophila melanogaster Rab2 and Rab3 bound to GMPPNP. Lardong JA, Driller JH, Depner H, Weise C, Petzoldt A, Wahl MC, Sigrist SJ, Loll B. Acta Crystallogr F Struct Biol Commun 71 34-40 (2015)
  9. Structures of bacterial polynucleotide kinase in a michaelis complex with nucleoside triphosphate (NTP)-Mg2+ and 5'-OH RNA and a mixed substrate-product complex with NTP-Mg2+ and a 5'-phosphorylated oligonucleotide. Das U, Wang LK, Smith P, Munir A, Shuman S. J Bacteriol 196 4285-4292 (2014)
  10. An investigation into the role of ATP in the mammalian pre-mRNA 3' cleavage reaction. Khleborodova A, Pan X, Nagre NN, Ryan K. Biochimie 125 213-222 (2016)
  11. Nonradioactive Assay to Measure Polynucleotide Phosphorylation of Small Nucleotide Substrates. Pillon MC, Stanley RE. J Vis Exp (2020)
  12. Systematic Analysis of Diverse Polynucleotide Kinase Clp1 Family Proteins in Eukaryotes: Three Unique Clp1 Proteins of Trypanosoma brucei. Saito M, Inose R, Sato A, Tomita M, Suzuki H, Kanai A. J Mol Evol 91 669-686 (2023)


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