Substrate Recognition and Cleavage-site Selection by a Single-subunit Protein-only RNase P

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2016 Feb 21

PMID 26896801

Citations 24

Authors

Nadia Brillante

Markus Gossringer

Dominik Lindenhofer

Ursula Toth

Walter Rossmanith

Roland K Hartmann

Affiliations

Soon will be listed here.

Abstract

RNase P is the enzyme that removes 5' extensions from tRNA precursors. With its diversity of enzyme forms-either protein- or RNA-based, ranging from single polypeptides to multi-subunit ribonucleoproteins-the RNase P enzyme family represents a unique model system to compare the evolution of enzymatic mechanisms. Here we present a comprehensive study of substrate recognition and cleavage-site selection by the nuclear single-subunit proteinaceous RNase P PRORP3 from Arabidopsis thaliana. Compared to bacterial RNase P, the best-characterized RNA-based enzyme form, PRORP3 requires a larger part of intact tRNA structure, but little to no determinants at the cleavage site or interactions with the 5' or 3' extensions of the tRNA. The cleavage site depends on the combined dimensions of acceptor stem and T domain, but also requires the leader to be single-stranded. Overall, the single-subunit PRORP appears mechanistically more similar to the complex nuclear ribonucleoprotein enzymes than to the simpler bacterial RNase P. Mechanistic similarity or dissimilarity among different forms of RNase P thus apparently do not necessarily reflect molecular composition or evolutionary relationship.

Citing Articles

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A tRNA-modifying enzyme facilitates RNase P activity in Arabidopsis nuclei.

Arrive M, Bruggeman M, Skaltsogiannis V, Coudray L, Quan Y, Schelcher C Nat Plants. 2023; 9(12):2031-2041.

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Cleavage kinetics of human mitochondrial RNase P and contribution of its non-nuclease subunits.

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References

Li D, Willkomm D, Hartmann R . Minor changes largely restore catalytic activity of archaeal RNase P RNA from Methanothermobacter thermoautotrophicus. Nucleic Acids Res. 2008; 37(1):231-42. PMC: 2615603. DOI: 10.1093/nar/gkn915. View

Hartmann R, Gossringer M, Spath B, Fischer S, Marchfelder A . The making of tRNAs and more - RNase P and tRNase Z. Prog Mol Biol Transl Sci. 2009; 85:319-68. DOI: 10.1016/S0079-6603(08)00808-8. View

Gutmann B, Gobert A, Giege P . PRORP proteins support RNase P activity in both organelles and the nucleus in Arabidopsis. Genes Dev. 2012; 26(10):1022-7. PMC: 3360558. DOI: 10.1101/gad.189514.112. View

Taschner A, Weber C, Buzet A, Hartmann R, Hartig A, Rossmanith W . Nuclear RNase P of Trypanosoma brucei: a single protein in place of the multicomponent RNA-protein complex. Cell Rep. 2012; 2(1):19-25. PMC: 3807811. DOI: 10.1016/j.celrep.2012.05.021. View

Pinker F, Bonnard G, Gobert A, Gutmann B, Hammani K, Sauter C . PPR proteins shed a new light on RNase P biology. RNA Biol. 2013; 10(9):1457-68. PMC: 3858429. DOI: 10.4161/rna.25273. View

Weber C, Hartig A, Hartmann R, Rossmanith W . Playing RNase P evolution: swapping the RNA catalyst for a protein reveals functional uniformity of highly divergent enzyme forms. PLoS Genet. 2014; 10(8):e1004506. PMC: 4125048. DOI: 10.1371/journal.pgen.1004506. View

Imai T, Nakamura T, Maeda T, Nakayama K, Gao X, Nakashima T . Pentatricopeptide repeat motifs in the processing enzyme PRORP1 in Arabidopsis thaliana play a crucial role in recognition of nucleotide bases at TψC loop in precursor tRNAs. Biochem Biophys Res Commun. 2014; 450(4):1541-6. DOI: 10.1016/j.bbrc.2014.07.030. View

Zhou W, Karcher D, Fischer A, Maximova E, Walther D, Bock R . Multiple RNA processing defects and impaired chloroplast function in plants deficient in the organellar protein-only RNase P enzyme. PLoS One. 2015; 10(3):e0120533. PMC: 4368725. DOI: 10.1371/journal.pone.0120533. View

Howard M, Klemm B, Fierke C . Mechanistic Studies Reveal Similar Catalytic Strategies for Phosphodiester Bond Hydrolysis by Protein-only and RNA-dependent Ribonuclease P. J Biol Chem. 2015; 290(21):13454-64. PMC: 4505592. DOI: 10.1074/jbc.M115.644831. View

10.

Lechner M, Rossmanith W, Hartmann R, Tholken C, Gutmann B, Giege P . Distribution of Ribonucleoprotein and Protein-Only RNase P in Eukarya. Mol Biol Evol. 2015; 32(12):3186-93. DOI: 10.1093/molbev/msv187. View

11.

Thomas B, Li X, Gegenheimer P . Chloroplast ribonuclease P does not utilize the ribozyme-type pre-tRNA cleavage mechanism. RNA. 2000; 6(4):545-53. PMC: 1369935. DOI: 10.1017/s1355838200991465. View

12.

Pfeiffer T, Tekos A, Warnecke J, Drainas D, Engelke D, Seraphin B . Effects of phosphorothioate modifications on precursor tRNA processing by eukaryotic RNase P enzymes. J Mol Biol. 2000; 298(4):559-65. DOI: 10.1006/jmbi.2000.3655. View

13.

Busch S, Kirsebom L, Notbohm H, Hartmann R . Differential role of the intermolecular base-pairs G292-C(75) and G293-C(74) in the reaction catalyzed by Escherichia coli RNase P RNA. J Mol Biol. 2000; 299(4):941-51. DOI: 10.1006/jmbi.2000.3789. View

14.

Ziehler W, Day J, Fierke C, Engelke D . Effects of 5' leader and 3' trailer structures on pre-tRNA processing by nuclear RNase P. Biochemistry. 2000; 39(32):9909-16. DOI: 10.1021/bi000603n. View

15.

Hansen A, Pfeiffer T, Zuleeg T, Limmer S, Ciesiolka J, Feltens R . Exploring the minimal substrate requirements for trans-cleavage by RNase P holoenzymes from Escherichia coli and Bacillus subtilis. Mol Microbiol. 2001; 41(1):131-43. DOI: 10.1046/j.1365-2958.2001.02467.x. View

16.

Zahler N, Christian E, Harris M . Recognition of the 5' leader of pre-tRNA substrates by the active site of ribonuclease P. RNA. 2003; 9(6):734-45. PMC: 1370440. DOI: 10.1261/rna.5220703. View

17.

Crooks G, Hon G, Chandonia J, Brenner S . WebLogo: a sequence logo generator. Genome Res. 2004; 14(6):1188-90. PMC: 419797. DOI: 10.1101/gr.849004. View

18.

Barkan A, Rojas M, Fujii S, Yap A, Chong Y, Bond C . A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet. 2012; 8(8):e1002910. PMC: 3420917. DOI: 10.1371/journal.pgen.1002910. View

19.

Howard M, Lim W, Fierke C, Koutmos M . Mitochondrial ribonuclease P structure provides insight into the evolution of catalytic strategies for precursor-tRNA 5' processing. Proc Natl Acad Sci U S A. 2012; 109(40):16149-54. PMC: 3479547. DOI: 10.1073/pnas.1209062109. View

20.

Pavlova L, Gossringer M, Weber C, Buzet A, Rossmanith W, Hartmann R . tRNA processing by protein-only versus RNA-based RNase P: kinetic analysis reveals mechanistic differences. Chembiochem. 2012; 13(15):2270-6. DOI: 10.1002/cbic.201200434. View