PPR Proteins Shed a New Light on RNase P Biology

Overview

Journal RNA Biol

Specialty Molecular Biology

Date 2013 Aug 9

PMID 23925311

Citations 23

Authors

Franziska Pinker

Geraldine Bonnard

Anthony Gobert

Bernard Gutmann

Kamel Hammani

Claude Sauter

Peter A Gegenheimer

Philippe Giege

Affiliations

Soon will be listed here.

Abstract

A fast growing number of studies identify pentatricopeptide repeat (PPR) proteins as major players in gene expression processes. Among them, a subset of PPR proteins called PRORP possesses RNase P activity in several eukaryotes, both in nuclei and organelles. RNase P is the endonucleolytic activity that removes 5' leader sequences from tRNA precursors and is thus essential for translation. Before the characterization of PRORP, RNase P enzymes were thought to occur universally as ribonucleoproteins, although some evidence implied that some eukaryotes or cellular compartments did not use RNA for RNase P activity. The characterization of PRORP reveals a two-domain enzyme, with an N-terminal domain containing multiple PPR motifs and assumed to achieve target specificity and a C-terminal domain holding catalytic activity. The nature of PRORP interactions with tRNAs suggests that ribonucleoprotein and protein-only RNase P enzymes share a similar substrate binding process.

Citing Articles

The protein-only RNase Ps, endonucleases that cleave pre-tRNA: Biological relevance, molecular architectures, substrate recognition and specificity, and protein interactomes.

Wilhelm C, Kaitany K, Kelly A, Yacoub M, Koutmos M Wiley Interdiscip Rev RNA. 2024; 15(2):e1836.

PMID: 38453211 PMC: 11740979. DOI: 10.1002/wrna.1836.

Discovery, structure, mechanisms, and evolution of protein-only RNase P enzymes.

Rossmanith W, Giege P, Hartmann R J Biol Chem. 2024; 300(3):105731.

PMID: 38336295 PMC: 10941002. DOI: 10.1016/j.jbc.2024.105731.

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.

PMID: 37945696 DOI: 10.1038/s41477-023-01564-0.

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

Vilardo E, Toth U, Hazisllari E, Hartmann R, Rossmanith W Nucleic Acids Res. 2023; 51(19):10536-10550.

PMID: 37779095 PMC: 10602865. DOI: 10.1093/nar/gkad713.

The Dynamic Network of RNP RNase P Subunits.

Shaukat A, Kaliatsi E, Skeparnias I, Stathopoulos C Int J Mol Sci. 2021; 22(19).

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References

Li Y, Altman S . A specific endoribonuclease, RNase P, affects gene expression of polycistronic operon mRNAs. Proc Natl Acad Sci U S A. 2003; 100(23):13213-8. PMC: 263755. DOI: 10.1073/pnas.2235589100. View

Altman S, Wesolowski D, Guerrier-Takada C, Li Y . RNase P cleaves transient structures in some riboswitches. Proc Natl Acad Sci U S A. 2005; 102(32):11284-9. PMC: 1183601. DOI: 10.1073/pnas.0505271102. View

Morales M, Dang Y, Lou Y, Sulo P, Martin N . A 105-kDa protein is required for yeast mitochondrial RNase P activity. Proc Natl Acad Sci U S A. 1992; 89(20):9875-9. PMC: 50236. DOI: 10.1073/pnas.89.20.9875. View

Vilardo E, Nachbagauer C, Buzet A, Taschner A, Holzmann J, Rossmanith W . A subcomplex of human mitochondrial RNase P is a bifunctional methyltransferase--extensive moonlighting in mitochondrial tRNA biogenesis. Nucleic Acids Res. 2012; 40(22):11583-93. PMC: 3526285. DOI: 10.1093/nar/gks910. View

Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere C . Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell. 2004; 16(8):2089-103. PMC: 519200. DOI: 10.1105/tpc.104.022236. View

Bhagwat M, Meara D, Nossal N . Identification of residues of T4 RNase H required for catalysis and DNA binding. J Biol Chem. 1997; 272(45):28531-8. DOI: 10.1074/jbc.272.45.28531. View

Williams-Carrier R, Kroeger T, Barkan A . Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA. 2008; 14(9):1930-41. PMC: 2525963. DOI: 10.1261/rna.1077708. View

Goldfarb K, Borah S, Cech T . RNase P branches out from RNP to protein: organelle-triggered diversification?. Genes Dev. 2012; 26(10):1005-9. PMC: 3360556. DOI: 10.1101/gad.193581.112. View

Gardiner K, Marsh T, Pace N, Altman S . The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell. 1983; 35(3 Pt 2):849-57. DOI: 10.1016/0092-8674(83)90117-4. View

10.

Wang M, Davis N, Gegenheimer P . Novel mechanisms for maturation of chloroplast transfer RNA precursors. EMBO J. 1988; 7(6):1567-74. PMC: 457138. DOI: 10.1002/j.1460-2075.1988.tb02981.x. View

11.

Ojala D, Montoya J, Attardi G . tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981; 290(5806):470-4. DOI: 10.1038/290470a0. View

12.

Marvin M, Engelke D . RNase P: increased versatility through protein complexity?. RNA Biol. 2008; 6(1):40-2. PMC: 2798119. DOI: 10.4161/rna.6.1.7566. View

13.

Manam S, Van Tuyle G . Separation and characterization of 5'- and 3'-tRNA processing nucleases from rat liver mitochondria. J Biol Chem. 1987; 262(21):10272-9. View

14.

Small I, Peeters N . The PPR motif - a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci. 2000; 25(2):46-7. DOI: 10.1016/s0968-0004(99)01520-0. View

15.

Seif E, Cadieux A, Lang B . Hybrid E. coli--Mitochondrial ribonuclease P RNAs are catalytically active. RNA. 2006; 12(9):1661-70. PMC: 1557692. DOI: 10.1261/rna.52106. View

16.

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

17.

Kurz J, Niranjanakumari S, Fierke C . Protein component of Bacillus subtilis RNase P specifically enhances the affinity for precursor-tRNAAsp. Biochemistry. 1998; 37(8):2393-400. DOI: 10.1021/bi972530m. View

18.

Hanic-Joyce P, Gray M . Processing of transfer RNA precursors in a wheat mitochondrial extract. J Biol Chem. 1990; 265(23):13782-91. View

19.

Gobert A, Pinker F, Fuchsbauer O, Gutmann B, Boutin R, Roblin P . Structural insights into protein-only RNase P complexed with tRNA. Nat Commun. 2013; 4:1353. PMC: 3562450. DOI: 10.1038/ncomms2358. View

20.

Rossmanith W, Tullo A, Potuschak T, Karwan R, Sbisa E . Human mitochondrial tRNA processing. J Biol Chem. 1995; 270(21):12885-91. DOI: 10.1074/jbc.270.21.12885. View