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Archaeal RNase P: A Mosaic of Its Bacterial and Eukaryal Relatives

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Ribonuclease P

Part of the book series: Protein Reviews ((PRON,volume 10))

Abstract

Being a mosaic of its bacterial and eukaryal relatives, archaeal RNase P presents an attractive model for biochemical and structural comparative studies. The archaeal RNase P RNA subunit is more conserved with the bacterial counterpart, but its protein subunits share homology only with those associated with the eukaryal RNase P. This review summarizes recent advances in understanding protein-aided RNA catalysis in archaeal RNase P, and highlights findings that exemplify the diversity of RNase P and the dynamic co-evolution of this catalytic ribonucleoprotein complex.

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References

  • Amero CD, Boomershine WP, Xu Y, Foster M (2008) Solution structure of Pyrococcus furiosus RPP21, a component of the archaeal RNase P holoenzyme, and interactions with its RPP29 protein partner. Biochemistry 47:11704–11710

    Article  PubMed  CAS  Google Scholar 

  • Andrews AJ, Hall TA, Brown JW (2001) Characterization of RNase P holoenzymes from Methanococcus jannaschii and Methanothermobacter thermoautotrophicus. Biol Chem 382:1171–1177

    Article  PubMed  CAS  Google Scholar 

  • Aravind L, Iyer LM, Anantharaman V (2003) The two faces of Alba: the evolutionary connection between proteins participating in chromatin structure and RNA metabolism. Genome Biol 4:R64

    Article  PubMed  CAS  Google Scholar 

  • Barrera A, Pan T (2004) Interaction of the Bacillus subtilis RNase P with the 30 S ribosomal subunit. RNA 10:482–492

    Article  PubMed  CAS  Google Scholar 

  • Boomershine WP, McElroy CA, Tsai HY, Wilson RC, Gopalan V, Foster MP (2003) Structure of Mth11/Mth Rpp 29, an essential protein subunit of archaeal and eukaryotic RNase P. Proc Natl Acad Sci USA 100:15398–15403

    Article  PubMed  CAS  Google Scholar 

  • Brannvall M, Kikovska E, Wu S, Kirsebom LA (2007) Evidence for induced fit in bacterial RNase P RNA-mediated cleavage. J Mol Biol 372:1149–1164

    Article  PubMed  CAS  Google Scholar 

  • Brown JW (1999) The ribonuclease P database. Nucleic Acids Res 27:314

    Article  PubMed  CAS  Google Scholar 

  • Chamberlain JR, Lee Y, Lane WS, Engelke DR (1998) Purification and characterization of the nuclear RNase P holoenzyme complex reveals extensive subunit overlap with RNase MRP. Genes Dev 12:1678–1690

    Article  PubMed  CAS  Google Scholar 

  • Chen JL, Nolan JM, Harris ME, Pace NR (1998) Comparative photocross-linking analysis of the tertiary structures of Escherichia coli and Bacillus subtilis RNase P RNAs. EMBO J 17:1515–1525

    Article  PubMed  CAS  Google Scholar 

  • Christian EL, Smith KM, Perera N, Harris ME (2006) The P4 metal binding site in RNase P RNA affects active site metal affinity through substrate positioning. RNA 12:1463–1467

    Article  PubMed  CAS  Google Scholar 

  • Crary SM, Niranjanakumari S, Fierke CA (1998) The protein component of Bacillus subtilis ribonuclease P increases catalytic efficiency by enhancing interactions with the 5′ leader sequence of pre-tRNAAsp. Biochemistry 37:9409–9416

    Article  PubMed  CAS  Google Scholar 

  • Darr SC, Pace B, Pace NR (1990) Characterization of ribonuclease P from the archaebacterium Sulfolobus solfataricus. J Biol Chem 265:12927–12932

    PubMed  CAS  Google Scholar 

  • Eder PS, Kekuda R, Stolc V, Altman S (1997) Characterization of two scleroderma autoimmune antigens that copurify with human ribonuclease P. Proc Natl Acad Sci USA 94:1101–1106

    Article  PubMed  CAS  Google Scholar 

  • Ellis JC, Brown JW (2003) Genes within genes within bacteria. Trends Biochem Sci 28:521–523

    Google Scholar 

  • Ellis JC, Barnes J, Brown JW (2007) Is Alba an RNase P subunit? RNA Biol 4:169–172

    PubMed  CAS  Google Scholar 

  • Fukuhara H, Kifusa M, Watanabe M, Terada A, Honda T, Numata T, Kakuta Y, Kimura M (2006) A fifth protein subunit Ph1496p elevates the optimum temperature for the ribonuclease P activity from Pyrococcus horikoshii OT3. Biochem Biophys Res Commun 343:956–964

    Article  PubMed  CAS  Google Scholar 

  • Gil MA, Sherwood KE, Maupin-Furlow JA (2007) Transcriptional linkage of Haloferax volcanii proteasomal genes with non-proteasomal gene neighbours including RNase P, MOSC domain and SAM-methyltransferase homologues. Microbiology 153:3009–3022

    Article  PubMed  CAS  Google Scholar 

  • Gopalan V, Altman S (2006) Ribonuclease P: structure and catalysis. In: Gesteland RF, Cech TR, Atlkins JF (eds) The RNA world. Cold Spring Harbor Laboratory Press, New York (only online at http://rna.cshl.edu)

  • Gopalan V (2007) Uniformity amid diversity in RNase P. Proc Natl Acad Sci USA 104:2031–2032

    Article  PubMed  CAS  Google Scholar 

  • Gossringer M, Hartmann RK (2007) Function of heterologous and truncated RNase P proteins in Bacillus subtilis. Mol Microbiol 66:801–813

    Article  CAS  Google Scholar 

  • Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35:849–857

    Article  PubMed  CAS  Google Scholar 

  • Guerrier-Takada C, Altman S (2000) Inactivation of gene expression using ribonuclease P and external guide sequences. Methods Enzymol 313:442–456

    Article  PubMed  CAS  Google Scholar 

  • Hada K, Nakashima T, Osawa T, Shimada H, Kakuta Y, Kimura M (2008) Crystal structure and functional analysis of an archaeal chromatin protein Alba from the hyperthermophilic archaeon Pyrococcus horikoshii OT3. Biosci Biotechnol Biochem 72:749–758

    Article  PubMed  CAS  Google Scholar 

  • Hall TA, Brown JW (2001) The ribonuclease P family. Methods Enzymol 341:56–77

    Article  PubMed  CAS  Google Scholar 

  • Hall TA, Brown JW (2002) Archaeal RNase P has multiple protein subunits homologous to eukaryotic nuclear RNase P proteins. RNA 8:296–306

    Article  PubMed  CAS  Google Scholar 

  • Hall TA, Brown JW (2004) Interactions between RNase P protein subunits in archaea. Archaea 1:247–254

    Article  PubMed  CAS  Google Scholar 

  • Hamilton MG, Kivie M, Lawrence G (1971) Isodensity equilibrium centrifugation of ribosomal particles; the calculation of the protein content of ribosomes and other ribonucleo-proteins from buoyant density measurements. Methods Enzymol 20:512–521

    Article  Google Scholar 

  • Hansen FG, Hansen EB, Atlung T (1985) Physical mapping and nucleotide sequence of the rnpA gene that encodes the protein component of ribonuclease P in Escherichia coli. Gene 38:85–93

    Article  PubMed  CAS  Google Scholar 

  • Harris JK, Haas ES, Williams D, Frank DN, Brown JW (2001) New insight into RNase P RNA structure from comparative analysis of the archaeal RNA. RNA 7:220–232

    Article  PubMed  CAS  Google Scholar 

  • Harris ME, Christian EL (2003) Recent insights into the structure and function of the ribonucleoprotein enzyme ribonuclease P. Curr Opin Struct Biol 13:325–333

    Article  PubMed  CAS  Google Scholar 

  • Hartmann E, Hartmann RK (2003) The enigma of ribonuclease P evolution. Trends Genet 19:561–569

    Article  PubMed  CAS  Google Scholar 

  • Holzmann J, Frank P, Loffler E, Bennett KL, Gerner C, Rossmanith W (2008) RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 135:462–474

    Article  PubMed  CAS  Google Scholar 

  • Honda T, Kakuta Y, Kimura K, Saho J, Kimura M (2008) Structure of an archaeal homolog of the human protein complex Rpp 21-Rpp29 that is a key core component for the assembly of active ribonuclease P. J Mol Biol 384:652–662

    Article  PubMed  CAS  Google Scholar 

  • Houser-Scott F, Xiao S, Millikin CE, Zengel JM, Lindahl L, Engelke DR (2002) Interactions among the protein and RNA subunits of Saccharomyces cerevisiae nuclear RNase P. Proc Natl Acad Sci USA 99:2684–2689

    Article  PubMed  CAS  Google Scholar 

  • Jarrous N, Wolenski JS, Wesolowski D, Lee C, Altman S (1999) Localization in the nucleolus and coiled bodies of protein subunits of the ribonucleoprotein ribonuclease P. J Cell Biol 146:559–572

    Article  PubMed  CAS  Google Scholar 

  • Jarrous N (2002) Human ribonuclease P: subunits, function, and intranuclear localization. RNA 8:1–7

    Article  PubMed  CAS  Google Scholar 

  • Jiang T, Altman S (2001) Protein-protein interactions with subunits of human nuclear RNase P. Proc Natl Acad Sci USA 98:920–925

    Article  PubMed  CAS  Google Scholar 

  • Kakuta Y, Ishimatsu I, Numata T, Kimura K, Yao M, Tanaka I, Kimura M (2005) Crystal structure of a ribonuclease P protein Ph1601p from Pyrococcus horikoshii OT3: an archaeal homologue of human nuclear ribonuclease P protein Rpp 21. Biochemistry 44:12086–12093

    Article  PubMed  CAS  Google Scholar 

  • Kawamoto SA, Sudhahar CG, Hatfield CL, Sun J, Behrman EJ, Gopalan V (2008) Studies on the mechanism of inhibition of bacterial ribonuclease P by aminoglycoside derivatives. Nucleic Acids Res 36:697–704

    Article  PubMed  CAS  Google Scholar 

  • Kawano S, Nakashima T, Kakuta Y, Tanaka I, Kimura M (2006) Crystal structure of protein Ph1481p in complex with protein Ph1877p of archaeal RNase P from Pyrococcus horikoshii OT3: implication of dimer formation of the holoenzyme. J Mol Biol 357:583–591

    Article  PubMed  CAS  Google Scholar 

  • Kaye NM, Zahler NH, Christian EL, Harris ME (2002) Conservation of helical structure contributes to functional metal ion interactions in the catalytic domain of ribonuclease P RNA. J Mol Biol 324:429–442

    Article  PubMed  CAS  Google Scholar 

  • Kazantsev AV, Krivenko AA, Harrington DJ, Holbrook SR, Adams PD, Pace NR (2005) Crystal structure of a bacterial ribonuclease P RNA. Proc Natl Acad Sci USA 102:13392–13397

    Article  PubMed  CAS  Google Scholar 

  • Kifusa M, Fukuhara H, Hayashi T, Kimura M (2005) Protein-protein interactions in the subunits of ribonuclease P in the hyperthermophilic archaeon Pyrococcus horikoshii OT3. Biosci Biotechnol Biochem 69:1209–1212

    Article  PubMed  CAS  Google Scholar 

  • Kikovska E, Svard SG, Kirsebom LA (2007) Eukaryotic RNase P RNA mediates cleavage in the absence of protein. Proc Natl Acad Sci USA 104:2062–2067

    Article  PubMed  CAS  Google Scholar 

  • Kirsebom LA, Svard SG (1994) Base pairing between Escherichia coli RNase P RNA and its substrate. EMBO J 13:4870–4876

    PubMed  CAS  Google Scholar 

  • Kirsebom LA (2007) RNase P RNA mediated cleavage: substrate recognition and catalysis. Biochimie 89:1183–1194

    Article  PubMed  CAS  Google Scholar 

  • Koonin EV, Wolf YI, Aravind L (2001) Prediction of the archaeal exosome and its connections with the proteasome and the translation and transcription machineries by a comparative-genomic approach. Genome Res 11:240–252

    Article  PubMed  CAS  Google Scholar 

  • Kouzuma Y, Mizoguchi M, Takagi H, Fukuhara H, Tsukamoto M, Numata T, Kimura M (2003) Reconstitution of archaeal ribonuclease P from RNA and four protein components. Biochem Biophys Res Commun 306:666–673

    Article  PubMed  CAS  Google Scholar 

  • Krasilnikov AS, Xiao Y, Pan T, Mondragon A (2004) Basis for structural diversity in homologous RNAs. Science 306:104–107

    Article  PubMed  CAS  Google Scholar 

  • Kurz JC, Fierke CA (2002) The affinity of magnesium binding sites in the Bacillus subtilis RNase P x pre-tRNA complex is enhanced by the protein subunit. Biochemistry 41:9545–9558

    Article  PubMed  CAS  Google Scholar 

  • LaGrandeur TE, Darr SC, Haas ES, Pace NR (1993) Characterization of the RNase P RNA of Sulfolobus acidocaldarius. J Bacteriol 175:5043–5048

    PubMed  CAS  Google Scholar 

  • Lai LB, Chan PP, Cozen AE, Bernick DL, Brown JW, Gopalan V, Lowe T (2009) Discovery of the elusive Pyrobaculum RNase P: An unexpected form of an ancient RNA. Manuscript under review

    Google Scholar 

  • Lawrence N, Wesolowski D, Gold H, Bartkiewicz M, Guerrier-Takada C, McClain WH, Altman S (1987) Characteristics of ribonuclease P from various organisms. Cold Spring Harb Symp Quant Biol 52:233–238

    PubMed  CAS  Google Scholar 

  • Lentzen G, Schwarz T (2006) Extremolytes: Natural compounds from extremophiles for versatile applications. Appl Microbiol Biotechnol 72:623–634

    Article  PubMed  CAS  Google Scholar 

  • Li D, Willkomm DK, Hartmann RK (2009) Minor changes largely restore catalytic activity of archaeal RNase P RNA from Methanothermobacter thermoautotrophicus. Nucleic Acids Res 37(1):231–242

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Altman S (2004) In search of RNase P RNA from microbial genomes. RNA 10:1533–1540

    Article  PubMed  CAS  Google Scholar 

  • Loria A, Pan T (1996) Domain structure of the ribozyme from eubacterial ribonuclease P. RNA 2:551–563

    PubMed  CAS  Google Scholar 

  • Mann H, Ben-Asouli Y, Schein A, Moussa S, Jarrous N (2003) Eukaryotic RNase P: role of RNA and protein subunits of a primordial catalytic ribonucleoprotein in RNA-based catalysis. Mol Cell 12:925–935

    Article  PubMed  CAS  Google Scholar 

  • Marquez SM, Evans D, Kazantsev AV, Pace NR (2008) A structural analysis of ribonuclease P. In: Lilley DMJ, Eckstein F (eds) Ribozymes and RNA catalysis. RSC Publishing, Cambridge, pp 153–177

    Google Scholar 

  • Massire C, Jaeger L, Westhof E (1998) Derivation of the three-dimensional architecture of bacterial ribonuclease P RNAs from comparative sequence analysis. J Mol Biol 279:773–793

    Article  PubMed  CAS  Google Scholar 

  • Nieuwlandt DT, Haas ES, Daniels CJ (1991) The RNA component of RNase P from the archaebacterium Haloferax volcanii. J Biol Chem 266:5689–5695

    PubMed  CAS  Google Scholar 

  • Niranjanakumari S, Stams T, Crary SM, Christianson DW, Fierke CA (1998) Protein component of the ribozyme ribonuclease P alters substrate recognition by directly contacting precursor tRNA. Proc Natl Acad Sci USA 95:15212–15217

    Article  PubMed  CAS  Google Scholar 

  • Numata T, Ishimatsu I, Kakuta Y, Tanaka I, Kimura M (2004) Crystal structure of archaeal ribonuclease P protein Ph1771p from Pyrococcus horikoshii OT3: an archaeal homolog of eukaryotic ribonuclease P protein Rpp 29. RNA 10:1423–1432

    Article  PubMed  CAS  Google Scholar 

  • Oh BK, Pace NR (1994) Interaction of the 3′-end of tRNA with ribonuclease P RNA. Nucleic Acids Res 22:4087–4094

    Article  PubMed  CAS  Google Scholar 

  • Pan T, Loria A, Zhong K (1995) Probing of tertiary interactions in RNA: 2′-hydroxyl-base contacts between the RNase P RNA and pre-tRNA. Proc Natl Acad Sci USA 92:12510–12514

    Article  PubMed  CAS  Google Scholar 

  • Pannucci JA, Haas ES, Hall TA, Harris JK, Brown JW (1999) RNase P RNAs from some Archaea are catalytically active. Proc Natl Acad Sci USA 96:7803–7808

    Article  PubMed  CAS  Google Scholar 

  • Pulukkunat DK, Gopalan V (2008) Studies on Methanocaldococcus jannaschii RNase P reveal insights into the roles of RNA and protein cofactors in RNase P catalysis. Nucleic Acids Res 36:4172–4180

    Article  PubMed  CAS  Google Scholar 

  • Randau L, Schroder I, Soll D (2008) Life without RNase P. Nature 453:120–123

    Article  PubMed  CAS  Google Scholar 

  • Sidote DJ, Hoffman DW (2003) NMR structure of an archaeal homologue of ribonuclease P protein Rpp 29. Biochemistry 42:13541–13550

    Article  PubMed  CAS  Google Scholar 

  • Sidote DJ, Heideker J, Hoffman DW (2004) Crystal structure of archaeal ribonuclease P protein aRpp 29 from Archaeoglobus fulgidus. Biochemistry 43:14128–14138

    Article  PubMed  CAS  Google Scholar 

  • Stams T, Niranjanakumari S, Fierke CA, Christianson DW (1998) Ribonuclease P protein structure: evolutionary origins in the translational apparatus. Science 280:752–755

    Article  PubMed  CAS  Google Scholar 

  • Sun L, Campbell FE, Zahler NH, Harris ME (2006) Evidence that substrate-specific effects of C5 protein lead to uniformity in binding and catalysis by RNase P. EMBO J 25:3998–4007

    Article  PubMed  CAS  Google Scholar 

  • Sun L, Harris ME (2007) Evidence that binding of C5 protein to P RNA enhances ribozyme catalysis by influencing active site metal ion affinity. RNA 13:1505–1515

    Article  PubMed  CAS  Google Scholar 

  • Takagi H, Watanabe M, Kakuta Y, Kamachi R, Numata T, Tanaka I, Kimura M (2004) Crystal structure of the ribonuclease P protein Ph1877p from hyperthermophilic archaeon Pyrococcus horikoshii OT3. Biochem Biophys Res Commun 319:787–794

    Article  PubMed  CAS  Google Scholar 

  • Terada A, Honda T, Fukuhara H, Hada K, Kimura M (2006) Characterization of the archaeal ribonuclease P proteins from Pyrococcus horikoshii OT3. J Biochem 140:293–298

    Article  PubMed  CAS  Google Scholar 

  • Terada A, Yoshida T, Kimura M (2007) Identification of nucleotide residues essential for RNase P activity from the hyperthermophilic archaeon Pyrococcus horikoshii OT3. Biosci Biotechnol. Biochem. 71:1940–1945

    Article  PubMed  CAS  Google Scholar 

  • Torres-Larios A, Swinger KK, Krasilnikov AS, Pan T, Mondragon A (2005) Crystal structure of the RNA component of bacterial ribonuclease P. Nature 437:584–587

    Article  PubMed  CAS  Google Scholar 

  • Tsai HY, Masquida B, Biswas R, Westhof E, Gopalan V (2003) Molecular modeling of the three-dimensional structure of the bacterial RNase P holoenzyme. J Mol Biol 325:661–675

    Article  PubMed  CAS  Google Scholar 

  • Tsai HY, Pulukkunat DK, Woznick WK, Gopalan V (2006) Functional reconstitution and characterization of Pyrococcus furiosus RNase P. Proc Natl Acad Sci USA 103:16147–16152

    Article  PubMed  CAS  Google Scholar 

  • Ushida C, Muramatsu T, Mizushima H, Ueda T, Watanabe K, Stetter KO, Crain PF, McCloskey JA, Kuchino Y (1996) Structural feature of the initiator tRNA gene from Pyrodictium occultum and the thermal stability of its gene product, tRNA(imet). Biochimie 78:847–855

    Article  PubMed  CAS  Google Scholar 

  • Vioque A, Arnez J, Altman S (1988) Protein-RNA interactions in the RNase P holoenzyme from Escherichia coli. J Mol Biol 202:835–848

    Article  PubMed  CAS  Google Scholar 

  • Walker SC, Engelke DR (2006) Ribonuclease P: the evolution of an ancient RNA enzyme. Crit Rev Biochem Mol Biol 41:77–102

    Article  PubMed  CAS  Google Scholar 

  • Wilson RC, Bohlen CJ, Foster MP, Bell CE (2006) Structure of Pfu Pop5, an archaeal RNase P protein. Proc Natl Acad Sci USA 103:873–878

    Article  PubMed  CAS  Google Scholar 

  • Xiao S, Day-Storms JJ, Srisawat C, Fierke CA, Engelke DR (2005) Characterization of conserved sequence elements in eukaryotic RNase P RNA reveals roles in holoenzyme assembly and tRNA processing. RNA 11:885–896

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to Mark P. Foster (OSU) for assistance with preparation of Fig. 9.2 and for valuable discussions. The author, Venkat Gopalan, acknowledges support from the NSF (MCB-0238233 and MCB-0843543) and the NIH (GM067947 to MPF and VG).

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Authors and Affiliations

  1. Department of Biochemistry, The Center for RNA Biology, The Ohio State University, Columbus, OH, 43210, USA

    Lien B. Lai, I-Ming Cho, Wen-Yi Chen & Venkat Gopalan

  2. Department of Molecular Genetics, The Ohio State University, Columbus, OH, 43210, USA

    I-Ming Cho & Venkat Gopalan

  3. The Molecular Cellular and Developmental Biology Program, The Ohio State University, Columbus, OH, 43210, USA

    Wen-Yi Chen & Venkat Gopalan

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  1. Lien B. Lai
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  2. I-Ming Cho
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  3. Wen-Yi Chen
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Correspondence to Venkat Gopalan .

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Editors and Affiliations

  1. School of Public Health, University of California, Berkeley, Warren Hall 140, Berkeley, 94720, U.S.A.

    Fenyong Liu

  2. Dept. Molecular, Cellular &, Yale University, Whitney Avenue 266, New Haven, 06520-8104, U.S.A.

    Sidney Altman

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Lai, L.B., Cho, IM., Chen, WY., Gopalan, V. (2010). Archaeal RNase P: A Mosaic of Its Bacterial and Eukaryal Relatives. In: Liu, F., Altman, S. (eds) Ribonuclease P. Protein Reviews, vol 10. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1142-1_9

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