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Structural Studies of Ribonuclease P

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Ribonuclease P

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

Abstract

RNase P is a universal ribozyme involved in RNA processing, in particular the maturation of the 5′ end of tRNA. Unlike most naturally occurring ribozymes, it recognizes and cleaves its substrate in trans and is capable of multiple turnovers. RNase P is a ribonucleoprotein complex containing one RNA subunit and as few as one protein subunit. The RNA subunit alone can support catalysis in vitro. In recent years, structures of the specificity domain and of the entire RNA component of RNase P from two different bacteria have been described and provide the first atomic level information on the structure of the RNA component. Structures of the protein component of different bacteria as well as the structures of several of the protein components of archaeal organisms have also been elucidated. Despite all these structural studies of the RNA component and the protein components, the catalytic mechanism of action and the way RNase P recognizes its substrate are still not fully understood at the atomic level. Nevertheless, all these structures start to provide an atomic level understanding of the architecture of RNase P and help to clarifying the relationships between RNase P from all organisms.

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References

  • Adams PL, Stahley MR, Kosek AB, Wang J, Strobel SA (2004) Crystal structure of a self-splicing group I intron with both exons. Nature 430:45–50

    Article  CAS  PubMed  Google Scholar 

  • Alifano P, Rivellini F, Piscitelli C, Arraiano CM, Bruni CB, Carlomagno MS (1994) Ribonuclease E provides substrates for ribonuclease P-dependent processing of a polycistronic mRNA. Genes Dev 8:3021–3231

    Article  CAS  PubMed  Google Scholar 

  • Altman S, Kirsebom LA (1999) In: Gesteland RF, Cech TR, Atkins JF (eds) The RNA world. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 351–380

    Google Scholar 

  • Altman S, Wesolowski D, Guerrier-Takada C, Li Y (2005) RNase P cleaves transient structures in some riboswitches. Proc Natl Acad Sci U S A 102:11284–11289

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Beebe JA, Kurz JC, Fierke CA (1996) Magnesium ions are required by Bacillus subtilis ribonuclease P RNA for both binding and cleaving precursor tRNAAsp. Biochemistry 35:10493–10505

    Article  CAS  PubMed  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 U S A 100:15398–15403

    Article  CAS  PubMed  Google Scholar 

  • Buck AH, Kazantsev AV, Dalby AB, Pace NR (2005) Structural perspective on the activation of RNase P RNA by protein. Nat Struct Mol Biol 12(11):958–964

    CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Chen J-L, Pace NR (1997) Identification of the universally conserved core of ribonuclease P RNA. RNA 3:557–560

    CAS  PubMed  Google Scholar 

  • Christian EL, Zahler NH, Kaye NM, Harris ME (2002) Analysis of substrate recognition by the ribonucleoprotein endonuclease RNase P. Methods 28:307–322

    Article  CAS  PubMed  Google Scholar 

  • Costa M, Michel F (1995) Frequent use of the same tertiary motif by self-folding RNAs. EMBO J 14:1276–1285

    CAS  PubMed  Google Scholar 

  • Doudna JA, Cech TR (1995) Self-assembly of a group I intron active site from its component tertiary structural domains. RNA 1:36–45

    CAS  PubMed  Google Scholar 

  • Evans D, Marquez SM, Pace NR (2006) RNase P: interface of the RNA and protein worlds. Trends Biochem Sci 31:333–341

    Article  CAS  PubMed  Google Scholar 

  • Fang XW, Pan T, Sosnick TR (1999) Mg2+-dependent folding of a large ribozyme without kinetic traps. Nat Struct Biol 6:1091–1095

    Article  CAS  PubMed  Google Scholar 

  • Frank DN, Pace NR (1998) Ribonuclease P: unity and diversity in a tRNA processing ribozyme. Annu Rev Biochem 67:153–180

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Getz MM, Andrews AJ, Fierke CA, Al-Hashimi HM (2007) Structural plasticity and Mg2+ binding properties of RNase P P4 from combined analysis of NMR residual dipolar couplings and motionally decoupled spin relaxation. RNA 13:251–266

    Article  CAS  PubMed  Google Scholar 

  • Golden BL, Kim H, Chase E (2005) Crystal structure of a phage Twort group I ribozyme-product complex. Nat Struct Mol Biol 12:82–89

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Guo F, Gooding AR, Cech TR (2004) Structure of the Tetrahymena ribozyme: base triple sandwich and metal ion at the active site. Mol Cell 16:351–362

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Harris ME, Nolan JM, Malhotra A, Brown JW, Harvey SC, Pace NR (1994) Use of photoaffinity crosslinking and molecular modeling to analyze the global architecture of ribonuclease P RNA. EMBO J 13:3953–3963

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hartmann RK, Heinrich J, Schlegl J, Schuster H (1995) Precursor of C4 antisense RNA of bacteriophages P1 and P7 is a substrate for RNase P of Escherichia coli. Proc Natl Acad Sci U S A 92:5822–5826

    Article  CAS  PubMed  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  CAS  PubMed  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 U S A 99:2684–2689

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Kazantsev AV, Pace NR (2006) Bacterial RNase P: a new view of an ancient enzyme. Nat Rev Microbiol 4:729–740

    Article  CAS  PubMed  Google Scholar 

  • Kazantsev AV, Krivenko AA, Harrington DJ, Carter RJ, Holbrook SR, Adams PD, Pace NR (2003) High-resolution structure of RNase P protein from Thermotoga maritima. Proc Natl Acad Sci U S A 100:7497–7502

    Article  CAS  PubMed  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 U S A 102:13392–13397

    Article  CAS  PubMed  Google Scholar 

  • Kazantsev AV, Krivenko AA, Pace NR (2009) Mapping metal-binding sites in the catalytic domain of bacterial RNase P RNA. RNA 15:266–276

    Article  CAS  PubMed  Google Scholar 

  • Kent O, Chaulk SG, MacMillan AM (2000) Kinetic analysis of the M1 RNA folding pathway. J Mol Biol 304:699–705

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Komine Y, Kitabatake M, Yokogawa T, Nishikawa K, Inokuchi H (1994) A tRNA-like structure is present in 10Sa RNA, a small stable RNA from Escherichia coli. Proc Natl Acad Sci U S A 91:9223–9227

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Krasilnikov AS, Mondragon A (2003) On the occurrence of the T-loop RNA folding motif in large RNA molecules. RNA 9:640–643

    Article  CAS  PubMed  Google Scholar 

  • Krasilnikov AS, Yang X, Pan T, Mondragón A (2003) Crystal structure of the specificity domain of ribonuclease P. Nature 421:760–764

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kurz JC, Fierke CA (2000) Ribonuclease P: a ribonucleoprotein enzyme. Curr Opin Chem Biol 4:553–558

    Article  CAS  PubMed  Google Scholar 

  • LaGrandeur TE, Huttenhofer A, Noller HF, Pace NR (1994) Phylogenetic comparative chemical footprint analysis of the interaction between ribonuclease P RNA and tRNA. EMBO J 13:3945–3952

    CAS  PubMed  Google Scholar 

  • Lee JC, Cannone JJ, Gutell RR (2003) The lonepair triloop: a new motif in RNA structure. J Mol Biol 325:65–83

    Article  CAS  PubMed  Google Scholar 

  • Leeper TC, Martin MB, Kim H, Cox S, Semenchenko V, Schmidt FJ, Van Doren SR (2002) Structure of the UGAGAU hexaloop that braces Bacillus RNase P for action. Nat Struct Biol 9:397–403

    CAS  PubMed  Google Scholar 

  • Li Y, Altman S (2003) A specific endoribonuclease, RNase P, affects gene expression of polycistronic operon mRNAs. Proc Natl Acad Sci U S A 100:13213–13218

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Loria A, Pan T (1997) Recognition of the T stem-loop of a pre-tRNA substrate by the ribozyme from Bacillus subtilis ribonuclease P. Biochemistry 36:6317–6325

    Article  CAS  PubMed  Google Scholar 

  • Mans RM, Guerrier-Takada C, Altman S, Pleij CW (1990) Interaction of RNase P from Escherichia coli with pseudoknotted structures in viral RNAs. Nucleic Acids Res 18:3479–3487

    Article  CAS  PubMed  Google Scholar 

  • Marquez SM, Chen JL, Evans D, Pace NR (2006) Structure and function of eukaryotic ribonuclease P RNA. Mol Cell 24:445–456

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Nagaswamy U, Fox GE (2002) Frequent occurrence of the T-loop RNA folding motif in ribosomal RNAs. RNA 8:1112–1119

    Article  CAS  PubMed  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 U S A 95:15212–15217

    Article  CAS  PubMed  Google Scholar 

  • Nissen P, Ippolito JA, Ban N, Moore PB, Steitz TA (2001) RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc Natl Acad Sci U S A 98:4899–4903

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Odell L, Huang V, Jakacka M, Pan T (1998) Interaction of structural modules in substrate binding by the ribozyme from Bacillus subtilis RNase P. Nucleic Acids Res 26:3717–3723

    Article  CAS  PubMed  Google Scholar 

  • Pan T (1995) Higher order folding and domain analysis of the ribozyme from Bacillus subtilis ribonuclease P. Biochemistry 34:902–909

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Peck-Miller KA, Altman S (1991) Kinetics of the processing of the precursor to 4.5 S RNA, a naturally occurring substrate for RNase P from Escherichia coli. J Mol Biol 221:1–5

    Article  CAS  PubMed  Google Scholar 

  • Persson T, Cuzic S, Hartmann RK (2003) Catalysis by RNase P RNA: unique features and unprecedented active site plasticity. J Biol Chem 278:43394–43401

    Article  CAS  PubMed  Google Scholar 

  • Schmitz M, Tinoco I Jr (2000) Solution structure and metal-ion binding of the P4 element from bacterial RNase P RNA. RNA 6:1212–1225

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Siegel RW, Banta AB, Haas ES, Brown JW, Pace NR (1996) Mycoplasma fermentans simplifies our view of the catalytic core of ribonuclease P RNA. RNA 2:452–462

    CAS  PubMed  Google Scholar 

  • Smith D, Pace NR (1993) Multiple magnesium ions in the ribonuclease P reaction mechanism. Biochemistry 32:5273–5281

    Article  CAS  PubMed  Google Scholar 

  • Spitzfaden C, Nicholson N, Jones JJ, Guth S, Lehr R, Prescott CD, Hegg LA, Eggleston DS (2000) The structure of ribonuclease P protein from Staphylococcus aureus reveals a unique binding site for single-stranded RNA. J Mol Biol 295:105–115

    Article  CAS  PubMed  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  CAS  PubMed  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Torres-Larios A, Swinger KK, Pan T, Mondragon A (2006) Structure of ribonuclease P – a universal ribozyme. Curr Opin Struct Biol 16:327–335

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Vicens Q, Cech TR (2006) Atomic level architecture of group I introns revealed. Trends Biochem Sci 31(1):41–51

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Waugh DS, Pace NR (1990) Complementation of an RNase P RNA (rnpB) gene deletion in Escherichia coli by homologous genes from distantly related eubacteria. J Bacteriol 172:6316–6322

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Woodson SA (2005) Structure and assembly of group I introns. Curr Opin Struct Biol 15:324–330

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry, Molecular Biology, and Cell Biology, Northwestern University, 2205 Tech Drive, Evanston, IL, 60208, USA

    Alfonso Mondragón

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  1. Alfonso Mondragón
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Correspondence to Alfonso Mondragón .

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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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Mondragón, A. (2010). Structural Studies of Ribonuclease P. 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_4

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