Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA

Reiter, Nicholas J.; Osterman, Amy; Torres‐Larios, Alfredo; Swinger, Kerren K.; Pan, Tao; Mondragón, Alfonso

doi:10.1038/nature09516

Cited by 262 publications

(493 citation statements)

References 54 publications

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“…1A; Reiter et al 2010). The overall architecture of the Thermotoga maritima RNase P holoenzyme structure is strikingly similar to previous low-resolution models of the B. subtilis and Bacillus stearothermophilus enzymes derived from biochemical data (Buck et al 2005b;Niranjanakumari et al 2007).…”

Section: Introductionsupporting

confidence: 76%

“…In the structure of the RNasePdtRNAdleader complex, the leader directly contacts the protein central cleft, consistent with cross-linking, time-resolved fluorescence resonance energy transfer, and binding studies of P protein-substrate interactions in B. subtilis and E. coli RNase P (Crary et al 1998;Niranjanakumari et al 1998b;Rueda et al 2005;Sun et al 2006;Koutmou et al 2010). Additionally, together with biochemical evidence the recent X-ray data indicate that the RNR motif of the P protein in the RNase P d pre-tRNA complex is positioned near helices P2-P4 of PRNA and both the 59 leader and 39 end of pre-tRNA (Niranjanakumari et al 2007;Reiter et al 2010). (Reiter et al 2010).…”

Section: Introductionsupporting

confidence: 67%

“…Additionally, together with biochemical evidence the recent X-ray data indicate that the RNR motif of the P protein in the RNase P d pre-tRNA complex is positioned near helices P2-P4 of PRNA and both the 59 leader and 39 end of pre-tRNA (Niranjanakumari et al 2007;Reiter et al 2010). (Reiter et al 2010). (Blue) PRNA; (red) P protein; (green) tRNA.…”

Section: Introductionmentioning

confidence: 92%

“…The central cleft is formed by the central b-sheet and an a-helix (Stams et al 1998). Time-resolved FRET (trFRET), affinity cleavage, cross-linking, structure variation, and crystallographic data provide evidence that the central cleft interacts with the 59 leader of pretRNA to enhance substrate recruitment and discrimination (Crary et al 1998;Kurz et al 1998;Rueda et al 2005;Niranjanakumari et al 2007;Koutmou et al 2010;Reiter et al 2010;Sun et al 2010). The second region of the protein identified as potentially important for RNA binding is the a-helix of an unusual left-handed bab crossover connection between parallel b-strands of the central cleft.…”

Section: Introductionmentioning

confidence: 99%

“…In the crystal structure, the P protein contacts the catalytic domain of PRNA at the interface of helices P2/P3, one side of helix P15, and the conserved regions CR-IV and CR-V ( Fig. 1A,C ;Reiter et al 2010). In the structure of the RNasePdtRNAdleader complex, the leader directly contacts the protein central cleft, consistent with cross-linking, time-resolved fluorescence resonance energy transfer, and binding studies of P protein-substrate interactions in B. subtilis and E. coli RNase P (Crary et al 1998;Niranjanakumari et al 1998b;Rueda et al 2005;Sun et al 2006;Koutmou et al 2010).…”

Section: Introductionmentioning

confidence: 99%

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The RNR motif of B. subtilis RNase P protein interacts with both PRNA and pre-tRNA to stabilize an active conformer

Koutmou¹,

Day-Storms²,

Fierke³

2011

RNA

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Ribonuclease P (RNase P) catalyzes the metal-dependent 59 end maturation of precursor tRNAs (pre-tRNAs). In Bacteria, RNase P is composed of a catalytic RNA (PRNA) and a protein subunit (P protein) necessary for function in vivo. The P protein enhances pre-tRNA affinity, selectivity, and cleavage efficiency, as well as modulates the cation requirement for RNase P function. Bacterial P proteins share little sequence conservation although the protein structures are homologous. Here we combine site-directed mutagenesis, affinity measurements, and single turnover kinetics to demonstrate that two residues (R60 and R62) in the most highly conserved region of the P protein, the RNR motif (R60-R68 in Bacillus subtilis), stabilize PRNA complexes with both P protein (PRNAdP protein) and pre-tRNA (PRNAdP proteindpre-tRNA). Additionally, these data indicate that the RNR motif enhances a metal-stabilized conformational change in RNase P that accompanies substrate binding and is essential for efficient catalysis. Stabilization of this conformational change contributes to both the decreased metal requirement and the enhanced substrate recognition of the RNase P holoenzyme, illuminating the role of the most highly conserved region of P protein in the RNase P reaction pathway.

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Section: Introductionsupporting

confidence: 76%

Section: Introductionsupporting

confidence: 67%

Section: Introductionmentioning

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

The RNR motif of B. subtilis RNase P protein interacts with both PRNA and pre-tRNA to stabilize an active conformer

Koutmou¹,

Day-Storms²,

Fierke³

2011

RNA

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Comparison of preribosomal RNA processing pathways in yeast, plant and human cells – focus on coordinated action of endo‐ and exoribonucleases

2017

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Edited by Michael IbbaProper regulation of ribosome biosynthesis is mandatory for cellular adaptation, growth and proliferation. Ribosome biogenesis is the most energetically demanding cellular process, which requires tight control. Abnormalities in ribosome production have severe consequences, including developmental defects in plants and genetic diseases (ribosomopathies) in humans. One of the processes occurring during eukaryotic ribosome biogenesis is processing of the ribosomal RNA precursor molecule (pre-rRNA), synthesized by RNA polymerase I, into mature rRNAs. It must not only be accurate but must also be precisely coordinated with other phenomena leading to the synthesis of functional ribosomes: RNA modification, RNA folding, assembly with ribosomal proteins and nucleocytoplasmic RNP export. A multitude of ribosome biogenesis factors ensure that these events take place in a correct temporal order. Among them are endo-and exoribonucleases involved in pre-rRNA processing. Here, we thoroughly present a wide spectrum of ribonucleases participating in rRNA maturation, focusing on their biochemical properties, regulatory mechanisms and substrate specificity. We also discuss cooperation between various ribonucleolytic activities in particular stages of pre-rRNA processing, delineating major similarities and differences between three representative groups of eukaryotes: yeast, plants and humans.Keywords: endoribonuclease; exoribonuclease; pre-rRNA processing; ribosome biogenesis; RNA quality control; RNA trimming Ribosome biosynthesis is a multistep process that includes several tightly controlled events -ribosomal DNA (rDNA) transcription, processing of rRNA precursors into mature molecules, accompanied by binding of ribosome biogenesis factors (RBFs) and ribosomal proteins (RPs), and the final assembly of all Abbreviations CD, catalytic domain; dsRBD, double-stranded RNA-binding domain; ETS, external transcribed spacer; ITS, internal transcribed spacer; LSU, large ribosome subunit (60S); miRNA, microRNA; mRNA, messenger RNA; MRP RNA, noncoding RNA component of the RNase MRP; mTOR, mammalian target of rapamycin; nt(s), nucleotide(s); PIN domain, PilT N-terminal domain; Pol I/II/III, RNA polymerase I/II/III; prerRNA, ribosomal RNA precursor; RBF, ribosome biogenesis factor; RMRP, RNase MRP (mitochondrial RNA processing ribonuclease); RNase, ribonuclease; RNB domain, RNase II domain; RNP, ribonucleoprotein; RP, ribosomal protein; rRNA, ribosomal RNA; siRNA, short interfering RNA; snoRNA, small nucleolar RNA; snoRNP, small nucleolar ribonucleoprotein; snRNA, small nuclear RNA; SSU, small ribosome subunit (40S); TRAMP4 or TRAMP5, Trf4/Air/Mtr4 or Trf5/Air/Mtr4 polyadenylation complex; tRNA, transfer RNA.

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Catalytic RNA

Burke

Lupták

2012

Encyclopedia of Life Sciences

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Ribonucleic acid (RNA) molecules have diverse roles in biological systems. Although some code for proteins or act to translate codons to amino acids, others fold into specific shapes that endow them with the ability to catalyse specific chemical transformations. These catalytic RNAs, ribozymes, are responsible for protein synthesis, transfer RNA (tRNA) processing, self‐splicing of certain introns, self‐scission during rolling circle replication of some single‐stranded RNA viruses and cofactor‐dependent gene regulation in bacteria. Other ribozymes have been evolved in vitro to perform a wide variety of transformations. Two of these, tRNA aminoacylase and RNA polymerase ribozymes, are featured here because molecules with such capabilities are thought to have existed on early Earth, before proteins took over as the dominant biological catalysts. Most of the ribozymes have been shown to perform multiturnover catalysis and thus act as true enzymes, either in their natural, biological form or as engineered constructs. Key Concepts: RNA molecules can fold into specific conformations and accelerate chemical transformations, thus acting as catalytic biomacromolecules, ribozymes. Ribozymes can accelerate chemical reactions by many orders of magnitude. Many ribozymes are capable of multiturnover catalysis, acting as enzymes. Protein synthesis templated by mRNA is catalysed by ribosomal RNA. Most ribozymes are phosphoryl transferases. In vitro selected ribozymes have been shown to catalyse a wide variety of reactions. The existence of ribozymes supports the RNA World hypothesis.

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Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA

Cited by 262 publications

References 54 publications

The RNR motif of B. subtilis RNase P protein interacts with both PRNA and pre-tRNA to stabilize an active conformer

The RNR motif of B. subtilis RNase P protein interacts with both PRNA and pre-tRNA to stabilize an active conformer

Comparison of preribosomal RNA processing pathways in yeast, plant and human cells – focus on coordinated action of endo‐ and exoribonucleases

Catalytic RNA

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