A Novel Endonucleolytic Mechanism to Generate the CCA 3′ Termini of tRNA Molecules in Thermotoga maritima

Minagawa, Asako; Takaku, Hiroaki; Takagi, Masamichi; Nashimoto, Masayuki

doi:10.1074/jbc.m313951200

Cited by 78 publications

(133 citation statements)

References 32 publications

(18 reference statements)

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“…The CCA sequence in 3 0 terminal of the tRNA is critical for tRNA maturation and function. RNase Z mainly processes CCA-less pre-tRNAs; however, it can process CCA-containing pre-tRNAs in the nucleus or mitochondria 26,27 . To investigate the enzymatic activity of RNase Z S1 , we tested whether RNase Z S1 cleaved two pre-tRNAs, pre-tRNA9-AspATC (without CCA) and pretRNA35-MetCAT (with CCA).…”

Section: Ans-1 and Zhu1s Are Temperature-sensitive Tgms Linesmentioning

confidence: 99%

RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice

et al. 2014

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Thermosensitive genic male-sterile (TGMS) lines, which are male-sterile at restrictive (high) temperatures but male-fertile at permissive (low) temperatures, have been widely used in breeding two-line hybrid rice (Oryza sativa L.). Here we find that mutation of thermosensitive genic male sterile 5 (tms5) in rice causes the TGMS trait through a loss of RNase Z S1 function. We show that RNase Z S1 processes the mRNAs of three ubiquitin fusion ribosomal protein L40 (Ub L40 ) genes into multiple fragments in vitro and in vivo. In tms5 mutants, high temperature results in increased levels of Ub L40 mRNAs. Overaccumulation of Ub L40 mRNAs causes defective pollen production and male sterility. Our results uncover a novel mechanism of RNase Z S1 -mediated Ub L40 mRNA regulation and shows that loss of this regulation produces TGMS in rice, a finding with potential applications in hybrid crop breeding.

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Section: Ans-1 and Zhu1s Are Temperature-sensitive Tgms Linesmentioning

confidence: 99%

RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice

et al. 2014

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“…The C-terminal half region of tRNase Z L has high similarity to the whole region of tRNase Z S and these regions contain a well-conserved histidine motif, which has been shown to be essential for the tRNase Z activity. 5,8 We have demonstrated in vitro that mammalian tRNase Z L can cleave any target RNA at any desired site by recognizing a pre-tRNA-like or micro-pre-tRNAlike complex formed between the target RNA and artificial small-guide RNA (sgRNA). [9][10][11][12] sgRNA is divided into four categories: 5 0 -half-tRNA, 10 14-nucleotide (nt) linear RNA, 13 RNA heptamer 11,12 and hook RNA.…”

Section: Introductionmentioning

confidence: 99%

“…[2][3][4] Most tRNase Zs cleave pre-tRNAs immediately downstream of a discriminator nucleotide, onto which the CCA residues are added to produce mature tRNA, whereas tRNase Z from Thermotoga maritima exceptionally cleaves pre-tRNAs containing the CCA sequence precisely after the A residue to create the mature 3 0 -termini. 5 tRNase Zs can be divided into two groups: a short form (tRNase Z S ) that consists of 300-400 amino acids and a long form (tRNase Z L ) that contains 800-900 amino acids. 6 Bacteria and archaea genomes contain a tRNase Z S gene only, whereas eucaryotic genomes encode either only tRNase Z L or both forms.…”

Section: Introductionmentioning

confidence: 99%

Gene silencing by the tRNA maturase tRNase ZL under the direction of small-guide RNA

et al. 2006

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We have been developing a unique system for the downregulation of a gene expression through cutting a specific mRNA by the long form of tRNA 3 0 -processing endoribonuclease (tRNase Z L ) under the direction of small-guide RNA (sgRNA). However, the efficacy of this system and the involvement of tRNase Z L in the living cells were not clear. Here we show, by targeting the exogenous luciferase gene, that the efficacy of the sgRNA/tRNase Z L method can become comparable to that of the RNA interference technology and that the gene silencing is owing to tRNase Z L directed by sgRNA not owing to a simple antisense effect. We also show that tRNase Z L together with sgRNA can downregulate expression of the endogenous human genes Bcl-2 and glycogen synthase kinase-3b by degrading their mRNAs in cell culture. Furthermore, we demonstrate that a gene expression in the livers of postnatal mice can be inhibited by an only seven-nucleotide sgRNA. These data suggest that sgRNA might be utilized as therapeutic agents to treat diseases such as cancers and AIDS.

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“…This conclusion was strengthened by the subsequent finding that the enzyme is also a zinc phosphodiesterase (10). However, study of RNase Z enzymes from various other organisms showed that these enzymes are endoribonucleases (6,18,19), and the E. coli enzyme was also found to display endoribonuclease activity on certain tRNA precursors in vitro (14,20). To help clarify this situation, we recently carried out a detailed analysis of RNase BN/RNase Z action on a variety of oligoribonucleotide substrates and showed that the enzyme can act both as a distributive exoribonuclease and an endoribonuclease depending on the nature of the substrate and on its 3Ј-terminal structure (21).…”

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confidence: 99%

“…3Ј-Maturation of tRNA precursors differs among organisms depending on whether or not the universal 3Ј-terminal CCA sequence is encoded (1)(2)(3)(4)(5)(6). In eukaryotic cells, this sequence is absent from tRNA precursors, and the 3Ј-processing step is catalyzed by the endoribonuclease, RNase Z or 3Ј-tRNase, which cleaves at the discriminator base to allow subsequent CCA addition by tRNA nucleotidyltransferase (3,5,7).…”

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confidence: 99%

Mode of Action of RNase BN/RNase Z on tRNA Precursors

Dutta

Deutscher

2010

Journal of Biological Chemistry

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RNase BN, the Escherichia coli homolog of RNase Z, was previously shown to act as both a distributive exoribonuclease and an endoribonuclease on model RNA substrates and to be inhibited by the presence of a 3-terminal CCA sequence. Here, we examined the mode of action of RNase BN on bacteriophage and bacterial tRNA precursors, particularly in light of a recent report suggesting that RNase BN removes CCA sequences (Takaku, H., and Nashimoto, M. (2008) Genes Cells 13, 1087-1097). We show that purified RNase BN can process both CCAless and CCA-containing tRNA precursors. On CCA-less precursors, RNase BN cleaved endonucleolytically after the discriminator nucleotide to allow subsequent CCA addition. On CCA-containing precursors, RNase BN acted as either an exoribonuclease or endoribonuclease depending on the nature of the added divalent cation. Addition of Co 2؉ resulted in higher activity and predominantly exoribonucleolytic activity, whereas in the presence of Mg 2؉ , RNase BN was primarily an endoribonuclease. In no case was any evidence obtained for removal of the CCA sequence. Certain tRNA precursors were extremely poor substrates under any conditions tested. These findings provide important information on the ability of RNase BN to process tRNA precursors and help explain the known physiological properties of this enzyme. In addition, they call into question the removal of CCA sequences by RNase BN.3Ј-Maturation of tRNA precursors differs among organisms depending on whether or not the universal 3Ј-terminal CCA sequence is encoded (1-6). In eukaryotic cells, this sequence is absent from tRNA precursors, and the 3Ј-processing step is catalyzed by the endoribonuclease, RNase Z or 3Ј-tRNase, which cleaves at the discriminator base to allow subsequent CCA addition by tRNA nucleotidyltransferase (3, 5, 7). In contrast, in some bacteria, such as Escherichia coli, the CCA sequence is encoded, and maturation of the 3Ј terminus is carried out by exoribonucleases (8, 9), whereas in other organisms, such as Bacillus subtilis, both types of 3Ј-processing are operative (3). Surprisingly, in E. coli, despite the fact that the CCA sequence is present in all known tRNA precursors, an RNase Z homolog, termed RNase BN, is present (10). As a consequence, it has been of considerable interest to understand the function in E. coli of this apparently unnecessary enzyme.RNase BN was originally discovered as an enzyme required for the maturation of those bacteriophage T4 precursor tRNAs that lack a CCA sequence (11). Subsequently, RNase BN was shown to also be able to process the CCA-encoded host E. coli tRNA precursors in vivo (8, 9). However, of the five E. coli RNases able to carry out the 3Ј-processing reaction, RNase BN was the least efficient (12, 13). Thus, under normal growth conditions, RNase BN is unlikely to function in total tRNA maturation, although it cannot be ruled out that the enzyme may participate in 3Ј-maturation of some select tRNA species (8). However, because E. coli mutants lacking RNase BN grow essentially nor...

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A Novel Endonucleolytic Mechanism to Generate the CCA 3′ Termini of tRNA Molecules in Thermotoga maritima

Cited by 78 publications

References 32 publications

RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice

RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice

Gene silencing by the tRNA maturase tRNase ZL under the direction of small-guide RNA

Mode of Action of RNase BN/RNase Z on tRNA Precursors

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