Nucleic Acids Research, 2000, Vol. 28, No. 7 1542-1547
© 2000 Oxford University Press
A missense mutation in the nuclear gene coding for the mitochondrial aspartyl-tRNA synthetase suppresses a mitochondrial tRNAAsp mutation
1Department of Medical Research, Mackay Memorial Hospital, Tamshui, Taipei 251, Taiwan, Republic of China, 2Department of General Education, National Taipei College of Nursing, Taiwan, Republic of China and 3Department of Life Science, National Yang-Ming University, Shih-Pai, Taipei 112, Taiwan, Republic of China
Received December 30, 1999; Revised and Accepted February 15, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The nuclear suppressor allele NSM3 in strain FF1210-6C/170-E22 (E22), which suppresses a mutation of the yeast mitochondrial tRNAAsp gene in Saccharomyces cerevisiae, was cloned and identified. To isolate the NSM3 allele, a genomic DNA library using the vector YEp13 was constructed from strain E22. Nine YEp13 recombinant plasmids were isolated and shown to suppress the mutation in the mitochondrial tRNAAsp gene. These nine plasmids carry a common 4.5-kb chromosomal DNA fragment which contains an open reading frame coding for yeast mitochondrial aspartyl-tRNA synthetase (AspRS) on the basis of its sequence identity to the MSD1 gene. The comparison of NSM3 DNA sequences between the suppressor and the wild-type version, cloned from the parental strain FF1210-6C/170, revealed a G to A transition that causes the replacement of amino acid serine (AGU) by an asparagine (AAU) at position 388. In experiments switching restriction fragments between the wild type and suppressor versions of the NSM3 gene, the rescue of respiratory deficiency was demonstrated only when the substitution was present in the construct. We conclude that the base substitution causes the respiratory rescue and discuss the possible mechanism as one which enhances interaction between the mutated tRNAAsp and the suppressor version of AspRS.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Mitochondria have their own translational machinery to synthesize the proteins encoded by their DNA. Production of these proteins is coordinated with the production of proteins from nuclear genes, which are required for mitochondrial biogenesis (1). Although most protein components of the translational machinery are encoded in the nucleus, the mitochondrial genome encodes a complete set of the RNAs necessary for translation. In the yeast Saccharomyces cerevisiae, the mitochondrial genome encodes 24 tRNAs, the large and small subunits of rRNAs, the tsl (tRNA synthesis locus) RNA and the var1 protein (a subunit of the mitochondrial ribosome) (2,3).
Several steps are involved in expression of mitochondrial tRNA genes: (i) transcription initiation to synthesize the primary RNA molecules; (ii) maturation of tRNAs by 5'- and 3'-processing enzymes, modification enzymes, and CCA terminal transferase; (iii) recognition of tRNAs by mitochondrial aminoacyl-tRNA synthetases; and (iv) interaction of amino-acylated tRNAs with mitochondrial ribosomes and translational factors (3). Except the tsl RNA for the 5'-processing of tRNA molecule (4), the genes encoding the enzymes that catalyze these steps are located in nucleus. These enzymes are synthesized on cytoplasmic ribosomes and subsequently transported into the mitochondria (5).
Mutations in the yeast mitochondrial tRNA genes result in the loss of mitochondrial protein synthesis and a phenotype of respiratory deficiency that is unable to use glycerol as a carbon source. This type of mitochondrial mutant is designated as syn– (6). A number of yeast syn– mutants have been characterized at the molecular level, and in most cases, a single base substitution in the tRNA genes has been found (7–10). In most syn– mutants, the mitochondrial genome is gradually lost (11). However, a syn– mutant FF1210-6C/170 contains a stable mitochondrial genome. It has a single base substitution (C to T transition) at position 72 in the tRNAAsp gene, resulting in two adjacent non-Watson–Crick base pairings at the acceptor stem. This mutant has a decreased level of tRNAAsp and shows no detectable mitochondrial protein synthesis (12). To understand the structural features of the mutated tRNAAsp that are responsible for the respiratory deficiency, revertants of this syn– mutant were isolated, including four independent nuclear suppressors and three other types of revertants (13).
The original mutation of the tRNAAsp gene was located at the acceptor stem which was demonstrated to play a vital role in the recognition by cognate aminoacyl tRNA synthetases (14–19). Several suppression mechanisms are possible, i.e. the mutated tRNAAsp is recognized by a mutated aspartyl-tRNA synthetase or by proteins involved in the processing of pre-tRNAs or translation elongation (20,21). To distinguish between these possibilities, we characterized one of these suppressor strains, FF1210-6C/170-E22 (hereafter referred to as strain E22) which contains NSM3 allele (nuclear suppressor of a mitochondrial mutation). A genomic DNA library was constructed from strain E22 and transformed into yeast strain H95 containing the mutated tRNAAsp gene to isolate recombinant plasmids that are able to suppress respiratory deficiency in strain H95. Here, we show that the NSM3 allele is a mutated mitochondrial aspartyl-tRNA synthetase gene and that a G to A transition, which results in an amino acid substitution, is responsible for respiratory rescue.
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MATERIALS AND METHODS |
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Plasmids and strains
Plasmids. The shuttle vector YEp13 (22) was used to construct a genomic DNA library from the suppressor strain E22 (MAT
ura1 ura2 NSM3 rho+ syn–) (13). Plasmid pIBI24 (International Biotechnologies Inc., Eastman Kodak Co., Rochester, NY) was used to clone the wild-type allele corresponding to the suppressor allele. Plasmid pBR322 was used as a vector to construct all YIp plasmids.
Strains. Escherichia coli strain YMC9 [F–, endA1, hsdR17 (r–, m+), supE44, thia-1, 
lacU169] (23) was used for the construction of the genomic library. Saccharomyces cerevisiae strains FF1210-6C/170 (MAT ura1 ura2 rho+ syn–), KAR (MAT leu2 kar1 rho+ syn–) and W303/A (MATa ade2 his3 leu2 ura3 can1 rho+) were used to construct a yeast recipient strain, H95, for screening recombinant plasmids that suppress the respiration deficient phenotype. To transfer the mitochondrial genome in strain FF1210-6C/170 into strain KAR, the mating type of FF1210-6C/170 was changed to type a, referred as FF1210-6C/170-a. Prior to its mating with FF1210-6C/170-a and segregation to obtain haploid cells, the ethidium bromide (50 µg/ml) treatment was applied to strain KAR to remove its mitochondrial genome (24). The mutated tRNAAsp gene in the new KAR strain was confirmed by Southern blot hybridization (25) (data not shown). However, the mitochondrial genome in the new KAR strain was lost within a few passages. A diploid strain, H95, was constructed by mating the new KAR with strain W303/A in which its mitochondrial genome was completely removed by the ethidium bromide treatment (24). The mitochondrial tRNAAsp mutation in strain H95 was confirmed by Southern blot hybridization (data not shown). The genotype of strain H95 is MATa/MAT leu2/leu2 KAR1/kar1 ade2/ADE2 his3/HIS3 ura3/URA3 can1/CAN1 rho+ syn–. Yeast strain XRD9 (MATa ade leu2 his3 ura3 rho+) was used for the gene disruption experiments.
Construction of a genomic DNA library
The strain E22 was grown in 500 ml of YPG medium (1% yeast extract, 1% Bacto-peptone, 50 mM sodium phosphate buffer pH 6.5 and 2% glycerol). The chromosomal DNA was isolated as described in Sherman et al. (24) and partially digested with Sau3AI. DNA fragments >3 kb were purified using a 10–40% sucrose density gradient, and ligated with BamHI-digested YEp13 plasmid DNA. The ligated DNA was then transformed into E.coli strain YMC9. All ampicillin resistant transformants were pooled and the recombinant plasmid DNA was isolated as described in Sambrook et al. (26).
Yeast transformation
Yeast transformation with strain XRD9 was performed as described in Ito et al. (27). When strain H95 was used, the same method with two modifications was used. Yeast cells were harvested at OD640 = 1.0 and concentration of lithium chloride was increased to 1.0 M.
Inactivation of the wild-type NSM3 allele by gene disruption
The 3.2-kb XhoI–ClaI DNA fragment isolated from the recombinant plasmid YEp13-NSM3 (Fig. 1) was inserted into the ClaI and SalI sites of pBR322. Subsequently, a 1.1-kb HindIII DNA fragment containing the URA3 gene from plasmid YEp24 was inserted into the two neighboring HindIII sites (Fig. 1) in the NSM3 allele. The resulting plasmid containing the URA3-disrupted nsm3 gene (nsm3::URA3) was designated as YIpGL143. This plasmid was linearized with ClaI and DraI before it was transformed into strain XRD9 to select for URA+ transformants.
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Chromosomal DNAs of six URA+ prototrophs were isolated and used to check the disrupted version of nsm3 allele by Southern blot hybridization. Fifty URA+ prototrophs were randomly picked and spotted onto the YPG plate to test for respiratory deficiency. The stability of mitochondrial DNA was revealed by colony hybridization (28).
Cloning of the wild-type version of the NSM3 allele
Chromosomal DNA of strain FF1210-6C/170 grown in YPD medium (1% yeast extract, 1% Bacto-peptone and 2% dextrose) was isolated and digested with both HindIII and XhoI. DNA fragments ~1.5 kb were isolated from a low-melting-point agarose gel and inserted into the HindIII and XhoI sites of plasmid pIBI24. Recombinant plasmids carrying the wild-type version of the NSM3 allele were isolated by colony hybridization (28) and used to determine its DNA sequence.
S1 nuclease protection experiment
Total yeast RNA was isolated from a 50-ml culture at OD640 = 2.0 in YPG medium as described in Sherman et al. (24). Approximately 100 µg RNA was mixed with 32P-end-labeled DNA fragments in 1x formamide hybridization buffer (40 mM PIPES pH 4.6, 1 mM EDTA, 0.4 M NaCl, 80% formamide). Hybridization was carried out at 42°C for 4 h. The RNA–DNA mixture was subjected to S1 nuclease digestion (29) and the protected DNA fragments were visualized by autoradiography after electrophoresis on 4% polyacrylamide, 7 M urea gels (30).
Other methods
Yeast plasmid DNAs were isolated from 10-ml cultures in minimal medium [2% glucose and 0.67% yeast nitrogen base without amino acids (Difco Laboratories, Detroit, MI)] as described by Nasmyth and Reed (31).
Sequences of the recombinant DNA fragments were determined using the chemical modification method (32).
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RESULTS |
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Cloning of the NSM3 allele
To clone the NSM3 allele, a chromosomal DNA library using the YEp13 shuttle vector was constructed from strain E22. Since the BamHI site in YEp13 is located in a gene giving resistance to tetracycline (Tetr), transformants harboring plasmids with chromosomal inserts are sensitive to tetracycline (Tets), and those without inserts are Tetr. Plasmid DNA isolated from about 16 000 ampicillin resistant E.coli transformants (60% Tets) was used to transform the yeast leucine auxotroph, H95, to leucine prototroph. About 32 000 LEU+ transformants were obtained and transferred to YPG plates by replica plating to select for respiration positive colonies. Nine respiration positives were obtained.
To eliminate the possibility that the respiratory rescue was due to reversion of the mitochondrial tRNAAsp mutation, each respiratory positive transformant was grown in YPD medium without selection for overnight and spread onto YPD plates to obtain single colonies. These colonies were subsequently transferred onto both minimal medium and YPG plates to examine leucine auxotroph and respiratory deficiency, respectively. Fifteen percent of colonies showed leucine auxotroph, indicating the loss of YEp plasmid. All of these leucine auxotrophs were also respiration deficient. These results indicated that the respiratory rescue in the nine transformants is due to existence of the YEp13-recombinant plasmids.
Plasmid DNAs from the nine transformants were amplified in E.coli before they were transformed back into strain H95 to re-confirm that the YEp13-recombinant plasmids contained the suppressor alleles. All LEU+ transformants were shown to be respiration positive. The restriction enzyme maps of the recombinant DNA fragments in these nine transformants were determined and shown to be identical. Each plasmid contained the same 4.5-kb chromosomal DNA fragment (Fig. 1). This recombinant plasmid was designated as YEp13-NSM3.
Gene amplification is not required for suppression
To determine if the respiratory rescue resulted from amplification of a wild-type gene due to the high copy number of YEp plasmids and not from a mutation, the 4.5-kb chromosomal DNA fragment was subcloned into vectors YCp and YIp, which are single-copy plasmid per haploid genome (33), and the resulting plasmid DNAs were transformed into strain H95. In both cases, the transformants were respiratory competent, indicating that a high copy number of plasmid is not necessary for the rescue.
The wild-type NSM3 allele is required for maintenance of the mitochondrial DNA (mtDNA)
The URA3 gene in a 1.1-kb HindIII DNA fragment was inserted at the two neighboring HindIII sites (Fig. 1), resulting in a disrupted version of the NSM3 allele. This disrupted allele was used to substitute for the wild-type allele in strain XRD9 by a double crossover event of homologous recombination (34). The substitution was confirmed by Southern blot hybridization (data not shown). In contrast to the recipient strain XRD9 that is able to grow stably on YPG medium, the URA+ transformants rapidly became unable to grow on YPG medium, indicating the loss of mitochondrial function. Hybridization of the URA+ colonies with radiolabeled mtDNA showed that these colonies had lost their mtDNA (Fig. 2). These results indicated that the wild-type NSM3 allele is essential for maintenance of mtDNA.
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Identification of the suppression mutation in the NSM3 allele
Since vector YEp13 contains two HindIII sites, the chromosomal DNA fragment of plasmid YEp13-NSM3 was divided into three regions by HindIII digestion. The two large fragments, containing either the left or the right end of chromosomal DNA fragment (Fig. 1), were subcloned into YEp13 and the resulting plasmid DNAs were transformed into strain H95 to test for respiratory rescue. The results showed that neither region was able to rescue the respiratory deficiency.
To identify the suppression mutation, the 3.5 kb of DNA surrounding the two HindIII sites in the chromosomal insert was sequenced. Among the six possible reading frames, only one was found to be significant, as indicated by an open box below the restriction enzyme map (Fig. 1). The first AUG codon of the open reading frame is 228 nucleotides downstream of the NcoI site. The open reading frame ends 121 nucleotides upstream of the ClaI site. This open reading frame codes for a protein of 658 amino acids (Fig. 1).
The expression of this open reading frame was examined by northern blot hybridization and S1 nuclease protection experiments. A single transcript of ~2000 nucleotides in length was detected (data not shown), slightly larger than the size of the open reading frame. The results of S1-nuclease protection experiments revealed three possible initiation sites at the 5' end of the open reading frame (indicated by filled circles with vertical bars in Fig. 1). The middle site is about five times stronger than the other two, suggesting that this may represent the major site for initiation of transcription, 251 bp upstream of the start codon (Fig. 1).
The deduced amino acid sequence was used to search for homology with known proteins. Except one amino acid difference at position 388, this protein is identical to the yeast mitochondrial aspartyl-tRNA synthetase (AspRS) encoded by the MSD1 gene (35). At the nucleotide level, these two proteins have only one base difference, a G to A transition, 1160 bp downstream of the start codon.
To distinguish the base difference as the suppression mutation from DNA sequence polymorphism, the wild-type allele in this region was cloned from strain FF1210-6C/170 and its DNA sequence was determined, which was found to be identical to that of the MSD1 gene. Thus, the G to A transition results in the substitution of asparagine (AAU) for a serine (AGU), (S388N).
To confirm that this G to A transition is the cause of the suppression, four chimeric YCp plasmids were constructed with the DNA fragments from either the wild-type or the suppressor version of the NSM3 allele (Fig. 3B). The base substitution, as indicated by an asterisk, is located between the HincII and HindIII sites (Fig. 3A). YCpGL852, carrying the entire suppressor DNA fragment, caused suppression and served as a positive control. YCpGL1104-1, substitution of wild-type NcoI–HincII and HindIII–BglII fragments, did not affect suppression, but YCpGL901-4, substitution of the wild-type HincII–HindIII fragment, eliminated suppression (Fig. 3C). Since the mutation encoding the Ser to Asn substitution is located in this fragment, we conclude that the S388N substitution is responsible for the suppression of the mitochondrial tRNAAsp mutation.
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Based on the structural information of AspRS from Thermus thermophilus, the S388N mutation is located at the end of
-helix H7 (36). An amino acid sequence alignment among 21 sequenced AspRSs revealed that positively charged amino acids at the third position of the -helix H7 are highly conserved (Fig. 4). An implication that the -helix H7 contacts the tRNA molecule and the possible suppression mechanism are discussed below.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In the present work, we characterized the nuclear suppressor NSM3 allele. It appears to encode the mitochondrial AspRS based on its sequence identity to the MSD1 gene, which codes for yeast mitochondrial AspRS in strain D272-10B (35). The MSD1 gene activity is required for maintenance of the mitochondrial genome. The NSM3 allele contains a single amino acid substitution from serine to asparagine at position 388 in the mitochondrial AspRS, S388N, which is responsible for the suppression of the mitochondrial tRNAAsp mutation in strain E22.
The original mutation of the mitochondrial tRNAAsp gene in strain FF1210-6C/170 was a C to T transition at position 72 (C72T) in the acceptor stem (9,37), resulting in two consecutive non-Watson–Crick base-pairings and causing mitochondrial defect. Since a lower level of tRNAAsp was observed in strain FF1210-6C/170, this mutation might affect the numerous post-transcriptional modifications. The results of both primer-extension and S1 nuclease protection experiments indicated that the 5' end of the mutant tRNAAsp molecule is properly processed (37,38). The results of northern blot hybridization further revealed that the mutated tRNAAsp appears to be the same size as that of the wild-type molecules. No accumulation of larger pre-tRNA molecules was observed (21,37,38), in contrast to a mitochondrial tRNAAsp mutant in which the 3' end processing is abolished (39). These results suggested that a certain amount of mutated tRNAAsp molecules are properly processed at both the 5' and 3' ends.
The acceptor stem where the C72U mutation is located has been proven to play a critical role in recognition of tRNAs by their cognate aminoacyl-tRNA synthetases (14–16,18,19,40,41). AspRS is required for maintenance of the mitochondrial genome (this study), therefore, the stable mitochondrial genome in strain FF1210-6C/170 (12) suggested that the mutated tRNAAsp was probably recognized by AspRS at a lower efficiency. This is consistent with the observation that the defective phenotype of strain FF1210-6C/170 was corrected by over-production of the mutated tRNAAsp (13).
The mitochondrial function in two temperature-sensitive mutants, caused by mutations at either mitochondrial tRNAPhe or tRNAAsp, was restored by over-expression of the mutated tRNAPhe or wild-type AspRS (13,20,21). In this work, one copy of a mutated version of the gene coding for mitochondrial AspRS per haploid cell was sufficient to recover the mitochondrial function. Thus, the respiratory rescue is not due to NSM3 over-production.
Yeast mitochondrial AspRS is a member of class II aminoacyl-tRNA synthetases, containing characteristic conserved motifs 1, 2 and 3 (42–44). Built on these motifs is the active site, six antiparallel ß-sheets surrounded by three -helices, which promotes aminoacylation by activating and transferring amino acid onto the acceptor stem of tRNA molecules (45,46). A comparison of amino acid sequences among seven cloned AspRSs first revealed that enzymes from E.coli, T.thermophilus and S.cerevisiae mitochondria have an insertion sequence of about 100 amino acids located between motifs 2 and 3. This insertion sequence forms an extra domain in the crystal structure of T.thermophilus AspRS (36). This domain seems to be a characteristic of prokaryotic AspRSs (47). The function of the extra domain is unknown, however, it has been suggested that the extra domain modulates function of the active site by stabilizing the complex with tRNA (36,47). The extra domain of T.thermophilus AspRS is similar to E.coli ThrRS in its N-terminal domain from which two -helices contact tRNAThr in the ThrRS:tRNAThr complex (48). One helix, H7 in the extra domain, at a similar position as one of these two helices (36) implicates that the C-terminus of the helix H7 likely contacts the D arm and/or the acceptor stem of tRNAAsp.
Based on the amino acid sequence alignment and the structure of T.thermophilus AspRS (36), the amino acid substitution in the NSM3 allele, S388N, is mapped to the 13th position of the helix H7 (Fig. 4). This is the first reported mutation in the extra domain, indicating a possible biological function of this domain. An alignment among 21 sequenced AspRSs revealed that the amino acid residue at the third position of H7 is highly conserved. The S388N mutation resides on the same side of H7 as this conserved residue, presumably facing tRNA toward the active site (see figure 5C in ref. 36). This amino acid substitution results in four consecutive asparagine residues at the C-terminus of the helix H7. Amino acid asparagine with a longer side chain than serine might push the acceptor stem of mutant tRNAAsp closer to the active site of AspRS, restoring aminoacylation of the mutated tRNAAsp and resulting in the respiratory rescue. The examination of the aminoacylation efficiency of mutant tRNAAsp by the mutant AspRS would be required to support this explanation. Either a crystal structure or molecular modeling of the mutant AspRS:mutant tRNAAsp complex should reveal the proposed contacts. In addition, a systemic analysis of mutations in the helix H7 in the presence or absence of mutations in the acceptor stem of tRNA would bring better insights into the interactions between the helix H7 of AspRS and tRNAAsp.
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ACKNOWLEDGEMENTS |
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We are grateful to Dr D. L. Miller for his support during most of this work. This work was supported by the Mackay Memorial Hospital grant (8739) to C.C. and the National Science Council grant (NSC-87-2314-B010-084) to G.L. G.L. is awarded by Medical Research and Advancement Foundation in Memory of Dr Chi-Shuen Tsou.
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FOOTNOTES |
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* To whom correspondence should be addressed. Tel: +886 2 2826 7232; Fax: +886 2 2820 2449; Email: gjliaw@mailsrv.ym.edu.tw
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