Skip Navigation

This Article
Right arrow Abstract Freely available
Right arrow Print PDF (241K) Freely available
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (27)
Right arrowRequest Permissions
Right arrow Commercial Re-use Guidelines
for Open Access NAR Content
Google Scholar
Right arrow Articles by Tomita, K
Right arrow Articles by Watanabe, K
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Tomita, K
Right arrow Articles by Watanabe, K
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

© 1996 Oxford University Press 4987-4992

Footnote

RNA editing in the acceptor stem of squid mitochondrial tRNATyr

RNA editing in the acceptor stem of squid mitochondrial tRNA Tyr Kozo Tomita, Takuya Ueda* and Kimitsuna Watanabe

Department of Chemistry and Biotechnology, School of Engineering, University of Tokyo, Bunkyo-ku, Tokyo 113, Japan

Received July 30, 1996; Revised and Accepted October 25, 1996DDBJ/EMBL/GenBank accession nos D17537D17537, D17539D17539

ABSTRACT

In squid (Loligo bleekeri) mitochondria, the two 3'-terminal nucleotides (G72-G73) of the tRNATyr gene overlap with the two 5'-terminal nucleotides (G1-G2) of the downstream tRNACys gene. To elucidate the processing mechanism(s) of the tRNA molecules derived from this region, tRNAs were analyzed by sequencing cDNAs synthesized from circularized tRNAs. Nucleotides G1-G2 in tRNACys appeared to be without post-transcriptional conversion, whereas CCA was post-transcriptionally added to the 3'-terminus. In contrast, in the majority of tRNAsTyr, G72-G73 were found to be converted to A72-A73, accompanied by the CCA addition. These results indicate that a precursor of tRNATyr is processed at U71 and two adenosines are attached prior to the CCA addition. Thus, we suggest that 5' processing of the precursor tRNA dominates 3' processing and maturation of the tRNA is mediated by a polyadenylylation enzyme in the mitochondria, a scenario which is consistent with the editing process proposed in land snail mitochondria. We also obtained intermediates, such as a premature tRNA lacking CCA that terminated at U71 and one with a single adenosine attached at position 72, which support the suggested maturation process. However, although we failed to detect a tRNACys lacking G1-G2 at the 5'-terminus, we obtained cDNAs for tRNATyr with G72-G73 and the CCA terminus. This inconsistent result suggests the co-existence of another process(es) in the maturation of these tRNA molecules in squid mitochondria.

INTRODUCTION

RNA editing is a phenomenon in which RNAs are generated with nucleotide sequences different from those predicted from the corresponding sequences of the template DNA genome. The biological significance and detailed molecular basis of this puzzling process remain unsolved. Although this novel RNA maturation process has been described mainly in mitochondrial (mt) systems (1 -3 ), it has also been shown to exist in mammalian nuclear (4 ,5 ) and plant chloroplast (6 ) systems. In the last few years, characterization of the enzyme(s) or RNAs involved in the above mentioned mRNA editing have been elucidated. U insertion/deletion editing in Trypanosoma mitochondria was found to be mediated by small RNAs termed guide RNAs (gRNA), which are complementary to the pre-edited mRNA and are considered to guide the editing process (7 ). The substitution editing event observed in mammalian nuclear mRNAs for the glutamate receptor subunit is mediated by adenosine deaminases, which convert a specific A residue to inosine (8 ). RNA editing in mammalian nuclear mRNA for apolipoprotein B is considered to be mediated by cytidine deaminases and a specific C is converted to U (9 ). The substitution editing C -> U in plant mitochondrial mRNAs is also thought to be mediated by a form of cytidine deaminase (10 ).

Besides mRNA editing, tRNAs have also been found to be edited in mitochondria of an amoeboid protozoan (Acanthamoeba castellanii; 11 ), potato (12 ), marsupials (13 ,14 ), a land snail (15 ) and the platypus (14 ). In the amoeboid protozoan and potato mitochondria, tRNA editing has been detected in the 5'-parts of the acceptor stems (11 ,12 ), where mismatched base pairs are converted to more stable usual pairs (A-U, G-C and G-U) by nucleotide substitutions such as U -> A, U -> G, A -> G or C -> U. In marsupial mitochondria, the anticodon second position of tRNAGlyGCC is edited from C to U, resulting in the generation of a tRNA specific to aspartic acid codons (13 ,14 ). In land snail and platypus mitochondria, tRNA editing is observed in the 3'-parts of the acceptor stems. In these mitochondria, it is unique that tRNA genes whose transcripts are to be edited usually have overlapping nucleotides with their downstream genes and display mismatched base pairs in their inferred acceptor stems (15 ,16 ). RNA editing is thought to repair these irrelevant mismatched stem regions. The molecular mechanisms and the molecules mediating tRNA editing are completely unknown. tRNA editing in land snail mitochondria is considered to be mediated by polyadenylylation (15 ), but there is no direct evidence to support this idea.

Overlapping tRNA genes have been observed in the mt genomes of some animals other than the land snail or platypus (15 ), e.g. those of human (17 ), mouse (18 ) and chicken (19 ).

We have sequenced two thirds of the mt genome of the squid Loligo bleekeri in our laboratory and noticed that the two 3'-terminal nucleotides (G72-G73) in the tRNATyr gene overlap with the two 5'-terminal nucleotides in the tRNACys gene (unpublished results). However, there are no mismatches in the inferred acceptor stems in either of the tRNA genes, which is contrary to the cases of the land snail and platypus mt tRNA genes, in which RNA editing occurs.

In order to verify that RNA editing also takes place in mt tRNATyr and tRNACys in the squid, we analyzed cDNAs synthesized from circularized tRNAs. Comparison of the cDNA sequences with the corresponding mt genome sequences leads to the suggestion that RNA editing proceeds in a manner similar to that in the land snail. Intermediates of RNA editing were obtained. In the light of these results, the editing process in squid mitochondria is discussed.

MATERIALS AND METHODS

Preparation of total RNAs and DNAs from squid liver

Total RNAs were prepared from the liver of one individual squid (L.bleekeri) by the guanidinium thiocyanate method (21 ). The total RNAs were applied to a DEAE-Sepharose (Pharmacia) column from which the tRNA fraction was eluted with a buffer containing 20 mM Tris-HCl, pH 7.5, 10 mM MgCl2 and 0.6 M NaCl. Total DNA was also prepared by phenol extraction from the same individual used for the preparation of total RNA and treated with RNase A to remove the RNA.

Cloning of a mt DNA fragment containing tRNA genes

Squid mt DNA encoding the tRNA genes for cysteine and tyrosine and their flanking regions was amplified by PCR from the total squid DNA prepared from one individual. PCR was performed in 50 [mu]l of a solution containing 10 mM Tris-HCl, pH 8.4, 2 mM MgCl2, 400 [mu]M dNTPs, 25 pmol each PCR primer, 2.5 U Taq DNA polymerase and 1.5 [mu]l total squid DNA (150 ng). The mixtures were subjected to one cycle of incubation at 94oC for 3 min, followed by 30 cycles of PCR, each cycle consisting of incubations at 94, 50 and 72oC for 1, 1.5 and 1.5 min respectively. The primers used for PCR were SM-CY1B (5'-GGGggatccATAGCCTATCTGAAACTGG-3') and SM-CY1H (5'-GGGaagcttGCACTATTAAAGTTATTAGTGT-3'). These primers have restriction endonuclease recognition sites for cloning (BamHI, lower case letters; HindIII, underlined lower case letters). The DNA fragment amplified by PCR was purified using a QIAquick spin column (Qiagen) to remove the PCR primers according to the manufacture's protocol, digested with BamHI and HindIII and ligated to pUC19, which was used for the transformation of Escherichia coli JM109. DNA sequencing was carried out by the dideoxy termination method using a 7-deaza sequence kit (version 2.0, US Biochemicals).

Circularization of total tRNA, synthesis of cDNAs and molecular cloning

Circularization of total tRNA was carried out as described (15 ) except that the final concentration of BSA was adjusted to 10 [mu]g/ml. For cDNA synthesis, 1 pmol primer was annealed to 2 [mu]g circularized tRNA in 20.5 [mu]l of a solution containing 10 mM Tris-HCl, pH 8.0, and 1 mM EDTA by heating at 80oC for 2 min followed by standing at room temperature for 30 min. Then, 6 [mu]l of a 5* concentrated buffer (250 mM Tris-HCl, pH 8.3, 375 mM KCl and 50 mM DTT), 1 [mu]l 1.5 mM dNTPs, 1 [mu]l 150 mM MgCl2 and 1 [mu]l (25 U) M-MLV reverse transcriptase (US Biochemicals) were added and the mixture was incubated at 37oC for 1 h. The primers used for synthesis of single-strand cDNAs were SM-Y1 (5'-GGgaattcCGACTTTTAATCGACCAC-3') for mt tRNATyr and SM-C1 (5'-GGgaattcTAATGTTTTTATTAAACTAT-3') for mt tRNACys respectively. The nucleotides indicated by lower case letters are restriction enzyme sites for further cloning. PCR was carried out in 50 [mu]l of the above buffer using a 1.5 [mu]l aliquot withdrawn from 30 [mu]l cDNA solution. The mixtures were subjected to 30 cycles of PCR, one cycle consisting of incubations at 94, 48 and 72oC for 1, 1 and 1.5 min respectively. The primers used for the PCR were SM-Y1 and SM-Y2 (5'-GGaagcttCTATGAATAAGTTGTAGGA-3') for mt tRNATyr and SM-C1 and SM-C2 (5'-GGaagcttCCTAAAGATGTAATGATA-3') for mt tRNACys respectively. These primers have restriction endonuclease recognition sites for cloning (EcoRI, lower case letters; HindIII, underlined lower case letters). Purification of the PCR products, molecular cloning and DNA sequencing were performed as described above. As controls, non-circularized tRNAs, DNAs treated with RNase A and DNAs treated with both RNase A and T4 RNA ligase were subjected to the same procedures as described above.

Southern hybridization

Total squid DNA isolated as described above (5 [mu]g) was digested with SalI and HindIII or SalI and PstI at 37oC for 12 h, separated on a 1.0% (w/v) agarose gel and transferred to a nylon membrane (Pall Biosupport) according to the manufacturer's instructions. Hybridization was carried out overnight at 60oC in 6* SSC (900 mM NaCl, 90 mM sodium citrate) containing 5* Denhardt's solution and 0.5% (w/v) SDS (22 ). Hybridization probes were prepared from the cloned squid mt DNA fragment containing the tRNACys and tRNATyr genes using a random priming labeling kit (Takara Shuzo) according to the manufacturer's protocol. Subsequently, the membrane was washed in 3* SSC at room temperature for 15 min and then in 2* SSC at 60oC for 60 min. The radioactivities were detected with an imaging analyzer (Fiji Photo Film).

RESULTS AND DISCUSSION

A mt DNA fragment containing the genes for tRNACys and tRNATyr was amplified from total DNA of a squid, L.bleekeri. The sequences of all the clones analyzed (28 in total) were identical to those previously determined in our laboratory. The two 3'-terminal nucleotides (G72-G73) in the tRNATyr gene overlapped with the two 5'-terminal nucleotides (G1-G2) in the tRNACys gene (Figs 1 A and 2 A). The 3'- and 5'-ends of these two tRNAs were analyzed according to the literature (15 ). In order to rule out the possibility of polymorphism of mt DNA sequences, the cDNAs for tRNATyr and tRNACys were synthesized from the total tRNAs prepared from the same individual used to analyze the mt genome sequence. DNA fragments with the expected lengths were obtained only when circularized tRNAs were subjected to reverse transcription followed by PCR amplification. In the experiments using either non-circularized tRNAs, DNAs treated with RNase A or DNAs treated with both RNase A and T4 RNA ligase, no DNA fragment was amplified, indicating that the PCR products were actually derived from the circularized tRNA molecules (data not shown).


Figure 1. (A) Gene order of squid (L.breekeri) mt tRNACys and tRNATyr. The shaded area indicates the overlapping region between the tRNACys and tRNATyr genes. The nucleotide sequences on either side of the overlap (GG, underlined) are shown. (B and C) Inferred secondary structures of tRNACys (B) and tRNATyr (C). The overlapping regions are indicated by shading. The difference between the cDNA and the corresponding genome sequence in tRNATyr is indicated by arrows (from G72-G73 to A72-A73). Outlined letters indicate the regions used for RT-PCR (see Materials and Methods).

More than 20 different cDNA clones were analyzed for tRNACys and more than 40 for tRNATyr. In the case of tRNACys, the cDNA sequences of all the 21 clones analyzed were completely identical to the corresponding genomic sequence except that the sequence CCA was found to be post-transcriptionally added to the 3'-end (Figs 1 B and 2 ). In contrast, in the case of tRNATyr, an apparent discrepancy was observed between the cDNA and the genomic sequences. Out of a total of 45 clones, 32 had A72-A73 instead of G72-G73 in the genomic sequence and possessed the CCA sequence at the 3'-terminus (Fig. 3 A, Type I). In this case, the U1:G72 wobble base pair in the acceptor stem was changed to a U1:A72 Watson-Crick base pair and the discriminator base was also changed from G73 to A73. In seven of the 45 clones, the nucleotides at positions 72 and 73 and the CCA sequence were lacking (Fig. 3 B, Type II); in four others, G72-G73 remained unchanged, but the CCA sequence was added to the 3'-end (Fig. 3 C, Type III). The smallest group, comprising just two clones, terminated at position 72 with adenosine and lacked nucleotide 73 and the CCA sequence (Fig. 3 D, Type IV).


Figure 2. Sequence comparison of mt genome sequence (A) with the cDNA for mt tRNACys (B). The acceptor stem region of tRNACys is also shown. The G1-G2 overlap in tRNACys is indicated by shading. There is no difference between the genome sequence and cDNA for tRNACys except that the CCA sequence is added to the 3'-end of tRNACys. The numbers of clones obtained are indicated in parentheses.


Figure 3. Variations of cDNA clones for tRNATyr (A-D; Types I-IV). Only the acceptor stem regions of tRNATyr are shown. The shaded letters indicate regions mentioned in Results and Discussion. DNA sequencing ladders of cDNA clones for edited (A) and non-edited (C) tRNATyr and intermediates of tRNATyr in the RNA editing process (B and D) are shown. The numbers of clones obtained of each type are shown in parentheses.

In order to exclude the possibility that other tRNA genes with the same sequence in the acceptor stem as mt tRNATyr are present in the nuclear genome or in other mt genome regions which have not yet been determined, Southern hybridization was carried out using total DNA. The result indicated that the tRNATyr gene was located only in the region of mt genome which had been previously determined (Fig. 4 ).

The above results led us to the following interpretation. A72-A73 in Type I tRNA is created by RNA editing, while the clones having Type II and Type IV tRNAs are derived from intermediates formed during the same RNA editing process. The clones of tRNATyr with G72-G73 (Type III tRNA) are produced by another processing pathway. Possible mechanisms of RNA editing in squid mt tRNATyr are illustrated in Figure 5 .


Figure 4. Southern hybridization of squid total DNA with randomly primed probes prepared from the cloned mt tRNATyr gene. Only the expected lengths of mt DNA fragments were detected. Digestion with HindIII and PstI (H-P, left lane) gave a 3.5 kb mt DNA fragment and with HindIII and SalI (H-S, right lane) a 6.1 kb fragment, as expected.


Figure 5. Possible mechanisms of RNA editing in squid mt tRNATyr. Different pathways may be involved in the processing of primary transcripts of tRNATyr and tRNACys (1A, 1B and 2). Framed tRNA configurations indicate cDNA clones for tRNATyr and tRNACys obtained in this study.

RNA editing in squid mt tRNATyr is considered to occur in a manner similar to that of the recently reported RNA editing in the land snail (15 ). In overlapping tRNA genes, 5' processing of the downstream gene dominates over 3' processing of the upstream gene. The resulting truncated tRNA species derived from the upstream gene is repaired by an enzyme(s) involved in the editing process. One of the plausible candidates for this process is a polyadenylylation enzyme, since all the nucleotides found in the edited sites in the land snail mt tRNAs are adenosine. The occurrence of the Type I, II and IV clones obtained from squid mt tRNATyr is explained by this mechanism. Processing on the tRNA precursor containing tRNATyr and tRNACys occurs at U71 (Fig. 5 -1), resulting in mature tRNACys and truncated tRNATyr molecules. Identification of the intermediate Type II and IV tRNAs confirms the existence of this process. The truncated tRNATyr is matured through the addition of two adenosines at the 3'-end, followed by CCA addition as represented in Type I tRNA (Fig. 5 -1A). Thus, the main editing pathway in squid mitochondria proceeds in the order Type II -> IV -> I.

However, the existence of Type III clones is inconsistent with a process mediated by polyadenylylation, suggesting that the tRNA precursor undergoes another maturation process(es). Two possible mechanisms can be postulated to explain the generation of Type III clones. One is that processing might occur at the same site at which Type II tRNA is generated. An enzyme other than the polyadenylylation enzyme might insert the two guanosines into this truncated tRNATyr (Fig. 5 -1B). In the case of tRNA editing in platypus mt tRNA (16 ), cytidines are added to the 3'-part of the acceptor stem except for the discriminator position. Thus, a polymerase(s) which adds nucleotides to the 3'-end of tRNAs might exist in animal mitochondria. The other possible mechanism is that 3' processing at position G73 of tRNATyr might dominate over 5' processing of tRNACys and the CCA sequence might be added to the 3'-end of RNATyr having G72-G73 (Fig. 5 -2). tRNACys truncated at the 5'-terminus might be degraded too rapidly to be detected. At present, we cannot conclude which mechanism is actually operating in the generation of tRNATyr with G72-G73. In any case, besides a mechanism mediated by polyadenylylation such as described above, another mechanism(s) is considered to be involved in RNA processing in squid mt tRNATyr to generate Type III tRNA.

We do not know whether the tRNA corresponding to Type III tRNA, which possesses G at position 73, functions as a Tyr acceptor tRNA. The discriminator nucleotide largely functions as a recognition site for cognate aminoacyl tRNA synthetase. In E.coli tRNATyr, the adenosine at the discriminator nucleotide has been shown to be recognized strictly by tyrosyl-tRNA synthetase (23 ). If the recognition mechanism of the mt enzyme is similar to that of E.coli, the tRNATyr for Type III tRNA may be inactive in mitochondria. It can be speculated that the anticodon of the tRNA molecule was edited so as to be converted to a tRNA acceptable to another amino acid. To verify this possibility, we examined whether there were any differences in the anticodon sequences of edited tRNATyr with A72-A73 and non-edited tRNATyr with G72-G73. In order to distinguish between the cDNAs for the edited and non-edited tRNAsTyr, we used different primers for cDNA synthesis from the circularized tRNAs. To amplify cDNA for only the edited tRNATyr, a primer for cDNA synthesis with the sequence TGGTT at its 3'-end was used and for only the non-edited tRNATyr, a primer with TGGCC at its 3'-end was used. cDNAs, including the anticodon regions, were then amplified, cloned and sequenced. All the clones had a GUA anticodon corresponding to the tyrosine codon and no difference in anticodon was observed among all the edited and non-edited tRNATyr molecules (data not shown). Thus, if conversion of the discriminator nucleoside from G73 to A73 changed the specificity of the amino acid acceptance of the tRNAs (23 -25 ), this would not affect the codon recognition capability of tRNATyr.

Nucleotide overlap between mt tRNATyr and tRNACys genes has also been observed in the mitochondria of other animals besides squid, e.g. those of human (17 ), chicken (19 ), chiton (20 ) and Xenopus (26 ). Because all animal mt tRNATyr genes, including those mentioned above except chicken and squid, have adenosine at the discriminator position (27 ), the efficiency or specificity of the acceptance of the amino acid might differ between edited and non-edited tRNAsTyr in squid mitochondria. Interestingly, in the case of the chicken mt tRNATyr gene, the 3'-terminal nucleotide G73 overlaps with the 5'-terminal nucleotide G1 of the downstream tRNACys gene and this tRNATyr is also edited (S.Yokobori, and S.Pääbo, personal communication).

In this study, we found that RNA editing occurs in squid mt tRNA and we were able to obtain cDNA clones which seemed to be intermediates of the RNA editing process, as well as non-edited tRNA. Certain common features can be observed in our results and the recently reported RNA editing in land snail and platypus mt tRNAs. Some overlapping tRNA genes in mitochondria, if not all, may undergo an editing process in the 3'-part of their acceptor stems due to the action of a certain polymerase(s), which adds nucleotides at the 3'-end. To further elucidate the molecular mechanism of tRNA editing described here, where tRNA genes whose transcripts are to be edited usually overlap with their downstream genes, and its biological function, the construction of an in vitro editing assay system together with an in vitro processing system will be essential. Further work will clarify whether RNA editing in squid mt tRNAs or any other tRNAs is mediated by alternative processing, polyadenylylation or some other mechanism, as well as its biological function.

ACKNOWLEDGEMENTS

We thank Mr Sasuga for his early work on squid mt DNA sequence determination and Mr Nanbu for valuable discussions. This work was supported by a Grant-in Aid for Scientific Research on Priority Areas from the Ministry of Education, Science, Sports and Culture of Japan and the Human Frontier Science Program Organization.

REFERENCES

1 Cattaneo,R. (1991) Annu. Rev. Genet., 25, 71-88. MEDLINE Abstract

2 Gray,M.W. (1993) Curr. Opin. Genet., 3, 884-890.

3 Bass,B.L. (1993) In Gesteland,R.F. and Atkins,J,F. (eds), RNA World. Cold Spring Harbor Laboratory Press, Plainsview, NY, pp. 383-418.

4 Chen,S.H., Habib,G., Young,C.Y., Gu,Z.W., Lee,B.R., Weng,S.A., Silberman,S.R., Cai,S.J., Deslypere,J.P., Rosseneu,M. et al. (1987) Science, 238, 363-366. MEDLINE Abstract

5 Sommer,B., Köhler,M., Sprengel,R. and Seeburg,P.H. (1991) Cell, 67, 11-19. MEDLINE Abstract

6 Hoch,B., Naier,E.M., Appel,K., Igloi,G.L. and Kössel,H. (1991) Nature, 353, 178-180. MEDLINE Abstract

7 Blum,B., Bakarala,N. and Simpson,L. (1990) Cell, 60, 189-198. MEDLINE Abstract

8 Melcher,T., Maas,S., Herb,A., Sprengel,R., Seeburg,P.H. and Higuchi,M. (1996) Nature, 397, 460-464.

9 Teng.B., Burabt,C.F. and Davidson,N.O. (1993) Science, 260, 1816-1819. MEDLINE Abstract

10 Yu,W. and Schuster,W. (1995) J. Biol. Chem., 270, 18227-18233. MEDLINE Abstract

11 Lonergan,K.M. and Gray,M.W. (1993) Science, 259, 812-815. MEDLINE Abstract

12 Maréchal-Drouard,L., Ramamonjisoa,D., Cosset,A., Weil,J.H. and Dietrich,A. (1993) Nucleic Acids Res., 21, 4909-4914. MEDLINE Abstract

13 Janke,A. and Pääbo,S. (1993) Nucleic Acids Res., 21, 1523-1525. MEDLINE Abstract

14 Mörl,M., Dörner,M. and Pääbo,S. (1995) Nucleic Acids Res., 23, 3380-3384. MEDLINE Abstract

15 Yokobori,S. and Pääbo,S. (1995) Proc. Natl. Acad. Sci. USA, 92, 10432-10435. MEDLINE Abstract

16 Yokobori,S. and Pääbo,S. (1995) Nature, 377, 490. MEDLINE Abstract

17 Anderson,S., Bankier,A.T., Barrell,B.G., de Bruijn,M.H.L., Coulson,A.R., Drouin,J., Eperon,I.C., Nierlich,D.P., Roe,B.A., Sanger,F. et al. (1981) Nature, 290, 457-465. MEDLINE Abstract

18 Bibb,M.J., VanEtten,R.A., Wright,C.T., Walberg,M.W. and Clayton,D.A. (1981) Cell, 26, 167-180. MEDLINE Abstract

19 Desjardins,P. and Morias,R. (1990) J. Mol. Biol., 212, 599-634. MEDLINE Abstract

20 Boore,J.L. and Brown,W.M. (1994) Genetics, 138, 423-443. MEDLINE Abstract

21 Chomczynski,P. and Sacchi,N. (1987) Anal. Biochem., 162, 156-159. MEDLINE Abstract

22 Maniatis,T., Fritsch,E.F. and Sambrook,J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, p. 382.

23 Himeno,H., Hasegawa,T., Ueda,T., Watanabe,K. and Shimizu,M. (1990) Nucleic Acids Res., 18, 6815-6819. MEDLINE Abstract

24 Breitschopf,K. and Gross,H.J. (1994) EMBO J., 13, 3166-3167. MEDLINE Abstract

25 Breitschopf,K. and Gross,H.J. (1996) Nucleic Acids Res., 24, 405-410. MEDLINE Abstract

26 Roe,B.A., Ma,D.P., Wilson,R.K. and Wong,J.F. (1985) J. Biol. Chem., 260, 9759-9774. MEDLINE Abstract

27 Steinberg,S., Misch,A. and Sprinzl,M. (1993) Nucleic Acids Res., 21, 3011-3015. MEDLINE Abstract

Return

*To whom correspondence should be addressed. Tel/Fax: +81 3 5800 3914; Email: ueda@kwl.t.u-tokyo.ac.jp
Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 J. Biol. Chem.Home page
T. Nagaike, T. Suzuki, T. Katoh, and T. Ueda
Human Mitochondrial mRNAs Are Stabilized with Polyadenylation Regulated by Mitochondria-specific Poly(A) Polymerase and Polynucleotide Phosphorylase
J. Biol. Chem., May 20, 2005; 280(20): 19721 - 19727.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
C. E. Bullerwell and M. W. Gray
In Vitro Characterization of a tRNA Editing Activity in the Mitochondria of Spizellomyces punctatus, a Chytridiomycete Fungus
J. Biol. Chem., January 28, 2005; 280(4): 2463 - 2470.
[Abstract] [Full Text] [PDF]

Home page
 RNAHome page
M.-J. LAFOREST, C. E. BULLERWELL, L. FORGET, and B. F. LANG
Origin, evolution, and mechanism of 5' tRNA editing in chytridiomycete fungi
RNA, August 1, 2004; 10(8): 1191 - 1199.
[Abstract] [Full Text] [PDF]

Home page
 RNAHome page
Y. JACOB, E. SEIF, P.-O. PAQUET, and B. F. LANG
Loss of the mRNA-like region in mitochondrial tmRNAs of jakobids
RNA, April 1, 2004; 10(4): 605 - 614.
[Abstract] [Full Text] [PDF]

Home page
 RNAHome page
J. LEIGH and B. F. LANG
Mitochondrial 3' tRNA editing in the jakobid Seculamonas ecuadoriensis: A novel mechanism and implications for tRNA processing
RNA, April 1, 2004; 10(4): 615 - 621.
[Abstract] [Full Text] [PDF]

Home page
 Genes Dev.Home page
A. K. Hopper and E. M. Phizicky
tRNA transfers to the limelight
Genes & Dev., January 15, 2003; 17(2): 162 - 180.
[Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
D. V. Lavrov, W. M. Brown, and J. L. Boore
A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus
PNAS, November 22, 2000; (2000) 250402997.
[Abstract] [Full Text]

Home page
 Nucleic Acids ResHome page
A. S. Reichert and M. Morl
Repair of tRNAs in metazoan mitochondria
Nucleic Acids Res., May 15, 2000; 28(10): 2043 - 2048.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
A. Kurabayashi and R. Ueshima
Complete Sequence of the Mitochondrial DNA of the Primitive Opisthobranch Gastropod Pupa strigosa: Systematic Implication of the Genome Organization
Mol. Biol. Evol., February 1, 2000; 17(2): 266 - 277.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
T. Antes, H. Costandy, R. Mahendran, M. Spottswood, and D. Miller
Insertional Editing of Mitochondrial tRNAs of Physarum polycephalum and Didymium nigripes
Mol. Cell. Biol., December 1, 1998; 18(12): 7521 - 7527.
[Abstract] [Full Text]

Home page
 J. Biol. Chem.Home page
A. Reichert, U. Rothbauer, and M. Morl
Processing and Editing of Overlapping tRNAs in Human Mitochondria
J. Biol. Chem., November 27, 1998; 273(48): 31977 - 31984.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
D. V. Lavrov, W. M. Brown, and J. L. Boore
A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus
PNAS, December 5, 2000; 97(25): 13738 - 13742.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Print PDF (241K) Freely available
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (27)
Right arrowRequest Permissions
Right arrow Commercial Re-use Guidelines
for Open Access NAR Content
Google Scholar
Right arrow Articles by Tomita, K
Right arrow Articles by Watanabe, K
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Tomita, K
Right arrow Articles by Watanabe, K
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?