Reverse transcriptase and reverse splicing activities encoded by the mobile group II intron cobI1 of fission yeast mitochondrial DNA

Journal of Molecular Biology

Volumn 329, Issue 2, 2003, Pages 191-206

  Schäfer, Bernd ^a   Gan, Lin ^a   Perlman, Philip S ^b  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Fission yeast mitochondria; Group II intron; Retrohoming; Reverse splicing; Reverse transcription

Indexed keywords

COMPLEMENTARY DNA; DOUBLE STRANDED DNA; MESSENGER RNA; MITOCHONDRIAL DNA; PRIMER DNA; RIBONUCLEOPROTEIN; RNA DIRECTED DNA POLYMERASE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL ANALYSIS; COBI1 GENE; DNA DETERMINATION; DNA STRAND; DNA SYNTHESIS; EXON; EXPERIMENT; FUNGAL GENE; FUNGAL STRAIN; GENE MAPPING; GENE SEQUENCE; GENE TARGETING; GENETIC CODE; INTRON; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; REACTION ANALYSIS; RNA SPLICING; SCHIZOSACCHAROMYCES POMBE; SEQUENCE ANALYSIS; STIMULATION; WILD TYPE; YEAST;

SCHIZOSACCHAROMYCES POMBE;

EID: 0037723901     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00441-8     Document Type: Article

References (46)

1. Xiong Y., Eickbush T.H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9:1990;3353-3362.
2. Eickbush T.H. Telomerase and retrotransposons: which came first? Science. 277:1997;911-912.
3. Lambowitz A.M., Caprara M.G., Zimmerly S., Perlman P.S. Group I and group II ribozymes as RNPs: clues to the past and guides to the future. Gesteland R.F., Cech T.R., Atkins J.F. The RNA World. 1999;451-485 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Zimmerly S., Hausner G., Wu X. Phylogenetic relationships among group II intron ORFs. Nucl. Acids Res. 29:2001;1238-1250.
5. Michel F., Lang B. Mitochondrial class II introns encode proteins related to the reverse transcriptases of retroviruses. Nature. 316:1985;641-643.
6. Mohr G., Perlman P.S., Lambowitz A.M. Evolutionary relationships among group II intron-encoded proteins and identification of a conserved domain that may be related to maturase function. Nucl. Acids Res. 21:1993;4991-4997.
7. Shub D.A., Goodrich-Blair H., Eddy S.R. Amino acid sequence motif of group I intron endonucleases is conserved in open reading frames of group II introns. Trends Biochem. Sci. 19:1994;402-404.
8. Eskes R., Liu L., Ma H., Chao M.Y., Dickson L., Lambowitz A.M., Perlman P.S. Multiple homing pathways used by yeast mitochondrial group II introns. Mol. Cell Biol. 20:2000;8432-8446.
9. Zimmerly S., Guo H., Eskes R., Yang J., Perlman P.S., Lambowitz A.M. A group II intron RNA is a catalytic component of a DNA endonuclease involved in intron mobility. Cell. 83:1995;529-538.
10. Kennell J.C., Moran J.V., Perlman P.S., Butow R.A., Lambowitz A.M. Reverse transcriptase activity associated with maturase-encoding group II introns in yeast mitochondria. Cell. 73:1993;133-146.
11. Zimmerly S., Guo H., Perlman P.S., Lambowitz A.M. Group II intron mobility occurs by target DNA-primed reverse transcription. Cell. 82:1995;545-554.
12. Cousineau B., Smith D., Lawrence-Cavanagh S., Mueller J.E., Yang J., Mills D., et al. Retrohoming of bacterial group II intron: mobility via complete reverse splicing, independent of homologous DNA recombination. Cell. 94:1998;451-462.
13. Eskes R., Yang J., Lambowitz A.M., Perlman P.S. Mobility of yeast mitochondrial group II introns: engineering a new site specificity and retrohoming via full reverse splicing. Cell. 88:1997;865-874.
14. Matsuura M., Saldanha R.J., Ma H., Wank H., Yang J., Mohr G., et al. A bacterial group II intron encoding reverse transcriptase, maturase, and DNA endonuclease activities: biochemical demonstration of maturase activity and insertion of new genetic information within the intron. Genes Dev. 11:1997;2910-2924.
15. Moran J.V., Zimmerly S., Eskes R., Kennell J.C., Lambowitz A.M., Butow R.A., Perlman P.S. Mobile group II introns of yeast mitochondrial DNA are novel site-specific retroelements. Mol. Cell Biol. 15:1995;2828-2838.
16. Kennell J.C., Saville B.J., Mohr S., Kuiper M.T., Sabourin J.R., Collins R.A., Lambowitz A.M. The VS replicates by reverse transcription as a satellite of a retroplasmid. Genes Dev. 9:1995;294-303.
17. Zimmerly S., Moran J.V., Perlman P.S., Lambowitz A.M. Group II intron reverse transcriptase in yeast mitochondria. Stabilization and regulation of reverse transcriptase activity by the intron RNA. J. Mol. Biol. 289:1999;473-490.
18. Morozova T., Seo W., Zimmerly S. Non-cognate template usage and alternative priming by a group II intron-encoded reverse transcriptase. J. Mol. Biol. 315:2002;951-963.
19. Yang J., Zimmerly S., Perlman P.S., Lambowitz A.M. Efficient integration of an intron RNA into double-stranded DNA by reverse splicing. Nature. 381:1996;332-335.
20. Zimmer M., Welser F., Oraler G., Wolf K. Distribution of mitochondrial introns in the species Schizosaccharomyces pombe and the origin of the group II intron in the gene encoding apocytochrome b. Curr. Genet. 12:1987;329-336.
21. Schäfer B., Merlos-Lange A.M., Anderl C., Welser F., Zimmer M., Wolf K. The mitochondrial genome of Schizosaccharomyces pombe: inability of all introns to splice autocatalytically, and construction of an intronless genome. Mol. Gen. Genet. 225:1991;158-167.
22. Schäfer B., Wolf K. A novel group II intron in the cox1 gene of the fission yeast Schizosaccharomyces pombe is inserted in the same codon as the mobile group II intron aI2 in the Saccharomyces cerevisiae cox1 homologue. Curr. Genet. 35:1999;602-608.
23. Schäfer B., Kaulich K., Wolf K. Mosaic structure of the cox2 gene in the petite negative yeast Schizosaccharomyces pombe: a group II intron is inserted at the same location as the otherwise unrelated group II introns in the mitochondria of higher plants. Gene. 214:1998;101-112.
24. Lang B.F., Ahne F., Bonen L. The mitochondrial genome of the fission yeast Schizosaccharomyces pombe. The cytochrome b gene has an intron closely related to the first two introns in the Saccharomyces cerevisiae cox1 gene. J. Mol. Biol. 184:1985;353-366.
25. Paschke T., Meurer P., Schäfer B., Wolf K. Homing of mitochondrial introns in the fission yeast Schizosaccharomyces pombe. Endocytobiosis Cell Res. 10:1994;205-213.
26. Schmidt W.M., Schweyen R.J., Wolf K., Mueller M.W. Transposable group II introns in fission and budding yeast. Site-specific genomic instabilities and formation of group II IVS plDNAs. J. Mol. Biol. 243:1994;157-166.
27. Massardo D.R., Manna F., Schäfer B., Wolf K., Del Giudice L. Complete absence of mitochondrial DNA in the petite-negative yeast Schizosaccharomyces pombe leads to resistance towards lycorine. Curr. Genet. 25:1994;80-83.
28. Yang J., Mohr G., Perlman P.S., Lambowitz A.M. Group II intron mobility in yeast mitochondria: target DNA-primed reverse transcription activity of aI1 and reverse splicing into DNA transposition sites in vitro. J. Mol. Biol. 282:1998;505-523.
29. Tabor S., Richardson C.C. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc. Natl Acad. Sci. USA. 84:1987;4767-4771.
30. Wank H., SanFilippo J., Singh R.N., Matsuura M., Lambowitz A.M. A reverse transcriptase/maturase promotes splicing by binding at its own coding segment in a group II intron RNA. Mol. Cell. 4:1999;239-250.
31. Guo H., Zimmerly S., Perlman P.S., Lambowitz A.M. Group II intron endonucleases use both RNA and protein subunits for recognition of specific sequences in double-stranded DNA. EMBO J. 16:1997;6835-6848.
32. Saldanha R.J., Chen B., Wank H., Matsuura M., Edwards J., Lambowitz A.M. RNA and protein catalysis in group II intron splicing and mobility reactions using purified components. Biochemistry. 38:1999;9069-9083.
33. Matsuura M., Noah J.W., Lambowitz A.M. Mechanism of maturase-promoted group II intron splicing. EMBO J. 20:2001;7259-7270.
34. Singh R.N., Saldanha R.J., D'Souza L.M., Lambowitz A.M. Binding of a group II intron-encoded reverse transcriptase/maturase to its high affinity intron RNA binding site involves sequence-specific recognition and autoregulates translation. J. Mol. Biol. 318:2002;287-303.
35. Eickbush T.H. Origin and evolutionary relation-ships of retroelements. Morse S.S. The Evolutionary Biology of Viruses. 1994;121-157 Raven Press, New York.
36. Nakamura T.M., Cech T.R. Reversing time: origin of telomerase. Cell. 92:1998;587-590.
37. Michel F., Ferat J.L. Structure and activities of group II introns. Annu. Rev. Biochem. 64:1995;435-461.
38. Jacquier A. Group II introns: elaborate ribozymes. Biochimie. 78:1996;474-487.
39. Swisher J.F., Su L.J., Brenowitz M., Anderson V.E., Pyle A.M. Productive folding to the native state by a group II intron ribozyme. J. Mol. Biol. 315:2002;297-310.
40. Dickson L., Huang H.R., Liu L., Matsuura M., Lambowitz A.M., Perlman P.S. Retrotransposition of a yeast group II intron occurs by reverse splicing directly into ectopic DNA sites. Proc. Natl Acad. Sci. USA. 98:2001;13207-13212.
41. Singh N.N., Lambowitz A.M. Interaction of a group II intron ribonucleoprotein endonuclease with its DNA target site investigated by DNA footprinting and modification interference. J. Mol. Biol. 309:2001;361-386.
42. Martinez-Abarca F., Garcia-Rodriguez F.M., Toro N. Homing of a bacterial group II intron with an intron-encoded protein lacking a recognizable endonuclease domain. Mol. Microbiol. 35:2000;1405-1412.
43. Locker J. Analytical and preparative electrophoresis of RNA in agarose-urea. Anal. Biochem. 98:1979;358-367.
44. Lang B.F., Wolf K. The mitochondrial genome of the fission yeast Schizosaccharomyces pombe 2. Localization of genes by interspecific hybridization in strain ade 7-50h- and cloning of the genome in small fragments. Mol. Gen. Genet. 196:1984;465-472.
45. Sambrook J., Frisch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. SanFilippo J., Lambowitz A.M. Characterization of the C-terminal DNA-binding/DNA endonuclease region of a group II intron-encoded protein. J. Mol. Biol. 324:2002;933-951.