Group II intron reverse transcriptase in yeast mitochondria. Stabilization and regulation of reverse transcriptase activity by the intron RNA

Journal of Molecular Biology

Volumn 289, Issue 3, 1999, Pages 473-490

  Zimmerly, Steven ^a,d   Moran, John V ^b,e   Perlman, Philip S ^b   Lambowitz, Alan M ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d UNIVERSITY OF CALGARY   (Canada)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Group II intron; Reverse transcriptase; Ribozyme; RNA splicing; Transposition

Indexed keywords

COMPLEMENTARY DNA; DEOXYRIBONUCLEASE; FUNGAL PROTEIN; RIBONUCLEOPROTEIN; RNA DIRECTED DNA POLYMERASE;

ARTICLE; CROSS LINKING; GEL ELECTROPHORESIS; IMMUNOBLOTTING; INTRON; MITOCHONDRION; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; RNA SPLICING; YEAST;

EID: 0033546397     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2778     Document Type: Article

References (46)

1. Arlt, H., Steglich, G., Perryman, R., Guiard, B., Neupert, W. & Langer, T. (1998). The formation of respiratory chain complexes in mitochondria is under the proteolytic control of the m-AAA protease. Embo J. 17, 4837-4847.
2. Bergantino, E. & Carignani, G. (1990). Antibodies against a fused gene product identify the protein encoded by a group II yeast mitochondrial intron. Mol. Gen. Genet. 223, 249-257.
3. Blum, H., Beier, H. & Gross, H. J. (1987). Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis, 8, 93-99.
4. Bonitz, S. G., Coruzzi, G., Thalenfeld, B. E. & Tzagoloff, A. (1980). Assembly of the mitochondrial membrane system: Structure and nucleotide sequence of the gene coding for subunit 1 of yeast cytochrome oxidase. J. Biol. Chem. 255, 11927-11941.
5. Carignani, G., Netter, P., Bergantino, E. & Robineau, S. (1986). Expression of the mitochondrial split gene coding for cytochrome oxidase subunit I in S. cerevisiae: RNA splicing pathway. Curr. Genet. 11, 55-63.
6. Chen, B. & Lambowitz, A. M. (1997). De novo and DNA primer-mediated initiation of cDNA synthesis by the Mauriceville retroplasmid reverse transcriptase involve recognition of a 3′ CCA sequence. J. Mol. Biol. 271, 311-332.
7. Cousineau, B., Smith, D., Lawrence-Cavanagh, S., Mueller, J. E., Yang, J., Mills, D., Manias, D., Dunny, G., Lambowitz, A. M. & Belfort, M. (1998). Retrohoming of a bacterial group II intron: Mobility, via complete reverse splicing, independent of homologous DNA recombination. Cell, 94, 451-462.
8. Doolittle, R. F., Feng, D-F., Johnson, M. S. & McClure, M. A. (1989). Origins and evolutionary relationships of retroviruses. Quart. Rev. Biol. 64, 1-30.
9. Eickbush, T. H. (1994). Origin and evolutionary relationships of retroelements. In The Evolutionary Biology of Viruses (Morse, S. S., ed.), pp. 121-157, Raven Press, New York.
10. Eskes, R., Yang, J., Lambowitz, A. M. & Perlman, P. S. (1997). Mobility of yeast mitochondrial group II introns: Engineering a new site specificity and retrohoming via full reverse splicing. Cell, 88, 865-874.
11. Feng, Q., Moran, J. V., Kazazian, H. H., Jr & Boeke, J. D. (1996). Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell, 87, 905-916.
12. Gorbalenya, A. E. (1994). Self-splicing group I and group II introns encode homologous (putative) DNA endonucleases of a new family. Protein Sci. 3, 1117-1120.
13. Guo, H., Zimmerly, S., Perlman, P. S. & Lambowitz, A. M. (1997). Group II intron endonucleases use both RNA and protein subunits for recognition of specific sequences in double-stranded DNA. Embo J. 16, 6835-6848.
14. Hensgens, L. A., Arnberg, A. C., Roosendaal, E., van der Horst, G., van der Veen, R., van Ommen, G. J. & Grivell, L. A. (1983). Variation, transcription and circular RNAs of the mitochondrial gene for subunit I of cytochrome c oxidase. J. Mol. Biol. 164, 35-58.
15. Inouye, S. & Inouye, M. (1993). The retron: A bacterial retroelement required for the synthesis of msDNA. Curr. Opin. Gen. Dev. 3, 713-718.
16. Insdorf, N. F. & Bogenhagen, D. F. (1989). DNA polymerase γ from Xenopus laevis: The identification of a high molecular weight catalytic subunit by a novel DNA polymerase photolabeling procedure. J. Biol. Chem. 264, 21491-21497.
17. Kazazian, H. H., Jr & Moran, J. V. (1998). The impact of L1 retrotransposons on the human genome. Nature Genet. 19, 19-24.
18. Kennell, J. C., Moran, J. V., Perlman, P. S., Butow, R. A. & Lambowitz, A. M. (1993). Reverse transcriptase activity associated with maturase-encoding group II introns in yeast mitochondria. Cell, 73, 133-146.
19. Lanford, R. E., Notvall, L. & Beames, B. (1995). Nucleotide priming and reverse transcriptase activity of hepatitis B virus polymerase expressed in insect cells. J. Virol. 69, 4431-4439.
20. Lazowska, J., Meunier, B. & Macadre, C. (1994). Homing of a group II intron in yeast mitochondrial DNA is accompanied by unidirectional co-conversion of upstream-located markers. Embo J. 13, 4963-4972.
21. Levra-Juillet, E., Boulet, A., Séraphin, B., Simon, M. & Faye, G. (1989). Mitochondrial introns aI1 and/or aI2 are needed for the in vivo deletion of intervening sequences. Mol. Gen. Genet. 217, 168-171.
22. Luan, D. D., Korman, M. H., Jakubczak, J. L. & Eickbush, T. H. (1993). Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: A mechanism for non-LTR retrotransposition. Cell, 72, 595-605.
23. Matsuura, M., Saldanha, R., Ma, H., Wank, H., Yang, J., Mohr, G., Cavanagh, S., Dunny, G., Belfort, M. & Lambowitz, A. M. (1997). 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, 2910-2924.
24. Melek, M. & Shippen, D. E. (1996). Chromosome healing: Spontaneous and programmed de novo telomere formation by telomerase. Bioessays, 18, 301-308.
25. Mills, D. A., Manias, D. A., McKay, L. L. & Dunny, G. M. (1997). Homing of a group II intron from Lactococcus lactis subsp. lactis ML3. J. Bacteriol. 179, 6107-6111.
26. Mohr, G., Perlman, P. S. & Lambowitz, A. M. (1993). 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, 4991-4997.
27. Moran, J. V. (1994). Studies of Mobile Introns in the Mitochondrial Genome of Saccharomyces Cerevisiae. PhD thesis, University of Texas Southwestern Medical Center, Dallas, TX.
28. Moran, J. V., Mecklenburg, K. L., Sass, P., Belcher, S. M., Mahnke, D., Lewin, A. & Perlman, P. (1994). Splicing defective mutants of the COX1 gene of yeast mitochondrial DNA: Initial definition of the maturase domain of the group II intron AI2. Nucl. Acids Res. 22, 2057-2064.
29. Moran, J. V., Zimmerly, S., Eskes, R., Kennell, J. C., Lambowitz, A. M., Butow, R. A. & Perlman, P. S. (1995). Mobile group II introns of yeast mitochondrial DNA are novel site-specific retroelements. Mol. Cell. Biol. 15, 2828-2838.
30. Moran, J. V., Holmes, S. E., Naas, T. P., DeBerardinis, R. J., Boeke, J. D. & Kazazian, H. H., Jr. (1996). High frequency retrotransposition in cultured mammalian cells. Cell, 87, 917-927.
31. Mueller, M. W., Allmaier, M., Eskes, R. & Schweyen, R. J. (1993). Transposition of group II intron aI1 in yeast and invasion of mitochondrial genes at new locations. Nature, 366, 174-176.
32. Nakamura, T. M. & Cech, T. R. (1998). Reversing time: Origin of telomerase. Cell, 92, 587-590.
33. Saldanha, R., Chen, B., Wank, H., Matsuura, M., Edwards, J. & Lambowitz, A. M. (1999). RNA and protein catalysis in group II intron splicing and mobility reactions using purified components. Biochemistry, in the press.
34. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. Schmidt, W. M., Schweyen, R. J., Wolf, K. & Mueller, M. W. (1994). Transposable group II introns in fission and budding yeast: Site-specific genomic instabilities and formation of group II IVS p1DNAs. J. Mol. Biol. 243, 157-166.
36. Sellem, C. H., Lecellier, G. & Belcour, L. (1993). Transposition of a group II intron. Nature, 366, 176-178.
37. Shub, D. A., Goodrich-Blair, H. & Eddy, S. R. (1994). Amino acid sequence motif of group I intron endonucleases is conserved in open reading frames of group II introns. Trends Biochem. Sci. 19, 402-404.
38. van Dyck, L., Neupert, W. & Langer, T. (1998). The ATP-dependent PIM1 protease is required for the expression of intron-containing genes in mitochondria. Genes Dev. 12, 1515-1524.
39. Wang, H. & Blackburn, E. H. (1997). De novo telomere addition by Tetrahymena telomerase in vitro. Embo J. 16, 866-879.
40. Wang, H. & Lambowitz, A. M. (1993). The Mauriceville plasmid reverse transcriptase can initiate cDNA synthesis de novo and may be related to reverse transcriptase and DNA polymerase progenitor. Cell, 75, 1071-1081.
41. Wang, G.-H. & Seeger, C. (1992). The reverse transcriptase of hepatitis B virus acts as a protein primer for viral DNA synthesis. Cell, 71, 663-670.
42. Yang, J. & Eickbush, T. H. (1998). RNA-induced changes in the activity of the endonuclease encoded by the R2 retrotransposable element. Mol. Cell. Biol. 18, 3455-3465.
43. Yang, J., Zimmerly, S., Perlman, P. S. & Lambowitz, A. M. (1996). Efficient integration of an intron RNA into double-stranded DNA by reverse splicing. Nature, 381, 332-335.
44. Yang, J., Mohr, G., Perlman, P. S. & Lambowitz, A. M. (1998). 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, 505-523.
45. Zimmerly, S., Guo, H., Perlman, P. S. & Lambowitz, A. M. (1995a). Group II intron mobility occurs by target DNA-primed reverse transcription. Cell, 82, 545-554.
46. Zimmerly, S., Guo, H., Eskes, R., Yang, J., Perlman, P. S. & Lambowitz, A. M. (1995b). A group II intron RNA is a catalytic component of a DNA endonuclease involved in intron mobility. Cell, 83, 529-538.