Balance between transcription and RNA degradation is vital for Saccharomyces cerevisiae mitochondria: Reduced transcription rescues the phenotype of deficient RNA degradation

Molecular Biology of the Cell

Volumn 17, Issue 3, 2006, Pages 1184-1193

  Rogowska, Agata T ^a,b   Puchta, Olga ^a   Czarnecka, Anna M ^a   Kaniak, Aneta ^b   Stepien, Piotr P ^a,b   Golik, Pawel ^a,b  

^a UNIVERSITY OF WARSAW   (Poland)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

EXORIBONUCLEASE; HELICASE; MITOCHONDRIAL RNA; RNA POLYMERASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FUNGAL GENE; GENE EXPRESSION; GENE INACTIVATION; INTRON; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY FUNCTION; RNA DEGRADATION; RNA SYNTHESIS; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; SUV3 GENE;

ALLELES; AMINO ACID SUBSTITUTION; CELL NUCLEUS; CELL RESPIRATION; DEAD-BOX RNA HELICASES; DNA-DIRECTED RNA POLYMERASES; GENE DELETION; GENOME, FUNGAL; INTRONS; MITOCHONDRIA; PHENOTYPE; RNA HELICASES; RNA STABILITY; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUPPRESSION, GENETIC; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ANIMALIA; SACCHAROMYCES CEREVISIAE;

EID: 33644851218     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-08-0796     Document Type: Article

References (58)

1. Bryan, A. C., Rodeheffer, M. S., Wearn, C. M., and Shadel, G. S. (2002). Sls1p is a membrane-bound regulator of transcription-coupled processes involved in Saccharomyces cerevisiae mitochondrial gene expression. Genetics 160, 75-82.
2. Burke, D., Dawson, D., and Stearns, T. (2000). Methods in Yeast Genetics, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
3. Carpousis, A. J. (2002). The Escherichia coli RNA degradosome: structure, function and relationship in other ribonucleolytic multienzyme complexes. Biochem. Soc. Trans. 30, 150-155.
4. Chen, W., Islas-Osuna, M. A., and Dieckmann, C. L. (1999). Suppressor analysis of mutations in the 5′-untranslated region of COB mRNA identifies components of general pathways for mitochondrial mRNA processing and decay in Saccharomyces ceremsiae. Genetics 151, 1315-1325.
5. Cheng, Z. F., and Deutscher, M. P. (2003). Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proc. Natl. Acad. Sci. USA 100, 6388-6393.
6. Cheng, Z. F., and Deutscher, M. P. (2005). An important role for RNase R in mRNA decay. Mol. Cell 17, 313-318.
7. Christianson, T., and Rabinowitz, M. (1983). Identification of multiple transcriptional initiation sites on the yeast mitochondrial genome by in vitro capping with guanylyltransferase. J. Biol. Chem. 258, 14025-14033.
8. Cliften, P. F., Jang, S. H., and Jaehning, J. A. (2000). Identifying a core RNA polymerase surface critical for interactions with a sigma-like specificity factor. Mol. Cell. Biol. 20, 7013-7023.
9. Cliften, P. F., Park, J. Y., Davis, B. P., Jang, S. H., and Jaehning, J. A. (1997). Identification of three regions essential for interaction between a sigma-like factor and core RNA polymerase. Genes Dev. 11, 2897-2909.
10. Deutscher, M. P., and Li, Z. (2001). Exoribonucleases and their multiple roles in RNA metabolism. Prog. Nucleic Acid Res. Mol. Biol. 66, 67-105.
11. Dmochowska, A., Golik, P., and Stepien, P. P. (1995). The novel nuclear gene DSS-1 of Saccharomyces cerevisiae is necessary for mitochondrial biogenesis. Curr. Genet. 28, 108-112.
12. Dujardin, G., Pajot, P., Groudinsky, O., and Slonimski, P. P. (1980). Long range control circuits within mitochondria and between nucleus and mitochondria. I. Methodology and phenomenology of suppressors. Mol. Gen. Genet. 279, 469-482.
13. Dziembowski, A., Malewicz, M., Minczuk, M., Golik, P., Dmochowska, A., and Stepien, P. P. (1998). The yeast nuclear gene DSS1, which codes for a putative RNase II, is necessary for the function of the mitochondrial degradosome in processing and turnover of RNA. Mol. Gen. Genet. 260, 108-114.
14. Dziembowski, A., Piwowarski, J., Hoser, R., Minczuk, M., Dmochowska, A., Siep, M., van der Spek, H., Grivell, L., and Stepien, P. P. (2003). The yeast mitochondrial degradosome. Its composition, interplay between RNA helicase and RNase activities and the role in mitochondrial RNA metabolism. J. Biol. Chem. 278, 1603-1611.
15. Foury, F., Roganti, T., Lecrenier, N., and Purnelle, B. (1998). The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett. 440, 325-331.
16. Gagliardi, D., Stepien, P. P., Temperley, R. J., Lightowlers, R. N., and Chrzanowska-Lightowlers, Z. M. (2004). Messenger RNA stability in mitochondria: different means to an end. Trends Genet. 20, 260-267.
17. Giaever, G.; et al. (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391.
18. Gietz, R. D., and Sugino, A. (1988). New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534.
19. Gietz, R. D., and Woods, R. A. (2002). Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350, 87-96.
20. Golik, P., Szczepanek, T., Bartnik, E., Stepien, P. P., and Lazowska, J. (1995). The S. cerevisiae nuclear gene SUV3 encoding a putative RNA helicase is necessary for the stability of mitochondrial transcripts containing multiple introns. Curr. Genet. 28, 217-224.
21. Groudinsky, O., Dujardin, G., and Slonimski, P. P. (1981). Long range control circuits within mitochondria and between nucleus and mitochondria. II. Genetic and biochemical analyses of suppressors which selectively alleviate the mitochondrial intron mutations. Mol. Gen. Genet. 184, 493-503.
22. Hanekamp, T., and Thorsness, P. E. (1999). YNT20, a bypass suppressor of ymel yme2, encodes a putative 3′-5′ exonuclease localized in mitochondria of Saccharomyces cerevisiae. Curr. Genet. 34, 438-448.
23. Hoffman, C. S., and Winston, F. (1987). A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57, 267-272.
24. Jang, S. H., and Jaehning, J. A. (1991). The yeast mitochondrial RNA polymerase specificity factor, MTF1, is similar to bacterial sigma factors. J. Biol. Chem. 266, 22671-22677.
25. Karlok, M. A., Jang, S. H., and Jaehning, J. A. (2002). Mutations in the yeast mitochondrial RNA polymerase specificity factor, Mtf1, verify an essential role in promoter utilization. J. Biol. Chem. 277, 28143-28149.
26. Kelly, J. L., Greenleaf, A. L., and Lehman, I. R. (1986). Isolation of the nuclear gene encoding a subunit of the yeast mitochondrial RNA polymerase. J. Biol. Chem. 261, 10348-10351.
27. Krause, K., and Dieckmann, C. L. (2004). Analysis of transcription asymmetries along the tRNAE-COB operon: evidence for transcription attenuation and rapid RNA degradation between coding sequences. Nucleic Acids Res. 32, 6276-6283.
28. Krause, K., Lopes de Souza, R., Roberts, D. G., and Dieckmann, C. L. (2004). The mitochondrial message-specific mRNA protectors Cbp1 and Pet309 are associated in a high-molecular weight complex. Mol. Biol. Cell 15, 2674-2683.
29. Mangus, D. A., Jang, S. H., and Jaehning, J. A. (1994). Release of the yeast mitochondrial RNA polymerase specificity factor from transcription complexes. J. Biol. Chem. 269, 26568-26574.
30. Margossian, S. P., and Butow, R. A. (1996). RNA turnover and the control of mitochondrial gene expression. Trends Biochem. Sci. 21, 392-396.
31. Margossian, S. P., Li, H., Zassenhaus, H. P., and Butow, R. A. (1996). The DExH box protein Suv3p is a component of a yeast mitochondrial 3′-to-5′ exoribonuclease that suppresses group 1 intron toxicity. Cell 84, 199-209.
32. Masters, B. S., Stohl, L. L., and Clayton, D. A. (1987). Yeast mitochondrial RNA polymerase is homologous to those encoded by bacteriophages T3 and T7. Cell 51, 89-99.
33. Matsunaga, M., and Jaehning, J. A. (2004). A mutation in the yeast mitochondrial core RNA polymerase, Rpo41, confers defects in both specificity factor interaction and promoter utilization. J. Biol. Chem. 279, 2012-2019.
34. Minczuk, M., Dmochowska, A., Palczewska, M., and Stepien, P. P. (2002). Overexpressed yeast mitochondrial putative RNA helicase Mss116 partially restores proper mtRNA metabolism in strains lacking the Suv3 mtRNA helicase. Yeast 29, 1285-1293.
35. Myers, A. M., Pape, L. K., and Tzagoloff, A. (1985). Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes in Saccharomyces cerevisiae. EMBO J. 4, 2087-2092.
36. Nguyen, L. H., Erzberger, J. P., Root, J., and Wilson, D. M., 3rd. (2000). The human homolog of Escherichia coli Orn degrades small single-stranded RNA and DNA oligomers. J. Biol. Chem. 275, 25900-25906.
37. Osinga, K. A., De Haan, M., Christianson, T., and Tabak, H. F. (1982). A nonanucleotide sequence involved in promotion of ribosomal RNA synthesis and RNA priming of DNA replication in yeast mitochondria. Nucleic Acids Res. 10, 7993-8006.
38. Piwowarski, J., Grzechnik, P., Dziembowski, A., Dmochowska, A., Minczuk, M., and Stepien, P. P. (2003). Human polynucleotide phosphorylase, hPN-Pase, is localized in mitochondria. J. Mol. Biol. 329, 853-857.
39. Rodeheffer, M. S., Boone, B. E., Bryan, A. C., and Shadel, G. S. (2001). Nam1p, a protein involved in RNA processing and translation, is coupled to transcription through an interaction with yeast mitochondrial RNA polymerase. J. Biol. Chem. 276, 8616-8622.
40. Schafer, B. (2005). RNA maturation in mitochondria of S. cerevisiae and S. pombe. Gene 354, 80-85.
41. Schinkel, A. H., Koerkamp, M. J., Touw, E. P., and Tabak, H. F. (1987). Specificity factor of yeast mitochondrial RNA polymerase. Purification and interaction with core RNA polymerase. J. Biol. Chem. 262, 12785-12791.
42. Schmidt, U., Maue, L, Lehmann, K., Belcher, S. M., Stahl, U., and Perlman, P. S. (1998). Mutant alleles of the MRS2 gene of yeast nuclear DNA suppress mutations in the catalytic core of a mitochondrial group II intron. J. Mol. Biol. 282, 525-541.
43. Seraphin, B., Boulet, A., Simon, M., and Faye, G. (1987). Construction of a yeast strain devoid of mitochondrial introns and its use to screen nuclear genes involved in mitochondrial splicing. Proc. Natl. Acad. Sci. USA 84, 6810-6814.
44. Seraphin, B., Simon, M., Boulet, A., and Faye, G. (1989). Mitochondrial splicing requires a protein from a novel helicase family. Nature 337, 84-87.
45. Shadel, G. S., and Clayton, D. A. (1995). A Saccharomyces cerevisiae mitochondrial transcription factor, sc-mtTFB, shares features with sigma factors but is functionally distinct. Mol. Cell. Biol. 15, 2101-2108.
46. Sikorski, R. S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
47. Stepien, P. P., Kokot, L., Leski, T., and Bartnik, E. (1995). The suv3 nuclear gene product is required for the in vivo processing of the yeast mitochondrial 21s rRNA transcripts containing the r1 intron. Curr. Genet. 27, 234-238.
48. Stepien, P. P., Margossian, S. P., Landsman, D., and Butow, R. A. (1992). The yeast nuclear gene suv3 affecting mitochondrial post-transcriptional processes encodes a putative ATP-dependent RNA helicase. Proc. Natl. Acad. Sci. USA 89, 6813-6817.
49. Tomecki, R., Dmochowska, A., Gewartowski, K., Dziembowski, A., and Stepien, P. P. (2004). Identification of a novel human nuclear-encoded mitochondrial poly(A) polymerase. Nucleic Acids Res. 32, 6001-6014.
50. Tzagoloff, A., and Myers, A. M. (1986). Genetics of mitochondrial biogenesis. Annu. Rev. Biochem. 55, 249-285.
51. Ulery, T. L., and Jaehning, J. A. (1994). MTF1, encoding the yeast mitochondrial RNA polymerase specificity factor, is located on chromosome XIII. Yeast 10, 839-841.
52. van Hoof, A., Lennertz, P., and Parker, R. (2000). Three conserved members of the RNase II family have unique and overlapping functions in the processing of 5S, 5.8S, U4, U5, RNase MRP and RNase P RNAs in yeast. EMBO J. 19, 1357-1365.
53. Vasudevan, S., and Peltz, S. W. (2003). Nuclear mRNA surveillance. Curr. Opin. Cell Biol. 15, 332-337.
54. Wegierski, T., Dmochowska, A., Jablonowska, A., Dziembowski, A., Bartnik, E., and Stepien, P. P. (1998). Yeast nuclear PET127 gene can suppress deletions of the SUV3 or DSS1 genes: an indication of a functional interaction between 3′ and 5′ ends of mitochondrial mRNAs. Acta Biochim. Pol. 45, 935-940.
55. Wiesenberger, G., and Fox, T. D. (1997). Pet127p, a membrane-associated protein involved in stability and processing of Saccharomyces cerevisiae mitochondrial RNAs. Mol. Cell. Biol. 17, 2816-2824.
56. Winzeler, E. A., et al. (1999). Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906.
57. Zassenhaus, H. P., Hofmann, T. J., Uthayashanker, R., Vincent, R. D., and Zona, M. (1988). Construction of a yeast mutant lacking the mitochondrial nuclease. Nucleic Acids Res. 16, 3283-3296.
58. Zuo, Y., and Deutscher, M. P. (2001). Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res. 29, 1017-1026.