Two independent activities define Ccm1p as a moonlighting protein in Saccharomyces cerevisiae

Bioscience Reports

Volumn 32, Issue 6, 2012, Pages 549-557

  Moreno, J Ignacio ^a   Patlolla, Babu ^a   Belton, Kerry R ^a   Jenkins, Brenita C ^a   Radchenkova, Polina V ^a   Piva, Marta A ^a  

^a ALCORN STATE UNIVERSITY   (United States)

Author keywords

CCM1; Mitochondria; Moonlighting protein; Splicing; Stability of 15S rRNA; Yeast

Indexed keywords

CARRIER PROTEIN; CCM1P PROTEIN; CYCLOOXYGENASE 1; CYTOCHROME C OXIDASE; LYSINE; MITOCHONDRIAL DNA; PENTATRICOPEPTIDE REPEAT PROTEIN; RIBOSOME RNA; RNA 15S; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; INTRON; MITOCHONDRION; NONHUMAN; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; RIBOSOME; RNA STABILITY; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; DNA, MITOCHONDRIAL; ENDORIBONUCLEASES; INTRONS; LYSINE; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEOTIDYLTRANSFERASES; REPETITIVE SEQUENCES, AMINO ACID; RNA, FUNGAL; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION;

SACCHAROMYCES CEREVISIAE;

EID: 84872397792     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20120066     Document Type: Article

References (40)

1. 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 (Pubitemid 29052308)
2. Pel, H. J. and Grivell, L. A. (1993) The biology of yeast mitochondrial introns. Mol. Biol. Rep. 18, 1-13
3. Lambowitz, A. M. and Belfort, M. (1993) Introns as mobile genetic elements. Annu. Rev. Biochem. 62, 587-622 (Pubitemid 23237882)
4. Belfort, M. (2003) Two for the price of one: a bifunctional intron-encoded DNA endonuclease-RNA maturase. Genes Dev. 17, 2860-2863
5. Huang, H. R., Rowe, C. E., Mohr, S., Jiang, Y., Lambowitz, A. M. and Perlman, P. S. (2005) The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function. Proc. Natl. Acad. Sci. U.S.A. 102, 163-168 (Pubitemid 40094446)
6. Watts, T., Khalimonchuk, O., Wolf, R. Z., Turk, E. M., Mohr, G. and Winge, D. R. (2011) Mne1 is a novel component of the mitochondrial splicing apparatus responsible for processing of a COX1 group I intron in yeast. J. Biol. Chem. 286, 10137-10146
7. Banroques, J., Perea, J. and Jacq, C. (1987) Efficient splicing of two yeast mitochondrial introns controlled by a nuclear-encoded maturase. EMBO J. 6, 1085-1091
8. Huberts, D. H. and van der Klei, I. J. (2010) Moonlighting proteins: an intriguing mode of multitasking. Biochim. Biophys. Acta 1803, 520-525
9. Valencik, M. L., Kloeckener-Gruissem, B., Poyton, R. O. and McEwen, J. E. (1989) Disruption of the yeast nuclear PET54 gene blocks excision of mitochondrial intron aI5β from pre-mRNA for cytochrome c oxidase subunit I. EMBO J. 8, 3899-3904 (Pubitemid 20016073)
10. Costanzo, M. C., Seaver, E. C. and Fox, T. D. (1986) At least two nuclear gene products are specifically required for translation of a single yeast mitochondrial mRNA. EMBO J. 5, 3637-3641
11. Kaspar, B. J., Bifano, A. L. and Caprara, M. G. (2008) A shared RNA-binding site in the Pet54 protein is required for translational activation and group I intron splicing in yeast mitochondria. Nucleic Acids Res. 36, 2958-2968 (Pubitemid 351737188)
12. Herbert, C. J., Labouesse, M., Dujardin, G. and Slonimski, P. P. (1988) The NAM2 proteins from S. cerevisiae and S. douglasii are mitochondrial leucyl-tRNA synthetases, and are involved in mRNA splicing. EMBO J. 7, 473-483
13. Labouesse, M. (1990) The yeast mitochondrial leucyl-tRNA synthetase is a splicing factor for the excision of several group I introns. Mol. Gen. Genet. 224, 209-221
14. Moreno, J. I., Buie, K. S., Price, R. E. and Piva, M. A. (2009) Ccm1p/Ygr150cp, a pentatricopeptide repeat protein, is essential to remove the fourth intron of both COB and COX1 pre-mRNAs in Saccharomyces cerevisiae. Curr. Genet. 55, 475-484
15. Boniecki, M. T., Rho, S. B., Tukalo, M., Hsu, J. L., Romero, E. P. and Martinis, S. A. (2009) Leucyl-tRNA synthetase-dependent and -independent activation of a group I intron. J. Biol. Chem. 284, 26243-26250
16. Sigrist, C. J. A., Cerutti, L., de Castro, E., Langendijk-Genevaux, P. S., Bulliard, V., Bairoch, A. and Hulo, N. (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res. 38, 161-166
17. Lurin, C., Andrés, C., Aubourg, S., Bellaoui, M., Bitton, F., Bruyère, C., Caboche, M., Debast, C., Gualberto, J., Hoffmann, B. et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16, 2089-2103 (Pubitemid 39059730)
18. Delannoy, E., Stanley, W. A., Bond, C. S. and Small, I. D. (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem. Soc. Trans. 35, 1643-1647
19. Kobayashi, K., Kawabata, M., Hisano, K., Kazama, T., Matsuoka, K., Sugita, M. and Nakamura, T. (2012) Identification and characterization of the RNA binding surface of the pentatricopeptide repeat protein. Nucleic Acids Res. 40, 2712-2723
20. Small, I. D. and Peeters, N. (2000) The PPR motif - a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 46-47 (Pubitemid 30100363)
21. Pfalz, J., Bayraktar, O. A., Prikryl, J. and Barkan, A. (2009) Site-specific binding of a PPR protein defines and stabilizes 5′ and 3′ mRNA termini in chloroplasts. EMBO J. 28, 2042-2052
22. Kotera, E., Tasaka, M. and Shikanai, T. (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433, 326-330
23. Tavares-Carreón, F., Camacho-Villasana, Y., Zamudio-Ochoa, A., Shingú-Vázquez, M., Torres-Larios, A. and Pérez- Martínez, X. (2008) The pentatricopeptide repeats present in Pet309 are necessary for translation but not for stability of the mitochondrial COX1 mRNA in yeast. J. Biol. Chem. 283, 1472-1479
24. Gobert, A., Gutmann, B., Taschner, A., Gössringer, M., Holzmann, J., Hartmann, R. K., Rossmanith, W. and Giegé, P. (2010) A single Arabidopsis organellar protein has RNase P activity. Nat. Struct. Mol. Biol. 17, 740-744
25. Puchta, O., Lubas, M., Lipinski, K. A., Piatkowski, J., Malecki, M. and Golik, P. (2010) DMR1(CCM1/YGR150C) of Saccharomyces cerevisiae encodes an RNA-binding protein from the pentatricopeptide repeat family required for the maintenance of the mitochondrial 15S ribosomal RNA. Genetics 184, 959-973
26. Kühl, I., Dujeancourt, L., Gaisne, M., Herbert, C. J. and Bonnefoy, N. (2011) A genome wide study in fission yeast reveals nine PPR proteins that regulate mitochondrial gene expression. Nucleic Acids Res. 39, 8029-8041
27. Taylor, S. D., Zhang, H., Eaton, J. S., Rodeheffer, M. S., Lebedeva, M. A., O'Rourke, T. W., Siede, W. and Shadel, G. S. (2005) The conserved Mec1/Rad53 nuclear checkpoint pathway regulates mitochondrial DNA copy number in Saccharomyces cerevisiae. Mol. Biol. Cell 16, 3010-3018 (Pubitemid 40741243)
28. Sambrook, J. and Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
29. Groudinsky, O., Bousquet, I., Wallis, M. G., Slonimski, P. P. and Dujardin, G. (1993) The NAM1/MTF2 nuclear gene product is selectively required for the stability and/or processing of mitochondrial transcripts of the atp6 and of the mosaic, cox1 and cytb genes in Saccharomyces cerevisiae. Mol. Gen. Genet. 240, 419-427 (Pubitemid 23285959)
30. Ben Asher, E., Groudinsky, O., Dujardin, G., Altamura, N., Kermorgant, M. and Slonimski, P. P. (1989) Novel class of nuclear genes involved in both mRNA splicing and protein synthesis in Saccharomyces cerevisiae mitochondria. Mol. Gen. Genet. 215, 517-528 (Pubitemid 19061477)
31. Rieger, K. J., Aljinovic, G., Lazowska, J., Pohl, T. M., Slonimski, P. P. and Aljinovic, G. (1997) A novel nuclear gene, CBT1, essential for mitochondrial cytochrome b formation: terminal processing of mRNA and intron dependence. Curr. Genet. 32, 163-174 (Pubitemid 27458251)
32. Patterson, B. and Guthrie, C. (1987) An essential yeast snRNA with a U5-like domain is required for splicing in vivo. Cell 49, 613-624
33. Schülke, N., Sepuri, N. B. and Pain, D. (1997) In vivo zippering of inner and outer mitochondrial membranes by a stable translocation intermediate. Proc. Natl. Acad. Sci. U.S.A. 94, 7314-7319 (Pubitemid 27345312)
34. Mueller, D. M. and Getz, G. S. (1986) Steady state analysis of mitochondrial RNA after growth of yeast Saccharomyces cerevisiae under catabolite repression and derepression. J. Biol. Chem. 261, 11816-11822 (Pubitemid 17206109)
35. Gan, X., Kitakawa, M., Yoshino, K., Oshiro, N., Yonezawa, K. and Isono, K. (2002) Tag-mediated isolation of yeast mitochondrial ribosome and mass spectrometric identification of its new components. Eur. J. Biochem. 269, 5203-5214 (Pubitemid 35340827)
36. Dennerlein, S., Rozanska, A., Wydro, M., Chrzanowska-Lightowlers, Z. M. and Lightowlers, R. N. (2010) Human ERAL1 is a mitochondrial RNA chaperone involved in the assembly of the 28S small mitochondrial ribosomal subunit. Biochem. J. 430, 551-558
37. Ringel, R., Sologub, M., Morozov, Y. I., Litonin, D., Cramer, P. and Temiakov, D. (2011) Structure of human mitochondrial RNA polymerase. Nature 478, 269-273
38. Boniecki, M. T., Rho, S. B., Tukalo, M., Hsu, J. L., Romero, E. P. and Martinis, S. A. (2009) Leucyl-tRNA synthetase-dependent and -independent activation of a group I intron. J. Biol. Chem. 284, 26243-26250
39. Costanzo, M. C. and Fox, T. D. (1990) Control of mitochondrial gene expression in Saccharomyces cerevisiae. Annu. Rev. Genet. 24, 91-113 (Pubitemid 120011542)
40. Biswas, T. K. and Getz, G. S. (1999) The single amino acid changes in the yeast mitochondrial S4 ribosomal protein cause temperature-sensitive defect in the accumulation of mitochondrial 15S rRNA. Biochemistry 38, 13042-13054