LRPPRC/SLIRP suppresses PNPase-mediated mRNA decay and promotes polyadenylation in human mitochondria

Nucleic Acids Research

Volumn 40, Issue 16, 2012, Pages 8033-8047

  Chujo, Takeshi ^a   Ohira, Takayuki ^a   Sakaguchi, Yuriko ^a   Goshima, Naoki ^b   Nomura, Nobuo ^b,c   Nagao, Asuteka ^a   Suzuki, Tsutomu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c MUSASHINO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; LEUCINE RICH PENTATRICOPEPTIDE REPEAT MOTIF CONTAINING PROTEIN; MESSENGER RNA; MITOCHONDRIAL POLY(A) POLYMERASE; MITOCHONDRIAL PROTEIN; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; PROTEIN SUV3; RNA BINDING PROTEIN; SRA STEM LOOP INTERACTING RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DOSAGE; HALF LIFE TIME; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRION; MOLECULAR MECHANICS; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RNA DEGRADATION; RNA METABOLISM; RNA SEQUENCE; RNA STABILITY;

DEAD-BOX RNA HELICASES; DNA-DIRECTED RNA POLYMERASES; HELA CELLS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEOPLASM PROTEINS; POLYADENYLATION; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RNA; RNA PRECURSORS; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84869822219     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks506     Document Type: Article

References (53)

1. Anderson, S., Bankier, A.T., Barrell, B.G., de Bruijn, M.H., Coulson, A.R., Drouin, J., Eperon, I.C., Nierlich, D.P., Roe, B.A., Sanger, F. et al. (1981) Sequence and organization of the human mitochondrial genome. Nature, 290, 457-465.
2. Ojala, D., Montoya, J. and Attardi, G. (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature, 290, 470-474.
3. Duborjal, H., Beugnot, R., Mousson de Camaret, B. and Issartel, J.P. (2002) Large functional range of steady-state levels of nuclear and mitochondrial transcripts coding for the subunits of the human mitochondrial OXPHOS system. Genome Res., 12, 1901-1909.
4. Slomovic, S., Laufer, D., Geiger, D. and Schuster, G. (2005) Polyadenylation and degradation of human mitochondrial RNA: the prokaryotic past leaves its mark. Mol. Cell. Biol., 25, 6427-6435.
5. Nagao, A., Hino-Shigi, N. and Suzuki, T. (2008) Measuring mRNA decay in human mitochondria. Methods Enzymol., 447, 489-499.
6. Morin, C., Mitchell, G., Larochelle, J., Lambert, M., Ogier, H., Robinson, B.H. and De Braekeleer, M. (1993) Clinical, metabolic, and genetic aspects of cytochrome C oxidase deficiency in Saguenay-Lac-Saint-Jean. Am. J. Hum. Genet., 53, 488-496.
7. Merante, F., Petrova-Benedict, R., MacKay, N., Mitchell, G., Lambert, M., Morin, C., De Braekeleer, M., Laframboise, R., Gagne, R. and Robinson, B.H. (1993) A biochemically distinct form of cytochrome oxidase (COX) deficiency in the Saguenay-Lac-Saint-Jean region of Quebec. Am. J. Hum. Genet., 53, 481-487.
8. Mootha, V.K., Lepage, P., Miller, K., Bunkenborg, J., Reich, M., Hjerrild, M., Delmonte, T., Villeneuve, A., Sladek, R., Xu, F. et al. (2003) Identification of a gene causing human cytochrome c oxidase deficiency by integrative genomics. Proc. Natl Acad. Sci. USA, 100, 605-610.
9. Sasarman, F., Brunel-Guitton, C., Antonicka, H., Wai, T. and Shoubridge, E.A. (2010) LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Mol. Biol. Cell, 21, 1315-1323.
10. Xu, F., Morin, C., Mitchell, G., Ackerley, C. and Robinson, B.H. (2004) The role of the LRPPRC (leucine-rich pentatricopeptide repeat cassette) gene in cytochrome oxidase assembly: mutation causes lowered levels of COX (cytochrome c oxidase) I and COX III mRNA. Biochem. J., 382, 331-336.
11. Mili, S. and Pinol-Roma, S. (2003) LRP130, a pentatricopeptide motif protein with a noncanonical RNA-binding domain, is bound in vivo to mitochondrial and nuclear RNAs. Mol. Cell. Biol., 23, 4972-4982.
12. Sterky, F.H., Ruzzenente, B., Gustafsson, C.M., Samuelsson, T. and Larsson, N.G. (2010) LRPPRC is a mitochondrial matrix protein that is conserved in metazoans. Biochem. Biophys. Res. Commun., 398, 759-764.
13. 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.
14. Hatchell, E.C., Colley, S.M., Beveridge, D.J., Epis, M.R., Stuart, L.M., Giles, K.M., Redfern, A.D., Miles, L.E., Barker, A., MacDonald, L.M. et al. (2006) SLIRP, a small SRA binding protein, is a nuclear receptor corepressor. Mol. Cell, 22, 657-668.
15. Gohil, V.M., Nilsson, R., Belcher-Timme, C.A., Luo, B., Root, D.E. and Mootha, V.K. (2010) Mitochondrial and nuclear genomic responses to loss of LRPPRC expression. J. Biol. Chem., 285, 13742-13747.
16. Baughman, J.M., Nilsson, R., Gohil, V.M., Arlow, D.H., Gauhar, Z. and Mootha, V.K. (2009) A computational screen for regulators of oxidative phosphorylation implicates SLIRP in mitochondrial RNA homeostasis. PLoS Genet., 5, e1000590.
17. Ruzzenente, B., Metodiev, M.D., Wredenberg, A., Bratic, A., Park, C.B., Camara, Y., Milenkovic, D., Zickermann, V., Wibom, R., Hultenby, K. et al. (2012) LRPPRC is necessary for polyadenylation and coordination of translation of mitochondrial mRNAs. EMBO J., 31, 443-456.
18. Temperley, R.J., Wydro, M., Lightowlers, R.N. and Chrzanowska- Lightowlers, Z.M. (2010) Human mitochondrial mRNAs-like members of all families, similar but different. Biochim. Biophys. Acta, 1797, 1081-1085.
19. Nagaike, T., Suzuki, T., Katoh, T. and Ueda, T. (2005) Human mitochondrial mRNAs are stabilized with polyadenylation regulated by mitochondria-specific poly(A) polymerase and polynucleotide phosphorylase. J. Biol. Chem., 280, 19721-19727.
20. 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.
21. Wydro, M., Bobrowicz, A., Temperley, R.J., Lightowlers, R.N. and Chrzanowska-Lightowlers, Z.M. (2010) Targeting of the cytosolic poly(A) binding protein PABPC1 to mitochondria causes mitochondrial translation inhibition. Nucleic Acids Res., 38, 3732-3742.
22. Rorbach, J., Nicholls, T.J. and Minczuk, M. (2011) PDE12 removes mitochondrial RNA poly(A) tails and controls translation in human mitochondria. Nucleic Acids Res., 39, 7750-7763.
23. Borowski, L.S., Szczesny, R.J., Brzezniak, L.K. and Stepien, P.P. (2010) RNA turnover in human mitochondria: more questions than answers? Biochim. Biophys. Acta, 1797, 1066-1070.
24. Zuo, Y. and Deutscher, M.P. (2001) Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res., 29, 1017-1026.
25. Chen, H.W., Rainey, R.N., Balatoni, C.E., Dawson, D.W., Troke, J.J., Wasiak, S., Hong, J.S., McBride, H.M., Koehler, C.M., Teitell, M.A. et al. (2006) Mammalian polynucleotide phosphorylase is an intermembrane space RNase that maintains mitochondrial homeostasis. Mol. Cell. Biol., 26, 8475-8487.
26. Wang, G., Chen, H.W., Oktay, Y., Zhang, J., Allen, E.L., Smith, G.M., Fan, K.C., Hong, J.S., French, S.W., McCaffery, J.M. et al. (2010) PNPASE regulates RNA import into mitochondria. Cell, 142, 456-467.
27. Sarkar, D., Leszczyniecka, M., Kang, D.C., Lebedeva, I.V., Valerie, K., Dhar, S., Pandita, T.K. and Fisher, P.B. (2003) Down-regulation of Myc as a potential target for growth arrest induced by human polynucleotide phosphorylase (hPNPaseold-35) in human melanoma cells. J. Biol. Chem., 278, 24542-24551.
28. Das, S.K., Sokhi, U.K., Bhutia, S.K., Azab, B., Su, Z.Z., Sarkar, D. and Fisher, P.B. (2010) Human polynucleotide phosphorylase selectively and preferentially degrades microRNA-221 in human melanoma cells. Proc. Natl Acad. Sci. USA, 107, 11948-11953.
29. 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.
30. Wang, D.D., Shu, Z., Lieser, S.A., Chen, P.L. and Lee, W.H. (2009) Human mitochondrial SUV3 and polynucleotide phosphorylase form a 330-kDa heteropentamer to cooperatively degrade double-stranded RNA with a 30-to-50 directionality. J. Biol. Chem., 284, 20812-20821.
31. Szczesny, R.J., Borowski, L.S., Brzezniak, L.K., Dmochowska, A., Gewartowski, K., Bartnik, E. and Stepien, P.P. (2010) Human mitochondrial RNA turnover caught in flagranti: involvement of hSuv3p helicase in RNA surveillance. Nucleic Acids Res., 38, 279-298.
32. Milligan, J.F., Groebe, D.R., Witherell, G.W. and Uhlenbeck, O.C. (1987) Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res., 15, 8783-8798.
33. Katoh, T. and Suzuki, T. (2007) Specific residues at every third position of siRNA shape its efficient RNAi activity. Nucleic Acids Res., 35, e27.
34. Parrott, A.M., Walsh, M.R. and Mathews, M.B. (2007) Analysis of RNA:protein interactions in vivo: identification of RNA-binding partners of nuclear factor 90. Methods Enzymol., 429, 243-260.
35. Goshima, N., Kawamura, Y., Fukumoto, A., Miura, A., Honma, R., Satoh, R., Wakamatsu, A., Yamamoto, J., Kimura, K., Nishikawa, T. et al. (2008) Human protein factory for converting the transcriptome into an in vitro-expressed proteome. Nat. Methods, 5, 1011-1017.
36. Temperley, R.J., Seneca, S.H., Tonska, K., Bartnik, E., Bindoff, L.A., Lightowlers, R.N. and Chrzanowska-Lightowlers, Z.M. (2003) Investigation of a pathogenic mtDNA microdeletion reveals a translation-dependent deadenylation decay pathway in human mitochondria. Hum. Mol. Genet., 12, 2341-2348.
37. Mercer, T.R., Neph, S., Dinger, M.E., Crawford, J., Smith, M.A., Shearwood, A.M., Haugen, E., Bracken, C.P., Rackham, O., Stamatoyannopoulos, J.A. et al. (2011) The human mitochondrial transcriptome. Cell, 146, 645-658.
38. Poulsen, J.B., Andersen, K.R., Kjaer, K.H., Durand, F., Faou, P., Vestergaard, A.L., Talbo, G.H., Hoogenraad, N., Brodersen, D.E., Justesen, J. et al. (2011) Human 20-phosphodiesterase localizes to the mitochondrial matrix with a putative function in mitochondrial RNA turnover. Nucleic Acids Res., 39, 3754-3770.
39. Prikryl, J., Rojas, M., Schuster, G. and Barkan, A. (2011) Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc. Natl Acad. Sci. USA, 108, 415-420.
40. Rackham, O., Shearwood, A.M., Mercer, T.R., Davies, S.M., Mattick, J.S. and Filipovska, A. (2011) Long noncoding RNAs are generated from the mitochondrial genome and regulated by nuclear-encoded proteins. RNA, 17, 2085-2093.
41. Denslow, N.D., Michaels, G.S., Montoya, J., Attardi, G. and O'Brien, T.W. (1989) Mechanism of mRNA binding to bovine mitochondrial ribosomes. J. Biol. Chem., 264, 8328-8338.
42. Minczuk, M., He, J., Duch, A.M., Ettema, T.J., Chlebowski, A., Dzionek, K., Nijtmans, L.G., Huynen, M.A. and Holt, I.J. (2011) TEFM (c17orf42) is necessary for transcription of human mtDNA. Nucleic Acids Res., 39, 4284-4299.
43. Cline, S.D., Lodeiro, M.F., Marnett, L.J., Cameron, C.E. and Arnold, J.J. (2010) Arrest of human mitochondrial RNA polymerase transcription by the biological aldehyde adduct of DNA, M1dG. Nucleic Acids Res., 38, 7546-7557.
44. 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.
45. Schmitz-Linneweber, C. and Small, I. (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci., 13, 663-670.
46. Liao, H.X. and Spremulli, L.L. (1989) Interaction of bovine mitochondrial ribosomes with messenger RNA. J. Biol. Chem., 264, 7518-7522.
47. Pagliarini, D.J., Calvo, S.E., Chang, B., Sheth, S.A., Vafai, S.B., Ong, S.E., Walford, G.A., Sugiana, C., Boneh, A., Chen, W.K. et al. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell, 134, 112-123.
48. Holzmann, J., Frank, P., Loffler, E., Bennett, K.L., Gerner, C. and Rossmanith, W. (2008) RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell, 135, 462-474.
49. Brzezniak, L.K., Bijata, M., Szczesny, R.J. and Stepien, P.P. (2011) Involvement of human ELAC2 gene product in 30 end processing of mitochondrial tRNAs. RNA Biol., 8, 616-626.
50. de Narvaez, C.C. and Schaup, H.W. (1979) In vivo transcriptionally coupled assembly of Escherichia coli ribosomal subunits. J. Mol. Biol., 134, 1-22.
51. Slomovic, S. and Schuster, G. (2008) Stable PNPase RNAi silencing: its effect on the processing and adenylation of human mitochondrial RNA. RNA, 14, 310-323.
52. Chang, D.D. and Clayton, D.A. (1985) Priming of human mitochondrial DNA replication occurs at the light-strand promoter. Proc. Natl Acad. Sci. USA, 82, 351-355.
53. Bratic, A., Wredenberg, A., Gronke, S., Stewart, J.B., Mourier, A., Ruzzenente, B., Kukat, C., Wibom, R., Habermann, B., Partridge, L. et al. (2011) The bicoid stability factor controls polyadenylation and expression of specific mitochondrial mRNAs in Drosophila melanogaster. PLoS Genet., 7, e1002324.