The leucine-rich pentatricopeptide repeat-containing protein (LRPPRC) does not activate transcription in mammalian mitochondria

Journal of Biological Chemistry

Volumn 288, Issue 22, 2013, Pages 15510-15519

  Harmel, Julia ^a   Ruzzenente, Benedetta ^a   Terzioglu, Mügen ^a   Spåhr, Henrik ^a   Falkenberg, Maria ^b   Larsson, Nils Göran ^a,c  

^a MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ARTIFICIAL CHROMOSOMES; HUMAN CELL LINES; IMMUNOPRECIPITATIONS; MITOCHONDRIAL TRANSCRIPTION; OXIDATIVE PHOSPHORYLATION; PHYSIOLOGICAL RANGE; POST-TRANSCRIPTIONAL; STEADY-STATE LEVEL;

AMINO ACIDS; CELL CULTURE; MAMMALS; PLANTS (BOTANY); PROTEINS; RNA; TRANSCRIPTION;

MITOCHONDRIA;

DNA DIRECTED RNA POLYMERASE; LEUCINE RICH PENTATRICOPEPTIDE REPEAT CONTAINING PROTEIN; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; POLRMT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATOGRAPHY; CONTROLLED STUDY; DNA TRANSCRIPTION; GENE EXPRESSION; HETEROZYGOTE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; STEADY STATE; TRANSCRIPTION REGULATION;

LRPPRC; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MITOCHONDRIAL DNA; MITOCHONDRIAL RNA POLYMERASE; MITOCHONDRIAL TRANSCRIPTION; MOUSE GENETICS; MRNA; POST-TRANSCRIPTIONAL REGULATION;

ANIMALS; CYTOCHROMES B; DNA, MITOCHONDRIAL; DNA-DIRECTED RNA POLYMERASES; ELECTRON TRANSPORT COMPLEX I; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MITOCHONDRIA, LIVER; MITOCHONDRIAL PROTEINS; NADH DEHYDROGENASE; NEOPLASM PROTEINS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); MAMMALIA; MUS; MUS MUSCULUS;

EID: 84878408163     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.471649     Document Type: Article

References (38)

1. Barkan, A., Rojas, M., Fujii, S., Yap, A., Chong, Y. S., Bond, C. S., and Small, I. (2012) A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet. 8, e1002910
2. Schmitz-Linneweber, C., and Small, I. (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 13, 663-670
3. Zehrmann, A., Verbitskiy, D., Härtel, B., Brennicke, A., and Takenaka, M. (2011) PPR proteins network as site-specific RNA editing factors in plant organelles. RNA Biol. 8, 67-70
4. Tiranti, V., Savoia, A., Forti, F., D'Apolito, M. F., Centra, M., Rocchi, M., and Zeviani, M. (1997) Identification of the gene encoding the human mitochondrial RNA polymerase (h-mtRPOL) by cyberscreening of the Expressed Sequence Tags database. Hum. Mol. Genet. 6, 615-625 (Pubitemid 27142114)
5. Rackham, O., Davies, S. M. K., Shearwood, A.-M. J., Hamilton, K. L., Whelan, J., and Filipovska, A. (2009) Pentatricopeptide repeat domain protein 1 lowers the levels of mitochondrial leucine tRNAs in cells. Nucleic Acids Res. 37, 5859-5867
6. Xu, F., Ackerley, C., Maj, M. C., Addis, J. B. L., Levandovskiy, V., Lee, J., Mackay, N., Cameron, J. M., and Robinson, B. H. (2008) Disruption of a mitochondrial RNA-binding protein gene results in decreased cytochrome b expression and a marked reduction in ubiquinol-cytochrome c reductase activity in mouse heart mitochondria. Biochem. J. 416, 15-26
7. Davies, S. M. K., Rackham, O., Shearwood, A.-M. J., Hamilton, K. L., Narsai, R., Whelan, J., and Filipovska, A. (2009) Pentatricopeptide repeat domain protein 3 associates with the mitochondrial small ribosomal subunit and regulates translation. FEBS Lett. 583, 1853-1858
8. Davies, S. M. K., Lopez Sanchez, M. I. G., Narsai, R., Shearwood, A.-M. J., Razif, M. F. M., Small, I. D., Whelan, J., Rackham, O., and Filipovska, A. (2012) MRPS27 is a pentatricopeptide repeat domain protein required for the translation of mitochondrially encoded proteins. FEBS Lett. 586, 3555-3561
9. Holzmann, J., Frank, P., Löffler, 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
10. Mili, S., and Piñol-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 (Pubitemid 36793342)
11. Sasarman, F., Brunel-Guitton, C., Antonicka, H., Wai, T., Shoubridge, E. A., and LSFC Consortium (2010) LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates post-transcriptional gene expression in mitochondria. Mol. Biol. Cell 21, 1315-1323
12. Ruzzenente, B., Metodiev, M. D., Wredenberg, A., Bratic, A., Park, C. B., Cámara, Y., Milenkovic, D., Zickermann, V., Wibom, R., Hultenby, K., Erdjument-Bromage, H., Tempst, P., Brandt, U., Stewart, J. B., Gustafsson, C. M., and Larsson, N.-G. (2012) LRPPRC is necessary for polyadenylation and coordination of translation of mitochondrial mRNAs. EMBO J. 31, 443-456
13. Chujo, T., Ohira, T., Sakaguchi, Y., Goshima, N., Nomura, N., Nagao, A., and Suzuki, T. (2012) LRPPRC/SLIRP suppresses PNPase-mediated mRNA decay and promotes polyadenylation in human mitochondria. Nucleic Acids Res. 40, 8033-8047
14. 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 (Pubitemid 39141597)
15. Topisirovic, I., Siddiqui, N., Orolicki, S., Skrabanek, L. A., Tremblay, M., Hoang, T., and Borden, K. L. B. (2009) Stability of eukaryotic translation initiation factor 4E mRNA is regulated by HuR, and this activity is dysregulated in cancer. Mol. Cell. Biol. 29, 1152-1162
16. Cooper, M. P., Uldry, M., Kajimura, S., Arany, Z., and Spiegelman, B. M. (2008) Modulation of PGC-1 coactivator pathways in brown fat differentiation through LRP130. J. Biol. Chem. 283, 31960-31967
17. 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
18. Liu, L., Sanosaka, M., Lei, S., Bestwick, M. L., Frey, J. H., Jr., Surovtseva, Y. V., Shadel, G. S., and Cooper, M. P. (2011) LRP130 protein remodels mitochondria and stimulates fatty acid oxidation. J. Biol. Chem. 286, 41253-41264
19. Ekstrand, M. I., Falkenberg, M., Rantanen, A., Park, C. B., Gaspari, M., Hultenby, K., Rustin, P., Gustafsson, C. M., and Larsson, N.-G. (2004) Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum. Mol. Genet. 13, 935-944 (Pubitemid 38628429)
20. Falkenberg, M., Gaspari, M., Rantanen, A., Trifunovic, A., Larsson, N.-G., and Gustafsson, C. M. (2002) Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat. Genet. 31, 289-294
21. Spåhr, H., Habermann, B., Gustafsson, C. M., Larsson, N.-G., and Hällberg, B. M. (2012) Structure of the human MTERF4-NSUN4 protein complex that regulates mitochondrial ribosome biogenesis. Proc. Natl. Acad. Sci. U.S.A. 109, 15253-15258
22. Gaspari, M., Falkenberg, M., Larsson, N.-G., and Gustafsson, C. M. (2004) The mitochondrial RNA polymerase contributes critically to promoter specificity in mammalian cells. EMBO J. 23, 4606-4614 (Pubitemid 39657860)
23. Wong, T. S., Rajagopalan, S., Freund, S. M., Rutherford, T. J., Andreeva, A., Townsley, F. M., Petrovich, M., and Fersht, A. R. (2009) Biophysical characterizations of human mitochondrial transcription factor A and its binding to tumor suppressor p53. Nucleic Acids Res. 37, 6765-6783
24. Shi, Y., Dierckx, A., Wanrooij, P. H., Wanrooij, S., Larsson, N.-G., Wilhelmsson, L. M., Falkenberg, M., and Gustafsson, C. M. (2012) Mammalian transcription factor A is a core component of the mitochondrial transcription machinery. Proc. Natl. Acad. Sci. U.S.A. 109, 16510-16515
25. Bogenhagen, D. F., Rousseau, D., and Burke, S. (2008) The layered structure of human mitochondrial DNA nucleoids. J. Biol. Chem. 283, 3665-3675
26. Larsson, N.-G. (2010) Somatic mitochondrial DNA mutations in mammalian aging. Annu. Rev. Biochem. 79, 683-706
27. Cooper, M. P., Qu, L., Rohas, L. M., Lin, J., Yang, W., Erdjument-Bromage, H., Tempst, P., and Spiegelman, B. M. (2006) Defects in energy homeostasis in Leigh syndrome French Canadian variant through PGC-1α/LRP130 complex. Genes Dev. 20, 2996-3009 (Pubitemid 44771734)
28. Park, C. B., Asin-Cayuela, J., Cámara, Y., Shi, Y., Pellegrini, M., Gaspari, M., Wibom, R., Hultenby, K., Erdjument-Bromage, H., Tempst, P., Falkenberg M, Gustafsson, C. M., and Larsson N.-G. (2007) MTERF3 is a negative regulator of mammalian mtDNA transcription. Cell 130, 273-285 (Pubitemid 47081137)
29. Metodiev, M. D., Lesko, N., Park, C. B., Cámara, Y., Shi, Y., Wibom, R., Hultenby, K., Gustafsson, C. M., and Larsson, N.-G. (2009) Methylation of 12S rRNA is necessary for in vivo stability of the small subunit of the mammalian mitochondrial ribosome. Cell Metab. 9, 386-397
30. Cámara, Y., Asin-Cayuela, J., Park, C. B., Metodiev, M. D., Shi, Y., Ruzzenente, B., Kukat, C., Habermann, B., Wibom, R., Hultenby, K., Franz T, Erdjument-Bromage, H., Tempst, P., Hallberg, B. M., Gustafsson, C. M., and Larsson, N.-G. (2011) MTERF4 regulates translation by targeting the methyltransferase NSUN4 to the mammalian mitochondrial ribosome. Cell Metab. 13, 527-539
31. Bratic, A., Wredenberg, A., Grönke, S., Stewart, J. B., Mourier, A., Ruzzenente, B., Kukat, C., Wibom, R., Habermann, B., Partridge, L., and Larsson, N.-G. (2011) The bicoid stability factor controls polyadenylation and expression of specific mitochondrial mRNAs in Drosophila melanogaster. PLoS Genet. 7, e1002324
32. Parisi, M. A., and Clayton, D. A. (1991) Similarity of human mitochondrial transcription factor 1 to high mobility group proteins. Science 252, 965-969 (Pubitemid 21917015)
33. Falkenberg, M., Larsson, N.-G., and Gustafsson, C. M. (2007) DNA replication and transcription in mammalian mitochondria. Annu. Rev. Biochem. 76, 679-699
34. Hällberg, B. M., and Larsson, N.-G. (2011) TFAM forces mtDNA to make a U-turn. Nat. Struct. Mol. Biol. 18, 1179-1181
35. Liu, L., and McKeehan, W. L. (2002) Sequence analysis of LRPPRC and its SEC1 domain interaction partners suggests roles in cytoskeletal organization, vesicular trafficking, nucleocytosolic shuttling, and chromosome activity. Genomics 79, 124-136 (Pubitemid 34112074)
36. Mancebo, R., Zhou, X., Shillinglaw, W., Henzel, W., and Macdonald, P. M. (2001) BSF binds specifically to the bicoid mRNA 3′ untranslated region and contributes to stabilization of bicoid mRNA. Mol. Cell. Biol. 21, 3462-3471 (Pubitemid 32381782)
37. Mili, S., Shu, H. J., Zhao, Y., and Piñol-Roma, S. (2001) Distinct RNP complexes of shuttling hnRNP proteins with pre-mRNA and mRNA: candidate intermediates in formation and export of mRNA. Mol. Cell. Biol. 21, 7307-7319 (Pubitemid 32953484)
38. Sondheimer, N., Fang, J.-K., Polyak, E., Falk, M. J., and Avadhani, N. G. (2010) Leucine-rich pentatricopeptide-repeat containing protein regulates mitochondrial transcription. Biochemistry 49, 7467-7473