Tissue-specific responses to the LRPPRC founder mutation in French Canadian Leigh Syndrome

Human Molecular Genetics

Volumn 24, Issue 2, 2015, Pages 480-491

  Sasarman, Florin ^a   Nishimura, Tamiko ^a   Antonicka, Hana ^a   Weraarpachai, Woranontee ^a   Shoubridge, Eric A ^a,b   Allen, Bruce ^b   Burelle, Yan ^b   Charron, Guy ^b   Coderre, Lise ^b   DesRosiers, Christine ^b   Laprise, Catherine ^b   Morin, Charles ^b   Rioux, John ^b  

^a MCGILL UNIVERSITY   (Canada)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; DETERGENT; MESSENGER RNA; MITOCHONDRIAL RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); LRPPRC PROTEIN, HUMAN; PROTEIN BINDING; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; SLIRP PROTEIN, HUMAN; TUMOR PROTEIN;

ARTICLE; CASE REPORT; COMPLEX I DEFICIENCY; CONTROLLED STUDY; CYTOCHROME C OXIDASE DEFICIENCY; FIBROBLAST; GENE; GENE MUTATION; HEART MITOCHONDRION; HUMAN; HUMAN CELL; HUMAN TISSUE; LEIGH DISEASE; LIVER MITOCHONDRION; LRPPRC GENE; MITOCHONDRIAL MEMBRANE; MUSCLE CELL; MUSCLE MITOCHONDRION; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; PRIORITY JOURNAL; RNA TRANSLATION; SKELETAL MUSCLE; SMALL RIBOSOMAL SUBUNIT; STEADY STATE; STOICHIOMETRY; TISSUE SPECIFICITY; ANTIBODY SPECIFICITY; CELL CULTURE; GENETICS; LIVER; METABOLISM; MITOCHONDRION; MUTATION;

CELLS, CULTURED; HUMANS; LEIGH DISEASE; LIVER; MITOCHONDRIA; MUSCLE CELLS; MUSCLE, SKELETAL; MUTATION; NEOPLASM PROTEINS; ORGAN SPECIFICITY; OXIDATIVE PHOSPHORYLATION; PROTEIN BINDING; RIBONUCLEOPROTEINS; RNA-BINDING PROTEINS;

EID: 84922475667     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu468     Document Type: Article

References (33)

1. Koopman, W.J., Willems, P.H. and Smeitink, J.A. (2012) Monogenic mitochondrial disorders. N. Engl. J. Med., 366, 1132-1141.
2. Nunnari, J. and Suomalainen, A. (2012) Mitochondria: in sickness and in health. Cell, 148, 1145-1159.
3. Schon, E.A. and Przedborski, S. (2011) Mitochondria: the next (neurode) generation. Neuron, 70, 1033-1053.
4. Leigh, D. (1951) Subacute necrotizing encephalomyelopathy in an infant. J. Neurochem., 14, 216-221.
5. Zhu, Z., Yao, J., Johns, T., Fu, K., De Bie, I., Macmillan, C., Cuthbert, A.P., Newbold, R.F., Wang, J., Chevrette, M. et al. (1998) SURF1, encoding a factor involved in the biogenesis of cytochrome c oxidase, is mutated in Leigh syndrome. Nat. Genet., 20, 337-343.
6. Rahman, S., Blok, R.B., Dahl, H.H., Danks, D.M., Kirby, D.M., Chow, C.W., Christodoulou, J. and Thorburn, D.R. (1996) Leigh syndrome: clinical features and biochemical and DNA abnormalities. Ann. Neurol., 39, 343-351.
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. Debray, F.G., Morin, C., Janvier, A., Villeneuve, J., Maranda, B., Laframboise, R., Lacroix, J., Decarie, J.C., Robitaille, Y., Lambert, M. et al. (2011) LRPPRC mutations cause a phenotypically distinct form of Leigh syndrome with cytochrome c oxidase deficiency. J. Med. Genet., 48, 183-189.
9. 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.
10. 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.
11. Barkan, A. and Small, I. (2014) Pentatricopeptide repeat proteins in plants. Ann. Rev. Plant Biol., 65, 415-442.
12. 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.
13. Yin, P., Li, Q., Yan, C., Liu, Y., Liu, J., Yu, F., Wang, Z., Long, J., He, J., Wang, H.W. et al. (2013) Structural basis for the modular recognition of single-stranded RNA by PPR proteins. Nature, 504, 168-171.
14. Davies, S.M., Lopez Sanchez, M.I., Narsai, R., Shearwood, A.M., Razif, M.F., 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.
15. 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.
16. 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.
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. (2011) LRPPRC is necessary for polyadenylation and coordination of translation of mitochondrial mRNAs. EMBO J., 31, 443-456.
18. 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.
19. Antonicka, H., Sasarman, F., Kennaway, N.G. and Shoubridge, E.A. (2006) The molecular basis for tissue specificity of the oxidative phosphorylation deficiencies in patients with mutations in the mitochondrial translation factor EFG1. Hum. Mol. Genet., 15, 1835-1846.
20. Colley, S.M., Wintle, L., Searles, R., Russell, V., Firman, R.C., Smith, S., Deboer, K., Merriner, D.J., Genevieve, B., Bentel, J.M. et al. (2013) Loss of the nuclear receptor corepressor SLIRP compromises male fertility. PLoS One, 8, e70700.
21. Antonicka, H., Sasarman, F., Nishimura, T., Paupe, V. and Shoubridge, E.A. (2013) The mitochondrial RNA-binding protein GRSF1 localizes to RNA granules and is required for posttranscriptional mitochondrial gene expression. Cell Metab., 17, 386-398.
22. Jourdain, A.A., Koppen, M., Wydro, M., Rodley, C.D., Lightowlers, R.N., Chrzanowska-Lightowlers, Z.M. and Martinou, J.C. (2013) GRSF1 regulates RNA processing in mitochondrial RNA granules. Cell Metab., 17, 399-410.
23. Borowski, L.S., Dziembowski, A., Hejnowicz, M.S., Stepien, P.P. and Szczesny, R.J. (2013) Human mitochondrial RNA decay mediated by PNPase-hSuv3 complex takes place in distinct foci. Nucleic Acids Res., 41, 1223-12240.
24. 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.
25. Brzezniak, L.K., Bijata, M., Szczesny, R.J. and Stepien, P.P. (2011) Involvement of human ELAC2 gene product in 3' end processing of mitochondrial tRNAs. RNA Biol., 8, 616-626.
26. Ojala, D., Montoya, J. and Attardi, G. (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature, 290, 470-474.
27. Shoubridge, E.A., Johns, T. and Boulet, L. (1996) Use of myoblast cultures to study mitochondrial myopathies. Methods Enzymol., 264, 465-475.
28. Lochmuller, H., Johns, T. and Shoubridge, E.A. (1999) Expression of the E6 and E7 genes of human papillomavirus (HPV16) extends the life span of human myoblasts. Exp. Cell Res., 248, 186-193.
29. Boulet, L., Karpati, G. and Shoubridge, E.A. (1992) Distribution and threshold expression of the tRNA(Lys) mutation in skeletal muscle of patients with myoclonic epilepsy and ragged-red fibers (MERRF). Am. J. Hum. Genet., 51, 1187-1200.
30. Sasarman, F. and Shoubridge, E.A. (2012) Radioactive labeling of mitochondrial translation products in cultured cells. Methods Mol. Biol., 837, 207-217.
31. Leary, S.C. and Sasarman, F. (2009) Oxidative phosphorylation: synthesis of mitochondrially encoded proteins and assembly of individual structural subunits into functional holoenzyme complexes. Methods Mol. Biol., 554, 143-162.
32. Antonicka, H., Ogilvie, I., Taivassalo, T., Anitori, R.P., Haller, R.G., Vissing, J., Kennaway, N.G. and Shoubridge, E.A. (2003) Identification and characterization of a common set of complex I assembly intermediates in mitochondria from patients with complex I deficiency. J. Biol. Chem., 278, 43081-43088.
33. Weraarpachai, W., Antonicka, H., Sasarman, F., Seeger, J., Schrank, B., Kolesar, J.E., Lochmuller, H., Chevrette, M., Kaufman, B.A., Horvath, R. et al. (2009) Mutation in TACO1, encoding a translational activator of COX I, results in cytochrome c oxidase deficiency and late-onset Leigh syndrome. Nat. Genet., 41, 833-837.