Loss of LRPPRC causes ATP synthase deficiency

Human Molecular Genetics

Volumn 23, Issue 10, 2014, Pages 2580-2592

  Mourier, Arnaud ^a   Ruzzenente, Benedetta ^a   Brandt, Tobias ^b   Kühlbrandt, Werner ^b   Larsson, Nils Göran ^a  

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

^b MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CREATINE KINASE MM; LEUCINE RICH PENTATRICOPEPTIDE REPEAT CONTAINING PROTEIN; MESSENGER RNA; PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; CYTOCHROME C OXIDASE; LRPPRC PROTEIN, MOUSE; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOENERGY; CONTROLLED STUDY; CYTOCHROME C OXIDASE DEFICIENCY; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME SYNTHESIS; GENE LOSS; HEART MITOCHONDRION; HYPERPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOUSE; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NONHUMAN; OLIGOMERIZATION; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN QUATERNARY STRUCTURE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE DEFICIENCY; RNA STABILITY; STEADY STATE; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DEFICIENCY; ENERGY METABOLISM; ENZYMOLOGY; GENETICS; HUMAN; LEIGH DISEASE; METABOLISM; PATHOLOGY; PROTEIN MULTIMERIZATION; TRANSGENIC MOUSE;

ADENOSINE TRIPHOSPHATE; ANIMALS; ELECTRON TRANSPORT COMPLEX IV; ENERGY METABOLISM; HUMANS; LEIGH DISEASE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA, HEART; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; NEOPLASM PROTEINS; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PROTEIN MULTIMERIZATION; REACTIVE OXYGEN SPECIES;

EID: 84898772400     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt652     Document Type: Article

References (70)

1. Leigh, D. (1951) Subacute necrotizing encephalomyelopathy in an infant. J. Neurol. Neurosurg. Psychiatr., 14, 216-221.
2. 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.
3. López, L.C., Schuelke, M., Quinzii, C.M., Kanki, T., Rodenburg, R.J.T., Naini, A., Dimauro, S. and Hirano, M. (2006) Leigh syndrome with nephropathy and CoQ10 deficiency due to decaprenyl diphosphate synthase subunit 2 (PDSS2) mutations. Am. J. Hum. Genet., 79, 1125-1129.
4. Taylor, R.W., Morris, A.A.M., Hutchinson, M. and Turnbull, D.M. (2002) Leigh disease associated with a novel mitochondrial DNA ND5 mutation. Eur. J. Hum. Genet., 10, 141-144.
5. Horváth, R., Abicht, A., Holinski-Feder, E., Laner, A., Gempel, K., Prokisch, H., Lochmüller, H., Klopstock, T. and Jaksch, M. (2006) Leigh syndrome caused by mutations in the flavoprotein (Fp) subunit of succinate dehydrogenase (SDHA). J. Neurol. Neurosurg. Psychiatr., 77, 74-76.
6. Willems, J.L., Monnens, L.A., Trijbels, J.M., Veerkamp, J.H., Meyer, A.E., van Dam, K. and van Haelst, U. (1977) Leigh's encephalomyelopathy in a patient with cytochrome c oxidase deficiency in muscle tissue. Pediatrics, 60, 850-857.
7. Uziel, G., Moroni, I., Lamantea, E., Fratta, G.M., Ciceri, E., Carrara, F. and Zeviani, M. (1997) Mitochondrial disease associated with the T8993G mutation of the mitochondrial ATPase 6 gene: a clinical, biochemical, and molecular study in six families. J. Neurol. Neurosurg. Psychiatr., 63, 16-22.
8. Tiranti, V., Hoertnagel, K., Carrozzo, R., Galimberti, C., Munaro, M., Granatiero, M., Zelante, L., Gasparini, P., Marzella, R., Rocchi, M. et al. (1998) Mutations of SURF-1 in Leigh disease associated with cytochrome c oxidase deficiency. Am. J. Hum. Genet., 63, 1609-1621.
9. 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.
10. Valnot, I., Osmond, S., Gigarel, N., Mehaye, B., Amiel, J., Cormier-Daire, V., Munnich, A., Bonnefont, J.P., Rustin, P. and Rötig, A. (2000) Mutations of the SCO1 gene in mitochondrial cytochrome c oxidase deficiency with neonatal-onset hepatic failure and encephalopathy. Am. J. Hum. Genet., 67, 1104-1109.
11. Papadopoulou, L.C., Sue, C.M., Davidson, M.M., Tanji, K., Nishino, I., Sadlock, J.E., Krishna, S., Walker, W., Selby, J., Glerum, D.M. et al. (1999) Fatal infantile cardioencephalomyopathy with COX deficiency and mutations in SCO2, a COX assembly gene. Nat. Genet., 23, 333-337.
12. Valnot, I., von Kleist-Retzow, J.C., Barrientos, A., Gorbatyuk, M., Taanman, J.W., Mehaye, B., Rustin, P., Tzagoloff, A., Munnich, A. and Rötig, A. (2000) A mutation in the human heme A: farnesyltransferase gene (COX10) causes cytochrome c oxidase deficiency. Hum. Mol. Genet., 9, 1245-1249.
13. Oquendo, C.E., Antonicka, H., Shoubridge, E.A., Reardon, W. and Brown, G.K. (2004) Functional and genetic studies demonstrate that mutation in the COX15 gene can cause Leigh syndrome. J. Med. Genet., 41, 540-544.
14. Agostino, A., Invernizzi, F., Tiveron, C., Fagiolari, G., Prelle, A., Lamantea, E., Giavazzi, A., Battaglia, G., Tatangelo, L., Tiranti, V. et al. (2003) Constitutive knockout of Surf1 is associated with high embryonic lethality, mitochondrial disease and cytochrome c oxidase deficiency in mice. Hum. Mol. Genet., 12, 399-413.
15. Dell'agnello, C., Leo, S., Agostino, A., Szabadkai, G., Tiveron, C., Zulian, A., Prelle, A., Roubertoux, P., Rizzuto, R. and Zeviani, M. (2007) Increased longevity and refractoriness to Ca(2+)-dependent neurodegeneration in Surf1 knockout mice. Hum. Mol. Genet., 16, 431-444.
16. Yang, H., Brosel, S., Acin-Perez, R., Slavkovich, V., Nishino, I., Khan, R., Goldberg, I.J., Graziano, J., Manfredi, G. and Schon, E.A. (2010) Analysis of mouse models of cytochrome c oxidase deficiency owing to mutations in Sco2. Hum. Mol. Genet., 19, 170-180.
17. Radford, N.B., Wan, B., Richman, A., Szczepaniak, L.S., Li, J.-L., Li, K., Pfeiffer, K., Schägger, H., Garry, D.J. and Moreadith, R.W. (2002) Cardiac dysfunction in mice lacking cytochrome-c oxidase subunit VIaH. Am. J. Physiol. Heart. Circ. Physiol., 282, H726-H733.
18. Hüttemann, M., Klewer, S., Lee, I., Pecinova, A., Pecina, P., Liu, J., Lee, M., Doan, J.W., Larson, D., Slack, E. et al. (2012) Mice deleted for heart-type cytochrome c oxidase subunit 7a1 develop dilated cardiomyopathy. Mitochondrion, 12, 294-304.
19. 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.
20. Ruzzenente, B., Metodiev, M.D., Wredenberg, A., Bratic, A., Park, C.B., Cámara, 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.
21. Finsterer, J. (2008) Leigh and Leigh-like syndrome in children and adults. Pediatr. Neurol., 39, 223-235.
22. 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.
23. Xu, F., Addis, J.B.L., Cameron, J.M. and Robinson, B.H. (2012) LRPPRC mutation suppresses cytochrome oxidase activity by altering mitochondrial RNA transcript stability in a mouse model. Biochem. J., 441, 275-283.
24. 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.
25. Sasarman, F., Brunel-Guitton, C., Antonicka, H., Wai, T. and Shoubridge, E.A.; LSFC Consortium (2010) LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Mol. Biol. Cell, 21, 1315-1323.
26. Bratic, A., Wredenberg, A., Grönke, 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 mitochondrialmRNAsin Drosophila melanogaster. PLoS Genet., 7, e1002324.
27. Mourier, A., Devin, A. and Rigoulet, M. (2010) Active proton leak in mitochondria: a new way to regulate substrate oxidation. Biochim. Biophys. Acta., 1797, 255-261.
28. Tzagoloff, A., Byington, K.H. and MacLennan, D.H. (1968) Studies on the mitochondrial adenosine triphosphatase system. II. The isolation and characterization of an oligomycin-sensitive adenosine triphosphatase from bovine heart mitochondria. J. Biol. Chem., 243, 2405-2412.
29. Wittig, I. and Schägger, H. (2005) Advantages and limitations of clear-native PAGE. Proteomics, 5, 4338-4346.
30. Grandier-Vazeille, X. and Guérin, M. (1996) Separation by blue native and colorless native polyacrylamide gel electrophoresis of the oxidative phosphorylation complexes of yeast mitochondria solubilized by different detergents: specific staining of the different complexes. Anal. Biochem., 242, 248-254.
31. Allen, R.D., Schroeder, C.C. and Fok, A.K. (1989) An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. J. Cell. Biol., 108, 2233-2240.
32. Davies, K.M., Strauss, M., Daum, B., Kief, J.H., Osiewacz, H.D., Rycovska, A., Zickermann, V. and Kühlbrandt, W. (2011) Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc. Natl Acad. Sci. USA, 108, 14121-14126.
33. Strauss, M., Hofhaus, G., Schröder, R.R. and Kühlbrandt, W. (2008) Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J., 27, 1154-1160.
34. Habersetzer, J., Ziani, W., Larrieu, I., Stines-Chaumeil, C., Giraud, M.-F., Brèthes, D., Dautant, A. and Paumard, P. (2013) ATP synthase oligomerization: from the enzyme models to the mitochondrial morphology. Int. J. Biochem. Cell Biol., 45, 99-105.
35. Davies, K.M., Anselmi, C., Wittig, I., Faraldo-Gómez, J.D. and Kühlbrandt, W. (2012) Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl Acad. Sci. USA, 109, 13602-13607.
36. Paumard, P., Vaillier, J., Coulary, B., Schaeffer, J., Soubannier, V., Mueller, D.M., Brèthes, D., di Rago, J.-P. and Velours, J. (2002) The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J., 21, 221-230.
37. Goyon, V., Fronzes, R., Salin, B., di Rago, J.-P., Velours, J. and Brèthes, D. (2008) Yeast cells depleted in Atp14p fail to assemble Atp6p within theATP synthase and exhibit altered mitochondrial cristae morphology. J. Biol. Chem., 283, 9749-9758.
38. Jesina, P., Tesarová, M., Fornůsková, D., Vojtísková, A., Pecina, P., Kaplanová, V., Hansíková, H., Zeman, J. and Houstek, J. (2004) Diminished synthesis of subunit a (ATP6) and altered function of ATP synthase and cytochrome c oxidase due to the mtDNA 2 bp microdeletion of TA at positions 9205 and 9206. Biochem. J., 383, 561-571.
39. Mayr, J.A., Havlícková, V., Zimmermann, F., Magler, I., Kaplanová, V., Jesina, P., Pecinova, A., Nůsková, H., Koch, J., Sperl, W. et al. (2010) MitochondrialATPsynthase deficiency due to a mutation in theATP5Egene for the F1 epsilon subunit. Hum. Mol. Genet., 19, 3430-3439.
40. Pullman, M.E. and Monroy, G.C. (1963) A naturally occuring inhibitor of mitochondrial adenosine triphosphatase. J. Biol. Chem., 238, 3762-3769.
41. Venard, R., Brèthes, D., Giraud, M.-F., Vaillier, J., Velours, J. and Haraux, F. (2003) Investigation of the role and mechanism of IF1 and STF1 proteins, twin inhibitory peptides which interact with the yeast mitochondrial ATP synthase. Biochemistry, 42, 7626-7636.
42. Rigoulet, M., Mourier, A., Galinier, A., Casteilla, L. and Devin, A. (2010) Electron competition process in respiratory chain: regulatory mechanisms and physiological functions. Biochim. Biophys. Acta., 1797, 671-677.
43. Mrácek, T., Pecina, P., Vojtísková, A., Kalous, M., Sebesta, O. and Houstek, J. (2006) Two components in pathogenic mechanism of mitochondrial ATPase deficiency: energy deprivation andROSproduction. Exp. Gerontol., 41, 683-687.
44. Mattiazzi, M., Vijayvergiya, C., Gajewski, C.D., DeVivo, D.C., Lenaz, G., Wiedmann, M. and Manfredi, G. (2004) The mtDNA T8993G (NARP) mutation results in an impairment of oxidative phosphorylation that can be improved by antioxidants. Hum. Mol. Genet., 13, 869-879.
45. Houstek, J., Pícková, A., Vojtísková, A., Mrácek, T., Pecina, P. and Jesina, P. (2006) Mitochondrial diseases and genetic defects of ATP synthase. Biochim. Biophys. Acta., 1757, 1400-1405.
46. Villani, G., Greco, M., Papa, S. and Attardi, G. (1998) Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J. Biol. Chem., 273, 31829-31836.
47. Kunz, W.S., Kudin, A., Vielhaber, S., Elger, C.E., Attardi, G. and Villani, G. (2000) Flux control of cytochrome c oxidase in human skeletal muscle. J. Biol. Chem., 275, 27741-27745.
48. Rossignol, R., Malgat, M., Mazat, J.P. and Letellier, T. (1999) Threshold effect and tissue specificity. Implication for mitochondrial cytopathies. J. Biol. Chem., 274, 33426-33432.
49. Rees, D.M., Leslie, A.G.W. and Walker, J.E. (2009) The structure of the membrane extrinsic region of bovine ATP synthase. Proc. Natl Acad. Sci. USA, 106, 21597-21601.
50. Symersky, J., Osowski, D., Walters, D.E. and Mueller, D.M. (2012) Oligomycin frames a common drug-binding site in the ATP synthase. Proc. Natl Acad. Sci. USA, 109, 13961-13965.
51. Macino, G. and Tzagoloff, A. (1980) Assembly of the mitochondrial membrane system: sequence analysis of a yeast mitochondrial ATPase gene containing the oli-2 and oli-4 loci. Cell, 20, 507-517.
52. Ooi, B.G., Novitski, C.E. and Nagley, P. (1985) DNA sequence analysis of the oli1 gene reveals amino acid changes in mitochondrial ATPase subunit 9 from oligomycin-resistant mutants of Saccharomyces cerevisiae. Eur. J. Biochem., 152, 709-714.
53. John, U.P. and Nagley, P. (1986) Amino acid substitutions in mitochondrial ATPase subunit 6 of Saccharomyces cerevisiae leading to oligomycin resistance. FEBS Lett., 207, 79-83.
54. Campanella, M., Casswell, E., Chong, S., Farah, Z., Wieckowski, M.R., Abramov, A.Y., Tinker, A. and Duchen, M.R. (2008) Regulation of mitochondrial structure and function by the F1Fo-ATPase inhibitor protein, IF1. Cell Metab., 8, 13-25.
55. Nijtmans, L.G., Henderson, N.S., Attardi, G. and Holt, I.J. (2001) Impaired ATP synthase assembly associated with a mutation in the human ATP synthase subunit 6 gene. J. Biol. Chem., 276, 6755-6762.
56. Houstek, J., Klement, P., Hermanská, J., Houstková, H., Hansíková, H., Van den Bogert, C. and Zeman, J. (1995) Altered properties of mitochondrial ATP-synthase in patients with a T→.Gmutation in the ATPase 6 (subunit a) gene at position 8993 of mtDNA. Biochim. Biophys. Acta., 1271, 349-357.
57. Jonckheere, A.I., Hogeveen, M., Nijtmans, L.G.J., van den Brand, M.A.M., Janssen, A.J.M., Diepstra, J.H.S., van den Brandt, F.C.A., van den Heuvel, L.P., Hol, F.A., Hofste, T.G.J. et al. (2008) A novel mitochondrial ATP8 gene mutation in a patient with apical hypertrophic cardiomyopathy and neuropathy. J. Med. Genet., 45, 129-133.
58. Wittig, I., Meyer, B., Heide, H., Steger, M., Bleier, L., Wumaier, Z., Karas, M. and Schägger, H. (2010) Assembly and oligomerization of human ATP synthase lacking mitochondrial subunits a and A6L. Biochim. Biophys. Acta., 1797, 1004-1011.
59. Milenkovic, D., Matic, S., Kühl, I., Ruzzenente, B., Freyer, C., Jemt, E., Park, C.B., Falkenberg, M. and Larsson, N.-G. (2013) TWINKLE is an essential mitochondrial helicase required for synthesis of nascent D-loop strands and complete mtDNA replication. Hum. Mol. Genet., 22, 1983-1993.
60. 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.
61. Cámara, Y., Asin-Cayuela, J., Park, C.B., Metodiev, M.D., Shi, Y., Ruzzenente, B., Kukat, C., Habermann, B., Wibom, R., Hultenby, K. et al. (2011) MTERF4 regulates translation by targeting the methyltransferase NSUN4 to the mammalian mitochondrial ribosome. Cell Metab., 13, 527-539.
62. Park, C.B., Asin-Cayuela, J., Cámara, Y., Shi, Y., Pellegrini, M., Gaspari, M., Wibom, R., Hultenby, K., Erdjument-Bromage, H., Tempst, P. et al. (2007) MTERF3 is a negative regulator of mammalian mtDNA transcription. Cell, 130, 273-285.
63. Merante, F., Petrova-Benedict, R., MacKay, N., Mitchell, G., Lambert, M., Morin, C., De Braekeleer, M., Laframboise, R., Gagné, 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.
64. Freyer, C., Cree, L.M., Mourier, A., Stewart, J.B., Koolmeister, C., Milenkovic, D., Wai, T., Floros, V.I., Hagström, E., Chatzidaki, E.E. et al. (2012) Variation in germline mtDNA heteroplasmy is determined prenatally but modified during subsequent transmission. Nat. Genet., 44, 1282-1285.
65. Somlo, M. (1968) Induction and repression of mitochondrial ATPase in yeast. Eur. J. Biochem., 5, 276-284.
66. Habersetzer, J., Larrieu, I., Priault, M., Salin, B., Rossignol, R., Brèthes, D. and Paumard, P. (2013) Human F1F0 ATP synthase, mitochondrial ultrastructure and OXPHOS impairment: A (Super-)complex matter? PLoS One, 8, e75429.
67. Larsson, N.G., Wang, J., Wilhelmsson, H., Oldfors, A., Rustin, P., Lewandoski, M., Barsh, G.S. and Clayton, D.A. (1998) Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet., 18, 231-236.
68. Franz, T. and Li, X. (2012) The OASIS® HLB μElution plate as a one-step platform for manual high-throughput in-gel digestion of proteins and peptide desalting. Proteomics, 12, 2487-2492.
69. Kremer, J.R., Mastronarde, D.N. and McIntosh, J.R. (1996) Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol., 116, 71-76.
70. Frangakis, A.S. and Hegerl, R. (2001) Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J. Struct. Biol., 135, 239-250.