A founder mutation in PET100 causes isolated complex IV deficiency in lebanese individuals with Leigh syndrome

American Journal of Human Genetics

Volumn 94, Issue 2, 2014, Pages 209-222

  Lim, Sze Chern ^a,b,j   Smith, Katherine R ^b,c   Stroud, David A ^d   Compton, Alison G ^a,b   Tucker, Elena J ^a,b   Dasvarma, Ayan ^a,b   Gandolfo, Luke C ^b,c   Marum, Justine E ^a,j   McKenzie, Matthew ^e   Peters, Heidi L ^a   Mowat, David ^f   Procopis, Peter G ^g,h   Wilcken, Bridget ^h   Christodoulou, John ^g,h   Brown, Garry K ⁱ   Ryan, Michael T ^d   Bahlo, Melanie ^b,c   Thorburn, David R ^a,b  

^a ROYAL CHILDREN'S HOSPITAL   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d LA TROBE UNIVERSITY   (Australia)

^e HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

^g CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^h UNIVERSITY OF SYDNEY   (Australia)

ⁱ UNIVERSITY OF OXFORD   (United Kingdom)

^j CENTRE FOR CANCER BIOLOGY   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOMES, HUMAN, PAIR 19; CYCLOOXYGENASE 2; CYTOCHROME-C OXIDASE DEFICIENCY; DNA, MITOCHONDRIAL; FEMALE; FOUNDER EFFECT; GENETIC COMPLEMENTATION TEST; GENETIC LINKAGE; GENOME-WIDE ASSOCIATION STUDY; HAPLOTYPES; HOMOZYGOTE; HUMANS; INFANT; LEBANON; LEIGH DISEASE; MALE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUTATION; PEDIGREE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEOMICS; SEQUENCE ANALYSIS, DNA;

EID: 84893717400     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2013.12.015     Document Type: Article

References (72)

1. D. Leigh Subacute necrotizing encephalomyelopathy in an infant J. Neurol. Neurosurg. Psychiatry 14 1951 216 221
2. V. Tiranti, K. Hoertnagel, R. Carrozzo, C. Galimberti, M. Munaro, M. Granatiero, L. Zelante, P. Gasparini, R. Marzella, and M. Rocchi et al. Mutations of SURF-1 in Leigh disease associated with cytochrome c oxidase deficiency Am. J. Hum. Genet. 63 1998 1609 1621 (Pubitemid 30415723)
3. Z. Zhu, J. Yao, T. Johns, K. Fu, I. De Bie, C. Macmillan, A.P. Cuthbert, R.F. Newbold, J. Wang, and M. Chevrette et al. SURF1, encoding a factor involved in the biogenesis of cytochrome c oxidase, is mutated in Leigh syndrome Nat. Genet. 20 1998 337 343 (Pubitemid 28541630)
4. H.-H.M. Dahl Getting to the nucleus of mitochondrial disorders: identification of respiratory chain-enzyme genes causing Leigh syndrome Am. J. Hum. Genet. 63 1998 1594 1597 (Pubitemid 30415721)
5. D.M. Kirby, and D.R. Thorburn Approaches to finding the molecular basis of mitochondrial oxidative phosphorylation disorders Twin Res. Hum. Genet. 11 2008 395 411
6. E.J. Tucker, A.G. Compton, and D.R. Thorburn Recent advances in the genetics of mitochondrial encephalopathies Curr. Neurol. Neurosci. Rep. 10 2010 277 285
7. Y.S. Hong, D.S. Kerr, W.J. Craigen, J. Tan, Y. Pan, M. Lusk, and M.S. Patel Identification of two mutations in a compound heterozygous child with dihydrolipoamide dehydrogenase deficiency Hum. Mol. Genet. 5 1996 1925 1930 (Pubitemid 26413636)
8. P.M. Matthews, D.R. Marchington, M. Squier, J. Land, R.M. Brown, and G.K. Brown Molecular genetic characterization of an X-linked form of Leigh's syndrome Ann. Neurol. 33 1993 652 655 (Pubitemid 23161889)
9. K. Muramoto, K. Hirata, K. Shinzawa-Itoh, S. Yoko-o, E. Yamashita, H. Aoyama, T. Tsukihara, and S. Yoshikawa A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase Proc. Natl. Acad. Sci. USA 104 2007 7881 7886 (Pubitemid 47185845)
10. L. Stiburek, H. Hansikova, M. Tesarova, L. Cerna, and J. Zeman Biogenesis of eukaryotic cytochrome c oxidase Physiol. Res. 55 Suppl 2 2006 S27 S41
11. F. Fontanesi, I.C. Soto, D. Horn, and A. Barrientos Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process Am. J. Physiol. Cell Physiol. 291 2006 C1129 C1147
12. J.E. McEwen, C. Ko, B. Kloeckner-Gruissem, and R.O. Poyton Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae. Characterization of mutants in 34 complementation groups J. Biol. Chem. 261 1986 11872 11879 (Pubitemid 17206116)
13. A. Tzagoloff, and C.L. Dieckmann PET genes of Saccharomyces cerevisiae Microbiol. Rev. 54 1990 211 225
14. E. Fernández-Vizarra, V. Tiranti, and M. Zeviani Assembly of the oxidative phosphorylation system in humans: what we have learned by studying its defects Biochim. Biophys. Acta 1793 2009 200 211
15. R.D. Pitceathly, S. Rahman, Y. Wedatilake, J.M. Polke, S. Cirak, A.R. Foley, A. Sailer, M.E. Hurles, J. Stalker, I. Hargreaves UK10K Consortium NDUFA4 mutations underlie dysfunction of a cytochrome c oxidase subunit linked to human neurological disease Cell Rep. 3 2013 1795 1805
16. A. Indrieri, V.A. van Rahden, V. Tiranti, M. Morleo, D. Iaconis, R. Tammaro, I. D'Amato, I. Conte, I. Maystadt, and S. Demuth et al. Mutations in COX7B cause microphthalmia with linear skin lesions, an unconventional mitochondrial disease Am. J. Hum. Genet. 91 2012 942 949
17. M. Huigsloot, L.G. Nijtmans, R. Szklarczyk, M.J. Baars, M.A. van den Brand, M.G. Hendriksfranssen, L.P. van den Heuvel, J.A. Smeitink, M.A. Huynen, and R.J. Rodenburg A mutation in C2orf64 causes impaired cytochrome c oxidase assembly and mitochondrial cardiomyopathy Am. J. Hum. Genet. 88 2011 488 493
18. W. Weraarpachai, F. Sasarman, T. Nishimura, H. Antonicka, K. Auré, A. Rötig, A. Lombès, and E.A. Shoubridge Mutations in C12orf62, a factor that couples COX I synthesis with cytochrome c oxidase assembly, cause fatal neonatal lactic acidosis Am. J. Hum. Genet. 90 2012 142 151
19. E. Balsa, R. Marco, E. Perales-Clemente, R. Szklarczyk, E. Calvo, M.O. Landázuri, and J.A. Enríquez NDUFA4 is a subunit of complex IV of the mammalian electron transport chain Cell Metab. 16 2012 378 386
20. V.K. Mootha, P. Lepage, K. Miller, J. Bunkenborg, M. Reich, M. Hjerrild, T. Delmonte, A. Villeneuve, R. Sladek, and F. Xu et al. Identification of a gene causing human cytochrome c oxidase deficiency by integrative genomics Proc. Natl. Acad. Sci. USA 100 2003 605 610 (Pubitemid 36126099)
21. W. Weraarpachai, H. Antonicka, F. Sasarman, J. Seeger, B. Schrank, J.E. Kolesar, H. Lochmüller, M. Chevrette, B.A. Kaufman, R. Horvath, and E.A. Shoubridge Mutation in TACO1, encoding a translational activator of COX I, results in cytochrome c oxidase deficiency and late-onset Leigh syndrome Nat. Genet. 41 2009 833 837
22. H. Antonicka, S.C. Leary, G.H. Guercin, J.N. Agar, R. Horvath, N.G. Kennaway, C.O. Harding, M. Jaksch, and E.A. Shoubridge Mutations in COX10 result in a defect in mitochondrial heme A biosynthesis and account for multiple, early-onset clinical phenotypes associated with isolated COX deficiency Hum. Mol. Genet. 12 2003 2693 2702 (Pubitemid 37304691)
23. C.E. Oquendo, H. Antonicka, E.A. Shoubridge, W. Reardon, and G.K. Brown Functional and genetic studies demonstrate that mutation in the COX15 gene can cause Leigh syndrome J. Med. Genet. 41 2004 540 544 (Pubitemid 38932115)
24. M. Bugiani, V. Tiranti, L. Farina, G. Uziel, and M. Zeviani Novel mutations in COX15 in a long surviving Leigh syndrome patient with cytochrome c oxidase deficiency J. Med. Genet. 42 2005 e28
25. Y. Wedatilake, R. Brown, R. McFarland, J. Yaplito-Lee, A.A. Morris, M. Champion, P.E. Jardine, A. Clarke, D.R. Thorburn, and R.W. Taylor et al. SURF1 deficiency: a multi-centre natural history study Orphanet J. Rare Dis. 8 2013 96
26. V. Tiranti, M. Jaksch, S. Hofmann, C. Galimberti, K. Hoertnagel, L. Lulli, P. Freisinger, L. Bindoff, K.D. Gerbitz, and G.P. Comi et al. Loss-of-function mutations of SURF-1 are specifically associated with Leigh syndrome with cytochrome c oxidase deficiency Ann. Neurol. 46 1999 161 166 (Pubitemid 29382871)
27. F.A. Bundschuh, A. Hannappel, O. Anderka, and B. Ludwig Surf1, associated with Leigh syndrome in humans, is a heme-binding protein in bacterial oxidase biogenesis J. Biol. Chem. 284 2009 25735 25741
28. D. Smith, J. Gray, L. Mitchell, W.E. Antholine, and J.P. Hosler Assembly of cytochrome-c oxidase in the absence of assembly protein Surf1p leads to loss of the active site heme J. Biol. Chem. 280 2005 17652 17656 (Pubitemid 41389000)
29. S.C. Leary, F. Sasarman, T. Nishimura, and E.A. Shoubridge Human SCO2 is required for the synthesis of CO II and as a thiol-disulphide oxidoreductase for SCO1 Hum. Mol. Genet. 18 2009 2230 2240
30. B. Ruzzenente, M.D. Metodiev, A. Wredenberg, A. Bratic, C.B. Park, Y. Cámara, D. Milenkovic, V. Zickermann, R. Wibom, and K. Hultenby et al. LRPPRC is necessary for polyadenylation and coordination of translation of mitochondrial mRNAs EMBO J. 31 2012 443 456
31. F. Sasarman, C. Brunel-Guitton, H. Antonicka, T. Wai, E.A. Shoubridge LSFC Consortium LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria Mol. Biol. Cell 21 2010 1315 1323
32. V. Tiranti, C. Viscomi, T. Hildebrandt, I. Di Meo, R. Mineri, C. Tiveron, M.D. Levitt, A. Prelle, G. Fagiolari, M. Rimoldi, and M. Zeviani Loss of ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy Nat. Med. 15 2009 200 205
33. D. Ghezzi, A. Saada, P. D'Adamo, E. Fernandez-Vizarra, P. Gasparini, V. Tiranti, O. Elpeleg, and M. Zeviani FASTKD2 nonsense mutation in an infantile mitochondrial encephalomyopathy associated with cytochrome c oxidase deficiency Am. J. Hum. Genet. 83 2008 415 423
34. D.M. Kirby, M. Crawford, M.A. Cleary, H.H. Dahl, X. Dennett, and D.R. Thorburn Respiratory chain complex I deficiency: an underdiagnosed energy generation disorder Neurology 52 1999 1255 1264 (Pubitemid 29177931)
35. M. Bahlo, and C.J. Bromhead Generating linkage mapping files from Affymetrix SNP chip data Bioinformatics 25 2009 1961 1962
36. A.L. Leutenegger, A. Labalme, E. Genin, A. Toutain, E. Steichen, F. Clerget-Darpoux, and P. Edery Using genomic inbreeding coefficient estimates for homozygosity mapping of rare recessive traits: application to Taybi-Linder syndrome Am. J. Hum. Genet. 79 2006 62 66 (Pubitemid 43927377)
37. A.L. Leutenegger, B. Prum, E. Génin, C. Verny, A. Lemainque, F. Clerget-Darpoux, and E.A. Thompson Estimation of the inbreeding coefficient through use of genomic data Am. J. Hum. Genet. 73 2003 516 523 (Pubitemid 37076266)
38. G.R. Abecasis, S.S. Cherny, W.O. Cookson, and L.R. Cardon Merlin - rapid analysis of dense genetic maps using sparse gene flow trees Nat. Genet. 30 2002 97 101
39. H. Thiele, and P. Nürnberg HaploPainter: a tool for drawing pedigrees with complex haplotypes Bioinformatics 21 2005 1730 1732 (Pubitemid 40542746)
40. F.-O. Desmet, D. Hamroun, M. Lalande, G. Collod-Béroud, M. Claustres, and C. Béroud Human Splicing Finder: an online bioinformatics tool to predict splicing signals Nucleic Acids Res. 37 2009 e67
41. M.G. Reese, F.H. Eeckman, D. Kulp, and D. Haussler Improved splice site detection in Genie J. Comput. Biol. 4 1997 311 323 (Pubitemid 27355870)
42. S.E. Calvo, A.G. Compton, S.G. Hershman, S.C. Lim, D.S. Lieber, E.J. Tucker, A. Laskowski, C. Garone, S. Liu, and D.B. Jaffe et al. Molecular diagnosis of infantile mitochondrial disease with targeted next-generation sequencing Sci. Transl. Med. 4 2012 18ra10
43. M.A. DePristo, E. Banks, R. Poplin, K.V. Garimella, J.R. Maguire, C. Hartl, A.A. Philippakis, G. del Angel, M.A. Rivas, and M. Hanna et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data Nat. Genet. 43 2011 491 498
44. A. McKenna, M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis, A. Kernytsky, K. Garimella, D. Altshuler, S. Gabriel, M. Daly, and M.A. DePristo The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data Genome Res. 20 2010 1297 1303
45. H. Li, B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, R. Durbin 1000 Genome Project Data Processing Subgroup The Sequence Alignment/Map format and SAMtools Bioinformatics 25 2009 2078 2079
46. H. Li, J. Ruan, and R. Durbin Mapping short DNA sequencing reads and calling variants using mapping quality scores Genome Res. 18 2008 1851 1858
47. P.A. Fujita, B. Rhead, A.S. Zweig, A.S. Hinrichs, D. Karolchik, M.S. Cline, M. Goldman, G.P. Barber, H. Clawson, and A. Coelho et al. The UCSC Genome Browser database: update 2011 Nucleic Acids Res. 39 Database issue 2011 D876 D882
48. S.T. Sherry, M.H. Ward, M. Kholodov, J. Baker, L. Phan, E.M. Smigielski, and K. Sirotkin dbSNP: the NCBI database of genetic variation Nucleic Acids Res. 29 2001 308 311 (Pubitemid 32054478)
49. The 1000 Genomes Project Consortium A map of human genome variation from population-scale sequencing Nature 467 2010 1061 1073
50. K. Wang, M. Li, and H. Hakonarson ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data Nucleic Acids Res. 38 2010 e164
51. R. Colombo Dating mutations D.N. Cooper, H. Kehrer-Sawatzki, Handbook of Human Molecular Evolution 2008 John Wiley & Sons, Ltd Chichester 138
52. M. Slatkin, and B. Rannala Estimating allele age Annu. Rev. Genomics Hum. Genet. 1 2000 225 249
53. M.A. Corbett, M. Schwake, M. Bahlo, L.M. Dibbens, M. Lin, L.C. Gandolfo, D.F. Vears, J.D. O'Sullivan, T. Robertson, and M.A. Bayly et al. A mutation in the Golgi Qb-SNARE gene GOSR2 causes progressive myoclonus epilepsy with early ataxia Am. J. Hum. Genet. 88 2011 657 663
54. L. Boissé Lomax, M.A. Bayly, H. Hjalgrim, R.S. Møller, A.M. Vlaar, K.M. Aaberg, I. Marquardt, L.C. Gandolfo, M. Willemsen, and E.-J. Kamsteeg et al. 'North Sea' progressive myoclonus epilepsy: phenotype of subjects with GOSR2 mutation Brain 136 2013 1146 1154
55. M.S. McPeek, and A. Strahs Assessment of linkage disequilibrium by the decay of haplotype sharing, with application to fine-scale genetic mapping Am. J. Hum. Genet. 65 1999 858 875 (Pubitemid 30468730)
56. Y.Y. Yeap, I.H. Ng, B. Badrian, T.V. Nguyen, Y.Y. Yip, A.S. Dhillon, S.E. Mutsaers, J. Silke, M.A. Bogoyevitch, and D.C. Ng c-Jun N-terminal kinase/c-Jun inhibits fibroblast proliferation by negatively regulating the levels of stathmin/oncoprotein 18 Biochem. J. 430 2010 345 354
57. S.E. Calvo, E.J. Tucker, A.G. Compton, D.M. Kirby, G. Crawford, N.P. Burtt, M. Rivas, C. Guiducci, D.L. Bruno, and O.A. Goldberger et al. High-throughput, pooled sequencing identifies mutations in NUBPL and FOXRED1 in human complex I deficiency Nat. Genet. 42 2010 851 858
58. A.J. Johnston, J. Hoogenraad, D.A. Dougan, K.N. Truscott, M. Yano, M. Mori, N.J. Hoogenraad, and M.T. Ryan Insertion and assembly of human tom7 into the preprotein translocase complex of the outer mitochondrial membrane J. Biol. Chem. 277 2002 42197 42204 (Pubitemid 35257538)
59. D. Stojanovski, N. Pfanner, and N. Wiedemann Import of proteins into mitochondria Methods Cell Biol. 80 2007 783 806
60. M. McKenzie, M. Lazarou, D.R. Thorburn, and M.T. Ryan Analysis of mitochondrial subunit assembly into respiratory chain complexes using Blue Native polyacrylamide gel electrophoresis Anal. Biochem. 364 2007 128 137 (Pubitemid 46559922)
61. M. McKenzie, M. Lazarou, and M.T. Ryan Chapter 18 Analysis of respiratory chain complex assembly with radiolabeled nuclear- and mitochondrial-encoded subunits Methods Enzymol. 456 2009 321 339
62. B.H. Robinson, R. Petrova-Benedict, J.R. Buncic, and D.C. Wallace Nonviability of cells with oxidative defects in galactose medium: a screening test for affected patient fibroblasts Biochem. Med. Metab. Biol. 48 1992 122 126
63. M.G. Claros, and P. Vincens Computational method to predict mitochondrially imported proteins and their targeting sequences Eur. J. Biochem. 241 1996 779 786 (Pubitemid 26379380)
64. C. Guda, P. Guda, E. Fahy, and S. Subramaniam MITOPRED: a web server for the prediction of mitochondrial proteins Nucleic Acids Res. 32 Web Server issue 2004 W372 W374
65. D.J. Pagliarini, S.E. Calvo, B. Chang, S.A. Sheth, S.B. Vafai, S.-E. Ong, G.A. Walford, C. Sugiana, A. Boneh, and W.K. Chen et al. A mitochondrial protein compendium elucidates complex I disease biology Cell 134 2008 112 123 (Pubitemid 351916708)
66. R. Szklarczyk, B.F. Wanschers, T.D. Cuypers, J.J. Esseling, M. Riemersma, M.A. van den Brand, J. Gloerich, E. Lasonder, L.P. van den Heuvel, L.G. Nijtmans, and M.A. Huynen Iterative orthology prediction uncovers new mitochondrial proteins and identifies C12orf62 as the human ortholog of COX14, a protein involved in the assembly of cytochrome c oxidase Genome Biol. 13 2012 R12
67. C. Church, B. Goehring, D. Forsha, P. Wazny, and R.O. Poyton A role for Pet100p in the assembly of yeast cytochrome c oxidase: interaction with a subassembly that accumulates in a pet100 mutant J. Biol. Chem. 280 2005 1854 1863
68. A. Chacinska, C.M. Koehler, D. Milenkovic, T. Lithgow, and N. Pfanner Importing mitochondrial proteins: machineries and mechanisms Cell 138 2009 628 644
69. D.U. Mick, T.D. Fox, and P. Rehling Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation Nat. Rev. Mol. Cell Biol. 12 2011 14 20
70. C. Church, C. Chapon, and R.O. Poyton Cloning and characterization of PET100, a gene required for the assembly of yeast cytochrome c oxidase J. Biol. Chem. 271 1996 18499 18507 (Pubitemid 26322708)
71. F.-G. Debray, C. Morin, A. Janvier, J. Villeneuve, B. Maranda, R. Laframboise, J. Lacroix, J.-C. Decarie, Y. Robitaille, and M. Lambert et al. LRPPRC mutations cause a phenotypically distinct form of Leigh syndrome with cytochrome c oxidase deficiency J. Med. Genet. 48 2011 183 189
72. C. Morin, G. Mitchell, J. Larochelle, M. Lambert, H. Ogier, B.H. Robinson, and M. De Braekeleer Clinical, metabolic, and genetic aspects of cytochrome C oxidase deficiency in Saguenay-Lac-Saint-Jean Am. J. Hum. Genet. 53 1993 488 496 (Pubitemid 23308943)