Deep sequencing unearths Nuclear mitochondrial sequences under Leber's hereditary optic neuropathy-associated false heteroplasmic mitochondrial DNA variants

Human Molecular Genetics

Volumn 21, Issue 17, 2012, Pages 3753-3764

  Petruzzella, Vittoria ^a   Carrozzo, Rosalba ^b   Calabrese, Claudia ^c   Dell'aglio, Rosa ^a   Trentadue, Raffaella ^a   Piredda, Roberta ^a   Artuso, Lucia ^a   Rizza, Teresa ^b   Bianchi, Marzia ^b   Porcelli, Anna Maria ^c   Guerriero, Silvana ^a   Gasparre, Giuseppe ^c   Attimonelli, Marcella ^a  

^a UNIVERSITY OF BARI   (Italy)

^b BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; MITOCHONDRIAL DNA; MITOCHONDRIAL DNA 5; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BLOOD SAMPLING; CASE REPORT; CONTROLLED STUDY; DNA SEQUENCE; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; FOLLOW UP; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HAPLOTYPE; HEREDITY; HETEROPLASMY; HUMAN; HUMAN CELL; LEBER HEREDITARY OPTIC NEUROPATHY; MALE; MITOCHONDRIAL GENOME; OPTICAL COHERENCE TOMOGRAPHY; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PYROSEQUENCING; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; UREA NITROGEN BLOOD LEVEL;

ADENOSINE TRIPHOSPHATE; ADOLESCENT; ADULT; CELL NUCLEUS; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX I; ENERGY METABOLISM; FEMALE; FIBROBLASTS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUTATION; OPTIC ATROPHY, HEREDITARY, LEBER; PEDIGREE; TEMPERATURE; YOUNG ADULT;

EID: 84865098230     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds182     Document Type: Article

References (47)

1. Yen, M.Y., Wang, A.G. and Wei, Y.H. (2006) Leber's hereditary optic neuropathy: a multifactorial disease. Prog. Retin. Eye Res., 25, 381-396.
2. Carelli, V., Ross-Cisneros, F.N. and Sadun, A.A. (2004) Mitochondrial dysfunction as a cause of optic neuropathies. Prog. Retin. Eye Res., 23, 53-89.
3. Carelli, V., Giordano, C. and d'Amati, G. (2003) Pathogenic expression of homoplasmic mtDNA mutations needs a complex nuclear-mitochondrial interaction. Trends Genet., 19, 257-262.
4. Hudson, G., Carelli, V., Spruijt, L., Gerards, M., Mowbray, C., Achilli, A., Pyle, A., Elson, J., Howell, N., La Morgia, C. et al. (2007) Clinical expression of Leber hereditary optic neuropathy is affected by the mitochondrial DNA-haplogroup background. Am. J. Hum. Genet., 81, 228-233.
5. Man, P.Y., Turnbull, D.M. and Chinnery, P.F. (2002) Leber hereditary optic neuropathy. J. Med. Genet., 39, 162-169.
6. Zoccolella, S., Petruzzella, V., Prascina, F., Artuso, L., Pacillo, F., Dell'Aglio, R., Avolio, C., Delle Noci, N., Attimonelli, M. and Specchio, L.M. (2010) Late-onset Leber hereditary optic neuropathy mimicking Susac's syndrome. J. Neurol., 257, 1999-2003.
7. Ghelli, A., Porcelli, A.M., Zanna, C., Vidoni, S., Mattioli, S., Barbieri, A., Iommarini, L., Pala, M., Achilli, A., Torroni, A. et al. (2009) The background of mitochondrial DNA haplogroup J increases the sensitivity of Leber's hereditary optic neuropathy cells to 2,5-hexanedione toxicity. PLoS ONE, 4, e7922.
8. Torroni, A., Petrozzi, M., D'Urbano, L., Sellitto, D., Zeviani, M., Carrara, F., Carducci, C., Leuzzi, V., Carelli, V., Barboni, P. et al. (1997) Haplotype and phylogenetic analyses suggest that one European-specific mtDNA background plays a role in the expression of Leber hereditary optic neuropathy by increasing the penetrance of the primary mutations 11778 and 14484. Am. J. Hum. Genet., 60, 1107-1121.
9. Hudson, G., Keers, S., Yu Wai Man, P., Griffiths, P., Huoponen, K., Savontaus, M.L., Nikoskelainen, E., Zeviani, M., Carrara, F., Horvath, R. et al. (2005) Identification of an X-chromosomal locus and haplotype modulating the phenotype of a mitochondrial DNA disorder. Am. J. Hum. Genet., 77, 1086-1091.
10. Howell, N., Miller, N.R., Mackey, D.A., Arnold, A., Herrnstadt, C., Williams, I.M. and Kubacka, I. (2002) Lightning strikes twice: Leber hereditary optic neuropathy families with two pathogenic mtDNA mutations. J. Neuroophthalmol., 22, 262-269.
11. Yu-Wai-Man, P., Griffiths, P.G., Hudson, G. and Chinnery, P.F. (2009) Inherited mitochondrial optic neuropathies. J. Med. Genet., 46, 145-158.
12. McFarland, R., Chinnery, P.F., Blakely, E.L., Schaefer, A.M., Morris, A.A., Foster, S.M., Tuppen, H.A., Ramesh, V., Dorman, P.J., Turnbull, D.M. et al. (2007) Homoplasmy, heteroplasmy, and mitochondrial dystonia. Neurology, 69, 911-916.
13. Smith, K.H., Johns, D.R., Heher, K.L. and Miller, N.R. (1993) Heteroplasmy in Leber's hereditary optic neuropathy. Arch. Ophthalmol., 111, 1486-1490.
14. Huoponen, K. (2001) Leber hereditary optic neuropathy: clinical and molecular genetic findings. Neurogenetics, 3, 119-125.
15. Bolhuis, P.A., Bleeker-Wagemakers, E.M., Ponne, N.J., Van Schooneveld, M.J., Westerveld, A., Van den Bogert, C. and Tabak, H.F. (1990) Rapid shift in genotype of human mitochondrial DNA in a family with Leber's hereditary optic neuropathy. Biochem. Biophys. Res. Commun., 170, 994-997.
16. Howell, N., Xu, M., Halvorson, S., Bodis-Wollner, I. and Sherman, J. (1994) A heteroplasmic LHON family: tissue distribution and transmission of the 11778 mutation. Am. J. Hum. Genet., 55, 203-206.
17. Lightowlers, R.N., Chinnery, P.F., Turnbull, D.M. and Howell, N. (1997) Mammalian mitochondrial genetics: heredity, heteroplasmy and disease. Trends Genet., 13, 450-455.
18. Lott, M.T., Voljavec, A.S. and Wallace, D.C. (1990) Variable genotype of Leber's hereditary optic neuropathy patients. Am. J. Ophthalmol., 109, 625-631.
19. He, Y., Wu, J., Dressman, D.C., Iacobuzio-Donahue, C., Markowitz, S.D., Velculescu, V.E., Diaz, L.A. Jr, Kinzler, K.W., Vogelstein, B. and Papadopoulos, N. (2010) Heteroplasmic mitochondrial DNA mutations in normal and tumour cells. Nature, 464, 610-614.
20. Li, M., Schonberg, A., Schaefer, M., Schroeder, R., Nasidze, I. and Stoneking, M. (2010) Detecting heteroplasmy from high-throughput sequencing of complete human mitochondrial DNA genomes. Am. J. Hum. Genet., 87, 237-249.
21. Moraes, C.T. (2001) What regulates mitochondrial DNA copy number in animal cells? Trends Genet., 17, 199-205.
22. Mayorov, V., Biousse, V., Newman, N.J. and Brown, M.D. (2005) The role of the ND5 gene in LHON: characterization of a new, heteroplasmic LHON mutation. Ann. Neurol., 58, 807-811.
23. McKenzie, M., Liolitsa, D., Akinshina, N., Campanella, M., Sisodiya, S., Hargreaves, I., Nirmalananthan, N., Sweeney, M.G., Abou-Sleiman, P.M., Wood, N.W. et al. (2007) Mitochondrial ND5 gene variation associated with encephalomyopathy and mitochondrial ATP consumption. J. Biol. Chem., 282, 36845-36852.
24. Petruzzella, V., Di Giacinto, G., Scacco, S., Piemonte, F., Torraco, A., Carrozzo, R., Vergari, R., Dionisi-Vici, C., Longo, D., Tessa, A. et al. (2003) Atypical Leigh syndrome associated with the D393N mutation in the mitochondrial ND5 subunit. Neurology, 61, 1017-1018.
25. Batandier, C., Picard, A., Tessier, N. and Lunardi, J. (2000) Identification of a novel T398A mutation in the ND5 subunit of the mitochondrial complex I and of three novel mtDNA polymorphisms in two patients presenting ocular symptoms. Hum. Mutat., 16, 532.
26. Dobrowolski, S.F., Hendrickx, A.T., van den Bosch, B.J., Smeets, H.J., Gray, J., Miller, T. and Sears, M. (2009) Identifying sequence variants in the human mitochondrial genome using high-resolution melt (HRM) profiling. Hum. Mutat., 30, 891-898.
27. Herrnstadt, C., Elson, J.L., Fahy, E., Preston, G., Turnbull, D.M., Anderson, C., Ghosh, S.S., Olefsky, J.M., Beal, M.F., Davis, R.E. et al. (2002) Reduced-median-network analysis of complete mitochondrial DNA coding-region sequences for the major African, Asian, and European haplogroups. Am. J. Hum. Genet., 70, 1152-1171.
28. Mitchell, A.L., Elson, J.L., Howell, N., Taylor, R.W. and Turnbull, D.M. (2006) Sequence variation in mitochondrial complex I genes: mutation or polymorphism? J. Med. Genet., 43, 175-179.
29. Adzhubei, I.A., Schmidt, S., Peshkin, L., Ramensky, V.E., Gerasimova, A., Bork, P., Kondrashov, A.S. and Sunyaev, S.R. (2010) A method and server for predicting damaging missense mutations. Nat. Methods, 7, 248-249.
30. Park, J.S., Sharma, L.K., Li, H., Xiang, R., Holstein, D., Wu, J., Lechleiter, J., Naylor, S.L., Deng, J.J., Lu, J. et al. (2009) A heteroplasmic, not homoplasmic, mitochondrial DNA mutation promotes tumorigenesis via alteration in reactive oxygen species generation and apoptosis. Hum. Mol. Genet., 18, 1578-1589.
31. Lascaro, D., Castellana, S., Gasparre, G., Romeo, G., Saccone, C. and Attimonelli, M. (2008) The RHNumtS compilation: features and bioinformatics approaches to locate and quantify human NumtS. BMC Genomics, 9, 267.
32. Simone, D., Calabrese, F.M., Lang, M., Gasparre, G. and Attimonelli, M. (2011) The reference human nuclear mitochondrial sequences compilation validated and implemented on the UCSC genome browser. BMC Genomics, 12, 517.
33. D'Aurelio, M., Gajewski, C.D., Lenaz, G. and Manfredi, G. (2006) Respiratory chain supercomplexes set the threshold for respiration defects in human mtDNA mutant cybrids. Hum. Mol. Genet., 15, 2157-2169.
34. Gasparre, G., Kurelac, I., Capristo, M., Iommarini, L., Ghelli, A., Ceccarelli, C., Nicoletti, G., Nanni, P., De Giovanni, C., Scotlandi, K. et al. (2011) A mutation threshold distinguishes the antitumorigenic effects of the mitochondrial gene MTND1, an oncojanus function. Cancer Res., 71, 6220-6229.
35. Dimauro, S. and Davidzon, G. (2005) Mitochondrial DNA and disease. Ann. Med., 37, 222-232.
36. Petruzzella, V., Moraes, C.T., Sano, M.C., Bonilla, E., DiMauro, S. and Schon, E.A. (1994) Extremely high levels of mutant mtDNAs co-localize with cytochrome c oxidase-negative ragged-red fibers in patients harboring a point mutation at nt 3243. Hum. Mol. Genet., 3, 449-454.
37. Rossignol, R., Faustin, B., Rocher, C., Malgat, M., Mazat, J.P. and Letellier, T. (2003) Mitochondrial threshold effects. Biochem. J., 370, 751-762.
38. Sacconi, S., Salviati, L., Nishigaki, Y., Walker, W.F., Hernandez-Rosa, E., Trevisson, E., Delplace, S., Desnuelle, C., Shanske, S., Hirano, M. et al. (2008) A functionally dominant mitochondrial DNA mutation. Hum. Mol. Genet., 17, 1814-1820.
39. Srivastava, S., Diaz, F., Iommarini, L., Aure, K., Lombes, A. and Moraes, C.T. (2009) PGC-1alpha/beta induced expression partially compensates for respiratory chain defects in cells from patients with mitochondrial disorders. Hum. Mol. Genet., 18, 1805-1812.
40. Yao, Y.G., Kong, Q.P., Salas, A. and Bandelt, H.J. (2008) Pseudomitochondrial genome haunts disease studies. J. Med. Genet., 45, 769-772.
41. Yao, Y.G., Salas, A., Logan, I. and Bandelt, H.J. (2009) mtDNA data mining in GenBank needs surveying. Am. J. Hum. Genet., 85, 929-933. author reply 933.
42. King, M.P. and Attardi, G. (1989) Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science, 246, 500-503.
43. Rizza, T., Vazquez-Memije, M.E., Meschini, M.C., Bianchi, M., Tozzi, G., Nesti, C., Piemonte, F., Bertini, E., Santorelli, F.M. and Carrozzo, R. (2009) Assaying ATP synthesis in cultured cells: a valuable tool for the diagnosis of patients with mitochondrial disorders. Biochem. Biophys. Res. Commun. 383, 58-62.
44. Kurelac, I., Lang, M., Zuntini, R., Calabrese, C., Simone, D., Vicario, S., Santamaria, M., Attimonelli, M., Romeo, G. and Gasparre, G. (2012) Searching for a needle in the haystack: comparing six methods to evaluate heteroplasmy in difficult sequence context. Biotechnol. Adv., 30, 363-371.
45. Margulies, M., Egholm, M., Altman, W.E., Attiya, S., Bader, J.S., Bemben, L.A., Berka, J., Braverman, M.S., Chen, Y.J., Chen, Z. et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376-380.
46. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G. and Durbin, R. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078-2079.
47. Kent, W.J., Sugnet, C.W., Furey, T.S., Roskin, K.M., Pringle, T.H., Zahler, A.M. and Haussler, D. (2002) The human genome browser at UCSC. Genome Res., 12, 996-1006.