Prevalence of mitochondrial ND4 mutations in 1281 han Chinese subjects with leber’s hereditary optic neuropathy

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 8, 2015, Pages 4778-4788

  Jiang, Pingping ^a,b   Liang, Min ^a,c   Zhang, Juanjuan ^a,c   Gao, Yinglong ^c   He, Zheyun ^c   Yu, Han ^c   Zhao, Fuxin ^c   Ji, Yanchun ^a   Liu, Xiaoling ^c   Zhang, Minglian ^d   Fu, Qun ^e   Tong, Yi ^c   Sun, Yanhong ^f   Zhou, Xiangtian ^c   Huang, Taosheng ^g   Qu, Jia ^c   Guan, Min Xin ^a,b,g,h  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c WENZHOU MEDICAL UNIVERSITY   (China)

^d School of Ophthalmology and Optometry Wenzhou Medical University ^*  (China)

^e XINXIANG MEDICAL UNIVERSITY   (China)

^f BEIJING UNIVERSITY OF CHINESE MEDICINE   (China)

^g CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^h ZHEJIANG UNIVERSITY   (China)

Author keywords

Leber s hereditary optic neuropathy; Mitochondrial DNA; Mutational screening; ND4 gene; Prevalence

Indexed keywords

MITOCHONDRIAL DNA;

ADOLESCENT; ADULT; ARTICLE; CHILD; CHINESE; CLINICAL ASSESSMENT; CONTROLLED STUDY; DNA POLYMORPHISM; DNA SEQUENCE; ENZYMATIC ASSAY; FEMALE; GENE; GENE MUTATION; HUMAN; LEBER HEREDITARY OPTIC NEUROPATHY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MISSENSE MUTATION; MITOCHONDRIAL HAPLOGROUP; ND4 GENE; OPHTHALMOLOGY; OXIDATIVE PHOSPHORYLATION; PEDIGREE ANALYSIS; PHYLOGENY; POLYMERASE CHAIN REACTION; PRESCHOOL CHILD; PREVALENCE; PRIORITY JOURNAL; SCHOOL CHILD; VISUAL IMPAIRMENT; YOUNG ADULT; CELL CULTURE; CHINA; CLINICAL TRIAL; EPIDEMIOLOGY; ETHNIC GROUP; ETHNOLOGY; GENETICS; MULTICENTER STUDY; MUTATION; NUCLEOTIDE SEQUENCE; PATHOLOGY; PEDIGREE;

ADOLESCENT; ADULT; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; CHINA; DNA MUTATIONAL ANALYSIS; DNA, MITOCHONDRIAL; ETHNIC GROUPS; FEMALE; HUMANS; MALE; MIDDLE AGED; MUTATION; OPTIC ATROPHY, HEREDITARY, LEBER; PEDIGREE; PREVALENCE; YOUNG ADULT;

EID: 84939795897     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.14-16158     Document Type: Article

References (62)

1. Yu-Wai-Man P, Griffiths PG, Hudson G, Chinnery PF. Inherited mitochondrial optic neuropathies. J Med Genet. 2009;46:145-158
2. Man PY, Griffiths PG, Brown DT, et al. The epidemiology of Leber hereditary optic neuropathy in the North East of England. Am J Hum Genet. 2003;72:333–339
3. Kerrison JB, Newman NJ. Clinical spectrum of Leber’s hereditary optic neuropathy. Clin Neurosci. 1997;4:295–301
4. Carelli V, La Morgia C, Valentino ML, et al. Retinal ganglion cell neurodegeneration in mitochondrial inherited disorders. Biochim Biophys Acta. 2009;1787:518–528
5. Newman NJ, Wallace DC. Mitochondria and Leber’s hereditary optic neuropathy. Am J Ophthalmol. 1990;109:726–730
6. Newman NJ, Lott MT, Wallace DC. The clinical characteristics of pedigrees of Leber’s hereditary optic neuropathy with the 11778 mutation. Am J Ophthal. 1991;111:750–762
7. Giles RE, Blanc H, Cann HM, Wallace DC. Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci U S A. 1980; 77:6715–6719
8. Wallace DC, Singh G, Lott MT, et al. Mitochondrial DNA mutation associated with Leber’s hereditary optic neuropathy. Science. 1988;242:1427–1430
9. Ruiz-Pesini E, Lott MT, Procaccio V, et al. An enhanced mitomap with a global mtDNA mutational phylogeny. Nucleic Acids Res. 2007;35:D823–D828
10. Brown MD, Torroni A, Reckord CL, Wallace DC. Phylogenetic analysis of Leber’s hereditary optic neuropathy mitochondrial DNA’s indicates multiple independent occurrences of the common mutations. Hum Mutat. 1995;6:311–325
11. Mashima Y, Yamada K, Wakakura M, et al. Spectrum of pathogenic mitochondrial DNA mutations and clinical features in Japanese families with Leber’s hereditary optic neuropathy. Curr Eye Res. 1998;17:403–408
12. Mackey DA, Oostra RJ, Rosenberg T, et al. Primary pathogenic mtDNA mutations in multigeneration pedigrees with Leber hereditary optic neuropathy. Am J Hum Genet. 1996;59:481-485
13. Jia X, Li S, Xiao X, et al. Molecular epidemiology of mtDNA mutations in 903 Chinese families suspected with Leber hereditary optic neuropathy. J Hum Genet. 2006;51:851–856
14. Kirches E. LHON: mitochondrial mutations and more. Curr Genomics. 2011;12:44–54
15. Korkiamaki P, Kervinen M, Karjalainen K, et al. Prevalence of the primary LHON mutations in Northern Finland associated with bilateral optic atrophy and tobacco-alcohol amblyopia. Acta Ophthalmol. 2013;91:630–634
16. Riordan-Eva P, Sanders MD, Govan GG, et al. The clinical features of Leber’s hereditary optic neuropathy defined by the presence of a pathogenic mitochondrial DNA mutation. Brain. 1995;118(pt 2):319–337
17. Chinnery PF, Brown DT, Andrews RM, et al. The mitochondrial ND6 gene is a hot spot for mutations that cause Leber’s hereditary optic neuropathy. Brain. 2001;124(pt 1):209–218
18. Valentino ML, Barboni P, Ghelli A, et al. The ND1 gene of complex I is a mutational hot spot for Leber’s hereditary optic neuropathy. Ann Neurol. 2004;56:631–641
19. Chen J, Xu K, Zhang X, et al. Mutation screening of mitochondrial DNA as well as OPA1 and OPA3 in a Chinese cohort with suspected hereditary optic atrophy. Invest Ophthalmol Vis Sci. 2014;55:6987–6995
20. Liang M, Jiang P, Li F, et al. Frequency and spectrum of mitochondrial ND6 mutations in 1218 Han Chinese subjects with Leber’s hereditary optic neuropathy. Invest Ophthalmol Vis Sci. 2014;55:1321–1331
21. Andrews RM, Kubacka I, Chinnery PF, et al. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet. 1999;23:147
22. Rieder MJ, Taylor SL, Tobe VO, Nickerson DA. Automating the identification of DNA variations using quality-based fluorescence re-sequencing: analysis of the human mitochondrial genome. Nucleic Acids Res. 1998;26:967–973
23. Qu J, Li R, Zhou X, et al. The novel A4435G mutation in the mitochondrial tRNAMet may modulate the phenotypic expression of the LHON-associated ND4 G11778A mutation. Invest Ophthalmol Vis Sci. 2006;47:475–483
24. Miller G, Lipman M. Release of infectious Epstein-Barr virus by transformed marmoset leukocytes. Proc Natl Acad Sci U S A. 1973;70:190–194
25. Qian Y, Zhou X, Hu Y, et al. Clinical evaluation and mitochondrial DNA sequence analysis in three Chinese families with Leber’s hereditary optic neuropathy. Biochem Biophys Res Commun. 2005;332:614–621
26. Birch-Machin MA, Turnbull DM. Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods Cell Biol. 2001;65:97–117
27. Zhang J, Jiang P, Jin X, et al. Leber’s hereditary optic neuropathy caused by the homoplasmic ND1 m.3635G>A mutation in nine Han Chinese families. Mitochondrion. 2014; 18:18–26
28. Tanaka M, Cabrera VM, Gonzalez AM, et al. Mitochondrial genome variation in eastern Asia and the peopling of Japan. Genome Res. 2004;14:1832–1850
29. Kong QP, Bandelt HJ, Sun C, et al. Updating the East Asian mtDNA phylogeny: a prerequisite for the identification of pathogenic mutations. Hum Mol Genet. 2006;15:2076–2086
30. Fauser S, Luberichs J, Besch D, Leo-Kottler B. Sequence analysis of the complete mitochondrial genome in patients with Leber’s hereditary optic neuropathy lacking the three most common pathogenic DNA mutations. Biochem Biophys Res Commun. 2002;295:342–347
31. De Vries DD, Went LN, Bruyn GW, et al. Genetic and biochemical impairment of mitochondrial complex I activity in a family with Leber hereditary optic neuropathy and hereditary spastic dystonia. Am J Hum Genet. 1996;58:703-711
32. Ruiz-Pesini E, Wallace DC. Evidence for adaptive selection acting on the tRNA and rRNA genes of human mitochondrial DNA. Hum Mutat. 2006;27:1072–1081
33. Qu J, Zhou X, Zhao F, et al. Low penetrance of Leber’s hereditary optic neuropathy in ten Han Chinese families carrying the ND6 T11484C mutation. Biochim Biophys Acta. 2010;1800:305–312
34. Zhang J, Zhao F, Fu Q, et al. Mitochondrial haplotypes may modulate the phenotypic manifestation of the LHON-associated m.14484T>C (MT-ND6) mutation in Chinese families. Mitochondrion. 2013;13:772–781
35. Zhou X, Wei Q, Yang L, et al. Leber’s hereditary optic neuropathy is associated with the mitochondrial ND4 G11696A mutation in five Chinese families. Biochem Biophys Res Commun. 2006;340:69–75
36. Qu J, Li R, Zhou X, et al. Cosegregation of the ND4 G11696A mutation with the LHON-associated ND4 G11778A mutation in a four generation Chinese family. Mitochondrion. 2007;7: 140–146
37. Cai W, Fu Q, Zhou X, et al. Mitochondrial variants may influence the phenotypic manifestation of Leber’s hereditary optic neuropathy-associated ND4 G11778A mutation. J Genet Genomics. 2008;35:649–655
38. Qu J, Zhou X, Zhang J, et al. Extremely low penetrance of Leber’s hereditary optic neuropathy in 8 Han Chinese families carrying the ND4 G11778A mutation. Ophthalmology. 2009; 116:558–564.e3
39. Qu J, Li R, Tong Y, et al. Only male matrilineal relatives with Leber’s hereditary optic neuropathy in a large Chinese family carrying the mitochondrial DNA G11778A mutation. Biochem Biophys Res Commun. 2005;328:1139–1145
40. Zhou X, Zhang H, Zhao F, et al. Very high penetrance and occurrence of Leber’s hereditary optic neuropathy in a large Han Chinese pedigree carrying the ND4 G11778A mutation. Mol Genet Metab. 2010;100:379–384
41. Zhang J, Zhou X, Zhou J, et al. Mitochondrial ND6 T14502C variant may modulate the phenotypic expression of LHONassociated G11778A mutation in four Chinese families. Biochem Biophys Res Commun. 2010;399:647–653
42. Qu J, Wang Y, Tong Y, et al. Leber’s hereditary optic neuropathy affects only female matrilineal relatives in two Chinese families. Invest Ophthalmol Vis Sci. 2010;51:4906-4912
43. Zhang M, Zhou X, Li C, et al. Mitochondrial haplogroup M9a specific variant ND1 T3394C may have a modifying role in the phenotypic expression of the LHON-associated ND4 G11778A mutation. Mol Genet Metab. 2010;101:192–199
44. Li R, Qu J, Zhou X, et al. The mitochondrial tRNAThr A15951G mutation may influence the phenotypic expression of the LHON-associated ND4 G11778A mutation in a Chinese family. Gene. 2006;376:79–86
45. Sundaresan P, Kumar SM, Thompson S, Fingert JH. Reduced frequency of known mutations in a cohort of LHON patients from India. Ophthalmic Genet. 2010;31:196–199
46. Kim JY, Hwang JM, Chang BL, Park SS. Spectrum of the mitochondrial DNA mutations of Leber’s hereditary optic neuropathy in Koreans. J Neurol. 2003;250:278–281
47. Yum HR, Chae H, Shin SY, Kim Y, Kim M, Park SH. Pathogenic mitochondrial DNA mutations and associated clinical features in Korean patients with Leber’s hereditary optic neuropathy. Invest Ophthalmol Vis Sci. 2014;55:8095–8101
48. Carelli V, Achilli A, Valentino ML, et al. Haplogroup effects and recombination of mitochondrial DNA: novel clues from the analysis of Leber hereditary optic neuropathy pedigrees. Am J Hum Genet. 2006;78:564–574
49. Howell N, Oostra RJ, Bolhuis PA, et al. Sequence analysis of the mitochondrial genomes from Dutch pedigrees with Leber hereditary optic neuropathy. Am J Hum Genet. 2003;72:1460-1469
50. Huoponen K, Lamminen T, Juvonen V, et al. The spectrum of mitochondrial DNA mutations in families with Leber hereditary optic neuroretinopathy. Hum Genet. 1993;92:379–384
51. Wallace DC. Why do we still have a maternally inherited mitochondrial DNA: insights from evolutionary medicine. Annu Rev Biochem. 2007;76:781–821
52. Hudson G, Carelli V, Spruijt L, et al. Clinical expression of Leber hereditary optic neuropathy is affected by the mitochondrial DNA-haplogroup background. Am J Hum Genet. 2007;81:228–233
53. Istikharah R, Tun AW, Kaewsutthi S, et al. Identification of the variants in PARL, the nuclear modifier gene, responsible for the expression of LHON patients in Thailand. Exp Eye Res. 2013;116:55–57
54. Carroll J, Fearnley IM, Skehel JM, Shannon RJ, Hirst J, Walker JE. Bovine complex I is a complex of 45 different subunits. J Biol Chem. 2006;281:32724–32727
55. Scheffler IE. Mitochondrial disease associated with complex I (NADH-CoQ oxidoreductase) deficiency. J Inherit Metab Dis. 2015;38:405–415
56. Hofhaus G, Johns DR, Hurko O, et al. Respiration and growth defects in transmitochondrial cell lines carrying the 11778 mutation associated with Leber’s hereditary optic neuropathy. J Biol Chem. 1996;271:13155–13161
57. Brown MD, Trounce IA, Jun AS, et al. Functional analysis of lymphoblast and cybrid mitochondria containing the 3460, 11778, or 14484 Leber’s hereditary optic neuropathy mitochondrial DNA mutation. J Biol Chem. 2000;275:39831-39836
58. Zhou X, Qian Y, Zhang J, et al. Leber’s hereditary optic neuropathy is associated with the T3866C mutation in mitochondrial ND1 gene in three Han Chinese families. Invest Ophthalmol Vis Sci. 2012;53:4586–4594
59. Wong A, Cavelier L, Collins-Schramm HE, et al. Differentiationspecific effects of LHON mutations introduced into neuronal NT2 cells. Hum Mol Genet. 2002;11:431–438
60. Torroni A, Petrozzi M, D’Urbano L, et al. 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. 1997;60:1107–1121
61. Ji Y, Zhang AM, Jia X, et al. Mitochondrial DNA haplogroups M7b102 and M8a affect clinical expression of leber hereditary optic neuropathy in Chinese families with the m.11778G–>a mutation. Am J Hum Genet. 2008;83:760–768
62. Ji Y, Liang M, Zhang J, et al. Mitochondrial haplotypes may modulate the phenotypic manifestation of the LHON-associated ND1 G3460A mutation in Chinese families. J Hum Genet. 2014;59:134–140.