Abstract
We studied several affected and one nonaffected individuals belonging to three unrelated pedigrees. The pathological trait was an autosomal dominant mitochondrial myopathy due to large-scale multiple deletions of the mitochondrial genome. Clinically, symptomatic patients had progressive external ophthalmoplegia, muscle weakness and wasting, sensorineural hypoacusia, and, in some cases, vestibular areflexia and tremor. The muscle biopsies of all patients examined showed ragged-red fibers, neurogenic changes, and a partially decreased histochemical reaction to cytochrome c oxidase. Multiple mtDNA heteroplasmy was detected in the patients by both Southern blot analysis and PCR amplification, whereas the unaffected individual had the normal homoplasmic hybridization pattern. These findings confirm and add further details to the existence of a new human disease--defined clinically as a mitochondrial myopathy, genetically as a Mendelian autosomal dominant trait, and molecularly by the accumulation of multiple, large-scale deletions of the mitochondrial genome--that is due to impaired nuclear control during mtDNA replication.
MeSH Terms
Adolescent
Adult
Base Sequence
Blotting, Southern
Cell Nucleus/metabolism
Chromosome Deletion
Chromosomes, Human
DNA Replication
DNA, Mitochondrial/biosynthesis,genetics
Female
Genes, Dominant
Humans
Male
Middle Aged
Mitochondria, Muscle/metabolism
Molecular Sequence Data
Muscular Diseases/genetics,metabolism,pathology
Mutation
Ophthalmoplegia/genetics
Pedigree
Polymerase Chain Reaction
Polymorphism, Restriction Fragment Length
Chemicals
DNA, Mitochondrial
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Zeviani M
National Neurological Institute, Carlo Besta, Department of Biochemistry and Genetics, State University School of Medicine, Milan, Italy.
Bresolin N
Gellera C
Bordoni A
Pannacci M
Amati P
Moggio M
Servidei S
Scarlato G
DiDonato S
References (29)
29 references, click to expand
-
Identical mitochondrial DNA deletion in blood and muscle.
Lancet. 1989 Feb 18;1(8634):393-4
PMID: 2563557
-
Deletions of mitochondrial DNA in Kearns-Sayre syndrome.
Neurology. 1988 Sep;38(9):1339-46
PMID: 3412580
-
A direct repeat is a hotspot for large-scale deletion of human mitochondrial DNA.
Science. 1989 Apr 21;244(4902):346-9
PMID: 2711184
-
Molecular population genetics of mtDNA size variation in crickets.
Genetics. 1989 Mar;121(3):551-69
PMID: 2565855
-
Mitochondrial DNA deletions in progressive external ophthalmoplegia and Kearns-Sayre syndrome.
N Engl J Med. 1989 May 18;320(20):1293-9
PMID: 2541333
-
An autosomal dominant disorder with multiple deletions of mitochondrial DNA starting at the D-loop region.
Nature. 1989 May 25;339(6222):309-11
PMID: 2725645
-
Spontaneous Kearns-Sayre/chronic external ophthalmoplegia plus syndrome associated with a mitochondrial DNA deletion: a slip-replication model and metabolic therapy.
Proc Natl Acad Sci U S A. 1989 Oct;86(20):7952-6
PMID: 2554297
-
Directly repeated sequences associated with pathogenic mitochondrial DNA deletions.
Proc Natl Acad Sci U S A. 1989 Oct;86(20):8059-62
PMID: 2813377
-
Mitochondrial encephalomyopathies.
Rev Neurol (Paris). 1989;145(10):671-89
PMID: 2682927
-
Multiple deletions in mitochondrial DNA at direct repeats of non-D-loop regions in cases of familial mitochondrial myopathy.
Biochem Biophys Res Commun. 1989 Nov 15;164(3):1352-7
PMID: 2590206
-
Mitochondrial myopathies: clinical and biochemical features of 30 patients with major deletions of muscle mitochondrial DNA.
Ann Neurol. 1989 Dec;26(6):699-708
PMID: 2604380
-
Widespread tissue distribution of mitochondrial DNA deletions in Kearns-Sayre syndrome.
Neurology. 1990 Jan;40(1):24-8
PMID: 2296377
-
Recombination via flanking direct repeats is a major cause of large-scale deletions of human mitochondrial DNA.
Nucleic Acids Res. 1990 Feb 11;18(3):561-7
PMID: 2308845
-
Tissue distribution and transmission of mitochondrial DNA deletions in mitochondrial myopathies.
Ann Neurol. 1990 Jul;28(1):94-7
PMID: 2375642
-
Maternal inheritance of mammalian mitochondrial DNA.
Nature. 1974 Oct 11;251(5475):536-8
PMID: 4423884
-
Detection of specific sequences among DNA fragments separated by gel electrophoresis.
J Mol Biol. 1975 Nov 5;98(3):503-17
PMID: 1195397
-
DNA sequencing with chain-terminating inhibitors.
Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7
PMID: 271968
-
The structure and evolution of the human beta-globin gene family.
Cell. 1980 Oct;21(3):653-68
PMID: 6985477
-
Sequence and organization of the human mitochondrial genome.
Nature. 1981 Apr 9;290(5806):457-65
PMID: 7219534
-
Characterization of a rat liver mitochondrial DNA-protein complex. Replicative intermediates are protected against branch migrational loss.
J Biol Chem. 1981 Dec 25;256(24):12772-9
PMID: 6273406
-
Replication of animal mitochondrial DNA.
Cell. 1982 Apr;28(4):693-705
PMID: 6178513
-
Structure and evolution of organelle genomes.
Microbiol Rev. 1982 Jun;46(2):208-40
PMID: 6750346
-
Electron transfer flavoprotein from pig liver mitochondria. A simple purification and re-evaluation of some of the molecular properties.
Biochem J. 1983 Feb 1;209(2):541-5
PMID: 6847633
-
A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
Anal Biochem. 1983 Jul 1;132(1):6-13
PMID: 6312838
-
Characterization of a mitochondrial protein binding to single-stranded DNA.
Nucleic Acids Res. 1985 Mar 11;13(5):1703-16
PMID: 4039816
-
Rapid isolation of animal mitochondrial DNA by alkaline extraction.
FEBS Lett. 1985 Nov 18;192(2):267-70
PMID: 2998870
-
Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase.
Science. 1988 Jan 29;239(4839):487-91
PMID: 2448875
-
Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies.
Nature. 1988 Feb 25;331(6158):717-9
PMID: 2830540
-
An improved method for directly sequencing PCR amplified material using dimethyl sulphoxide.
Nucleic Acids Res. 1989 Feb 11;17(3):1266
PMID: 2922271