Mitochondrial DNA–Deletion Mutations Accumulate Intracellularly to Detrimental Levels in Aged Human Skeletal Muscle Fibers
Open accessAbstract
Skeletal muscle-mass loss with age has severe health consequences, yet the molecular basis of the loss remains obscure. Although mitochondrial DNA (mtDNA)-deletion mutations have been shown to accumulate with age, for these aberrant genomes to be physiologically relevant, they must accumulate to high levels intracellularly and be present in a significant number of cells. We examined mtDNA-deletion mutations in vastus lateralis (VL) muscle of human subjects aged 49-93 years, using both histologic and polymerase-chain-reaction (PCR) analyses, to determine the physiological and genomic integrity of mitochondria in aging human muscle. The number of VL muscle fibers exhibiting mitochondrial electron-transport-system (ETS) abnormalities increased from an estimated 6% at age 49 years to 31% at age 92 years. We analyzed the mitochondrial genotype of 48 single ETS-abnormal, cytochrome c oxidase-negative/succinate dehydrogenase-hyperreactive (COX-/SDH++) fibers from normal aging human subjects and identified mtDNA-deletion mutations in all abnormal fibers. Deletion mutations were clonal within a fiber and concomitant to the COX-/SDH++ region. Quantitative PCR analysis of wild-type and deletion-containing mtDNA genomes within ETS-abnormal regions of single fibers demonstrated that these deletion mutations accumulate to detrimental levels (>90% of the total mtDNA).
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The role of mitochondrial dysfunction in the etiology of sarcopenia has been extensively characterized.
“The role of mitochondrial dysfunction in the etiology of sarcopenia has been extensively characterized (17, 18, 19, 20).”
From Discovering pathways of sarcopenia in older adults: a role for insulin resistance on mitochondria dysfunction (2011) · cites this paper as [18]
Accumulations of mtDNA damage in the form of point mutations, deletions and depletions are correlated with aging and age-related diseases as observed in human skeletal muscle, liver, brain, heart, skin fibroblasts and colonic crypt stem cells.
“Accumulations of mtDNA damage in the form of point mutations, deletions and depletions are correlated with aging and age-related diseases as observed in human skeletal muscle (Bua et al., 2006; Fayet et al., 2002), liver (Yen et al., 1991), brain (Corral-Debrinski et al., 1992a; Corral-Debrinski et al., 1994; Lin et al., 2002), heart (Corral-Debrinski et al., 1992b; Cortopassi and Arnheim, 1990),”
From Role of the mitochondrial DNA replication machinery in mitochondrial DNA mutagenesis, aging and age-related diseases (2017) · cites this paper as Bua et al., 2006
Most mtDNA deletions share common features: they mainly occur between the origins of replication, O_H and O_L, and are typically flanked by short direct repeats.
“They mainly occur between the origins of replication, O H and O L , and are typically flanked by short direct repeats [94,95].”
From Mitochondrial DNA mutations and human disease (2010) · cites this paper as [94]
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Tarnopolsky, M. A. (2009) · Applied Physiology Nutrition and Metabolism · doi:10.1139/h09-022 · Cited by 59 · see citing works
Transient systemic mtDNA damage leads to muscle wasting by reducing the satellite cell pool
Wang, X., Pickrell, A. M., Rossi, S. G., Pinto, M., Dillon, L. M., Hida, A., Rotundo, R. L., & Moraes, C. T. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt251 · Cited by 54 · see citing works
Do mtDNA deletions drive premature aging in mtDNA mutator mice?
Kraytsberg, Y., Simon, D. K., Turnbull, D. M., & Khrapko, K. (2009) · Aging Cell · doi:10.1111/j.1474-9726.2009.00484.x · Cited by 42 · see citing works
Organotypic cultures as aging associated disease models
Sanchez, M. M., Bagdasarian, I. A., Darch, W., & Morgan, J. T. (2022) · Aging · doi:10.18632/aging.204361 · Cited by 12 · see citing works
- Authors
- Bua, E., Johnson, J., Herbst, A., Delong, B., McKenzie, D., Salamat, S., & Aiken, J. M.
- Affiliations
- University of Wisconsin–Madison (US)
- Corresponding author
- Aiken, Judd M.
- Venue
- The American Journal of Human Genetics
- Publisher
- Elsevier BV
- Published
- 2006-09
- Volume
- 79
- Issue
- 3
- Pages
- 469-480
- ISSN
- 0002-9297 (ISSN-L)
- PMC
- PMC1559550
- OpenAlex
- W2054511417
- Cited by
- 442
- References
- 47
- Citations by year
- 2026: 25 · 2025: 16 · 2024: 23 · 2023: 19 · 2022: 20 · 2021: 16 · 2020: 39 · 2019: 32 · 2018: 23 · 2017: 23 · 2016: 25 · 2015: 25 · 2014: 20 · 2013: 19 · 2012: 19
- FWCI
- 7.49
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- The American Journal of Human Genetics (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (AG-11604, R01AG011604)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- skeletal muscle aging, cytochrome c oxidase deficiency, mitochondrial genotype, muscle mass loss, human aging
- MeSH terms
- Aged, Aged, 80 and over, Aging, Electron Transport Complex IV, DNA, Mitochondrial, Electron Transport, Female, Humans, Male, Middle Aged, Mitochondria, Muscle, Succinate Dehydrogenase, Sequence Deletion, Muscle, Skeletal, Muscle Fibers, Skeletal, Electron Transport Chain Complex Proteins
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