Mitochondrial degeneration precedes the development of muscle atrophy in progression of cancer cachexia in tumour-bearing mice
Open accessAbstract
Background: Cancer cachexia is largely irreversible, at least via nutritional means, and responsible for 20–40% of cancer‐related deaths. Therefore, preventive measures are of primary importance; however, little is known about muscle perturbations prior to onset of cachexia. Cancer cachexia is associated with mitochondrial degeneration; yet, it remains to be determined if mitochondrial degeneration precedes muscle wasting in cancer cachexia. Therefore, our purpose was to determine if mitochondrial degeneration precedes cancer‐induced muscle wasting in tumour‐bearing mice. Methods: First, weight‐stable (MinStable) and cachectic (MinCC) ApcMin/+ mice were compared with C57Bl6/J controls for mRNA contents of mitochondrial quality regulators in quadriceps muscle. Next, Lewis lung carcinoma (LLC) cells or PBS (control) were injected into the hind flank of C57Bl6/J mice at 8 week age, and tumour allowed to develop for 1, 2, 3, or 4 weeks to examine time course of cachectic development. Succinate dehydrogenase stain was used to measure oxidative phenotype in tibialis anterior muscle. Mitochondrial quality and function were assessed using the reporter MitoTimer by transfection to flexor digitorum brevis and mitochondrial function/ROS emission in permeabilized adult myofibres from plantaris. RT‐qPCR and immunoblot measured the expression of mitochondrial quality control and antioxidant proteins. Data were analysed by one‐way ANOVA with Student–Newman–Kuels post hoc test. Results: MinStable mice displayed ~50% lower Pgc‐1α, Pparα, and Mfn2 compared with C57Bl6/J controls, whereas MinCC exhibited 10‐fold greater Bnip3 content compared with C57Bl6/J controls. In LLC, cachectic muscle loss was evident only at 4 weeks post‐tumour implantation. Oxidative capacity and mitochondrial content decreased by ~40% 4 weeks post‐tumour implantation. Mitochondrial function decreased by ~25% by 3 weeks after tumour implantation. Mitochondrial degeneration was evident by 2 week LLC compared with PBS control, indicated by MitoTimer red/green ratio and number of pure red puncta. Mitochondrial ROS production was elevated by ~50 to ~100% when compared with PBS at 1–3 weeks post‐tumour implantation. Mitochondrial quality control was dysregulated throughout the progression of cancer cachexia in tumour‐bearing mice. In contrast, antioxidant proteins were not altered in cachectic muscle wasting. Conclusions: Functional mitochondrial degeneration is evident in LLC tumour‐bearing mice prior to muscle atrophy. Contents of mitochondrial quality regulators across ApcMin/+ and LLC mice suggest impaired mitochondrial quality control as a commonality among pre‐clinical models of cancer cachexia. Our data provide novel evidence for impaired mitochondrial health prior to cachectic muscle loss and provide a potential therapeutic target to prevent cancer cachexia.
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Muscle loss in aging sarcopenia, cancer cachexia, chemotherapy-induced cachexia, and in a model of myasthenia gravis is characterized by the decline of both fusion and fission machinery.
“Muscle loss in aging sarcopenia [185, 187, 215], cancer cachexia, chemotherapy-induced cachexia [157–159], and in a model of myasthenia gravis [216], is characterized by the decline of both fusion and fission machinery.”
From The connection between the dynamic remodeling of the mitochondrial network and the regulation of muscle mass (2021) · cites this paper as [159]
Both fusion and fission machinery are suppressed in aging sarcopenia, cancer cachexia, and chemotherapy-induced muscle wasting.
“However, both fusion and fission machinery are suppressed in aging sarcopenia, cancer cachexia, and chemotherapy-induced muscle wasting.”
From Inhibition of the Fission Machinery Mitigates OPA1 Impairment in Adult Skeletal Muscles (2019) · cites this paper as [16]
The concomitant decrease of Opa1 and Drp1 also occurs in cancer cachexia and chemotherapy-induced cachexia as well as a model of myasthenia gravis.
“Moreover, the concomitant decrease of Opa1 and Drp1 also occurs in cancer cachexia and chemotherapy-induced cachexia [15,16,17] as well as a model of myasthenia gravis [18].”
From Inhibition of the Fission Machinery Mitigates OPA1 Impairment in Adult Skeletal Muscles (2019) · cites this paper as [16]
Muscle loss in aging sarcopenia, cancer cachexia, and myasthenia gravis is characterized by the decline of both fusion machinery and fission machinery.
“However, muscle loss in aging sarcopenia, cancer cachexia, and myasthenia gravis are characterized by the decline of both fusion machinery and fission machinery [6,11,12,15,16,17,18].”
From Inhibition of the Fission Machinery Mitigates OPA1 Impairment in Adult Skeletal Muscles (2019) · cites this paper as [16]
In skeletal muscle, mitochondrial fission proteins are reduced in ageing sarcopenia, cancer cachexia, and chemotherapy-induced muscle wasting.
“In skeletal muscle the mitochondrial fission proteins are reduced in different physiopathological conditions including ageing sarcopenia, cancer cachexia and chemotherapy-induced muscle wasting.”
From DRP1-mediated mitochondrial shape controls calcium homeostasis and muscle mass (2019) · cites this paper as [18]
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Self-citationThe Effect of Wheel Exercise on Functional Indices of Cachexia in Tumor-bearing Mice
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Self-citationIL-17A contributes skeletal muscle atrophy in lung cancer-induced cachexia via JAK2/STAT3 pathway.
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Self-citationExercise as a therapy for cancer-induced muscle wasting
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PGAM5 interacts with and maintains BNIP3 to license cancer-associated muscle wasting
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Lee, D. E., Brown, J. L., Rosa‐Caldwell, M. E., Perry, R. A., Brown, L. A., Haynie, W. S., Washington, T. A., Wiggs, M. P., Rajaram, N., & Greene, N. P. (2020) · JCSM Rapid Communications · doi:10.1002/rco2.18 · Cited by 24 · see citing works
Self-citation
- Authors
- Brown, J. L., Rosa‐Caldwell, M. E., Lee, D. E., Blackwell, T. A., Brown, L. A., Perry, R. A., Haynie, W. S., Hardee, J. P., Carson, J. A., Wiggs, M. P., Washington, T. A., & Greene, N. P.
- Affiliations
- University of Arkansas at Fayetteville (US)
- University of South Carolina (US)
- The University of Texas at Tyler (US)
- Corresponding author
- Greene, Nicholas P.
- ORCID
- Venue
- Journal of Cachexia, Sarcopenia and Muscle
- Publisher
- Wiley
- Published
- 2017-08-28
- Volume
- 8
- Issue
- 6
- Pages
- 926-938
- ISSN
- 2190-5991 (ISSN-L)
- 2190-6009
- PMC
- PMC5700433
- OpenAlex
- W2747686805
- Cited by
- 288
- References
- 70
- Citations by year
- 2026: 23 · 2025: 36 · 2024: 36 · 2023: 34 · 2022: 35 · 2021: 39 · 2020: 40 · 2019: 28 · 2018: 15 · 2017: 2
- FWCI
- 9.45
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Journal of Cachexia Sarcopenia and Muscle (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- Scholar Works at UT Tyler (The University of Texas at Tyler) (submittedVersion, cc-by-nc)
- Funders
- National Institutes of Health (5P30GM103336, R01CA121249A501)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- cancer cachexia, mitochondrial degeneration, muscle atrophy, mitochondrial quality control, PGC-1α, PPARα, mitofusin 2, BNIP3, reactive oxygen species, oxidative capacity, Lewis lung carcinoma, tumor-bearing mice, antioxidant proteins, cachexia prevention
- MeSH terms
- Animals, Antioxidants, Cachexia, Disease Models, Animal, Humans, Male, Microscopy, Fluorescence, Mitochondria, Muscular Atrophy, Neoplasms, Phenotype, Reactive Oxygen Species, Mice, Knockout, Oxidative Stress, Disease Progression, Carcinoma, Lewis Lung, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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