Musclin, A Myokine Induced by Aerobic Exercise, Retards Muscle Atrophy During Cancer Cachexia in Mice

Re Cecconi, Andrea D.; Forti, Mara; Chiappa, Michela; Zhu, Zhiyong; Zingman, Leonid V.; Cervo, Luigi; Beltrame, Luca; Marchini, Sergio; Piccirillo, Rosanna

doi:10.3390/cancers11101541

Cited by 66Muscle Physiology and DisordersNutrition and Health in AgingExercise and Physiological Responses

Musclin, A Myokine Induced by Aerobic Exercise, Retards Muscle Atrophy During Cancer Cachexia in Mice

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Re Cecconi, Andrea D., Forti, Mara, Chiappa, Michela, Zhu, Zhiyong, Zingman, Leonid V., Cervo, Luigi, Beltrame, Luca, Marchini, Sergio +1 more·2019·Cancers

DOI 10.3390/cancers11101541PMC PMC6826436

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Abstract

Physical activity improves the prognosis of cancer patients, partly by contrasting the associated muscle wasting (cachexia), through still unknown mechanisms. We asked whether aerobic exercise causes secretion by skeletal muscles of proteins (myokines) that may contrast cachexia. Media conditioned by peroxisome proliferator-activated receptor γ coactivator 1α (PGC1α)-expressing myotubes, reproducing some metabolic adaptations of aerobic exercise, as increased mitochondrial biogenesis and oxidative phosphorylation, restrained constitutively active Forkhead box-containing subfamily O3 (caFoxO3)-induced proteolysis. Microarray analysis identified amphiregulin (AREG), natriuretic peptide precursor B (NppB), musclin and fibroblast growth factor 18 (FGF18) as myokines highly induced by PGC1α. Notably, only musclin tended to be low in muscle of mice with a rare human renal carcinoma; it was reduced in plasma and in muscles of C26-bearing mice and in atrophying myotubes, where PGC1α expression is impaired. Therefore, we electroporated the Tibialis Anterior (TA) of C26-bearing mice with musclin or (its receptor) natriuretic peptide receptor 3 (Npr3)-encoding plasmids and found a preserved fiber area, as a result of restrained proteolysis. Musclin knockout (KO) mice lose more muscle tissue during growth of two distinct cachexia-causing tumors. Running protected C26-bearing mice from cachexia, not changing tumor growth, and rescued the C26-induced downregulation of musclin in muscles and plasma. Musclin expression did not change in overloaded plantaris of mice, recapitulating partially muscle adaptations to anaerobic exercise. Musclin might, therefore, be beneficial to cancer patients who cannot exercise and are at risk of cachexia and may help to explain how aerobic exercise alleviates cancer-induced muscle wasting.

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Musclin abolishes muscle atrophy related with cancer in mice.
“Recent evidence shows that musclin abolishes muscle atrophy related with cancer in mice (66).”
From Muscle–Organ Crosstalk: The Emerging Roles of Myokines (2020) · cites this paper as [66]

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Dynamic Response of Musclin, a Myokine, to Aerobic Exercise and Its Interplay With Natriuretic Peptides and Receptor C
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Mustn1 ablation in skeletal muscle results in increased glucose tolerance concomitant with upregulated GLUT expression in male mice
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Genome-wide analysis of a cellular exercise model based on electrical pulse stimulation
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Apelin Resistance Contributes to Muscle Loss during Cancer Cachexia in Mice
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Effect of resistance training on satellite cells in old mice – a transcriptome study
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Trabectedin and Lurbinectedin Extend Survival of Mice Bearing C26 Colon Adenocarcinoma, without Affecting Tumor Growth or Cachexia
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Swimming Attenuates Muscle Wasting and Mediates Multiple Signaling Pathways and Metabolites in CT-26 Bearing Mice
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Skeletal Muscle as Endocrine Organ
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The augmentation of cytotoxic immune cell functionality through physical exertion bolsters the potency of chemotherapy in models of mammary carcinoma
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Myokines: A central point in managing redox homeostasis and quality of life
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Decreased serum musclin concentration is independently associated with the high prevalence of sarcopenia in Chinese middle‐elderly patients with type 2 diabetes mellitus
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Exercise-induced myokines in metabolic regulation: mechanisms, mimetics, and translational potential
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Effects of Exercise on Cardiovascular and Metabolic Responses in Adults and Childhood Cancer Survivors: The Role of NETosis and Low-Grade Inflammation as a Novel Therapeutic Target—A Narrative Review
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Effects of Aerobic-Anaerobic Exercise on Social Avoidance, Positive and Negative Affects, and Self-Consciousness of Obese Women
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Integrated procedures for accelerating, deepening, and leading genetic inquiry: A first application on human muscle secretome
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Relationship between myostatin, musclin, nutritional status, and functionality in older Colombian community-dwelling adults: A cross-sectional study
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Cancer Cachexia
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Pathogenesis and Nutritional Intervention of Chronic Obstructive Pulmonary Disease-Associated Frailty
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Myokine Expression in Cancer Cachexia
Manole, E., Ceafalan, L. C., Gaina, G. F., Mosoia, O., & Hinescu, M. E. (2023) · Interdisciplinary cancer research · doi:10.1007/16833_2023_138 · Cited by 1 · see citing works
Circulating Musclin is associated with skeletal muscle function and subclinical cardiac dysfunction in patients with cancer
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Exercise training promotes the immune cytotoxicity to enhance the inhibition of Doxorubicin in a Breast Cancer ModelPreprint
Qin, B., Gui, J., He, Z., Xie, L., Feng, S., Ye, J., Sun, X., & Sang, M. (2023) · Research Square · doi:10.21203/rs.3.rs-2896087/v1 · Cited by 1 · see citing works
The Effect of Cancer Cachexia Progression on the Feeding Regulation of Skeletal Muscle Protein Turnover
Counts, B. R. (2021) · doi:10.21007/etd.cghs.2021.0559
Targeting phosphatase DUSP22 ameliorates skeletal muscle wasting via Akt independent JNK-FOXO3a repressionPreprint
Lee, S., Kim, H., Kim, S.-W., Lee, H., Jung, D., & Williams, D. R. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.08.588643
Comparison of Muscle Damage Markers and Myokines between Adult and Middle-Aged Marathon Runners
Zocoler, C. A. S., Sierra, A., Lima, G. H. O., Galán, B. S. M., Barbeiro, H. V., de Souza, H. P., & Cury‐Boaventura, M. F. (2025) · OBM Geriatrics · doi:10.21926/obm.geriatr.2501301
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Role of the glucocorticoid pathway in skeletal muscle wasting and hepatic metabolism rewiring during cancer cachexia in ApcMin/+ mice – Functional implication of myostatin gene invalidation
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Gu, H., Albrecht, E., Deng, Z., & Maak, S. (2026) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2026.102115
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PL-013 Musclin: a myokine induced by aerobic exercise useful to contrast muscle wasting during cancer
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Aerobic Exercise Ameliorates Cancer Cachexia-Induced Muscle Wasting through Adiponectin Signaling
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Dissecting the possible role of p97 in muscle wasting during cancer cachexia
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PGC-1α overexpression is not sufficient to mitigate cancer cachexia in either male or female mice
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16th Meeting of the Interuniversity Institute of Myology (IIM) - Assisi (Italy), October 17-20, 2019: Foreword, Program and Abstracts
Gabellini, D., & Musarò, A. (2020) · European Journal of Translational Myology · doi:10.4081/ejtm.2020.9345 · Cited by 1 · see citing works

Authors: Re Cecconi, A. D., Forti, M., Chiappa, M., Zhu, Z., Zingman, L. V., Cervo, L., Beltrame, L., Marchini, S., & Piccirillo, R.
Affiliations: Department of Neurosciences, Mario Negri Institute for Pharmacological Research IRCCS, 20156 Milan, Italy
Mario Negri Institute for Pharmacological Research (IT)
University of Iowa (US)
Corresponding author: Piccirillo, Rosanna
ORCID: Re Cecconi, Andrea D.
Chiappa, Michela
Zhu, Zhiyong
Zingman, Leonid V.
Cervo, Luigi
Beltrame, Luca
Marchini, Sergio
Piccirillo, Rosanna
Venue: Cancers
Publisher: MDPI AG
Published: 2019-10-12
Volume: 11
Issue: 10
Pages: 1541
ISSN: 2072-6694 (ISSN-L)
DOI: 10.3390/cancers11101541
PMC: PMC6826436
OpenAlex: W2979643525
Cited by: 66
References: 82
Citations by year: 2026: 6 · 2025: 7 · 2024: 6 · 2023: 13 · 2022: 14 · 2021: 6 · 2020: 14
FWCI: 2.81
Type: journal article
Language: en
Open access: gold
dx.doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Cancers (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Associazione Italiana per la Ricerca sul Cancro (11423)
Fondazione Cariplo (2014-1164)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
Keywords: musclin, myokines, cancer cachexia, muscle atrophy, aerobic exercise, PGC-1α, renal carcinoma, C26 tumor, mitochondrial biogenesis

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Musclin, A Myokine Induced by Aerobic Exercise, Retards Muscle Atrophy During Cancer Cachexia in Mice

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