A negative feedback loop between fibroadipogenic progenitors and muscle fibres involving endothelin promotes human muscle fibrosis Article Swipe
Mona Bensalah
,
Laura Muraine
,
Alexis Boulinguiez
,
Lorenzo Giordani
,
Victorine Albert
,
Victor Ythier
,
Jamila Dhiab
,
A. Oliver
,
Valentine Hanique
,
Teresa Gidaro
,
Sophie Périé
,
J. Lacau St-Guily
,
Aurélien Corneau
,
Gillian Butler‐Browne
,
Anne Bigot
,
Vincent Mouly
,
Elisa Négroni
,
Capucine Trollet
·
YOU?
·
· 2022
· Open Access
·
· DOI: https://doi.org/10.1002/jcsm.12974
YOU?
·
· 2022
· Open Access
·
· DOI: https://doi.org/10.1002/jcsm.12974
Background Fibrosis is defined as an excessive accumulation of extracellular matrix (ECM) components. Many organs are subjected to fibrosis including the lung, liver, heart, skin, kidney, and muscle. Muscle fibrosis occurs in response to trauma, aging, or dystrophies and impairs muscle function. Fibrosis represents a hurdle for the treatment of human muscular dystrophies. While data on the mechanisms of fibrosis have mostly been investigated in mice, dystrophic mouse models often do not recapitulate fibrosis as observed in human patients. Consequently, the cellular and molecular mechanisms that lead to fibrosis in human muscle still need to be identified. Methods Combining mass cytometry, transcriptome profiling, in vitro co‐culture experiments, and in vivo transplantation in immunodeficient mice, we investigated the role and nature of nonmyogenic cells (fibroadipogenic progenitors, FAPs) from human fibrotic muscles of healthy individuals (FibM CT ) and individuals with oculopharyngeal muscular dystrophy (OPMD; FibM OP ), as compared with nonmyogenic cells from human nonfibrotic muscle (M CT ). Results We found that the proliferation rate of FAPs from fibrotic muscle is 3–4 times higher than those of FAPs from nonfibrotic muscle (population doubling per day: M CT 0.2 ± 0.1, FibM CT 0.7 ± 0.1, and FibM OP 0.8 ± 0.3). When cocultured with muscle cells, FAPs from fibrotic muscle impair the fusion index unlike M CT FAPs (myoblasts alone 57.3 ± 11.1%, coculture with M CT 43.1 ± 8.9%, with FibM CT 31.7 ± 8.2%, and with FibM OP 36.06 ± 10.29%). We also observed an increased proliferation of FAPs from fibrotic muscles in these co‐cultures in differentiation conditions (FibM CT +17.4%, P < 0.01 and FibM OP +15.1%, P < 0.01). This effect is likely linked to the increased activation of the canonical TGFβ‐SMAD pathway in FAPs from fibrotic muscles evidenced by pSMAD3 immunostaining ( P < 0.05). In addition to the profibrogenic TGFβ pathway, we identified endothelin as a new actor implicated in the altered cross‐talk between muscle cells and fibrotic FAPs, confirmed by an improvement of the fusion index in the presence of bosentan, an endothelin receptor antagonist (from 33.8 ± 10.9% to 52.9 ± 10.1%, P < 0.05). Conclusions Our data demonstrate the key role of FAPs and their cross‐talk with muscle cells through a paracrine signalling pathway in fibrosis of human skeletal muscle and identify endothelin as a new druggable target to counteract human muscle fibrosis.
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- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.1002/jcsm.12974
- https://onlinelibrary.wiley.com/doi/pdfdirect/10.1002/jcsm.12974
- OA Status
- gold
- Cited By
- 26
- References
- 40
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4221044901
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W4221044901Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.1002/jcsm.12974Digital Object Identifier
- Title
-
A negative feedback loop between fibroadipogenic progenitors and muscle fibres involving endothelin promotes human muscle fibrosisWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2022Year of publication
- Publication date
-
2022-03-22Full publication date if available
- Authors
-
Mona Bensalah, Laura Muraine, Alexis Boulinguiez, Lorenzo Giordani, Victorine Albert, Victor Ythier, Jamila Dhiab, A. Oliver, Valentine Hanique, Teresa Gidaro, Sophie Périé, J. Lacau St-Guily, Aurélien Corneau, Gillian Butler‐Browne, Anne Bigot, Vincent Mouly, Elisa Négroni, Capucine TrolletList of authors in order
- Landing page
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https://doi.org/10.1002/jcsm.12974Publisher landing page
- PDF URL
-
https://onlinelibrary.wiley.com/doi/pdfdirect/10.1002/jcsm.12974Direct link to full text PDF
- Open access
-
YesWhether a free full text is available
- OA status
-
goldOpen access status per OpenAlex
- OA URL
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https://onlinelibrary.wiley.com/doi/pdfdirect/10.1002/jcsm.12974Direct OA link when available
- Concepts
-
Fibrosis, Muscular dystrophy, Myocyte, Biology, Population, Skeletal muscle, Extracellular matrix, Idiopathic pulmonary fibrosis, Transplantation, Medicine, Pathology, Cancer research, Internal medicine, Endocrinology, Cell biology, Lung, Environmental healthTop concepts (fields/topics) attached by OpenAlex
- Cited by
-
26Total citation count in OpenAlex
- Citations by year (recent)
-
2025: 5, 2024: 6, 2023: 7, 2022: 8Per-year citation counts (last 5 years)
- References (count)
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40Number of works referenced by this work
- Related works (count)
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10Other works algorithmically related by OpenAlex
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| citation_normalized_percentile.value | 0.89701413 |
| citation_normalized_percentile.is_in_top_1_percent | False |
| citation_normalized_percentile.is_in_top_10_percent | True |