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Cited by 32Muscle Physiology and DisordersCellular transport and secretionCaveolin-1 and cellular processes

Sarcolemma wounding activates dynamin‐dependent endocytosis in striated muscle

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McDade, Joel R., Naylor, Molly T., Michele, Daniel E.·2021·The FEBS Journal
DOI 10.1111/febs.15556PMC PMC9720729
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Abstract

Plasma membrane repair is an evolutionarily conserved mechanism by which cells can seal breaches in the plasma membrane. Mutations in several proteins with putative roles in sarcolemma integrity, membrane repair, and membrane transport result in several forms of muscle disease; however, the mechanisms that are activated and responsible for sarcolemma resealing are not well understood. Using the standard assays for membrane repair, which track the uptake of FM 1‐43 dye into adult skeletal muscle fibers following laser‐induced sarcolemma disruption, we show that labeling of resting fibers by FM1‐43 prior to membrane wounding and the induced FM1‐43 dye uptake after sarcolemma wounding occurs via dynamin‐dependent endocytosis. Dysferlin‐deficient muscle fibers show elevated dye uptake following wounding, which is the basis for the assertion that membrane repair is defective in this model. Our data show that dynamin inhibition mitigates the differences in FM1‐43 dye uptake between dysferlin‐null and wild‐type muscle fibers, suggesting that elevated wound‐induced FM1‐43 uptake in dysferlin‐deficient muscle may actually be due to enhanced dynamin‐dependent endocytosis following wounding, though dynamin inhibition had no effect on dysferlin trafficking after wounding. By monitoring calcium flux after membrane wounding, we show that reversal of calcium precedes the sustained, slower increase of dynamin‐dependent FM1‐43 uptake in WT fibers, and that dysferlin‐deficient muscle fibers have persistently increased calcium after wounding, consistent with its proposed role in resealing. These data highlight a previously unappreciated role for dynamin‐dependent endocytosis in wounded skeletal muscle fibers and identify overactive dynamin‐dependent endocytosis following sarcolemma wounding as a potential mechanism or consequence of dysferlin deficiency.

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  • Paralogue dynamin-2 participates in membrane repair by wound-induced endocytosis in skeletal muscle.

    “Interestingly, the paralog dynamin-2 participates in membrane repair by wound-induced endocytosis in skeletal muscle45, which may point to a convergence of mechanisms with DYSF.”

    From Locus for severity implicates CNS resilience in progression of multiple sclerosis (2023) · cites this paper as [45]

    The Introduction reports that wounding stimulates dynamin-dependent endocytosis in adult skeletal muscle fibers and identifies dynamin-2 as an isoform highly expressed in that muscle. But the Discussion says it remains unclear whether wound-induced endocytosis contributes to membrane resealing or is a detrimental consequence of wounding. The claim presents participation in repair as established when the paper describes it as a potential role. (LLM, conf=0.88)

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Authors
McDade, J. R., Naylor, M. T., & Michele, D. E.
Affiliations
University of Michigan (US)
Corresponding author
Michele, Daniel E.
ORCID
Venue
The FEBS Journal
Publisher
Wiley
Published
2020-09-25
Volume
288
Issue
1
Pages
160-174
ISSN
  • 1742-464X (ISSN-L)
  • 1742-4658
DOI
10.1111/febs.15556
PMC
PMC9720729
OpenAlex
W3083108491
Cited by
32
References
40
Citations by year
2026: 4 · 2025: 5 · 2024: 11 · 2023: 5 · 2022: 6 · 2021: 1
FWCI
0.97
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • FEBS Journal (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • Deep Blue (University of Michigan) (submittedVersion)
Funders
  • American Heart Association (12PRE12050130)
  • National Institutes of Health (AR066213, AR068428, GM007315, HL125242)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
Keywords
dynamin-dependent endocytosis, plasma membrane repair, dysferlin deficiency, skeletal muscle, calcium flux, myopathy
MeSH terms
Dysferlin, Quaternary Ammonium Compounds, Animals, Calcium, Dimethyl Sulfoxide, Endocytosis, Fluorescent Dyes, Gene Expression Regulation, Hydrazones, Mice, Inbred C57BL, Pyridinium Compounds, Sarcolemma, Staining and Labeling, Muscle Fibers, Skeletal, Animals, Genetically Modified, Dynamins, Green Fluorescent Proteins, Mice

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