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@ARTICLE{Shahriyari:165318,
author = {Shahriyari, Mina and Islam, Rezaul and Sakib, Sadman M and
Rinn, Malte and Rika, Anastasia and Krüger, Dennis and
Kaurani, Lalit and Gisa, Verena and Winterhoff, Mandy and
Anandakumar, Harithaa and Shomroni, Orr and Schmidt,
Matthias and Salinas, Gabriela and Unger, Andreas and Linke,
Wolfgang A and Zschüntzsch, Jana and Schmidt, Jens and
Bassel-Duby, Rhonda and Olson, Eric N and Fischer, André
and Zimmermann, Wolfram-Hubertus and Tiburcy, Malte},
title = {{E}ngineered skeletal muscle recapitulates human muscle
development, regeneration and dystrophy.},
journal = {Journal of cachexia, sarcopenia and muscle},
volume = {13},
number = {6},
issn = {2190-5991},
address = {Hoboken, NJ},
publisher = {Wiley},
reportid = {DZNE-2022-01596},
pages = {3106-3121},
year = {2022},
abstract = {Human pluripotent stem cell-derived muscle models show
great potential for translational research. Here, we
describe developmentally inspired methods for the derivation
of skeletal muscle cells and their utility in skeletal
muscle tissue engineering with the aim to model skeletal
muscle regeneration and dystrophy in vitro.Key steps include
the directed differentiation of human pluripotent stem cells
to embryonic muscle progenitors followed by primary and
secondary foetal myogenesis into three-dimensional muscle.
To simulate Duchenne muscular dystrophy (DMD), a
patient-specific induced pluripotent stem cell line was
compared to a CRISPR/Cas9-edited isogenic control line.The
established skeletal muscle differentiation protocol
robustly and faithfully recapitulates critical steps of
embryonic myogenesis in two-dimensional and
three-dimensional cultures, resulting in functional human
skeletal muscle organoids (SMOs) and engineered skeletal
muscles (ESMs) with a regeneration-competent satellite-like
cell pool. Tissue-engineered muscle exhibits organotypic
maturation and function (up to 5.7 ± 0.5 mN tetanic twitch
tension at 100 Hz in ESM). Contractile performance could be
further enhanced by timed thyroid hormone treatment,
increasing the speed of contraction (time to peak
contraction) as well as relaxation (time to $50\%$
relaxation) of single twitches from 107 ± 2 to 75 ± 4 ms
(P < 0.05) and from 146 ± 6 to 100 ± 6 ms (P < 0.05),
respectively. Satellite-like cells could be documented as
largely quiescent PAX7+ cells (75 ± $6\%$ Ki67- ) located
adjacent to muscle fibres confined under a
laminin-containing basal membrane. Activation of the
engineered satellite-like cell niche was documented in a
cardiotoxin injury model with marked recovery of
contractility to 57 ± $8\%$ of the pre-injury force 21 days
post-injury (P < 0.05 compared to Day 2 post-injury), which
was completely blocked by preceding irradiation. Absence of
dystrophin in DMD ESM caused a marked reduction of
contractile force (-35 ± $7\%,$ P < 0.05) and impaired
expression of fast myosin isoforms resulting in prolonged
contraction (175 ± 14 ms, P < 0.05 vs. gene-edited control)
and relaxation (238 ± 22 ms, P < 0.05 vs. gene-edited
control) times. Restoration of dystrophin levels by gene
editing rescued the DMD phenotype in ESM.We introduce human
muscle models with canonical properties of bona fide
skeletal muscle in vivo to study muscle development,
maturation, disease and repair.},
keywords = {Humans / Muscular Dystrophy, Duchenne: genetics / Muscle,
Skeletal: metabolism / Muscle Development: genetics /
Satellite Cells, Skeletal Muscle: metabolism / Muscle
Fibers, Skeletal: metabolism / Duchenne muscular dystrophy
(Other) / hypaxial dermomyotome (Other) / limb muscle
(Other) / satellite cells (Other) / skeletal muscle organoid
(Other) / somite (Other) / tissue engineering (Other)},
cin = {AG Fischer 1 / Bioinformatics and Genome Dynamics Core},
ddc = {610},
cid = {I:(DE-2719)1410002 / I:(DE-2719)1440016},
pnm = {352 - Disease Mechanisms (POF4-352)},
pid = {G:(DE-HGF)POF4-352},
typ = {PUB:(DE-HGF)16},
pmc = {pmc:PMC9745484},
pubmed = {pmid:36254806},
doi = {10.1002/jcsm.13094},
url = {https://pub.dzne.de/record/165318},
}