Generation of craniofacial myogenic progenitor cells from human induced pluripotent stem cells for skeletal muscle tissue regeneration

Janssen, 1985, Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr, J. Appl. Physiol., 89, 81, 10.1152/jappl.2000.89.1.81 Randolph, 2015, A muscle stem cell for every muscle: variability of satellite cell biology among different muscle groups, Front. Aging Neurosci., 7, 190, 10.3389/fnagi.2015.00190 Sambasivan, 2007, 870 Buckingham, 2003, The formation of skeletal muscle: from somite to limb, J. Anat., 202, 59, 10.1046/j.1469-7580.2003.00139.x Lescroart, 2010, Clonal analysis reveals common lineage relationships between head muscles and second heart field derivatives in the mouse embryo, Development, 137, 3269, 10.1242/dev.050674 Tirosh-Finkel, 2006, Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract, Development, 133, 1943, 10.1242/dev.02365 Relaix, 2005, A Pax3/Pax7-dependent population of skeletal muscle progenitor cells, Nature, 435, 948, 10.1038/nature03594 Sambasivan, 2009, Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates, Dev. Cell, 16, 810, 10.1016/j.devcel.2009.05.008 Zammit, 2017, Function of the myogenic regulatory factors Myf5, MyoD, Myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis, Semin. Cell Dev. Biol., 72, 19, 10.1016/j.semcdb.2017.11.011 Ganassi, 2018, Myogenin promotes myocyte fusion to balance fibre number and size, Nat. Commun., 9, 4232, 10.1038/s41467-018-06583-6 Bottinelli, 1994, Myofibrillar ATPase activity during isometric contraction and isomyosin composition in rat single skinned muscle fibres, J. Physiol., 481, 663, 10.1113/jphysiol.1994.sp020472 Bottinelli, 1991, Force-velocity relations and myosin heavy chain isoform compositions of skinned fibres from rat skeletal muscle, J. Physiol., 437, 655, 10.1113/jphysiol.1991.sp018617 Lim, 2006, Postnatal development of myosin heavy chain isoforms in rat extraocular muscles, Mol. Vis., 12, 243 Randolph, 2014, Ageing and muscular dystrophy differentially affect murine pharyngeal muscles in a region-dependent manner, J. Physiol., 592, 5301, 10.1113/jphysiol.2014.280420 Rossi, 2010, Two novel/ancient myosins in mammalian skeletal muscles: MYH14/7b and MYH15 are expressed in extraocular muscles and muscle spindles, J. Physiol., 588, 353, 10.1113/jphysiol.2009.181008 Wieczorek, 1985, Co-expression of multiple myosin heavy chain genes, in addition to a tissue-specific one, in extraocular musculature, J. Cell Biol., 101, 618, 10.1083/jcb.101.2.618 Zhou, 2010, Myosin heavy chain expression in mouse extraocular muscle: more complex than expected, Invest. Ophthalmol. Vis. Sci., 51, 6355, 10.1167/iovs.10-5937 Zhou, 2011, Pitx2 regulates myosin heavy chain isoform expression and multi-innervation in extraocular muscle, J. Physiol., 589, 4601, 10.1113/jphysiol.2011.207076 Mauro, 1961, Satellite cell of skeletal muscle fibers, J. Biophys. Biochem. Cytol., 9, 493, 10.1083/jcb.9.2.493 Lepper, 2011, An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration, Development, 138, 3639, 10.1242/dev.067595 Sambasivan, 2011, Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration, Development, 138, 3647, 10.1242/dev.067587 Murphy, 2011, Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration, Development, 138, 3625, 10.1242/dev.064162 Seale, 2000, Pax7 is required for the specification of myogenic satellite cells, Cell, 102, 777, 10.1016/S0092-8674(00)00066-0 Hacker, 1998, A distinct developmental programme for the cranial paraxial mesoderm in the chick embryo, Development, 125, 3461, 10.1242/dev.125.17.3461 Nogueira, 2015, The emergence of Pax7-expressing muscle stem cells during vertebrate head muscle development, Front. Aging Neurosci., 7, 62, 10.3389/fnagi.2015.00062 Hebert, 2013, The role of Pitx2 in maintaining the phenotype of myogenic precursor cells in the extraocular muscles, PloS One, 8, 10.1371/journal.pone.0058405 Randolph, 2015, Pharyngeal satellite cells undergo myogenesis under basal conditions and are required for pharyngeal muscle maintenance, Stem Cell., 33, 3581, 10.1002/stem.2098 Stuelsatz, 2015, Extraocular muscle satellite cells are high performance myo-engines retaining efficient regenerative capacity in dystrophin deficiency, Dev. Biol., 397, 31, 10.1016/j.ydbio.2014.08.035 Hosoyama, 2012, Applications of skeletal muscle progenitor cells for neuromuscular diseases, Am. J. Stem Cells, 1, 253 Park, 2008, Disease-specific induced pluripotent stem cells, Cell, 134, 877, 10.1016/j.cell.2008.07.041 Jiwlawat, 2018, Current progress and challenges for skeletal muscle differentiation from human pluripotent stem cells using transgene-free approaches, Stem Cell. Int., 2018 Young, 2016, A single CRISPR-Cas9 deletion strategy that targets the majority of DMD patients restores dystrophin function in hiPSC-derived muscle cells, Cell Stem Cell, 18, 533, 10.1016/j.stem.2016.01.021 Hicks, 2018, ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs, Nat. Cell Biol., 20, 46, 10.1038/s41556-017-0010-2 Emery, 2002, Muscular dystrophy into the new millennium, Neuromuscul. Disord., 12, 343, 10.1016/S0960-8966(01)00303-0 Shelton, 2014, Derivation and expansion of PAX7-positive muscle progenitors from human and mouse embryonic stem cells, Stem Cell Rep., 3, 516, 10.1016/j.stemcr.2014.07.001 Shelton, 2016, Robust generation and expansion of skeletal muscle progenitors and myocytes from human pluripotent stem cells, Methods, 101, 73, 10.1016/j.ymeth.2015.09.019 Chal, 2016, Generation of human muscle fibers and satellite-like cells from human pluripotent stem cells in vitro, Nat. Protoc., 11, 1833, 10.1038/nprot.2016.110 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method, Methods, 25, 402, 10.1006/meth.2001.1262 Pavlath, 1996, 307 Zhang, 2008, Short-term BMP-4 treatment initiates mesoderm induction in human embryonic stem cells, Blood, 111, 1933, 10.1182/blood-2007-02-074120 Jang, 2008, Notch inhibition promotes human embryonic stem cell‐derived cardiac mesoderm differentiation, Stem Cell., 26, 2782, 10.1634/stemcells.2007-1053 Ryan, 2012, Retinoic acid enhances skeletal myogenesis in human embryonic stem cells by expanding the premyogenic progenitor population, Stem Cell Rev. Rep., 8, 482, 10.1007/s12015-011-9284-0 Buckingham, 2014, Gene regulatory networks and transcriptional mechanisms that control myogenesis, Dev. Cell, 28, 225, 10.1016/j.devcel.2013.12.020 Chan, 2016, Development of bipotent cardiac/skeletal myogenic progenitors from MESP1+ mesoderm, Stem cell Rep., 6, 26, 10.1016/j.stemcr.2015.12.003 Morita, 2007, Expression and function of the HNK-1 carbohydrate, J. Biochem., 143, 719, 10.1093/jb/mvm221 Borchin, 2013, Derivation and FACS-mediated purification of PAX3+/PAX7+ skeletal muscle precursors from human pluripotent stem cells, Stem cell Rep., 1, 620, 10.1016/j.stemcr.2013.10.007 Lindsley, 2006, Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm, Development, 133, 3787, 10.1242/dev.02551 Gadue, 2006, Wnt and TGF-β signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells, Proc. Natl. Acad. Sci. Unit. States Am., 103, 16806, 10.1073/pnas.0603916103 Nakanishi, 2009, Directed induction of anterior and posterior primitive streak by Wnt from embryonic stem cells cultured in a chemically defined serum-free medium, Faseb. J., 23, 114, 10.1096/fj.08-111203 Sumi, 2008, Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/β-catenin, Activin/Nodal and BMP signaling, Development, 135, 2969, 10.1242/dev.021121 Chal, 2018, Recapitulating early development of mouse musculoskeletal precursors of the paraxial mesoderm in vitro, Development, 145, dev157339, 10.1242/dev.157339 Kim, 2017, Expansion and purification are critical for the therapeutic application of pluripotent stem cell-derived myogenic progenitors, Stem cell Rep., 9, 12, 10.1016/j.stemcr.2017.04.022 Tonegawa, 1997, Mesodermal subdivision along the mediolateral axis in chicken controlled by different concentrations of BMP-4, Development, 124, 1975, 10.1242/dev.124.10.1975 Den Hartogh, 2016, A comprehensive gene expression analysis at sequential stages of in vitro cardiac differentiation from isolated MESP1-expressing-mesoderm progenitors, Sci. Rep., 6, 19386, 10.1038/srep19386 Giacomelli, 2017, Three-dimensional cardiac microtissues composed of cardiomyocytes and endothelial cells co-differentiated from human pluripotent stem cells, Development, 144, 1008, 10.1242/dev.143438 Razy-Krajka, 2014, Collier/OLF/EBF-dependent transcriptional dynamics control pharyngeal muscle specification from primed cardiopharyngeal progenitors, Dev. Cell, 29, 263, 10.1016/j.devcel.2014.04.001 Grifone, 2007, Heartening news for head muscle development, Trends Genet., 23, 365, 10.1016/j.tig.2007.05.002 von Scheven, 2006, Neural tube derived signals and Fgf8 act antagonistically to specify eye versus mandibular arch muscles, Development, 133, 2731, 10.1242/dev.02426 Harel, 2009, Distinct origins and genetic programs of head muscle satellite cells, Dev. Cell, 16, 822, 10.1016/j.devcel.2009.05.007 Chan, 2013, Mesp1 patterns mesoderm into cardiac, hematopoietic, or skeletal myogenic progenitors in a context-dependent manner, Cell stem cell, 12, 587, 10.1016/j.stem.2013.03.004 Bondue, 2008, Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification, Cell stem cell, 3, 69, 10.1016/j.stem.2008.06.009 Shih, 2007, Cranial muscle defects of Pitx2 mutants result from specification defects in the first branchial arch, Proc. Natl. Acad. Sci. Unit. States Am., 104, 5907, 10.1073/pnas.0701122104 Kelly, 2004, The del22q11. 2 candidate gene Tbx1 regulates branchiomeric myogenesis, Hum. Mol. Genet., 13, 2829, 10.1093/hmg/ddh304 Lu, 2002, Control of facial muscle development by MyoR and capsulin, Science, 298, 2378, 10.1126/science.1078273 Cusella-De Angelis, 1994, Differential response of embryonic and fetal myoblasts to TGF beta: a possible regulatory mechanism of skeletal muscle histogenesis, Development, 120, 925, 10.1242/dev.120.4.925 Sakai-Takemura, 2018, Premyogenic progenitors derived from human pluripotent stem cells expand in floating culture and differentiate into transplantable myogenic progenitors, Sci. Rep., 8, 6555, 10.1038/s41598-018-24959-y Schwartzentruber, 2018, Molecular and functional variation in iPSC-derived sensory neurons, Nat. Genet., 50, 54, 10.1038/s41588-017-0005-8 Sayed, 2016, Translation of human-induced pluripotent stem cells: from clinical trial in a dish to precision medicine, J. Am. Coll. Cardiol., 67, 2161, 10.1016/j.jacc.2016.01.083 Pashos, 2017, Large, diverse population cohorts of hiPSCs and derived hepatocyte-like cells reveal functional genetic variation at blood lipid-associated loci, Cell stem cell, 20, 558, 10.1016/j.stem.2017.03.017 Nandkishore, 2018, Divergent early mesoderm specification underlies distinct head and trunk muscle programmes in vertebrates, Development, 145, 10.1242/dev.160945