Preloader

Skeletal muscle differentiation of human iPSCs meets bioengineering strategies: perspectives and challenges

  • Fu, X., Wang, H. & Hu, P. Stem cell activation in skeletal muscle regeneration. Cell. Mol. Life Sci. 72, 1663–1677 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nowak, K. J. & Davies, K. E. Duchenne muscular dystrophy and dystrophin: pathogenesis and opportunities for treatment. EMBO Rep. 5, 872–876 (2004).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Grogan, B. F. & Hsu, M. A. J. J. R. Volumetric Muscle Loss. J. Am. Acad. Orthop. Surg. 19, 35–37 (2011).

    Google Scholar 

  • Osaki, T., Uzel, S. G. M. & Kamm, R. D. On-chip 3D neuromuscular model for drug screening and precision medicine in neuromuscular disease. Nat. Protoc. 15, 421–449 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Takahashi, K. & Yamanaka, S. Induction of pluripotent stem. Cells Mouse Embryonic Adult Fibroblast Cult. Defined Factors Cell 126, 663–676 (2006).

    CAS 

    Google Scholar 

  • Sato, T. Induction of skeletal muscle progenitors and stem cells from human induced pluripotent stem cells. J. Neuromuscul. Dis. 7, 395–405 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • del Carmen Ortuño-Costela, M. et al. iPSCs: a powerful tool for skeletal muscle tissue engineering. J. Cell. Mol. Med. 23, 3784–3794 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Jiwlawat, N., Lynch, E., Jeffrey, J., Van Dyke, J. M. & Suzuki, M. Current progress and challenges for skeletal muscle differentiation from human pluripotent stem cells using transgene-free approaches. Stem Cells Int 2018, 1–18 (2018).

    Google Scholar 

  • Kodaka, Y., Rabu, G. & Asakura, A. Skeletal muscle cell induction from pluripotent stem cells. Stem Cells Int 2017, 1–16 (2017).

    Google Scholar 

  • Khodabukus, A., Prabhu, N., Wang, J. & Bursac, N. In vitro tissue-engineered skeletal muscle models for studying muscle physiology and disease. Adv. Healthc. Mater. 7, e1701498 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Darabi, R. et al. Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 10, 610–619 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tedesco, F. S. et al. Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Sci. Transl. Med. 4, 140ra89 (2012).

    PubMed 

    Google Scholar 

  • Tanaka, A. et al. Efficient and reproducible myogenic differentiation from human iPS cells: prospects for modeling miyoshi myopathy in vitro. PLoS One 8, e61540 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Quattrocelli, M. et al. Mesodermal iPSC-derived progenitor cells functionally regenerate cardiac and skeletal muscle. J. Clin. Invest 125, 4463–4482 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Rao, L., Qian, Y., Khodabukus, A., Ribar, T. & Bursac, N. Engineering human pluripotent stem cells into a functional skeletal muscle tissue. Nat. Commun. 9, 126 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Awaya, T. et al. Selective development of myogenic mesenchymal cells from human embryonic and induced pluripotent stem cells. PLoS ONE 7, e51638 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sakai-Takemura, F. et al. Premyogenic progenitors derived from human pluripotent stem cells expand in floating culture and differentiate into transplantable myogenic progenitors. Sci. Rep. 8, 6555 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • van der Wal, E. et al. Large-scale expansion of human iPSC-derived skeletal muscle cells for disease modeling and cell-based therapeutic strategies. Stem cell Rep. 10, 1975–1990 (2018).

    Google Scholar 

  • Baci, D. et al. Extracellular vesicles from skeletal muscle cells efficiently promote myogenesis in induced pluripotent stem cells. Cells 9, 1527 (2020).

    PubMed Central 

    Google Scholar 

  • He, R. et al. Engraftment of human induced pluripotent stem cell-derived myogenic progenitors restores dystrophin in mice with duchenne muscular dystrophy. Biol. Res. 53, 22 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Maffioletti, S. M. et al. Three-dimensional human iPSC-derived artificial skeletal muscles model muscular dystrophies and enable multilineage tissue engineering. Cell Rep. 23, 899–908 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Selvaraj, S. & Perlingeiro, R. C. R. Induced pluripotent stem cells for neuromuscular diseases: potential for disease modeling, drug screening, and regenerative medicine. 13, 471–481 (2019).

  • Madden, L., Juhas, M., Kraus, W. E., Truskey, G. A. & Bursac, N. Bioengineered human myobundles mimic clinical responses of skeletal muscle to drugs. Elife 2015, e04885 (2015).

    Google Scholar 

  • Abujarour, R. et al. Myogenic differentiation of muscular dystrophy-specific induced pluripotent stem cells for use in drug discovery. Stem Cells Transl. Med 3, 149–160 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Shoji, E. et al. Early pathogenesis of Duchenne muscular dystrophy modelled in patient-derived human induced pluripotent stem cells. Sci. Rep. 5, 1−13 (2015).

  • Lenzi, J. et al. Differentiation of control and ALS mutant human iPSCs into functional skeletal muscle cells, a tool for the study of neuromuscolar diseases. Stem Cell Res 17, 140–147 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ricotti, L. et al. Biohybrid actuators for robotics: a review of devices actuated by living cells. Sci. Robot. 2, eaaq0495 (2017).

    PubMed 

    Google Scholar 

  • Piga, D. et al. Human induced pluripotent stem cell models for the study and treatment of Duchenne and Becker muscular dystrophies. Ther. Adv. Neurol. Disord. 12, 1–28 (2019).

    Google Scholar 

  • Nogami, K., Blanc, M., Takemura, F., Takeda, S. & Miyagoe-Suzuki, Y. Making Skeletal Muscle from Human Pluripotent Stem Cells. Muscle Cell and Tissue – Current Status of Research Field (2018).

  • Jiwlawat, N. et al. Micropatterned substrates with physiological stiffness promote cell maturation and Pompe disease phenotype in human induced pluripotent stem cell-derived skeletal myocytes. Biotechnol. Bioeng. 116, 2377–2392 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Watt, F. M. & Hogan, B. L. M. Out of eden: Stem cells and their niches. Science 287, 1427–1430 (2000).

    CAS 
    PubMed 

    Google Scholar 

  • Ricotti, L. & Menciassi, A. Engineering stem cells for future medicine. IEEE Trans. Biomed. Eng. 60, 727–734 (2013).

    PubMed 

    Google Scholar 

  • Maleiner, B. et al. The importance of biophysical and biochemical stimuli in dynamic skeletal muscle models. Front. Physiol. 9, 1130 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689 (2006).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chal, J. & Pourquié, O. Making muscle: skeletal myogenesis in vivo and in vitro. Development 144, 2104–2122 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Buckingham, M. Skeletal muscle formation in vertebrates. Curr. Opin. Genet. Dev. 11, 440–448 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • Bentzinger, C. F., Wang, Y. X. & Rudnicki, M. A. Building muscle: molecular regulation of myogenesis. Cold Spring Harb. Perspect. Biol. 4, a008342 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Sakuma, K. The Plasticity of Skeletal Muscle: From Molecular Mechanism to Clinical Applications. (Springer Singapore, 2017).

  • Pownall, M. E., Gustafsson, M. K. & Emerson, C. P. J. Myogenic Regulatory Factors and the Specification of Muscle Progenitors in Vertebrate Embryos. Annu. Rev. Cell Dev. Biol. 18, 747–783 (2003).

    Google Scholar 

  • Sato, Y. Dorsal aorta formation: separate origins, lateral-to-medial migration, and remodeling. Dev. Growth Differ. 55, 113–129 (2013).

    PubMed 

    Google Scholar 

  • Purslow, P. P. The structure and role of intramuscular connective tissue in muscle function. Front. Physiol. 11, 495 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Gillies, A. R. & Lieber, R. L. Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve 44, 318–331 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Csapo, R., Gumpenberger, M. & Wessner, B. Skeletal muscle extracellular matrix – what do we know about its composition, regulation, and physiological roles? a narrative review. Front. Physiol. 11, 253 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Armulik, A., Genové, G. & Betsholtz, C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Developmental Cell 21, 193–215 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • Stifani, N. Motor neurons and the generation of spinal motor neuron diversity. Front. Cell. Neurosci. 8, 293 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Selvaraj, S. et al. Screening identifies small molecules that enhance the maturation of human pluripotent stem cell-derived myotubes. Elife 8, (2019).

  • Constantinides, P. G., Jones, P. A. & Gevers, W. Functional striated muscle cells from non-myoblast precursors following 5-azacytidine treatment. Nature 267, 364–366 (1977).

    CAS 
    PubMed 

    Google Scholar 

  • Davis, R. L., Weintraub, H. & Lassar, A. B. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51, 987–1000 (1987).

    CAS 
    PubMed 

    Google Scholar 

  • Nabeshima, Y. et al. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532–535 (1993).

    CAS 
    PubMed 

    Google Scholar 

  • Albini, S. et al. Epigenetic reprogramming of human embryonic stem cells into skeletal muscle cells and generation of contractile myospheres. Cell Rep. 3, 661–670 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Uchimura, T., Otomo, J., Sato, M. & Sakurai, H. A human iPS cell myogenic differentiation system permitting high-throughput drug screening. Stem Cell Res 25, 98–106 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Pettinato, G., Wen, X. & Zhang, N. Formation of well-defined embryoid bodies from dissociated human induced pluripotent stem cells using microfabricated cell-repellent microwell arrays. Sci. Rep. 4, 1–11 (2014). 2014 41.

    Google Scholar 

  • Rungarunlert, S., Techakumphu, M., Pirity, M. K. & Dinnyes, A. Embryoid body formation from embryonic and induced pluripotent stem cells: Benefits of bioreactors. World J. Stem Cells 1, 11 (2009).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Sato, T. et al. Core transcription factors promote induction of PAX3-positive skeletal muscle stem cells. Stem cell Rep. 13, 352–365 (2019).

    CAS 

    Google Scholar 

  • Magli, A. et al. PAX7 Targets, CD54, Integrin α9β1 and SDC2, Allow Isolation of Human ES/iPS Cell-Derived Myogenic Progenitors. Cell Rep. 19, 2867 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Warren, L. et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7, 618–630 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mizuno, Y. et al. Generation of skeletal muscle stem/progenitor cells from murine induced pluripotent stem cells. FASEB J. Publ. Fed. Am. Soc. Exp. Biol. 24, 2245–2253 (2010).

    CAS 

    Google Scholar 

  • Shelton, M., Kocharyan, A., Liu, J., Skerjanc, I. S. & Stanford, W. L. Robust generation and expansion of skeletal muscle progenitors and myocytes from human pluripotent stem cells. Methods 101, 73–84 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Chal, J. et al. Recapitulating early development of mouse musculoskeletal precursors of the paraxial mesoderm in vitro. Development 145, dev157339 (2018).

  • Swartz, E. W. et al. A novel protocol for directed differentiation of C9orf72-associated human induced pluripotent stem cells into contractile skeletal myotubes. Stem Cells Transl. Med 5, 1461–1472 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Iovino, S., Burkart, A. M., Warren, L., Patti, M. E. & Kahn, C. R. Myotubes derived from human-induced pluripotent stem cells mirror in vivo insulin resistance. Proc. Natl Acad. Sci. U. S. A. 113, 1889–1894 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chal, J. et al. Generation of human muscle fibers and satellite-like cells from human pluripotent stem cells in vitro. Nat. Protoc. 11, 1833–1850 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Hosoyama, T., McGivern, J. V., Van Dyke, J. M., Ebert, A. D. & Suzuki, M. Derivation of myogenic progenitors directly from human pluripotent stem cells using a sphere-based culture. Stem Cells Transl. Med 3, 564–574 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tey, S.-R., Robertson, S., Lynch, E. & Suzuki, M. Coding cell identity of human skeletal muscle progenitor cells using cell surface markers: current status and remaining challenges for characterization and isolation. Front. Cell Dev. Biol. 0, 284 (2019).

    Google Scholar 

  • Hicks, M. R. et al. ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs. Nat. Cell Biol. 20, 46–57 (2018).

  • Nalbandian, M. et al. Characterization of hiPSC-derived muscle progenitors reveals distinctive markers for myogenic cell purification toward cell therapy. Stem cell Rep. 16, 883–898 (2021).

    CAS 

    Google Scholar 

  • Al Tanoury, Z. et al. Differentiation of the human PAX7-positive myogenic precursors/satellite cell lineage in vitro. Dev 147, dev187344 (2020).

    CAS 

    Google Scholar 

  • Rocheteau, P., Gayraud-Morel, B., Siegl-Cachedenier, I., Blasco, M. A. & Tajbakhsh, S. A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 148, 112–125 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • SS, C. et al. Skeletal muscle stem cells from PSC-derived teratomas have functional regenerative capacity. Cell Stem Cell 23, 74–85.e6 (2018).

    Google Scholar 

  • Iberite, F. et al. Combined effects of electrical stimulation and protein coatings on myotube formation in a soft porous scaffold. Ann. Biomed. Eng. 48, 734–746 (2020).

    PubMed 

    Google Scholar 

  • Khodabukus, A. et al. Electrical stimulation increases hypertrophy and metabolic flux in tissue-engineered human skeletal muscle. Biomaterials 198, 259–269 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Hasebe, A. et al. Biohybrid actuators based on skeletal muscle-powered microgrooved ultrathin films consisting of poly(styrene- block-butadiene- block-styrene). ACS Biomater. Sci. Eng. 5, 5734–5743 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Mueller, C. et al. Effects of External Stimulators on Engineered Skeletal Muscle Tissue Maturation. Adv. Mater. Interfaces 8, 2001167 (2020).

    Google Scholar 

  • Ma, R. et al. Electrical stimulation enhances cardiac differentiation of human induced pluripotent stem cells for myocardial infarction therapy. Antioxid. Redox Signal 28, 371–384 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ruan, J. L. et al. Mechanical stress conditioning and electrical stimulation promote contractility and force maturation of induced pluripotent stem cell-derived human cardiac tissue. Circulation 134, 1557–1567 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hernández, D. et al. Electrical stimulation promotes cardiac differentiation of human induced pluripotent stem cells. Stem Cells Int. 2016, 1718041 (2016).

  • Yamada, M. et al. Electrical stimulation modulates fate determination of differentiating embryonic stem cells. Stem Cells 25, 562–570 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • Merrill, D. R., Bikson, M. & Jefferys, J. G. R. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J. Neurosci. Methods 141, 171–198 (2005).

    PubMed 

    Google Scholar 

  • Zheng, X. S., Tan, C., Castagnola, E. & Cui, X. T. Electrode materials for chronic electrical microstimulation. Adv. Healthc. Mater. 10, 2100119 (2021).

    CAS 

    Google Scholar 

  • Stewart, D. M. The role of tension in muscle growth. in Regulation of Organ and Tissue Growth. 77–100 (New York: Associated Press, 1972).

  • Orr, A. W., Helmke, B. P., Blackman, B. R. & Schwartz, M. A. Mechanisms of mechanotransduction. Developmental Cell 10, 11–20 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Burkholder, T. J. Mechanotransduction in skeletal muscle. Front. Biosci. 12, 174–191 (2007).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Somers, S. M., Spector, A. A., DiGirolamo, D. J. & Grayson, W. L. Biophysical stimulation for engineering functional skeletal muscle. Tissue Eng. Part B Rev. 23, 362–372 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Thomas, C. H., Collier, J. H., Sfeir, C. S. & Healy, K. E. Engineering gene expression and protein synthesis by modulation of nuclear shape. Proc. Natl Acad. Sci. U. S. A. 99, 1972–1977 (2002).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Formigli, L. et al. Cytoskeleton/stretch-activated ion channel interaction regulates myogenic differentiation of skeletal myoblasts. J. Cell. Physiol. 211, 296–306 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • Tidball, J. G. et al. Mechanical loading regulates NOS expression and activity in developing and adult skeletal muscle. Am. J. Physiol. -Cell Physiol. 275, C260–C266 (1998).

    CAS 

    Google Scholar 

  • Bodine, S. C. et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3, 1014–1019 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • De Deyne, P. G. Formation of sarcomeres in developing myotubes: Role of mechanical stretch and contractile activation. Am. J. Physiol. – Cell Physiol. 279, C1801–C1811 (2000).

    PubMed 

    Google Scholar 

  • Heher, P. et al. A novel bioreactor for the generation of highly aligned 3D skeletal muscle-like constructs through orientation of fibrin via application of static strain. Acta Biomater. 24, 251–265 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Juhas, M. & Bursac, N. Roles of adherent myogenic cells and dynamic culture in engineered muscle function and maintenance of satellite cells. Biomaterials 35, 9438–9446 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wang, Y. et al. Multiple effects of mechanical stretch on myogenic progenitor cells. Stem Cells Dev. 29, 336–352 (2020).

    PubMed 

    Google Scholar 

  • Bursac, N., Juhas, M. & Rando, T. A. Synergizing engineering and biology to treat and model skeletal muscle injury and disease. Annu. Rev. Biomed. Eng. 17, 217–242 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Vandenburgh, H. H. & Karlisch, P. Longitudinal growth of skeletal myotubes in vitro in a new horizontal mechanical cell stimulator. Vitr. Cell. Dev. Biol. 25, 607–616 (1989).

    CAS 

    Google Scholar 

  • Powell, C. A., Smiley, B. L., Mills, J. & Vandenburgh, H. H. Mechanical stimulation improves tissue-engineered human skeletal muscle. Am. J. Physiol. Physiol. 283, C1557–C1565 (2002).

    CAS 

    Google Scholar 

  • Candiani, G. et al. Cyclic mechanical stimulation favors myosin heavy chain accumulation in engineered skeletal muscle constructs. J. Appl. Biomater. Biomech. 8, 68–75 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Moon, D. G., Christ, G., Stitzel, J. D., Atala, A. & Yoo, J. J. Cyclic mechanical preconditioning improves engineered muscle contraction. Tissue Eng. – Part A 14, 473–482 (2008).

    CAS 

    Google Scholar 

  • Pennisi, C. P., Olesen, C. G., De Zee, M., Rasmussen, J. & Zachar, V. Uniaxial cyclic strain drives assembly and differentiation of skeletal myocytes. Tissue Eng. – Part A 17, 2543–2550 (2011).

    PubMed 

    Google Scholar 

  • Liao, I.-C., Liu, J. B., Bursac, N. & Leong, K. W. Effect of electromechanical stimulation on the maturation of myotubes on aligned electrospun fibers. Cell. Mol. Bioeng. 1, 133 (2008).

    CAS 
    PubMed 

    Google Scholar 

  • Teramura, T. et al. Mechanical stimulation of cyclic tensile strain induces reduction of pluripotent related gene expressions via activation of Rho/ROCK and subsequent decreasing of AKT phosphorylation in human induced pluripotent stem cells. Biochem. Biophys. Res. Commun. 417, 836–841 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Czaplewski, S. K., Tsai, T. L., Duenwald-Kuehl, S. E., Vanderby, R. & Li, W. J. Tenogenic differentiation of human induced pluripotent stem cell-derived mesenchymal stem cells dictated by properties of braided submicron fibrous scaffolds. Biomaterials 35, 6907–6917 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Geuss, L. R. & Suggs, L. J. Making cardiomyocytes: How mechanical stimulation can influence differentiation of pluripotent stem cells. Biotechnol. Prog. 29, 1089–1096 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Kok, H. P. et al. Heating technology for malignant tumors: a review. Int. J. Hyperth. 37, 711–741 (2020).

    CAS 

    Google Scholar 

  • Elhelf, I. A. S. et al. High intensity focused ultrasound: the fundamentals, clinical applications and research trends. Diagnostic Interventional Imaging 99, 349–359 (2018).

    PubMed 

    Google Scholar 

  • Burks, S. R., Lorsung, R. M., Nagle, M. E., Tu, T. W. & Frank, J. A. Focused ultrasound activates voltage-gated calcium channels through depolarizing TRPC1 sodium currents in kidney and skeletal muscle. Theranostics 9, 5517–5531 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Moncion, A. et al. Spatiotemporally-controlled transgene expression in hydroxyapatite-fibrin composite scaffolds using high intensity focused ultrasound. Biomaterials 194, 14–24 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Jiang, X. et al. A review of low-intensity pulsed ultrasound for therapeutic applications. IEEE Trans. Biomed. Eng. 66, 2704–2718 (2019).

    PubMed 

    Google Scholar 

  • Liu, D. D., Ullah, M., Concepcion, W., Dahl, J. J. & Thakor, A. S. The role of ultrasound in enhancing mesenchymal stromal cell-based therapies. Stem Cells Transl. Med 9, 850–866 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Salgarella, A. R. et al. Optimal ultrasound exposure conditions for maximizing C2C12 muscle cell proliferation and differentiation. Ultrasound Med. Biol. 43, 1452–1465 (2017).

    PubMed 

    Google Scholar 

  • Fontana, F. et al. Highly controlled and usable system for Low-Intensity Pulsed Ultrasound Stimulation of Cells. in Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society 2513–2516 (Institute of Electrical and Electronics Engineers (IEEE), 2019).

  • Leskinen, J. J. & Hynynen, K. Study of factors affecting the magnitude and nature of ultrasound exposure with in vitro set-ups. Ultrasound Med. Biol. 38, 777–794 (2012).

    PubMed 

    Google Scholar 

  • Shaw, A. & Ter Haar, G. R. Telling it like it is. J. Ther. Ultrasound 1, 1–2 (2013).

    Google Scholar 

  • Cafarelli, A. et al. Piezoelectric nanomaterials activated by ultrasound: the pathway from discovery to future clinical adoption. ACS Nano 15, 11066–11086 (2021).

    CAS 
    PubMed Central 

    Google Scholar 

  • Lv, Y., Zhao, P., Chen, G., Sha, Y. & Yang, L. Effects of low-intensity pulsed ultrasound on cell viability, proliferation and neural differentiation of induced pluripotent stem cells-derived neural crest stem cells. Biotechnol. Lett. 35, 2201–2212 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Xia, B., Zou, Y., Xu, Z. & Lv, Y. Gene expression profiling analysis of the effects of low-intensity pulsed ultrasound on induced pluripotent stem cell-derived neural crest stem cells. Biotechnol. Appl. Biochem. 64, 927–937 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Xia, B. et al. Low‐intensity pulsed ultrasound combination with induced pluripotent stem cells‐derived neural crest stem cells and growth differentiation factor 5 promotes sciatic nerve regeneration and functional recovery. J. Tissue Eng. Regen. Med. 13, 625–636 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Morey-Holton, E. R. The impact of gravity on life. In Evolution on Planet Earth: The Impact of the Physical Environment 143–159 (Elsevier Ltd, 2003).

  • Clément, G. The Musculo-Skeletal System in Space. In Fundamentals of Space Medicine 181–216 (Springer Science & Business Media, 2011).

  • Cadena, S. M. et al. Skeletal muscle in MuRF1 null mice is not spared in low-gravity conditions, indicating atrophy proceeds by unique mechanisms in space. Sci. Rep. 9, (2019).

  • Slentz, D. H., Truskey, G. A. & Kraus, W. E. Effects of chronic exposure to simulated microgravity on skeletal muscle cell proliferation and differentiation. Vitr. Cell. Dev. Biol. – Anim. 37, 148–156 (2001).

    CAS 

    Google Scholar 

  • Zhou, J. et al. Real microgravity condition promoted regeneration capacity of induced pluripotent stem cells during the TZ‐1 space mission. Cell Prolif. 52, e12574 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Wnorowski, A. et al. Effects of spaceflight on human induced pluripotent stem cell-derived cardiomyocyte structure and function. Stem cell Rep. 13, 960–969 (2019).

    CAS 

    Google Scholar 

  • Tominari, T. et al. Hypergravity and microgravity exhibited reversal effects on the bone and muscle mass in mice. Sci. Rep. 9, 1–10 (2019).

    CAS 

    Google Scholar 

  • Ciofani, G. et al. Hypergravity effects on myoblast proliferation and differentiation. J. Biosci. Bioeng. 113, 258–261 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Acharya, A. et al. Modulation of differentiation processes in murine embryonic stem cells exposed to parabolic flight-induced acute hypergravity and microgravity. Stem Cells Dev. 27, 838–847 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dunn, A. et al. Biomaterial and stem cell‐based strategies for skeletal muscle regeneration. J. Orthop. Res. 37, 1246–1262 (2019).

    PubMed 

    Google Scholar 

  • Discher, D. E., Janmey, P. & Wang, Y.-L. Tissue cells feel and respond to the stiffness of their substrate. Sci. (80-.) 310, 1139–1143 (2005).

    CAS 

    Google Scholar 

  • Gilbert, P. M. et al. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078–1081 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Iberite, F., Salerno, M., Canale, C., Rosa, A. & Ricotti, L. Influence of substrate stiffness on human induced pluripotent stem cells: preliminary results. In Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society 1039–1043 (Institute of Electrical and Electronics Engineers (IEEE), 2019).

  • Ricotti, L. et al. Proliferation and skeletal myotube formation capability of C2C12 and H9c2 cells on isotropic and anisotropic electrospun nanofibrous PHB scaffolds. Biomed. Mater. 7, 035010 (2012).

    PubMed 

    Google Scholar 

  • Xu, B. et al. Nanotopography-responsive myotube alignment and orientation as a sensitive phenotypic biomarker for Duchenne Muscular Dystrophy. Biomaterials 183, 54–66 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sakurai, H. et al. In vitro modeling of paraxial mesodermal progenitors derived from induced pluripotent stem cells. PLoS ONE 7, e47078 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hughes, C. S., Postovit, L. M. & Lajoie, G. A. Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics 10, 1886–1890 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Kim, J. H. et al. 3D bioprinted human skeletal muscle constructs for muscle function restoration. Sci. Rep. 8, 12307 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kim, J. H. et al. Neural cell integration into 3D bioprinted skeletal muscle constructs accelerates restoration of muscle function. Nat. Commun. 11, 1–12 (2020).

    Google Scholar 

  • Khodabukus, A. & Baar, K. Regulating fibrinolysis to engineer skeletal muscle from the C2C12 cell line. Tissue Eng. – Part C. Methods 15, 501–511 (2009).

    CAS 
    PubMed 

    Google Scholar 

  • Cvetkovic, C. et al. Investigating the life expectancy and proteolytic degradation of engineered skeletal muscle biological machines. Sci. Rep. 7, 1–13 (2017).

    CAS 

    Google Scholar 

  • Kang, H. W. et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat. Biotechnol. 34, 312–319 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Zhuang, P., An, J., Chua, C. K. & Tan, L. P. Bioprinting of 3D in vitro skeletal muscle models: A review. Mater. Des. 193, 108794 (2020).

    CAS 

    Google Scholar 

  • Agrawal, A., Raut, A., Bagde, A., Fulzele, P. & Quazi Syed, Z. A mini review on 3-D bioprinting in skeletal muscle tissue engineering. Mater. Today Proc. (2021).

  • Choi, Y. J. et al. A 3D cell printed muscle construct with tissue-derived bioink for the treatment of volumetric muscle loss. Biomaterials 206, 160–169 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Jodat, Y. A. et al. hiPSC-derived 3D Bioprinted Skeletal Muscle Tissue Implants Regenerate Skeletal Muscle Following Volumetric Muscle Loss. Res. Sq. Preprint, (2021).

  • Pantelic, M. N. & Larkin, L. M. Stem cells for skeletal muscle tissue engineering. Tissue Eng. – Part B Rev. 24, 373–391 (2018).

    PubMed 

    Google Scholar 

  • Kim, K. et al. Epigenetic memory in induced pluripotent stem cells. Nature 467, 285–290 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Malik, N. & Rao, M. S. A review of the methods for human iPSC derivation. in Methods in Molecular Biology 997, 23–33 (NIH Public Access, 2013).

  • Huang, C.-Y. et al. Human iPSC banking: barriers and opportunities. J. Biomed. Sci. 26, 1–14 (2019).

    Google Scholar 

  • De Almeida, P. E. et al. Transplanted terminally differentiated induced pluripotent stem cells are accepted by immune mechanisms similar to self-tolerance. Nat. Commun. 5, 3903 (2014).

    PubMed 

    Google Scholar 

  • Hallett, P. J. et al. Successful function of autologous iPSC-derived dopamine neurons following transplantation in a non-human primate model of Parkinson’s disease. Cell Stem Cell 16, 269–274 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Alvarez-Palomo, B. et al. Adapting cord blood collection and banking standard operating procedures for hla-homozygous induced pluripotent stem cells production and banking for clinical application. J. Clin. Med. 8, 476 (2019).

    PubMed Central 

    Google Scholar 

  • Doss, M. X. & Sachinidis, A. Current challenges of iPSC-based disease modeling and therapeutic implications. Cells 8, 403 (2019).

    CAS 
    PubMed Central 

    Google Scholar 

  • Deinsberger, J., Reisinger, D. & Weber, B. Global trends in clinical trials involving pluripotent stem cells: a systematic multi-database analysis. npj Regen. Med. 5, 1–13 (2020).

    Google Scholar 

  • Sanjurjo-Rodríguez, C. et al. Versatility of induced pluripotent stem cells (iPSCs) for improving the knowledge on musculoskeletal diseases. Int. J. Mol. Sci. 21, 1–28 (2020).

    Google Scholar 

  • Han, W. M., Jang, Y. C. & García, A. J. Engineered matrices for skeletal muscle satellite cell engraftment and function. Matrix Biol. 60–61, 96–109 (2017).

    PubMed 

    Google Scholar 

  • Giordani, L. et al. High-dimensional single-cell cartography reveals novel skeletal muscle-resident cell populations. Mol. Cell 74, 609–621.e6 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Bolívar-Monsalve, E. J. et al. Continuous chaotic bioprinting of skeletal muscle-like constructs. Bioprinting 21, e00125 (2021).

    Google Scholar 

  • Lee, H. et al. Self-aligned myofibers in 3D bioprinted extracellular matrix-based construct accelerate skeletal muscle function restoration. Appl. Phys. Rev. 8, 021405 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • Yang, G. H., Kim, W., Kim, J. & Kim, G. A skeleton muscle model using GelMA-based cell-aligned bioink processed with an electric-field assisted 3D/4D bioprinting. Theranostics 11, 48 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kim, W. et al. A bioprinting process supplemented with in situ electrical stimulation directly induces significant myotube formation and myogenesis. Adv. Funct. Mater. 31, 2105170 (2021).

    CAS 

    Google Scholar 

  • Bakht, S. M. et al. Engineering next-generation bioinks with nanoparticles: moving from reinforcement fillers to multifunctional nanoelements. J. Mater. Chem. B 9, 5025–5038 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • Waters, S. L., Schumacher, L. J. & El Haj, A. J. Regenerative medicine meets mathematical modelling: developing symbiotic relationships. npj Regen. Med 6, 1–8 (2021). 2021 61.

    Google Scholar 

  • Zhu, Y. et al. Deep learning-based predictive identification of neural stem cell differentiation. Nat. Commun. 12, 1–13 (2021). 2021 121.

    CAS 

    Google Scholar 

  • Waisman, A. et al. Deep learning neural networks highly predict very early onset of pluripotent stem cell differentiation. Stem Cell Rep. 12, 845–859 (2019).

    Google Scholar 

  • del Sol, A. & Jung, S. The importance of computational modeling in stem cell research. Trends Biotechnol. 39, 126–136 (2021).

    PubMed 

    Google Scholar 

  • Thavandiran, N. et al. Functional arrays of human pluripotent stem cell-derived cardiac microtissues. Sci. Rep. 10, 1–13 (2020).

    Google Scholar 

  • Ortiz-Catalan, M., Håkansson, B. & Brånemark, R. Real-time and simultaneous control of artificial limbs based on pattern recognition algorithms. IEEE Trans. NEURAL Syst. Rehabil. Eng. 22, (2014).

  • Parker, P., Englehart, K. & Hudgins, B. Myoelectric signal processing for control of powered limb prostheses. J. Electromyogr. Kinesiol. 16, 541–548 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Kung, T. A. et al. Regenerative peripheral nerve interface viability and signal transduction with an implanted electrode. Plast. Reconstr. Surg. 133, 1380–1394 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Speck, N., Peeters, M. & Dzierzak, E. Development of the Vertebrate Hematopoietic System. in Mouse Development 191–210 (Elsevier, 2002).

  • Coultas, L., Chawengsaksophak, K. & Rossant, J. Endothelial cells and VEGF in vascular development. Nature 438, 937–945 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • De Val, S. Key transcriptional regulators of early vascular development. Arteriosclerosis, Thrombosis, Vasc. Biol. 31, 1469–1475 (2011).

    Google Scholar 

  • Majesky, M. W. Developmental basis of vascular smooth muscle diversity. Arterioscler. Thromb. Vasc. Biol. 27, 1248–1258 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • Sinha, S., Iyer, D. & Granata, A. Embryonic origins of human vascular smooth muscle cells: Implications for in vitro modeling and clinical application. Cell. Mol. Life Sci. 71, 2271–2288 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Murray, I. R. et al. Skeletal and cardiac muscle pericytes: functions and therapeutic potential. Pharmacol. Therapeutics 171, 65–74 (2017).

    CAS 

    Google Scholar 

  • Armulik, A., Abramsson, A. & Betsholtz, C. Endothelial/pericyte interactions. Circulation Res 97, 512–523 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • Ozerdem, U., Grako, K. A., Dahlin-Huppe, K., Monosov, E. & Stallcup, W. B. NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev. Dyn. 222, 218–227 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • Bitto, F. F. et al. Myogenic differentiation of mesenchymal stem cells in a newly developed neurotised AV-loop model. Biomed Res. Int. 2013, 935046 (2013).

  • Rosa, S. et al. Functional characterization of ipsC-derived arterial-and venous-like endothelial cells. Sci. Rep. 9, 1–15 (2019).

    Google Scholar 

  • Gholobova, D. et al. Endothelial network formation within human tissue-engineered skeletal muscle. Tissue Eng. Part A 21, 2548–2558 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Beach, R. L., Rao, J. S. & Festoff, B. W. Extracellular-matrix synthesis by skeletal muscle in culture. Major secreted collagenous protein of clonal myoblasts. Biochem. J. 225, 619–627 (1985).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Brent, A. E., Braun, T. & Tabin, C. J. Genetic analysis of interactions between the somitic muscle, cartilage and tendon cell lineages during mouse development. Development 132, 515–528 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • Chang, Y., Li, H. & Guo, Z. Mesenchymal stem cell-like properties in fibroblasts. Cell. Physiol. Biochem. 34, 703–714 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Chapman, M. A., Meza, R. & Lieber, R. L. Skeletal muscle fibroblasts in health and disease. Differentiation 92, 108–115 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sefton, E. M. & Kardon, G. Connecting muscle development, birth defects, and evolution: An essential role for muscle connective tissue. in Current Topics in Developmental Biology 132, 137–176 (Academic Press Inc., 2019).

  • Biferali, B., Proietti, D., Mozzetta, C. & Madaro, L. Fibro–adipogenic progenitors cross-talk in skeletal muscle: the social network. Front. Physiol. 10, 1074 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Wosczyna, M. N. et al. Mesenchymal stromal cells are required for regeneration and homeostatic maintenance of skeletal muscle. Cell Rep. 27, 2029–2035.e5 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Joe, A. W. B. et al. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12, 153–163 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nassari, S., Duprez, D. & Fournier-Thibault, C. Non-myogenic contribution to muscle development and homeostasis: The role of connective tissues. Front. Cell Developmental Biol. 5, 22 (2017).

    Google Scholar 

  • Dennis, R. G. & Kosnik II, P. E. Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cellular & Developmental Biology – Animal 36, 327–335 (2000).

    CAS 

    Google Scholar 

  • Li, M., Dickinson, C. E., Finkelstein, E. B., Neville, C. M. & Sundback, C. A. The role of fibroblasts in self-assembled skeletal muscle. Tissue Eng. – Part A 17, 2641–2650 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • Mackey, A. L., Magnan, M., Chazaud, B. & Kjaer, M. Human skeletal muscle fibroblasts stimulate in vitro myogenesis and in vivo muscle regeneration. J. Physiol. 595, 5115–5127 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Thummarati, P. & Kino-oka, M. Effect of co-culturing fibroblasts in human skeletal muscle cell sheet on angiogenic cytokine balance and angiogenesis. Front. Bioeng. Biotechnol. 8, 1121 (2020).

    Google Scholar 

  • Murchison, N. D. et al. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development 134, 2697–2708 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • Brent, A. E. & Tabin, C. J. Developmental regulation of somite derivatives: muscle, cartilage and tendon. Curr. Opin. Genet. Dev. 12, 548–557 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • Chen, C. M. A., Kraut, N., Groudine, M. & Weintraub, H. I-mf, a novel myogenic repressor, interacts with members of the MyoD family. Cell 86, 731–741 (1996).

    CAS 
    PubMed 

    Google Scholar 

  • Wayburn, B. & Volk, T. LRT, a tendon-specific leucine-rich repeat protein, promotes muscle-tendon targeting through its interaction with Robo. Development 136, 3607–3615 (2009).

    CAS 
    PubMed 

    Google Scholar 

  • Huang, A. H. et al. Repositioning forelimb superficialis muscles: tendon attachment and muscle activity enable active relocation of functional myofibers. Dev. Cell 26, 544–551 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Valdivia, M., Vega-Macaya, F. & Olguín, P. Mechanical control of myotendinous junction formation and tendon differentiation during development. Front. cell Dev. Biol. 5, 26 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Larkin, L. M., Calve, S., Kostrominova, T. Y. & Arruda, E. M. Structure and functional evaluation of tendon-skeletal muscle constructs engineered in vitro. Tissue Eng. 12, 3149–3158 (2006).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Laternser, S. et al. A novel microplate 3D bioprinting platform for the engineering of muscle and tendon tissues. SLAS Technol. 23, 599–613 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Laine, J. et al. Development of the excitation-contraction coupling machinery and its relation to myofibrillogenesis in human iPSC-derived skeletal myocytes. Skelet. Muscle 8, 1 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Osaki, T., Uzel, S. G. M. M. M. & Kamm, R. D. Microphysiological 3D model of amyotrophic lateral sclerosis (ALS) from human iPS-derived muscle cells and optogenetic motor neurons. Sci. Adv. 4, eaat5847 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lin, C.-Y. et al. iPSC-derived functional human neuromuscular junctions model the pathophysiology of neuromuscular diseases. JCI insight 4, e124299 (2019).

    PubMed Central 

    Google Scholar 

  • Demestre, M. et al. Formation and characterisation of neuromuscular junctions between hiPSC derived motoneurons and myotubes. Stem Cell Res. 15, 328–336 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Mazaleyrat, K. et al. Multilineage differentiation for formation of innervated skeletal muscle fibers from healthy and diseased human pluripotent stem cells. Cells 9, 1531 (2020).

    CAS 
    PubMed Central 

    Google Scholar 

  • Sato, Y. et al. TFEB overexpression promotes glycogen clearance of Pompe disease iPSC-derived skeletal muscle. Mol. Ther. Methods Clin. Dev. 3, 16054 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Wu, J., Hunt, S. D., Xue, H., Liu, Y. & Darabi, R. Generation and Characterization of a MYF5 Reporter Human iPS Cell Line Using CRISPR/Cas9 Mediated Homologous Recombination. 6, (2016).

  • Gilbert, S. & Barresi, M. J. F. Developmental Biology, Eleventh Edition. (Sinauer Associates, Inc., 2016).

  • Source link