1932

Abstract

Although skeletal muscle is one of the most regenerative organs in our body, various genetic defects, alterations in extrinsic signaling, or substantial tissue damage can impair muscle function and the capacity for self-repair. The diversity and complexity of muscle disorders have attracted much interest from both cell biologists and, more recently, bioengineers, leading to concentrated efforts to better understand muscle pathology and develop more efficient therapies. This review describes the biological underpinnings of muscle development, repair, and disease, and discusses recent bioengineering efforts to design and control myomimetic environments, both to study muscle biology and function and to aid in the development of new drug, cell, and gene therapies for muscle disorders. The synergy between engineering-aided biological discovery and biology-inspired engineering solutions will be the path forward for translating laboratory results into clinical practice.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-bioeng-071114-040640
2015-12-07
2024-12-02
Loading full text...

Full text loading...

/deliver/fulltext/bioeng/17/1/annurev-bioeng-071114-040640.html?itemId=/content/journals/10.1146/annurev-bioeng-071114-040640&mimeType=html&fmt=ahah

Literature Cited

  1. Clark KA, McElhinny AS, Beckerle MC, Gregorio CC. 1.  2002. Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell Dev. Biol. 18:637–706 [Google Scholar]
  2. Charge SB, Rudnicki MA. 2.  2004. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84:209–38 [Google Scholar]
  3. Yin H, Price F, Rudnicki MA. 3.  2013. Satellite cells and the muscle stem cell niche. Physiol. Rev. 93:23–67 [Google Scholar]
  4. Brack AS, Rando TA. 4.  2007. Intrinsic changes and extrinsic influences of myogenic stem cell function during aging. Stem Cell Rev. 3:226–37 [Google Scholar]
  5. Juhas M, Bursac N. 5.  2013. Engineering skeletal muscle repair. Curr. Opin. Biotechnol. 24:880–86 [Google Scholar]
  6. Kelly AM, Zacks SI. 6.  1969. The histogenesis of rat intercostal muscle. J. Cell Biol. 42:135–53 [Google Scholar]
  7. Biressi S, Molinaro M, Cossu G. 7.  2007. Cellular heterogeneity during vertebrate skeletal muscle development. Dev. Biol. 308:281–93 [Google Scholar]
  8. Cusella-De Angelis MG, Molinari S, Le Donne A, Coletta M, Vivarelli E. 8.  et al. 1994. Differential response of embryonic and fetal myoblasts to TGF β: a possible regulatory mechanism of skeletal muscle histogenesis. Development 120:925–33 [Google Scholar]
  9. Dale JK, Maroto M, Dequeant ML, Malapert P, McGrew M, Pourquie O. 9.  2003. Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature 421:275–78 [Google Scholar]
  10. Schuster-Gossler K, Cordes R, Gossler A. 10.  2007. Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. PNAS 104:537–42 [Google Scholar]
  11. Shawber C, Nofziger D, Hsieh JJ, Lindsell C, Bogler O. 11.  et al. 1996. Notch signaling inhibits muscle cell differentiation through a CBF1-independent pathway. Development 122:3765–73 [Google Scholar]
  12. Dahlqvist C, Blokzijl A, Chapman G, Falk A, Dannaeus K. 12.  et al. 2003. Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 130:6089–99 [Google Scholar]
  13. Luo D, Renault VM, Rando TA. 13.  2005. The regulation of Notch signaling in muscle stem cell activation and postnatal myogenesis. Semin. Cell Dev. Biol. 16:612–22 [Google Scholar]
  14. Sartori R, Gregorevic P, Sandri M. 14.  2014. TGFβ and BMP signaling in skeletal muscle: potential significance for muscle-related disease. Trends Endocrinol. Metab. 25:464–71 [Google Scholar]
  15. Chakkalakal J, Brack A. 15.  2012. Extrinsic regulation of satellite cell function and muscle regeneration capacity during aging. J. Stem Cell Res. Ther. 2:Suppl. 11001 [Google Scholar]
  16. Lepper C, Partridge TA, Fan CM. 16.  2011. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138:3639–46 [Google Scholar]
  17. Cheung TH, Rando TA. 17.  2013. Molecular regulation of stem cell quiescence. Nat. Rev. Mol. Cell Biol. 14:329–40 [Google Scholar]
  18. Cheung TH, Quach NL, Charville GW, Liu L, Park L. 18.  et al. 2012. Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482:524–28 [Google Scholar]
  19. Bjornson CR, Cheung TH, Liu L, Tripathi PV, Steeper KM, Rando TA. 19.  2012. Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30:232–42 [Google Scholar]
  20. Mourikis P, Sambasivan R, Castel D, Rocheteau P, Bizzarro V, Tajbakhsh S. 20.  2012. A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30:243–52 [Google Scholar]
  21. Gopinath SD, Webb AE, Brunet A, Rando TA. 21.  2014. FOXO3 promotes quiescence in adult muscle stem cells during the process of self-renewal. Stem Cell Rep. 2:414–26 [Google Scholar]
  22. Joe AW, Yi L, Natarajan A, Le Grand F, So L. 22.  et al. 2010. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12:153–63 [Google Scholar]
  23. Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K. 23.  2010. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 12:143–52 [Google Scholar]
  24. Ito T, Ogawa R, Uezumi A, Ohtani T, Watanabe Y. 24.  et al. 2013. Imatinib attenuates severe mouse dystrophy and inhibits proliferation and fibrosis-marker expression in muscle mesenchymal progenitors. Neuromuscul. Disord. 23:349–56 [Google Scholar]
  25. Heredia JE, Mukundan L, Chen FM, Mueller AA, Deo RC. 25.  et al. 2013. Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell 153:376–88 [Google Scholar]
  26. Saclier M, Yacoub-Youssef H, Mackey AL, Arnold L, Ardjoune H. 26.  et al. 2013. Differentially activated macrophages orchestrate myogenic precursor cell fate during human skeletal muscle regeneration. Stem Cells 31:384–96 [Google Scholar]
  27. Schofield R. 27.  1978. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4:7–25 [Google Scholar]
  28. Watt FM, Hogan BL. 28.  2000. Out of Eden: stem cells and their niches. Science 287:1427–30 [Google Scholar]
  29. Mauro A. 29.  1961. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9:493–95 [Google Scholar]
  30. Christov C, Chretien F, Abou-Khalil R, Bassez G, Vallet G. 30.  et al. 2007. Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol. Biol. Cell 18:1397–409 [Google Scholar]
  31. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. 31.  2005. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433:760–64 [Google Scholar]
  32. Villeda SA, Plambeck KE, Middeldorp J, Castellano JM, Mosher KI. 32.  et al. 2014. Young blood reverses age-related impairments in cognitive function and synaptic plasticity in mice. Nat. Med. 20:659–63 [Google Scholar]
  33. Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M. 33.  et al. 2011. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 477:90–94 [Google Scholar]
  34. Katsimpardi L, Litterman NK, Schein PA, Miller CM, Loffredo FS. 34.  et al. 2014. Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science 344:630–34 [Google Scholar]
  35. Sinha M, Jang YC, Oh J, Khong D, Wu EY. 35.  et al. 2014. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 344:649–52 [Google Scholar]
  36. Emery AE. 36.  1993. Duchenne muscular dystrophy—Meryon's disease. Neuromuscul. Disord. 3:263–66 [Google Scholar]
  37. Goyenvalle A, Seto JT, Davies KE, Chamberlain J. 37.  2011. Therapeutic approaches to muscular dystrophy. Hum. Mol. Genet. 20:R1R69–78 [Google Scholar]
  38. Abdel-Hamid H, Clemens PR. 38.  2012. Pharmacological therapies for muscular dystrophies. Curr. Opin. Neurol. 25:604–8 [Google Scholar]
  39. Tedesco FS, Cossu G. 39.  2012. Stem cell therapies for muscle disorders. Curr. Opin. Neurol. 25:597–603 [Google Scholar]
  40. Grogan BF, Hsu JR. 40.  Skelet. Trauma Res. Consort 2011. Volumetric muscle loss. J. Am. Acad. Orthop. Surg. 19:Suppl. 1S35–37 [Google Scholar]
  41. Turner NJ, Badylak SF. 41.  2012. Regeneration of skeletal muscle. Cell Tissue Res. 347:759–74 [Google Scholar]
  42. Pedersen BK, Febbraio MA. 42.  2012. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat. Rev. Endocrinol. 8:457–65 [Google Scholar]
  43. Vandenburgh HH, Karlisch P, Farr L. 43.  1988. Maintenance of highly contractile tissue-cultured avian skeletal myotubes in collagen gel. In Vitro Cell. Dev. Biol. 24:166–74 [Google Scholar]
  44. Shansky J, Del Tatto M, Chromiak J, Vandenburgh H. 44.  1997. A simplified method for tissue engineering skeletal muscle organoids in vitro. In Vitro Cell. Dev. Biol. Anim. 33:659–61 [Google Scholar]
  45. Strohman RC, Bayne E, Spector D, Obinata T, Micou-Eastwood J, Maniotis A. 45.  1990. Myogenesis and histogenesis of skeletal muscle on flexible membranes in vitro. In Vitro Cell. Dev. Biol. 26:201–8 [Google Scholar]
  46. Dennis RG, Kosnik PE 2nd. 46.  2000. Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cell. Dev. Biol. Anim. 36:327–35 [Google Scholar]
  47. Dennis RG, Kosnik PE 2nd, Gilbert ME, Faulkner JA. 47.  2001. Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. Am. J. Physiol. Cell Physiol. 280:C288–95 [Google Scholar]
  48. Bian W, Juhas M, Pfeiler TW, Bursac N. 48.  2012. Local tissue geometry determines contractile force generation of engineered muscle networks. Tissue Eng. Part A 18:957–67 [Google Scholar]
  49. Vandenburgh HH, Hatfaludy S, Karlisch P, Shansky J. 49.  1989. Skeletal muscle growth is stimulated by intermittent stretch-relaxation in tissue culture. Am. J. Physiol. 256:C674–82 [Google Scholar]
  50. Grefte S, Vullinghs S, Kuijpers-Jagtman AM, Torensma R, Von den Hoff JW. 50.  2012. Matrigel, but not collagen I, maintains the differentiation capacity of muscle derived cells in vitro. Biomed. Mater. 7:055004 [Google Scholar]
  51. Huang YC, Dennis RG, Larkin L, Baar K. 51.  2005. Rapid formation of functional muscle in vitro using fibrin gels. J. Appl. Physiol. 98:706–13 [Google Scholar]
  52. Hosseini V, Ahadian S, Ostrovidov S, Camci-Unal G, Chen S. 52.  et al. 2012. Engineered contractile skeletal muscle tissue on a microgrooved methacrylated gelatin substrate. Tissue Eng. Part A 18:2453–65 [Google Scholar]
  53. Fuoco C, Salvatori ML, Biondo A, Shapira-Schweitzer K, Santoleri S. 53.  et al. 2012. Injectable polyethylene glycol-fibrinogen hydrogel adjuvant improves survival and differentiation of transplanted mesoangioblasts in acute and chronic skeletal-muscle degeneration. Skeletal Muscle 2:24 [Google Scholar]
  54. Hinds S, Bian W, Dennis RG, Bursac N. 54.  2011. The role of extracellular matrix composition in structure and function of bioengineered skeletal muscle. Biomaterials 32:3575–83 [Google Scholar]
  55. Juhas M, Bursac N. 55.  2014. Roles of adherent myogenic cells and dynamic culture in engineered muscle function and maintenance of satellite cells. Biomaterials 35:9438–46 [Google Scholar]
  56. Juhas M, Engelmayr GC Jr, Fontanella AN, Palmer GM, Bursac N. 56.  2014. Biomimetic engineered muscle with capacity for vascular integration and functional maturation in vivo. PNAS 111:5508–13 [Google Scholar]
  57. Bian W, Liau B, Badie N, Bursac N. 57.  2009. Mesoscopic hydrogel molding to control the 3D geometry of bioartificial muscle tissues. Nat. Protoc. 4:1522–34 [Google Scholar]
  58. Bian W, Bursac N. 58.  2009. Engineered skeletal muscle tissue networks with controllable architecture. Biomaterials 30:1401–12 [Google Scholar]
  59. Borselli C, Cezar CA, Shvartsman D, Vandenburgh HH, Mooney DJ. 59.  2011. The role of multifunctional delivery scaffold in the ability of cultured myoblasts to promote muscle regeneration. Biomaterials 32:8905–14 [Google Scholar]
  60. Liao IC, Leong KW. 60.  2011. Efficacy of engineered FVIII-producing skeletal muscle enhanced by growth factor-releasing co-axial electrospun fibers. Biomaterials 32:1669–77 [Google Scholar]
  61. Yun YR, Lee S, Jeon E, Kang W, Kim KH. 61.  et al. 2012. Fibroblast growth factor 2-functionalized collagen matrices for skeletal muscle tissue engineering. Biotechnol. Lett. 34:771–78 [Google Scholar]
  62. Wylie RG, Ahsan S, Aizawa Y, Maxwell KL, Morshead CM, Shoichet MS. 62.  2011. Spatially controlled simultaneous patterning of multiple growth factors in three-dimensional hydrogels. Nat. Mater. 10:799–806 [Google Scholar]
  63. Yamamoto Y, Ito A, Kato M, Kawabe Y, Shimizu K. 63.  et al. 2009. Preparation of artificial skeletal muscle tissues by a magnetic force-based tissue engineering technique. J. Biosci. Bioeng. 108:538–43 [Google Scholar]
  64. Takahashi H, Shimizu T, Nakayama M, Yamato M, Okano T. 64.  2013. The use of anisotropic cell sheets to control orientation during the self-organization of 3D muscle tissue. Biomaterials 34:7372–80 [Google Scholar]
  65. Teodori L, Costa A, Marzio R, Perniconi B, Coletti D. 65.  et al. 2014. Native extracellular matrix: a new scaffolding platform for repair of damaged muscle. Front. Physiol. 5:218 [Google Scholar]
  66. Sicari BM, Rubin JP, Dearth CL, Wolf MT, Ambrosio F. 66.  et al. 2014. An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss. Sci. Transl. Med. 6:234ra58 [Google Scholar]
  67. Machingal MA, Corona BT, Walters TJ, Kesireddy V, Koval CN. 67.  et al. 2011. A tissue-engineered muscle repair construct for functional restoration of an irrecoverable muscle injury in a murine model. Tissue Eng. Part A 17:2291–303 [Google Scholar]
  68. Saxena AK, Willital GH, Vacanti JP. 68.  2001. Vascularized three-dimensional skeletal muscle tissue-engineering. Biomed. Mater. Eng. 11:275–81 [Google Scholar]
  69. Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS. 69.  et al. 2005. Engineering vascularized skeletal muscle tissue. Nat. Biotechnol. 23:879–84 [Google Scholar]
  70. Ju YM, Atala A, Yoo JJ, Lee SJ. 70.  2014. In situ regeneration of skeletal muscle tissue through host cell recruitment. Acta Biomater. 10:4332–39 [Google Scholar]
  71. Miyagawa S, Saito A, Sakaguchi T, Yoshikawa Y, Yamauchi T. 71.  et al. 2010. Impaired myocardium regeneration with skeletal cell sheets—a preclinical trial for tissue-engineered regeneration therapy. Transplantation 90:364–72 [Google Scholar]
  72. Larkin LM, Calve S, Kostrominova TY, Arruda EM. 72.  2006. Structure and functional evaluation of tendon-skeletal muscle constructs engineered in vitro. Tissue Eng. 12:3149–58 [Google Scholar]
  73. VanDusen KW, Syverud BC, Williams ML, Lee JD, Larkin LM. 73.  2014. Engineered skeletal muscle units for repair of volumetric muscle loss in the tibialis anterior muscle of a rat. Tissue Eng. Part A. 20:2920–30 [Google Scholar]
  74. Das M, Rumsey JW, Bhargava N, Stancescu M, Hickman JJ. 74.  2010. A defined long-term in vitro tissue engineered model of neuromuscular junctions. Biomaterials 31:4880–88 [Google Scholar]
  75. Larkin LM, Van der Meulen JH, Dennis RG, Kennedy JB. 75.  2006. Functional evaluation of nerve-skeletal muscle constructs engineered in vitro. In Vitro Cell. Dev. Biol. Anim. 42:75–82 [Google Scholar]
  76. Morimoto Y, Kato-Negishi M, Onoe H, Takeuchi S. 76.  2013. Three-dimensional neuron-muscle constructs with neuromuscular junctions. Biomaterials 34:9413–19 [Google Scholar]
  77. Li M, Dickinson CE, Finkelstein EB, Neville CM, Sundback CA. 77.  2011. The role of fibroblasts in self-assembled skeletal muscle. Tissue Eng. Part A 17:2641–50 [Google Scholar]
  78. Hinds S, Tyhovych N, Sistrunk C, Terracio L. 78.  2013. Improved tissue culture conditions for engineered skeletal muscle sheets. Sci. World J. 2013:370151 [Google Scholar]
  79. Carosio S, Barberi L, Rizzuto E, Nicoletti C, Del Prete Z, Musaro A. 79.  2013. Generation of eX vivo-vascularized Muscle Engineered Tissue (X-MET). Sci. Rep. 3:1420 [Google Scholar]
  80. Corona BT, Ward CL, Baker HB, Walters TJ, Christ GJ. 80.  2014. Implantation of in vitro tissue engineered muscle repair constructs and bladder acellular matrices partially restore in vivo skeletal muscle function in a rat model of volumetric muscle loss injury. Tissue Eng. Part A 20:705–15 [Google Scholar]
  81. Corona BT, Machingal MA, Criswell T, Vadhavkar M, Dannahower AC. 81.  et al. 2012. Further development of a tissue engineered muscle repair construct in vitro for enhanced functional recovery following implantation in vivo in a murine model of volumetric muscle loss injury. Tissue Eng. Part A 18:1213–28 [Google Scholar]
  82. Borselli C, Storrie H, Benesch-Lee F, Shvartsman D, Cezar C. 82.  et al. 2010. Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. PNAS 107:3287–92 [Google Scholar]
  83. Koffler J, Kaufman-Francis K, Shandalov Y, Egozi D, Pavlov DA. 83.  et al. 2011. Improved vascular organization enhances functional integration of engineered skeletal muscle grafts. PNAS 108:14789–94 [Google Scholar]
  84. Smith AS, Long CJ, Pirozzi K, Najjar S, McAleer C. 84.  et al. 2014. A multiplexed chip-based assay system for investigating the functional development of human skeletal myotubes in vitro. J. Biotechnol. 185C:15–18 [Google Scholar]
  85. Ciciliot S, Rossi AC, Dyar KA, Blaauw B, Schiaffino S. 85.  2013. Muscle type and fiber type specificity in muscle wasting. Int. J. Biochem. Cell Biol. 45:2191–99 [Google Scholar]
  86. Powell CA, Smiley BL, Mills J, Vandenburgh HH. 86.  2002. Mechanical stimulation improves tissue-engineered human skeletal muscle. Am. J. Physiol. Cell Physiol. 283:C1557–65 [Google Scholar]
  87. Chiron S, Tomczak C, Duperray A, Laine J, Bonne G. 87.  et al. 2012. Complex interactions between human myoblasts and the surrounding 3D fibrin-based matrix. PLOS ONE 7:e36173 [Google Scholar]
  88. Moon DG, Christ G, Stitzel JD, Atala A, Yoo JJ. 88.  2008. Cyclic mechanical preconditioning improves engineered muscle contraction. Tissue Eng. Part A 14:473–82 [Google Scholar]
  89. Martin NR, Passey SL, Player DJ, Khodabukus A, Ferguson RA. 89.  et al. 2013. Factors affecting the structure and maturation of human tissue engineered skeletal muscle. Biomaterials 34:5759–65 [Google Scholar]
  90. Madden L, Juhas M, Kraus WE, Truskey GA, Bursac N. 90.  2015. Bioengineered human myobundles mimic clinical responses of skeletal muscle to drugs. eLife 4:e04885 [Google Scholar]
  91. Serena E, Zatti S, Reghelin E, Pasut A, Cimetta E, Elvassore N. 91.  2010. Soft substrates drive optimal differentiation of human healthy and dystrophic myotubes. Integr. Biol. (Camb.) 2:193–201 [Google Scholar]
  92. Sengupta D, Gilbert PM, Johnson KJ, Blau HM, Heilshorn SC. 92.  2012. Protein-engineered biomaterials to generate human skeletal muscle mimics. Adv. Healthc. Mater. 1:785–89 [Google Scholar]
  93. Koning M, Werker PM, van Luyn MJ, Harmsen MC. 93.  2011. Hypoxia promotes proliferation of human myogenic satellite cells: a potential benefactor in tissue engineering of skeletal muscle. Tissue Eng. Part A 17:1747–58 [Google Scholar]
  94. Bentzinger CF, von Maltzahn J, Dumont NA, Stark DA, Wang YX. 94.  et al. 2014. Wnt7a stimulates myogenic stem cell motility and engraftment resulting in improved muscle strength. J. Cell Biol. 205:97–111 [Google Scholar]
  95. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S. 95.  et al. 2005. Direct isolation of satellite cells for skeletal muscle regeneration. Science 309:2064–67 [Google Scholar]
  96. Sacco A, Doyonnas R, Kraft P, Vitorovic S, Blau HM. 96.  2008. Self-renewal and expansion of single transplanted muscle stem cells. Nature 456:502–6 [Google Scholar]
  97. Cosgrove BD, Sacco A, Gilbert PM, Blau HM. 97.  2009. A home away from home: challenges and opportunities in engineering in vitro muscle satellite cell niches. Differentiation 78:185–94 [Google Scholar]
  98. McCullagh KJ, Perlingeiro RC. 98.  2014. Coaxing stem cells for skeletal muscle repair. Adv. Drug Deliv. Rev. 84:198–207 [Google Scholar]
  99. Gilbert PM, Havenstrite KL, Magnusson KE, Sacco A, Leonardi NA. 99.  et al. 2010. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329:1078–81 [Google Scholar]
  100. Cosgrove BD, Gilbert PM, Porpiglia E, Mourkioti F, Lee SP. 100.  et al. 2014. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat. Med. 20:255–64 [Google Scholar]
  101. Zhu X, Fu L, Yi F, Liu GH, Ocampo A. 101.  et al. 2014. Regeneration: making muscle from hPSCs. Cell Res. 24:1159–61 [Google Scholar]
  102. Darabi R, Arpke RW, Irion S, Dimos JT, Grskovic M. 102.  et al. 2012. Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 10:610–19 [Google Scholar]
  103. Skoglund G, Laine J, Darabi R, Fournier E, Perlingeiro R, Tabti N. 103.  2014. Physiological and ultrastructural features of human induced pluripotent and embryonic stem cell-derived skeletal myocytes in vitro. PNAS 111:8275–80 [Google Scholar]
  104. Abujarour R, Bennett M, Valamehr B, Lee TT, Robinson M. 104.  et al. 2014. Myogenic differentiation of muscular dystrophy-specific induced pluripotent stem cells for use in drug discovery. Stem Cells Transl. Med. 3:149–60 [Google Scholar]
  105. Tanaka A, Woltjen K, Miyake K, Hotta A, Ikeya M. 105.  et al. 2013. Efficient and reproducible myogenic differentiation from human iPS cells: prospects for modeling Miyoshi Myopathy in vitro. PLOS ONE 8:e61540 [Google Scholar]
  106. Goudenege S, Lebel C, Huot NB, Dufour C, Fujii I. 106.  et al. 2012. Myoblasts derived from normal hESCs and dystrophic hiPSCs efficiently fuse with existing muscle fibers following transplantation. Mol. Ther. 20:2153–67 [Google Scholar]
  107. Yasuno T, Osafune K, Sakurai H, Asaka I, Tanaka A. 107.  et al. 2014. Functional analysis of iPSC-derived myocytes from a patient with carnitine palmitoyltransferase II deficiency. Biochem. Biophys. Res. Commun. 448:175–81 [Google Scholar]
  108. Hosoyama T, McGivern JV, Van Dyke JM, Ebert AD, Suzuki M. 108.  2014. Derivation of myogenic progenitors directly from human pluripotent stem cells using a sphere-based culture. Stem Cells Transl. Med. 3:564–74 [Google Scholar]
  109. Borchin B, Chen J, Barberi T. 109.  2013. Derivation and FACS-mediated purification of PAX3+/PAX7+skeletal muscle precursors from human pluripotent stem cells. Stem Cell Rep. 1:620–31 [Google Scholar]
  110. Xu C, Tabebordbar M, Iovino S, Ciarlo C, Liu J. 110.  et al. 2013. A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species. Cell 155:909–21 [Google Scholar]
  111. Leung M, Cooper A, Jana S, Tsao CT, Petrie TA, Zhang M. 111.  2013. Nanofiber-based in vitro system for high myogenic differentiation of human embryonic stem cells. Biomacromolecules 14:4207–16 [Google Scholar]
  112. Hwang Y, Suk S, Shih YR, Seo T, Du B. 112.  et al. 2014. WNT3A promotes myogenesis of human embryonic stem cells and enhances in vivo engraftment. Sci. Rep. 4:5916 [Google Scholar]
  113. Mamchaoui K, Trollet C, Bigot A, Negroni E, Chaouch S. 113.  et al. 2011. Immortalized pathological human myoblasts: towards a universal tool for the study of neuromuscular disorders. Skeletal Muscle 1:34 [Google Scholar]
  114. Kaully T, Kaufman-Francis K, Lesman A, Levenberg S. 114.  2009. Vascularization—the conduit to viable engineered tissues. Tissue Eng. Part B Rev. 15:159–69 [Google Scholar]
  115. Levenberg S, Langer R. 115.  2004. Advances in tissue engineering. Curr. Top. Dev. Biol. 61:113–34 [Google Scholar]
  116. Shvartsman D, Storrie-White H, Lee K, Kearney C, Brudno Y. 116.  et al. 2014. Sustained delivery of VEGF maintains innervation and promotes reperfusion in ischemic skeletal muscles via NGF/GDNF Signaling. Mol. Ther. 22:1243–53 [Google Scholar]
  117. Wang L, Cao L, Shansky J, Wang Z, Mooney D, Vandenburgh H. 117.  2014. Minimally invasive approach to the repair of injured skeletal muscle with a shape-memory scaffold. Mol. Ther. 22:1441–49 [Google Scholar]
  118. Zhou W, He DQ, Liu JY, Feng Y, Zhang XY. 118.  et al. 2013. Angiogenic gene-modified myoblasts promote vascularization during repair of skeletal muscle defects. J. Tissue Eng. Regen. Med. In press. doi: 10.1002/term.1692 [Google Scholar]
  119. Messina A, Bortolotto SK, Cassell OC, Kelly J, Abberton KM, Morrison WA. 119.  2005. Generation of a vascularized organoid using skeletal muscle as the inductive source. FASEB J. 19:1570–72 [Google Scholar]
  120. Shandalov Y, Egozi D, Koffler J, Dado-Rosenfeld D, Ben-Shimol D. 120.  et al. 2014. An engineered muscle flap for reconstruction of large soft tissue defects. PNAS 111:6010–15 [Google Scholar]
  121. Tilkorn DJ, Bedogni A, Keramidaris E, Han X, Palmer JA. 121.  et al. 2010. Implanted myoblast survival is dependent on the degree of vascularization in a novel delayed implantation/prevascularization tissue engineering model. Tissue Eng. Part A 16:165–78 [Google Scholar]
  122. Skouras E, Ozsoy U, Sarikcioglu L, Angelov DN. 122.  2011. Intrinsic and therapeutic factors determining the recovery of motor function after peripheral nerve transection. Ann. Anat. 193:286–303 [Google Scholar]
  123. Dhawan V, Lytle IF, Dow DE, Huang YC, Brown DL. 123.  2007. Neurotization improves contractile forces of tissue-engineered skeletal muscle. Tissue Eng. 13:2813–21 [Google Scholar]
  124. Kang SB, Olson JL, Atala A, Yoo JJ. 124.  2012. Functional recovery of completely denervated muscle: implications for innervation of tissue-engineered muscle. Tissue Eng. Part A 18:1912–20 [Google Scholar]
  125. Bryson JB, Machado CB, Crossley M, Stevenson D, Bros-Facer V. 125.  et al. 2014. Optical control of muscle function by transplantation of stem cell-derived motor neurons in mice. Science 344:94–97 [Google Scholar]
  126. Guo X, Das M, Rumsey J, Gonzalez M, Stancescu M, Hickman J. 126.  2010. Neuromuscular junction formation between human stem-cell-derived motoneurons and rat skeletal muscle in a defined system. Tissue Eng. Part C Methods 16:1347–55 [Google Scholar]
  127. Colomar A, Robitaille R. 127.  2004. Glial modulation of synaptic transmission at the neuromuscular junction. Glia 47:284–89 [Google Scholar]
  128. Bezakova G, Helm JP, Francolini M, Lomo T. 128.  2001. Effects of purified recombinant neural and muscle agrin on skeletal muscle fibers in vivo. J. Cell Biol. 153:1441–52 [Google Scholar]
  129. Bian W, Bursac N. 129.  2012. Soluble miniagrin enhances contractile function of engineered skeletal muscle. FASEB J. 26:955–65 [Google Scholar]
  130. Ko IK, Lee BK, Lee SJ, Andersson KE, Atala A, Yoo JJ. 130.  2013. The effect of in vitro formation of acetylcholine receptor (AChR) clusters in engineered muscle fibers on subsequent innervation of constructs in vivo. Biomaterials 34:3246–55 [Google Scholar]
  131. Filareto A, Parker S, Darabi R, Borges L, Iacovino M. 131.  et al. 2013. An ex vivo gene therapy approach to treat muscular dystrophy using inducible pluripotent stem cells. Nat. Commun. 4:1549 [Google Scholar]
  132. Tedesco FS, Gerli MF, Perani L, Benedetti S, Ungaro F. 132.  et al. 2012. Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Sci. Transl. Med. 4:140ra89 [Google Scholar]
  133. Li M, Suzuki K, Kim NY, Liu GH, Izpisua Belmonte JC. 133.  2014. A cut above the rest: targeted genome editing technologies in human pluripotent stem cells. J. Biol. Chem. 289:4594–99 [Google Scholar]
  134. Hsu PD, Lander ES, Zhang F. 134.  2014. Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:1262–78 [Google Scholar]
  135. Long C, McAnally JR, Shelton JM, Mireault AA, Bassel-Duby R, Olson EN. 135.  2014. Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA. Science 345:1184–88 [Google Scholar]
  136. Maffioletti SM, Noviello M, English K, Tedesco FS. 136.  2014. Stem cell transplantation for muscular dystrophy: the challenge of immune response. BioMed Res. Int. 2014:964010 [Google Scholar]
  137. Hubbell JA, Thomas SN, Swartz MA. 137.  2009. Materials engineering for immunomodulation. Nature 462:449–60 [Google Scholar]
  138. Partridge TA. 138.  2013. The mdx mouse model as a surrogate for Duchenne muscular dystrophy. FEBS J. 280:4177–86 [Google Scholar]
  139. Sacco A, Mourkioti F, Tran R, Choi J, Llewellyn M. 139.  et al. 2010. Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143:1059–71 [Google Scholar]
  140. Kamphoven JH, Stubenitsky R, Reuser AJ, Van Der Ploeg AT, Verdouw PD, Duncker DJ. 140.  2001. Cardiac remodeling and contractile function in acid α-glucosidase knockout mice. Physiol. Genomics 5:171–79 [Google Scholar]
  141. Truskey GA, Achneck HE, Bursac N, Chan H, Cheng CS. 141.  et al. 2013. Design considerations for an integrated microphysiological muscle tissue for drug and tissue toxicity testing. Stem Cell Res. Ther. 4:Suppl. 1S10 [Google Scholar]
  142. Gilbreath HR, Castro D, Iannaccone ST. 142.  2014. Congenital Myopathies and muscular dystrophies. Neurol. Clin. 32:689–703 [Google Scholar]
  143. Meng J, Chun S, Asfahani R, Lochmuller H, Muntoni F, Morgan J. 143.  2014. Human skeletal muscle-derived CD133+ cells form functional satellite cells after intramuscular transplantation in immunodeficient host mice. Mol. Ther. 22:1008–17 [Google Scholar]
  144. Fitts RH, McDonald KS, Schluter JM. 144.  1991. The determinants of skeletal muscle force and power: their adaptability with changes in activity pattern. J. Biomech. 24:Suppl. 1111–22 [Google Scholar]
  145. Rüegg MA, Glass DJ. 145.  2011. Molecular mechanisms and treatment options for muscle wasting diseases. Annu. Rev. Pharmacol. Toxicol. 51:373–95 [Google Scholar]
  146. Agbulut O, Noirez P, Beaumont F, Butler-Browne G. 146.  2003. Myosin heavy chain isoforms in postnatal muscle development of mice. Biol. Cell 95:399–406 [Google Scholar]
  147. Ramachandran I, Terry M, Ferrari MB. 147.  2003. Skeletal muscle myosin cross-bridge cycling is necessary for myofibrillogenesis. Cell Motil. Cytoskelet. 55:61–72 [Google Scholar]
  148. Schiaffino S, Reggiani C. 148.  2011. Fiber types in mammalian skeletal muscles. Physiol. Rev. 91:1447–531 [Google Scholar]
  149. DeVol DL, Rotwein P, Sadow JL, Novakofski J, Bechtel PJ. 149.  1990. Activation of insulin-like growth factor gene expression during work-induced skeletal muscle growth. Am. J. Physiol. 259:E89–95 [Google Scholar]
  150. Velloso CP. 150.  2008. Regulation of muscle mass by growth hormone and IGF-I. Br. J. Pharmacol. 154:557–68 [Google Scholar]
  151. Barnard RJ, Youngren JF. 151.  1992. Regulation of glucose transport in skeletal muscle. FASEB J. 6:3238–44 [Google Scholar]
  152. Aas V, Bakke SS, Feng YZ, Kase ET, Jensen J. 152.  et al. 2013. Are cultured human myotubes far from home?. Cell Tissue Res. 354:671–82 [Google Scholar]
  153. Davis TA, Fiorotto ML. 153.  2009. Regulation of muscle growth in neonates. Curr. Opin. Clin. Nutr. 12:78–85 [Google Scholar]
  154. Saltiel AR, Kahn CR. 154.  2001. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414:799–806 [Google Scholar]
  155. Langelaan ML, Boonen KJ, Rosaria-Chak KY, van der Schaft DW, Post MJ, Baaijens FP. 155.  2011. Advanced maturation by electrical stimulation: differences in response between C2C12 and primary muscle progenitor cells. J. Tissue Eng. Regen. Med. 5:529–39 [Google Scholar]
  156. Donnelly K, Khodabukus A, Philp A, Deldicque L, Dennis RG, Baar K. 156.  2010. A novel bioreactor for stimulating skeletal muscle in vitro. Tissue Eng. Part C Methods 16:711–18 [Google Scholar]
  157. Ito A, Yamamoto Y, Sato M, Ikeda K, Yamamoto M. 157.  et al. 2014. Induction of functional tissue-engineered skeletal muscle constructs by defined electrical stimulation. Sci. Rep. 4:4781 [Google Scholar]
  158. Cheema U, Yang SY, Mudera V, Goldspink GG, Brown RA. 158.  2003. 3-D in vitro model of early skeletal muscle development. Cell Motil. Cytoskelet. 54:226–36 [Google Scholar]
  159. Vandenburgh HH, Karlisch P. 159.  1989. Longitudinal growth of skeletal myotubes in vitro in a new horizontal mechanical cell stimulator. In Vitro Cell. Dev. Biol. 25:607–16 [Google Scholar]
  160. Kuang S, Charge SB, Seale P, Huh M, Rudnicki MA. 160.  2006. Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J. Cell Biol. 172:103–13 [Google Scholar]
  161. Kawano F, Takeno Y, Nakai N, Higo Y, Terada M. 161.  et al. 2008. Essential role of satellite cells in the growth of rat soleus muscle fibers. Am. J. Physiol. Cell Physiol. 295:C458–67 [Google Scholar]
  162. Slater CR. 162.  1982. Postnatal maturation of nerve-muscle junctions in hindlimb muscles of the mouse. Dev. Biol. 94:11–22 [Google Scholar]
  163. d'Albis A, Couteaux R, Janmot C, Roulet A, Mira JC. 163.  1988. Regeneration after cardiotoxin injury of innervated and denervated slow and fast muscles of mammals. Myosin isoform analysis. Eur. J. Biochem. 174:103–10 [Google Scholar]
  164. Bryan BA, Walshe TE, Mitchell DC, Havumaki JS, Saint-Geniez M. 164.  et al. 2008. Coordinated vascular endothelial growth factor expression and signaling during skeletal myogenic differentiation. Mol. Biol. Cell 19:994–1006 [Google Scholar]
  165. Tengan CH, Rodrigues GS, Godinho RO. 165.  2012. Nitric oxide in skeletal muscle: role on mitochondrial biogenesis and function. Int. J. Mol. Sci. 13:17160–84 [Google Scholar]
  166. Weist MR, Wellington MS, Bermudez JE, Kostrominova TY, Mendias CL. 166.  et al. 2013. TGF-β1 enhances contractility in engineered skeletal muscle. J. Tissue Eng. Regen. Med. 7:562–71 [Google Scholar]
  167. Vandenburgh H, Shansky J, Benesch-Lee F, Barbata V, Reid J. 167.  et al. 2008. Drug-screening platform based on the contractility of tissue-engineered muscle. Muscle Nerve 37:438–47 [Google Scholar]
  168. Griffith LG, Naughton G. 168.  2002. Tissue engineering—current challenges and expanding opportunities. Science 295:1009–14 [Google Scholar]
  169. Acker JP. 169.  2007. Biopreservation of cells and engineered tissues. Adv. Biochem. Eng. Biotechnol. 103:157–87 [Google Scholar]
  170. Karlsson JO, Toner M. 170.  1996. Long-term storage of tissues by cryopreservation: critical issues. Biomaterials 17:243–56 [Google Scholar]
  171. Thorrez L, Shansky J, Wang L, Fast L, VandenDriessche T. 171.  et al. 2008. Growth, differentiation, transplantation and survival of human skeletal myofibers on biodegradable scaffolds. Biomaterials 29:75–84 [Google Scholar]
  172. Rossi CA, Flaibani M, Blaauw B, Pozzobon M, Figallo E. 172.  et al. 2011. In vivo tissue engineering of functional skeletal muscle by freshly isolated satellite cells embedded in a photopolymerizable hydrogel. FASEB J. 25:2296–304 [Google Scholar]
  173. Ding K, Yang Z, Zhang YL, Xu JZ. 173.  2013. Injectable thermosensitive chitosan/β-glycerophosphate/collagen hydrogel maintains the plasticity of skeletal muscle satellite cells and supports their in vivo viability. Cell Biol. Int. 37:977–87 [Google Scholar]
  174. Sicari BM, Dziki JL, Siu BF, Medberry CJ, Dearth CL, Badylak SF. 174.  2014. The promotion of a constructive macrophage phenotype by solubilized extracellular matrix. Biomaterials 35:8605–12 [Google Scholar]
  175. He WA, Berardi E, Cardillo VM, Acharyya S, Aulino P. 175.  et al. 2013. NF-κB-mediated Pax7 dysregulation in the muscle microenvironment promotes cancer cachexia. J. Clin. Investig. 123:4821–35 [Google Scholar]
  176. Bhatia SN, Ingber DE. 176.  2014. Microfluidic organs-on-chips. Nat. Biotechnol. 32:760–72 [Google Scholar]
  177. Huh D, Leslie DC, Matthews BD, Fraser JP, Jurek S. 177.  et al. 2012. A human disease model of drug toxicity-induced pulmonary edema in a lung-on-a-chip microdevice. Sci. Transl. Med. 4:159ra47 [Google Scholar]
  178. von Keutz E, Schluter G. 178.  1998. Preclinical safety evaluation of cerivastatin, a novel HMG-CoA reductase inhibitor. Am. J. Cardiol. 82:11J–17J [Google Scholar]
  179. Furberg CD, Pitt B. 179.  2001. Withdrawal of cerivastatin from the world market. Curr. Control. Trials Cardiovasc. Med. 2:205–7 [Google Scholar]
  180. Rangarajan S, Madden L, Bursac N. 180.  2014. Use of flow, electrical, and mechanical stimulation to promote engineering of striated muscles. Ann. Biomed. Eng. 42:1391–405 [Google Scholar]
  181. Cheng CS, Davis BN, Madden L, Bursac N, Truskey GA. 181.  2014. Physiology and metabolism of tissue-engineered skeletal muscle. Exp. Biol. Med.(Maywood) 239:1203–14 [Google Scholar]
  182. van der Schaft DW, van Spreeuwel AC, van Assen HC, Baaijens FP. 182.  2011. Mechanoregulation of vascularization in aligned tissue-engineered muscle: a role for vascular endothelial growth factor. Tissue Eng. Part A 17:2857–65 [Google Scholar]
  183. Gundersen K. 183.  2011. Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol. Rev. Camb. Philos. Soc. 86:564–600 [Google Scholar]
  184. Westgaard RH, Lomo T. 184.  1988. Control of contractile properties within adaptive ranges by patterns of impulse activity in the rat. J. Neurosci. 8:4415–26 [Google Scholar]
  185. Raben N, Fukuda T, Gilbert AL, de Jong D, Thurberg BL. 185.  et al. 2005. Replacing acid α-glucosidase in Pompe disease: recombinant and transgenic enzymes are equipotent, but neither completely clears glycogen from type II muscle fibers. Mol. Ther. 11:48–56 [Google Scholar]
  186. Webster C, Silberstein L, Hays AP, Blau HM. 186.  1988. Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 52:503–13 [Google Scholar]
  187. Tian L, George SC. 187.  2011. Biomaterials to prevascularize engineered tissues. J. Cardiovasc. Transl. Res. 4:685–98 [Google Scholar]
  188. Renault MA, Vandierdonck S, Chapouly C, Yu Y, Qin G. 188.  et al. 2013. Gli3 regulation of myogenesis is necessary for ischemia-induced angiogenesis. Circ. Res. 113:1148–58 [Google Scholar]
  189. Mounier R, Chretien F, Chazaud B. 189.  2011. Blood vessels and the satellite cell niche. Curr. Top. Dev. Biol. 96:121–38 [Google Scholar]
  190. Lee SL, Pevec WC, Carlsen RC. 190.  2001. Functional outcome of new blood vessel growth into ischemic skeletal muscle. J. Vasc. Surg. 34:1096–102 [Google Scholar]
/content/journals/10.1146/annurev-bioeng-071114-040640
Loading
/content/journals/10.1146/annurev-bioeng-071114-040640
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error