Skip to main content

Advertisement

SpringerLink
Log in

Striated muscle function, regeneration, and repair

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

As the only striated muscle tissues in the body, skeletal and cardiac muscle share numerous structural and functional characteristics, while exhibiting vastly different size and regenerative potential. Healthy skeletal muscle harbors a robust regenerative response that becomes inadequate after large muscle loss or in degenerative pathologies and aging. In contrast, the mammalian heart loses its regenerative capacity shortly after birth, leaving it susceptible to permanent damage by acute injury or chronic disease. In this review, we compare and contrast the physiology and regenerative potential of native skeletal and cardiac muscles, mechanisms underlying striated muscle dysfunction, and bioengineering strategies to treat muscle disorders. We focus on different sources for cellular therapy, biomaterials to augment the endogenous regenerative response, and progress in engineering and application of mature striated muscle tissues in vitro and in vivo. Finally, we discuss the challenges and perspectives in translating muscle bioengineering strategies to clinical practice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

CM:

Cardiomyocyte

CSC:

Cardiac stem cell

CV:

Conduction velocity

CHD:

Congenital heart defect

DGC:

Dystrophin-associated glycoprotein complex

ECM:

Extracellular matrix

FAP:

Fibroadipogenic progenitors

hESC:

Human embryonic stem cell

hiPSC:

Human induced pluripotent stem cell

mESC-CM:

Mouse embryonic stem cell-derived cardiomyocyte

MHC:

Myosin heavy chain

MMP:

Matrix metalloproteinase

MSC:

Mesenchymal stem cells

NRVM:

Neonatal rat ventricular myocyte

PIC:

Pw1 interstitial cell

RyR:

Ryanodine receptor

SR:

Sarcoplasmic reticulum

SERCA:

Sarcoplasmic reticulum Ca2+ ATPase

SC:

Satellite cell

SIS:

Small intestine submucosa

T-tubule:

Transverse tubule

References

  1. Schiaffino S, Reggiani C (2011) Fiber types in mammalian skeletal muscles. Physiol Rev 91:1447–1531

    Article  CAS  PubMed  Google Scholar 

  2. Janssen I, Heymsfield SB, Wang ZM, Ross R (1985) Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol 2000(89):81–88

    Google Scholar 

  3. Arnold HD (1899) Weight of the “Normal” Heart in Adults. J Boston Soc Med Sci 3:174–184

    PubMed  PubMed Central  Google Scholar 

  4. Dumont NA, Wang YX, Rudnicki MA (2015) Intrinsic and extrinsic mechanisms regulating satellite cell function. Development 142:1572–1581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Uygur A, Lee RT (2016) Mechanisms of Cardiac Regeneration. Dev Cell 36:362–374

    Article  CAS  PubMed  Google Scholar 

  6. Wallace GQ, McNally EM (2009) Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu Rev Physiol 71:37–57

    Article  CAS  PubMed  Google Scholar 

  7. DiMauro S, Spiegel R (2011) Progress and problems in muscle glycogenoses. Acta Myol 30:96–102

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Grogan BF, Hsu JR (2011) Skeletal trauma research C. Volumetric muscle loss. J Am Acad Orthop Surg 19(Suppl 1):S35–S37

    Article  PubMed  Google Scholar 

  9. Mann CJ, Perdiguero E, Kharraz Y, Aguilar S, Pessina P, Serrano AL et al (2011) Aberrant repair and fibrosis development in skeletal muscle. Skelet Muscle 1:21

    Article  PubMed  PubMed Central  Google Scholar 

  10. Jessup M, Brozena S (2003) Heart failure. N Engl J Med 348:2007–2018

    Article  PubMed  Google Scholar 

  11. Fahed AC, Gelb BD, Seidman JG, Seidman CE (2013) Genetics of congenital heart disease: the glass half empty. Circ Res 112:707–720

    Article  CAS  PubMed  Google Scholar 

  12. Hanson J, Huxley HE (1953) Structural basis of the cross-striations in muscle. Nature 172:530–532

    Article  CAS  PubMed  Google Scholar 

  13. Huxley HE (1953) Electron microscope studies of the organisation of the filaments in striated muscle. Biochim Biophys Acta 12:387–394

    Article  CAS  PubMed  Google Scholar 

  14. Luther PK (2009) The vertebrate muscle Z-disc: sarcomere anchor for structure and signalling. J Muscle Res Cell Motil 30:171–185

    Article  PubMed  PubMed Central  Google Scholar 

  15. Knöll R, Buyandelger B, Lab M (2011) The sarcomeric Z-disc and Z-discopathies. J Biomed Biotechnol 2011:569628

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Al-Qusairi L, Laporte J (2011) T-tubule biogenesis and triad formation in skeletal muscle and implication in human diseases. Skelet Muscle 1:26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Fill M, Copello JA (2002) Ryanodine receptor calcium release channels. Physiol Rev 82:893–922

    Article  CAS  PubMed  Google Scholar 

  18. Schiaffino S, Margreth A (1969) Coordinated development of the sarcoplasmic reticulum and T system during postnatal differentiation of rat skeletal muscle. J Cell Biol 41:855–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Franzini-Armstrong C, Ferguson DG, Champ C (1988) Discrimination between fast- and slow-twitch fibres of guinea pig skeletal muscle using the relative surface density of junctional transverse tubule membrane. J Muscle Res Cell Motil 9:403–414

    Article  CAS  PubMed  Google Scholar 

  20. Sawada K, Kawamura K (1991) Architecture of myocardial cells in human cardiac ventricles with concentric and eccentric hypertrophy as demonstrated by quantitative scanning electron microscopy. Heart Vessels 6:129–142

    Article  CAS  PubMed  Google Scholar 

  21. Mollova M, Bersell K, Walsh S, Savla J, Das LT, Park SY et al (2013) Cardiomyocyte proliferation contributes to heart growth in young humans. Proc Natl Acad Sci USA 110:1446–1451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Soonpaa MH, Kim KK, Pajak L, Franklin M, Field LJ (1996) Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol 271:H2183–H2189

    CAS  PubMed  Google Scholar 

  23. Venable JH (1966) Constant cell populations in normal, testosterone-deprived and testosterone-stimulated levator ani muscles. Am J Anat 119:263–270

    Article  CAS  PubMed  Google Scholar 

  24. Enesco M, Puddy D (1964) Increase in the Number of Nuclei and Weight in Skeletal Muscle of Rats of Various Ages. Am J Anat 114:235–244

    Article  CAS  PubMed  Google Scholar 

  25. Banerjee I, Fuseler JW, Price RL, Borg TK, Baudino TA (2007) Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol 293:H1883–H1891

    Article  CAS  PubMed  Google Scholar 

  26. Souders CA, Borg TK, Banerjee I, Baudino TA (2012) Pressure overload induces early morphological changes in the heart. Am J Pathol 181:1226–1235

    Article  PubMed  PubMed Central  Google Scholar 

  27. Bergmann O, Zdunek S, Felker A, Salehpour M, Alkass K, Bernard S et al (2015) Dynamics of cell generation and turnover in the human heart. Cell 161:1566–1575

    Article  CAS  PubMed  Google Scholar 

  28. Pinto AR, Ilinykh A, Ivey MJ, Kuwabara JT, D’Antoni ML, Debuque R et al (2016) Revisiting cardiac cellular composition. Circ Res 118:400–409

    Article  CAS  PubMed  Google Scholar 

  29. Gaudesius G, Miragoli M, Thomas SP, Rohr S (2003) Coupling of cardiac electrical activity over extended distances by fibroblasts of cardiac origin. Circ Res 93:421–428

    Article  CAS  PubMed  Google Scholar 

  30. McSpadden LC, Kirkton RD, Bursac N (2009) Electrotonic loading of anisotropic cardiac monolayers by unexcitable cells depends on connexin type and expression level. Am J Physiol Cell Physiol 297:C339–C351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Rohr S (2012) Arrhythmogenic implications of fibroblast-myocyte interactions. Circ Arrhyth Electrophysiol 5:442–452

    Article  Google Scholar 

  32. Ongstad E, Kohl P (2016) Fibroblast-myocyte coupling in the heart: Potential relevance for therapeutic interventions. J Mol Cell Cardiol 91:238–246

    Article  CAS  PubMed  Google Scholar 

  33. Bourdeau-Martini J, Odoroff CL, Honig CR (1974) Dual effect of oxygen on magnitude and uniformity of coronary intercapillary distance. Am J Physiol 226:800–810

    CAS  PubMed  Google Scholar 

  34. Korthuis RJ (2011) Skeletal Muscle Circulation. San Rafael

  35. Andersen P, Kroese AJ (1978) Capillary supply in soleus and gastrocnemius muscles of man. Pflugers Arch 375:245–249

    Article  CAS  PubMed  Google Scholar 

  36. Poole DC, Mathieu-Costello O (1989) Skeletal muscle capillary geometry: adaptation to chronic hypoxia. Respir Physiol 77:21–29

    Article  CAS  PubMed  Google Scholar 

  37. Poole DC, Mathieu-Costello O (1990) Analysis of capillary geometry in rat subepicardium and subendocardium. Am J Physiol 259:H204–H210

    CAS  PubMed  Google Scholar 

  38. Layland J, Kentish JC (1999) Positive force- and [Ca2+]i-frequency relationships in rat ventricular trabeculae at physiological frequencies. Am J Physiol 276:H9–H18

    CAS  PubMed  Google Scholar 

  39. Henneman E, Somjen G, Carpenter DO (1965) Excitability and inhibitability of motoneurons of different sizes. J Neurophysiol 28:599–620

    CAS  PubMed  Google Scholar 

  40. Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255–318

    CAS  PubMed  Google Scholar 

  41. Allen DG, Kentish JC (1985) The cellular basis of the length-tension relation in cardiac muscle. J Mol Cell Cardiol 17:821–840

    Article  CAS  PubMed  Google Scholar 

  42. Granzier HL, Irving TC (1995) Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys J 68:1027–1044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Lepper C, Partridge TA, Fan CM (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138:3639–3646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Sambasivan R, Comai G, Le Roux I, Gomes D, Konge J, Dumas G et al (2013) Embryonic founders of adult muscle stem cells are primed by the determination gene Mrf4. Dev Biol 381:241–255

    Article  CAS  PubMed  Google Scholar 

  46. Biressi S, Bjornson CR, Carlig PM, Nishijo K, Keller C, Rando TA (2013) Myf5 expression during fetal myogenesis defines the developmental progenitors of adult satellite cells. Dev Biol 379:195–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kuang S, Kuroda K, Le Grand F, Rudnicki MA (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129:999–1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Cossu G, Tajbakhsh S (2007) Oriented cell divisions and muscle satellite cell heterogeneity. Cell 129:859–861

    Article  CAS  PubMed  Google Scholar 

  49. Gunther S, Kim J, Kostin S, Lepper C, Fan CM, Braun T (2013) Myf5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells. Cell Stem Cell 13:590–601

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Charge SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238

    Article  CAS  PubMed  Google Scholar 

  51. Yin H, Price F, Rudnicki MA (2013) Satellite cells and the muscle stem cell niche. Physiol Rev 93:23–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Leri A, Rota M, Pasqualini FS, Goichberg P, Anversa P (2015) Origin of cardiomyocytes in the adult heart. Circ Res 116:150–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. van Berlo JH, Molkentin JD (2016) Most of the Dust Has Settled: cKit+ Progenitor Cells Are an Irrelevant Source of Cardiac Myocytes In Vivo. Circ Res 118:17–19

    Article  PubMed  CAS  Google Scholar 

  54. Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, Plonquet A et al (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204:1057–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Madaro L, Bouche M (2014) From innate to adaptive immune response in muscular dystrophies and skeletal muscle regeneration: the role of lymphocytes. Biomed Res Int 2014:438675

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Aurora AB, Olson EN (2014) Immune modulation of stem cells and regeneration. Cell Stem Cell 15:14–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Webster MT, Manor U, Lippincott-Schwartz J, Fan CM (2016) Intravital Imaging Reveals Ghost Fibers as Architectural Units Guiding Myogenic Progenitors during Regeneration. Cell Stem Cell 18:243–252

    Article  CAS  PubMed  Google Scholar 

  58. Saclier M, Cuvellier S, Magnan M, Mounier R, Chazaud B (2013) Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration. FEBS J 280:4118–4130

    Article  CAS  PubMed  Google Scholar 

  59. Joe AW, Yi L, Natarajan A, Le Grand F, So L, Wang J et al (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12:153–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Heredia JE, Mukundan L, Chen FM, Mueller AA, Deo RC, Locksley RM et al (2013) Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell 153:376–388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Foglia MJ, Poss KD (2016) Building and re-building the heart by cardiomyocyte proliferation. Development 143:729–740

    Article  CAS  PubMed  Google Scholar 

  62. Haubner BJ, Schneider J, Schweigmann U, Schuetz T, Dichtl W, Velik-Salchner C et al (2016) Functional recovery of a human neonatal heart after severe myocardial infarction. Circ Res 118:216–221

    Article  CAS  PubMed  Google Scholar 

  63. Xin M, Olson EN, Bassel-Duby R (2013) Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair. Nat Rev Mol Cell Biol 14:529–541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Aurora AB, Porrello ER, Tan W, Mahmoud AI, Hill JA, Bassel-Duby R et al (2014) Macrophages are required for neonatal heart regeneration. J Clin Investig 124:1382–1392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Sutton MG, Sharpe N (2000) Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation 101:2981–2988

    Article  CAS  PubMed  Google Scholar 

  66. Morrison JI, Loof S, He P, Simon A (2006) Salamander limb regeneration involves the activation of a multipotent skeletal muscle satellite cell population. J Cell Biol 172:433–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Poss KD, Keating MT, Nechiporuk A (2003) Tales of regeneration in zebrafish. Dev Dyn 226:202–210

    Article  PubMed  Google Scholar 

  68. Turner NJ, Badylak SF (2012) Regeneration of skeletal muscle. Cell Tissue Res 347:759–774

    Article  PubMed  Google Scholar 

  69. Janssen I, Shepard DS, Katzmarzyk PT, Roubenoff R (2004) The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc 52:80–85

    Article  PubMed  Google Scholar 

  70. Berger MJ, Doherty TJ (2010) Sarcopenia: prevalence, mechanisms, and functional consequences. Interdiscip Top Gerontol 37:94–114

    Article  PubMed  Google Scholar 

  71. Ryall JG, Schertzer JD, Lynch GS (2008) Cellular and molecular mechanisms underlying age-related skeletal muscle wasting and weakness. Biogerontology 9:213–228

    Article  CAS  PubMed  Google Scholar 

  72. Morse CI, Thom JM, Reeves ND, Birch KM, Narici MV (1985) In vivo physiological cross-sectional area and specific force are reduced in the gastrocnemius of elderly men. J Appl Physiol 2005(99):1050–1055

    Google Scholar 

  73. Hughes VA, Frontera WR, Wood M, Evans WJ, Dallal GE, Roubenoff R et al (2001) Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health. J Gerontol A Biol Sci Med Sci 56:B209–B217

    Article  CAS  PubMed  Google Scholar 

  74. Porter MM, Vandervoort AA, Lexell J (1995) Aging of human muscle: structure, function and adaptability. Scand J Med Sci Sports 5:129–142

    Article  CAS  PubMed  Google Scholar 

  75. Cosgrove BD, Gilbert PM, Porpiglia E, Mourkioti F, Lee SP, Corbel SY et al (2014) Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat Med 20:255–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Bernet JD, Doles JD, Hall JK (2014) Kelly Tanaka K, Carter TA, Olwin BB. p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat Med 20:265–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Johnson NB, Hayes LD, Brown K, Hoo EC, Ethier KA, Centers for Disease C et al (2014) CDC national health report: leading causes of morbidity and mortality and associated behavioral risk and protective factors–United States, 2005–2013. Morb Mort Week Rep Surveill Summ 63(Suppl 4):3–27

    Google Scholar 

  78. Satpathy C, Mishra TK, Satpathy R, Satpathy HK, Barone E (2006) Diagnosis and management of diastolic dysfunction and heart failure. Am Fam Physician 73:841–846

    PubMed  Google Scholar 

  79. Yang Q, Chen H, Correa A, Devine O, Mathews TJ, Honein MA (2006) Racial differences in infant mortality attributable to birth defects in the United States, 1989–2002. Birth Defects Res A 76:706–713

    Article  CAS  Google Scholar 

  80. Hoffman JI, Kaplan S (2002) The incidence of congenital heart disease. J Am Coll Cardiol 39:1890–1900

    Article  PubMed  Google Scholar 

  81. Avolio E, Caputo M, Madeddu P (2015) Stem cell therapy and tissue engineering for correction of congenital heart disease. Front Cell Dev Biol 3

  82. Mercuri E, Muntoni F (2013) Muscular dystrophy: new challenges and review of the current clinical trials. Curr Opin Pediatr 25:701–707

    Article  CAS  PubMed  Google Scholar 

  83. Lapidos KA, Kakkar R, McNally EM (2004) The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res 94:1023–1031

    Article  CAS  PubMed  Google Scholar 

  84. Gaeta M, Messina S, Mileto A, Vita GL, Ascenti G, Vinci S et al (2012) Muscle fat-fraction and mapping in Duchenne muscular dystrophy: evaluation of disease distribution and correlation with clinical assessments. Preliminary experience. Skeletal Radiol 41:955–961

    Article  PubMed  Google Scholar 

  85. Khurana TS, Prendergast RA, Alameddine HS, Tome FM, Fardeau M, Arahata K et al (1995) Absence of extraocular muscle pathology in Duchenne’s muscular dystrophy: role for calcium homeostasis in extraocular muscle sparing. J Exp Med 182:467–475

    Article  CAS  PubMed  Google Scholar 

  86. Goldstein JA, McNally EM (2010) Mechanisms of muscle weakness in muscular dystrophy. J General Physiol 136:29–34

    Article  CAS  Google Scholar 

  87. Kim HK, Laor T, Horn PS, Racadio JM, Wong B, Dardzinski BJ (2010) T2 mapping in Duchenne muscular dystrophy: distribution of disease activity and correlation with clinical assessments. Radiology 255:899–908

    Article  PubMed  Google Scholar 

  88. Kinali M, Arechavala-Gomeza V, Cirak S, Glover A, Guglieri M, Feng L et al (2011) Muscle histology vs MRI in Duchenne muscular dystrophy. Neurology 76:346–353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. McNally EM, Pytel P (2007) Muscle diseases: the muscular dystrophies. Annu Rev Pathol 2:87–109

    Article  CAS  PubMed  Google Scholar 

  90. Melacini P, Fanin M, Danieli GA, Villanova C, Martinello F, Miorin M et al (1996) Myocardial involvement is very frequent among patients affected with subclinical Becker’s muscular dystrophy. Circulation 94:3168–3175

    Article  CAS  PubMed  Google Scholar 

  91. Verhaert D, Richards K, Rafael-Fortney JA, Raman SV (2011) Cardiac involvement in patients with muscular dystrophies: magnetic resonance imaging phenotype and genotypic considerations. Circ Cardiovas Imaging 4:67–76

    Article  Google Scholar 

  92. Mouly V, Aamiri A, Perie S, Mamchaoui K, Barani A, Bigot A et al (2005) Myoblast transfer therapy: is there any light at the end of the tunnel? Acta Myol 24:128–133

    CAS  PubMed  Google Scholar 

  93. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A et al (2005) Direct isolation of satellite cells for skeletal muscle regeneration. Science 309:2064–2067

    Article  CAS  PubMed  Google Scholar 

  94. Machida S, Spangenburg EE, Booth FW (2004) Primary rat muscle progenitor cells have decreased proliferation and myotube formation during passages. Cell Prolif 37:267–277

    Article  CAS  PubMed  Google Scholar 

  95. Beauchamp JR, Morgan JE, Pagel CN, Partridge TA (1999) Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source. J Cell Biol 144:1113–1121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Ono Y, Masuda S, Nam HS, Benezra R, Miyagoe-Suzuki Y, Takeda S (2012) Slow-dividing satellite cells retain long-term self-renewal ability in adult muscle. J Cell Sci 125:1309–1317

    Article  CAS  PubMed  Google Scholar 

  97. Engler AJ, Griffin MA, Sen S, Bonnemann CG, Sweeney HL, Discher DE (2004) Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 166:877–887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Gilbert PM, Havenstrite KL, Magnusson KE, Sacco A, Leonardi NA, Kraft P et al (2010) Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329:1078–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Périé S, Trollet C, Mouly V, Vanneaux V, Mamchaoui K, Bouazza B et al (2014) Autologous myoblast transplantation for oculopharyngeal muscular dystrophy: a phase I/IIa clinical study. Mol Ther 22:219–225

    Article  PubMed  CAS  Google Scholar 

  100. Barberi T, Bradbury M, Dincer Z, Panagiotakos G, Socci ND, Studer L (2007) Derivation of engraftable skeletal myoblasts from human embryonic stem cells. Nat Med 13:642–648

    Article  CAS  PubMed  Google Scholar 

  101. Darabi R, Arpke RW, Irion S, Dimos JT, Grskovic M, Kyba M et al (2012) Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 10:610–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Darabi R, Santos FN, Filareto A, Pan W, Koene R, Rudnicki MA et al (2011) Assessment of the myogenic stem cell compartment following transplantation of Pax3/Pax7-induced embryonic stem cell-derived progenitors. Stem Cells 29:777–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Darabi R, Pan W, Bosnakovski D, Baik J, Kyba M, Perlingeiro RC (2011) Functional Myogenic Engraftment from Mouse iPS Cells. Stem Cell Rev 7:948–957

    Article  PubMed  PubMed Central  Google Scholar 

  104. Abujarour R, Bennett M, Valamehr B, Lee TT, Robinson M, Robbins D et al (2014) Myogenic differentiation of muscular dystrophy-specific induced pluripotent stem cells for use in drug discovery. Stem Cells Trans Med 3:149–160

    Article  CAS  Google Scholar 

  105. Albini S, Coutinho P, Malecova B, Giordani L, Savchenko A, Forcales SV et al (2013) Epigenetic reprogramming of human embryonic stem cells into skeletal muscle cells and generation of contractile myospheres. Cell Rep 3:661–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Goudenege S, Lebel C, Huot NB, Dufour C, Fujii I, Gekas J et al (2012) Myoblasts derived from normal hESCs and dystrophic hiPSCs efficiently fuse with existing muscle fibers following transplantation. Mol Ther 20:2153–2167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Shelton M, Metz J, Liu J, Carpenedo RL, Demers SP, Stanford WL et al (2014) Derivation and expansion of PAX7-positive muscle progenitors from human and mouse embryonic stem cells. Stem Cell Rep 3:516–529

    Article  CAS  Google Scholar 

  108. Borchin B, Chen J, Barberi T (2013) Derivation and FACS-mediated purification of PAX3 +/PAX7 + skeletal muscle precursors from human pluripotent stem cells. Stem Cell Reports. 1:620–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Xu C, Tabebordbar M, Iovino S, Ciarlo C, Liu J, Castiglioni A et al (2013) A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species. Cell 155:909–921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Chal J, Oginuma M, Al Tanoury Z, Gobert B, Sumara O, Hick A et al (2015) Differentiation of pluripotent stem cells to muscle fiber to model Duchenne muscular dystrophy. Nat Biotechnol 33:962–969

    Article  CAS  PubMed  Google Scholar 

  111. Relaix F, Weng X, Marazzi G, Yang E, Copeland N, Jenkins N et al (1996) Pw1, a novel zinc finger gene implicated in the myogenic and neuronal lineages. Dev Biol 177:383–396

    Article  CAS  PubMed  Google Scholar 

  112. Mitchell KJ, Pannerec A, Cadot B, Parlakian A, Besson V, Gomes ER et al (2010) Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol 12:257–266

    CAS  PubMed  Google Scholar 

  113. Arrighi N, Moratal C, Clement N, Giorgetti-Peraldi S, Peraldi P, Loubat A et al (2015) Characterization of adipocytes derived from fibro/adipogenic progenitors resident in human skeletal muscle. Cell Death Dis 6:e1733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K (2010) Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 12:143–152

    Article  CAS  PubMed  Google Scholar 

  115. Mozzetta C, Consalvi S, Saccone V, Tierney M, Diamantini A, Mitchell KJ et al (2013) Fibroadipogenic progenitors mediate the ability of HDAC inhibitors to promote regeneration in dystrophic muscles of young, but not old Mdx mice. EMBO Mol Med 5:626–639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Formicola L, Marazzi G, Sassoon DA (2014) The extraocular muscle stem cell niche is resistant to ageing and disease. Front Aging Neurosci 6:328

    Article  PubMed  PubMed Central  Google Scholar 

  117. Tonlorenzi R, Dellavalle A, Schnapp E, Cossu G, Sampaolesi M (2007) Isolation and characterization of mesoangioblasts from mouse, dog, and human tissues. Curr Protoc Stem Cell Biol 2 (Unit 2B 1)

  118. Minasi MG, Riminucci M, De Angelis L, Borello U, Berarducci B, Innocenzi A et al (2002) The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129:2773–2783

    CAS  PubMed  Google Scholar 

  119. De Angelis L, Berghella L, Coletta M, Lattanzi L, Zanchi M, Cusella-De Angelis MG et al (1999) Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J Cell Biol 147:869–878

    Article  PubMed  PubMed Central  Google Scholar 

  120. Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A et al (2013) Skeletal muscle pericyte subtypes differ in their differentiation potential. Stem Cell Res 10:67–84

    Article  CAS  PubMed  Google Scholar 

  121. Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L et al (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9:255–267

    Article  CAS  PubMed  Google Scholar 

  122. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313

    Article  CAS  PubMed  Google Scholar 

  123. Tedesco FS, Cossu G (2012) Stem cell therapies for muscle disorders. Curr Opin Neurol 25:597–603

    Article  PubMed  Google Scholar 

  124. Tedesco FS, Gerli MF, Perani L, Benedetti S, Ungaro F, Cassano M et al (2012) Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Sci Trans Med 4:140ra89

  125. Sampaolesi M, Blot S, D’Antona G, Granger N, Tonlorenzi R, Innocenzi A et al (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444:574–579

    Article  CAS  PubMed  Google Scholar 

  126. Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D’Antona G, Pellegrino MA et al (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301:487–492

    Article  CAS  PubMed  Google Scholar 

  127. Quattrocelli M, Swinnen M, Giacomazzi G, Camps J, Barthelemy I, Ceccarelli G et al (2015) Mesodermal iPSC-derived progenitor cells functionally regenerate cardiac and skeletal muscle. J Clin Investig 125:4463–4482

    Article  PubMed  PubMed Central  Google Scholar 

  128. Bonfanti C, Rossi G, Tedesco FS, Giannotta M, Benedetti S, Tonlorenzi R et al (2015) PW1/Peg3 expression regulates key properties that determine mesoangioblast stem cell competence. Nat Commun. 6:6364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Alrefai MT, Murali D, Paul A, Ridwan KM, Connell JM, Shum-Tim D (2015) Cardiac tissue engineering and regeneration using cell-based therapy. Stem Cells Cloning Adv Appl 8:81–101

    Google Scholar 

  130. Wang X, Zhang J, Zhang F, Li J, Li Y, Tan Z et al (2015) The clinical status of stem cell therapy for ischemic cardiomyopathy. Stem Cells Int 2015:135023

    PubMed  PubMed Central  Google Scholar 

  131. Menasché P, Hagège AA, Scorsin M, Pouzet B, Desnos M, Duboc D et al (2001) Myoblast transplantation for heart failure. Lancet 357:279–280

    Article  PubMed  Google Scholar 

  132. Siminiak T, Kalawski R, Fiszer D, Jerzykowska O, Rzeźniczak J, Rozwadowska N et al (2004) Autologous skeletal myoblast transplantation for the treatment of postinfarction myocardial injury: phase I clinical study with 12 months of follow-up. Am Heart J 148:531–537

    Article  PubMed  Google Scholar 

  133. Hagège AA, Marolleau JP, Vilquin JT, Alhéritière A, Peyrard S, Duboc D et al (2006) Skeletal myoblast transplantation in ischemic heart failure: long-term follow-up of the first phase I cohort of patients. Circulation 114:I108–I113

    Article  PubMed  Google Scholar 

  134. Menasche P, Alfieri O, Janssens S, McKenna W, Reichenspurner H, Trinquart L et al (2008) The Myoblast Autologous Grafting in Ischemic Cardiomyopathy (MAGIC) Trial. First Randomized Placebo-Controlled Study of Myoblast Transplantation. Circulation

  135. Duckers HJ, Houtgraaf J, Hehrlein C, Schofer J, Waltenberger J, Gershlick A et al (2011) Final results of a phase IIa, randomised, open-label trial to evaluate the percutaneous intramyocardial transplantation of autologous skeletal myoblasts in congestive heart failure patients: the SEISMIC trial. EuroIntervention 6:805–812

    Article  PubMed  Google Scholar 

  136. Reinecke H, Murry CE (2000) Transmural replacement of myocardium after skeletal myoblast grafting into the heart. Too much of a good thing? Cardiovasc Pathol 9:337–344

    Article  CAS  PubMed  Google Scholar 

  137. Farahmand P, Lai TY, Weisel RD, Fazel S, Yau T, Menasche P et al (2008) Skeletal myoblasts preserve remote matrix architecture and global function when implanted early or late after coronary ligation into infarcted or remote myocardium. Circulation 118:S130–S137

    Article  PubMed  Google Scholar 

  138. Shintani Y, Fukushima S, Varela-Carver A, Lee J, Coppen SR, Takahashi K et al (2009) Donor cell-type specific paracrine effects of cell transplantation for post-infarction heart failure. J Mol Cell Cardiol 47:288–295

    Article  CAS  PubMed  Google Scholar 

  139. Dimmeler S, Zeiher AM (2009) Cell therapy of acute myocardial infarction: open questions. Cardiology 113:155–160

    Article  PubMed  Google Scholar 

  140. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317

    Article  CAS  PubMed  Google Scholar 

  141. Mizuno H, Tobita M, Uysal AC (2012) Concise review: Adipose-derived stem cells as a novel tool for future regenerative medicine. Stem Cells 30:804–810

    Article  CAS  PubMed  Google Scholar 

  142. Jeevanantham V, Butler M, Saad A, Abdel-Latif A, Zuba-Surma EK, Dawn B (2012) Adult bone marrow cell therapy improves survival and induces long-term improvement in cardiac parameters: a systematic review and meta-analysis. Circulation 126:551–568

    Article  PubMed  PubMed Central  Google Scholar 

  143. Sadat K, Ather S, Aljaroudi W, Heo J, Iskandrian AE, Hage FG (2014) The effect of bone marrow mononuclear stem cell therapy on left ventricular function and myocardial perfusion. J Nuclear Cardiol Off Publ Am Soc Nuclear Cardiol 21:351–367

    Article  Google Scholar 

  144. de Jong R, Houtgraaf JH, Samiei S, Boersma E, Duckers HJ (2014) Intracoronary stem cell infusion after acute myocardial infarction: a meta-analysis and update on clinical trials. Circ Cardiovas Interven 7:156–167

    Article  CAS  Google Scholar 

  145. Fisher SA, Brunskill SJ, Doree C, Mathur A, Taggart DP, Martin-Rendon E (2014) Stem cell therapy for chronic ischaemic heart disease and congestive heart failure. Cochrane Database Syst Rev 4:CD007888

  146. Terzic A, Behfar A (2014) Regenerative heart failure therapy headed for optimization. Eur Heart J

  147. Nadal-Ginard B, Kajstura J, Leri A, Anversa P (2003) Myocyte death, growth, and regeneration in cardiac hypertrophy and failure. Circ Res 92:139–150

    Article  CAS  PubMed  Google Scholar 

  148. Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F et al (2004) Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95:911–921

    Article  CAS  PubMed  Google Scholar 

  149. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E et al (2007) Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115:896–908

    Article  PubMed  CAS  Google Scholar 

  150. Bolli R, Chugh AR, D’Amario D, Loughran JH, Stoddard MF, Ikram S et al (2011) Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 378:1847–1857

    Article  PubMed  PubMed Central  Google Scholar 

  151. Malliaras K, Makkar RR, Smith RR, Cheng K, Wu E, Bonow RO et al (2014) Intracoronary cardiosphere-derived cells after myocardial infarction: evidence of therapeutic regeneration in the final 1-year results of the CADUCEUS trial (CArdiosphere-Derived aUtologous stem CElls to reverse ventricUlar dySfunction). J Am Coll Cardiol 63:110–122

    Article  PubMed  Google Scholar 

  152. Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A et al (2001) Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Investig 108:407–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Zhang J, Wilson GF, Soerens AG, Koonce CH, Yu J, Palecek SP et al (2009) Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 104:e30–e41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. van Laake LW, Passier R, Monshouwer-Kloots J, Verkleij AJ, Lips DJ, Freund C et al (2007) Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction. Stem Cell Res. 1:9–24

    Article  PubMed  Google Scholar 

  155. Caspi O, Huber I, Kehat I, Habib M, Arbel G, Gepstein A et al (2007) Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. J Am Coll Cardiol 50:1884–1893

    Article  PubMed  Google Scholar 

  156. Laflamme MA, Gold J, Xu C, Hassanipour M, Rosler E, Police S et al (2005) Formation of human myocardium in the rat heart from human embryonic stem cells. Am J Pathol 167:663–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Fernandes S, Naumova AV, Zhu WZ, Laflamme MA, Gold J, Murry CE (2010) Human embryonic stem cell-derived cardiomyocytes engraft but do not alter cardiac remodeling after chronic infarction in rats. J Mol Cell Cardiol 49:941–949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK et al (2007) Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25:1015–1024

    Article  CAS  PubMed  Google Scholar 

  159. Shiba Y, Fernandes S, Zhu WZ, Filice D, Muskheli V, Kim J et al (2012) Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 489:322–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Shiba Y, Filice D, Fernandes S, Minami E, Dupras SK, Biber BV et al (2014) Electrical Integration of Human Embryonic Stem Cell-Derived Cardiomyocytes in a Guinea Pig Chronic Infarct Model. J Cardiovas Pharmacol Therap

  161. Ye L, Chang YH, Xiong Q, Zhang P, Zhang L, Somasundaram P et al (2014) Cardiac repair in a porcine model of acute myocardial infarction with human induced pluripotent stem cell-derived cardiovascular cells. Cell Stem Cell 15:750–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Chong JJ, Yang X, Don CW, Minami E, Liu YW, Weyers JJ et al (2014) Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510:273–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Jackman CP, Shadrin IY, Carlson AL, Bursac N (2015) Human Cardiac Tissue Engineering: from Pluripotent Stem Cells to Heart Repair. Curr Opin Chem Eng 7:57–64

    Article  PubMed  PubMed Central  Google Scholar 

  164. Sicari BM, Rubin JP, Dearth CL, Wolf MT, Ambrosio F, Boninger M et al (2014) An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss. Sci Trans Med 6:234ra58

  165. Keane TJ, Londono R, Turner NJ, Badylak SF (2012) Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 33:1771–1781

    Article  CAS  PubMed  Google Scholar 

  166. Brown BN, Valentin JE, Stewart-Akers AM, McCabe GP, Badylak SF (2009) Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30:1482–1491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Valentin JE, Stewart-Akers AM, Gilbert TW, Badylak SF (2009) Macrophage participation in the degradation and remodeling of extracellular matrix scaffolds. Tissue Eng Part A 15:1687–1694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Londono R, Badylak SF (2015) Biologic Scaffolds for Regenerative Medicine: Mechanisms of In vivo Remodeling. Ann Biomed Eng 43:577–592

    Article  PubMed  Google Scholar 

  169. Wolf MT, Daly KA, Reing JE, Badylak SF (2012) Biologic scaffold composed of skeletal muscle extracellular matrix. Biomaterials 33:2916–2925

    Article  CAS  PubMed  Google Scholar 

  170. Valentin JE, Turner NJ, Gilbert TW, Badylak SF (2010) Functional skeletal muscle formation with a biologic scaffold. Biomaterials 31:7475–7484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Corona BT, Ward CL, Baker HB, Walters TJ, Christ GJ (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 20:705–715

    CAS  PubMed  Google Scholar 

  172. Mase VJ, Jr., Hsu JR, Wolf SE, Wenke JC, Baer DG, Owens J et al (2010) Clinical application of an acellular biologic scaffold for surgical repair of a large, traumatic quadriceps femoris muscle defect. Orthopedics 33

  173. Aurora A, Garg K, Corona BT, Walters TJ (2014) Physical rehabilitation improves muscle function following volumetric muscle loss injury. BMC Sports Sci Med Rehabil 6:41

    Article  PubMed  PubMed Central  Google Scholar 

  174. Scholl FG, Boucek MM, Chan KC, Valdes-Cruz L, Perryman R (2010) Preliminary experience with cardiac reconstruction using decellularized porcine extracellular matrix scaffold: human applications in congenital heart disease. World J Pediat Congen Heart Surg 1:132–136

    Article  Google Scholar 

  175. Okada M, Payne TR, Oshima H, Momoi N, Tobita K, Huard J (2010) Differential efficacy of gels derived from small intestinal submucosa as an injectable biomaterial for myocardial infarct repair. Biomaterials 31:7678–7683

    Article  CAS  PubMed  Google Scholar 

  176. Toeg HD, Tiwari-Pandey R, Seymour R, Ahmadi A, Crowe S, Vulesevic B et al (2013) Injectable small intestine submucosal extracellular matrix in an acute myocardial infarction model. Ann Thorac Surg 96:1686–1694 (discussion 94)

  177. Tan MY, Zhi W, Wei RQ, Huang YC, Zhou KP, Tan B et al (2009) Repair of infarcted myocardium using mesenchymal stem cell seeded small intestinal submucosa in rabbits. Biomaterials 30:3234–3240

    Article  CAS  PubMed  Google Scholar 

  178. Dai W, Gerczuk P, Zhang Y, Smith L, Kopyov O, Kay GL et al (2013) Intramyocardial injection of heart tissue-derived extracellular matrix improves postinfarction cardiac function in rats. J Cardiovas Pharmacol Therap 18:270–279

    Article  Google Scholar 

  179. Singelyn JM, Sundaramurthy P, Johnson TD, Schup-Magoffin PJ, Hu DP, Faulk DM et al (2012) Catheter-deliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. J Am Coll Cardiol 59:751–763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Seif-Naraghi SB, Singelyn JM, Salvatore MA, Osborn KG, Wang JJ, Sampat U et al (2013) Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction. Sci Transl Med 5:173ra25

  181. Johnson TD, Christman KL (2013) Injectable hydrogel therapies and their delivery strategies for treating myocardial infarction. Expert Opin Drug Deliv 10:59–72

    Article  CAS  PubMed  Google Scholar 

  182. Burdick JA, Mauck RL, Gorman JH, 3rd, Gorman RC (2013) Acellular biomaterials: an evolving alternative to cell-based therapies. Sci Trans Med 5:176ps4

  183. Cohen JE, Purcell BP, MacArthur JW Jr, Mu A, Shudo Y, Patel JB et al (2014) A bioengineered hydrogel system enables targeted and sustained intramyocardial delivery of neuregulin, activating the cardiomyocyte cell cycle and enhancing ventricular function in a murine model of ischemic cardiomyopathy. Circ Heart Fail 7:619–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Miyagi Y, Chiu LL, Cimini M, Weisel RD, Radisic M, Li RK (2011) Biodegradable collagen patch with covalently immobilized VEGF for myocardial repair. Biomaterials 32:1280–1290

    Article  CAS  PubMed  Google Scholar 

  185. Miyagi Y, Zeng F, Huang XP, Foltz WD, Wu J, Mihic A et al (2010) Surgical ventricular restoration with a cell- and cytokine-seeded biodegradable scaffold. Biomaterials 31:7684–7694

    Article  CAS  PubMed  Google Scholar 

  186. Ungerleider JL, Christman KL (2014) Concise review: injectable biomaterials for the treatment of myocardial infarction and peripheral artery disease: translational challenges and progress. Stem Cells Trans Med 3:1090–1099

    Article  CAS  Google Scholar 

  187. Malliaras K, Marban E (2011) Cardiac cell therapy: where we’ve been, where we are, and where we should be headed. Br Med Bull 98:161–185

    Article  PubMed  PubMed Central  Google Scholar 

  188. Bach AD, Beier JP, Stern-Staeter J, Horch RE (2004) Skeletal muscle tissue engineering. J Cell Mol Med 8:413–422

    Article  CAS  PubMed  Google Scholar 

  189. Rosso F, Giordano A, Barbarisi M, Barbarisi A (2004) From cell-ECM interactions to tissue engineering. J Cell Physiol 199:174–180

    Article  CAS  PubMed  Google Scholar 

  190. Even-Ram S, Artym V, Yamada KM (2006) Matrix control of stem cell fate. Cell 126:645–647

    Article  CAS  PubMed  Google Scholar 

  191. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689

    Article  CAS  PubMed  Google Scholar 

  192. Berry MF, Engler AJ, Woo YJ, Pirolli TJ, Bish LT, Jayasankar V et al (2006) Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am J Physiol Heart Circ Physiol 290:H2196–H2203

    Article  CAS  PubMed  Google Scholar 

  193. Nagueh SF, Shah G, Wu Y, Torre-Amione G, King NM, Lahmers S et al (2004) Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 110:155–162

    Article  CAS  PubMed  Google Scholar 

  194. Light N, Champion AE (1984) Characterization of muscle epimysium, perimysium and endomysium collagens. Biochem J 219:1017–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  195. Vandenburgh HH, Karlisch P, Farr L (1988) Maintenance of highly contractile tissue-cultured avian skeletal myotubes in collagen gel. In Vitro Cell Dev Biol 24:166–174

    Article  CAS  PubMed  Google Scholar 

  196. Shansky J, Del Tatto M, Chromiak J, Vandenburgh H (1997) A simplified method for tissue engineering skeletal muscle organoids in vitro. In Vitro Cell Dev Biol Anim 33:659–661

    Article  CAS  PubMed  Google Scholar 

  197. Okano T, Matsuda T (1998) Tissue engineered skeletal muscle: preparation of highly dense, highly oriented hybrid muscular tissues. Cell Transpl 7:71–82

    Article  CAS  Google Scholar 

  198. Okano T, Matsuda T (1997) Hybrid muscular tissues: preparation of skeletal muscle cell-incorporated collagen gels. Cell Transpl 6:109–118

    Article  CAS  Google Scholar 

  199. Okano T, Satoh S, Oka T, Matsuda T (1997) Tissue engineering of skeletal muscle. Highly dense, highly oriented hybrid muscular tissues biomimicking native tissues. ASAIO J 43:M749–M753

    Article  CAS  PubMed  Google Scholar 

  200. Lee PH, Vandenburgh HH (2013) Skeletal muscle atrophy in bioengineered skeletal muscle: a new model system. Tissue Eng Part A 19:2147–2155

    Article  CAS  PubMed  Google Scholar 

  201. Vandenburgh H, Shansky J, Benesch-Lee F, Skelly K, Spinazzola JM, Saponjian Y et al (2009) Automated drug screening with contractile muscle tissue engineered from dystrophic myoblasts. FASEB J. 23:3325–3334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Vandenburgh H, Shansky J, Benesch-Lee F, Barbata V, Reid J, Thorrez L et al (2008) Drug-screening platform based on the contractility of tissue-engineered muscle. Muscle Nerve 37:438–447

    Article  CAS  PubMed  Google Scholar 

  203. Mudera V, Smith AS, Brady MA, Lewis MP (2010) The effect of cell density on the maturation and contractile ability of muscle derived cells in a 3D tissue-engineered skeletal muscle model and determination of the cellular and mechanical stimuli required for the synthesis of a postural phenotype. J Cell Physiol 225:646–653

    Article  CAS  PubMed  Google Scholar 

  204. Brady MA, Lewis MP, Mudera V (2008) Synergy between myogenic and non-myogenic cells in a 3D tissue-engineered craniofacial skeletal muscle construct. Journal of tissue engineering and regenerative medicine. 2:408–417

    Article  CAS  PubMed  Google Scholar 

  205. Yan W, George S, Fotadar U, Tyhovych N, Kamer A, Yost MJ et al (2007) Tissue engineering of skeletal muscle. Tissue Eng 13:2781–2790

    Article  CAS  PubMed  Google Scholar 

  206. Close RI (1972) Dynamic properties of mammalian skeletal muscles. Physiol Rev 52:129–197

    CAS  PubMed  Google Scholar 

  207. Collet JP, Shuman H, Ledger RE, Lee S, Weisel JW (2005) The elasticity of an individual fibrin fiber in a clot. Proc Natl Acad Sci USA 102:9133–9137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  208. Chiron S, Tomczak C, Duperray A, Lainé J, Bonne G, Eder A et al (2012) Complex interactions between human myoblasts and the surrounding 3D fibrin-based matrix. PLoS One 7:e36173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. Huang YC, Dennis RG, Larkin L, Baar K (2005) Rapid formation of functional muscle in vitro using fibrin gels. J Appl Physiol 98:706–713

    Article  PubMed  Google Scholar 

  210. Juhas M, Engelmayr GC Jr, Fontanella AN, Palmer GM, Bursac N (2014) Biomimetic engineered muscle with capacity for vascular integration and functional maturation in vivo. Proc Natl Acad Sci USA 111:5508–5513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Hinds S, Bian W, Dennis RG, Bursac N (2011) The role of extracellular matrix composition in structure and function of bioengineered skeletal muscle. Biomaterials 32:3575–3583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Khodabukus A, Baar K (2015) Contractile and metabolic properties of engineered skeletal muscle derived from slow and fast phenotype mouse muscle. J Cell Physiol 230:1750–1757

    Article  CAS  PubMed  Google Scholar 

  214. Khodabukus A, Baar K (2009) Regulating Fibrinolysis to Engineer Skeletal Muscle from the C2C12 Cell Line. Tissue Eng Part C Methods 15:501–511

    Article  CAS  PubMed  Google Scholar 

  215. Madden L, Juhas M, Kraus WE, Truskey GA, Bursac N (2015) Bioengineered human myobundles mimic clinical responses of skeletal muscle to drugs. Elife. 4:e04885

    Article  PubMed  PubMed Central  Google Scholar 

  216. Strohman RC, Bayne E, Spector D, Obinata T, Micou-Eastwood J, Maniotis A (1990) Myogenesis and histogenesis of skeletal muscle on flexible membranes in vitro. In Vitro Cell Dev Biol 26:201–208

    Article  CAS  PubMed  Google Scholar 

  217. Dennis RG, Kosnik PE 2nd, Gilbert ME, Faulkner JA (2001) Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. Am J Physiol Cell Physiol 280:C288–C295

    CAS  PubMed  Google Scholar 

  218. Nagamori E, Ngo TX, Takezawa Y, Saito A, Sawa Y, Shimizu T et al (2013) Network formation through active migration of human vascular endothelial cells in a multilayered skeletal myoblast sheet. Biomaterials 34:662–668

    Article  CAS  PubMed  Google Scholar 

  219. Takahashi H, Okano T (2015) Cell sheet-based tissue engineering for organizing anisotropic tissue constructs produced using microfabricated thermoresponsive substrates. Adv Healthc Mater. 4:2388–2407

    Article  CAS  PubMed  Google Scholar 

  220. Takahashi H, Shimizu T, Nakayama M, Yamato M, Okano T (2013) The use of anisotropic cell sheets to control orientation during the self-organization of 3D muscle tissue. Biomaterials 34:7372–7380

    Article  CAS  PubMed  Google Scholar 

  221. Khodabukus A, Baar K (2014) The effect of serum origin on tissue engineered skeletal muscle function. J Cell Biochem 115:2198–2207

    Article  CAS  PubMed  Google Scholar 

  222. Huang YC, Dennis RG, Baar K (2006) Cultured slow vs. fast skeletal muscle cells differ in physiology and responsiveness to stimulation. Am J Physiol Cellphysiol 291:C11–C17

    Article  CAS  Google Scholar 

  223. Li M, Dickinson CE, Finkelstein EB, Neville CM, Sundback CA (2011) The role of fibroblasts in self-assembled skeletal muscle. Tissue Eng Part A 17:2641–2650

    Article  CAS  PubMed  Google Scholar 

  224. Hinds S, Tyhovych N, Sistrunk C, Terracio L (2013) Improved tissue culture conditions for engineered skeletal muscle sheets. Sci World J 2013:370151

    Article  CAS  Google Scholar 

  225. Merceron TK, Burt M, Seol YJ, Kang HW, Lee SJ, Yoo JJ et al (2015) A 3D bioprinted complex structure for engineering the muscle-tendon unit. Biofabrication 7:035003

    Article  PubMed  CAS  Google Scholar 

  226. Ladd MR, Lee SJ, Stitzel JD, Atala A, Yoo JJ (2011) Co-electrospun dual scaffolding system with potential for muscle-tendon junction tissue engineering. Biomaterials 32:1549–1559

    Article  CAS  PubMed  Google Scholar 

  227. Larkin LM, Calve S, Kostrominova TY, Arruda EM (2006) Structure and functional evaluation of tendon-skeletal muscle constructs engineered in vitro. Tissue Eng 12:3149–3158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  228. Kostrominova TY, Calve S, Arruda EM, Larkin LM (2009) Ultrastructure of myotendinous junctions in tendon-skeletal muscle constructs engineered in vitro. Histol Histopathol 24:541–550

    PubMed  PubMed Central  Google Scholar 

  229. VanDusen KW, Syverud BC, Williams ML, Lee JD, Larkin LM (2014) Engineered Skeletal Muscle Units for Repair of Volumetric Muscle Loss in the Tibialis Anterior Muscle of a Rat. Tissue Eng Part A

  230. Das M, Rumsey JW, Bhargava N, Stancescu M, Hickman JJ (2010) A defined long-term in vitro tissue engineered model of neuromuscular junctions. Biomaterials 31:4880–4888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  231. Guo X, Gonzalez M, Stancescu M, Vandenburgh HH, Hickman JJ (2011) Neuromuscular junction formation between human stem cell-derived motoneurons and human skeletal muscle in a defined system. Biomaterials 32:9602–9611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Morimoto Y, Kato-Negishi M, Onoe H, Takeuchi S (2013) Three-dimensional neuron-muscle constructs with neuromuscular junctions. Biomaterials 34:9413–9419

    Article  CAS  PubMed  Google Scholar 

  233. Larkin LM, Van der Meulen JH, Dennis RG, Kennedy JB (2006) Functional evaluation of nerve-skeletal muscle constructs engineered in vitro. In Vitro Cell Dev Biol Anim 42:75–82

    Article  CAS  PubMed  Google Scholar 

  234. Bian W, Bursac N (2012) Soluble miniagrin enhances contractile function of engineered skeletal muscle. FASEB J 26:955–965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  235. Wang L, Shansky J, Vandenburgh H (2013) Induced formation and maturation of acetylcholine receptor clusters in a defined 3D bio-artificial muscle. Mol Neurobiol 48:397–403

    Article  CAS  PubMed  Google Scholar 

  236. Ko IK, Lee BK, Lee SJ, Andersson KE, Atala A, Yoo JJ (2013) The effect of in vitro formation of acetylcholine receptor (AChR) clusters in engineered muscle fibers on subsequent innervation of constructs in vivo. Biomaterials 34:3246–3255

    Article  CAS  PubMed  Google Scholar 

  237. Olwin BB, Arthur K, Hannon K, Hein P, McFall A, Riley B et al (1994) Role of FGFs in skeletal muscle and limb development. Mol Reprod Dev 39:90–100 (discussion-1)

  238. Tidball JG (2005) Mechanical signal transduction in skeletal muscle growth and adaptation. J Appl Physiol 98:1900–1908

    Article  CAS  PubMed  Google Scholar 

  239. Vandenburgh HH (1982) Dynamic mechanical orientation of skeletal myofibers in vitro. Dev Biol 93:438–443

    Article  CAS  PubMed  Google Scholar 

  240. Vandenburgh HH, Swasdison S, Karlisch P (1991) Computer-aided mechanogenesis of skeletal muscle organs from single cells in vitro. Faseb J. 5:2860–2867

    CAS  PubMed  Google Scholar 

  241. Powell CA, Smiley BL, Mills J, Vandenburgh HH (2002) Mechanical stimulation improves tissue-engineered human skeletal muscle. Am J Physiol Cell Physiol 283:C1557–C1565

    Article  CAS  PubMed  Google Scholar 

  242. du Moon G, Christ G, Stitzel JD, Atala A, Yoo JJ (2008) Cyclic mechanical preconditioning improves engineered muscle contraction. Tissue Eng Part A 14:473–482

    Article  CAS  Google Scholar 

  243. Harris AJ (1981) Embryonic growth and innervation of rat skeletal muscles. I. Neural regulation of muscle fibre numbers. Philos Trans R Soc Lond B Biol Sci 293:257–277

    Article  CAS  PubMed  Google Scholar 

  244. Duxson MJ, Sheard PW (1995) Formation of new myotubes occurs exclusively at the multiple innervation zones of an embryonic large muscle. Dev Dyn 204:391–405

    Article  CAS  PubMed  Google Scholar 

  245. Kern H, Boncompagni S, Rossini K, Mayr W, Fanò G, Zanin ME et al (2004) Long-term denervation in humans causes degeneration of both contractile and excitation-contraction coupling apparatus, which is reversible by functional electrical stimulation (FES): a role for myofiber regeneration? J Neuropathol Exp Neurol 63:919–931

    Article  PubMed  Google Scholar 

  246. Salmons S, Sreter FA (1976) Significance of impulse activity in the transformation of skeletal muscle type. Nature 263:30–34

    Article  CAS  PubMed  Google Scholar 

  247. Khodabukus A, Baar K (2015) Streptomycin decreases the functional shift to a slow phenotype induced by electrical stimulation in engineered muscle. Tissue Eng Part A 21:1003–1012

    Article  CAS  PubMed  Google Scholar 

  248. Khodabukus A, Baehr LM, Bodine SC, Baar K (2015) Role of Contraction Duration in Inducing Fast-To-Slow Contractile and Metabolic Protein and Functional Changes in Engineered Muscle. J Cell Physiol

  249. Khodabukus A, Baar K (2012) Defined electrical stimulation emphasizing excitability for the development and testing of engineered skeletal muscle. Tissue Eng Part C Methods 18:349–357

    Article  CAS  PubMed  Google Scholar 

  250. Donnelly K, Khodabukus A, Philp A, Deldicque L, Dennis RG, Baar K (2010) A novel bioreactor for stimulating skeletal muscle in vitro. Tissue Eng Part C Methods 16:711–718

    Article  CAS  PubMed  Google Scholar 

  251. Ito A, Yamamoto Y, Sato M, Ikeda K, Yamamoto M, Fujita H et al (2014) Induction of functional tissue-engineered skeletal muscle constructs by defined electrical stimulation. Sci Rep 4:4781

    PubMed  PubMed Central  Google Scholar 

  252. Eschenhagen T, Fink C, Remmers U, Scholz H, Wattchow J, Weil J et al (1997) Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J 11:683–694

    CAS  PubMed  Google Scholar 

  253. Bursac N, Papadaki M, Cohen RJ, Schoen FJ, Eisenberg SR, Carrier R et al (1999) Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. Am J Physiol 277:H433–H444

    CAS  PubMed  Google Scholar 

  254. Li RK, Jia ZQ, Weisel RD, Mickle DA, Choi A, Yau TM (1999) Survival and function of bioengineered cardiac grafts. Circulation 100:II63–II69

  255. Leor J, Aboulafia-Etzion S, Dar A, Shapiro L, Barbash IM, Battler A et al (2000) Bioengineered cardiac grafts: A new approach to repair the infarcted myocardium? Circulation 102:III56-II61

  256. Kofidis T, Akhyari P, Wachsmann B, Boublik J, Mueller-Stahl K, Leyh R et al (2002) A novel bioartificial myocardial tissue and its prospective use in cardiac surgery. Eur J Cardiothorac Surg 22:238–243

    Article  PubMed  Google Scholar 

  257. Zimmermann WH, Fink C, Kralisch D, Remmers U, Weil J, Eschenhagen T (2000) Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. Biotechnol Bioeng 68:106–114

    Article  CAS  PubMed  Google Scholar 

  258. Zimmermann WH, Schneiderbanger K, Schubert P, Didie M, Munzel F, Heubach JF et al (2002) Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90:223–230

    Article  CAS  PubMed  Google Scholar 

  259. Shimizu T, Yamato M, Isoi Y, Akutsu T, Setomaru T, Abe K et al (2002) Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res 90:e40

    Article  CAS  PubMed  Google Scholar 

  260. Baar K, Birla R, Boluyt MO, Borschel GH, Arruda EM, Dennis RG (2005) Self-organization of rat cardiac cells into contractile 3-D cardiac tissue. Faseb J. 19:275–277

    CAS  PubMed  Google Scholar 

  261. Black LD, Meyers JD, Weinbaum JS, Shvelidze YA, Tranquillo RT (2009) Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification. Tissue Eng Part A

  262. Hirt MN, Sorensen NA, Bartholdt LM, Boeddinghaus J, Schaaf S, Eder A et al (2012) Increased afterload induces pathological cardiac hypertrophy: a new in vitro model. Basic Res Cardiol 107:307

    Article  PubMed  PubMed Central  Google Scholar 

  263. Tao ZW, Mohamed M, Hogan M, Gutierrez L, Birla RK (2014) Optimizing a spontaneously contracting heart tissue patch with rat neonatal cardiac cells on fibrin gel. J Tissue Eng Regen Med

  264. Bian W, Jackman CP, Bursac N (2014) Controlling the structural and functional anisotropy of engineered cardiac tissues. Biofabrication 6:024109

    Article  PubMed  PubMed Central  Google Scholar 

  265. Bian W, Liau B, Badie N, Bursac N (2009) Mesoscopic hydrogel molding to control the 3D geometry of bioartificial muscle tissues. Nat Protoc 4:1522–1534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  266. Solaro RJ, Lee JA, Kentish JC, Allen DG (1988) Effects of acidosis on ventricular muscle from adult and neonatal rats. Circ Res 63:779–787

    Article  CAS  PubMed  Google Scholar 

  267. Raman S, Kelley MA, Janssen PM (2006) Effect of muscle dimensions on trabecular contractile performance under physiological conditions. Pflugers Arch 451:625–630

    Article  CAS  PubMed  Google Scholar 

  268. Radisic M, Fast VG, Sharifov OF, Iyer RK, Park H, Vunjak-Novakovic G (2009) Optical mapping of impulse propagation in engineered cardiac tissue. Tissue Eng Part A 15:851–860

    Article  CAS  PubMed  Google Scholar 

  269. Sondergaard CS, Mathews G, Wang L, Jeffreys A, Sahota A, Wood M et al (2012) Contractile and electrophysiologic characterization of optimized self-organizing engineered heart tissue. The Annals of thoracic surgery 94:1241–1248 (discussion 9)

  270. Bursac N, Loo Y, Leong K, Tung L (2007) Novel anisotropic engineered cardiac tissues: studies of electrical propagation. Biochem Biophys Res Commun 361:847–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  271. Shimizu T, Sekine H, Isoi Y, Yamato M, Kikuchi A, Okano T (2006) Long-term survival and growth of pulsatile myocardial tissue grafts engineered by the layering of cardiomyocyte sheets. Tissue Eng 12:499–507

    Article  CAS  PubMed  Google Scholar 

  272. Bian W, Badie N, Himel HDt, Bursac N (2014) Robust T-tubulation and maturation of cardiomyocytes using tissue-engineered epicardial mimetics. Biomaterials 35:3819–3828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  273. Nygren A, Kondo C, Clark RB, Giles WR (2003) Voltage-sensitive dye mapping in Langendorff-perfused rat hearts. Am J Physiol Heart Circ Physiol 284:H892–H902

    Article  CAS  PubMed  Google Scholar 

  274. Zimmermann WH, Melnychenko I, Wasmeier G, Didie M, Naito H, Nixdorff U et al (2006) Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12:452–458

    Article  CAS  PubMed  Google Scholar 

  275. Godier-Furnemont AF, Tiburcy M, Wagner E, Dewenter M, Lammle S, El-Armouche A et al (2015) Physiologic force-frequency response in engineered heart muscle by electromechanical stimulation. Biomaterials 60:82–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  276. Liau B, Christoforou N, Leong KW, Bursac N (2011) Pluripotent stem cell-derived cardiac tissue patch with advanced structure and function. Biomaterials 32:9180–9187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  277. Masumoto H, Matsuo T, Yamamizu K, Uosaki H, Narazaki G, Katayama S et al (2012) Pluripotent stem cell-engineered cell sheets reassembled with defined cardiovascular populations ameliorate reduction in infarct heart function through cardiomyocyte-mediated neovascularization. Stem Cells 30:1196–1205

    Article  CAS  PubMed  Google Scholar 

  278. Miki K, Uenaka H, Saito A, Miyagawa S, Sakaguchi T, Higuchi T et al (2012) Bioengineered myocardium derived from induced pluripotent stem cells improves cardiac function and attenuates cardiac remodeling following chronic myocardial infarction in rats. Stem Cells Transl Med 1:430–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  279. Didie M, Christalla P, Rubart M, Muppala V, Doker S, Unsold B et al (2013) Parthenogenetic stem cells for tissue-engineered heart repair. J Clin Investig 123:1285–1298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  280. Christoforou N, Liau B, Chakraborty S, Chellapan M, Bursac N, Leong KW (2013) Induced pluripotent stem cell-derived cardiac progenitors differentiate to cardiomyocytes and form biosynthetic tissues. PLoS One 8:e65963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  281. Hirt MN, Hansen A, Eschenhagen T (2014) Cardiac tissue engineering: state of the art. Circ Res 114:354–367

    Article  CAS  PubMed  Google Scholar 

  282. Kerscher P, Turnbull IC, Hodge AJ, Kim J, Seliktar D, Easley CJ et al (2015) Direct Hydrogel Encapsulation of Pluripotent Stem Cells Enables Ontomimetic Differentiation and Growth of Engineered Human Heart Tissues. Biomaterials

  283. Riegler J, Tiburcy M, Ebert A, Tzatzalos E, Raaz U, Abilez OJ et al (2015) Human engineered heart muscles engraft and survive long term in a rodent myocardial infarction model. Circ Res 117:720–730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  284. Eng G, Lee BW, Protas L, Gagliardi M, Brown K, Kass RS et al (2016) Autonomous beating rate adaptation in human stem cell-derived cardiomyocytes. Nat Commun 7:10312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  285. Guyette JP, Charest J, Mills RW, Jank B, Moser PT, Gilpin SE et al (2015) Bioengineering Human Myocardium on Native Extracellular Matrix. Circ Res

  286. Tulloch NL, Muskheli V, Razumova MV, Korte FS, Regnier M, Hauch KD et al (2011) Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res 109:47–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  287. Zhang D, Shadrin IY, Lam J, Xian HQ, Snodgrass HR, Bursac N (2013) Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 34:5813–5820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  288. Kensah G, Roa Lara A, Dahlmann J, Zweigerdt R, Schwanke K, Hegermann J et al (2013) Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue in vitro. Eur Heart J 34:1134–1146

    Article  CAS  PubMed  Google Scholar 

  289. Thavandiran N, Dubois N, Mikryukov A, Masse S, Beca B, Simmons CA et al (2013) Design and formulation of functional pluripotent stem cell-derived cardiac microtissues. Proc Natl Acad Sci USA 110:E4698–E4707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  290. Mulieri LA, Hasenfuss G, Leavitt B, Allen PD, Alpert NR (1992) Altered myocardial force-frequency relation in human heart failure. Circulation 85:1743–1750

    Article  CAS  PubMed  Google Scholar 

  291. Hasenfuss G, Mulieri L, Blanchard E, Holubarsch C, Leavitt B, Ittleman F et al (1991) Energetics of isometric force development in control and volume- overload human myocardium. Comparison with animal species. Circ Res 68:836–846

    Article  CAS  PubMed  Google Scholar 

  292. Durrer D, van Dam RT, Freud GE, Janse MJ, Meijler FL, Arzbaecher RC (1970) Total excitation of the isolated human heart. Circulation 41:899–912

    Article  CAS  PubMed  Google Scholar 

  293. Yang X, Pabon L, Murry CE (2014) Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res 114:511–523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  294. Feric NT, Radisic M (2015) Maturing human pluripotent stem cell-derived cardiomyocytes in human engineered cardiac tissues. Adv Drug Deliv Rev

  295. Yang X, Rodriguez M, Pabon L, Fischer KA, Reinecke H, Regnier M et al (2014) Tri-iodo-l-thyronine promotes the maturation of human cardiomyocytes-derived from induced pluripotent stem cells. J Mol Cell Cardiol 72:296–304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  296. Rangarajan S, Madden L, Bursac N (2014) Use of flow, electrical, and mechanical stimulation to promote engineering of striated muscles. Ann Biomed Eng 42:1391–1405

    Article  PubMed  Google Scholar 

  297. Lundy SD, Zhu W-Z, Regnier M, Laflamme MA (2013) Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev 22:1991–2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  298. Kamakura T, Makiyama T, Sasaki K, Yoshida Y, Wuriyanghai Y, Chen J et al (2013) Ultrastructural maturation of human-induced pluripotent stem cell-derived cardiomyocytes in a long-term culture. Circ J Off J Japn Circ Soc 77:1307–1314

    CAS  Google Scholar 

  299. Hirt MN, Boeddinghaus J, Mitchell A, Schaaf S, Börnchen C, Müller C et al (2014) Functional improvement and maturation of rat and human engineered heart tissue by chronic electrical stimulation. J Mol Cell Cardiol 74:151–161

    Article  CAS  PubMed  Google Scholar 

  300. Nunes SS, Miklas JW, Liu J, Aschar-Sobbi R, Xiao Y, Zhang B et al (2013) Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat Methods 10:781–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  301. Zhang Y, King OD, Rahimov F, Jones TI, Ward CW, Kerr JP et al (2014) Human skeletal muscle xenograft as a new preclinical model for muscle disorders. Hum Mol Genet 23:3180–3188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  302. Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC et al (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23:879–884

    Article  CAS  PubMed  Google Scholar 

  303. Koffler J, Kaufman-Francis K, Shandalov Y, Egozi D, Pavlov DA, Landesberg A et al (2011) Improved vascular organization enhances functional integration of engineered skeletal muscle grafts. Proc Natl Acad Sci USA 108:14789–14794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  304. Kajbafzadeh AM, Payabvash S, Salmasi AH, Sadeghi Z, Elmi A, Vejdani K et al (2007) Time-dependent neovasculogenesis and regeneration of different bladder wall components in the bladder acellular matrix graft in rats. J Surg Res 139:189–202

    Article  CAS  PubMed  Google Scholar 

  305. Criswell TL, Corona BT, Wang Z, Zhou Y, Niu G, Xu Y et al (2013) The role of endothelial cells in myofiber differentiation and the vascularization and innervation of bioengineered muscle tissue in vivo. Biomaterials 34:140–149

    Article  CAS  PubMed  Google Scholar 

  306. Borschel GH, Dow DE, Dennis RG, Brown DL (2006) Tissue-engineered axially vascularized contractile skeletal muscle. Plast Reconstr Surg 117:2235–2242

    Article  CAS  PubMed  Google Scholar 

  307. Mian R, Morrison WA, Hurley JV, Penington AJ, Romeo R, Tanaka Y et al (2000) Formation of new tissue from an arteriovenous loop in the absence of added extracellular matrix. Tissue Eng 6:595–603

    Article  CAS  PubMed  Google Scholar 

  308. Messina A, Bortolotto SK, Cassell OC, Kelly J, Abberton KM, Morrison WA (2005) Generation of a vascularized organoid using skeletal muscle as the inductive source. Faseb J. 19:1570–1572

    CAS  PubMed  Google Scholar 

  309. Bach AD, Arkudas A, Tjiawi J, Polykandriotis E, Kneser U, Horch RE et al (2006) A new approach to tissue engineering of vascularized skeletal muscle. J Cell Mol Med 10:716–726

    Article  CAS  PubMed  Google Scholar 

  310. Shandalov Y, Egozi D, Koffler J, Dado-Rosenfeld D, Ben-Shimol D, Freiman A et al (2014) An engineered muscle flap for reconstruction of large soft tissue defects. Proc Natl Acad Sci USA 111:6010–6015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  311. Dhawan V, Lytle IF, Dow DE, Huang YC, Brown DL (2007) Neurotization improves contractile forces of tissue-engineered skeletal muscle. Tissue Eng 13:2813–2821

    Article  CAS  PubMed  Google Scholar 

  312. Zhou W, He DQ, Liu JY, Feng Y, Zhang XY, Hua CG et al (2013) Angiogenic gene-modified myoblasts promote vascularization during repair of skeletal muscle defects. J Tissue Eng Regen Med

  313. Shvartsman D, Storrie-White H, Lee K, Kearney C, Brudno Y, Ho N et al (2014) Sustained delivery of VEGF maintains innervation and promotes reperfusion in ischemic skeletal muscles via NGF/GDNF signaling. Mol Ther 22:1243–1253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  314. Lu Y, Shansky J, Del Tatto M, Ferland P, Wang X, Vandenburgh H (2001) Recombinant vascular endothelial growth factor secreted from tissue-engineered bioartificial muscles promotes localized angiogenesis. Circulation 104:594–599

    Article  CAS  PubMed  Google Scholar 

  315. Borselli C, Storrie H, Benesch-Lee F, Shvartsman D, Cezar C, Lichtman JW et al (2010) Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. Proc Natl Acad Sci USA 107:3287–3292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  316. Borselli C, Cezar CA, Shvartsman D, Vandenburgh HH, Mooney DJ (2011) The role of multifunctional delivery scaffold in the ability of cultured myoblasts to promote muscle regeneration. Biomaterials 32:8905–8914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  317. Fuoco C, Rizzi R, Biondo A, Longa E, Mascaro A, Shapira-Schweitzer K et al (2015) In vivo generation of a mature and functional artificial skeletal muscle. EMBO Mol Med 7:411–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  318. Gargioli C, Coletta M, De Grandis F, Cannata SM, Cossu G (2008) PlGF-MMP-9-expressing cells restore microcirculation and efficacy of cell therapy in aged dystrophic muscle. Nat Med 14:973–978

    Article  CAS  PubMed  Google Scholar 

  319. Lesman A, Habib M, Caspi O, Gepstein A, Arbel G, Levenberg S et al (2010) Transplantation of a tissue-engineered human vascularized cardiac muscle. Tissue Eng Part A 16:115–125

    Article  CAS  PubMed  Google Scholar 

  320. Sekine H, Shimizu T, Hobo K, Sekiya S, Yang J, Yamato M et al (2008) Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 118:S145–S152

    Article  CAS  PubMed  Google Scholar 

  321. Masumoto H, Ikuno T, Takeda M, Fukushima H, Marui A, Katayama S et al (2014) Human iPS cell-engineered cardiac tissue sheets with cardiomyocytes and vascular cells for cardiac regeneration. Sci Rep 4:6716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  322. Stevens KR, Kreutziger KL, Dupras SK, Korte FS, Regnier M, Muskheli V et al (2009) Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc Natl Acad Sci USA 106:16568–16573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  323. Sun X, Altalhi W, Nunes SS (2015) Vascularization strategies of engineered tissues and their application in cardiac regeneration. Adv Drug Deliv Rev

  324. Xiong Q, Hill KL, Li Q, Suntharalingam P, Mansoor A, Wang X et al (2011) A fibrin patch-based enhanced delivery of human embryonic stem cell-derived vascular cell transplantation in a porcine model of postinfarction left ventricular remodeling. Stem Cells 29:367–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  325. Thomson KS, Korte FS, Giachelli CM, Ratner BD, Regnier M, Scatena M (2013) Prevascularized microtemplated fibrin scaffolds for cardiac tissue engineering applications. Tissue Eng Part A 19:967–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  326. Dvir T, Kedem A, Ruvinov E, Levy O, Freeman I, Landa N et al (2009) Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc Natl Acad Sci USA 106:14990–14995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  327. Gerbin KA, Yang X, Murry CE, Coulombe KL (2015) Enhanced Electrical Integration of Engineered Human Myocardium via Intramyocardial versus Epicardial Delivery in Infarcted Rat Hearts. PLoS One 10:e0131446

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  328. Menasche P, Vanneaux V, Hagege A, Bel A, Cholley B, Cacciapuoti I et al (2015) Human embryonic stem cell-derived cardiac progenitors for severe heart failure treatment: first clinical case report. Euro Heart J

  329. Miyagawa S, Sawa Y, Sakakida S, Taketani S, Kondoh H, Memon IA et al (2005) Tissue cardiomyoplasty using bioengineered contractile cardiomyocyte sheets to repair damaged myocardium: their integration with recipient myocardium. Transplantation 80:1586–1595

    Article  CAS  PubMed  Google Scholar 

  330. Sekine H, Shimizu T, Dobashi I, Matsuura K, Hagiwara N, Takahashi M et al (2011) Cardiac cell sheet transplantation improves damaged heart function via superior cell survival in comparison with dissociated cell injection. Tissue Eng Part A

  331. Fujimoto KL, Clause KC, Liu LJ, Tinney JP, Verma S, Wagner WR et al (2011) Engineered fetal cardiac graft preserves its cardiomyocyte proliferation within postinfarcted myocardium and sustains cardiac function. Tissue Eng Part A 17:585–596

    Article  CAS  PubMed  Google Scholar 

  332. Wendel JS, Ye L, Zhang P, Tranquillo RT, Zhang JJ (2014) Functional consequences of a tissue-engineered myocardial patch for cardiac repair in a rat infarct model. Tissue Eng Part A 20:1325–1335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  333. Marsano A, Maidhof R, Luo J, Fujikara K, Konofagou EE, Banfi A et al (2013) The effect of controlled expression of VEGF by transduced myoblasts in a cardiac patch on vascularization in a mouse model of myocardial infarction. Biomaterials 34:393–401

    Article  CAS  PubMed  Google Scholar 

  334. Leontyev S, Schlegel F, Spath C, Schmiedel R, Nichtitz M, Boldt A et al (2013) Transplantation of engineered heart tissue as a biological cardiac assist device for treatment of dilated cardiomyopathy. Eur J Heart Fail 15:23–35

    Article  CAS  PubMed  Google Scholar 

  335. Chen YL, Sun CK, Tsai TH, Chang LT, Leu S, Zhen YY et al (2015) Adipose-derived mesenchymal stem cells embedded in platelet-rich fibrin scaffolds promote angiogenesis, preserve heart function, and reduce left ventricular remodeling in rat acute myocardial infarction. Am J Trans Res 7:781–803

    CAS  Google Scholar 

  336. Kawamura M, Miyagawa S, Miki K, Saito A, Fukushima S, Higuchi T et al (2012) Feasibility, safety, and therapeutic efficacy of human induced pluripotent stem cell-derived cardiomyocyte sheets in a porcine ischemic cardiomyopathy model. Circulation 126:S29–S37

    Article  CAS  PubMed  Google Scholar 

  337. Mihic A, Li J, Miyagi Y, Gagliardi M, Li S-H, Zu J et al (2014) The effect of cyclic stretch on maturation and 3D tissue formation of human embryonic stem cell-derived cardiomyocytes. Biomaterials 35:2798–2808

    Article  CAS  PubMed  Google Scholar 

  338. Xiong Q, Ye L, Zhang P, Lepley M, Tian J, Li J et al (2013) Functional consequences of human induced pluripotent stem cell therapy: myocardial ATP turnover rate in the in vivo swine heart with postinfarction remodeling. Circulation 127:997–1008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  339. Simpson DL, Dudley SC Jr (2013) Modulation of human mesenchymal stem cell function in a three-dimensional matrix promotes attenuation of adverse remodelling after myocardial infarction. J Tissue Eng Regen Med 7:192–202

    Article  CAS  PubMed  Google Scholar 

  340. Roura S, Soler-Botija C, Bago JR, Llucia-Valldeperas A, Fernandez MA, Galvez-Monton C et al (2015) Postinfarction Functional recovery driven by a three-dimensional engineered fibrin patch composed of human umbilical cord blood-derived mesenchymal stem cells. Stem Cells Trans Med 4:956–966

    Article  CAS  Google Scholar 

  341. VanDusen KW, Syverud BC, Williams ML, Lee JD, Larkin LM (2014) Engineered skeletal muscle units for repair of volumetric muscle loss in the tibialis anterior muscle of a rat. Tissue Eng Part A 20:2920–2930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  342. Long C, Amoasii L, Mireault AA, McAnally JR, Li H, Sanchez-Ortiz E et al (2016) Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science 351:400–403

    Article  CAS  PubMed  Google Scholar 

  343. Tabebordbar M, Zhu K, Cheng JK, Chew WL, Widrick JJ, Yan WX et al (2016) In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science 351:407–411

    Article  CAS  PubMed  Google Scholar 

  344. Nelson CE, Hakim CH, Ousterout DG, Thakore PI, Moreb EA, Castellanos Rivera RM et al (2016) In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351:403–407

    Article  CAS  PubMed  Google Scholar 

  345. Wright AV, Nunez JK, Doudna JA (2016) Biology and applications of CRISPR systems: harnessing nature’s toolbox for genome engineering. Cell 164:29–44

    Article  CAS  PubMed  Google Scholar 

  346. Shuman JA, Zurcher JR, Sapp AA, Burdick JA, Gorman RC, Gorman JH 3rd et al (2013) Localized targeting of biomaterials following myocardial infarction: a foundation to build on. Trends Cardiovasc Med 23:301–311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  347. Sakellariou P, O’Neill A, Mueller AL, Stadler G, Wright WE, Roche JA et al (2015) Neuromuscular electrical stimulation promotes development in mice of mature human muscle from immortalized human myoblasts. Skelet Muscle 6:4

    Article  Google Scholar 

  348. Kirkton RD, Bursac N (2011) Engineering biosynthetic excitable tissues from unexcitable cells for electrophysiological and cell therapy studies. Nat Commun 2:300

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the NIH Grants AR055226 and AR065873 from National Institute of Arthritis and Musculoskeletal and Skin Disease, NIH Grants HL104326 and HL122079 from National Heart, Lung, and Blood Institute, NIH Grant T32 GM007171-Medical Scientist Training Program, UH3TR000505 Grant from the NIH Common Fund for the Microphysiological Systems Initiative, and a Grant from the Fondation Leducq. The content of the manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the funding agencies.

Author information

Author notes

    Authors and Affiliations

    1. Department of Biomedical Engineering, Duke University, 3000 Science Drive, Hudson Hall 136, Durham, NC, 27708-90281, USA

      I. Y. Shadrin, A. Khodabukus & N. Bursac

    Authors
    1. I. Y. Shadrin
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. A. Khodabukus
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. N. Bursac
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to N. Bursac.

    Additional information

    I. Y. Shadrin and A. Khodabukus equally contributing authors.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Shadrin, I.Y., Khodabukus, A. & Bursac, N. Striated muscle function, regeneration, and repair. Cell. Mol. Life Sci. 73, 4175–4202 (2016). https://doi.org/10.1007/s00018-016-2285-z

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00018-016-2285-z

    Keywords

    Search

    Navigation