Engineering skeletal muscle tissue - new perspectives in vitro and in vivo

Journal of Cellular and Molecular Medicine

Volumn 14, Issue 11, 2010, Pages 2622-2629

  Klumpp, Dorothee ^a   Horch, Raymund E ^a   Kneser, Ulrich ^a   Beier, Justus P ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

Electrospun nanofibre matrices; Nanotechnology; Satellite cells; Skeletal muscle tissue engineering

Indexed keywords

ARTICLE; CYTOLOGY; HUMAN; NANOTECHNOLOGY; PHYSIOLOGY; SKELETAL MUSCLE; TISSUE ENGINEERING;

HUMANS; MUSCLE, SKELETAL; NANOTECHNOLOGY; TISSUE ENGINEERING;

EID: 78649702041     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2010.01183.x     Document Type: Article

References (107)

1. Mooney DJ, Mikos AG. Growing new organs. Sci Am. 1999; 280: 60-5.
2. Law PK, Goodwin TG, Fang Q, et al Cell transplantation as an experimental treatment for Duchenne muscular dystrophy. Cell Transplant. 1993; 2: 485-505.
3. Guettier-Sigrist S, Coupin G, Braun S, et al Muscle could be the therapeutic target in SMA treatment. J Neurosci Res. 1998; 53: 663-9.
4. Klumpp D, Horch RE, Bitto F, et al. Skeletal muscle tissue engineering - current concepts and future perspectives. Handchir Mikrochir Plast Chir. 2010. DOI: .
5. Bach AD, Arkudas A, Tjiawi J, et al A new approach to tissue engineering of vascularized skeletal muscle. J Cell Mol Med. 2006; 10: 716-26.
6. Vandenburgh HH, Karlisch P, Farr L. Maintenance of highly contractile tissue-cultured avian skeletal myotubes in collagen gel. In Vitro Cell Dev Biol. 1988; 24: 166-74.
7. Beier JP, Klumpp D, Rudisile M, et al Collagen matrices from sponge to nano: new perspectives for tissue engineering of skeletal muscle. BMC Biotechnol. 2009; 9: 34-47.
8. Strohman RC, Bayne E, Spector D, et al Myogenesis and histogenesis of skeletal muscle on flexible membranes in vitro. In Vitro Cell Dev Biol. 1990; 26: 201-8.
9. Dennis RG, Kosnik PE 2nd, Gilbert ME, et al Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. Am J Physiol Cell Physiol. 2001; 280: 288-95.
10. Kannan RY, Salacinski HJ, Sales K, et al The roles of tissue engineering and vascularisation in the development of micro-vascular networks: a review. Biomaterials. 2005; 26: 1857-75.
11. Lesman A, Gepstein L, Levenberg S. Vascularization shaping the heart. Ann N Y Acad Sci. 2010; 1188: 46-51.
12. Levenberg S, Rouwkema J, Macdonald M, et al Engineering vascularized skeletal muscle tissue. Nat Biotechnol. 2005; 23: 879-84.
13. Messina A, Bortolotto SK, Cassell OC, et al Generation of a vascularized organoid using skeletal muscle as the inductive source. FASEB J. 2005; 19: 1570-2.
14. Hutmacher DW, Horch RE, Loessner D, et al Translating tissue engineering technology platforms into cancer research. J Cell Mol Med. 2009; 13: 1417-27.
15. Fiegel HC, Pryymachuk G, Rath S, et al Foetal hepatocyte transplantation in a vascularized AV-Loop transplantation model in the rat. J Cell Mol Med. 2010; 14: 267-74.
16. Erol OO, Spira M. New capillary bed formation with a surgically constructed arteriovenous fistula. Plast Reconstr Surg. 1980; 66: 109-15.
17. Kneser U, Polykandriotis E, Ohnolz J, et al Engineering of vascularized transplantable bone tissues: induction of axial vascularization in an osteoconductive matrix using an arteriovenous loop. Tissue Eng. 2006; 12: 1721-31.
18. Beier JP, Horch RE, Arkudas A, et al De novo generation of axially vascularized tissue in a large animal model. Microsurgery. 2009; 29: 42-51.
19. Beier JP, Horch RE, Hess A, et al Axial vascularization of a large volume calcium phosphate ceramic bone substitute in the sheep AV loop model. J Tissue Eng Regen Med. 2010; 4: 216-23.
20. Beier JP, Horch RE, Bach AD. Tissue engineering of skeletal muscle. Minerva Biotecnologica. 2006; 18: 89-95.
21. Cassell OC, Morrison WA, Messina A, et al The influence of extracellular matrix on the generation of vascularized, engineered, transplantable tissue. Ann N Y Acad Sci. 2001; 944: 429-42.
22. Boontheekul T, Hill EE, Kong HJ, et al Regulating myoblast phenotype through controlled gel stiffness and degradation. Tissue Eng. 2007; 13: 1431-42.
23. Shimizu K, Fujita H, Nagamori E. Alignment of skeletal muscle myoblasts and myotubes using linear micropatterned surfaces ground with abrasives. Biotechnol Bioeng. 2009; 103: 631-8.
24. Walboomers XF, Jansen JA. Cell and tissue behavior on micro-grooved surfaces. Odontology. 2001; 89: 2-11.
25. Kriparamanan R, Aswath P, Zhou A, et al Nanotopography: cellular responses to nanostructured materials. J Nanosci Nanotechnol. 2006; 6: 1905-19.
26. Meyle J, Gultig K, Wolburg H, et al Fibroblast anchorage to microtextured surfaces. J Biomed Mater Res. 1993; 27: 1553-7.
27. Patrito N, McCague C, Norton PR, et al Spatially controlled cell adhesion via micropatterned surface modification of poly(dimethylsiloxane). Langmuir. 2007; 23: 715-9.
28. Huang NF, Thakar RG, Wong M, et al Tissue engineering of muscle on micropatterned polymer films. Conf Proc IEEE Eng Med Biol Soc. 2004; 7: 4966-9.
29. Lee W, Parpura V. Micropatterned substrates for studying astrocytes in culture. Front Neurosci. 2009; 3: 381-7.
30. Lin YL, Jen JC, Hsu SH, et al Sciatic nerve repair by microgrooved nerve conduits made of chitosan-gold nanocomposites. Surg Neurol. 2008; 70: 9-18.
31. Curtis A, Wilkinson C. Topographical control of cells. Biomaterials. 1997; 18: 1573-83.
32. Gingras J, Rioux RM, Cuvelier D, et al Controlling the orientation and synaptic differentiation of myotubes with micropatterned substrates. Biophys J. 2009; 97: 2771-9.
33. Flaibani M, Boldrin L, Cimetta E, et al Muscle differentiation and myotubes alignment is influenced by micropatterned surfaces and exogenous electrical stimulation. Tissue Eng A. 2009; 15: 2447-57.
34. Madaghiele M, Sannino A, Yannas IV, et al Collagen-based matrices with axially oriented pores. J Biomed Mater Res A. 2008; 85: 757-67.
35. Zhang H, Hussain I, Brust M, et al Aligned two- and three-dimensional structures by directional freezing of polymers and nanoparticles. Nat Mater. 2005; 4: 787-93.
36. Schoof H, Apel J, Heschel I, et al Control of pore structure and size in freeze-dried collagen sponges. J Biomed Mater Res. 2001; 58: 352-7.
37. Mandal BB, Kundu SC. Cell proliferation and migration in silk fibroin 3D scaffolds. Biomaterials. 2009; 30: 2956-65.
38. Ren L, Tsuru K, Hayakawa S, et al Novel approach to fabricate porous gelatin-siloxane hybrids for bone tissue engineering. Biomaterials. 2002; 23: 4765-73.
39. Boudriot U, Dersch R, Greiner A, et al Electrospinning approaches toward scaffold engineering-a brief overview. Artif Organs. 2006; 30: 785-92.
40. Sell SA, McClure MJ, Garg K, et al Electrospinning of collagen/biopolymers for regenerative medicine and cardiovascular tissue engineering. Adv Drug Deliv Rev. 2009; 61: 1007-19.
41. Buttafoco L, Kolkman NG, Engbers-Buijtenhuijs P, et al Electrospinning of collagen and elastin for tissue engineering applications. Biomaterials. 2006; 27: 724-34.
42. Lee KY, Jeong L, Kang YO, et al Electrospinning of polysaccharides for regenerative medicine. Adv Drug Deliv Rev. 2009; 61: 1020-32.
43. Barnes CP, Sell SA, Boland ED, et al Nanofiber technology: designing the next generation of tissue engineering scaffolds. Adv Drug Deliv Rev. 2007; 59: 1413-33.
44. Schnell E, Klinkhammer K, Balzer S, et al Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-epsilon-caprolactone and a collagen/poly-epsilon-caprolactone blend. Biomaterials. 2007; 28: 3012-25.
45. Morrison WA, Hussey AJ. Extracellular matrix as a bioactive material for soft tissue reconstruction. ANZ J Surg. 2006; 76: 1047.
46. Bolgen N, Menceloglu YZ, Acatay K, et al In vitro and in vivo degradation of non-woven materials made of poly(epsilon-caprolactone) nanofibers prepared by electrospinning under different conditions. J Biomater Sci Polym Ed. 2005; 16: 1537-55.
47. Riboldi SA, Sampaolesi M, Neuenschwander P, et al Electrospun degradable polyesterurethane membranes: potential scaffolds for skeletal muscle tissue engineering. Biomaterials. 2005; 26: 4606-15.
48. Zhang YZ, Venugopal J, Huang ZM, et al Characterization of the surface biocompatibility of the electrospun PCL-collagen nanofibers using fibroblasts. Biomacromolecules. 2005; 6: 2583-9.
49. Huang NF, Patel S, Thakar RG, et al Myotube assembly on nanofibrous and micropatterned polymers. Nano Lett. 2006; 6: 537-42.
50. Ayres C, Bowlin GL, Henderson SC, et al Modulation of anisotropy in electrospun tissue-engineering scaffolds: analysis of fiber alignment by the fast Fourier transform. Biomaterials. 2006; 27: 5524-34.
51. Baker BM, Mauck RL. The effect of nanofiber alignment on the maturation of engineered meniscus constructs. Biomaterials. 2007; 28: 1967-77.
52. Telemeco TA, Ayres C, Bowlin GL, et al Regulation of cellular infiltration into tissue engineering scaffolds composed of submicron diameter fibrils produced by electrospinning. Acta Biomater. 2005; 1: 377-85.
53. Baker BM, Gee AO, Metter RB, et al The potential to improve cell infiltration in composite fiber-aligned electrospun scaffolds by the selective removal of sacrificial fibers. Biomaterials. 2008; 29: 2348-58.
54. Jiang H, Hu Y, Li Y, et al A facile technique to prepare biodegradable coaxial electrospun nanofibers for controlled release of bioactive agents. J Control Release. 2005; 108: 237-43.
55. Moroni L, De Wijn JR, Van Blitterswijk CA. Integrating novel technologies to fabricate smart scaffolds. J Biomater Sci Polym Ed. 2008; 19: 543-72.
56. Sill TJ, Von Recum HA. Electrospinning: applications in drug delivery and tissue engineering. Biomaterials. 2008; 29: 1989-2006.
57. Williams JH, Schray RC, Sirsi SR, et al. Nanopolymers improve delivery of exon skipping oligonucleotides and concomitant dystrophin expression in skeletal muscle of mdx mice. BMC Biotechnol. 2008; 8: 35.
58. Nelson SF, Crosbie RH, Miceli MC, et al Emerging genetic therapies to treat Duchenne muscular dystrophy. Curr Opin Neurol. 2009; 22: 532-8.
59. Sahoo S, Ang LT, Goh JC, et al Growth factor delivery through electrospun nanofibers in scaffolds for tissue engineering applications. J Biomed Mater Res A. 2010; 93: 1539-50.
60. Yang F, Cho SW, Son SM, et al Genetic engineering of human stem cells for enhanced angiogenesis using biodegradable polymeric nanoparticles. Proc Natl Acad Sci USA. 2010; 107: 3317-22.
61. Yancopoulos GD, Davis S, Gale NW, et al Vascular-specific growth factors and blood vessel formation. Nature. 2000; 407: 242-8.
62. Arkudas A, Tjiawi J, Bleiziffer O, et al Fibrin gel-immobilized VEGF and bFGF efficiently stimulate angiogenesis in the AV loop model. Mol Med. 2007; 13: 480-7.
63. Duan C, Ren H, Gao S. Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: roles in skeletal muscle growth and differentiation. Gen Comp Endocrinol. 2010; 167: 344-51.
64. Rende M, Brizi E, Conner J, et al Nerve growth factor (NGF) influences differentiation and proliferation of myogenic cells in vitro via TrKA. Int J Dev Neurosci. 2000; 18: 869-85.
65. Lavasani M, Lu A, Peng H, et al Nerve growth factor improves the muscle regeneration capacity of muscle stem cells in dystrophic muscle. Hum Gene Ther. 2006; 17: 180-92.
66. Sugiyama N, Yoshimura A, Fujitsuka C, et al Acceleration by MS-818 of early muscle regeneration and enhanced muscle recovery after surgical transection. Muscle Nerve. 2002; 25: 218-29.
67. Martins A, Duarte AR, Faria S, et al Osteogenic induction of hBMSCs by electrospun scaffolds with dexamethasone release functionality. Biomaterials. 2010; 31: 5875-85.
68. Wang F, Li Z, Tamama K, et al Fabrication and characterization of prosurvival growth factor releasing, anisotropic scaffolds for enhanced mesenchymal stem cell survival/growth and orientation. Biomacromolecules. 2009; 10: 2609-18.
69. Fujita H, Nedachi T, Kanzaki M. Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes. Exp Cell Res. 2007; 313: 1853-65.
70. Genovese JA, Spadaccio C, Chachques E, et al Cardiac pre-differentiation of human mesenchymal stem cells by electrostimulation. Front Biosci. 2009; 14: 2996-3002.
71. Shafy A, Lavergne T, Latremouille C, et al Association of electrostimulation with cell transplantation in ischemic heart disease. J Thorac Cardiovasc Surg. 2009; 138: 994-1001.
72. Gaetani R, Ledda M, Barile L, et al Differentiation of human adult cardiac stem cells exposed to extremely low-frequency electromagnetic fields. Cardiovasc Res. 2009; 82: 411-20.
73. Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, et al Electrical stimulation of nerve cells using conductive nanofibrous scaffolds for nerve tissue engineering. Tissue Eng A. 2009; 15: 3605-19.
74. Li M, Guo Y, Wei Y, et al Electrospinning polyaniline-contained gelatin nanofibers for tissue engineering applications. Biomaterials. 2006; 27: 2705-15.
75. Jun I, Jeong S, Shin H. The stimulation of myoblast differentiation by electrically conductive sub-micron fibers. Biomaterials. 2009; 30: 2038-47.
76. Le Grand F, Rudnicki MA. Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol. 2007; 19: 628-33.
77. Tajbakhsh S. Stem cells to tissue: molecular, cellular and anatomical heterogeneity in skeletal muscle. Curr Opin Genet Dev. 2003; 13: 413-22.
78. Zammit P, Beauchamp J. The skeletal muscle satellite cell: stem cell or son of stem cell Differentiation. 2001; 68: 193-204.
79. Seale P, Sabourin LA, Girgis-Gabardo A, et al Pax7 is required for the specification of myogenic satellite cells. Cell. 2000; 102: 777-86.
80. Kuang S, Kuroda K, Le Grand F, et al Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell. 2007; 129: 999-1010.
81. Weintraub H, Davis R, Tapscott S, et al The myoD gene family: nodal point during specification of the muscle cell lineage. Science. 1991; 251: 761-6.
82. Collins CA, Olsen I, Zammit PS, et al Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell. 2005; 122: 289-301.
83. Kottlors M, Kirschner J. Elevated satellite cell number in Duchenne muscular dystrophy. Cell Tissue Res. 2010; 340: 541-8.
84. Yaffe D. Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc Natl Acad Sci USA. 1968; 61: 477-83.
85. Blau HM, Brazelton TR, Weimann JM. The evolving concept of a stem cell: entity or function Cell. 2001; 105: 829-41.
86. Boonen KJ, Post MJ. The muscle stem cell niche: regulation of satellite cells during regeneration. Tissue Eng B Rev. 2008; 14: 419-31.
87. Deans TL, Elisseeff JH. Stem cells in musculoskeletal engineered tissue. Curr Opin Biotechnol. 2009; 20: 537-44.
88. Kern S, Eichler H, Stoeve J, et al Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells. 2006; 24: 1294-301.
89. Zhu Y, Liu T, Song K, et al Adipose-derived stem cell: a better stem cell than BMSC. Cell Biochem Funct. 2008; 26: 664-75.
90. Garbade J, Schubert A, Rastan AJ, et al Fusion of bone marrow-derived stem cells with cardiomyocytes in a heterologous in vitro model. Eur J Cardiothorac Surg. 2005; 28: 685-91.
91. Brazelton TR, Nystrom M, Blau HM. Significant differences among skeletal muscles in the incorporation of bone marrow-derived cells. Dev Biol. 2003; 262: 64-74.
92. Gussoni E, Blau HM, Kunkel LM. The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat Med. 1997; 3: 970-7.
93. Meirelles Lda S, Nardi NB. Methodology, biology and clinical applications of mesenchymal stem cells. Front Biosci. 2009; 14: 4281-98.
94. Satija NK, Singh VK, Verma YK, et al Mesenchymal stem cell-based therapy: a new paradigm in regenerative medicine. J Cell Mol Med. 2009; 13: 4385-402.
95. Popescu LM, Faussone-Pellegrini MS. Telocytes - a case of serendipity: the winding way from Interstitial cells of Cajal (ICC), via interstitial Cajal-like cells (ICLC) to Telocytes. J Cell Mol Med. 2010; 14: 729-40.
96. Gherghiceanu M, Popescu LM. Cardiomyocyte precursors and telocytes in epicardial stem cell niche: electron microscope images. J Cell Mol Med. 2010; 14: 871-7.
97. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006; 126: 663-76.
98. Lee H, Park J, Forget BG, et al Induced pluripotent stem cells in regenerative medicine: an argument for continued research on human embryonic stem cells. Regen Med. 2009; 4: 759-69.
99. Amabile G, Meissner A. Induced pluripotent stem cells: current progress and potential for regenerative medicine. Trends Mol Med. 2009; 15: 59-68.
100. Yuasa S, Fukuda K. Cardiac regenerative medicine. Circ J. 2008; 72: 49-55.
101. Moretti A, Bellin M, Welling A, et al Patient-specific induced pluripotent stem-cell models for long-QT syndrome. N Engl J Med. 2010. DOI: .
102. Hanna J, Wernig M, Markoulaki S, et al Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science. 2007; 318: 1920-3.
103. Chen L, Liu L. Current progress and prospects of induced pluripotent stem cells. Sci China C Life Sci. 2009; 52: 622-36.
104. Kaji K, Norrby K, Paca A, et al Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature. 2009; 458: 771-5.
105. Sun X, Fu X, Han W, et al Can controlled cellular reprogramming be achieved using microRNAs Ageing Res Rev. 2010; 9: 475-83.
106. Meyer N, Penn LZ. MYC - timeline reflecting on 25 years with MYC. Nat Rev Cancer. 2008; 8: 976-90.
107. Rowland BD, Peeper DS. KLF4, p21 and context-dependent opposing forces in cancer. Nat Rev Cancer. 2006; 6: 11-23.