Skip to main content
NCBI home page
Journal of Cellular and Molecular Medicine logoLink to Journal of Cellular and Molecular Medicine
. 2007 May 1;8(4):413–422. doi: 10.1111/j.1582-4934.2004.tb00466.x

Skeletal muscle tissue engineering

A D Bach 1,✉, J P Beier 2, J Stern‐Staeter 2, R E Horch 1
PMCID: PMC6740234  PMID: 15601570

Abstract

The reconstruction of skeletal muscle tissue either lost by traumatic injury or tumor ablation or functional damage due to myopathies is hampered by the lack of availability of functional substitution of this native tissue. Until now, only few alternatives exist to provide functional restoration of damaged muscle tissues. Loss of muscle mass and their function can surgically managed in part using a variety of muscle transplantation or transposition techniques. These techniques represent a limited degree of success in attempts to restore the normal functioning, however they are not perfect solutions. A new alternative approach to addresssing difficult tissue reconstruction is to engineer new tissues. Although those tissue engineering techniques attempting regeneration of human tissues and organs have recently entered into clinical practice, the engineering of skletal muscle tissue ist still a scientific challenge. This article reviews some of the recent findings resulting from tissue engineering science related to the attempt of creation and regeneration of functional skeletal muscle tissue.

Keywords: tissue engineering, skeletal muscle, cell culture, myoblasts, satellite cells, myopathies

References

  • 1. Mooney D.J., Mikos A.G., Growing new organs, Sci. Am., 280: 60–65, 1999. [DOI] [PubMed] [Google Scholar]
  • 2. Law P.K., Goodwin T.G., Fang Q., Deering M.B., Duggirala V., Larkin C., Florendo J.A., Kirby D.S., Li H.J., Chen M. et al., Cell transplantation as an experimental treatment for Duchenne muscular dystrophy, Cell Transplant., 2: 485–505, 1993. [DOI] [PubMed] [Google Scholar]
  • 3. Guettier‐Sigrist S., Coupin G., Braun S., Warter J.M., Poindron P., Muscle could be the therapeutic target in SMA treatment, J. Neurosci. Res., 53: 663–669, 1998. [DOI] [PubMed] [Google Scholar]
  • 4. DiEdwardo C.A., Petrosko P., Acarturk T.O., DiMilla P.A., LaFramboise W.A., Johnson P.C., Muscle tissue engineering, Clin. Plast. Surg., 26: 647–656, 1999. [PubMed] [Google Scholar]
  • 5. Bach A.D., Stem‐Straeter J., Beier J.P., Bannasch H., Stark G.B., Engineering of muscle tissue, Clin. Plast. Surg., 30: 589–599, 2003. [DOI] [PubMed] [Google Scholar]
  • 6. Bonassar L.J., Vacanti C.A., Tissue engineering: the first decade and beyond, J. Cell Biochem. Suppl., 30–31: 297–303, 1998. [PubMed] [Google Scholar]
  • 7. Vangsness C.T. Jr., Kurzweil P.R., Lieberman J.R., Restoring articular cartilage in the knee, Am. J. Orthop., 33: 29–34, 2004. [PubMed] [Google Scholar]
  • 8. Oakes B.W., Orthopaedic tissue engineering: from laboratory to the clinic, Med. J. Aust., 180: S35–S38, 2004. [DOI] [PubMed] [Google Scholar]
  • 9. Kopp J., Jeschke M.G., Bach A.D., Kneser U., Horch R. E., Applied tissue engineering in the closure of severe burns and chronic wounds using cultured human autologous keratinocytes in a natural fibrin matrix, Cell Tissue Bank, 5: 81–87, 2004. [DOI] [PubMed] [Google Scholar]
  • 10. Kojima K., Bonassar L.J., Ignotz R.A., Syed K., Cortiella J., Vacanti C.A., Comparison of tracheal and nasal chondrocytes for tissue engineering of the trachea, Ann. Thorac. Surg., 76: 1884–1888, 2003. [DOI] [PubMed] [Google Scholar]
  • 11. Chang S. C., Tobias G., Roy A.K., Vacanti C.A., Bonassar L.J., Tissue engineering of autologous cartilage for craniofacial reconstruction by injection molding, Plast. Reconstr. Surg., 112: 793–799, 2003. [DOI] [PubMed] [Google Scholar]
  • 12. Horch R.E., Debus M., Wagner G., Stark G. B., Cultured human keratinocytes on type I collagen membranes to reconstitute the epidermis, Tissue Eng., 6: 53–67, 2000. [DOI] [PubMed] [Google Scholar]
  • 13. Hurme T., Kalimo H., Lehto M., Jarvinen M., Healing of skeletal muscle injury: an ultrastructural and immuno‐histochemical study, Med. Sci. Sports Exerc., 23: 801–810, 1991. [PubMed] [Google Scholar]
  • 14. Campion D.R., The muscle satellite cell: a review, Int. Rev. Cytol., 87: 225–251, 1984. [DOI] [PubMed] [Google Scholar]
  • 15. Allen R.E., Temm‐Grove C.J., Sheehan S.M., Rice G., Skeletal muscle satellite cell cultures, Methods Cell Biol., 52: 155–176, 1997. [DOI] [PubMed] [Google Scholar]
  • 16. Hill M., Wernig A., Goldspink G., Muscle satellite (stem) cell activation during local tissue injury and repair, J. Anat., 203: 89–99, 2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17. Li Y., Huard J., Differentiation of muscle‐derived cells into myofibroblasts in injured skeletal muscle, Am. J. Pathol., 161: 895–907, 2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18. Guettier‐Sigrist S., Coupin G., Braun S., Rogovitz D., Courdier I., Warter J.M., Poindron P., On the possible role of muscle in the pathogenesis of spinal muscular atrophy, Fundam. Clin. Pharmacol., 15: 31–40, 2001. [DOI] [PubMed] [Google Scholar]
  • 19. Fauza D.O., Marler J.J., Koka R., Forse R.A., Mayer J. E., Vacanti J.P., Fetal tissue engineering: diaphragmatic replacement, J. Pediatr. Surg., 36: 146–151, 2001. [DOI] [PubMed] [Google Scholar]
  • 20. Blau H.M., Webster C., Isolation and characterization of human muscle cells, Proc. Natl. Acad. Sci. USA, 78: 5623–5627, 1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21. Vandenburgh H.H., Functional assessment and tissue design of skeletal muscle, Ann. N.Y. Acad. Sci., 961: 201–202, 2002. [DOI] [PubMed] [Google Scholar]
  • 22. Okano T., Satoh S., Oka T., Matsuda T., Tissue engineering of skeletal muscle. Highly dense, highly oriented hybrid muscular tissues biomimicking native tissues, Asaio. J., 43: M749–753, 1997. [PubMed] [Google Scholar]
  • 23. Acarturk T.O., Peel M.M., Petrosko P., LaFramboise W., Johnson P. C., DiMilla P.A., Control of attachment, morphology, and proliferation of skeletal myoblasts on silanized glass, J. Biomed. Mater. Res., 44: 355–370, 1999. [DOI] [PubMed] [Google Scholar]
  • 24. Okano T., Matsuda T., Muscular tissue engineering: capillary‐incorporated hybrid muscular tissues in vivo tissue culture, Cell Transplant., 7: 435–442, 1998. [DOI] [PubMed] [Google Scholar]
  • 25. Fuhrer C., Gautam M., Sugiyama J.E., Hall Z.W., Roles of rapsyn and agrin in interaction of postsynaptic proteins with acetylcholine receptors, J. Neurosci., 19: 6405–6416, 1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26. Marzaro M., Conconi M.T., Perin L., Giuliani S., Gamba P., De Coppi P., Perrino G.P., Parnigotto P.P., Nussdorfer G.G., Autologous satellite cell seeding improves in vivo biocompatibility of homologous muscle acellular matrix implants, Int. J. Mol. Med., 10: 177–182, 2002. [PubMed] [Google Scholar]
  • 27. Blanco‐Bose W.E., Yao C.C., Kramer R.H., Blau H.M., Purification of mouse primary myoblasts based on alpha 7 integrin expression, Exp. Cell Res., 265: 212–220, 2001. [DOI] [PubMed] [Google Scholar]
  • 28. Kosnik P.E., Faulkner J.A., Dennis R.G., Functional development of engineered skeletal muscle from adult and neonatal rats, Tissue Eng., 7: 573–584, 2001. [DOI] [PubMed] [Google Scholar]
  • 29. Neumann T., Hauschka S.D., Sanders J.E., Tissue engineering of skeletal muscle using polymer fiber arrays, Tissue Eng., 9: 995–1003, 2003. [DOI] [PubMed] [Google Scholar]
  • 30. Delfini M., Hirsinger E., Pourquie O., Duprez D., Delta 1‐activated notch inhibits muscle differentiation without affecting Myf5 and Pax3 expression in chick limb myogenesis, Development, 127: 5213–5224, 2000. [DOI] [PubMed] [Google Scholar]
  • 31. Bach A.D., Beier J.P., Stark G.B., Expression of Trisk 51, agrin and nicotinic‐acetycholine receptor epsilon‐subunit during muscle development in a novel three‐dimensional muscle‐neuronal co‐culture system, Cell Tissue Res., 314: 263–274, 2003. [DOI] [PubMed] [Google Scholar]
  • 32. Weintraub H., The MyoD family and myogenesis: redundancy, networks, and thresholds, Cell, 75: 1241–1244, 1993. [DOI] [PubMed] [Google Scholar]
  • 33. Molkentin J.D., Olson E.N., Combinatorial control of muscle development by basic helix‐loop‐helix and MADS‐box transcription factors, Proc. Natl. Acad. Sci. USA, 93: 9366–9373, 1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34. Molkentin J.D., Olson E.N., Defining the regulatory networks for muscle development, Curr. Opin. Genet. Dev., 6: 445–453, 1996. [DOI] [PubMed] [Google Scholar]
  • 35. Goldspink G., Gene expression in muscle in response to exercise, J. Muscle Res. Cell. Motil., 24: 121–126, 2003. [DOI] [PubMed] [Google Scholar]
  • 36. Goldspink G., Scutt A., Loughna P.T., Wells D.J., Jaenicke T., Gerlach G.F., Gene expression in skeletal muscle in response to stretch and force generation, Am. J. Physiol., 262: R356–R363, 1992. [DOI] [PubMed] [Google Scholar]
  • 37. Powell C.A., Smiley B.L., Mills J., Vandenburgh H.H., Mechanical stimulation improves tissue‐engineered human skeletal muscle, Am. J. Physiol. Cell Physiol., 283: C1557–C1565, 2002. [DOI] [PubMed] [Google Scholar]
  • 38. Tatsumi R., Sheehan S.M., Iwasaki H., Hattori A., Allen R.E., Mechanical stretch induces activation of skeletal muscle satellite cells in vitro , Exp. Cell Res., 267: 107–114, 2001. [DOI] [PubMed] [Google Scholar]
  • 39. Noah E.M., Winkel R., Schramm U., Kuhnel W., Impact of innervation and exercise on muscle regeneration in neovascularized muscle grafts in rats, Ann. Anat., 184: 189–197, 2002. [DOI] [PubMed] [Google Scholar]
  • 40. Dusterhoft S., Pette D., Effects of electrically induced contractile activity on cultured embryonic chick breast muscle cells, Differentiation, 44: 178–184, 1990. [DOI] [PubMed] [Google Scholar]
  • 41. Wehrle U., Dusterhoft S., Pette D., Effects of chronic electrical stimulation on myosin heavy chain expression in satellite cell cultures derived from rat muscles of different fiber‐type composition, Differentiation, 58: 37–46, 1994. [DOI] [PubMed] [Google Scholar]
  • 42. Dennis R.G., Kosnik P.E. 2nd, Gilbert M.E., Faulkner J.A., Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines, Am. J. Physiol. Cell. Physiol., 280: C288–C295, 2001. [DOI] [PubMed] [Google Scholar]
  • 43. Kanno S., Oda N., Abe M., Saito S., Hori K., Handa Y., Tabayashi K., Sato Y., Establishment of a simple and practical procedure applicable to therapeutic angiogenesis, Circulation, 99: 2682–2687, 1999. [DOI] [PubMed] [Google Scholar]
  • 44. Adams J.C., Watt F.M., Regulation of development and differentiation by the extracellular matrix, Development, 117: 1183–1198, 1993. [DOI] [PubMed] [Google Scholar]
  • 45. Mulder M.M., Hitchcock R.W., Tresco P.A., Skeletal myogenesis on elastomeric substrates: implications for tissue engineering, J. Biomater. Sci. Polym. Ed., 9: 731–748, 1998. [DOI] [PubMed] [Google Scholar]
  • 46. Freed L.E., Vunjak‐Novakovic G., Biron R.J., Eagles D. B., Lesnoy D.C., Barlow S.K., Langer R., Biodegradable polymer scaffolds for tissue engineering, Biotechnology (N Y), 12: 689–93, 1994. [DOI] [PubMed] [Google Scholar]
  • 47. Grande D.A., Halberstadt C., Naughton G., Schwartz R., Manji R., Evaluation of matrix scaffolds for tissue engineering of articular cartilage grafts, J. Biomed. Mater. Res, 34: 211–220, 1997. [DOI] [PubMed] [Google Scholar]
  • 48. Cronin E.M., Thurmond F.A., Bassel‐Duby R., Williams R.S., Wright W. E., Nelson K. D., Garner H. R., Protein‐coated poly(L‐lactic acid) fibers provide a substrate for differentiation of human skeletal muscle cells, J. Biomed. Mater. Res., 69A: 373–381, 2004. [DOI] [PubMed] [Google Scholar]
  • 49. Saxena A.K., Marler J., Benvenuto M., Willital G.H., Vacanti J.P., Skeletal muscle tissue engineering using isolated myoblasts on synthetic biodegradable polymers: preliminary studies, Tissue Eng., 5: 525–532, 1999. [DOI] [PubMed] [Google Scholar]
  • 50. Dusterhoft S., Pette D., Satellite cells from slow rat muscle express slow myosin under appropriate culture conditions, Differentiation, 53: 25–33, 1993. [DOI] [PubMed] [Google Scholar]
  • 51. Rowley J.A., Madlambayan G., Mooney D.J., Alginate hydrogels as synthetic extracellular matrix materials, Biomaterials, 20: 45–53, 1999. [DOI] [PubMed] [Google Scholar]
  • 52. Borschel G. H., Dennis R.G., Kuzon W.M. Jr., Contractile skeletal muscle tissue‐engineered on an acellular scaffold, Plast Reconstr Surg, 113: 595–602; discussion 603–604, 2004. [DOI] [PubMed] [Google Scholar]
  • 53. Rando T.A., Blau H.M., Methods for myoblast transplantation, Methods Cell Biol, 52: 261–272, 1997. [DOI] [PubMed] [Google Scholar]
  • 54. Ye Q., Zund G., Benedikt P., Jockenhoevel S., Hoerstrup S.P., Sakyama S., Hubbell J.A., Turina M., Fibrin gel as a three dimensional matrix in cardiovascular tissue engineering, Eur. J. Cardiothorac. Surg., 17: 587–591, 2000. [DOI] [PubMed] [Google Scholar]
  • 55. Bach A.D., Bannasch H., Galla T.J., Bittner K.M., Stark G.B., Fibrin glue as matrix for cultured autologous urothelial cells in urethral reconstruction, Tissue Eng, 7: 45–53, 2001. [DOI] [PubMed] [Google Scholar]
  • 56. Albelda S.M., Buck C.A., Integrins and other cell adhesion molecules, FASEB J., 4: 2868–2880, 1990. [PubMed] [Google Scholar]
  • 57. Saxena A.K., Willital G.H., Vacanti J.P., Vascularized three‐dimensional skeletal muscle tissue‐engineering, Biomed. Mater. Eng., 11: 275–281, 2001. [PubMed] [Google Scholar]
  • 58. Miller R.G., Sharma K.R., Pavlath G.K., Gussoni E., Mynhier M., Lanctot A.M., Greco C.M., Steinman L., Blau H.M., Myoblast implantation in Duchenne muscular dystrophy: the San Francisco study, Muscle Nerve, 20: 469–478, 1997. [DOI] [PubMed] [Google Scholar]
  • 59. Menasche P., Myoblast transfer in heart failure, Surg. Clin. North Am., 84: 125–139, 2004. [DOI] [PubMed] [Google Scholar]
  • 60. Atkins B.Z., Lewis C.W., Kraus W.E., Hutcheson K.A., Glower D.D., Taylor D.A., Intracardiac transplantation of skeletal myoblasts yields two populations of striated cells in situ, Ann. Thorac. Surg., 67: 124–129, 1999. [DOI] [PubMed] [Google Scholar]
  • 61. Gussoni E., Pavlath G.K., Lanctot A.M., Sharma K.R., Miller R.G., Steinman L., Blau H.M., Normal dystrophin transcripts detected in Duchenne muscular dystrophy patients after myoblast transplantation, Nature, 356: 435–438, 1992. [DOI] [PubMed] [Google Scholar]
  • 62. Rando T.A., Pavlath G.K., Blau H.M., The fate of myoblasts following transplantation into mature muscle, Exp. Cell Res., 220: 383–389, 1995. [DOI] [PubMed] [Google Scholar]
  • 63. Prelle K., Wobus A.M., Krebs O., Blum W.F., Wolf E., Overexpression of insulin‐like growth factor‐II in mouse embryonic stem cells promotes myogenic differentiation, Biochem. Biophys. Res. Commun., 277: 631–638, 2000. [DOI] [PubMed] [Google Scholar]
  • 64. Powell C., Shansky J., Del Tatto M., Forman D.E., Hennessey J., Sullivan K., Zielinski B.A., Vandenburgh H.H., Tissue‐engineered human bioartificial muscles expressing a foreign recombinant protein for gene therapy, Hum. Gene Ther., 10: 565–577, 1999. [DOI] [PubMed] [Google Scholar]
  • 65. Barr E., Leiden J.M., Systemic delivery of recombinant proteins by genetically modified myoblasts, Science, 254: 1507–1509, 1991. [DOI] [PubMed] [Google Scholar]
  • 66. Oakley R.M., Brand N.J., Burton P.B., McMullen M.C., Adams G.B., Poznansky M.C., Barton P.J., Yacoub M.H., Efficiency of a high‐titer retroviral vector for gene transfer into skeletal myoblasts, J. Thorac. Cardiovasc. Surg., 115: 1–8, 1998. [DOI] [PubMed] [Google Scholar]
  • 67. Law P.K., Goodwin T.G., Fang Q., Quinley T., Vastagh G., Hall T., Jackson T., Deering M. B., Duggirala V., Larkin C., Florendo J. A., Li L.M., Yoo T.J., Chase N., Neel M., Krahn T., Holcomb R.L., Human gene therapy with myoblast transfer, Transplant. Proc., 29: 2234–2237, 1997. [DOI] [PubMed] [Google Scholar]
  • 68. Deasy B.M., Huard J., Gene therapy and tissue engineering based on muscle‐derived stem cells, Curr. Opin. Mol. Ther., 4: 382–389, 2002. [PubMed] [Google Scholar]
  • 69. Beier J.P., Kneser U., Stern‐Strater J., Stark G.B., Bach A.D., Y chromosome detection of three‐dimensional tissue‐engineered skeletal muscle constructs in a syngeneic rat animal model, Cell Transplant, 13: 45–53, 2004. [DOI] [PubMed] [Google Scholar]
  • 70. Young H.E., Duplaa C., Romero‐Ramos M., Chesselet M.F., Vourc'h P., Yost M.J., Ericson K., Terracio L., Asahara T., Masuda H., Tamura‐Ninomiya S., Detmer K., Bray R.A., Steele T.A., Hixson D., El‐Kalay M., Tobin B.W., Russ R.D., Horst M.N., Floyd J.A., Henson N.L., Hawkins K.C., Groom J., Parikh A., Blake L., Bland L.J., Thompson A.J., Kirincich A., Moreau C., Hudson J., Bowyer F.P. 3rd, Lin T.J., Black A.C. Jr., Adult reserve stem cells and their potential for tissue engineering, Cell Biochem. Biophys., 40: 1–80, 2004. [DOI] [PubMed] [Google Scholar]
  • 71. Korbling M., Estrov Z., Champlin R., Adult stem cells and tissue repair, Bone Marrow Transplant, 32 Suppl 1: S23–S24, 2003. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Cellular and Molecular Medicine are provided here courtesy of Blackwell Publishing

RESOURCES