A tissue-engineered muscle repair construct for functional restoration of an irrecoverable muscle injury in a murine model

Tissue Engineering - Part A

Volumn 17, Issue 17-18, 2011, Pages 2291-2303

  MacHingal, Masood A ^a,b   Corona, Benjamin T ^a   Walters, Thomas J ^c   Kesireddy, Venu ^a   Koval, Christine N ^a   Dannahower, Ashley ^a   Zhao, Weixin ^a   Yoo, James J ^a,b   Christ, George J ^a,b  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c US ARMY INSTITUTE OF SURGICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSELS; MAMMALS; RESTORATION;

CLINICAL TREATMENTS; DEGENERATIVE DISEASE; FUNCTIONAL RECOVERY; HISTOLOGICAL ANALYSIS; INJURY MODELS; MATRIX; MURINE MODEL; MUSCLE FORCE; MUSCLE INJURIES; MYOBLASTS; MYOFIBERS; NUDE MICE; PROOF OF CONCEPT; SKELETAL MUSCLE; TRAUMATIC INJURY;

MUSCLE;

MURINAE; MUS MUSCULUS; RATTUS; SUS;

TISSUE SCAFFOLD;

ANIMAL; ARTICLE; CELL CULTURE; CHEMISTRY; CYTOLOGY; FEMALE; IMMUNOCHEMISTRY; INJURY; MALE; METABOLISM; METHODOLOGY; MOUSE; NUDE MOUSE; RAT; SCANNING ELECTRON MICROSCOPY; SKELETAL MUSCLE; STEM CELL; TISSUE ENGINEERING; ULTRASTRUCTURE;

ANIMALS; CELLS, CULTURED; FEMALE; IMMUNOCHEMISTRY; MALE; MICE; MICE, NUDE; MICROSCOPY, ELECTRON, SCANNING; MUSCLE, SKELETAL; RATS; STEM CELLS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 80053148320     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2010.0682     Document Type: Article

References (53)

1. Ambrosio, F., Kadi, F., Lexell, J., Fitzgerald, G.K., Boninger, M.L., and Huard, J. The effect of muscle loading on skeletal muscle regenerative potential: an update of current research findings relating to aging and neuromuscular pathology. Am J Phys Med Rehabil 88, 145, 2009.
2. Ciciliot, S., and Schiaffino, S. Regeneration of mammalian skeletal muscle. Basic mechanisms and clinical implications. Curr Pharm Des 16, 906, 2010.
3. Jarvinen, T.A., Jarvinen, T.L., Kaariainen, M., Kalimo, H., and Jarvinen, M. Muscle injuries: biology and treatment. Am J Sports Med 33, 745, 2005.
4. Lee, J.Y., Qu-Petersen, Z., Cao, B., Kimura, S., Jankowski, R., Cummins, J., Usas, A., Gates, C., Robbins, P., Wernig, A., and Huard, J. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol 150, 1085, 2000.
5. Moss, F.P., and Leblond, C.P. Nature of dividing nuclei in skeletal muscle of growing rats. J Cell Biol 44, 459, 1970.
6. Snow, M.H. An autoradiographic study of satellite cell differentiation into regenerating myotubes following transplantation of muscles in young rats. Cell Tissue Res 186, 535, 1978.
7. LaBarge, M.A., and Blau, H.M. Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 111, 589, 2002.
8. Relaix, F., Rocancourt, D., Mansouri, A., and Buckingham, M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435, 948, 2005.
9. Ten Broek, R.W., Grefte, S., and Von den Hoff, J.W. Regulatory factors and cell populations involved in skeletal muscle regeneration. J Cell Physiol 224, 7, 2010.
10. Holcomb, J.B., Stansbury, L.G., Champion, H.R., Wade, C., and Bellamy, R.F. Understanding combat casualty care statistics. J Trauma 60, 397, 2006.
11. Lew, T.A., Walker, J.A., Wenke, J.C., Blackbourne, L.H., and Hale, R.G. Characterization of craniomaxillofacial battle injuries sustained by United States service members in the current conflicts of Iraq and Afghanistan. J Oral Maxillofac Surg 68, 3, 2010.
12. Mazurek, M.T., and Ficke, J.R. The scope of wounds encountered in casualties from the global war on terrorism: from the battlefield to the tertiary treatment facility. J Am Acad Orthop Surg 14, S18, 2006.
13. Owens, B.D., Kragh, J.F., Jr., Wenke, J.C., Macaitis, J., Wade, C.E., and Holcomb, J.B. Combat wounds in operation Iraqi Freedom and operation Enduring Freedom. J Trauma 64, 295, 2008.
14. Grogan, B.F., and Hsu, J.R. Volumetric muscle loss. J Am Acad Orthop Surg 19 Suppl 1, S35, 2011.
15. Norris, B.L., and Kellam, J.F. Soft-tissue injuries associated with high-energy extremity trauma: principles of management. J Am Acad Orthop Surg 5, 37, 1997.
16. Lawson, R., and Levin, L.S. Principles of free tissue transfer in orthopaedic practice. J Am Acad Orthop Surg 15, 290, 2007.
17. Khouri, R.K., Cooley, B.C., Kunselman, A.R., Landis, J.R., Yeramian, P., Ingram, D., Natarajan, N., Benes, C.O., and Wallemark, C. A prospective study of microvascular freeflap surgery and outcome. Plast Reconstr Surg 102, 711, 1998.
18. Lin, C.H., Wei, F.C., Levin, L.S., and Chen, M.C. Donor-site morbidity comparison between endoscopically assisted and traditional harvest of free latissimus dorsi muscle flap. Plast Reconstr Surg 104, 1070, 1999.
19. Koning, M., Harmsen, M.C., van Luyn, M.J., and Werker, P.M. Current opportunities and challenges in skeletal muscle tissue engineering. J Tissue Eng Regen Med 3, 407, 2009.
20. Dennis, R.G., Kosnik, P.E., 2nd, Gilbert, M.E., and Faulkner, J.A. Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. Am J Physiol Cell Physiol 280, C288, 2001.
21. Levenberg, S., Rouwkema, J., Macdonald, M., Garfein, E.S., Kohane, D.S., Darland, D.C., Marini, R., van Blitterswijk, C.A., Mulligan, R.C., D'Amore, P.A., and Langer, R. Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23, 879, 2005.
22. Powell, C.A., Smiley, B.L., Mills, J., and Vandenburgh, H.H. Mechanical stimulation improves tissue-engineered human skeletal muscle. Am J Physiol Cell Physiol 283, C1557, 2002.
23. Shansky, J., Del Tatto, M., Chromiak, J., and Vandenburgh, H. A simplified method for tissue engineering skeletal muscle organoids in vitro. In Vitro Cell Dev Biol Anim 33, 659, 1997.
24. Vandenburgh, H.H., Karlisch, P., and Farr, L. Maintenance of highly contractile tissue-cultured avian skeletal myotubes in collagen gel. In Vitro Cell Dev Biol 24, 166, 1988.
25. Turner, N.J., Yates, A.J., Weber, D.J., Qureshi, I.R., Stolz, D.B., Gilbert, T.W., and Badylak, S.F. Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction. Tissue Eng Part A 16, 3309, 2010.
26. Valentin, J.E., Turner, N.J., Gilbert, T.W., and Badylak, S.F. Functional skeletal muscle formation with a biologic scaffold. Biomaterials 31, 7475, 2010.
27. Gamba, P.G., Conconi, M.T., Lo Piccolo, R., Zara, G., Spinazzi, R., and Parnigotto, P.P. Experimental abdominal wall defect repaired with acellular matrix. Pediatr Surg Int 18, 327, 2002.
28. Kin, S., Hagiwara, A., Nakase, Y., Kuriu, Y., Nakashima, S., Yoshikawa, T., Sakakura, C., Otsuji, E., Nakamura, T., and Yamagishi, H. Regeneration of skeletal muscle using in situ tissue engineering on an acellular collagen sponge scaffold in a rabbit model. ASAIO J 53, 506, 2007.
29. Merritt, E.K., Hammers, D.W., Tierney, M., Suggs, L.J., Walters, T.J., and Farrar, R.P. Functional assessment of skeletal muscle regeneration utilizing homologous extracellular matrix as scaffolding. Tissue Eng Part A 16, 1395, 2010.
30. Merritt, E.K., Cannon, M.V., Hammers, D.W., Le, L.N., Gokhale, R., Sarathy, A., Song, T.J., Tierney, M.T., Suggs, L.J., Walters, T.J., and Farrar, R.P. Repair of traumatic skeletal muscle injury with bone-marrow-derived mesenchymal stem cells seeded on extracellular matrix. Tissue Eng Part A 16, 2871, 2010.
31. Moon du G, Christ, G., Stitzel, J.D., Atala, A., and Yoo, J.J. Cyclic mechanical preconditioning improves engineered muscle contraction. Tissue Eng Part A 14, 473, 2008.
32. Corona, B.T., Rouviere, C., Hamilton, S.L., and Ingalls, C.P. Eccentric contractions do not induce rhabdomyolysis in malignant hyperthermia susceptible mice. J Appl Physiol 105, 1542, 2008.
33. Corona, B.T., Rouviere, C., Hamilton, S.L., and Ingalls, C.P. FKBP12 deficiency reduces strength deficits after eccentric contraction-induced muscle injury. J Appl Physiol 105, 527, 2008.
34. Shah, A.J., Pagala, M.K., Subramani, V., Venkatachari, S.A., and Sahgal, V. Effect of fiber types, fascicle size and halothane on caffeine contractures in rat muscles. J Neurol Sci 88, 247, 1988.
35. Balnave, C.D., and Allen, D.G. Intracellular calcium and force in single mouse muscle fibres following repeated contractions with stretch. J Physiol 488 (Pt 1), 25, 1995.
36. Ingalls, C.P., Warren, G.L., Williams, J.H., Ward, C.W., and Armstrong, R.B. E-C coupling failure in mouse EDL muscle after in vivo eccentric contractions. J Appl Physiol 85, 58, 1998.
37. Kong, H., Jones, P.P., Koop, A., Zhang, L., Duff, H.J., and Chen, S.R. Caffeine induces Ca2 + release by reducing the threshold for luminal Ca2 + activation of the ryanodine receptor. Biochem J 414, 441, 2008.
38. Brooks, S.V., and Faulkner, J.A. Contraction-induced injury: recovery of skeletal muscles in young and old mice. Am J Physiol 258, C436, 1990.
39. Corona, B.T., Balog, E.M., Doyle, J.A., Rupp, J.C., Luke, R.C., and Ingalls, C.P. Junctophilin damage contributes to early strength deficits and EC coupling failure after eccentric contractions. Am J Physiol Cell Physiol 298, C365, 2010.
40. Ingalls, C.P., Warren, G.L., and Armstrong, R.B. Dissociation of force production from MHC and actin contents in muscles injured by eccentric contractions. J Muscle Res Cell Motil 19, 215, 1998.
41. Warren, G.L., O'Farrell, L., Summan, M., Hulderman, T., Mishra, D., Luster, M.I., Kuziel, W.A., and Simeonova, P.P. Role of CC chemokines in skeletal muscle functional restoration after injury. Am J Physiol Cell Physiol 286, C1031, 2004.
42. Adam, A., and De Luca, C.J. Firing rates of motor units in human vastus lateralis muscle during fatiguing isometric contractions. J Appl Physiol 99, 268, 2005.
43. de Luca, C.J., Foley, P.J., and Erim, Z. Motor unit control properties in constant-force isometric contractions. J Neurophysiol 76, 1503, 1996.
44. Ashley, Z., Sutherland, H., Lanmuller, H., Russold, M.F., Unger, E., Bijak, M., Mayr, W., Boncompagni, S., Protasi, F., Salmons, S., and Jarvis, J.C. Atrophy, but not necrosis, in rabbit skeletal muscle denervated for periods up to one year. Am J Physiol Cell Physiol 292, C440, 2007.
45. Mase, V.J., Jr., Hsu, J.R., Wolf, S.E., Wenke, J.C., Baer, D.G., Owens, J., Badylak, S.F., and Walters, T.J. Clinical application of an acellular biologic scaffold for surgical repair of a large, traumatic quadriceps femoris muscle defect. Orthopedics 33, 511, 2010.
46. Ayele, T., Zuki, A.B., Noorjahan, B.M., and Noordin, M.M. Tissue engineering approach to repair abdominal wall defects using cell-seeded bovine tunica vaginalis in a rabbit model. J Mater Sci Mater Med 21, 1721, 2010.
47. Moopanar, T.R., and Allen, D.G. Reactive oxygen species reduce myofibrillar Ca2 + sensitivity in fatiguing mouse skeletal muscle at 37 degrees C. J Physiol 564, 189, 2005.
48. Patel, T.J., Das, R., Friden, J., Lutz, G.J., and Lieber, R.L. Sarcomere strain and heterogeneity correlate with injury to frog skeletal muscle fiber bundles. J Appl Physiol 97, 1803, 2004.
49. Posterino, G.S., and Dunn, S.L. Comparison of the effects of inorganic phosphate on caffeine-induced Ca2 + release in fast-and slow-twitch mammalian skeletal muscle. Am J Physiol Cell Physiol 294, C97, 2008.
50. Warren, G.L., Lowe, D.A., Hayes, D.A., Karwoski, C.J., Prior, B.M., and Armstrong, R.B. Excitation failure in eccentric contraction-induced injury of mouse soleus muscle. J Physiol 468, 487, 1993.
51. Linderman, J.K., and Blough, E.R. Aging does not attenuate plantaris muscle hypertrophy in male Fischer 344 rats. Med Sci Sports Exerc 34, 1115, 2002.
52. Spector, S.A., Gardiner, P.F., Zernicke, R.F., Roy, R.R., and Edgerton, V.R. Muscle architecture and force-velocity characteristics of cat soleus and medial gastrocnemius: implications for motor control. J Neurophysiol 44, 951, 1980.
53. Sacks, R.D., and Roy, R.R. Architecture of the hind limb muscles of cats: functional significance. J Morphol 173, 185, 1982.