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 Engineering - Part A

Volumn 20, Issue 3-4, 2014, Pages 705-715

  Corona, Benjamin T ^a,b   Ward, Catherine L ^a,b   Baker, Hannah B ^a   Walters, Thomas J ^b   Christ, George J ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

DEFECTS; RESTORATION; SCAFFOLDS (BIOLOGY); TISSUE REGENERATION;

CELLULAR COMPONENTS; CLINICAL TREATMENTS; FUNCTIONAL CAPACITY; FUNCTIONAL IMPROVEMENTS; FUNCTIONAL RECOVERY; MUSCLE-DERIVED CELLS; PHYSICAL REHABILITATION; SKELETAL MUSCLE FIBERS;

MUSCLE;

SILICON; TISSUE SCAFFOLD;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLADDER; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; IMPLANTATION; LEWIS RAT; MALE; MUSCLE FUNCTION; MUSCLE INJURY; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; RAT MODEL; SWINE; TIBIALIS ANTERIOR MUSCLE; TISSUE ENGINEERING;

ANIMALS; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; INFLAMMATION; MALE; MUSCLE, SKELETAL; PROSTHESIS IMPLANTATION; RATS; RATS, INBRED LEW; RECOVERY OF FUNCTION; REGENERATION; SUS SCROFA; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TORQUE; URINARY BLADDER; WOUND HEALING;

EID: 84894117026     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0761     Document Type: Article

References (50)

1. Grogan, B.F., and Hsu, J.R. Volumetric muscle loss. J Am Acad Orthop Surg 19 Suppl 1, S35, 2011.
2. Vekris, M.D., Beris, A.E., Lykissas, M.G., Korompilias, A.V., Vekris, A.D., and Soucacos, P.N. Restoration of elbow function in severe brachial plexus paralysis via muscle transfers. Injury 39 Suppl 3, S15, 2008.
3. Lin, C.H., Lin, Y.T., Yeh, J.T., and Chen, C.T. Free functioning muscle transfer for lower extremity posttraumatic composite structure and functional defect. Plast Reconstr Surg 119, 2118, 2007.
4. Owens, J.G., Blair, J.A., Patzkowski, J.C., Blanck, R.V., and Hsu, J.R. Return to running and sports participation after limb salvage. J Trauma 71, S120, 2011.
5. Corona, B.T., Machingal, M.A., Criswell, T., Vadhavkar, M., Dannahower, A.C., Bergman, C., et al. Further development of a tissue engineered muscle repair construct in vitro for enhanced functional recovery following implantation in vivo in a murine model of volumetric muscle loss injury. Tissue Eng Part A 18, 1213, 2012.
6. De Coppi, P., Bellini, S., Conconi, M.T., Sabatti, M., Simo-nato, E., Gamba, P.G., et al. Myoblast-acellular skeletal muscle matrix constructs guarantee a long-term repair of experimental full-thickness abdominal wall defects. Tissue Eng 12, 1929, 2006.
7. Gamba, P.G., Conconi, M.T., Lo Piccolo, R., Zara, G., Spi-nazzi, R., and Parnigotto, P.P. Experimental abdominal wall defect repaired with acellular matrix. Pediatr Surg Int 18, 327, 2002.
8. Machingal, M.A., Corona, B.T., Walters, T.J., Kesireddy, V., Koval, C.N., Dannahower, A., et al. A Tissue-engineered muscle repair construct for functional restoration of an irrecoverable muscle injury in a murine model. Tissue Eng Part A 17, 2291, 2011.
9. Merritt, E.K., Cannon, M.V., Hammers, D.W., Le, L.N., Go-khale, R., Sarathy, A., et al. Repair of traumatic skeletal muscle injury with bone-marrow-derived mesenchymal stem cells seeded on extracellular matrix. Tissue Eng Part A 16, 2871, 2010.
10. 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.
11. Perniconi, B., Costa, A., Aulino, P., Teodori, L., Adamo, S., and Coletti, D. The pro-myogenic environment provided by whole organ scale acellular scaffolds from skeletal muscle. Biomaterials 32, 7870, 2011.
12. Turner, N.J., Badylak, J.S., Weber, D.J., and Badylak, S.F. Biologic scaffold remodeling in a dog model of complex musculoskeletal injury. J Surg Res 176, 490, 2012.
13. 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.
14. Willett, N.J., Li, M.T., Uhrig, B.A., Boerckel, J.D., Huebsch, N., Lundgren, T.S., et al. Attenuated rhBMP-2 mediated bone regeneration in a rat model of composite bone and muscle injury. Tissue Eng Part C Methods 19, 316, 2013.
15. Wolf, M.T., Daly, K.A., Reing, J.E., and Badylak, S.F. Biologic scaffold composed of skeletal muscle extracellular matrix. Biomaterials 33, 2916, 2012.
16. Turner, N.J., Yates, A.J., Jr., Weber, D.J., Qureshi, I.R., Stolz, D.B., Gilbert, T.W., et al. Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction. Tissue Eng Part A 16, 3309, 2010.
17. Sicari, B.M., Agrawal, V., Siu, B.F., Medberry, C.J., Dearth, C.L., Turner, N.J., et al. A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng Part A 18, 1941, 2012.
18. Mase, V.J., Jr., Hsu, J.R., Wolf, S.E., Wenke, J.C., Baer, D.G., Owens, J., et al. Clinical application of an acellular biologic scaffold for surgical repair of a large, traumatic quadriceps femoris muscle defect. Orthopedics 33, 511, 2010.
19. Conconi, M.T., De Coppi, P., Bellini, S., Zara, G., Sabatti, M., Marzaro, M., et al. Homologous muscle acellular matrix seeded with autologous myoblasts as a tissue-engineering approach to abdominal wall-defect repair. Biomaterials 26, 2567, 2005.
20. Page, R.L., Malcuit, C., Vilner, L., Vojtic, I., Shaw, S., Hed-blom, E., et al. Restoration of skeletal muscle defects with adult human cells delivered on fibrin microthreads. Tissue Eng Part A 17, 2629, 2011.
21. Rossi, C.A., Flaibani, M., Blaauw, B., Pozzobon, M., Figallo, E., Reggiani, C., et al. In vivo tissue engineering of functional skeletal muscle by freshly isolated satellite cells embedded in a photopolymerizable hydrogel. FASEB J 25, 2296, 2011.
22. Gharaibeh, B., Lavasani, M., Cummins, J.H., and Huard, J. Terminal differentiation is not a major determinant for the success of stem cell therapy-cross-talk between muscle-derived stem cells and host cells. Stem Cell Res Ther 2, 31, 2011.
23. Singer, N.G., and Caplan, A.I. Mesenchymal stem cells: mechanisms of inflammation. Annu Rev Pathol 6, 457, 2011.
24. Zammit, P.S., Partridge, T.A., and Yablonka-Reuveni, Z. The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem 54, 1177, 2006.
25. Hawke, T.J., and Garry, D.J. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91, 534, 2001.
26. 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.
27. Wu, X., Corona, B.T., Chen, X., and Walters, T.J. A standardized rat model of volumetric muscle loss injury for the development of tissue engineering therapies. Biores Open Access 1, 280, 2012.
28. 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.
29. Criswell, T.L., Corona, B.T., Ward, C.L., Miller, M., Patel, M., Wang, Z., et al. Compression-induced muscle injury in rats that mimics compartment syndrome in humans. Am J Pa-thol 180, 787, 2012.
30. 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.
31. Kandarian, S.C., Young, J.C., and Gomez, E.E. Adaptation in synergistic muscles to soleus and plantaris muscle removal in the rat hindlimb. Life Sci 51, 1691, 1992.
32. 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.
33. Ingalls, C.P., Warren, G.L., Lowe, D.A., Boorstein, D.B., and Armstrong, R.B. Differential effects of anesthetics on in vivo skeletal muscle contractile function in the mouse. J Appl Physiol 80, 332, 1996.
34. Gollnick, P.D., Timson, B.F., Moore, R.L., and Riedy, M. Muscular enlargement and number of fibers in skeletal muscles of rats. J Appl Physiol 50, 936, 1981.
35. Lehto, M., Duance, V.C., and Restall, D. Collagen and fi-bronectin in a healing skeletal muscle injury. An im-munohistological study of the effects of physical activity on the repair of injured gastrocnemius muscle in the rat. J Bone Joint Surg Br 67, 820, 1985.
36. Purslow, P.P. The structure and functional significance of variations in the connective tissue within muscle. Comp Biochem Physiol A Mol Integr Physiol 133, 947, 2002.
37. Purslow, P.P. Muscle fascia and force transmission. J Bodyw Mov Ther 14, 411, 2010.
38. Street, S.F., and Ramsey, R.W. Sarcolemma: transmitter of active tension in frog skeletal muscle. Science 149, 1379, 1965.
39. Stauber, W.T., Knack, K.K., Miller, G.R., and Grimmett, J.G. Fibrosis and intercellular collagen connections from four weeks of muscle strains. Muscle Nerve 19, 423, 1996.
40. Stauber, W.T., Smith, C.A., Miller, G.R., and Stauber, F.D. Recovery from 6 weeks of repeated strain injury to rat soleus muscles. Muscle Nerve 23, 1819, 2000.
41. Corona, B.T., Wu, X., Ward, C.L., Mcdaniel, J.S., Rathbone, C.R., and Walters, T.J. The promotion of a functional fibrosis in skeletal muscle with volumetric muscle loss injury following the transplantation of muscle-ECM. Biomaterials 34, 3324, 2013.
42. Kaariainen, M., Kaariainen, J., Jarvinen, T.L., Sievanen, H., Kalimo, H., and Jarvinen, M. Correlation between biome-chanical and structural changes during the regeneration of skeletal muscle after laceration injury. J Orthop Res 16, 197, 1998.
43. Lim, A.Y., Lahiri, A., Pereira, B.P., Tan, J.A., Sebastin, S.J., Tan, B.L., et al. The role of intramuscular nerve repair in the recovery of lacerated skeletal muscles. Muscle Nerve 33, 377, 2006.
44. Pereira, B.P., Tan, J.A., Zheng, L., Tan, B.L., Lahiri, A., Lim, A.Y., et al. The cut intramuscular nerve affects the recovery in the lacerated skeletal muscle. J Orthop Res 24, 102, 2006.
45. Denny-Brown, D. The influence of tension and innervation on the regeneration of skeletal muscle. J Neuropathol Exp Neurol 10, 94, 1951.
46. Meyer, G.A., and Lieber, R.L. Skeletal muscle fibrosis develops in response to desmin deletion. Am J Physiol Cell Physiol 302, C1609, 2012.
47. Kragh, J.F., Jr., and Basamania, C.J. Surgical repair of acute traumatic closed transection of the biceps brachii. J Bone Joint Surg Am 84-A, 992, 2002.
48. Rhoads, R.P., Johnson, R.M., Rathbone, C.R., Liu, X., Temm-Grove, C., Sheehan, S.M., et al. Satellite cell-mediated angio-genesis in vitro coincides with a functional hypoxia-inducible factor pathway. Am J Physiol Cell Physiol 296, C1321, 2009.
49. Lecourt, S., Lepelletier, Y., Vanneaux, V., Jarray, R., Domet, T., Raynaud, F., et al. Human Muscle Progenitor Cells Displayed Immunosuppressive Effect through Galectin-1 and Semaphorin-3A. Stem Cells Int 2012, 412610, 2012.
50. Badylak, S.F., Valentin, J.E., Ravindra, A.K., Mccabe, G.P., and Stewart-Akers, A.M. Macrophage phenotype as a determinant of biologic scaffold remodeling. Tissue Eng Part A 14, 1835, 2008.