Skeletal muscle tissue engineering: Strategies for volume tric constructs

Frontiers in Physiology

Volumn 5, Issue , 2014, Pages

  Vigodarzere, Giorgio Cittadella ^a   Mantero, Sara ^a  

^a POLITECNICO DI MILANO   (Italy)

Author keywords

Mechanobiology; Physical stimulation; Skeletal muscle; Tissue engineering; Vascularization

Indexed keywords

ATTENTION; CARDIOVASCULAR SYSTEM; CELL MATURATION; COCULTURE; DIFFERENTIATION; ELECTRIC POTENTIAL; IMPLANTATION; MECHANICAL STIMULATION; PHYSICAL STIMULATION; REVIEW; SKELETAL MUSCLE; TISSUE ENGINEERING; VASCULARIZATION;

EID: 85020179466     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00362     Document Type: Review

References (174)

1. Aärimaa, V., Kääriäinen, M., Vaittinen, S., Tanner, J., Järvinen, T., Best, T., et al. (2004). Restoration of myofiber continuity after transection injury in the rat soleus. Neuromuscul. Disord. 14, 421-428. doi: 10.1016/j.nmd.2004.03.009
2. Agostini, T., Lazzeri, D., and Spinelli, G. (2013). Anterolateral thigh flap: systematic literature review of specific donor-site complications and their management. J. Craniomaxillofac. Surg. 41, 15-21. doi: 10.1016/j.jcms.2012.05.003
3. Ahmed, W. W., Wolfram, T., Goldyn, A. M., Bruellhoff, K., Rioja, B. A., Moller, M., et al. (2010). Myoblast morphology and organization on biochemically micro-patterned hydrogel coatings under cyclic mechanical strain. Biomaterials 31, 250-258. doi: 10.1016/j.biomaterials.2009.09.047
4. Alekseeva, T., Unger, R., Brochhausen, C., Brown, R., and Kirkpatrick, C. (2014). Engineering a micro-vascular capillary bed in a tissue-like collagen construct. Tissue Eng. Part A. doi: 10.1089/ten.tea.2013.0570. [Epub ahead of print].
5. Amariglio, N., Hirshberg, A., Scheithauer, B., Cohen, Y., Loewenthal, R., Trakhtenbrot, L., et al. (2009). Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med. 6:e1000029. doi: 10.1371/journal.pmed.1000029
6. Araki, R., Uda, M., Hoki, Y., Sunayama, M., Nakamura, M., Ando, S., et al. (2013). Negligible immunogenicity of terminally differentiated cells derived from induced pluripotent or embryonic stem cells. Nature 494, 100-104. doi: 10.1038/nature11807
7. Atala, A., Bauer, S., Soker, S., Yoo, J., and Retik, A. (2006). Tissue-engineered autol-ogous bladders for patients needing cystoplasty. Lancet 367, 1241-1246. doi: 10.1016/S0140-6736(06)68438-9
8. Badylak, S. F. (2014). Decellularized allogeneic and xenogeneic tissue as a bioscaf-fold for regenerative medicine: factors that influence the host response. Ann. Biomed. Eng. 42, 1517-1527. doi: 10.1007/s10439-013-0963-7
9. Bae, H., Puranik, A., Gauvin, R., Edalat, F., Carrillo-Conde, B., Peppas, N., et al. (2012). Building vascular networks. Sci. Transl. Med. 4, 160ps123. doi: 10.1126/ scitranslmed.3003688
10. Bareja, A., Holt, J., Luo, G., Chang, C., Lin, J., Hinken, A., et al. (2014). Human and mouse skeletal muscle stem cells: convergent and divergent mechanisms of myogenesis. PLoS ONE 9:e90398. doi: 10.1371/journal.pone.0090398
11. Bian, W., Juhas, M., Pfeiler, T., and Bursac, N. (2012). Local tissue geometry determines contractile force generation of engineered muscle networks. Tissue Eng. Part A 18, 957-967. doi: 10.1089/ten.tea.2011.0313
12. Biggs, M., Richards, R., and Dalby, M. (2010). Nanotopographical modification: a regulator of cellular function through focal adhesions. Nanomedicine 6, 619-633. doi: 10.1016/j.nano.2010.01.009
13. Boerckel, J., Uhrig, B., Willett, N., Huebsch, N., and Guldberg, R. (2011). Mechanical regulation of vascular growth and tissue regeneration in vivo. Proc. Natl. Acad. Sci. U.S.A. 108, 80. doi: 10.1073/pnas.1107019108
14. Bohgaki, T., Atsumi, T., and Koike, T. (2007). Multiple autoimmune diseases after autologous stem-cell transplantation. N. Engl. J. Med. 357, 2734-2736. doi: 10.1056/NEJMc076383
15. Boldrin, L., Muntoni, F., and Morgan, J. (2010). Are human and mouse satellite cells really the same? J. Histochem. Cytochem. 58, 941-955. doi: 10.1369/jhc.2010.956201
16. Boonen, K., Langelaan, M., Polak, R., van der Schaft, D., Baaijens, F., and Post, M. (2010). Effects of a combined mechanical stimulation protocol: value for skeletal muscle tissue engineering. J. Biomech. 43, 1514-1521. doi: 10.1016/j.jbiomech.2010.01.039
17. Borisov, A. (1999). Regeneration of skeletal and cardiac muscle in mammals: do nonprimate models resemble human pathology? Wound Repair Regen. 7, 26-35. doi: 10.1046/j.1524-475x.1999.00026.x
18. Bosurgi, L., Manfredi, A., and Rovere-Querini, P. (2011). Macrophages in injured skeletal muscle: a perpetuum mobile causing and limiting fibrosis, prompting or restricting resolution and regeneration. Front. Immunol. 2:62. doi: 10.3389/fimmu.2011.00062
19. Breymann, T., Blanz, U., Wojtalik, M., Daenen, W., Hetzer, R., Sarris, G., et al. (2009). European Contegra multicentre study: 7-year results after 165 valved bovine jugular vein graft implantations. Thorac. Cardiovasc. Surg. 57, 257-269. doi: 10.1055/s-0029-1185513
20. Burdick, J., Mauck, R., Gorman, J., and Gorman, R. (2013). Acellular biomaterials: an evolving alternative to cell-based therapies. Sci. Transl. Med. 5, 176ps174. doi: 10.1126/scitranslmed.3003997
21. Candiani, G., Riboldi, S., Sadr, N., Lorenzoni, S., Neuenschwander, P., Montevecchi, F., et al. (2010). Cyclic mechanical stimulation favors myosin heavy chain accumulation in engineered skeletal muscle constructs. J. Appl. Biomater. Biomech. 8, 68-75. doi: 10.5301/JABB.2010.4829
22. Carmeliet, P., and Tessier-Lavigne, M. (2005). Common mechanisms of nerve and blood vessel wiring. Nature 436, 193-200. doi: 10.1038/nature03875
23. Carosio, S., Barberi, L., Rizzuto, E., Nicoletti, C., Prete, Z., and Musarò, A. (2013). Generation of eX vivo-vascularized Muscle Engineered Tissue (X-MET). Sci. Rep. 3:1420. doi: 10.1038/srep01420
24. Chargé, S., and Rudnicki, M. (2004). Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84, 209-238. doi: 10.1152/physrev.00019.2003
25. Cheng, G., Liao, S., Kit Wong, H., Lacorre, D., di Tomaso, E., Au, P., et al. (2011). Engineered blood vessel networks connect to host vasculature via wrapping-and-tapping anastomosis. Blood 118, 4740-4749. doi: 10.1182/blood-2011-02-338426
26. Chiu, L., Montgomery, M., Liang, Y., Liu, H., and Radisic, M. (2012). Perfusable branching microvessel bed for vascularization of engineered tissues. Proc. Natl. Acad. Sci. U.S.A. 109, 23. doi: 10.1073/pnas.1210580109
27. Christoffersson, G., Vågesjö, E., Vandooren, J., Lidén, M., Massena, S., Reinert, R., et al. (2012). VEGF-A recruits a proangiogenic MMP-9-delivering neutrophil subset that induces angiogenesis in transplanted hypoxic tissue. Blood 120, 4653-4662. doi: 10.1182/blood-2012-04-421040
28. Ciciliot, S., and Schiaffino, S. (2010). Regeneration of mammalian skeletal muscle. Basic mechanisms and clinical implications. Curr. Pharm. Des. 16, 906-914. doi: 10.2174/138161210790883453
29. Conconi, M., De Coppi, P., Bellini, S., Zara, G., Sabatti, M., Marzaro, M., et al. (2005). Homologous muscle acellular matrix seeded with autologous myoblasts as a tissue-engineering approach to abdominal wall-defect repair. Biomaterials 26, 2567-2574. doi: 10.1016/j.biomaterials.2004.07.035
30. Corona, B., Garg, K., Ward, C., McDaniel, J., Walters, T., and Rathbone, C. (2013a). Autologous minced muscle grafts: a tissue engineering therapy for the volumetric loss of skeletal muscle. Am. J. Physiol. Cell Physiol. 305, C761-C775. doi: 10.1152/ajpcell.00189.2013
31. Corona, B., Ward, C., Baker, H., Walters, T., and Christ, G. (2014). Implantation of in vitro tissue engineered muscle repair constructs and bladder acel-lular matrices partially restore in vivo skeletal muscle function in a rat model of volumetric muscle loss injury. Tissue Eng. Part A 20, 705-715. doi: 10.1089/ten.TEA.2012.0761
32. Corona, B., Wu, X., Ward, C., McDaniel, J., Rathbone, C., and Walters, T. (2013b). The promotion of a functional fibrosis in skeletal muscle with volumetric muscle loss injury following the transplantation of muscle-ECM. Biomaterials 34, 3324-3335. doi: 10.1016/j.biomaterials.2013.01.061
33. Criswell, T., Corona, B., Wang, Z., Zhou, Y., Niu, G., Xu, Y., et al. (2013). The role of endothelial cells in myofiber differentiation and the vascularization and inner-vation of bioengineered muscle tissue in vivo. Biomaterials 34, 140-149. doi: 10.1016/j.biomaterials.2012.09.045
34. Dahl, S., Kypson, A., Lawson, J., Blum, J., Strader, J., Li, Y., et al. (2011). Readily available tissue-engineered vascular grafts. Sci. Transl. Med. 3, 68ra69. doi: 10.1126/scitranslmed.3001426
35. Dalby, M., McCloy, D., Robertson, M., Agheli, H., Sutherland, D., Affrossman, S., et al. (2006). Osteoprogenitor response to semi-ordered and random nanotopographies. Biomaterials 27, 2980-2987. doi: 10.1016/j.biomaterials. 2006.01.010
36. De Coppi, P., Bellini, S., Conconi, M., Sabatti, M., Simonato, E., Gamba, P., et al. (2006). Myoblast-acellular skeletal muscle matrix constructs guarantee a long-term repair of experimental full-thickness abdominal wall defects. Tissue Eng. 12, 1929-1936. doi: 10.1089/ten.2006.12.1929
37. De Coppi, P., Delo, D., Farrugia, L., Udompanyanan, K., Yoo, J., Nomi, M., et al. (2005). Angiogenic gene-modified muscle cells for enhancement of tissue formation. Tissue Eng. 11, 1034-1044. doi: 10.1089/ten.2005.11.1034
38. de Jonge, N., Foolen, J., Brugmans, M., Söntjens, S., Baaijens, F., and Bouten, C. (2014). Degree of scaffold degradation influences collagen (re)orientation in engineered tissues. Tissue Eng. Part A 20, 1747-1757. doi: 10.1089/ten.TEA.2013.0517
39. Dellavalle, A., Maroli, G., Covarello, D., Azzoni, E., Innocenzi, A., Perani, L., et al. (2011). Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat. Commun. 2, 499. doi: 10.1038/ncomms1508
40. Dennis, R., and Kosnik, P. (2000). Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cell. Dev. Biol. Anim. 36, 327-335. doi: 10.1290/1071-2690(2000)036<0327:EAICPO>2.0.CO;2
41. Dennis, R., Kosnik, P., and Gilbert, M. (2001). Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. Am. J. Physiol. Cell Physiol. 280, C288-C295.
42. Discher, D., Janmey, P., and Wang, Y.-L. (2005). Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143. doi: 10.1126/sci-ence.1116995
43. Egusa, H., Kobayashi, M., Matsumoto, T., Sasaki, J.-I., Uraguchi, S., and Yatani, H. (2013). Application of cyclic strain for accelerated skeletal myogenic differentiation of mouse bone marrow-derived mesenchymal stromal cells with cell alignment. Tissue Eng. Part A 19, 770-782. doi: 10.1089/ten.tea.2012.0164
44. Elmer, D. F. K., Amrinder, S. N., Lee, E. W., Ji, W., Joseph, S., Cristina, H. A., et al. (2011). Bioprinting of growth factors onto aligned sub-micron fibrous scaffolds for simultaneous control of cell differentiation and alignment. Biomaterials 32, 8097-8107. doi: 10.1016/j.biomaterials.2011.07.025
45. Engler, A., Griffin, M., Sen, S., Bönnemann, C., Sweeney, H., and Discher, D. (2004). Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 166, 877-887. doi: 10.1083/jcb.200405004
46. Engler, A., Sen, S., Sweeney, H., and Discher, D. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689. doi: 10.1016/j.cell.2006.06.044
47. Eyckmans, J., Boudou, T., Yu, X., and Chen, C. (2011). A hitchhiker's guide to mechanobiology. Dev. Cell 21, 35-47. doi: 10.1016/j.devcel.2011.06.015
48. Feaver, R., Gelfand, B., and Blackman, B. (2013). Human haemodynamic frequency harmonics regulate the inflammatory phenotype of vascular endothelial cells. Nat. Commun. 4, 1525. doi: 10.1038/ncomms2530
49. Fisher, M., and Mauck, R. (2013). Tissue engineering and regenerative medicine: recent innovations and the transition to translation. Tissue Eng. Part B Rev. 19, 1-13. doi: 10.1089/ten.teb.2012.0723
50. Fuoco, C., Sangalli, E., Vono, R., Testa, S., Sacchetti, B., Latronico, M. V. G., et al. (2014). 3D hydrogel environment rejuvenates aged pericytes for skeletal muscle tissue engineering. Front. Physiol. 5:203. doi: 10.3389/fphys.2014.00203
51. Garland, C., and Pomerantz, J. (2012). Regenerative strategies for craniofacial disorders. Front. Physiol. 3:453. doi: 10.3389/fphys.2012.00453
52. Gayraud-Morel, B., Chrétien, F., and Tajbakhsh, S. (2009). Skeletal muscle as a paradigm for regenerative biology and medicine. Regen. Med. 4, 293-319. doi: 10.2217/17460751.4.2.293
53. Gianni-Barrera, R., Trani, M., Fontanellaz, C., Heberer, M., Djonov, V., Hlushchuk, R., et al. (2013). VEGF over-expression in skeletal muscle induces angiogen-esis by intussusception rather than sprouting. Angiogenesis 16, 123-136. doi: 10.1007/s10456-012-9304-y
54. Goldring, C. E., Duffy, P. A., Benvenisty, N., Andrews, P. W., Ben-David, U., Eakins, R., et al. (2011). Assessing the safety of stem cell therapeutics. Cell Stem Cell 8, 618-628. doi: 10.1016/j.stem.2011.05.012
55. Griffith, C., Miller, C., Sainson, R., Calvert, J., Jeon, N., Hughes, C., et al. (2005). Diffusion limits of an in vitro thick prevascularized tissue. Tissue Eng. 11, 257-266. doi: 10.1089/ten.2005.11.257
56. Grogan, B., Hsu, J., and Skeletal Trauma Research, C. (2011). Volumetric muscle loss. J. Am. Acad. Orthop. Surg. 19(Suppl. 1), 7.
57. Gualandi, C., Zucchelli, A., Fernández Osorio, M., Belcari, J., and Focarete, M. (2013). Nanovascularization of polymer matrix: generation of nanochannels and nanotubes by sacrificial electrospun fibers. Nano Lett. 13, 5385-5390. doi: 10.1021/nl402930x
58. Guilak, F., Butler, D., Goldstein, S., and Baaijens, F. (2014). Biomechanics and mechanobiology in functional tissue engineering. J. Biomech. 47, 1933-1940. doi: 10.1016/j.jbiomech.2014.04.019
59. Gurtner, G., Werner, S., Barrandon, Y., and Longaker, M. (2008). Wound repair and regeneration. Nature 453, 314-321. doi: 10.1038/nature07039
60. Hanjaya-Putra, D., Shen, Y.-I., Wilson, A., Fox-Talbot, K., Khetan, S., Burdick, J., et al. (2013). Integration and regression of implanted engineered human vascular networks during deep wound healing. Stem Cells Transl. Med. 2, 297-306. doi: 10.5966/sctm.2012-0111
61. Haraguchi, Y., Shimizu, T., Sasagawa, T., Sekine, H., Sakaguchi, K., Kikuchi, T., et al. (2012). Fabrication of functional three-dimensional tissues by stacking cell sheets in vitro. Nat. Protoc. 7, 850-858. doi: 10.1038/nprot.2012.027
62. Heredia, J., Mukundan, L., Chen, F., Mueller, A., Deo, R., Locksley, R., et al. (2013). Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell 153, 376-388. doi: 10.1016/j.cell.2013.02.053
63. Hibino, N., Villalona, G., Pietris, N., Duncan, D. R., Schoffner, A., Roh, J. D., et al. (2011). Tissue-engineered vascular grafts form neovessels that arise from regeneration of the adjacent blood vessel. FASEB J. 25, 2731-2739. doi: 10.1096/fj.11-182246
64. Hong, S. G., Winkler, T., Wu, C., Guo, V., Pittaluga, S., Nicolae, A., et al. (2014). Path to the clinic: assessment of iPSC-based cell therapies in vivo in a nonhuman primate model. Cell Rep. 7, 1298-1309. doi: 10.1016/j.celrep.2014.04.019
65. Hooper, R., Hernandez, K., Boyko, T., Harper, A., Joyce, J., Golas, A., et al. (2014). Fabrication and in vivo microanastomosis of vascularized tissue-engineered constructs. Tissue Eng. Part A. doi: 10.1089/ten.tea.2013.0583. [Epub ahead of print].
66. Hosseini, V., Ahadian, S., Ostrovidov, S., Camci-Unal, G., Chen, S., Kaji, H., et al. (2012). Engineered contractile skeletal muscle tissue on a microgrooved methacrylated gelatin substrate. Tissue Eng. Part A 18, 2453-2465. doi: 10.1089/ten.tea.2012.0181
67. Huxley, H., and Hanson, J. (1954). Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173, 973-976. doi: 10.1038/173973a0
68. Järvinen, T., Järvinen, M., and Kalimo, H. (2013). Regeneration of injured skeletal muscle after the injury. Muscles Ligaments Tendons J. 3, 337-345. doi: 10.11138/ mltj/2013.3.4.337
69. Joe, A., 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. doi: 10.1038/ncb2015
70. Ju, Y. M., Atala, A., Yoo, J. J., and Lee, S. J. (2014). In situ regeneration of skeletal muscle tissue through host cell recruitment. Acta Biomater. 10, 4332-4339. doi: 10.1016/j.actbio.2014.06.022
71. Juhas, M., Engelmayr, G. C., Fontanella, A. N., Palmer, G. M., and Bursac, N. (2014). Biomimetic engineered muscle with capacity for vascular integration and functional maturation in vivo. Proc. Natl. Acad. Sci. U.S.A. 111, 5508-5513. doi: 10.1073/pnas.1402723111
72. Kang, K.-T., Allen, P., and Bischoff, J. (2011). Bioengineered human vascular networks transplanted into secondary mice reconnect with the host vasculature and re-establish perfusion. Blood 118, 6718-6721. doi: 10.1182/blood-2011-08-375188
73. Karande, T., Ong, J., and Agrawal, C. (2004). Diffusion in musculoskeletal tissue engineering scaffolds: design issues related to porosity, permeability, architecture, and nutrient mixing. Ann. Biomed. Eng. 32, 1728-1743. doi: 10.1007/s10439-004-7825-2
74. Keane, T., Londono, R., Turner, N., and Badylak, S. (2012). Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 33, 1771-1781. doi: 10.1016/j.biomaterials.2011.10.054
75. Kelc, R., Trapecar, M., Vogrin, M., and Cencic, A. (2013). Skeletal muscle-derived cell cultures as potent models in regenerative medicine research. Muscle Nerve 47, 477-482. doi: 10.1002/mus.23688
76. Kelly, R. (2010). Core issues in craniofacial myogenesis. Exp. Cell Res. 316, 3034-3041. doi: 10.1016/j.yexcr.2010.04.029
77. Kilarski, W., Samolov, B., Petersson, L., Kvanta, A., and Gerwins, P. (2009). Biomechanical regulation of blood vessel growth during tissue vascularization. Nat. Med. 15, 657-664. doi: 10.1038/nm.1985
78. Knoeplfer, P. S. (2009). Deconstructing stem cell tumorigenicity: a roadmap to safe regenerative medicine. Stem Cells 27, 1050-1056. doi: 10.1002/stem.37
79. Koffler, J., Kaufman-Francis, K., Shandalov, Y., Yulia, S., Egozi, D., Dana, E., et al. (2011). Improved vascular organization enhances functional integration of engineered skeletal muscle grafts. Proc. Natl. Acad. Sci. U.S.A. 108, 14789-14794. doi: 10.1073/pnas.1017825108
80. Kolesky, D., Truby, R., Gladman, A., Busbee, T., Homan, K., and Lewis, J. (2014). 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv. Mater. 26, 3124-3130. doi: 10.1002/adma.201305506
81. Koopman, R., Ly, C. H., and Ryall, J. G. (2014). A metabolic link to skeletal muscle wasting and regeneration. Front. Physiol. 5:32. doi: 10.3389/fphys.2014.00032
82. Lam, M., Huang, Y.-C., Birla, R., and Takayama, S. (2009). Microfeature guided skeletal muscle tissue engineering for highly organized 3-dimensional free-standing constructs. Biomaterials 30, 1150-1155. doi: 10.1016/j.biomaterials.2008.11.014
83. Langer, R., and Vacanti, J. (1993). Tissue engineering. Science 260, 920-926. doi: 10.1126/science.8493529
84. Lemos, D., Paylor, B., Chang, C., Sampaio, A., Underhill, T., and Rossi, F. (2012). Functionally convergent white adipogenic progenitors of different lineages participate in a diffused system supporting tissue regeneration. Stem Cells 30, 1152-1162. doi: 10.1002/stem.1082
85. Leong, M., Toh, J., Du, C., Narayanan, K., Lu, H., Lim, T., et al. (2013). Patterned prevascularised tissue constructs by assembly of polyelectrolyte hydrogel fibres. Nat. Commun. 4, 2353. doi: 10.1038/ncomms3353
86. Lesman, A., Gepstein, L., and Levenberg, S. (2010). Vascularization shaping the heart. Ann. N.Y. Acad. Sci. 1188, 46-51. doi: 10.1111/j.1749-6632.2009.05082.x
87. Lesman, A., Koffler, J., Atlas, R., Blinder, Y. J., Kam, Z., and Levenberg, S. (2011). Engineering vessel-like networks within multicellular fibrin-based constructs. Biomaterials 32, 7856-7869. doi: 10.1016/j.biomaterials.2011.07.003
88. Levenberg, S., Rouwkema, J., Macdonald, M., Garfein, E. S., Kohane, D. S., Darland, D. C., et al. (2005). Engineering vascularized skeletal muscle tissue. Nat. Biotechnol. 23, 879-884. doi: 10.1038/nbt1109
89. Li, M., Dickinson, C., Finkelstein, E., Neville, C., and Sundback, C. (2011). The role of fibroblasts in self-assembled skeletal muscle. Tissue Eng. Part A 17, 2641-2650. doi: 10.1089/ten.tea.2010.0700
90. Li, M., Willett, N., Uhrig, B., Guldberg, R., and Warren, G. (2013a). Functional analysis of limb recovery following autograft treatment of volumetric muscle loss in the quadriceps femoris. J. Biomech. 47, 2013-2021. doi: 10.1016/j. jbiomech.2013.10.057
91. Li, Y., Huang, G., Zhang, X., Wang, L., Du, Y., Lu, T., et al. (2013b). Engineering cell alignment in vitro. Biotechnol. Adv. 32, 347-365. doi: 10.1016/j.biotechadv. 2013.11.007
92. Lieber, R., and Fridén, J. (2000). Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23, 1647-1666. doi: 10.1002/1097-4598(200011)23:11<1647::AID-MUS1>3.0.co;2-M
93. Liu, G., Mac Gabhann, F., and Popel, A. (2012). Effects of fiber type and size on the heterogeneity of oxygen distribution in exercising skeletal muscle. PLoS ONE 7:e44375. doi: 10.1371/journal.pone.0044375
94. Liu, Z., Tang, Y., Lü, S., Zhou, J., Du, Z., Duan, C., et al. (2013). The tumourigenic-ity of iPS cells and their differentiated derivates. J. Cell. Mol. Med. 17, 782-791. doi: 10.1111/jcmm.12062
95. Livne, A., Bouchbinder, E., and Geiger, B. (2014). Cell reorientation under cyclic stretching. Nat. Commun. 5:3938. doi: 10.1038/ncomms4938
96. Lu, H., Hoshiba, T., Kawazoe, N., and Chen, G. (2011). Autologous extracellular matrix scaffolds for tissue engineering. Biomaterials 32, 2489-2499. doi: 10.1016/j.biomaterials.2010.12.016
97. Macchiarini, P., Jungebluth, P., Go, T., Asnaghi, M., Rees, L., Cogan, T., et al. (2008). Clinical transplantation of a tissue-engineered airway. Lancet 372, 2023-2030. doi: 10.1016/S0140-6736(08)61598-6
98. Mantovani, A., Biswas, S., Galdiero, M., Sica, A., and Locati, M. (2013). Macrophage plasticity and polarization in tissue repair and remodelling. J. Pathol. 229, 176-185. doi: 10.1002/path.4133
99. Martin, I., Simmons, P. J., and Williams, D. F. (2014). Manufacturing challenges in regenerative medicine. Sci. Transl. Med. 6, 232fs216. doi: 10.1126/scitranslmed. 3008558
100. Mase, V., Hsu, J., Wolf, S., Wenke, J., Baer, D., 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, 511. doi: 10.3928/01477447-20100526-24
101. Mauro, A. (1961). Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493-495. doi: 10.1083/jcb.9.2.493
102. McAllister, T., Maruszewski, M., Garrido, S., Wystrychowski, W., Dusserre, N., Marini, A., et al. (2009). Effectiveness of haemodialysis access with an autol-ogous tissue-engineered vascular graft: a multicentre cohort study. Lancet 373, 1440-1446. doi: 10.1016/S0140-6736(09)60248-8
103. Mei, Y., Saha, K., Bogatyrev, S. R., Yang, J., Hook, A. L., Kalcioglu, Z. I., et al. (2010). Combinatorial development of biomaterials for clonal growth of human pluripotent stem cells. Nat. Mater. 9, 768-778. doi: 10.1038/nmat2812
104. Mertens, J., Sugg, K., Lee, J., and Larkin, L. (2014). Engineering muscle constructs for the creation of functional engineered musculoskeletal tissue. Regen. Med. 9, 89-100. doi: 10.2217/rme.13.81
105. Miller, J., Stevens, K., Yang, M., Baker, B., Nguyen, D.-H. T., Cohen, D., et al. (2012). Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater. 11, 768-774. doi: 10.1038/nmat3357
106. Monge, C., Ren, K., Berton, K., Guillot, R., Peyrade, D., and Picart, C. (2012). Engineering muscle tissues on microstructured polyelectrolyte multilayer films. Tissue Eng. Part A 18, 1664-1676. doi: 10.1089/ten.tea.2012.0079
107. Morimoto, Y., Kato-Negishi, M., Onoe, H., and Takeuchi, S. (2013). Three-dimensional neuron-muscle constructs with neuromuscular junctions. Biomaterials 34, 9413-9419. doi: 10.1016/j.biomaterials.2013.08.062
108. Mozzetta, C., Consalvi, S., Saccone, V., Tierney, M., Diamantini, A., Mitchell, K., 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. doi: 10.1002/emmm.201202096
109. Mujagic, E., Gianni-Barrera, R., Trani, M., Patel, A., Gürke, L., Heberer, M., et al. (2013). Induction of aberrant vascular growth, but not of normal angiogen-esis, by cell-based expression of different doses of human and mouse VEGF is species-dependent. Hum. Gene Ther. Methods 24, 28-37. doi: 10.1089/hgtb. 2012.197
110. Muraoka, M., Shimizu, T., Itoga, K., Takahashi, H., and Okano, T. (2013). Control of the formation of vascular networks in 3D tissue engineered constructs. Biomaterials 34, 696-703. doi: 10.1016/j.biomaterials.2012.10.009
111. Murphy, M., Lawson, J., Mathew, S., Hutcheson, D., and Kardon, G. (2011). Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138, 3625-3637. doi: 10.1242/dev.064162
112. Nagamori, E., Ngo, T., 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. doi: 10.1016/j.biomaterials.2012.08.055
113. Naito, Y., Imai, Y., Shin'oka, T., Kashiwagi, J., Aoki, M., Watanabe, M., et al. (2003). Successful clinical application of tissue-engineered graft for extracardiac Fontan operation. J. Thorac. Cardiovasc. Surg. 125, 419-420. doi: 10.1067/mtc. 2003.134
114. Nava, M., Raimondi, M., and Pietrabissa, R. (2014). Bio-chemo-mechanical models for nuclear deformation in adherent eukaryotic cells. Biomech. Model. Mechanobiol. 13, 929-943. doi: 10.1007/s10237-014-0558-8
115. Nunes, S., Miklas, J., 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. doi: 10.1038/nmeth.2524
116. Ostrovidov, S., Hosseini, V., Ahadian, S., Fujie, T., Parthiban, S. P., Bae, H., et al. (2014). Skeletal muscle tissue engineering: methods to form skeletal myotubes and their applications. Tissue Eng. Part B Rev. doi: 10.1089/ten.teb.2013.0534. [Epub ahead of print].
117. Ott, H., Matthiesen, T., Goh, S.-K., Black, L., Kren, S., Netoff, T., et al. (2008). Perfusion-decellularized matrix: using nature's platform to engineer a bioartifi-cial heart. Nat. Med. 14, 213-221. doi: 10.1038/nm1684
118. Palamà, I., D'Amone, S., Coluccia, A., and Gigli, G. (2013). Micropatterned polyelectrolyte nanofilms promote alignment and myogenic differentiation of C2C12 cells in standard growth media. Biotechnol. Bioeng. 110, 586-596. doi: 10.1002/bit.24626
119. Pannérec, A., Marazzi, G., and Sassoon, D. (2012). Stem cells in the hood: the skeletal muscle niche. Trends Mol. Med. 18, 599-606. doi: 10.1016/j.molmed.2012. 07.004
120. Pashuck, E., and Stevens, M. (2012). Designing regenerative biomaterial therapies for the clinic. Sci. Transl. Med. 4, 160sr164. doi: 10.1126/scitranslmed.3002717
121. Pennisi, C., Olesen, C., de Zee, M., Rasmussen, J., and Zachar, V. (2011). Uniaxial cyclic strain drives assembly and differentiation of skeletal myocytes. Tissue Eng. Part A 17, 2543-2550. doi: 10.1089/ten.tea.2011.0089
122. Radisic, M., Malda, J., Epping, E., Geng, W., Langer, R., and Vunjak-Novakovic, G. (2006). Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol. Bioeng. 93, 332-343. doi: 10.1002/bit. 20722
123. Radisic, M., Yang, L., Boublik, J., Cohen, R., Langer, R., Freed, L., et al. (2004). Medium perfusion enables engineering of compact and contractile cardiac tissue. Am. J. Physiol. Heart Circ. Physiol. 286, 16. doi: 10.1152/ajpheart. 00171.2003
124. Raghavan, S., Nelson, C., Baranski, J., Lim, E., and Chen, C. (2010). Geometrically controlled endothelial tubulogenesis in micropatterned gels. Tissue Eng. Part A 16, 2255-2263. doi: 10.1089/ten.tea.2009.0584
125. Ranga, A., Gobaa, S., Okawa, Y., Mosiewicz, K., Negro, A., and Lutolf, M. P. (2014). 3D niche microarrays for systems-level analyses of cell fate. Nat. Commun. 5:4324. doi: 10.1038/ncomms5324
126. Riboldi, S., Sadr, N., Pigini, L., Neuenschwander, P., Simonet, M., Mognol, P., et al. (2008). Skeletal myogenesis on highly orientated microfibrous polyesterurethane scaffolds. J. Biomed. Mater. Res. Part A 84, 1094-1101. doi: 10.1002/jbm.a.31534
127. Roh, J., Sawh-Martinez, R., Brennan, M., Jay, S., Devine, L., Rao, D., et al. (2010). Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling. Proc. Natl. Acad. Sci. U.S.A. 107, 4669-4674. doi: 10.1073/pnas.0911465107
128. Rouwkema, J., Gibbs, S., Lutolf, M., Martin, I., Vunjak-Novakovic, G., and Malda, J. (2011). In vitro platforms for tissue engineering: implications for basic research and clinical translation. J. Tissue Eng. Regen. Med. 5, 7. doi: 10.1002/term.414
129. Saccone, V., Consalvi, S., Giordani, L., Mozzetta, C., Barozzi, I., Sandoná, M., et al. (2014). HDAC-regulated myomiRs control BAF60 variant exchange and direct the functional phenotype of fibro-adipogenic progenitors in dystrophic muscles. Genes Dev. 28, 841-857. doi: 10.1101/gad.234468.113
130. Saclier, M., Cuvellier, S., Magnan, M., Mounier, R., and Chazaud, B. (2013). Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration. FEBS J. 280, 4118-4130. doi: 10.1111/febs.12166
131. Sadr, N., Pippenger, B. E., Scherberich, A., Wendt, D., Mantero, S., Martin, I., et al. (2012). Enhancing the biological performance of synthetic polymeric materials by decoration with engineered, decellularized extracellular matrix. Biomaterials 33, 5085-5093. doi: 10.1016/j.biomaterials.2012.03.082
132. Sakaguchi, K., Shimizu, T., Horaguchi, S., Sekine, H., Yamato, M., Umezu, M., et al. (2013). In vitro engineering of vascularized tissue surrogates. Sci. Rep. 3:1316. doi: 10.1038/srep01316
133. Sala, A., Hänseler, P., Ranga, A., Lutolf, M. P., Vörös, J., Ehrbar, M., et al. (2011). Engineering 3D cell instructive microenvironments by rational assembly of artificial extracellular matrices and cell patterning. Integr. Biol. (Camb) 3, 1102-1111. doi: 10.1039/c1ib00045d
134. Salimath, A. S., and García, A. J. (2014). Biofunctional hydrogels for skeletal muscle constructs. J. Tissue Eng. Regen. Med. doi: 10.1002/term.1881. [Epub ahead of print].
135. Sawa, Y., Miyagawa, S., Sakaguchi, T., Fujita, T., Matsuyama, A., Saito, A., et al. (2012). Tissue engineered myoblast sheets improved cardiac function sufficiently to discontinue LVAS in a patient with DCM: report of a case. Surg. Today 42, 181-184. doi: 10.1007/s00595-011-0106-4
136. Schmalbruch, H. (1976). The morphology of regeneration of skeletal muscles in the rat. Tissue Cell 8, 673-692. doi: 10.1016/0040-8166(76)90039-2
137. Sekine, H., Shimizu, T., Sakaguchi, K., Dobashi, I., Wada, M., Yamato, M., et al. (2013). In vitro fabrication of functional three-dimensional tissues with perfusable blood vessels. Nat. Commun. 4, 1399. doi: 10.1038/ ncomms2406
138. Seok, J., Warren, H., Cuenca, A., Mindrinos, M., Baker, H., Xu, W., et al. (2013). Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. U.S.A. 110, 3507-3512. doi: 10.1073/pnas.1222 878110
139. Shah, R., Knowles, J., Hunt, N., and Lewis, M. (2013). Development of a novel smart scaffold for human skeletal muscle regeneration. J. Tissue Eng. Regen. Med. doi: 10.1002/term.1780. [Epub ahead of print].
140. 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. U.S.A. 111, 6010-6015. doi: 10.1073/pnas.1402679111
141. Sharples, A., Player, D., Martin, N., Mudera, V., Stewart, C., and Lewis, M. (2012). Modelling in vivo skeletal muscle ageing in vitro using three-dimensional bioengineered constructs. Aging cell 11, 986-995. doi: 10.1111/j.1474-9726.2012.00869.x
142. Shevchenko, E., Makarevich, P., Tsokolaeva, Z., Boldyreva, M., Sysoeva, V., Tkachuk, V., et al. (2013). Transplantation of modified human adipose derived stromal cells expressing VEGF165 results in more efficient angiogenic response in ischemic skeletal muscle. J. Transl. Med. 11:138. doi: 10.1186/1479-5876-11-138
143. Sicari, B. M., Rubin, J. P., Dearth, C. L., Wolf, M. T., Ambrosio, F., Boninger, M., et al. (2014). An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss. Sci. Transl. Med. 6, 234ra258. doi: 10.1126/scitranslmed.3008085
144. Snyman, C., Goetsch, K., Myburgh, K., and Niesler, C. (2013). Simple silicone chamber system for in vitro three-dimensional skeletal muscle tissue formation. Front. Physiol. 4:349. doi: 10.3389/fphys.2013.00349
145. Suzuki, N., Yamazaki, S., Yamaguchi, T., Okabe, M., Masaki, H., Takaki, S., et al. (2013). Generation of engraftable hematopoietic stem cells from induced pluripotent stem cells by way of teratoma formation. Mol. Ther. 21, 1424-1431. doi: 10.1038/mt.2013.71
146. Takahashi, K., and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676. doi: 10.1016/j.cell.2006.07.024
147. Takaza, M., Moerman, K., Gindre, J., Lyons, G., and Simms, C. (2013). The anisotropic mechanical behaviour of passive skeletal muscle tissue subjected to large tensile strain. J. Mech. Behav. Biomed. Mater. 17, 209-220. doi: 10.1016/j.jmbbm.2012.09.001
148. Tamaki, T., Soeda, S., Hashimoto, H., Saito, K., Sakai, A., Nakajima, N., et al. (2013). 3D reconstitution of nerve-blood vessel networks using skeletal muscle-derived multipotent stem cell sheet pellets. Regen. Med. 8, 437-451. doi: 10.2217/rme.13.30
149. Tedesco, F., and Cossu, G. (2012). Stem cell therapies for muscle disorders. Curr. Opin. Neurol. 25, 597-603. doi: 10.1097/WCO.0b013e328357f288
150. Tedesco, F., Dellavalle, A., Diaz-Manera, J., Messina, G., and Cossu, G. (2010). Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J. Clin. Invest. 120, 11-19. doi: 10.1172/JCI40373
151. Teixeira, C., Zamunér, S., Zuliani, J., Fernandes, C., Cruz-Hofling, M., Fernandes, I., et al. (2003). Neutrophils do not contribute to local tissue damage, but play a key role in skeletal muscle regeneration, in mice injected with Bothrops asper snake venom. Muscle Nerve 28, 449-459. doi: 10.1002/mus.10453
152. Ten Broek, R., Grefte, S., and Von den Hoff, J. (2010). Regulatory factors and cell populations involved in skeletal muscle regeneration. J. Cell. Physiol. 224, 7-16. doi: 10.1002/jcp.22127
153. Teodori, L., Costa, A., Marzio, R., Perniconi, B., Coletti, D., Adamo, S., et al. (2014). Native extracellular matrix: a new scaffolding platform for repair of damaged muscle. Front. Physiol. 5:218. doi: 10.3389/fphys.2014.00218
154. Thirabanjasak, D., Tantiwongse, K., and Thorner, P. S. (2010). Angiomyeloproliferative lesions following autologous stem cell therapy. J. Am. Soc. Nephrol. 21, 1218-1222. doi: 10.1681/ASN.2009111156
155. Tidball, J., Dorshkind, K., and Wehling-Henricks, M. (2014). Shared signaling systems in myeloid cell-mediated muscle regeneration. Development 141, 1184-1196. doi: 10.1242/dev.098285
156. Tidball, J., and Villalta, S. (2010). Regulatory interactions between muscle and the immune system during muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, 87. doi: 10.1152/ajpregu.00735.2009
157. Tirziu, D., and Simons, M. (2009). Endothelium as master regulator of organ development and growth. Vascul. Pharmacol. 50, 1-7. doi: 10.1016/j.vph.2008. 08.003
158. Turner, N., and Badylak, S. (2012). Regeneration of skeletal muscle. Cell Tissue Res. 347, 759-774. doi: 10.1007/s00441-011-1185-7
159. Turner, N. J., Badylak, J. S., Weber, D. J., and Badylak, S. F. (2012). Biologic scaffold remodeling in a dog model of complex musculoskeletal injury. J. Surg. Res. 176, 490-502. doi: 10.1016/j.jss.2011.11.1029
160. Uezumi, A., Ito, T., Morikawa, D., Shimizu, N., Yoneda, T., Segawa, M., et al. (2011). Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle. J. Cell Sci. 124, 3654-3664. doi: 10.1242/jcs.086629
161. Unadkat, H., Hulsman, M., Cornelissen, K., Papenburg, B., Truckenmüller, R., Carpenter, A., et al. (2011). An algorithm-based topographical biomaterials library to instruct cell fate. Proc. Natl. Acad. Sci. U.S.A. 108, 16565-16570. doi: 10.1073/pnas.1109861108
162. van der Schaft, D., van Spreeuwel, A. C., van Assen, H., and Baaijens, F. (2011). Mechanoregulation of vascularization in aligned tissue-engineered muscle: a role for vascular endothelial growth factor. Tissue Eng. Part A 17, 2857-2865. doi: 10.1089/ten.tea.2011.0214
163. Vandenburgh, H. (2010). High-content drug screening with engineered musculoskeletal tissues. Tissue Eng. Part B Rev. 16, 55-64. doi: 10.1089/ten.teb.2009.0445
164. Vandenburgh, H., Karlisch, P., and Farr, L. (1988). Maintenance of highly contractile tissue-cultured avian skeletal myotubes in collagen gel. In Vitro Cell. Dev. Biol. 24, 166-174. doi: 10.1007/BF02623542
165. Vandenburgh, H., Shansky, J., Del Tatto, M., and Chromiak, J. (1999). Organogenesis of skeletal muscle in tissue culture. Methods Mol. Med. 18, 217-225.
166. Vandenburgh, H. H., Swasdison, S., and Karlisch, P. (1991). Computer-aided mechanogenesis of skeletal muscle organs from single cells in vitro. FASEB J. 5, 2860-2867.
167. Wang, L., Shansky, J., and Vandenburgh, H. (2013). Induced formation and maturation of acetylcholine receptor clusters in a defined 3D bio-artificial muscle. Mol. Neurobiol. 48, 397-403. doi: 10.1007/s12035-013-8412-z
168. Wang, N., Tytell, J., and Ingber, D. (2009). Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10, 75-82. doi: 10.1038/nrm2594
169. Wang, Y., and Rudnicki, M. (2012). Satellite cells, the engines of muscle repair. Nat. Rev. Mol. Cell Biol. 13, 127-133. doi: 10.1038/nrm3265
170. Weist, M., Wellington, M., Bermudez, J., Kostrominova, T., Mendias, C., Arruda, E., et al. (2012). TGF-ß1 enhances contractility in engineered skeletal muscle. J. Tissue Eng. Regen. Med. 7, 562-571. doi: 10.1002/term.551
171. Williams, M., Kostrominova, T., Arruda, E., and Larkin, L. (2012). Effect of implantation on engineered skeletal muscle constructs. J. Tissue Eng. Regen. Med. 7, 434-442. doi: 10.1002/term.537
172. Wolf, M., Daly, K., Reing, J., and Badylak, S. (2012). Biologic scaffold composed of skeletal muscle extracellular matrix. Biomaterials 33, 2916-2925. doi: 10.1016/j.biomaterials.2011.12.055
173. Yamato, M., Akiyama, Y., Kobayashi, J., Yang, J., Kikuchi, A., and Okano, T. (2007). Temperature-responsive cell culture surfaces for regenerative medicine with cell sheet engineering. Prog. Polym. Sci. 32, 1123-1133. doi: 10.1016/j.progpolymsci. 2007.06.002
174. Zhang, H., Zhou, L., and Zhang, W. (2014). Control of scaffold degradation in tissue engineering: a review. Tissue Eng. Part B Rev. doi: 10.1089/ten.teb.2013. 0452. [Epub ahead of print].s