Biomaterial-based delivery for skeletal muscle repair

Advanced Drug Delivery Reviews

Volumn 84, Issue , 2015, Pages 188-197

  Cezar, Christine A ^a,b   Mooney, David J ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Cell therapy; Drug delivery; Microenvironmental cue; Muscle regeneration; Satellite cell; Synthetic niche; Tissue engineered muscle

Indexed keywords

CELLS; CONTROLLED DRUG DELIVERY; CYTOLOGY; DRUG DELIVERY; NEURONS; SATELLITES; TARGETED DRUG DELIVERY;

CELL THERAPY; MICROENVIRONMENTAL CUE; MUSCLE REGENERATION; SATELLITE CELLS; SYNTHETIC NICHE;

MUSCLE;

ALGINIC ACID; BIOMATERIAL; COLLAGEN; FIBRIN; FIBROBLAST GROWTH FACTOR 2; MACROGOL; MYOD PROTEIN; POLYACRYLAMIDE; SCATTER FACTOR; SOMATOMEDIN C; TRANSCRIPTION FACTOR PAX7; VASCULOTROPIN;

CELL DELIVERY SYSTEM; CELL EXPANSION; CELL FATE; CELL ISOLATION; CELL MANIPULATION; CELL MIGRATION; CELL THERAPY; CELL TRANSFER; CLINICAL EFFECTIVENESS; DISEASE SEVERITY; DRUG DELIVERY DEVICE; DRUG DELIVERY SYSTEM; DUCHENNE MUSCULAR DYSTROPHY; ELASTICITY; EXTRACELLULAR MATRIX; HEART INJURY; HUMAN; IN VIVO STUDY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MUSCLE ATROPHY; MUSCLE BIOPSY; MUSCLE INJURY; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; STEM CELL NICHE; TISSUE ENGINEERING; PHYSIOLOGY; PROCEDURES; REGENERATION; STEM CELL TRANSPLANTATION;

BIOCOMPATIBLE MATERIALS; HUMANS; MUSCLE, SKELETAL; REGENERATION; STEM CELL TRANSPLANTATION;

EID: 84929081287     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2014.09.008     Document Type: Review

References (116)

1. Juhas M., Bursac N. Engineering skeletal muscle repair. Curr. Opin. Biotechnol. 2013, 24:880-886.
2. Turner N.J., Badylak S.F. Regeneration of skeletal muscle. Cell Tissue Res. 2012, 347:759-774.
3. Jarvinen T.A.H.J., Jarvinen T.L.N., Kaariainen M., Kalimo A., Jarvinen M. Muscle injuries - biology and treatment. Am. J. Sports Med. 2005, 33:745-764.
4. Rossi C.A., Pozzobon M., De Coppi P. Advances in musculoskeletal tissue engineering moving towards therapy. Organogenesis 2010, 6:167-172.
5. Tedesco F.S., Cossu G. Stem cell therapies for muscle disorders. Curr. Opin. Neurol. 2012, 25:597-603.
6. Palmieri B., Tremblay J.P., Daniele L. Past, present and future of myoblast transplantation in the treatment of Duchenne muscular dystrophy. Pediatr. Transplant. 2010, 14:813-819.
7. McCullagh K.J., Perlingeiro R.C. Coaxing stem cells for skeletal muscle repair. Adv. Drug Deliv. Rev. 2014, (in press). 10.1016/j.addr.2014.07.007.
8. Dhawan J., Rando T.A. Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol. 2005, 15:666-673.
9. Ciciliot S., Schiaffino S. Regeneration of mammalian skeletal muscle: basic mechanisms and clinical implications. Curr. Pharm. Des. 2010, 16:906-914.
10. Wagers A.J., Conboy I.M. Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell 2005, 122:659-667.
11. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 1961, 9:493-495.
12. Murphy M.M., Lawson J.A., Mathew S.J., Hutcheson D.A., Kardon G. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 2011, 138:3625-3637.
13. Lepper C., Partridge T.A., Fan C.M. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 2011, 138:3639-3646.
14. Sambasivan R., Yao R., Kissenpfennig A., Van Wittenberghe L., Paldi A., Gayraud-Morel B., Guenou H., Malissen B., Tajbakhsh S., Galy A. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 2011, 138:3647-3656.
15. von Maltzahn J., Jones A.E., Parks R.J., Rudnicki M.A. Pax7 is critical for the normal function of satellite cells in adult skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:16474-16479.
16. Cerletti M., Jurga S., Witczak C.A., Hirshman M.F., Shadrach J.L., Goodyear L.J., Wagers A.J. Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 2008, 134:37-47.
17. Kuang S.H., Kuroda K., Le Grand F., Rudnicki M.A. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 2007, 129:999-1010.
18. Montarras D., Morgan J., Collins C., Relaix F., Zaffran S., Cumano A., Partridge T., Buckingham M. Direct isolation of satellite cells for skeletal muscle regeneration. Science 2005, 309:2064-2067.
19. Sacco A., Doyonnas R., Kraft P., Vitorovic S., Blau H.M. Self-renewal and expansion of single transplanted muscle stem cells. Nature 2008, 456:502-506.
20. Relaix F., Montarras D., Zaffran S., Gayraud-Morel B., Rocancourt D., Tajbakhsh S., Mansouri A., Cumano A., Buckingham M. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 2006, 172:91-102.
21. Rocheteau P., Gayraud-Morel B., Siegl-Cachedenier I., Blasco M.A., Tajbakhsh S. A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 2012, 148:112-125.
22. Day K., Paterson B., Yablonka-Reuveni Z. A distinct profile of myogenic regulatory factor detection within Pax7+ cells at S phase supports a unique role of Myf5 during posthatch chicken myogenesis. Dev. Dyn. 2009, 238:1001-1009.
23. Brack A.S., Rando T.A. Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell 2012, 10:504-514.
24. Biressi S., Rando T.A. Heterogeneity in the muscle satellite cell population. Semin. Cell Dev. Biol. 2010, 21:845-854.
25. Collins C.A., Olsen I., Zammit P.S., Heslop L., Petrie A., Partridge T.A., Morgan J.E. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 2005, 122:289-301.
26. Zammit P.S. All muscle satellite cells are equal, but are some more equal than others?. J. Cell Sci. 2008, 121:2975-2982.
27. Kuang S., Gillespie M.A., Rudnicki M.A. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2008, 2:22-31.
28. Cossu G., Tajbakhsh S. Oriented cell divisions and muscle satellite cell heterogeneity. Cell 2007, 129:859-861.
29. Ferrari G., Cusella-De Angelis G., Coletta M., Paolucci E., Stornaiuolo A., Cossu G., Mavilio F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998, 279:1528-1530.
30. Dellavalle A., Sampaolesi M., Tonlorenzi R., Tagliafico E., Sacchetti B., Perani L., Innocenzi A., Galvez B.G., Messina G., Morosetti R., Li S., Belicchi M., Peretti G., Chamberlain J.S., Wright W.E., Torrente Y., Ferrari S., Bianco P., Cossu G. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat. Cell Biol. 2007, 9:255-267.
31. Dellavalle A., Maroli G., Covarello D., Azzoni E., Innocenzi A., Perani L., Antonini S., Sambasivan R., Brunelli S., Tajbakhsh S., Cossu G. Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat. Commun. 2011, 2:499.
32. Sampaolesi M., Blot S., D'Antona G., Granger N., Tonlorenzi R., Innocenzi A., Mognol P., Thibaud J.L., Galvez B.G., Barthelemy I., Perani L., Mantero S., Guttinger M., Pansarasa O., Rinaldi C., Cusella De Angelis M.G., Torrente Y., Bordignon C., Bottinelli R., Cossu G. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 2006, 444:574-579.
33. Mitchell K.J., Pannerec A., Cadot B., Parlakian A., Besson V., Gomes E.R., Marazzi G., Sassoon D.A. Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat. Cell Biol. 2010, 12:257-U256.
34. Tidball J.G., Villalta S.A. Regulatory interactions between muscle and the immune system during muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R1173-R1187.
35. Nguyen H.X., Lusis A.J., Tidball J.G. Null mutation of myeloperoxidase in mice prevents mechanical activation of neutrophil lysis of muscle cell membranes in vitro and in vivo. J. Physiol. 2005, 565:403-413.
36. Saclier M., Yacoub-Youssef H., Mackey A.L., Arnold L., Ardjoune H., Magnan M., Sailhan F., Chelly J., Pavlath G.K., Mounier R., Kjaer M., Chazaud B. Differentially activated macrophages orchestrate myogenic precursor cell fate during human skeletal muscle regeneration. Stem Cells 2013, 31:384-396.
37. Mounier R., Theret M., Arnold L., Cuvellier S., Bultot L., Goransson O., Sanz N., Ferry A., Sakamoto K., Foretz M., Viollet B., Chazaud B. AMPK alpha 1 regulates macrophage skewing at the time of resolution of inflammation during skeletal muscle regeneration. Cell Metab. 2013, 18:251-264.
38. Arnold L., Henry A., Poron F., Baba-Amer Y., van Rooijen N., Plonquet A., Gherardi R.K., Chazaud B. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 2007, 204:1057-1069.
39. Chazaud B., Brigitte M., Yacoub-Youssef H., Arnold L., Gherardi R., Sonnet C., Lafuste P., Chretien F. Dual and beneficial roles of macrophages during skeletal muscle regeneration. Exerc. Sport Sci. Rev. 2009, 37:18-22.
40. Ten Broek R.W., Grefte S., Von den Hoff J.W. Regulatory factors and cell populations involved in skeletal muscle regeneration. J. Cell. Physiol. 2010, 224:7-16.
41. Yin H., Price F., Rudnicki M.A. Satellite cells and the muscle stem cell niche. Physiol. Rev. 2013, 93:23-67.
42. Slater C.R., Schiaffino S. Innervation of regenerating muscle. Skeletal muscle repair and regeneration 2008, 303-334. Springer. S. Schiaffino, T. Partridge (Eds.).
43. Kaariainen M., Jarvinen T., Jarvinen M., Rantanen J., Kalimo H. Relation between myofibers and connective tissue during muscle injury repair. Scand. J. Med. Sci. Sports 2000, 10:332-337.
44. Laschke M.W., Harder Y., Amon M., Martin I., Farhadi J., Ring A., Torio-Padron N., Schramm R., Rucker M., Junker D., Haufel J.M., Carvalho C., Heberer M., Germann G., Vollmar B., Menger M.D. Angiogenesis in tissue engineering: breathing life into constructed tissue substitutes. Tissue Eng. 2006, 12:2093-2104.
45. Smythe G.M., Hodgetts S.I., Grounds M.D. Problems and solutions in myoblast transfer therapy. J. Cell. Mol. Med. 2001, 5:33-47.
46. Gilbert P.M., Havenstrite K.L., Magnusson K.E., Sacco A., Leonardi N.A., Kraft P., Nguyen N.K., Thrun S., Lutolf M.P., Blau H.M. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 2010, 329:1078-1081.
47. Parker M.H., Loretz C., Tyler A.E., Duddy W.J., Hall J.K., Olwin B.B., Bernstein I.D., Storb R., Tapscott S.J. Activation of Notch signaling during ex vivo expansion maintains donor muscle cell engraftment. Stem Cells 2012, 30:2212-2220.
48. Hall J.K., Banks G.B., Chamberlain J.S., Olwin B.B. Prevention of muscle aging by myofiber-associated satellite cell transplantation. Sci. Transl. Med. 2010, 2:57-83.
49. Cosgrove B.D., Gilbert P.M., Porpiglia E., Mourkioti F., Lee S.P., Corbel S.Y., Llewellyn M.E., Delp S.L., Blau H.M. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat. Med. 2014, 20:255-264.
50. Boonen K.J., Post M.J. The muscle stem cell niche: regulation of satellite cells during regeneration. Tissue Eng. B 2008, 14:419-431.
51. Frisch S.M., Ruoslahti E. Integrins and anoikis. Curr. Opin. Cell Biol. 1997, 9:701-706.
52. Bouchentouf M., Benabdallah B.F., Rousseau J., Schwartz L.M., Tremblay J.P. Induction of anoikis following myoblast transplantation into SCID mouse muscles requires the Bit1 and FADD pathways. Am. J. Transplant. 2007, 7:1491-1505.
53. Rowley J.A., Madlambayan G., Mooney D.J. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 1999, 20:45-53.
54. Salimath A.S., Garcia A.J. Biofunctional hydrogels for skeletal muscle constructs. J. Tissue Eng Regen. Med. 2014, (in press). 10.1002/term.1881.
55. Rowley J.A., Mooney D.J. Alginate type and RGD density control myoblast phenotype. J. Biomed. Mater. Res. 2002, 60:217-223.
56. Boontheekul T., Kong H.J., Hsiong S.X., Huang Y.C., Mahadevan L., Vandenburgh H., Mooney D.J. Quantifying the relation between bond number and myoblast proliferation. Faraday Discuss. 2008, 139:53-70.
57. Borselli C., Cezar C.A., Shvartsman D., Vandenburgh H.H., Mooney D.J. The role of multifunctional delivery scaffold in the ability of cultured myoblasts to promote muscle regeneration. Biomaterials 2011, 32:8905-8914.
58. Urciuolo A., Quarta M., Morbidoni V., Gattazzo F., Molon S., Grumati P., Montemurro F., Tedesco F.S., Blaauw B., Cossu G., Vozzi G., Rando T.A., Bonaldo P. Collagen VI regulates satellite cell self-renewal and muscle regeneration. Nat. Commun. 2013, 4.
59. Fishman J.M., Lowdell M.W., Urbani L., Ansari T., Burns A.J., Turmaine M., North J., Sibbons P., Seifalian A.M., Wood K.J., Birchall M.A., De Coppi P. Immunomodulatory effect of a decellularized skeletal muscle scaffold in a discordant xenotransplantation model. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:14360-14365.
60. Sicari B.M., Rubin J.P., Dearth C.L., Wolf M.T., Ambrosio F., Boninger M., Turner N.J., Weber D.J., Simpson T.W., Wyse A., Brown E.H., Dziki J.L., Fisher L.E., Brown S., Badylak S.F. An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss. Sci. Transl. Med. 2014, 6:234-258.
61. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
62. Boontheekul T., Hill E.E., Kong H.J., Mooney D.J. Regulating myoblast phenotype through controlled gel stiffness and degradation. Tissue Eng. 2007, 13:1431-1442.
63. Engler A.J., Griffin M.A., Sen S., Bonnemann C.G., Sweeney H.L., Discher D.E. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 2004, 166:877-887.
64. Swift J., Ivanovska I.L., Buxboim A., Harada T., Dingal P.C., Pinter J., Pajerowski J.D., Spinler K.R., Shin J.W., Tewari M., Rehfeldt F., Speicher D.W., Discher D.E. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 2013, 341:1240104.
65. Guilak F., Cohen D.M., Estes B.T., Gimble J.M., Liedtke W., Chen C.S. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009, 5:17-26.
66. Kaully T., Kaufman-Francis K., Lesman A., Levenberg S. Vascularization - the conduit to viable engineered tissues. Tissue Eng. B Rev. 2009, 15:159-169.
67. Ikada Y. Challenges in tissue engineering. J. R. Soc. Interface 2006, 3:589-601.
68. Hill E., Boontheekul T., Mooney D.J. Designing scaffolds to enhance transplanted myoblast survival and migration. Tissue Eng. 2006, 12:1295-1304.
69. Serrano A.L., Munoz-Canoves P. Regulation and dysregulation of fibrosis in skeletal muscle. Exp. Cell Res. 2010, 316:3050-3058.
70. Huang N.F., Lee R.J., Li S. Engineering of aligned skeletal muscle by micropatterning. Am. J. Transl. Res. 2010, 2:43-55.
71. Page R.L., Malcuit C., Vilner L., Vojtic I., Shaw S., Hedblom E., Hu J., Pins G.D., Rolle M.W., Dominko T. Restoration of skeletal muscle defects with adult human cells delivered on fibrin microthreads. Tissue Eng. A 2011, 17:2629-2640.
72. Borselli C., Storrie H., Benesch-Lee F., Shvartsman D., Cezar C., Lichtman J.W., Vandenburgh H.H., Mooney D.J. Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3287-3292.
73. Hammers D.W., Sarathy A., Pham C.B., Drinnan C.T., Farrar R.P., Suggs L.J. Controlled release of IGF-I from a biodegradable matrix improves functional recovery of skeletal muscle from ischemia/reperfusion. Biotechnol. Bioeng. 2012, 109:1051-1059.
74. Webster M.T., Fan C.M. c-MET regulates myoblast motility and myocyte fusion during adult skeletal muscle regeneration. PLoS One 2013, 8.
75. Sisson T.H., Nguyen M.H., Yu B., Novak M.L., Simon R.H., Koh T.J. Urokinase-type plasminogen activator increases hepatocyte growth factor activity required for skeletal muscle regeneration. Blood 2009, 114:5052-5061.
76. Shansky J., Creswick B., Lee P., Wang X., Vandenburgh H. Paracrine release of insulin-like growth factor 1 from a bioengineered tissue stimulates skeletal muscle growth in vitro. Tissue Eng. 2006, 12:1833-1841.
77. Pelosi L., Giacinti C., Nardis C., Borsellino G., Rizzuto E., Nicoletti C., Wannenes F., Battistini L., Rosenthal N., Molinaro M., Musaro A. Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. FASEB J. 2007, 21:1393-1402.
78. Silva E.A., Mooney D.J. Spatiotemporal control of vascular endothelial growth factor delivery from injectable hydrogels enhances angiogenesis. J. Thromb. Haemost. 2007, 5:590-598.
79. Sheehan S.M., Allen R.E. Skeletal muscle satellite cell proliferation in response to members of the fibroblast growth factor family and hepatocyte growth factor. J. Cell. Physiol. 1999, 181:499-506.
80. Conboy I.M., Conboy M.J., Smythe G.M., Rando T.A. Notch-mediated restoration of regenerative potential to aged muscle. Science 2003, 302:1575-1577.
81. Conboy I.M., Rando T.A. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 2002, 3:397-409.
82. Le Grand F., Jones A.E., Seale V., Scime A., Rudnicki M.A. Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 2009, 4:535-547.
83. Bentzinger C.F., Wang Y.X., von Maltzahn J., Soleimani V.D., Yin H., Rudnicki M.A. Fibronectin regulates Wnt7a signaling and satellite cell expansion. Cell Stem Cell 2013, 12:75-87.
84. Hill E., Boontheekul T., Mooney D.J. Regulating activation of transplanted cells controls tissue regeneration. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2494-2499.
85. Gates C., Huard J. Management of skeletal muscle injuries in military personnel. Oper. Technol. Sport Med. 2005, 13:247-256.
86. Wang L., Cao L., Shansky J., Wang Z., Mooney D., Vandenburgh H. Minimally invasive approach to the repair of injured skeletal muscle with a shape-memory scaffold. Mol. Ther. 2014, 22:1441-1449.
87. Wang L., Shansky J., Borselli C., Mooney D., Vandenburgh H. Design and fabrication of a biodegradable, covalently crosslinked shape-memory alginate scaffold for cell and growth factor delivery. Tissue Eng A 2012, 18:2000-2007.
88. Dennis R.G., Kosnik P.E. Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cell. Dev. Biol. Anim. 2000, 36:327-335.
89. Shansky J., Del Tatto M., Chromiak J., Vandenburgh H. A simplified method for tissue engineering skeletal muscle organoids in vitro. In Vitro Cell. Dev. Biol. Anim. 1997, 33:659-661.
90. Vandenburgh H., Shansky J., Benesch-Lee F., Barbata V., Reid J., Thorrez L., Valentini R., Crawford G. Drug-screening platform based on the contractility of tissue-engineered muscle. Muscle Nerve 2008, 37:438-447.
91. Lu Y., Shansky J., Del Tatto M., Ferland P., Wang X., Vandenburgh H. Recombinant vascular endothelial growth factor secreted from tissue-engineered bioartificial muscles promotes localized angiogenesis. Circulation 2001, 104:594-599.
92. 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. 1999, 10:565-577.
93. Wang L., Shansky J., Vandenburgh H. Induced formation and maturation of acetylcholine receptor clusters in a defined 3D bio-artificial muscle. Mol. Neurobiol. 2013, 48:397-403.
94. Neal D., Sakar M.S., Ong L.L., Harry Asada H. Formation of elongated fascicle-inspired 3D tissues consisting of high-density, aligned cells using sacrificial outer molding. Lab Chip 2014, 14:1907-1916.
95. Bian W., Bursac N. Engineered skeletal muscle tissue networks with controllable architecture. Biomaterials 2009, 30:1401-1412.
96. Bian W., Liau B., Badie N., Bursac N. Mesoscopic hydrogel molding to control the 3D geometry of bioartificial muscle tissues. Nat. Protoc. 2009, 4:1522-1534.
97. Juhas M., Engelmayr G.C., Fontanella A.N., Palmer G.M., Bursac N. Biomimetic engineered muscle with capacity for vascular integration and functional maturation in vivo. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:5508-5513.
98. Colton C.K. Implantable biohybrid artificial organs. Cell Transplant. 1995, 4:415-436.
99. Koffler J., Kaufman-Francis K., Shandalov Y., Egozi D., Pavlov D.A., Landesberg A., Levenberg S. Improved vascular organization enhances functional integration of engineered skeletal muscle grafts. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14789-14794.
100. Shandalov Y., Egozi D., Koffler J., Dado-Rosenfeld D., Ben-Shimol D., Freiman A., Shor E., Kabala A., Levenberg S. An engineered muscle flap for reconstruction of large soft tissue defects. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:6010-6015.
101. Borisov A.B., Dedkov E.I., Carlson B.M. Interrelations of myogenic response, progressive atrophy of muscle fibers, and cell death in denervated skeletal muscle. Anat. Rec. 2001, 264:203-218.
102. Mendler L., Pinter S., Kiricsi M., Baka Z., Dux L. Regeneration of reinnervated rat soleus muscle is accompanied by fiber transition toward a faster phenotype. J. Histochem. Cytochem. 2008, 56:111-123.
103. Shvartsman D., Storrie-White H., Lee K., Kearney C., Brudno Y., Ho N., Cezar C., McCann C., Anderson E., Koullias J., Tapia J.C., Vandenburgh H., Lichtman J.W., Mooney D.J. Sustained delivery of VEGF maintains innervation and promotes reperfusion in ischemic skeletal muscles via NGF/GDNF signaling. Mol. Ther. 2014, 22:1243-1253.
104. Miller K.J., Thaloor D., Matteson S., Pavlath G.K. Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. Am. J. Physiol. Cell Physiol. 2000, 278:C174-C181.
105. Lesault P.F., Theret M., Magnan M., Cuvellier S., Niu Y., Gherardi R.K., Tremblay J.P., Hittinger L., Chazaud B. Macrophages improve survival, proliferation and migration of engrafted myogenic precursor cells into MDX skeletal muscle. PLoS One 2012, 7:e46698.
106. Bencze M., Negroni E., Vallese D., Yacoub-Youssef H., Chaouch S., Wolff A., Aamiri A., Di Santo J.P., Chazaud B., Butler-Browne G., Savino W., Mouly V., Riederer I. Proinflammatory macrophages enhance the regenerative capacity of human myoblasts by modifying their kinetics of proliferation and differentiation. Mol. Ther. 2012, 20:2168-2179.
107. Ota S., Uehara K., Nozaki M., Kobayashi T., Terada S., Tobita K., Fu F.H., Huard J. Intramuscular transplantation of muscle-derived stem cells accelerates skeletal muscle healing after contusion injury via enhancement of angiogenesis. Am. J. Sports Med. 2011, 39:1912-1922.
108. Li R.K., Mickle D.A., Weisel R.D., Rao V., Jia Z.Q. Optimal time for cardiomyocyte transplantation to maximize myocardial function after left ventricular injury. Ann. Thorac. Surg. 2001, 72:1957-1963.
109. Lin S., Xu L., Hu S., Zhang C., Wang Y., Xu J. Optimal time-point for neural stem cell transplantation to delay denervated skeletal muscle atrophy. Muscle Nerve 2013, 47:194-201.
110. Zhao X., Kim J., Cezar C.A., Huebsch N., Lee K., Bouhadir K., Mooney D.J. Active scaffolds for on-demand drug and cell delivery. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:67-72.
111. Cezar C.A., Kennedy S., Mehta M., Weaver J.C., Gu L., Vandenburgh H., Mooney D. Biphasic ferrogels for triggered drug and cell delivery. Adv. Healthc. Mater. 2014, (in press). 10.1002/adhm.201400095.
112. Ali O.A., Huebsch N., Cao L., Dranoff G., Mooney D.J. Infection-mimicking materials to program dendritic cells in situ. Nat. Mater. 2009, 8:151-158.
113. Ali O.A., Emerich D., Dranoff G., Mooney D.J. In situ regulation of DC subsets and T cells mediates tumor regression in mice. Sci. Transl. Med. 2009, 1:8-19.
114. Kin S., Hagiwara A., Nakase Y., Kuriu Y., Nakashima S., Yoshikawa T., Sakakura C., Otsuji E., Nakamura T., Yamagishi H. Regeneration of skeletal muscle using in situ tissue engineering on an acellular collagen sponge scaffold in a rabbit model. ASAIO J. 2007, 53:506-513.
115. Kroehne V., Heschel I., Schugner F., Lasrich D., Bartsch J.W., Jockusch H. Use of a novel collagen matrix with oriented pore structure for muscle cell differentiation in cell culture and in grafts. J. Cell. Mol. Med. 2008, 12:1640-1648.
116. Levy-Mishali M., Zoldan J., Levenberg S. Effect of scaffold stiffness on myoblast differentiation. Tissue Eng. A 2009, 15:935-944.