Engineered skeletal muscle tissue for soft robotics: Fabrication strategies, current applications, and future challenges

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 6, Issue 2, 2014, Pages 178-195

  Duffy, Rebecca M ^a   Feinberg, Adam W ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR MICROENVIRONMENT; FABRICATION STRATEGIES; FUNCTIONAL INTEGRATION; MECHANICAL AND ELECTRICAL; MECHANICAL ENVIRONMENT; MUSCLE PRECURSOR CELLS; REGENERATIVE MEDICINE; SPATIAL ORGANIZATION;

ACTUATORS; MEDICAL APPLICATIONS; ROBOTICS; SCAFFOLDS (BIOLOGY);

MUSCLE;

TISSUE SCAFFOLD;

ARTICLE; BIOREACTOR; CELL ADHESION; ELECTROSTIMULATION; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; MECHANICAL STRESS; MICROENVIRONMENT; MUSCLE BLOOD VESSEL; MUSCLE INNERVATION; MYOBLAST; MYOTUBE; PRIORITY JOURNAL; RIGIDITY; ROBOTICS; SKELETAL MUSCLE; SWIMMING; TISSUE DIFFERENTIATION; TISSUE ENGINEERING; WALKING; YOUNG MODULUS;

ANIMALS; BIOREACTORS; CELL LINE; CELLULAR MICROENVIRONMENT; HUMANS; MICE; MUSCLE, SKELETAL; ROBOTICS; TISSUE ENGINEERING;

EID: 84893798091     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.1254     Document Type: Article

References (99)

1. Van Ham R, Sugar TG, Vanderborght B, Hollander KW, Lefeber D. Compliant actuator designs review of actuators with passive adjustable compliance/controllable stiffness for robotic applications. IEEE Rob Autom Mag 2009, 16:81-94.
2. Pette D, Vrbová G. Invited review: neural control of phenotypic expression in mammalian muscle fibers. Muscle Nerve 1985, 8:676-689.
3. Trivedi DRC, Kier WK, Walker ID. Soft robotics: biological inspiration, state of the art, and future research. Appl Bionics Biomech 2008, 5:99-117.
4. Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev 2004, 84:209-238.
5. Rudnicki MA, Schnegelsberg PNJ, Stead RH, Braun T, Arnold HH, Jaenisch R. Myod or Myf-5 is required for the formation of skeletal-muscle. Cell 1993, 75:1351-1359.
6. Sanger JW, Wang JS, Fan YL, White J, Sanger JM. Assembly and dynamics of myofibrils. J Biomed Biotechnol 2010, 2010:1-8.
7. Turner NJ, Badylak SF. Regeneration of skeletal muscle. Cell Tissue Res 2012, 347:759-774.
8. Juhas M, Bursac N. Engineering skeletal muscle repair. Curr Opin Biotechnol 2013, 24:1-7.
9. Ghaemmaghami AM, Hancock MJ, Harrington H, Kaji H, Khademhosseini A. Biomimetic tissues on a chip for drug discovery. Drug Discov Today 2012, 17:173-181.
10. Collinsworth AM, Zhang S, Kraus WE, Truskey GA. Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am J Physiol Cell Physiol 2002, 283:C1219-C1227.
11. Madden JDW, Vandesteeg NA, Anquetil PA, Madden PGA, Takshi A, Pytel RZ, Lafontaine SR, Wieringa PA, Hunter IW. Artificial muscle technology: physical principles and naval prospects. IEEE J Ocean Eng 2004, 29:706-728.
12. Griffin MA, Sen S, Sweeney HL, Discher DE. Adhesion-contractile balance in myocyte differentiation. J Cell Sci 2004, 117:5855-5863.
13. Engler AJ, Griffin MA, Sen S, Bonnemann CG, Sweeney HL, Discher DE. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 2004, 166:877-887.
14. Palchesko RN, Zhang L, Sun Y, Feinberg AW. Development of polydimethylsiloxane substrates with tunable elastic modulus to study cell mechanobiology in muscle and nerve. PLoS One 2012, 7(12):e51499.
15. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
16. Bian W, Bursac N. Engineered skeletal muscle tissue networks with controllable architecture. Biomaterials 2009, 30:1401-1412.
17. Hinds S, Bian W, Dennis RG, Bursac N. The role of extracellular matrix composition in structure and function of bioengineered skeletal muscle. Biomaterials 2011, 32:3575-3583.
18. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE. Micropatterned surfaces for control of cell shape, position, and function. Biotechnol Prog 1998, 14:356-363.
19. Williams C, Tsuda Y, Isenberg BC, Yamato M, Shimizu T, Okano T, Wong JY. Aligned cell sheets grown on thermo-responsive substrates with microcontact printed protein patterns. Adv Mater 2009, 21:2161-2164.
20. Grosberg A, Nesmith AP, Goss JA, Brigham MD, McCain ML, Parker KK. Muscle on a chip: in vitro contractility assays for smooth and striated muscle. J Pharmacol Toxicol Methods 2012, 65:126-135.
21. Feinberg AW, Feigel A, Shevkoplyas SS, Sheehy S, Whitesides GM, Parker KK. Muscular thin films for building actuators and powering devices. Science 2007, 317:1366-1370.
22. Grosberg A, Alford PW, McCain ML, Parker KK. Ensembles of engineered cardiac tissues for physiological and pharmacological study: heart on a chip. Lab Chip 2011, 11:4165-4173.
23. Zatti S, Zoso A, Serena E, Luni C, Cimetta E, Elvassore N. Micropatterning topology on soft substrates affects myoblast proliferation and differentiation. Langmuir 2012, 28:2718-2726.
24. Altomare L, Riehle M, Gadegaard N, Tanzi MC, Fare S. Microcontact printing of fibronectin on a biodegradable polymeric surface for skeletal muscle cell orientation. Int J Artif Organs 2010, 33:535-543.
25. Sun Y, Duffy R, Lee A, Feinberg AW. Optimizing the structure and contractility of engineered skeletal muscle thin films. Acta Biomater 2013, 9:7885-7894.
26. Curtis A, Wilkinson C. Review: topographical control of cells. Biomaterials 1997, 18:1573-1583.
27. Flaibani M, Boldrin L, Cimetta E, Piccoli M, De Coppi P, Elvassore N. Muscle differentiation and myotubes alignment is influenced by micropatterned surfaces and exogenous electrical stimulation. Tissue Eng Part A 2009, 15:2447-2457.
28. Zhao Y, Zeng HS, Nam J, Agarwal S. Fabrication of skeletal muscle constructs by topographic activation of cell alignment. Biotechnol Bioeng 2009, 102:624-631.
29. Gingras J, Rioux RM, Cuvelier D, Geisse NA, Lichtman JW, Whitesides GM, Mahadevan L, Sanes JR. Controlling the orientation and synaptic differentiation of myotubes with micropatterned substrates. Biophys J 2009, 97:2771-2779.
30. Wang PY, Yu HT, Tsai WB. Modulation of alignment and differentiation of skeletal myoblasts by submicron ridges/grooves surface structure. Biotechnol Bioeng 2010, 106:285-294.
31. Hosseini V, Ahadian S, Ostrovidov S, Camci-Unal G, Chen S, Kaji H, Ramalingam M, Khademhosseini A. Engineered contractile skeletal muscle tissue on a microgrooved methacrylated gelatin substrate. Tissue Eng Part A 2012, 18:2453-2465.
32. Neumann T, Hauschka SD, Sanders JE. Tissue engineering of skeletal muscle using polymer fiber arrays. Tissue Eng 2003, 9:995-1003.
33. Ku SH, Lee SH, Park CB. Synergic effects of nanofiber alignment and electroactivity on myoblast differentiation. Biomaterials 2012, 33:6098-6104.
34. Ker ED, Nain AS, Weiss LE, Wang J, Suhan J, Amon CH, Campbell PG. Bioprinting of growth factors onto aligned sub-micron fibrous scaffolds for simultaneous control of cell differentiation and alignment. Biomaterials 2011, 32:8097-8107.
35. Yamasaki K, Hayashi H, Nishiyama K, Kobayashi H, Uto S, Kondo H, Hashimoto S, Fujisato T. Control of myotube contraction using electrical pulse stimulation for bio-actuator. J Artif Organs 2009, 12:131-137.
36. Donnelly K, Khodabukus A, Philp A, Deldicque L, Dennis RG, Baar K. A novel bioreactor for stimulating skeletal muscle in vitro. Tissue Eng Part C Methods 2010, 16:711-718.
37. Ahadian S, Ramón-Azcón J, Ostrovidov S, Camci-Unal G, Hosseini V, Kaji H, Ino K, Shiku H, Khademhosseini A, Matsue T. Interdigitated array of Pt electrodes for electrical stimulation and engineering of aligned muscle tissue. Lab Chip 2012, 12:3491-3503. doi: 10.1039/C2LC40479F.
38. Nagamine K, Kawashima T, Sekine S, Ido Y, Kanzaki M, Nishizawa M. Spatiotemporally controlled contraction of micropatterned skeletal muscle cells on a hydrogel sheet. Lab Chip 2011, 11:513-517.
39. Ahadian S, Ostrovidov S, Hosseini V, Kaji H, Ramalingam M, Bae H, Khademhosseini A. Electrical stimulation as a biomimicry tool for regulating muscle cell behavior. Organogenesis 2013, 9:87-92.
40. Fujita H, Nedachi T, Kanzaki M. Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes. Exp Cell Res 2007, 313:1853-1865.
41. Fujita H, Shimizu K, Nagamori E. Novel method for measuring active tension generation by C2C12 myotube using UV-crosslinked collagen film. Biotechnol Bioeng 2010, 106:482-489.
42. Edman KAP. Contractile properties of mouse single muscle fibers, a comparison with amphibian muscle fibers. J Exp Biol 2005, 208:1905-1913.
43. Ahadian S, Ramon-Azcon J, Ostrovidov S, Camci-Unal G, Kaji H, Ino K, Shiku H, Khademhosseini A, Matsue T. A contactless electrical stimulator: application to fabricate functional skeletal muscle tissue. Biomed Microdevices 2013, 15:109-115.
44. Dvir T, Timko BP, Brigham MD, Naik SR, Karajanagi SS, Levy O, Jin HW, Parker KK, Langer R, Kohane DS. Nanowired three-dimensional cardiac patches. Nat Nanotechnol 2011, 6:720-725.
45. Martinelli V, Cellot G, Toma FM, Long CS, Caldwell JH, Zentilin L, Giacca M, Turco A, Prato M, Ballerini L, et al. Carbon nanotubes instruct physiological growth and functionally mature syncytia: nongenetic engineering of cardiac myocytes. ACS Nano 2013, 7:5746-5756.
46. Fleischer S, Dvir T. Tissue engineering on the nanoscale: lessons from the heart. Curr Opin Biotechnol 2013, 24:664-671.
47. Ramon-Azcon J, Ahadian S, Estili M, Liang X, Ostrovidov S, Kaji H, Shiku H, Ramalingam M, Nakajima K, Sakka Y, et al. Dielectrophoretically aligned carbon nanotubes to control electrical and mechanical properties of hydrogels to fabricate contractile muscle myofibers. Adv Mater 2013, 25:4028-4034.
48. Edman KA, Elzinga G, Noble MI. Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. J Physiol 1978, 281:139-155.
49. Powell CA, Smiley BL, Mills J, Vandenburgh HH. Mechanical stimulation improves tissue-engineered human skeletal muscle. Am J Physiol Cell Physiol 2002, 283:C1557-C1565.
50. Cannizzaro C, Tandon N, Figallo E, Park H, Gerecht S, Radisic M, Elvassore N, Vunjak-Novakovic G. Practical aspects of cardiac tissue engineering with electrical stimulation. In: Hauser H, Fussenegger M, eds. Tissue Engineering, vol. 140. Totowa, New Jersey: Humana Press; 2007, 291-307.
51. Das M, Gregory CA, Molnar P, Riedel LM, Wilson K, Hickman JJ. A defined system to allow skeletal muscle differentiation and subsequent integration with silicon microstructures. Biomaterials 2006, 27:4374-4380.
52. Wilson K, Molnar P, Hickman J. Integration of functional myotubes with a Bio-MEMS device for non-invasive interrogation. Lab Chip 2007, 7:920-922.
53. Das M, Wilson K, Molnar P, Hickman JJ. Differentiation of skeletal muscle and integration of myotubes with silicon microstructures using serum-free medium and a synthetic silane substrate. Nat Protoc 2007, 2:1795-1801.
54. Wilson K, Das M, Wahl KJ, Colton RJ, Hickman J. Measurement of contractile stress generated by cultured rat muscle on silicon cantilevers for toxin detection and muscle performance enhancement. PLoS One 2010, 5(6): e11042.
55. Alford PW, Feinberg AW, Sheehy SP, Parker KK. Biohybrid thin films for measuring contractility in engineered cardiovascular muscle. Biomaterials 2011, 31:3613-3621.
56. Vandenburgh HH, Karlisch P, Farr L. Maintenance of highly contractile tissue-cultured avian skeletal myotubes in collagen gel. In Vitro Cell Dev Biol 1988, 24:166-174.
57. Rhim C, Lowell DA, Reedy MC, Slentz DH, Zhang SJ, Kraus WE, Truskey GA. Morphology and ultrastructure of differentiating three-dimensional mammalian skeletal muscle in a collagen gel. Muscle Nerve 2007, 36:71-80.
58. 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.
59. Dennis RG, Kosnik PE 2nd. Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cell Dev Biol Anim 2000, 36:327-335.
60. Haraguchi Y, Shimizu T, Sasagawa T, Sekine H, Sakaguchi K, Kikuchi T, Sekine W, Sekiya S, Yamato M, Umezu M, et al. Fabrication of functional three-dimensional tissues by stacking cell sheets in vitro. Nat Protoc 2012, 7:850-858.
61. Yamamoto Y, Ito A, Kato M, Kawabe Y, Shimizu K, Fujita H, Nagamori E, Kamihira M. Preparation of artificial skeletal muscle tissues by a magnetic force-based tissue engineering technique. J Biosci Bioeng 2009, 108:538-543.
62. Vandenburgh H, Shansky J, Benesch-Lee F, Skelly K, Spinazzola J, Saponjian Y, Tseng BS. Automated drug screening with contractile muscle tissue engineered from dystrophic myoblasts. Neuromuscul Disord 2009, 19:614-614.
63. Rhim C, Cheng CS, Kraus WE, Truskey GA. Effect of microRNA modulation on bioartificial muscle function. Tissue Eng Part A 2010, 16:3589-3597.
64. Vandenburgh H, DelTatto M, Shansky J, Lemaire J, Chang A, Payumo F, Lee P, Goodyear A, Raven L. Tissue-engineered skeletal muscle organoids for reversible gene therapy. Hum Gene Ther 1996, 7:2195-2200.
65. 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.
66. Dennis RG, Kosnik PE 2nd, Gilbert ME, Faulkner JA. Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. Am J Physiol Cell Physiol 2001, 280:C288-C295.
67. Dennis RG, Dow DE. Excitability of skeletal muscle during development, denervation, and tissue culture. Tissue Eng 2007, 13:2395-2404.
68. Huang YC, Dennis RG, Larkin L, Baar K. Rapid formation of functional muscle in vitro using fibrin gels. J Appl Physiol 2005, 98:706-713.
69. Larkin LM, Calve S, Kostrominova TY, Arruda EM. Structure and functional evaluation of tendon-skeletal muscle constructs engineered in vitro. Tissue Eng 2006, 12:3149-3158.
70. Akiyama Y, Kikuchi A, Yamato M, Okano T. Ultrathin poly(N-isopropylacrylamide) grafted layer on polystyrene surfaces for cell adhesion/detachment control. Langmuir 2004, 20:5506-5511.
71. Yamamoto Y, Ito A, Fujita H, Nagamori E, Kawabe Y, Kamihira M. Functional evaluation of artificial skeletal muscle tissue constructs fabricated by a magnetic force-based tissue engineering technique. Tissue Eng Part A 2011, 17:107-114.
72. Nawroth JC, Lee H, Feinberg AW, Ripplinger CM, McCain ML, Grosberg A, Dabiri JO, Parker KK. A tissue-engineered jellyfish with biomimetic propulsion. Nat Biotechnol 2012, 30:792-797.
73. Xi JZ, Schmidt JJ, Montemagno CD. Self-assembled microdevices driven by muscle. Nat Mater 2005, 4:180-U167.
74. Shimizu K, Sasaki H, Hida H, Fujita H, Obinata K, Shikida M, Nagamori E. Assembly of skeletal muscle cells on a Si-MEMS device and their generative force measurement. Biomed Microdevices 2010, 12:247-252.
75. Hoshino T, Morishima K. Muscle-powered cantilever for microtweezers with an artificial micro skeleton and rat primary myotubes. J Biomech Sci Eng 2010, 5:245-251.
76. Akiyama Y, Terada R, Hashimoto M, Hoshino T, Furukawa Y, Morishima K. Rod-shaped tissue engineered skeletal muscle with artificial anchors to utilize as a bio-actuator. J Biomech Sci Eng 2010, 5:236-244.
77. Kabumoto K, Hoshino T, Morishima K. Bio-robotics using interaction between neuron and muscle for development of living prosthesis. In: International Conference on Biomedical Robotics and Biomechatronics, The University of Tokyo, Tokyo, Japan, 2010.
78. Tanaka Y, Sato K, Shimizu T, Yamato M, Okano T, Kitamori T. A micro-spherical heart pump powered by cultured cardiomyocytes. Lab Chip 2007, 7:207-212.
79. Sakar MS, Neal D, Boudou T, Borochin MA, Li Y, Weiss R, Kamm RD, Chen CS, Asada HH. Formation and optogenetic control of engineered 3D skeletal muscle bioactuators. Lab Chip 2012, 12:4976-4985.
80. Pilarek M, Neubauer P, Marx U. Biological cardio-micro-pumps for microbioreactors and analytical micro-systems. Sens Actuat B Chem 2011, 156:517-526.
81. Herr H, Dennis RG. A swimming robot actuated by living muscle tissue. J Neuroeng Rehabil 2004, 1:6.
82. Kim J, Park J, Yang S, Baek J, Kim B, Lee SH, Yoon ES, Chun K, Park S. Establishment of a fabrication method for a long-term actuated hybrid cell robot. Lab Chip 2007, 7:1504-1508.
83. Chan V, Park K, Collens MB, Kong H, Saif TA, Bashir R. Development of miniaturized walking biological machines. Sci Rep 2012, 2:857.
84. Fujie T, Ahadian S, Liu H, Chang HX, Ostrovidov S, Wu HK, Bae H, Nakajima K, Kaji H, Khademhosseini A. Engineered nanomembranes for directing cellular organization toward flexible biodevices. Nano Lett 2013, 13:3185-3192.
85. Yaffe D, Saxel ORA. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 1977, 270:725-727.
86. Gilbert PM, Havenstrite KL, Magnusson KEG, Sacco A, Leonardi NA, Kraft P, Nguyen NK, Thrun S, Lutolf MP, Blau HM. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 2010, 329:1078-1081.
87. Salani S, Donadoni C, Rizzo F, Bresolin N, Comi GP, Corti S. Generation of skeletal muscle cells from embryonic and induced pluripotent stem cells as an in vitro model and for therapy of muscular dystrophies. J Cell Mol Med 2012, 16:1353-1364.
88. Bian W, Juhas M, Pfeiler TW, Bursac N. Local tissue geometry determines contractile force generation of engineered muscle networks. Tissue Eng Part A 2012, 18:957-967.
89. Baryshyan AL, Woods W, Trimmer BA, Kaplan DL. Isolation and maintenance-free culture of contractile myotubes from Manduca sexta embryos. PLoS One 2012, 7:e31598.
90. Sicari BM, Agrawal V, Siu BF, Medberry CJ, Dearth CL, Turner NJ, Badylak SF. A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng Part A 2012, 18:1941-1948.
91. Machingal MA, Corona BT, Walters TJ, Kesireddy V, Koval CN, Dannahower A, Zhao W, Yoo JJ, Christ GJ. A tissue-engineered muscle repair construct for functional restoration of an irrecoverable muscle injury in a murine model. Tissue Eng Part A 2011, 17:2291-2303.
92. Miller JS, Stevens KR, Yang MT, Baker BM, Nguyen D-HT, Cohen DM, Toro E, Chen AA, Galie PA, Yu X, et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 2012, 11:768-774.
93. Zheng Y, Chen J, Craven M, Choi NW, Totorica S, Diaz-Santana A, Kermani P, Hempstead B, Fischbach-Teschl C, López JA, et al. In vitro microvessels for the study of angiogenesis and thrombosis. Proc Natl Acad Sci 2012, 109:9342-9347.
94. Langhammer CG, Kutzing MK, Luo V, Zahn JD, Firestein BL. Skeletal myotube integration with planar microelectrode arrays in vitro for spatially selective recording and stimulation: a comparison of neuronal and myotube extracellular action potentials. Biotechnol Prog 2011, 27:891-895.
95. Langhammer CG, Kutzing MK, Luo V, Zahn JD, Firestein BL. A topographically modified substrate-embedded MEA for directed myotube formation at electrode contact sites. Ann Biomed Eng 2013, 41:408-420.
96. Tanaka Y, Sato K, Shimizu T, Yamato M, Okano T, Kitamori T. Biological cells on microchips: new technologies and applications. Biosens Bioelectron 2007, 23:449-458.
97. Pilarek M, Neubauer P, Marx U. Biological cardio-micro-pumps for microbioreactors and analytical micro-systems. Sens Actuat B Chem 2011, 156:517-526.
98. Turner NJ, Badylak SF. Regeneration of skeletal muscle. Cell Tissue Res 2012, 347:759-774.
99. Trivedi D, Rahn CD, Kier WK, Walker ID. Soft robotics: biological inspiration, state of the art, and future research. Appl Bionics Biomech 2008, 5:99-117.