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Annual Review of Biomedical Engineering

Volume 17, 2015

Biological Soft Robotics

Abstract

In nature, nanometer-scale molecular motors are used to generate force within cells for diverse processes from transcription and transport to muscle contraction. This adaptability and scalability across wide temporal, spatial, and force regimes have spurred the development of biological soft robotic systems that seek to mimic and extend these capabilities. This review describes how molecular motors are hierarchically organized into larger-scale structures in order to provide a basic understanding of how these systems work in nature and the complexity and functionality we hope to replicate in biological soft robotics. These span the subcellular scale to macroscale, and this article focuses on the integration of biological components with synthetic materials, coupled with bioinspired robotic design. Key examples include nanoscale molecular motor-powered actuators, microscale bacteria-controlled devices, and macroscale muscle-powered robots that grasp, walk, and swim. Finally, the current challenges and future opportunities in the field are addressed.

Keyword(s): bioinspired design, biomimetics, cardiac muscle, molecular motors, skeletal muscle, soft robotics, tissue engineering
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/content/journals/10.1146/annurev-bioeng-071114-040632
2015-12-07
2024-04-16
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Literature Cited

  1. Bustamante C, Chemla YR, Forde NR, Izhaky D. 1.  2004. Mechanical processes in biochemistry. Annu. Rev. Biochem. 73:705–48 [Google Scholar]
  2. Gelles J, Landick R. 2.  1998. RNA polymerase as a molecular motor. Cell 93:13–16 [Google Scholar]
  3. Berg HC. 3.  2003. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72:19–54 [Google Scholar]
  4. de Tombe PP. 4.  2003. Cardiac myofilaments: mechanics and regulation. J. Biomech. 36:721–30 [Google Scholar]
  5. Kiehn O. 5.  2006. Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci. 29:279–306 [Google Scholar]
  6. Brady AJ, Tan ST, Ricchiuti NV. 6.  1979. Contractile force measured in unskinned isolated adult rat heart fibres. Nature 282:728–29 [Google Scholar]
  7. Nishimura S, Yasuda S, Katoh M, Yamada KP, Yamashita H. 7.  et al. 2004. Single cell mechanics of rat cardiomyocytes under isometric, unloaded, and physiologically loaded conditions. Am. J. Physiol. Heart Circ. Physiol. 287:H196–202 [Google Scholar]
  8. Madden JDW, Vandesteeg NA, Anquetil PA, Madden PGA, Takshi A. 8.  et al. 2004. Artificial muscle technology: physical principles and naval prospects. IEEE J. Ocean. Eng. 29:706–28 [Google Scholar]
  9. Van Ham R, Sugar TG, Vanderborght B, Hollander KW, Lefeber D. 9.  2009. Compliant actuator designs review of actuators with passive adjustable compliance/controllable stiffness for robotic applications. IEEE Robot. Autom. Mag. 16:81–94 [Google Scholar]
  10. Pette D, Vrbová G. 10.  1985. Invited review: neural control of phenotypic expression in mammalian muscle fibers. Muscle Nerve 8:676–89 [Google Scholar]
  11. Kim S, Laschi C, Trimmer B. 11.  2013. Soft robotics: a bioinspired evolution in robotics. Trends Biotechnol. 31:287–94 [Google Scholar]
  12. Trivedi DRC, Kier WK, Walker ID. 12.  2008. Soft robotics: biological inspiration, state of the art, and future research. Appl. Bionics Biomech. 5:99–117 [Google Scholar]
  13. Behkam B, Sitti M. 13.  2007. Bacterial flagella-based propulsion and on/off motion control of microscale objects. Appl. Phys. Lett. 90:023902–3 [Google Scholar]
  14. Nawroth JC, Lee H, Feinberg AW, Ripplinger CM, McCain ML. 14.  et al. 2012. A tissue-engineered jellyfish with biomimetic propulsion. Nat. Biotechnol. 30:792–97 [Google Scholar]
  15. Tolley MT, Shephard RF, Mosadegh B, Galloway KC, Wehner M. 15.  et al. 2014. A resilient, untethered soft robot. Soft Robot. 1:213–23 [Google Scholar]
  16. Ilievski F, Mazzeo AD, Shepherd RE, Chen X, Whitesides GM. 16.  2011. Soft robotics for chemists. Angew. Chem. Int. Ed. 50:1890–95 [Google Scholar]
  17. Nawroth JC, Parker KK. 17.  2013. Design standards for engineered tissues. Biotechnol. Adv. 31:632–37 [Google Scholar]
  18. Pfeifer R, Lungarella M, Iida F. 18.  2007. Self-organization, embodiment, and biologically inspired robotics. Science 318:1088–93 [Google Scholar]
  19. Chan V, Asada HH, Bashir R. 19.  2014. Utilization and control of bioactuators across multiple length scales. Lab Chip 14:653–70 [Google Scholar]
  20. Duffy RM, Feinberg AW. 20.  2014. Engineered skeletal muscle tissue for soft robotics: fabrication strategies, current applications, and future challenges. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 6:178–95 [Google Scholar]
  21. Mallik R, Gross SP. 21.  2004. Molecular motors: strategies to get along. Curr. Biol. 14:R971–82 [Google Scholar]
  22. Kolomeisky AB, Fisher ME. 22.  2007. Molecular motors: a theorist's perspective. Annu. Rev. Phys. Chem. 58:675–95 [Google Scholar]
  23. Hirokawa N. 23.  1998. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279:519–26 [Google Scholar]
  24. Sengupta S, Spiering MM, Dey KK, Duan WT, Patra D. 24.  et al. 2014. DNA polymerase as a molecular motor and pump. ACS Nano 8:2410–18 [Google Scholar]
  25. Vale RD. 25.  2003. The molecular motor toolbox for intracellular transport. Cell 112:467–80 [Google Scholar]
  26. Goldstein LSB, Yang ZH. 26.  2000. Microtubule-based transport systems in neurons: the roles of kinesins and dyneins. Annu. Rev. Neurosci. 23:39–71 [Google Scholar]
  27. Sweeney HL, Houdusse A. 27.  2010. Structural and functional insights into the myosin motor mechanism. Annu. Rev. Biophys. 39:539–57 [Google Scholar]
  28. Dickinson RB, Caro L, Purich DL. 28.  2004. Force generation by cytoskeletal filament end-tracking proteins. Biophys. J. 87:2838–54 [Google Scholar]
  29. Zeile WL, Zhang FL, Dickinson RB, Purich DL. 29.  2005. Listeria's right-handed helical rocket-tail trajectories: mechanistic implications for force generation in actin-based motility. Cell Motil. Cytoskelet. 60:121–28 [Google Scholar]
  30. Fisher ME, Kolomeisky AB. 30.  1999. The force exerted by a molecular motor. PNAS 96:6597–602 [Google Scholar]
  31. Hess H. 31.  2011. Engineering applications of biomolecular motors. Annu. Rev. Biomed. Eng. 13:429–50 [Google Scholar]
  32. Bers DM. 32.  2001. Excitation-Contraction Coupling and Cardiac Contractile Force Boston: Kluwer Acad427
  33. Kreis TE, Birchmeier W. 33.  1980. Stress fiber sarcomeres of fibroblasts are contractile. Cell 22:555–61 [Google Scholar]
  34. Bond M, Somlyo AV. 34.  1982. Dense bodies and actin polarity in vertebrate smooth muscle. J. Cell Biol. 95:403–13 [Google Scholar]
  35. Piroddi N, Belus A, Scellini B, Tesi C, Giunti G. 35.  et al. 2007. Tension generation and relaxation in single myofibrils from human atrial and ventricular myocardium. Pflugers Arch. Eur. J. Physiol. 454:63–73 [Google Scholar]
  36. Katoh K, Kano Y, Masuda M, Onishi H, Fujiwara K. 36.  1998. Isolation and contraction of the stress fiber. Mol. Biol. Cell 9:1919–38 [Google Scholar]
  37. Hinz B. 37.  2010. The myofibroblast: paradigm for a mechanically active cell. J. Biomech. 43:146–55 [Google Scholar]
  38. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. 38.  2002. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3:349–63 [Google Scholar]
  39. Dabiri GA, Turnacioglu KK, Sanger JM, Sanger JW. 39.  1997. Myofibrillogenesis visualized in living embryonic cardiomyocytes. PNAS 94:9493–98 [Google Scholar]
  40. Somlyo AP, Somlyo AV. 40.  1994. Signal-transduction and regulation in smooth muscle. Nature 372:231–36 [Google Scholar]
  41. Bers DM. 41.  2002. Cardiac excitation-contraction coupling. Nature 415:198–205 [Google Scholar]
  42. Friend DS, Gilula NB. 42.  1972. Variations in tight and gap junctions in mammalian tissues. J. Cell Biol. 53:758–76 [Google Scholar]
  43. Pennisi DJ, Rentschler S, Gourdie RG, Fishman GI, Mikawa T. 43.  2002. Induction and patterning of the cardiac conduction system. Int. J. Dev. Biol. 46:765–75 [Google Scholar]
  44. Close RI. 44.  1972. Dynamic properties of mammalian skeletal muscles. Physiol. Rev. 52:129–97 [Google Scholar]
  45. Hirsch NP. 45.  2007. Neuromuscular junction in health and disease. Br. J. Anaesth. 99:132–38 [Google Scholar]
  46. Browne WR, Feringa BL. 46.  2006. Making molecular machines work. Nat. Nano 1:25–35 [Google Scholar]
  47. Carlsen RW, Sitti M. 47.  2014. Bio-hybrid cell-based actuators for microsystems. Small 10:3831–51 [Google Scholar]
  48. Howard J. 48.  2001. Mechanics of Motor Proteins and the Cytoskeleton Sunderland, MA: Sinauer384
  49. Lin C-T, Kao M-T, Kurabayashi K, Meyhofer E. 49.  2008. Self-contained, biomolecular motor-driven protein sorting and concentrating in an ultrasensitive microfluidic chip. Nano Lett. 8:1041–46 [Google Scholar]
  50. Bull J, Hunt A, Meyhöfer E. 50.  2005. A theoretical model of a molecular-motor-powered pump. Biomed. Microdevices 7:21–33 [Google Scholar]
  51. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR. 51.  2009. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10:778–90 [Google Scholar]
  52. Wakayama J, Shohara M, Yagi C, Ono H, Miyake N. 52.  et al. 2002. Zigzag motions of the myosin-coated beads actively sliding along actin filaments suspended between immobilized beads. Biochim. Biophys. Acta 157393–99
  53. Interliggi KA, Zeile WL, Ciftan-Hens SA, McGuire GE, Purich DL, Dickinson RB. 53.  2007. Guidance of actin filament elongation on filament-binding tracks. Langmuir 23:11911–16 [Google Scholar]
  54. Lund K, Manzo AJ, Dabby N, Michelotti N, Johnson-Buck A. 54.  et al. 2010. Molecular robots guided by prescriptive landscapes. Nature 465:206–10 [Google Scholar]
  55. Kamm RD, Bashir R. 55.  2014. Creating living cellular machines. Ann. Biomed. Eng. 42:445–59 [Google Scholar]
  56. Sokolov A, Apodaca MM, Grzybowski BA, Aranson IS. 56.  2010. Swimming bacteria power microscopic gears. PNAS 107:969–74 [Google Scholar]
  57. González LM, Ruder WC, Leduc PR, Messner WC. 57.  2014. Controlling magnetotactic bacteria through an integrated nanofabricated metallic island and optical microscope approach. Sci. Rep. 4:4104 [Google Scholar]
  58. Carlsen RW, Edwards MR, Zhuang J, Pacoret C, Sitti M. 58.  2014. Magnetic steering control of multi-cellular bio-hybrid microswimmers. Lab Chip 14:3850–59 [Google Scholar]
  59. Kim D, Liu A, Diller E, Sitti M. 59.  2012. Chemotactic steering of bacteria propelled microbeads. Biomed. Microdevices 14:1009–17 [Google Scholar]
  60. Steager E, Kim C-B, Patel J, Bith S, Naik C. 60.  et al. 2007. Control of microfabricated structures powered by flagellated bacteria using phototaxis. Appl. Phys. Lett. 90:263901 [Google Scholar]
  61. Pilarek M, Neubauer P, Marx U. 61.  2011. Biological cardio-micro-pumps for microbioreactors and analytical micro-systems. Sens. Actuators B Chem. 156:517–26 [Google Scholar]
  62. Das M, Gregory CA, Molnar P, Riedel LM, Wilson K, Hickman JJ. 62.  2006. A defined system to allow skeletal muscle differentiation and subsequent integration with silicon microstructures. Biomaterials 27:4374–80 [Google Scholar]
  63. Wilson K, Molnar P, Hickman J. 63.  2007. Integration of functional myotubes with a Bio-MEMS device for non-invasive interrogation. Lab Chip 7:920–22 [Google Scholar]
  64. Das M, Wilson K, Molnar P, Hickman JJ. 64.  2007. Differentiation of skeletal muscle and integration of myotubes with silicon microstructures using serum-free medium and a synthetic silane substrate. Nat. Protoc. 2:1795–801 [Google Scholar]
  65. Wilson K, Das M, Wahl KJ, Colton RJ, Hickman J. 65.  2010. Measurement of contractile stress generated by cultured rat muscle on silicon cantilevers for toxin detection and muscle performance enhancement. PLOS ONE 5:e11042 [Google Scholar]
  66. Xi JZ, Schmidt JJ, Montemagno CD. 66.  2005. Self-assembled microdevices driven by muscle. Nat. Mater. 4:180–84 [Google Scholar]
  67. Palchesko RN, Zhang L, Sun Y, Feinberg AW. 67.  2012. Development of polydimethylsiloxane substrates with tunable elastic modulus to study cell mechanobiology in muscle and nerve. PLOS ONE 7:1–13 [Google Scholar]
  68. Tanaka Y, Morishima K, Shimizu T, Kikuchi A, Yamato M. 68.  et al. 2006. Demonstration of a PDMS-based bio-microactuator using cultured cardiomyocytes to drive polymer micropillars. Lab Chip 6:230–35 [Google Scholar]
  69. Tanaka Y, Sato K, Shimizu T, Yamato M, Okano T. 69.  et al. 2008. Demonstration of a bio-microactuator powered by vascular smooth muscle cells coupled to polymer micropillars. Lab Chip 8:58–61 [Google Scholar]
  70. Morishima K, Tanaka Y, Ebara M, Shimizu T, Kikuchi A. 70.  et al. 2006. Demonstration of a bio-microactuator powered by cultured cardiomyocytes coupled to hydrogel micropillars. Sens. Actuators B Chem. 119:345–50 [Google Scholar]
  71. Akiyama Y, Iwabuchi K, Furukawa Y, Morishima K. 71.  2009. Long-term and room temperature operable bioactuator powered by insect dorsal vessel tissue. Lab Chip 9:140–4 [Google Scholar]
  72. Park J, Ryu J, Choi SK, Seo E, Cha JM. 72.  et al. 2005. Real-time measurement of the contractile forces of self-organized cardiomyocytes on hybrid biopolymer microcantilevers. Anal. Chem. 77:6571–80 [Google Scholar]
  73. Kim J, Park J, Yang S, Baek J, Kim B. 73.  et al. 2007. Establishment of a fabrication method for a long-term actuated hybrid cell robot. Lab Chip 7:1504–8 [Google Scholar]
  74. Chan V, Jeong JH, Bajaj P, Collens M, Saif T. 74.  et al. 2012. Multi-material bio-fabrication of hydrogel cantilevers and actuators with stereolithography. Lab Chip 12:88–98 [Google Scholar]
  75. Chan V, Park K, Collens MB, Kong H, Saif TA, Bashir R. 75.  2012. Development of miniaturized walking biological machines. Sci. Rep. 2:857 [Google Scholar]
  76. Cvetkovic C, Raman R, Chan V, Williams BJ, Tolish M. 76.  et al. 2014. Three-dimensionally printed biological machines powered by skeletal muscle. PNAS 111:10125–30 [Google Scholar]
  77. Feinberg AW, Feigel A, Shevkoplyas SS, Sheehy S, Whitesides GM, Parker KK. 77.  2007. Muscular thin films for building actuators and powering devices. Science 317:1366–70 [Google Scholar]
  78. Feinberg AW, Alford PW, Jin H, Ripplinger CM, Werdich AA. 78.  et al. 2012. Controlling the contractile strength of engineered cardiac muscle by hierarchal tissue architecture. Biomaterials 33:5732–41 [Google Scholar]
  79. Alford PW, Feinberg AW, Sheehy SP, Parker KK. 79.  2010. Biohybrid thin films for measuring contractility in engineered cardiovascular muscle. Biomaterials 31:3613–21 [Google Scholar]
  80. Alford PW, Nesmith AP, Seywerd JN, Grosberg A, Parker KK. 80.  2011. Vascular smooth muscle contractility depends on cell shape. Integr. Biol. 3:1063–70 [Google Scholar]
  81. Sun Y, Duffy R, Lee A, Feinberg AW. 81.  2013. Optimizing the structure and contractility of engineered skeletal muscle thin films. Acta Biomater. 9:7885–94 [Google Scholar]
  82. Feinberg AW, Ripplinger CM, van der Meer P, Sheehy SP, Domian I. 82.  et al. 2013. Functional differences in engineered myocardium from embryonic stem cell–derived versus neonatal cardiomyocytes. Stem Cell Rep. 1:387–96 [Google Scholar]
  83. Domian IJ, Chiravuri M, van der Meer P, Feinberg AW, Shi X. 83.  et al. 2009. Generation of functional ventricular heart muscle from mouse ventricular progenitor cells. Science 326:426–29 [Google Scholar]
  84. Balachandran K, Alford PW, Wylie-Sears J, Goss JA, Grosberg A. 84.  et al. 2011. Cyclic strain induces dual-mode endothelial-mesenchymal transformation of the cardiac valve. PNAS 108:19943–48 [Google Scholar]
  85. Agarwal A, Farouz Y, Nesmith AP, Deravi LF, McCain ML, Parker KK. 85.  2013. Micropatterning alginate substrates for in vitro cardiovascular muscle on a chip. Adv. Funct. Mater. 23:3738–46 [Google Scholar]
  86. McCain ML, Agarwal A, Nesmith HW, Nesmith AP, Parker KK. 86.  2014. Micromolded gelatin hydrogels for extended culture of engineered cardiac tissues. Biomaterials 35:5462–71 [Google Scholar]
  87. Novakovic GV, Eschenhagen T, Mummery C. 87.  2014. Myocardial tissue engineering: in vitro models. Cold Spring Harb. Perspect. Med. 4:a014076 [Google Scholar]
  88. Jallerat Q, Szymanski JM, Feinberg AW. 88.  2014. Nano- and microstructured ECM and biomimetic scaffolds for cardiac tissue engineering. Bio-Inspired Materials for Biomedical Engineering AB Brennan, CM Kirschner 195–226 Hoboken, NJ: Wiley [Google Scholar]
  89. Feinberg AW. 89.  2011. Engineered tissue grafts: opportunities and challenges in regenerative medicine. Wiley Interdiscip. Rev. Syst. Biol. Med. 4:207–20 [Google Scholar]
  90. Koning M, Harmsen MC, van Luyn MJA, Werker PMN. 90.  2009. Current opportunities and challenges in skeletal muscle tissue engineering. J. Tissue Eng. Regen. Med. 3:407–15 [Google Scholar]
  91. Vandenburgh HH, Karlisch P, Farr L. 91.  1988. Maintenance of highly contractile tissue-cultured avian skeletal myotubes in collagen gel. In Vitro Cell. Dev. Biol. 24:166–74 [Google Scholar]
  92. Rhim C, Lowell DA, Reedy MC, Slentz DH, Zhang SJ. 92.  et al. 2007. Morphology and ultrastructure of differentiating three-dimensional mammalian skeletal muscle in a collagen gel. Muscle Nerve 36:71–80 [Google Scholar]
  93. Turnbull IC, Karakikes I, Serrao GW, Backeris P, Lee JJ. 93.  et al. 2014. Advancing functional engineered cardiac tissues toward a preclinical model of human myocardium. FASEB J. 28:644–54 [Google Scholar]
  94. Black LD, Meyers JD, Weinbaum JS, Shvelidze YA, Tranquillo RT. 94.  2009. Cell-induced alignment augments twitch force in fibrin gel–based engineered myocardium via gap junction modification. Tissue Eng. Part A 15:3099–108 [Google Scholar]
  95. Bian W, Bursac N. 95.  2009. Engineered skeletal muscle tissue networks with controllable architecture. Biomaterials 30:1401–12 [Google Scholar]
  96. Bian W, Liau B, Badie N, Bursac N. 96.  2009. Mesoscopic hydrogel molding to control the 3D geometry of bioartificial muscle tissues. Nat. Protoc. 4:1522–34 [Google Scholar]
  97. Bian W, Juhas M, Pfeiler TW, Bursac N. 97.  2012. Local tissue geometry determines contractile force generation of engineered muscle networks. Tissue Eng. Part A 18:957–67 [Google Scholar]
  98. Dennis RG, Kosnik PE 2nd. 98.  2000. Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cell. Dev. Biol. Anim. 36:327–35 [Google Scholar]
  99. Dennis RG, Kosnik PE 2nd, Gilbert ME, Faulkner JA. 99.  2001. Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. Am. J. Physiol. Cell Physiol. 280:C288–95 [Google Scholar]
  100. Dennis RG, Dow DE. 100.  2007. Excitability of skeletal muscle during development, denervation, and tissue culture. Tissue Eng. 13:2395–404 [Google Scholar]
  101. Baar K, Birla R, Boluyt MO, Borschel GH, Arruda EM, Dennis RG. 101.  2004. Self-organization of rat cardiac cells into contractile 3-D cardiac tissue. FASEB J. 18:275–77 [Google Scholar]
  102. Larkin LM, Calve S, Kostrominova TY, Arruda EM. 102.  2006. Structure and functional evaluation of tendon-skeletal muscle constructs engineered in vitro. Tissue Eng. 12:3149–58 [Google Scholar]
  103. Akiyama Y, Kikuchi A, Yamato M, Okano T. 103.  2004. Ultrathin poly(N-isopropylacrylamide) grafted layer on polystyrene surfaces for cell adhesion/detachment control. Langmuir 20:5506–11 [Google Scholar]
  104. Shimizu T, Sekine H, Isoi Y, Yamato M, Kikuchi A, Okano T. 104.  2006. Long-term survival and growth of pulsatile myocardial tissue grafts engineered by the layering of cardiomyocyte sheets. Tissue Eng. 12:499–507 [Google Scholar]
  105. Haraguchi Y, Shimizu T, Sasagawa T, Sekine H, Sakaguchi K. 105.  et al. 2012. Fabrication of functional three-dimensional tissues by stacking cell sheets in vitro. Nat. Protoc. 7:850–58 [Google Scholar]
  106. Yamamoto Y, Ito A, Fujita H, Nagamori E, Kawabe Y, Kamihira M. 106.  2011. Functional evaluation of artificial skeletal muscle tissue constructs fabricated by a magnetic force-based tissue engineering technique. Tissue Eng. Part A 17:107–14 [Google Scholar]
  107. Stevens KR, Kreutziger KL, Dupras SK, Korte FS, Regnier M. 107.  et al. 2009. Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. PNAS 106:16568–73 [Google Scholar]
  108. Tanaka Y, Morishima K, Shimizu T, Kikuchi A, Yamato M. 108.  et al. 2006. An actuated pump on-chip powered by cultured cardiomyocytes. Lab Chip 6:362–68 [Google Scholar]
  109. Tanaka Y, Sato K, Shimizu T, Yamato M, Okano T, Kitamori T. 109.  2007. A micro-spherical heart pump powered by cultured cardiomyocytes. Lab Chip 7:207–12 [Google Scholar]
  110. Park J, Kim IC, Baek J, Cha M, Kim J. 110.  et al. 2007. Micro pumping with cardiomyocyte-polymer hybrid. Lab Chip 7:1367–70 [Google Scholar]
  111. Hoshino T, Morishima K. 111.  2010. Muscle-powered cantilever for microtweezers with an artificial micro skeleton and rat primary myotubes. J. Biomech. Sci. Eng. 5:245–51 [Google Scholar]
  112. Kabumoto K, Hoshino T, Morishima K. 112.  2010. Bio-robotics using interaction between neuron and muscle for development of living prosthesis. Proc. Int. Conf. Biomed. Robot. Biomechatronics, 3rd Univ. Tokyo, Sept. 26–29 419–24 Piscataway, NJ: IEEE [Google Scholar]
  113. Akiyama Y, Sakuma T, Funakoshi K, Hoshino T, Iwabuchi K, Morishima K. 113.  2013. Atmospheric-operable bioactuator powered by insect muscle packaged with medium. Lab Chip 13:4870–80 [Google Scholar]
  114. Akiyama Y, Hoshino T, Iwabuchi K, Morishima K. 114.  2012. Room temperature operable autonomously moving bio-microrobot powered by insect dorsal vessel tissue. PLOS ONE 7:e38274 [Google Scholar]
  115. Akiyama Y, Odaira K, Sakiyama K, Hoshino T, Iwabuchi K, Morishima K. 115.  2012. Rapidly-moving insect muscle-powered microrobot and its chemical acceleration. Biomed. Microdevices 14:979–86 [Google Scholar]
  116. Williams BJ, Anand SV, Rajagopalan J, Saif MTA. 116.  2014. A self-propelled biohybrid swimmer at low Reynolds number. Nat. Commun. 5:3081 [Google Scholar]
  117. Herr H, Dennis R. 117.  2004. A swimming robot actuated by living muscle tissue. J. Neuroeng. Rehabil. 1:6 [Google Scholar]
  118. Shimizu Y, Kuruma Y, Ying BW, Umekage S, Ueda T. 118.  2006. Cell-free translation systems for protein engineering. FEBS J. 273:4133–40 [Google Scholar]
  119. Varley J, Birch J. 119.  1999. Reactor design for large scale suspension animal cell culture. Cytotechnology 29:177–205 [Google Scholar]
  120. Grillberger L, Kreil TR, Nasr S, Reiter M. 120.  2009. Emerging trends in plasma-free manufacturing of recombinant protein therapeutics expressed in mammalian cells. Biotechnol. J. 4:186–201 [Google Scholar]
  121. Baryshyan AL, Domigan LJ, Hunt B, Trimmer BA, Kaplan DL. 121.  2014. Self-assembled insect muscle bioactuators with long term function under a range of environmental conditions. RSC Adv. 4:39962–68 [Google Scholar]
  122. Baryshyan AL, Woods W, Trimmer BA, Kaplan DL. 122.  2012. Isolation and maintenance-free culture of contractile myotubes from Manduca sexta embryos. PLOS ONE 7:e31598 [Google Scholar]
  123. Dinsmore J, Ratliff J, Deacon T, Pakzaban P, Jacoby D. 123.  et al. 1996. Embryonic stem cells differentiated in vitro as a novel source of cells for transplantation. Cell Transplant. 5:131–43 [Google Scholar]
  124. Lee T-H, Song S-H, Kim KL, Yi J-Y, Shin G-H. 124.  et al. 2010. Functional recapitulation of smooth muscle cells via induced pluripotent stem cells from human aortic smooth muscle cells. Circ. Res. 106:120–28 [Google Scholar]
  125. Passier R, van Laake LW, Mummery CL. 125.  2008. Stem-cell–based therapy and lessons from the heart. Nature 453:322–29 [Google Scholar]
  126. Ahadian S, Ostrovidov S, Hosseini V, Kaji H, Ramalingam M. 126.  et al. 2013. Electrical stimulation as a biomimicry tool for regulating muscle cell behavior. Organogenesis 9:87–92 [Google Scholar]
  127. Ogut O, Brozovich FV. 127.  2003. Regulation of force in vascular smooth muscle. J. Mol. Cell. Cardiol. 35:347–55 [Google Scholar]
  128. Akiyama Y, Iwabuchi K, Furukawa Y, Morishima K. 128.  2010. Electrical stimulation of cultured lepidopteran dorsal vessel tissue: an experiment for development of bioactuators. In Vitro Cell. Dev. Biol. Anim. 46:411–15 [Google Scholar]
  129. Bours MJL, Swennen ELR, Di Virgilio F, Cronstein BN, Dagnelie PC. 129.  2006. Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol. Ther. 112:358–404 [Google Scholar]
  130. Rakusan K, Flanagan MF, Geva T, Southern J, Van Praagh R. 130.  1992. Morphometry of human coronary capillaries during normal growth and the effect of age in left ventricular pressure-overload hypertrophy. Circulation 86:38–46 [Google Scholar]
  131. Lovett M, Lee K, Edwards A, Kaplan DL. 131.  2009. Vascularization strategies for tissue engineering. Tissue Eng. Part B Rev. 15:353–70 [Google Scholar]
  132. Sicari BM, Agrawal V, Siu BF, Medberry CJ, Dearth CL. 132.  et al. 2012. A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng. Part A 18:1941–48 [Google Scholar]
  133. Machingal MA, Corona BT, Walters TJ, Kesireddy V, Koval CN. 133.  et al. 2011. A tissue-engineered muscle repair construct for functional restoration of an irrecoverable muscle injury in a murine model. Tissue Eng. Part A 17:2291–303 [Google Scholar]
  134. Miller JS, Stevens KR, Yang MT, Baker BM, Nguyen D-HT. 134.  et al. 2012. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater. 11:768–74 [Google Scholar]
  135. Zheng Y, Chen J, Craven M, Choi NW, Totorica S. 135.  et al. 2012. In vitro microvessels for the study of angiogenesis and thrombosis. PNAS 109:9342–47 [Google Scholar]
  136. Nagamine K, Kawashima T, Sekine S, Ido Y, Kanzaki M, Nishizawa M. 136.  2011. Spatiotemporally controlled contraction of micropatterned skeletal muscle cells on a hydrogel sheet. Lab Chip 11:513–17 [Google Scholar]
  137. Sakar MS, Neal D, Boudou T, Borochin MA, Li Y. 137.  et al. 2012. Formation and optogenetic control of engineered 3D skeletal muscle bioactuators. Lab Chip 12:4976–85 [Google Scholar]
  138. Langhammer CG, Kutzing MK, Luo V, Zahn JD, Firestein BL. 138.  2011. 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. 27:891–95 [Google Scholar]
  139. Langhammer CG, Kutzing MK, Luo V, Zahn JD, Firestein BL. 139.  2013. A topographically modified substrate-embedded MEA for directed myotube formation at electrode contact sites. Ann. Biomed. Eng. 41:408–20 [Google Scholar]
  140. Huffard CL, Boneka F, Full RJ. 140.  2005. Underwater bipedal locomotion by octopuses in disguise. Science 307:1927 [Google Scholar]
/content/journals/10.1146/annurev-bioeng-071114-040632
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Biological Soft Robotics
Annual Review of Biomedical Engineering 17, 243 (2015); https://doi.org/10.1146/annurev-bioeng-071114-040632
/content/journals/10.1146/annurev-bioeng-071114-040632
/content/journals/10.1146/annurev-bioeng-071114-040632
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  • Article Type: Review Article

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