1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biomedical Engineering
  4. Volume 26, 2024
  5. Article

Annual Review of Biomedical Engineering

Volume 26, 2024

Biofabrication of Living Actuators

Abstract

The impact of tissue engineering has extended beyond a traditional focus in medicine to the rapidly growing realm of biohybrid robotics. Leveraging living actuators as functional components in machines has been a central focus of this field, generating a range of compelling demonstrations of robots capable of muscle-powered swimming, walking, pumping, gripping, and even computation. In this review, we highlight key advances in fabricating tissue-scale cardiac and skeletal muscle actuators for a range of functional applications. We discuss areas for future growth including scalable manufacturing, integrated feedback control, and predictive modeling and also propose methods for ensuring inclusive and bioethics-focused pedagogy in this emerging discipline. We hope this review motivates the next generation of biomedical engineers to advance rational design and practical use of living machines for applications ranging from telesurgery to manufacturing to on- and off-world exploration.

Keyword(s): bioactuators, biofabrication, biohybrid, cardiac muscle, skeletal muscle, soft robotics
Loading

Article metrics loading...

/content/journals/10.1146/annurev-bioeng-110122-013805
2024-07-03
2024-07-04
Loading full text...

Full text loading...

/deliver/fulltext/bioeng/26/1/annurev-bioeng-110122-013805.html?itemId=/content/journals/10.1146/annurev-bioeng-110122-013805&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Ripa R, George T, Sattar Y. 2023.. Physiology, cardiac muscle. . In StatPearls. Treasure Island, FL:: StatPearls Publishing
     [Google Scholar]
  2. 2.
    Hafen BB, Burns B. 2023.. Physiology, smooth muscle. . In StatPearls. Treasure Island, FL:: StatPearls Publishing
     [Google Scholar]
  3. 3.
    McCuller C, Jessu R, Callahan AL. 2023.. Physiology, skeletal muscle. . In StatPearls. Treasure Island, FL:: StatPearls Publishing
     [Google Scholar]
  4. 4.
    Frontera WR, Ochala J. 2015.. Skeletal muscle: a brief review of structure and function. . Behavior Genet. 45:(2):183–95
     [Google Scholar]
  5. 5.
    Raman R. 2021.. Biofabrication. Cambridge, MA:: MIT Press
     [Google Scholar]
  6. 6.
    Raman R, Bashir R. 2017.. Biomimicry, biofabrication, and biohybrid systems: the emergence and evolution of biological design. . Adv. Healthc. Mater. 6::1700496
     [Crossref] [Google Scholar]
  7. 7.
    Khademhosseini A, Langer R. 2016.. A decade of progress in tissue engineering. . Nat. Protoc. 11:(10):1775–81
     [Crossref] [Google Scholar]
  8. 8.
    Raman R, Langer R. 2019.. Biohybrid design gets personal: new materials for patient-specific therapy. . Adv. Mater. 32::1901969
     [Crossref] [Google Scholar]
  9. 9.
    Iyer RK, Chiu LLY, Reis LA, Radisic M. 2011.. Engineered cardiac tissues. . Curr. Opin. Biotechnol. 22:(5):706–14
     [Crossref] [Google Scholar]
  10. 10.
    Raman R. 2019.. Modeling muscle. . Science 363:(6431):1051
     [Crossref] [Google Scholar]
  11. 11.
    Yu JR, Navarro J, Coburn JC, Mahadik B, Molnar J, et al. 2019.. Current and future perspectives on skin tissue engineering: key features of biomedical research, translational assessment, and clinical application. . Adv. Healthc. Mater. 8:(5):e1801471
     [Crossref] [Google Scholar]
  12. 12.
    Neiman JAS, Raman R, Chan V, Rhoads MG, Raredon MSB, et al. 2015.. Photopatterning of hydrogel scaffolds coupled to filter materials using stereolithography for perfused 3D culture of hepatocytes. . Biotechnol. Bioeng. 112:(4):777–87
     [Crossref] [Google Scholar]
  13. 13.
    Gargus ES, Rogers HB, McKinnon KE, Edmonds ME, Woodruff TK. 2020.. Engineered reproductive tissues. . Nat. Biomed. Eng. 4::381–93. Erratum. 2020.. Nat. Biomed. Eng. 4::574
     [Google Scholar]
  14. 14.
    Aydin O, Passaro AP, Raman R, Spellicy SE, Weinberg RP, et al. 2022.. Principles for the design of multicellular engineered living systems. . APL Bioeng. 6:(1):010903
     [Crossref] [Google Scholar]
  15. 15.
    Ricotti L, Trimmer B, Feinberg AW, Raman R, Parker KK, et al. 2017.. Biohybrid actuators for robotics: a review of devices actuated by living cells. . Sci. Robot. 2::eaaq0495
     [Crossref] [Google Scholar]
  16. 16.
    Feinberg AW. 2015.. Biological soft robotics. . Annu. Rev. Biomed. Eng. 17::243–65
     [Crossref] [Google Scholar]
  17. 17.
    Chan V, Asada HH, Bashir R. 2014.. Utilization and control of bioactuators across multiple length scales. . Lab Chip 14:(4):653–70
     [Crossref] [Google Scholar]
  18. 18.
    Webster-Wood VA, Guix M, Xu NW, Behkam B, Sato H, et al. 2023.. Biohybrid robots: recent progress, challenges, and perspectives. . Bioinspir. Biomim. 18:(1):015001
     [Crossref] [Google Scholar]
  19. 19.
    Schätzlein E, Blaeser A. 2022.. Recent trends in bioartificial muscle engineering and their applications in cultured meat, biorobotic systems and biohybrid implants. . Commun. Biol. 5:(1):737
     [Crossref] [Google Scholar]
  20. 20.
    Herr H, Dennis RG. 2004.. A swimming robot actuated by living muscle tissue. . J. Neuroeng. Rehabil. 1::6
     [Crossref] [Google Scholar]
  21. 21.
    Yurke B, Turberfield AJ, Mills AP Jr., Simmel FC, Neumann JL. 2000.. A DNA-fuelled molecular machine made of DNA. . Nature 406::605–8
     [Crossref] [Google Scholar]
  22. 22.
    Simmel F, Yurke B. 2001.. Using DNA to construct and power a nanoactuator. . Phys. Rev. E 63:(4):63–67
     [Crossref] [Google Scholar]
  23. 23.
    Beamish JA, He P, Kottke-Marchant K, Marchant RE. 2010.. Molecular regulation of contractile smooth muscle cell phenotype: implications for vascular tissue engineering. . Tissue Eng. Part B Rev. 16:(5):467–91
     [Crossref] [Google Scholar]
  24. 24.
    Nawroth JC, Lee H, Feinberg AW, Ripplinger CM, McCain ML, et al. 2012.. A tissue-engineered jellyfish with biomimetic propulsion. . Nat. Biotechnol. 30:(8):792–97
     [Crossref] [Google Scholar]
  25. 25.
    Park S-J, Gazzola M, Park KS, Park S, Di Santo V, et al. 2016.. Phototactic guidance of a tissue-engineered soft-robotic ray. . Science 353:(6295):158–62
     [Crossref] [Google Scholar]
  26. 26.
    Williams BJ, Anand SV, Rajagopalan J, Saif MTA. 2014.. A self-propelled biohybrid swimmer at low Reynolds number. . Nat. Commun. 5::3081
     [Crossref] [Google Scholar]
  27. 27.
    Lee KY, Park S-J, Matthews DG, Kim SL, Marquez CA, et al. 2022.. An autonomously swimming biohybrid fish designed with human cardiac biophysics. . Science 375:(6581):639–47
     [Crossref] [Google Scholar]
  28. 28.
    Bliley JM, Vermeer MCSC, Duffy RM, Batalov I, Kramer D, et al. 2021.. Dynamic loading of human engineered heart tissue enhances contractile function and drives a desmosome-linked disease phenotype. . Sci. Transl. Med. 13:(603):eabd1817
     [Crossref] [Google Scholar]
  29. 29.
    Nazareth EJP, Ostblom JEE, Lücker PB, Shukla S, Alvarez MM, et al. 2013.. High-throughput fingerprinting of human pluripotent stem cell fate responses and lineage bias. . Nat. Methods 10:(12):1225–31
     [Crossref] [Google Scholar]
  30. 30.
    Aydin O, Zhang X, Nuethong S, Pagan-Diaz GJ, Bashir R, et al. 2019.. Neuromuscular actuation of biohybrid motile bots. . PNAS 116::19841–47
     [Crossref] [Google Scholar]
  31. 31.
    Raman R, Hua T, Gwynne D, Collins J, Tamang S, et al. 2020.. Light-degradable hydrogels as dynamic triggers in gastrointestinal applications. . Sci. Adv. 6:(3):eaay0065
     [Crossref] [Google Scholar]
  32. 32.
    Babaee S, Pajovic S, Kirtane AR, Shi J, Caffarel-Salvador E, et al. 2019.. Temperature-responsive biometamaterials for gastrointestinal applications. . Sci. Transl. Med. 11:(488):eaau8581
     [Crossref] [Google Scholar]
  33. 33.
    Liu J, Pang Y, Zhang S, Cleveland C, Yin X, et al. 2017.. Triggerable tough hydrogels for gastric resident dosage forms. . Nat. Commun. 8:(1):124
     [Crossref] [Google Scholar]
  34. 34.
    Xu B, Han X, Hu Y, Luo Y, Chen CH, et al. 2019.. A remotely controlled transformable soft robot based on engineered cardiac tissue construct. . Small 15:(18):1900006
     [Crossref] [Google Scholar]
  35. 35.
    Chan V, Park K, Collens MB, Kong H, Saif TA, Bashir R. 2012.. Development of miniaturized walking biological machines. . Sci. Rep. 2::857
     [Crossref] [Google Scholar]
  36. 36.
    Feinberg AW, Feigel A, Shevkoplyas SS, Sheehy S, Whitesides GM, Parker KK. 2007.. Muscular thin films for building actuators and powering devices. . Science 317:(5843):1366–70
     [Crossref] [Google Scholar]
  37. 37.
    Kriegman S, Blackiston D, Levin M, Bongard J. 2020.. A scalable pipeline for designing reconfigurable organisms. . PNAS 117::1853–59
     [Crossref] [Google Scholar]
  38. 38.
    Blackiston D, Lederer E, Kriegman S, Garnier S, Bongard J, Levin M. 2021.. A cellular platform for the development of synthetic living machines. . Sci. Robot. 6:(52):eabf1571
     [Crossref] [Google Scholar]
  39. 39.
    Cvetkovic C, Raman R, Chan V, Williams BJ, Tolish M, et al. 2014.. Three-dimensionally printed biological machines powered by skeletal muscle. . PNAS 111:(28):10125–30
     [Crossref] [Google Scholar]
  40. 40.
    Dennis RG, Kosnik PE, Gilbert ME, Faulkner JA. 2001.. Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. . Am. J. Physiol. Cell Physiol. 280:(2):C288–95
     [Crossref] [Google Scholar]
  41. 41.
    Hinds S, Bian W, Dennis RG, Bursac N. 2011.. The role of extracellular matrix composition in structure and function of bioengineered skeletal muscle. . Biomaterials 32:(14):3575–83
     [Crossref] [Google Scholar]
  42. 42.
    Raman R, Cvetkovic C, Uzel SGM, Platt RJ, Sengupta P, Kamm RD. 2016.. Optogenetic skeletal muscle-powered adaptive biological machines. . PNAS 113::3497–502
     [Crossref] [Google Scholar]
  43. 43.
    Raman R, Cvetkovic C, Bashir R. 2017.. A modular approach to the design, fabrication, and characterization of muscle-powered biological machines. . Nat. Protoc. 12:(3):519–33
     [Crossref] [Google Scholar]
  44. 44.
    Wang J, Wang Y, Kim Y, Yu T, Bashir R. 2022.. Multi-actuator light-controlled biological robots. . APL Bioeng. 6:(3):036103
     [Crossref] [Google Scholar]
  45. 45.
    Sambasivan R, Tajbakhsh S. 2015.. Vertebrate myogenesis. . Results Probl. Cell Differ. 56::191–213
     [Crossref] [Google Scholar]
  46. 46.
    Rangarajan S, Madden L, Bursac N. 2014.. Use of flow, electrical, and mechanical stimulation to promote engineering of striated muscles. . Ann. Biomed. Eng. 42:(7):1391–405
     [Crossref] [Google Scholar]
  47. 47.
    Pagan-Diaz GJ, Zhang X, Grant L, Kim Y, Aydin O, et al. 2018.. Simulation and fabrication of stronger, larger, and faster walking biohybrid machines. . Adv. Funct. Mater. 28::1801145
     [Crossref] [Google Scholar]
  48. 48.
    Raman R, Grant L, Seo Y, Cvetkovic C, Gapinske M, et al. 2017.. Damage, healing, and remodeling in optogenetic skeletal muscle bioactuators. . Adv. Healthc. Mater. 6::1700030
     [Crossref] [Google Scholar]
  49. 49.
    Rousseau E, Raman R, Tamir T, Bu A, Srinivasan S, et al. 2023.. Actuated tissue engineered muscle grafts restore functional mobility after volumetric muscle loss. . Biomaterials 302::122317
     [Crossref] [Google Scholar]
  50. 50.
    Kim Y, Yang Y, Zhang X, Li Z, Vázquez-Guardado A, et al. 2023.. Remote control of muscle-driven miniature robots with battery-free wireless optoelectronics. . Sci. Robot. 8:(74):eadd1053
     [Crossref] [Google Scholar]
  51. 51.
    Tanaka Y, Sato K, Shimizu T, Yamato M, Okano T, Kitamori T. 2007.. A micro-spherical heart pump powered by cultured cardiomyocytes. . Lab Chip 7:(2):207–12
     [Crossref] [Google Scholar]
  52. 52.
    Yamatsuta E, Ping Beh S, Uesugi K, Tsujimura H, Morishima K. 2019.. A micro peristaltic pump using an optically controllable bioactuator. . Engineering 5:(3):580–85
     [Crossref] [Google Scholar]
  53. 53.
    Li Z, Seo Y, Aydin O, Elhebeary M, Kamm RD, et al. 2019.. Biohybrid valveless pump-bot powered by engineered skeletal muscle. . PNAS 116::1543–48
     [Crossref] [Google Scholar]
  54. 54.
    Ko E, Aydin O, Li Z, Gapinske L, Huang KY, et al. 2022.. Empowering engineered muscle in biohybrid pump by extending connexin 43 duration with reduced graphene oxides. . Biomaterials 287::121643
     [Crossref] [Google Scholar]
  55. 55.
    Li Z, Balance WC, Joy MSH, Patel S, Hwang J, et al. 2022.. Adaptive biohybrid pumping machine with flow loop feedback. . Biofabrication 14:(2):025009
     [Crossref] [Google Scholar]
  56. 56.
    Akiyama Y, Sakuma T, Funakoshi K, Hoshino T, Iwabuchi K, Morishima K. 2013.. Atmospheric-operable bioactuator powered by insect muscle packaged with medium. . Lab Chip 13:(24):4870–80
     [Crossref] [Google Scholar]
  57. 57.
    Morimoto Y, Onoe H, Takeuchi S. 2018.. Biohybrid robot powered by an antagonistic pair of skeletal muscle tissues. . Sci. Robot. 3:(18):eaat4440
     [Crossref] [Google Scholar]
  58. 58.
    Morimoto Y, Onoe H, Takeuchi S. 2020.. Biohybrid robot with skeletal muscle tissue covered with a collagen structure for moving in air. . APL Bioeng. 4::026101
     [Crossref] [Google Scholar]
  59. 59.
    Can UI, Nagarajan N, Vural DC, Zorlutuna P. 2017.. Muscle-cell-based “living diodes. .” Adv. Biosyst. 1::e1600035
     [Crossref] [Google Scholar]
  60. 60.
    Ren X, Gomez J, Bashar MK, Ji J, Can UI, et al. 2021.. Cardiac muscle cell-based coupled oscillator network for collective computing. . Adv. Intel. Syst. 3:(4):2000253
     [Crossref] [Google Scholar]
  61. 61.
    Ji J, Ren X, Gomez J, Bashar MK, Shukla N, et al. 2023.. Large-scale cardiac muscle cell-based coupled oscillator network for vertex coloring problem. . Adv. Intel. Syst. 5::2200356
     [Crossref] [Google Scholar]
  62. 62.
    Webster VA, Chapin KJ, Hawley EL, Patel JM, Akkus O, et al. 2016.. Aplysia californica as a novel source of material for biohybrid robots and organic machines. . In Biomimetic and Biohybrid Systems, LNAI Vol. 9793, ed. N Lepora, A Mura, M Mangan, PFMJ Verschure, M Desmulliez, TJ Prescott , pp. 365–74. Cham, Switz.:: Springer
     [Google Scholar]
  63. 63.
    Webster-Wood VA, Akkus O, Gurkan UA, Chiel HJ, Quinn RD. 2017.. Organismal engineering: toward a robotic taxonomic key for devices using organic materials. . Sci. Robot. 2::eaap9281
     [Crossref] [Google Scholar]
  64. 64.
    Rajabasadi F, Moreno S, Fichna K, Aziz A, Appelhans D, et al. 2022.. Multifunctional 4D-printed sperm-hybrid microcarriers for assisted reproduction. . Adv. Mater. 34:(50):2204257
     [Crossref] [Google Scholar]
  65. 65.
    Akolpoglu MB, Alapan Y, Dogan NO, Baltaci SF, Yasa O, et al. 2022.. Magnetically steerable bacterial microrobots moving in 3D biological matrices for stimuli-responsive cargo delivery. . Sci. Adv. 8:(28):eabo6163
     [Crossref] [Google Scholar]
  66. 66.
    Gwisai T, Mirkhani N, Christiansen MG, Nguyen TT, Ling V, Schuerle S. 2022.. Magnetic torque-driven living microrobots for increased tumor infiltration. . Sci. Robot. 7:(71):eabo0665
     [Crossref] [Google Scholar]
  67. 67.
    Neal DM, Sakar MS, Asada HH. 2013.. Optogenetic control of live skeletal muscles: non-invasive, wireless, and precise activation of muscle tissues. . In 2013 American Control Conference, pp. 1513–18. New York:: IEEE
     [Google Scholar]
  68. 68.
    Dwenger M, Kowalski WJ, Ye F, Yuan F, Tinney JP, et al. 2019.. Chronic optical pacing conditioning of h-iPSC engineered cardiac tissues. . J. Tissue Eng. 10:. https://doi.org/10.1177/2041731419841748
    [Crossref] [Google Scholar]
  69. 69.
    Raman R. 2021.. Engineered neuromuscular actuators for medicine, meat, and machines. . MRS Bull. 46::522–33
     [Crossref] [Google Scholar]
  70. 70.
    Cvetkovic C, Rich MH, Raman R, Kong H, Bashir R. 2017.. A 3D-printed platform for modular neuromuscular motor units. . Microsyst. Nanoeng. 3::17015
     [Crossref] [Google Scholar]
  71. 71.
    Ko E, Yu SJ, Pagan-Diaz GJ, Mahmassani Z, Boppart MD, et al. 2019.. Matrix topography regulates synaptic transmission at the neuromuscular junction. . Adv. Sci. 6::1801521
     [Crossref] [Google Scholar]
  72. 72.
    Andersen J, Revah O, Miura Y, Thorn N, Amin ND, et al. 2020.. Generation of functional human 3D cortico-motor assembloids. . Cell 183::1913–29.e26
     [Crossref] [Google Scholar]
  73. 73.
    Pagan-Diaz GJ, Drnevich J, Ramos-Cruz KP, Sam R, Sengupta P, Bashir R. 2020.. Modulating electrophysiology of motor neural networks via optogenetic stimulation during neurogenesis and synaptogenesis. . Sci. Rep. 10:(1):12460
     [Crossref] [Google Scholar]
  74. 74.
    Adewole DO, Struzyna LA, Burrell JC, Harris JP, Nemes AD, et al. 2021.. Development of optically controlled “living electrodes” with long-projecting axon tracts for a synaptic brain-machine interface. . Sci. Adv. 7:(4):eaay5347
     [Crossref] [Google Scholar]
  75. 75.
    Colón A, Badu-Mensah A, Guo X, Goswami A, Hickman JJ. 2020.. Differentiation of intrafusal fibers from human induced pluripotent stem cells. . ACS Chem. Neurosci. 11:(7):1085–92
     [Crossref] [Google Scholar]
  76. 76.
    Badiola-Mateos M, Hervera A, del Río JA, Samitier J. 2018.. Challenges and future prospects on 3D in-vitro modeling of the neuromuscular circuit. . Front. Bioeng. Biotechnol. 6::194
     [Crossref] [Google Scholar]
  77. 77.
    Badiola-Mateos M, Osaki T, Kamm RD, Samitier J. 2022.. In vitro modelling of human proprioceptive sensory neurons in the neuromuscular system. . Sci. Rep. 12:(1):21318
     [Crossref] [Google Scholar]
  78. 78.
    Guo X, Colon A, Akanda N, Spradling S, Stancescu M, et al. 2017.. Tissue engineering the mechanosensory circuit of the stretch reflex arc with human stem cells: sensory neuron innervation of intrafusal muscle fibers. . Biomaterials 122::179–87
     [Crossref] [Google Scholar]
  79. 79.
    Zhao H, Kim Y, Wang H, Ning X, Xu C, et al. 2021.. Compliant 3D frameworks instrumented with strain sensors for characterization of millimeter-scale engineered muscle tissues. . PNAS 118::e2100077118
     [Crossref] [Google Scholar]
  80. 80.
    Yuk H, Varela CE, Nabzdyk CS, Mao X, Padera RF, et al. 2019.. Dry double-sided tape for adhesion of wet tissues and devices. . Nature 575:(7781):169–74
     [Crossref] [Google Scholar]
  81. 81.
    Yuk H, Lu B, Lin S, Qu K, Xu J, et al. 2020.. 3D printing of conducting polymers. . Nat. Commun. 11:(1):1604
     [Crossref] [Google Scholar]
  82. 82.
    Wang C, Chen X, Wang L, Makihata M, Liu H-C, et al. 2022.. Bioadhesive ultrasound for long-term continuous imaging of diverse organs. . Science 377::517–23
     [Crossref] [Google Scholar]
  83. 83.
    Nam S, Seo BR, Najibi AJ, McNamara SL, Mooney DJ. 2022.. Active tissue adhesive activates mechanosensors and prevents muscle atrophy. . Nat. Mater. 22::249–59
     [Crossref] [Google Scholar]
  84. 84.
    Raman R, Rousseau EB, Wade M, Tong A, Cotler MJ, et al. 2020.. Platform for micro-invasive membrane-free biochemical sampling of brain interstitial fluid. . Sci. Adv. 6:(39):eabb0657
     [Crossref] [Google Scholar]
  85. 85.
    Rios B, Bu A, Sheehan T, Kobeissi H, Kohli S, et al. 2023.. Mechanically programming anisotropy in engineered muscle with actuating extracellular matrices. . Device 1:(4):100097
     [Crossref] [Google Scholar]
  86. 86.
    Sun Han Chang RA, Shanley JF, Kersh ME, Harley BAC. 2020.. Tough and tunable scaffold-hydrogel composite biomaterial for soft-to-hard musculoskeletal tissue interfaces. . Sci. Adv. 6:(34):eabb6763
     [Crossref] [Google Scholar]
  87. 87.
    Raman R, Bashir R. 2015.. Stereolithographic 3D bioprinting for biomedical applications. . In Musculoskeletal Tissue Engineering, ed. Y Chen , pp. 89–121. Amsterdam:: Elsevier
     [Google Scholar]
  88. 88.
    Raman R, Bhaduri B, Mir M, Shkumatov A, Lee MK, et al. 2015.. High-resolution projection microstereolithography for patterning of neovasculature. . Adv. Healthc. Mater. 5:(5):610–19
     [Crossref] [Google Scholar]
  89. 89.
    Raman R, Clay NE, Sen S, Melhem M, Qin E, et al. 2016.. 3D printing enables separation of orthogonal functions within a hydrogel particle. . Biomed. Microdevices 18:(3):49
     [Crossref] [Google Scholar]
  90. 90.
    Hinton TJ, Jallerat Q, Palchesko RN, Park JH, Grodzicki MS, et al. 2015.. Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels. . Sci. Adv. 1:(9):e1500758
     [Crossref] [Google Scholar]
  91. 91.
    Lee A, Hudson AR, Shiwarski DJ, Tashman JW, Hinton TJ, et al. 2019.. 3D bioprinting of collagen to rebuild components of the human heart. . Science 365:(6452):482–87
     [Crossref] [Google Scholar]
  92. 92.
    Skylar-Scott MA, Uzel SGM, Nam LL, Ahrens JH, Truby RL, et al. 2019.. Biomanufacturing of organ-specific tissues with high cellular density and embedded vascular channels. . Sci. Adv. 5:(9):eaaw2459
     [Crossref] [Google Scholar]
  93. 93.
    Ostrovidov S, Salehi S, Costantini M, Suthiwanich K, Ebrahimi M, et al. 2019.. 3D bioprinting in skeletal muscle tissue engineering. . Small 15:(24):e1805530
     [Crossref] [Google Scholar]
  94. 94.
    Mestre R, Patino T, Barceló X, Anand S, Pérez-Jiménez A, Sánchez S. 2018.. Force modulation and adaptability of 3D-bioprinted biological actuators based on skeletal muscle tissue. . Adv. Mater. Technol. 4:(2):1800631
     [Crossref] [Google Scholar]
  95. 95.
    Samandari M, Quint J, Rodríguez-delaRosa A, Sinha I, Pourquié O, Tamayol A. 2022.. Bioinks and bioprinting strategies for skeletal muscle tissue engineering. . Adv. Mater. 34:(12):2105883
     [Crossref] [Google Scholar]
  96. 96.
    Choi YJ, Jun YJ, Kim DY, Yi HG, Chae SH, et al. 2019.. A 3D cell printed muscle construct with tissue-derived bioink for the treatment of volumetric muscle loss. . Biomaterials 206::160–69
     [Crossref] [Google Scholar]
  97. 97.
    Filippi M, Yasa O, Kamm RD, Raman R, Katzschmann RK. 2022.. Will microfluidics enable functionally integrated biohybrid robots?. PNAS 119:(35):e2200741119
     [Crossref] [Google Scholar]
  98. 98.
    Cagol N, Bonani W, Maniglio D, Migliaresi C, Motta A. 2018.. Effect of cryopreservation on cell-laden hydrogels: comparison of different cryoprotectants. . Tissue Eng. Part C Methods 24:(1):20–31
     [Crossref] [Google Scholar]
  99. 99.
    Grant L, Raman R, Cvetkovic C, Ferrall-Fairbanks MC, Pagan-Diaz GJ, et al. 2018.. Long-term cryopreservation and revival of tissue engineered skeletal muscle. . Tissue Eng. Part A 25::1023–36
     [Crossref] [Google Scholar]
  100. 100.
    Gapinske L, Clark L, Caro-Rivera LM, Bashir R. 2023.. Cryopreservation alters tissue structure and improves differentiation of engineered skeletal muscle. . Tissue Eng. Part A 29:(21–22):557–68
     [Crossref] [Google Scholar]
  101. 101.
    de Vries RJ, Tessier SN, Banik PD, Nagpal S, Cronin SEJ, et al. 2019.. Supercooling extends preservation time of human livers. . Nat. Biotechnol. 37:(10):1131–36
     [Crossref] [Google Scholar]
  102. 102.
    Han Z, Rao JS, Gangwar L, Namsrai B-E, Pasek-Allen JL, et al. 2023.. Vitrification and nanowarming enable long-term organ cryopreservation and life-sustaining kidney transplantation in a rat model. . Nat. Commun. 14:(1):3407
     [Crossref] [Google Scholar]
  103. 103.
    Specht L. 2019.. An analysis of culture medium costs and production volumes for cell-based meat. Rep. , Good Food Inst., Washington, DC:, updated Feb. 9, 2020. https://gfi.org/wp-content/uploads/2021/01/clean-meat-production-volume-and-medium-cost.pdf
    [Google Scholar]
  104. 104.
    Idiris A, Tohda H, Kumagai H, Takegawa K. 2010.. Engineering of protein secretion in yeast: strategies and impact on protein production. . Appl. Microbiol. Biotechnol. 86:(2):403–17
     [Crossref] [Google Scholar]
  105. 105.
    Zhang X, Chan FK, Parthasarathy T, Gazzola M. 2019.. Modeling and simulation of complex dynamic musculoskeletal architectures. . Nat. Commun. 10:(1):4825
     [Crossref] [Google Scholar]
  106. 106.
    Naughton N, Sun J, Tekinalp A, Parthasarathy T, Chowdhary G, Gazzola M. 2021.. Elastica: a compliant mechanics environment for soft robotic control. . IEEE Robot. Autom. Lett. 6:(2):3389–96
     [Crossref] [Google Scholar]
  107. 107.
    Wang J, Zhang X, Park J, Park I, Kilicarslan E, et al. 2021.. Computationally assisted design and selection of maneuverable biological walking machines. . Adv. Intel. Syst. 3:(5):2000237
     [Crossref] [Google Scholar]
  108. 108.
    Qian K, Liao AS, Gu S, Webster-Wood VA, Zhang YJ. 2023.. Biomimetic IGA neuron growth modeling with neurite morphometric features and CNN-based prediction. . arXiv:2304.11306 [math.NA]
  109. 109.
    Mohammadzadeh S, Lejeune E. 2023.. SarcGraph: a Python package for analyzing the contractile behavior of pluripotent stem cell-derived cardiomyocytes. . J. Open Source Softw. 8:(85):5322
     [Crossref] [Google Scholar]
  110. 110.
    Das SL, Sutherland BP, Lejeune E, Eyckmans J, Chen CS. 2022.. Mechanical response of cardiac microtissues to acute localized injury. . Am. J. Physiol. Heart Circ. Physiol. 323:(4):H738–48
     [Crossref] [Google Scholar]
  111. 111.
    Hyun I. 2017.. Engineering ethics and self-organizing models of human development: opportunities and challenges. . Cell Stem Cell 21:(6):718–20
     [Crossref] [Google Scholar]
  112. 112.
    Sample M, Boulicault M, Allen C, Bashir R, Hyun I, et al. 2019.. Multi-cellular engineered living systems: building a community around responsible research on emergence. . Biofabrication 11::043001
     [Crossref] [Google Scholar]
  113. 113.
    Blackiston D, Kriegman S, Bongard J, Levin M. 2023.. Biological robots: perspectives on an emerging interdisciplinary field. . Soft Robot. 10:(4):674–86
     [Crossref] [Google Scholar]
  114. 114.
    Cvetkovic C, Ferrall-Fairbanks MC, Ko E, Grant L, Kong H, et al. 2017.. Investigating the life expectancy and proteolytic degradation of engineered skeletal muscle biological machines. . Sci. Rep. 7::3775
     [Crossref] [Google Scholar]
  115. 115.
    Newstetter WC, Behravesh E, Nersessian NJ, Fasse BB. 2010.. Design principles for problem-driven learning laboratories in biomedical engineering education. . Ann. Biomed. Eng. 38:(10):3257–67
     [Crossref] [Google Scholar]
  116. 116.
    Raman R, Mitchell M, Perez-Pinera P, Bashir R, DeStefano L. 2016.. Design and integration of a problem-based biofabrication course into an undergraduate biomedical engineering curriculum. . J. Biol. Eng. 10::10
     [Crossref] [Google Scholar]
  117. 117.
    Brubaker ER, Maturi VR, Karanian BA, Sheppard S, Beach D. 2019.. Integrating mind, hand, and heart: how students are transformed by hands-on designing and making. . Paper presented at the 2019 ASEE Annual Conference & Exposition, Tampa, FL:. https://doi.org/10.18260/1-2--32988
  118. 118.
    Sun W, Feinberg A, Webster-Wood V. 2022.. Continuous fiber extruder for desktop 3D printers toward long fiber embedded hydrogel 3D printing. . HardwareX 11::e00297
     [Crossref] [Google Scholar]
  119. 119.
    Sun W, Tashman JW, Shiwarski DJ, Feinberg AW, Webster-Wood VA. 2022.. Long-fiber embedded hydrogel 3D printing for structural reinforcement. . ACS Biomater. Sci. Eng. 8:(1):303–13
     [Crossref] [Google Scholar]
  120. 120.
    Kobeissi H, Mohammadzadeh S, Lejeune E. 2022.. Enhancing mechanical metamodels with a generative model-based augmented training dataset. . J. Biomech. Eng. 144::121002
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-bioeng-110122-013805
Loading
Biofabrication of Living Actuators
Annual Review of Biomedical Engineering 26, 223 (2024); https://doi.org/10.1146/annurev-bioeng-110122-013805
/content/journals/10.1146/annurev-bioeng-110122-013805
/content/journals/10.1146/annurev-bioeng-110122-013805
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error