AccScience Publishing / IJB / Volume 10 / Issue 6 / DOI: 10.36922/ijb.4371
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RESEARCH ARTICLE

3D-bioprinted in vitro skeletal muscle with pennate fiber architecture to enhance contractile function

Lin Gao1,2* ,  Liuhe Li1,2 ,  Wenze Wu1,2 ,  Junnan Feng1,2 ,  Ziwei Liu1,2 ,  Jiankang He1,2 ,  Dichen Li1,2
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1 State Key Laboratory for Manufacturing System Engineering, School of Mechanical Engineering, Xi’an Jiaotong University, Xi’an, Shaanxi, China
2 National Medical Products Administration (NMPA) Key Laboratory for Research and Evaluation of Additive Manufacturing Medical Devices, Xi’an Jiaotong University, Xi’an, Shaanxi, China
IJB 2024, 10(6), 4371 https://doi.org/10.36922/ijb.4371
Submitted: 29 July 2024 | Accepted: 3 September 2024 | Published: 3 September 2024
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
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Abstract

Skeletal muscle tissue engineering (SMTE) has important research value and broad applicational prospects in areas such as muscle repair, disease modeling, drug testing, and biohybrid robotics. Despite advances in research on engineered skeletal muscles, it remains challenging to improve their functional performance, especially relatively large-sized muscles. Inspired by pennate muscles with a large force output capacity, a novel in vitro skeletal muscle tissue design mimicking the macro and microstructures of the gastrocnemius muscle in frogs was proposed and optimized through simulation. The cell-laden hydrogel was then 3D-bioprinted to fabricate tissues with fusiform geometry and induced microchannels with a pennate angle of 15°. The morphology, cell status, and contraction performance of 3D-bioprinted muscle tissues were evaluated after electrical stimulation, which induced the directional alignment of myotubes. The results indicated that our 3D-bioprinted pennate skeletal muscle tissues exhibited high cell viability (79.89%) and alignment of muscle fibers (51.93%), with a maximum contraction force of 443.085 μN, almost twice the force of 3D-printed parallel muscle tissues in our study. This work will support the exploration of design strategies and rapid manufacturing techniques for next-generation SMTEs with enhanced functional performance.

Graphical abstract
Keywords
Skeletal muscle
3D bioprinting
Pennate muscle
Contraction performance
Funding
This work is supported by the National Natural Science Foundation of China (grant number: 52175276) and the Program for Innovation Team of Shaanxi Province (2023-CX-TD-17).
Conflict of interest
Jiankang He serves as the Editorial Board Member of the journal, but was not in any way involved in the editorial and peer-review process conducted for this paper, directly or indirectly. Other authors declare they have no competing interests.
References
  1. Samandari M, Quint J, Rodríguez-delaRosa A, Sinha I, Pourquié O, Tamayol A. Bioinks and bioprinting strategies for skeletal muscle tissue engineering. Adv Mater. 2022;34(12):2105883. doi: 10.1002/adma.202105883
  2. Derakhshanfar S, Mbeleck R, Xu K, Zhang X, Zhong W, Xing M. 3D bioprinting for biomedical devices and tissue engineering: a review of recent trends and advances. Bioact Mater. 2018;3(2):144-156. doi: 10.1016/j.bioactmat.2017.11.008
  3. Corona BT, Rivera JC, Owens JG, Wenke JC, Rathbone CR. Volumetric muscle loss leads to permanent disability following extremity trauma. J Rehabil Res Dev. 2015;52(7):785-792. doi: 10.1682/jrrd.2014.07.0165
  4. Liu J, Saul D, Böker KO, Ernst J, Lehman W, Schilling AF. Current methods for skeletal muscle tissue repair and regeneration. Biomed Res Int. 2018;11:1984879. doi: 10.1155/2018/1984879
  5. Zhuang P, An J, Chua CK, Tan LP. Bioprinting of 3D in vitro skeletal muscle models: a review. Mater Des. 2020;193:108794. doi: 10.1016/j.matdes.2020.108794
  6. Kwee BJ, Mooney DJ. Biomaterials for skeletal muscle tissue engineering. Curr Opin Biotechnol. 2017;47:16-22. doi: 10.1016/j.copbio.2017.05.003
  7. Gholobova D, Terrie L, Gerard M, Declercq H, Thorrez L. Vascularization of tissue-engineered skeletal muscle constructs. Biomaterials. 2020;235:119708. doi: 10.1016/j.biomaterials.2019.119708
  8. Kang MS, Yu Y, Park R, et al. Highly aligned ternary nanofiber matrices loaded with MXene expedite regeneration of volumetric muscle loss. Nanomicro Lett. 2024;16(1):73. doi: 10.1007/s40820-023-01293-1
  9. Ricotti L, Trimmer B, Feinberg AW, et al. Biohybrid actuators for robotics: a review of devices actuated by living cells. Sci Robot. 2017;2(12):eaaq0495. doi: 10.1126/scirobotics.aaq0495
  10. Ostrovidov S, Hosseini V, Ahadian S, et al. Skeletal muscle tissue engineering: methods to form skeletal myotubes and their applications. Tissue Eng Part B Rev. 2014;20(5):403-436. doi: 10.1089/ten.teb.2013.0534
  11. Rao LJ, Qian Y, Khodabukus A, Ribar T, Bursac N. Engineering human pluripotent stem cells into a functional skeletal muscle tissue. Nat Commun. 2018;9126. doi: 10.1038/s41467-017-02636-4
  12. Martin NRW, Turner MC, Farrington R, Player DJ, Lewis MP. Leucine elicits myotube hypertrophy and enhances maximal contractile force in tissue engineered skeletal muscle in vitro. J Cell Physiol. 2017;232(10):2788-2797. doi: 10.1002/jcp.25960
  13. Madden L, Juhas M, Kraus WE, Truskey GA, Bursac N. Bioengineered human myobundles mimic clinical responses of skeletal muscle to drugs. Elife. 2015;4:e04885. doi: 10.7554/eLife.04885
  14. 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(3):513-517. doi: 10.1039/c0lc00364f
  15. Kamm RD, Bashir R. Creating living cellular machines. Ann of Biome Eng. 2013;42(2):445-459. doi: 10.1007/s10439-013-0902-7
  16. Chan V, Asada HH, Bashir R. Utilization and control of bioactuators across multiple length scales. Lab Chip. 2014;14(4):653-670. doi: 10.1039/c3lc50989c
  17. Ricotti L, Menciassi A. Bio-hybrid muscle cell-based actuators. Biomed Microdevices. 2012;14(6):987-998. doi: 10.1007/s10544-012-9697-9
  18. Zupan M, Ashby MF, Fleck NA. Actuator classification and selection—the development of a database. Adv Eng Mater. 2002;4(12):933-940. doi: 10.1002/adem.200290009
  19. Coyle S, Majidi C, LeDuc P, Hsia KJ. Bio-inspired soft robotics: material selection, actuation, and design. Extreme Mech Lett. 2018;22:51-59. doi: 10.1016/j.eml.2018.05.003
  20. Kim Y, Yang Y, Zhang X, et al. Remote control of muscle-driven miniature robots with battery-free wireless optoelectronics. Sci Robot. 2023;8(74):eadd1053. doi: 10.1126/scirobotics.add1053
  21. Morimoto Y, Onoe H, Takeuchi S. Biohybrid robot powered by an antagonistic pair of skeletal muscle tissues. Sci Robot. 2018;3(18):eaat4440. doi: 10.1126/scirobotics.aat4440
  22. Gao GF, Cui XF. Three-dimensional bioprinting in tissue engineering and regenerative medicine. Biotechnol Lett. 2016;38(2):203-211. doi: 10.1007/s10529-015-1975-1
  23. Kim JH, Seol YJ, Ko IK, et al. 3D bioprinted human skeletal muscle constructs for muscle function restoration. Sci Rep. 2018;8(1):12307. doi: 10.1038/s41598-018-29968-5
  24. Kang HW, Lee SJ, Ko IK, Kengla C, Yoo JJ, Atala A. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol. 2016;34(3):312-319. doi: 10.1038/nbt.3413
  25. Kim JH, Kim I, Seol YJ, et al. Neural cell integration into 3D bioprinted skeletal muscle constructs accelerates restoration of muscle function. Nat Commun. 2020;11(1)1025. doi: 10.1038/s41467-020-14930-9
  26. Bian WN, Liau B, Badie N, Bursac N. Mesoscopic hydrogel molding to control the 3D geometry of bioartificial muscle tissues. Nat Protoc. 2009;4(10):1522-1534. doi: 10.1038/nprot.2009.155
  27. Tanaka Y, Noguchi Y, Yalikun Y, Kamamichi N. Earthworm muscle driven bio-micropump. Sens Actuator B Chem. 2017;242:1186-1192. doi: 10.1016/j.snb.2016.09.123
  28. Liu L, Zhang C, Wang W, Xi N, Wang Y. Regulation of C2C12 differentiation and control of the beating dynamics of contractile cells for a muscle-driven biosyncretic crawler by electrical stimulation. Soft Robot. 2018;5(6):748-760. doi: 10.1089/soro.2018.0017
  29. Mita H, Mizuno Y, Tanaka H, Fujie T. UV laser-processed microstructure for building biohybrid actuators with anisotropic movement. Biofabrication. 2024;16(2):025010. doi: 10.1088/1758-5090/ad2080
  30. Roberts TJ, Eng CM, Sleboda DA, et al. The multi-scale, three-dimensional nature of skeletal muscle contraction. Physiology (Bethesda). 2019;34(6):402-408. doi: 10.1152/physiol.00023.2019
  31. Mestre R, Patiño T, Barceló X, Anand S, Pérez‐Jiménez A, Sánchez S. Force modulation and adaptability of 3d‐bioprinted biological actuators based on skeletal muscle tissue. Adv Mater Technol. 2018;4(2):1800631. doi: 10.1002/admt.201800631
  32. Markstedt K, Mantas A, Tournier I, Martínez Ávila H, Hägg D, Gatenholm P. 3D bioprinting human chondrocytes with nanocellulose–alginate bioink for cartilage tissue engineering applications. Biomacromolecules. 2015; 16(5):1489-1496. doi: 10.1021/acs.biomac.5b00188
  33. Kolesky DB, Truby RL, Gladman AS, Busbee TA, Homan KA, Lewis JA. 3D bioprinting of vascularized, heterogeneous cell‐laden tissue constructs. Adv Mater. 2014; 26(19):3124-3130. doi: 10.1002/adma.201305506
  34. Cernencu AI, Lungu A, Dragusin DM, et al. 3D bioprinting of biosynthetic nanocellulose-filled gelma inks highly reliable for soft tissue-oriented constructs. Materials. 2021;14(17):4891. doi: 10.3390/ma14174891
  35. Mao M, He J, Li Z, Han K, Li D. Multi-directional cellular alignment in 3D guided by electrohydrodynamically-printed microlattices. Acta Biomater. 2020;101:141-151. doi: 10.1016/j.actbio.2019.10.028
  36. Raman R, Cvetkovic C, Uzel SGM, et al. Optogenetic skeletal muscle-powered adaptive biological machines. Proc Natl Acad Sci. 2016;113(13):3497-3502. doi: 10.1073/pnas.1516139113
  37. Mestre R, Fuentes J, Lefaix L, et al. Improved performance of biohybrid muscle‐based bio‐bots doped with piezoelectric boron nitride nanotubes. Adv Mater Technol. 2022;8(2):2200505. doi: 10.1002/admt.202200505
  38. Cvetkovic C, Raman R, Chan V, et al. Three-dimensionally printed biological machines powered by skeletal muscle. Proc Natl Acad Sci U S A. 2014;111(28):10125-10130. doi: 10.1073/pnas.1401577111
  39. Pagan‐Diaz GJ, Zhang X, Grant L, et al. Simulation and fabrication of stronger, larger, and faster walking biohybrid machines. Adv Funct Mater. 2018;28(23):1801145. doi: 10.1002/adfm.201801145
  40. Wang J, Wang Y, Kim Y, Yu T, Bashir R. Multi-actuator light-controlled biological robots. APL Bioeng. 2022;6(3):036103. doi: 10.1063/5.0091507
  41. Choi YJ, Kim TG, Jeong J, et al. 3D cell printing of functional skeletal muscle constructs using skeletal muscle-derived bioink. Adv Healthc Mater. 2016;5(20):2636-2645. doi: 10.1002/adhm.201600483

 

 

 



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International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing
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