Efficient myotube formation in 3D bioprinted tissue construct by biochemical and topographical cues
Open accessAbstract
Biochemical and biophysical cues directly affect cell morphology, adhesion, proliferation, and phenotype, as well as differentiation; thus, they have been commonly utilized for designing and developing biomaterial systems for tissue engineering applications. To bioengineer skeletal muscle tissues, the efficient and stable formation of aligned fibrous multinucleated myotubes is essential. To achieve this goal, we employed a decellularized extracellular matrix (dECM) as a biochemical component and a modified three-dimensional (3D) cell-printing process to produce an in situ uniaxially aligned/micro-topographical structure. The dECM was derived from the decellularization of porcine skeletal muscles and chemically modified by methacrylate process to enhance mechanical stability. By using this ECM-based material and the 3D printing capability, we were able to produce a cell-laden dECM-based structure with unique topographical cues. The myoblasts (C2C12 cell line) laden in the printed structure were aligned and differentiated with a high degree of myotube formation, owing to the synergistic effect of the skeletal muscle-specific biochemical and topographical cues. In particular, the increase of the gene-expression levels of the dECM structure with topographical cues was approximately 1.5-1.8-fold compared with those of a gelatin methacrylate (GelMA)-based structure with the same topographical cues and a dECM-based structure without topographical cues. According to these in vitro cellular responses, the 3D printed dECM-based structures with topographical cues have the potential for bioengineering functional skeletal muscle tissues, and this strategy can be extended for many musculoskeletal tissues, such as tendons and ligaments and utilized for developing in vitro tissue-on-a-chip models in drug screening and development.
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Myoblast alignment and differentiation are crucial for myotube formation.
“This process ensures myoblast alignment and differentiation, crucial for myotube formation, by employing UV light for crosslinking and removing PVA post‐printing.[ 158 ]”
From Bioactive scaffolds for tissue engineering: A review of decellularized extracellular matrix applications and innovations (2025) · cites this paper as [158]
The bioprinting process for methacrylated skeletal muscle dECM with sacrificial PVA ensures myoblast alignment and differentiation.
“This process ensures myoblast alignment and differentiation, crucial for myotube formation, by employing UV light for crosslinking and removing PVA post‐printing.[ 158 ]”
From Bioactive scaffolds for tissue engineering: A review of decellularized extracellular matrix applications and innovations (2025) · cites this paper as [158]
Methacrylated dECM from porcine skeletal muscle combined with sacrificial fibrillated PVA has been bioprinted into aligned skeletal muscle structures.
“Similarly, methacrylated dECM from porcine skeletal muscle, when combined with sacrificial fibrillated PVA, has been bioprinted into aligned skeletal muscle structures.”
From Bioactive scaffolds for tissue engineering: A review of decellularized extracellular matrix applications and innovations (2025) · cites this paper as [158]
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3D bioprinting of tissues and organs
Murphy, S. V., & Atala, A. (2014) · Nature Biotechnology · doi:10.1038/nbt.2958 · Cited by 7,034 · see citing works
Self-citationAn overview of tissue and whole organ decellularization processes
Crapo, P. M., Gilbert, T. W., & Badylak, S. F. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.01.057 · Cited by 3,591 · see citing works
A 3D bioprinting system to produce human-scale tissue constructs with structural integrity
Kang, H.-W., Lee, S. J., Ko, I. K., Kengla, C., Yoo, J. J., & Atala, A. (2016) · Nature Biotechnology · doi:10.1038/nbt.3413 · Cited by 2,622 · see citing works
Self-citationDetermination of free amino groups in proteins by trinitrobenzenesulfonic acid
Habeeb, A. F. S. A. (1966) · Analytical Biochemistry · doi:10.1016/0003-2697(66)90275-2 · Cited by 2,040 · see citing works
Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink
Pati, F., Jang, J., Ha, D.-H., Won Kim, S., Rhie, J.-W., Shim, J.-H., Kim, D.-H., & Cho, D.-W. (2014) · Nature Communications · doi:10.1038/ncomms4935 · Cited by 1,904 · see citing works
Extracellular matrix as a biological scaffold material: Structure and function
BADYLAK, S., FREYTES, D., & GILBERT, T. (2009) · Acta Biomaterialia · doi:10.1016/j.actbio.2008.09.013 · Cited by 1,671 · see citing works
Structural and Rheological Properties of Methacrylamide Modified Gelatin Hydrogels
Van Den Bulcke, A. I., Bogdanov, B., De Rooze, N., Schacht, E. H., Cornelissen, M., & Berghmans, H. (2000) · Biomacromolecules · doi:10.1021/bm990017d · Cited by 1,536 · see citing works
Reprint of: Extracellular matrix as a biological scaffold material: Structure and function
Badylak, S. F., Freytes, D. O., & Gilbert, T. W. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.07.016 · Cited by 1,361 · see citing works
Printing and Prototyping of Tissues and Scaffolds
Derby, B. (2012) · Science · doi:10.1126/science.1226340 · Cited by 1,108 · see citing works
Leong, K. F., Cheah, C. M., & Chua, C. K. (2003) · Biomaterials · doi:10.1016/s0142-9612(03)00030-9 · Cited by 1,077 · see citing works
Ouyang, L., Yao, R., Zhao, Y., & Sun, W. (2016) · Biofabrication · doi:10.1088/1758-5090/8/3/035020 · Cited by 1,052 · see citing works
3D Printing of Personalized Thick and Perfusable Cardiac Patches and Hearts
Noor, N., Shapira, A., Edri, R., Gal, I., Wertheim, L., & Dvir, T. (2019) · Advanced Science · doi:10.1002/advs.201900344 · Cited by 1,042 · see citing works
The extracellular matrix as a biologic scaffold material
Badylak, S. F. (2007) · Biomaterials · doi:10.1016/j.biomaterials.2007.04.043 · Cited by 1,022 · see citing works
Yin, J., Yan, M., Wang, Y., Fu, J., & Suo, H. (2018) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.7b16059 · Cited by 602 · see citing works
A Multimaterial Bioink Method for 3D Printing Tunable, Cell‐Compatible Hydrogels
Rutz, A. L., Hyland, K. E., Jakus, A. E., Burghardt, W. R., & Shah, R. N. (2015) · Advanced Materials · doi:10.1002/adma.201405076 · Cited by 573 · see citing works
Extracellular matrix scaffolds for cartilage and bone regeneration
Benders, K. E. M., van Weeren, P. R., Badylak, S. F., Saris, D. B. F., Dhert, W. J. A., & Malda, J. (2013) · Trends in biotechnology · doi:10.1016/j.tibtech.2012.12.004 · Cited by 539 · see citing works
Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering
Singelyn, J. M., DeQuach, J. A., Seif-Naraghi, S. B., Littlefield, R. B., Schup-Magoffin, P. J., & Christman, K. L. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.06.045 · Cited by 535 · see citing works
Ouyang, L., Highley, C. B., Sun, W., & Burdick, J. A. (2016) · Advanced Materials · doi:10.1002/adma.201604983 · Cited by 525 · see citing works
The Basement Membrane/Basal Lamina of Skeletal Muscle
Sanes, J. R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.r200027200 · Cited by 471 · see citing works
Muscle injuries: optimising recovery
Järvinen, T. A. H., Järvinen, T. L. N., Kääriäinen, M., Äärimaa, V., Vaittinen, S., Kalimo, H., & Järvinen, M. (2007) · Best Practice & Research Clinical Rheumatology · doi:10.1016/j.berh.2006.12.004 · Cited by 440 · see citing works
Skardal, A., Devarasetty, M., Kang, H.-W., Mead, I., Bishop, C., Shupe, T., Lee, S. J., Jackson, J., Yoo, J., Soker, S., et al. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.07.030 · Cited by 428 · see citing works
Self-citationNavaei, A., Saini, H., Christenson, W., Sullivan, R., Ros, R., & Nikkhah, M. (2016) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.05.027 · Cited by 391 · see citing works
Aqueous Two‐Phase Emulsion Bioink‐Enabled 3D Bioprinting of Porous Hydrogels
Ying, G., Jiang, N., Maharjan, S., Yin, Y., Chai, R., Cao, X., Yang, J., Miri, A. K., Hassan, S., & Zhang, Y. S. (2018) · Advanced Materials · doi:10.1002/adma.201805460 · Cited by 378 · see citing works
Vascular endothelial growth factor stimulates skeletal muscle regeneration in Vivo
Arsic, N., Zacchigna, S., Zentilin, L., Ramirez‐Correa, G. A., Pattarini, L., Salvi, A., Sinagra, G., & Giacca, M. (2004) · Molecular Therapy · doi:10.1016/j.ymthe.2004.08.007 · Cited by 349 · see citing works
Tonkin, J. N., Temmerman, L., Sampson, R., Gallego-Colon, E., Barberi, L., Bilbao, D., Schneider, M., Musarò, A., & Rosenthal, N. (2015) · Molecular Therapy · doi:10.1038/mt.2015.66 · Cited by 322 · see citing works
Choi, Y., Jun, Y. J., Kim, D., Yi, H., Chae, S.-H., Kang, J.-S., Lee, J., Gao, G., Kong, J., Jang, J., et al. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.03.036 · Cited by 319 · see citing works
Self-citationRapid formation of functional muscle in vitro using fibrin gels
Huang, Y., Dennis, R. G., Larkin, L. M., & Baar, K. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00273.2004 · Cited by 317 · see citing works
Organ-Derived Decellularized Extracellular Matrix: A Game Changer for Bioink Manufacturing?
Choudhury, D., Tun, H. W., Wang, T., & Naing, M. W. (2018) · Trends in biotechnology · doi:10.1016/j.tibtech.2018.03.003 · Cited by 265 · see citing works
A Photo‐Crosslinkable Kidney ECM‐Derived Bioink Accelerates Renal Tissue Formation
Ali, M., PR, A. K., Yoo, J. J., Zahran, F., Atala, A., & Lee, S. J. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201800992 · Cited by 264 · see citing works
Self-citationEngineered Contractile Skeletal Muscle Tissue on a Microgrooved Methacrylated Gelatin Substrate
Hosseini, V., Ahadian, S., Ostrovidov, S., Camci‐Unal, G., Chen, S., Kaji, H., Ramalingam, M., & Khademhosseini, A. (2012) · Tissue Engineering Part A · doi:10.1089/ten.tea.2012.0181 · Cited by 242 · see citing works
Lee, J. S., Shin, J., Park, H.-M., Kim, Y.-G., Kim, B.-G., Oh, J.-W., & Cho, S.-W. (2014) · Biomacromolecules · doi:10.1021/bm4015039 · Cited by 236 · see citing works
Self-citationThe bone morphogenetic protein axis is a positive regulator of skeletal muscle mass
Winbanks, C. E., Chen, J. L., Qian, H., Liu, Y., Bernardo, B. C., Beyer, C., Watt, K. I., Thomson, R. E., Connor, T., Turner, B. J., et al. (2013) · Journal of Cell Biology · doi:10.1083/jcb.201211134 · Cited by 225 · see citing works
Naturally derived and synthetic scaffolds for skeletal muscle reconstruction
Wolf, M. T., Dearth, C. L., Sonnenberg, S. B., Loboa, E., & Badylak, S. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.08.011 · Cited by 214 · see citing works
Cytokines in exertion-induced skeletal muscle injury
Cannon, J., & Pierre, B. S. S. (1998) · Molecular and Cellular Biochemistry · doi:10.1023/a:1006828425418 · Cited by 191 · see citing works
Kim, Y. B., Lee, H., & Kim, G. (2016) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.6b11669 · Cited by 179 · see citing works
Self-citationCurrent opportunities and challenges in skeletal muscle tissue engineering
Koning, M., Harmsen, M. C., van Luyn, M. J. A., & Werker, P. M. N. (2009) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.190 · Cited by 162 · see citing works
Human versus porcine tissue sourcing for an injectable myocardial matrix hydrogel
Johnson, T. D., DeQuach, J. A., Gaetani, R., Ungerleider, J. L., Elhag, D., Nigam, V., Behfar, A., & Christman, K. L. (2014) · Biomaterials Science · doi:10.1039/c3bm60283d · Cited by 121 · see citing works
Crosslinkable Hydrogels Derived from Cartilage, Meniscus, and Tendon Tissue
Visser, J., Levett, P. A., Moller, N. C. R. T., Besems, J., Boere, K. W. M., van Rijen, M. H. P., de Grauw, J. C., Dhert, W. J. A., van Weeren, P. R., & Malda, J. (2015) · Tissue Engineering Part A · doi:10.1089/ten.tea.2014.0362 · Cited by 114 · see citing works
Jana, S., Leung, M. C., Chang, J., & Zhang, M. (2014) · Biofabrication · doi:10.1088/1758-5082/6/3/035012 · Cited by 114 · see citing works
Collagen architecture in pregnancy-induced protection from breast cancer
Maller, O., Hansen, K. C., Lyons, T. R., Acerbi, I., Weaver, V. M., Prekeris, R., Tan, A. C., & Schedin, P. S. (2013) · Journal of Cell Science · doi:10.1242/jcs.121590 · Cited by 114 · see citing works
3D‐Printed Biomimetic Scaffold Simulating Microfibril Muscle Structure
Kim, W.-J., Kim, M., & Kim, G. (2018) · Advanced Functional Materials · doi:10.1002/adfm.201800405 · Cited by 106 · see citing works
Self-citationDevelopment of Bioink from Decellularized Tendon Extracellular Matrix for 3D Bioprinting
Toprakhisar, B., Nadernezhad, A., Bakirci, E., Khani, N., Skvortsov, G. A., & Koc, B. (2018) · Macromolecular Bioscience · doi:10.1002/mabi.201800024 · Cited by 101 · see citing works
Vascular tissue engineering: biodegradable scaffold platforms to promote angiogenesis
Serbo, J. V., & Gerecht, S. (2013) · Stem Cell Research & Therapy · doi:10.1186/scrt156 · Cited by 97 · see citing works
Duffy, R. M., Sun, Y., & Feinberg, A. W. (2016) · Annals of Biomedical Engineering · doi:10.1007/s10439-016-1592-8 · Cited by 92 · see citing works
Linker proteins restore basement membrane and correct LAMA2 -related muscular dystrophy in mice
Reinhard, J. R., Lin, S., McKee, K. K., Meinen, S., Crosson, S. C., Sury, M., Hobbs, S., Maier, G., Yurchenco, P. D., & Rüegg, M. A. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aal4649 · Cited by 90 · see citing works
Snapshot: Biologic Scaffolds For Constructive Tissue Remodeling
Badylak, S. F., Brown, B. N., Gilbert, T. W., Daly, K. A., Huber, A., & Turner, N. J. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.09.018 · Cited by 75 · see citing works
Lyoo, W. S., Kim, J. H., Choi, J. H., Kim, B. C., & Blackwell, J. (2001) · Macromolecules · doi:10.1021/ma001338g · Cited by 52 · see citing works
Lyoo, W. S., & Ha, W. S. (1999) · Polymer · doi:10.1016/s0032-3861(98)00066-4 · Cited by 45 · see citing works
Kömez, A., Baran, E. T., Erdem, Ü., Hasırcı, N., & Hasırcı, V. (2016) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.35756 · Cited by 42 · see citing works
Kim, M., Kim, W.-J., & Kim, G. (2017) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.7b14192 · Cited by 40 · see citing works
Self-citationDirecting Mesenchymal Stem Cells with Gold Nanowire Arrays
Zhou, Q., Zhao, Z., Zhou, Z., Zhang, G., Chiechi, R. C., & van Rijn, P. (2018) · Advanced Materials Interfaces · doi:10.1002/admi.201800334 · Cited by 40 · see citing works
Choi, Y.-J., Park, S. J., Yi, H.-G., Lee, H., Kim, D. S., & Cho, D.-W. (2018) · Journal of Materials Chemistry B · doi:10.1039/c8tb01475b · Cited by 39 · see citing works
Self-citationThe Decellularized Extracellular Matrix in Regenerative Medicine
Rijal, G. (2017) · Regenerative Medicine · doi:10.2217/rme-2017-0046 · Cited by 34 · see citing works
Lagrange, M., Boulade-Ladame, C., Mailly, L., Weiss, É., Orfanoudakis, G., & Deryckère, F. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.07.040 · Cited by 27 · see citing works
Effect of growth hormone-secreting tumours on skeletal muscle cellularity in the rat
McCusker, R. H., & Campion, D. R. (1986) · Journal of Endocrinology · doi:10.1677/joe.0.1110279 · Cited by 21 · see citing works
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Kim, B. S., Das, S., Jang, J., & Cho, D.-W. (2020) · Chemical Reviews · doi:10.1021/acs.chemrev.9b00808 · Cited by 465 · see citing works
Extracellular matrix: an important regulator of cell functions and skeletal muscle development
Zhang, W., Liu, Y., & Zhang, H. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00579-4 · Cited by 289 · see citing works
Golebiowska, A. A., Intravaia, J. T., Sathe, V. M., Kumbar, S. G., & Nukavarapu, S. P. (2024) · Bioactive Materials · doi:10.1016/j.bioactmat.2023.09.017 · Cited by 236 · see citing works
Designing Decellularized Extracellular Matrix‐Based Bioinks for 3D Bioprinting
Abaci, A., & Güvendiren, M. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.202000734 · Cited by 181 · see citing works
3D bioprinting: current status and trends—a guide to the literature and industrial practice
Santoni, S., Gugliandolo, S. G., Sponchioni, M., Moscatelli, D., & Colosimo, B. M. (2021) · Bio-Design and Manufacturing · doi:10.1007/s42242-021-00165-0 · Cited by 172 · see citing works
Hydrogel-Based Fiber Biofabrication Techniques for Skeletal Muscle Tissue Engineering
Volpi, M., Paradiso, A., Costantini, M., & Święszkowski, W. (2022) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.1c01145 · Cited by 164 · see citing works
Lee, J., Hong, J., Kim, W., & Kim, G. H. (2020) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2020.116914 · Cited by 157 · see citing works
Self-citationVisscher, D. O., Lee, H., van Zuijlen, P. P. M., Helder, M. N., Atala, A., Yoo, J. J., & Lee, S. J. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.11.029 · Cited by 154 · see citing works
Self-citationBioinks and Bioprinting Strategies for Skeletal Muscle Tissue Engineering
Samandari, M., Quint, J. P., Rodríguez‐delaRosa, A., Sinha, I., Pourquié, O., & Tamayol, A. (2021) · Advanced Materials · doi:10.1002/adma.202105883 · Cited by 147 · see citing works
Liu, J., Song, Q., Yin, W., Li, C., An, N., Le, Y., Wang, Q., Feng, Y., Hu, Y., & Wang, Y. (2025) · Exploration · doi:10.1002/exp.20230078 · Cited by 140 · see citing works
Wang, D., Guo, Y., Zhu, J., Liu, F., Xue, Y., Huang, Y. H., Zhu, B., Wu, D., Pan, H., Gong, T., et al. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2022.06.036 · Cited by 131 · see citing works
In-vitro meat: a promising solution for sustainability of meat sector
Kumar, P., Sharma, N., Sharma, S., Mehta, N. R., Verma, A. K., Chemmalar, S., & Sazili, A. Q. (2021) · Journal of Animal Science and Technology · doi:10.5187/jast.2021.e85 · Cited by 130 · see citing works
Zhang, Y., Sheng, R., Chen, J., Wang, H., Zhu, Y. S., Cao, Z., Zhao, X., Wang, Z., Liu, C., Chen, Z., et al. (2023) · Advanced Materials · doi:10.1002/adma.202210517 · Cited by 128 · see citing works
Functional acellular matrix for tissue repair
Wang, B., Qinglai, T., Yang, Q., Li, M., Zeng, S., Yang, X., Xiao, Z., Tong, X., Lei, L., & Li, S. (2022) · Materials Today Bio · doi:10.1016/j.mtbio.2022.100530 · Cited by 111 · see citing works
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Hwangbo, H., Lee, H., Jin, E., Lee, J., Jo, Y., Ryu, D., & Kim, G. (2021) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.06.031 · Cited by 108 · see citing works
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Zhang, Q., Chang, C., Qian, C., Xiao, W., Zhu, H., Guo, J. X., Meng, Z., Cui, W., & Ge, Z. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.02.043 · Cited by 107 · see citing works
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Lee, S. J., Jeong, W., & Atala, A. (2024) · Advanced Materials · doi:10.1002/adma.202408032 · Cited by 102 · see citing works
Self-citationLu, K., Li, K., Zhang, M., Fang, Z., Wu, P., Feng, L., Deng, K., Yu, C., Deng, Y., Xiao, Y., et al. (2021) · Chemical Engineering Journal · doi:10.1016/j.cej.2021.130429 · Cited by 94 · see citing works
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Zhang, H., Wang, Y., Zheng, Z., Wei, X., Chen, L., Wu, Y., Huang, W., & Yang, L. (2023) · Theranostics · doi:10.7150/thno.81785 · Cited by 94 · see citing works
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Ramos, T., & Moroni, L. (2019) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2019.0344 · Cited by 90 · see citing works
Fan, J., Dorcheh, K. A., Vaziri, A. S., Kazemi-Aghdam, F., Rafieyan, S., Sohrabinejad, M., Ghorbani, M., Adib, F. R., Ghasemi, Z., Klavins, K., et al. (2022) · Polymers · doi:10.3390/polym14102097 · Cited by 89 · see citing works
Huo, Y., Xu, Y. F., Wu, X., Gao, E., Zhan, A., Chen, Y., Zhang, Y., Hua, Y., Święszkowski, W., Zhang, Y. S., et al. (2022) · Advanced Science · doi:10.1002/advs.202202181 · Cited by 87 · see citing works
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Costa, J. B., Park, J., Jorgensen, A. M., Silva‐Correia, J., Reis, R. L., Oliveira, J. M., Atala, A., Yoo, J. J., & Lee, S. J. (2020) · Chemistry of Materials · doi:10.1021/acs.chemmater.0c03556 · Cited by 66 · see citing works
Self-citationCurrent Trends on Protein Driven Bioinks for 3D Printing
Veiga, A., Silva, I. V., Duarte, M. M., & Oliveira, A. L. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13091444 · Cited by 67 · see citing works
Current Strategies for the Regeneration of Skeletal Muscle Tissue
Alarçın, E., Bal‐Öztürk, A., Avcı, H., Ghorbanpoor, H., Güzel, F. D., Akpek, A., YEŞİLTAŞ, G., Çanak-Ipek, T., & Avci‐Adali, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115929 · Cited by 63 · see citing works
Chen, H., Fei, F., Li, X., Nie, Z., Zhou, D., Liu, L., Zhang, J., Zhang, H., Fei, Z., & Xu, T. (2021) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.03.019 · Cited by 61 · see citing works
Decellularized kidney extracellular matrix bioinks recapitulate renal 3D microenvironment in vitro
Sobreiro‐Almeida, R., Gómez‐Florit, M., Quinteira, R., Reis, R. L., Gomes, M. E., & Neves, N. M. (2021) · Biofabrication · doi:10.1088/1758-5090/ac0fca · Cited by 58 · see citing works
Thangadurai, M., Ajith, A., Budharaju, H., Sethuraman, S., & Sundaramurthi, D. (2022) · Biomaterials Advances · doi:10.1016/j.bioadv.2022.213135 · Cited by 58 · see citing works
Boso, D., Maghin, E., Carraro, E., Giagante, M., Pavan, P. G., & Piccoli, M. (2020) · Materials · doi:10.3390/ma13112483 · Cited by 57 · see citing works
Xue, Y., Li, J., Jiang, T., Han, Q., Jing, Y., Bai, S., & Yan, X. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202302180 · Cited by 55 · see citing works
Idaszek, J., Volpi, M., Paradiso, A., Quoc, M. N., Górecka, Ż., Klak, M., Tymicki, G., Berman, A., Wierzbicki, M., Jaworski, S., et al. (2021) · Bioprinting · doi:10.1016/j.bprint.2021.e00163 · Cited by 54 · see citing works
Multiscale Hierarchical Architecture‐Based Bioactive Scaffolds for Versatile Tissue Engineering
Ma, H., Yang, C., Ma, Z., Wei, X., Younis, M. R., Wang, H., Li, W., Wang, Z., Wang, W., Luo, Y., et al. (2022) · Advanced Healthcare Materials · doi:10.1002/adhm.202102837 · Cited by 54 · see citing works
Randhawa, A., Dutta, S. D., Ganguly, K., Patel, D. K., Patil, T. V., & Lim, K. (2022) · Macromolecular Bioscience · doi:10.1002/mabi.202200278 · Cited by 54 · see citing works
Advanced Techniques for Skeletal Muscle Tissue Engineering and Regeneration
Kang, M. S., Lee, S. H., Park, W. J., Lee, J. E., Kim, B., & Han, D. (2020) · Bioengineering · doi:10.3390/bioengineering7030099 · Cited by 54 · see citing works
Self-citationLee, H., Kim, W.-J., Lee, J., Park, K.-S., Yoo, J. J., Atala, A., Kim, G., & Lee, S. J. (2021) · Applied Physics Reviews · doi:10.1063/5.0039639 · Cited by 54 · see citing works
Self-citationGosselin, M. R. F., Mournetas, V., Borczyk, M., Verma, S., Occhipinti, A., Róg, J., Bożycki, Ł., Korostyński, M., Robson, S. C., Angione, C., et al. (2022) · eLife · doi:10.7554/elife.75521 · Cited by 53 · see citing works
Recent trends in 3D bioprinting technology for skeletal muscle regeneration
Sabetkish, S., Currie, P. D., & Meagher, L. (2024) · Acta Biomaterialia · doi:10.1016/j.actbio.2024.04.038 · Cited by 53 · see citing works
Luo, C., Xie, R., Zhang, J., Liu, Y., Li, Z., Zhang, Y., Zhang, X., Yuan, T., Chen, Y., & Fan, W. (2020) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2020.0053 · Cited by 52 · see citing works
Kim, D., Kim, M., Lee, J., & Jang, J. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.764682 · Cited by 52 · see citing works
Self-citationBiomaterials‐Based Technologies in Skeletal Muscle Tissue Engineering
Luo, W., Zhang, H., Wan, R., Cai, Y., Liu, Y., Wu, Y., Yang, Y., Chen, J., Zhang, D., Luo, Z., et al. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202304196 · Cited by 53 · see citing works
Scalable macroporous hydrogels enhance stem cell treatment of volumetric muscle loss
Eugenis, I., Wu, D., Hu, C., Chiang, G., Huang, N. F., & Rando, T. A. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121818 · Cited by 50 · see citing works
Bioinks for 3D Bioprinting: A Scientometric Analysis of Two Decades of Progress
Pedroza-González, S. C., Rodríguez-Salvador, M., Pérez-Benítez, B. E., Álvarez, M. M., & Santiago, G. T. (2021) · International Journal of Bioprinting · doi:10.18063/ijb.v7i2.337 · Cited by 51 · see citing works
Zhe, M., Wu, X., Yu, P., Xu, J., Liu, M., Yang, G., Xiang, Z., Xing, F., & Ritz, U. (2023) · Materials · doi:10.3390/ma16083197 · Cited by 50 · see citing works
Bioengineered in vitro skeletal muscles as new tools for muscular dystrophies preclinical studies
Fernández‐Costa, J. M., Fernández‐Garibay, X., Velasco‐Mallorquí, F., & Ramón‐Azcón, J. (2021) · Journal of Tissue Engineering · doi:10.1177/2041731420981339 · Cited by 48 · see citing works
3D in vitro models of skeletal muscle: myopshere, myobundle and bioprinted muscle construct
Dessauge, F., Schleder, C., Perruchot, M., & Rouger, K. (2021) · Veterinary Research · doi:10.1186/s13567-021-00942-w · Cited by 48 · see citing works
Decellularization Strategies for Regenerating Cardiac and Skeletal Muscle Tissues
Tan, Y. H., Helms, H. R., & Nakayama, K. H. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.831300 · Cited by 45 · see citing works
Biomimetic hydrogel derived from decellularized dermal matrix facilitates skin wounds healing
Yu, Y., Xiao, H., Tang, G., Wang, H., Shen, J., Sun, Y., Wang, S., Kong, W., Chai, Y., Liu, X., et al. (2023) · Materials Today Bio · doi:10.1016/j.mtbio.2023.100725 · Cited by 47 · see citing works
Recent Advances in Decellularized Matrix-Derived Materials for Bioink and 3D Bioprinting
Liu, H., Gong, Y., Zhang, K., Ke, S., Wang, Y., Wang, J., & Wang, H. (2023) · Gels · doi:10.3390/gels9030195 · Cited by 49 · see citing works
Hua, Y., Huo, Y., Bai, B., Hao, J., Hu, G., Ci, Z., Wu, X., Yu, M., Wang, X., Chen, H., et al. (2022) · Materials Today Bio · doi:10.1016/j.mtbio.2022.100489 · Cited by 45 · see citing works
Myoblast 3D bioprinting to burst in vitro skeletal muscle differentiation
Ronzoni, F., Aliberti, F., Scocozza, F., Benedetti, L., Auricchio, F., Sampaolesi, M., Angelis, M. G. C. D., Redwan, I. N., Ceccarelli, G., & Conti, M. (2022) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.3293 · Cited by 43 · see citing works
3D printing topographic cues for cell contact guidance: A review
Lai, H., Gong, B., Yin, J., & Qian, J. W. (2022) · Materials & Design · doi:10.1016/j.matdes.2022.110663 · Cited by 43 · see citing works
Adhikari, J., Roy, A., Chanda, A., Gouripriya, D. A., Thomas, S., Ghosh, M., Kim, J., & Saha, P. (2022) · Biomaterials Science · doi:10.1039/d2bm01499h · Cited by 43 · see citing works
Bolívar‐Monsalve, E. J., Ceballos‐González, C. F., Chávez-Madero, C., de la Cruz‐Rivas, B. G., Velásquez‐Marín, S., Mora‐Godínez, S., Reyes‐Cortés, L. M., Khademhosseini, A., Weiss, P. S., Samandari, M., et al. (2022) · Advanced Healthcare Materials · doi:10.1002/adhm.202200448 · Cited by 41 · see citing works
Yeleswarapu, S., Dash, A., Chameettachal, S., & Pati, F. (2023) · Biomaterials Advances · doi:10.1016/j.bioadv.2023.213494 · Cited by 41 · see citing works
Baiguera, S., Gaudio, C. D., Nardo, P. D., Manzari, V., Carotenuto, F., & Teodori, L. (2020) · BioMed Research International · doi:10.1155/2020/2689701 · Cited by 41 · see citing works
Kim, W.-J., Lee, H., Lee, C. K., Kyung, J. W., An, S. B., Han, I., & Kim, G. (2021) · Advanced Functional Materials · doi:10.1002/adfm.202105170 · Cited by 41 · see citing works
Self-citationA bioprinted complex tissue model for myotendinous junction with biochemical and biophysical cues
Kim, W. J., & Kim, G. (2022) · Bioengineering & Translational Medicine · doi:10.1002/btm2.10321 · Cited by 40 · see citing works
Self-citationWang, Q., Karadaş, Ö., Rosenholm, J. M., Xu, C., Näreoja, T., & Wang, X. (2024) · Advanced Functional Materials · doi:10.1002/adfm.202400431 · Cited by 39 · see citing works
Kang, B., Park, Y., Hwang, D. G., Kim, D., Yong, U., Lim, K. S., & Jang, J. (2021) · Advanced Materials Technologies · doi:10.1002/admt.202100947 · Cited by 36 · see citing works
Kim, D., Lee, H., Lee, G., Hoang, T., Kim, H., & Kim, G. (2022) · Bioengineering & Translational Medicine · doi:10.1002/btm2.10317 · Cited by 34 · see citing works
Self-citationWang, X., Wang, M., Xu, Y., Yin, J., & Hu, J. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.131980 · Cited by 34 · see citing works
Lotus-Root-Like Microchanneled Collagen Scaffold
Hwangbo, H., Kim, W.-J., & Kim, G. (2020) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.0c14670 · Cited by 34 · see citing works
Self-citationBioprinted hASC-laden structures with cell-differentiation niches for muscle regeneration
Kim, W.-J., Jang, C. H., & Kim, G. (2021) · Chemical Engineering Journal · doi:10.1016/j.cej.2021.129570 · Cited by 33 · see citing works
Self-citationNeuromuscular disease modeling on a chip
Santoso, J. W., & McCain, M. L. (2020) · Disease Models & Mechanisms · doi:10.1242/dmm.044867 · Cited by 33 · see citing works
Pereira, R. F., Lourenço, B. N., Bártolo, P., & Granja, P. L. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.202001176 · Cited by 30 · see citing works
Bioprinting Au Natural: The Biologics of Bioinks
Willson, K., Atala, A., & Yoo, J. J. (2021) · Biomolecules · doi:10.3390/biom11111593 · Cited by 30 · see citing works
Self-citationDai, R., Chen, W., Chen, Y., Jin, J., Zhang, S., Zhang, C., & Liu, J. (2024) · Biofabrication · doi:10.1088/1758-5090/ad51a6 · Cited by 31 · see citing works
Enhancing Peptide Biomaterials for Biofabrication
Firipis, K., Nisbet, D. R., Franks, S. J., Kapsa, R. M. I., Pirogova, E., Williams, R. J., & Quigley, A. F. (2021) · Polymers · doi:10.3390/polym13162590 · Cited by 27 · see citing works
Jiang, Y., Torun, T., Maffioletti, S. M., Serio, A., & Tedesco, F. S. (2022) · Experimental Cell Research · doi:10.1016/j.yexcr.2022.113133 · Cited by 28 · see citing works
Kim, W.-J., Kwon, D. R., Lee, H., Lee, J., Moon, Y. S., Lee, S. C., & Kim, G. (2024) · Bioactive Materials · doi:10.1016/j.bioactmat.2024.10.002 · Cited by 27 · see citing works
Self-citationMa, H., Xing, F., Yu, P., Xu, J., Wu, X., Luo, R., Xiang, Z., Rommens, P. M., Duan, X., & Ritz, U. (2023) · Materials & Design · doi:10.1016/j.matdes.2023.111591 · Cited by 27 · see citing works
Extracellular matrix in skeletal muscle injury and atrophy: mechanisms and therapeutic implications
Ge, X., Jin, Y., He, J., Jia, Z., Liu, Y., & Xu, Y. X. (2025) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2025.03.004 · Cited by 33 · see citing works
Design and bioprinting for tissue interfaces
Altunbek, M., Afghah, F., Çalışkan, Ö. Ş., Yoo, J. J., & Koç, B. (2023) · Biofabrication · doi:10.1088/1758-5090/acb73d · Cited by 26 · see citing works
Self-citationAlmalla, A., Elomaa, L., Bechtella, L., Daneshgar, A., Yavvari, P. S., Mahfouz, Z., Tang, P., Koksch, B., Sauer, I. M., Pagel, K., et al. (2023) · Biomacromolecules · doi:10.1021/acs.biomac.3c00602 · Cited by 26 · see citing works
Liu, H., Xing, F., Yu, P., Lu, R., Ma, S., Shakya, S., Xiang, Z., Peng, K., Zhang, D., & Liu, M. (2024) · Materials & Design · doi:10.1016/j.matdes.2024.113072 · Cited by 29 · see citing works
Kim, M. S., Choi, Y., & Lee, K. Y. (2025) · Polymers · doi:10.3390/polym17172337 · Cited by 35 · see citing works
Hu, G., Liang, Z., Fan, Z., Yu, M., Pan, Q., Nan, Y., Zhang, W., Wang, L., Wang, X., Hua, Y., et al. (2023) · Materials Today Bio · doi:10.1016/j.mtbio.2023.100695 · Cited by 25 · see citing works
Elomaa, L., Almalla, A., Keshi, E., Hillebrandt, K. H., Sauer, I. M., & Weinhart, M. (2023) · Biomaterials and Biosystems · doi:10.1016/j.bbiosy.2023.100084 · Cited by 25 · see citing works
Generation of Chicken Contractile Skeletal Muscle Structure Using Decellularized Plant Scaffolds
Hong, T. K., & Tae, J. (2024) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.3c01625 · Cited by 24 · see citing works
Digital micro-mirror device -based light curing technology and its biological applications
Wang, Z., Yang, W., Qin, Y., Liang, W., Yu, H., & Liu, L. (2021) · Optics & Laser Technology · doi:10.1016/j.optlastec.2021.107344 · Cited by 24 · see citing works
3D printing tissue-engineered scaffolds for auricular reconstruction
Gao, S., Nie, T., Lin, Y., Jiang, L., Wang, L., Wu, J., & Jiao, Y. (2024) · Materials Today Bio · doi:10.1016/j.mtbio.2024.101141 · Cited by 22 · see citing works
Zhang, W., Sun, T., Zhang, J., Hu, X., Yang, M., Han, L., Xu, G., Zhao, Y., & Li, Z. (2022) · Materials Today Bio · doi:10.1016/j.mtbio.2022.100528 · Cited by 22 · see citing works
Bioactive Inorganic Materials for Innervated Multi‐Tissue Regeneration
Zhang, H., Zhao, Z., & Wu, C. (2025) · Advanced Science · doi:10.1002/advs.202415344 · Cited by 21 · see citing works
3D Bioprinting Models for Glioblastoma: From Scaffold Design to Therapeutic Application
Branco, F., Cunha, J., Mendes, M., Sousa, J., & Vitorino, C. (2025) · Advanced Materials · doi:10.1002/adma.202501994 · Cited by 24 · see citing works
3D printing a biocompatible elastomer for modeling muscle regeneration after volumetric muscle loss
Kiratitanaporn, W., Berry, D. B., Mudla, A., Fried, T., Lao, A., Yu, C., Hao, N., Ward, S. R., & Chen, S. (2022) · Biomaterials Advances · doi:10.1016/j.bioadv.2022.213171 · Cited by 20 · see citing works
Luo, S., Wang, Q., Li, M., Xu, P., Wang, Y., Wang, Y., Kankala, R. K., Wang, S., & Chen, A. (2024) · Regenerative Biomaterials · doi:10.1093/rb/rbae113 · Cited by 20 · see citing works
Biomaterials and Regenerative Medicine in Pain Management
Gu, X., Turpin, M. A. C., & Romero‐Ortega, M. I. (2022) · Current Pain and Headache Reports · doi:10.1007/s11916-022-01055-5 · Cited by 20 · see citing works
Bioink derived from human placenta supporting angiogenesis
Duan, Y., Huang, W., Zhan, B., Li, Y., Xu, X., Li, K., Li, X., Liu, X., Ding, S., Wang, S., et al. (2022) · Biomedical Materials · doi:10.1088/1748-605x/ac7b5b · Cited by 19 · see citing works
Merotto, E., Pavan, P. G., & Piccoli, M. (2023) · Biomedicines · doi:10.3390/biomedicines11061742 · Cited by 20 · see citing works
Biofabrication of anisotropic articular cartilage based on decellularized extracellular matrix
Puiggalí‐Jou, A., Hui, I., Baldi, L., Frischknecht, R., Asadikorayem, M., Janiak, J., Chansoria, P., McCabe, M. C., Stoddart, M. J., Hansen, K. C., et al. (2025) · Biofabrication · doi:10.1088/1758-5090/ad9cc2 · Cited by 19 · see citing works
- Authors
- Kim, W., Lee, H., Lee, J., Atala, A., Yoo, J. J., Lee, S. J., & Kim, G. H.
- Affiliations
- Wake Forest University Health Sciences (US)
- Corresponding author
- Lee, Sang Jin
- Venue
- Biomaterials
- Publisher
- Elsevier BV
- Published
- 2020-02
- Volume
- 230
- Pages
- 119632
- ISSN
- 0142-9612 (ISSN-L)
- PMC
- PMC7141931
- OpenAlex
- W2991322883
- Cited by
- 185
- References
- 55
- Citations by year
- 2026: 13 · 2025: 21 · 2024: 32 · 2023: 33 · 2022: 33 · 2021: 36 · 2020: 16 · 2019: 1
- FWCI
- 20.55
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biomaterials (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Research Foundation of Korea
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- myotube formation, 3D bioprinting, decellularized extracellular matrix, skeletal muscle tissue engineering, uniaxial alignment, microtopography, myogenesis, C2C12 myoblasts, porcine skeletal muscle, gelatin methacryloyl, gene expression
- MeSH terms
- Animals, Cues, Extracellular Matrix, Swine, Muscle Fibers, Skeletal, Tissue Engineering, Bioprinting, Printing, Three-Dimensional
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