Muscle-derived extracellular matrix on sinusoidal wavy surfaces synergistically promotes myogenic differentiation and maturation
Abstract
The generation of physiologically aligned multinucleated myotubes is critical in the fabrication of functional engineered skeletal muscle. Although micro-/nano-topographical contact guidance, such as groove/ridge structures, has induced the alignment of muscle fibers by providing cells with extracellular matrix (ECM) topography, the complex biochemical microenvironment of the ECM cannot be recapitulated. Here, we report the enhancement of myogenic differentiation and maturation using muscle decellularized ECM (mdECM) and sinusoidal wavy surfaces, which provided a biochemical microenvironment and microscale contact guidance, respectively. Sinusoidal wavy polystyrene surfaces with wavelengths of 20, 40, and 80 μm were fabricated by a deep X-ray lithography-based process. The mdECM was prepared by decellularization of porcine tibialis anterior skeletal muscle. An mdECM coating significantly improved the surface wettability of polystyrene substrates and exhibited higher seeding efficiency, cell viability, and proliferation compared with collagen- and non-coating cases. The sinusoidal wavy surfaces induced well-aligned myotubes and showed significantly enhanced formation of myotubes and myogenic differentiation when the surface was coated with mdECM. Particularly, there was an approximately 1.5-2 fold improvement in morphological analysis and gene expression for mdECM-compared to non-coated sinusoidal wavy surfaces. These results suggest that the consideration of both topographical and biochemical environmental cues can generate a highly mimicked ECM environment, thereby providing cells with a synergistic effect on myogenic differentiation and maturation. The outcome of this study will be useful in developing of functional engineered muscle for application in tissue regeneration or a high-throughput in vitro model for drug screening.
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Compared to collagen-coated and uncoated substrates, the sinusoidal polystyrene surface coated with decellularized muscle ECM yielded well-aligned myotubes with enhanced myogenic differentiation.
“Compared to collagen‐coated and uncoated substrates, this configuration yielded well‐aligned myotubes with enhanced myogenic differentiation.[ 191 ]”
From Bioactive scaffolds for tissue engineering: A review of decellularized extracellular matrix applications and innovations (2025) · cites this paper as [191]
Choi et al. fabricated a sinusoidal polystyrene surface coated with decellularized muscle ECM, facilitating formation of multinucleated myotubes.
“Choi et al. fabricated a sinusoidal polystyrene surface coated with decellularized muscle ECM, a combination that facilitated the formation of multinucleated myotubes.”
From Bioactive scaffolds for tissue engineering: A review of decellularized extracellular matrix applications and innovations (2025) · cites this paper as [191]
Cites
An 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
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
Self-citationNanotechnological strategies for engineering complex tissues
Dvir, T., Timko, B. P., Kohane, D. S., & Langer, R. (2011) · Nature Nanotechnology · doi:10.1038/nnano.2010.246 · Cited by 1,367 · see citing works
Structure and function of the skeletal muscle extracellular matrix
Gillies, A. R., & Lieber, R. L. (2011) · Muscle & Nerve · doi:10.1002/mus.22094 · Cited by 1,023 · see citing works
Muscle LIM protein, a novel essential regulator of myogenesis, promotes myogenic differentiation
Arber, S. (1994) · Cell · doi:10.1016/0092-8674(94)90192-9 · Cited by 441 · see citing works
Grogan, B. F., & Hsu, J. R. (2011) · American Academy of Orthopaedic Surgeon · doi:10.5435/00124635-201102001-00007 · Cited by 402 · see citing works
Biomimetic 3D tissue printing for soft tissue regeneration
Pati, F., Ha, D.-H., Jang, J., Han, H. H., Rhie, J.-W., & Cho, D.-W. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.05.043 · Cited by 368 · see citing works
Self-citationJang, J., Kim, T. G., Kim, B. S., Kim, S.-W., Kwon, S., & Cho, D. (2016) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.01.013 · Cited by 345 · see citing works
Self-citationGao, G., Lee, J. H., Jang, J., Lee, D., Kong, J., Kim, B. S., Choi, Y., Jang, W. B., Hong, Y. J., Kwon, S., et al. (2017) · Advanced Functional Materials · doi:10.1002/adfm.201700798 · Cited by 340 · see citing works
Self-citationLee, H., Han, W., Kim, H., Ha, D., Jang, J., Kim, B. S., & Cho, D. (2017) · Biomacromolecules · doi:10.1021/acs.biomac.6b01908 · Cited by 329 · see citing works
Self-citation3D cell printing of functional skeletal muscle constructs using skeletal muscle-derived bioink
Choi, Y., Kim, T. G., Jeong, J., Yi, H., Park, J. W., Hwang, W., & Cho, D. (2016) · Advanced Healthcare Materials · doi:10.1002/adhm.201600483 · Cited by 298 · see citing works
Self-citationDeQuach, J. A., Mezzano, V., Miglani, A., Lange, S., Keller, G. M., Sheikh, F., & Christman, K. L. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013039 · Cited by 263 · see citing works
Engineered 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
Kim, B. S., Kim, H., Gao, G., Jang, J., & Cho, D. (2017) · Biofabrication · doi:10.1088/1758-5090/aa7e98 · Cited by 207 · see citing works
Self-citationLam, M. T., Sim, S., Zhu, X. A., & Takayama, S. (2006) · Biomaterials · doi:10.1016/j.biomaterials.2006.04.012 · Cited by 206 · see citing works
Stern, M. M., Myers, R. L., Hammam, N., Stern, K. A., Eberli, D., Kritchevsky, S. B., Söker, S., & Dyke, M. E. V. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2008.12.069 · Cited by 185 · see citing works
Guo, X., Gonzalez, M., Stancescu, M., Vandenburgh, H. H., & Hickman, J. J. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.09.014 · Cited by 168 · see citing works
Engineering multi-layered skeletal muscle tissue by using 3D microgrooved collagen scaffolds
Chen, S., Nakamoto, T., Kawazoe, N., & Chen, G. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.09.010 · Cited by 167 · see citing works
DeQuach, J. A., Lin, J., Cam, C., Hu, D. P., Salvatore, M., Sheikh, F., & Christman, K. L. (2012) · European Cells and Materials · doi:10.22203/ecm.v023a31 · Cited by 159 · see citing works
Wu, X., Corona, B. T., Chen, X., & Walters, J. (2012) · BioResearch open access · doi:10.1089/biores.2012.0271 · Cited by 151 · see citing works
Zhang, J., Hu, Z. Q., Turner, N. J., Teng, S. F., Cheng, W. Y., Zhou, H. Y., Zhang, L., Hu, H. W., Wang, Q., & Badylak, S. F. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.02.040 · Cited by 141 · see citing works
Choi, Y. C., Choi, J. S., Kim, B. S., Kim, J. D., Yoon, H. I., & Cho, Y. W. (2012) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2012.0009 · Cited by 127 · see citing works
Self-citationAltomare, L., Gadegaard, N., Visai, L., Tanzi, M. C., & Farè, S. (2009) · Acta Biomaterialia · doi:10.1016/j.actbio.2009.12.040 · Cited by 120 · see citing works
3D Cell Printed Tissue Analogues: A New Platform for Theranostics
Choi, Y., Yi, H., Kim, S.-W., & Cho, D. (2017) · Theranostics · doi:10.7150/thno.19396 · Cited by 120 · see citing works
Self-citationOptimizing the structure and contractility of engineered skeletal muscle thin films
Sun, Y., Duffy, R. M., Lee, A., & Feinberg, A. W. (2013) · Acta Biomaterialia · doi:10.1016/j.actbio.2013.04.036 · Cited by 112 · 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
Engineering of aligned skeletal muscle by micropatterning.
Huang, N. F., Lee, R. J., & Li, S. (2010) · PubMed Central · Cited by 84 · see citing works
Lee, J., Chung, S., Song, H., Kim, S., & Hong, Y. (2013) · Journal of Physics D Applied Physics · doi:10.1088/0022-3727/46/10/105305 · Cited by 74 · see citing works
Sinusoidal wavy surfaces for curvature-guided migration of T lymphocytes
Song, K. H., Park, S. J., Kim, D. S., & Doh, J. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.01.071 · Cited by 70 · see citing works
Self-citationKim, B. S., Choi, J. S., Kim, J. D., Choi, Y. C., & Cho, Y. W. (2012) · Cell and Tissue Research · doi:10.1007/s00441-012-1391-y · Cited by 66 · see citing works
Self-citationElectrically regulated differentiation of skeletal muscle cells on ultrathin graphene-based films
Ahadian, S., Ramón‐Azcón, J., Chang, H., Liang, X., Kaji, H., Shiku, H., Nakajima, K., Ramalingam, M., Wu, H., Matsue, T., et al. (2014) · RSC Advances · doi:10.1039/c3ra46218h · Cited by 63 · see citing works
Microfabricated devices for cell biology: all for one and one for all
Lautenschläger, F., & Piel, M. (2012) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2012.10.017 · Cited by 52 · see citing works
Fabrication of 3D aligned nanofibrous tubes by direct electrospinning
Jana, S., & Zhang, M. (2013) · Journal of Materials Chemistry B · doi:10.1039/c3tb20197j · Cited by 51 · see citing works
Wedhas, N., Klamut, H. J., Dogra, C., Srivastava, A. K., Mohan, S., & Kumar, A. (2005) · The FASEB Journal · doi:10.1096/fj.05-4198com · Cited by 35 · see citing works
Hong, X., Yuan, Y., Sun, X., Zhou, M., Guo, G., Zhang, Q., Hescheler, J., & Xi, J. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000486813 · Cited by 35 · see citing works
Tissue Engineering for Artificial Organs
Hasan, A. (2017) · Wiley eBooks · doi:10.1002/9783527689934 · Cited by 34 · see citing works
Kim, J. H., Choi, Y., Yi, H., Wang, J. H., Cho, D., & Jeong, Y. H. (2017) · Biomedical Materials · doi:10.1088/1748-605x/aa7b51 · Cited by 29 · see citing works
Self-citationMurray, L., Nock, V., Evans, J. J., & Alkaisi, M. M. (2016) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.35696 · Cited by 27 · see citing works
Matrix Topographical Cue-Mediated Myogenic Differentiation of Human Embryonic Stem Cell Derivatives
Hwang, Y., Seo, T., Hariri, S., Choi, C., & Varghese, S. (2017) · Polymers · doi:10.3390/polym9110580 · Cited by 20 · see citing works
Extracellular matrix‐immobilized nanotopographical substrates for enhanced myogenic differentiation
Lee, E. A., Jung, G., Im, S. G., & Hwang, N. S.-Y. (2014) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.33308 · Cited by 10 · see citing works
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High-Throughput Methods in the Discovery and Study of Biomaterials and Materiobiology
Yang, L., Pijuan‐Galito, S., Rho, H. S., Vasilevich, A. S., Eren, A. D., Ge, L., Habibović, P., Alexander, M. R., de Boer, J., Carlier, A., et al. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.0c00752 · Cited by 187 · see citing works
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Kim, W., Lee, H., Lee, J., Atala, A., Yoo, J. J., Lee, S. J., & Kim, G. H. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2019.119632 · Cited by 185 · see citing works
Self-citationLiu, 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
3D organ models—Revolution in pharmacological research?
Weinhart, M., Hocke, A. C., Hippenstiel, S., Kurreck, J., & Hedtrich, S. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.11.002 · Cited by 89 · see citing works
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Kutluk, H., Bastounis, E. E., & Constantinou, I. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202203256 · Cited by 82 · see citing works
Yang, L., Ge, L., & van Rijn, P. (2020) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.0c05012 · Cited by 78 · see citing works
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Miao, S., Nowicki, M. A., Cui, H., Lee, S., Zhou, X., Mills, D. K., & Zhang, L. G. (2019) · Biofabrication · doi:10.1088/1758-5090/ab1d07 · Cited by 74 · see citing works
Park, W., Gao, G., & Cho, D. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22157837 · Cited by 70 · see citing works
Self-citationXia, N., Jin, D., Pan, C., Zhang, J., Yang, Z., Su, L., Zhao, J., Wang, L., & Zhang, L. (2022) · Nature Communications · doi:10.1038/s41467-022-35212-6 · Cited by 61 · see citing works
Choi, A., Seo, K. D., Yoon, H., Han, S. J., & Kim, D. S. (2019) · Biomaterials Science · doi:10.1039/c8bm01664j · Cited by 53 · see citing works
Self-citationAnderson, J. E. (2021) · European Journal of Applied Physiology · doi:10.1007/s00421-021-04865-4 · Cited by 52 · see citing works
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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
Yang, L., Ge, L., Zhou, Q., Mokabber, T., Pei, Y. T., Bron, R., & van Rijn, P. (2020) · Advanced Materials Interfaces · doi:10.1002/admi.202000385 · Cited by 43 · see citing works
Carthew, J., Taylor, J. B. J., Garcia-Cruz, M. R., Kiaie, N., Voelcker, N. H., Cadarso, V. J., & Frith, J. E. (2022) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.1c22109 · Cited by 42 · see citing works
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Baek, J., Jung, W., Cho, Y., Lee, E., Yun, G., Cho, S., Jung, H., & Im, S. G. (2019) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.9b03479 · Cited by 28 · see citing works
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Wang, Z. F., Wang, L., Song, M., An, C., Li, Y., Zhou, Y., & Cen, L. (2024) · European Polymer Journal · doi:10.1016/j.eurpolymj.2024.113301 · Cited by 3 · see citing works
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Kim, H. W., Lee, J. S., Park, S. J., Rhie, J. W., & Kim, D. S. (2020) · Advanced Materials Interfaces · doi:10.1002/admi.201901983 · Cited by 3 · see citing works
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- Authors
- Choi, Y.-J., Park, S. J., Yi, H.-G., Lee, H., Kim, D. S., & Cho, D.-W.
- Affiliations
- Pohang University of Science and Technology (KR)
- Corresponding author
- Kim, Dong Sung
- Cho, Dong-Woo
- Venue
- Journal of Materials Chemistry B
- Publisher
- Royal Society of Chemistry (RSC)
- Published
- 2018
- Volume
- 6
- Issue
- 35
- Pages
- 5530-5539
- ISSN
- 2050-750X (ISSN-L)
- 2050-7518
- OpenAlex
- W2887266009
- Cited by
- 39
- References
- 41
- Citations by year
- 2025: 5 · 2024: 5 · 2023: 4 · 2022: 7 · 2021: 4 · 2020: 8 · 2019: 5 · 2018: 1
- FWCI
- 4.71
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Materials Chemistry B (publishedVersion)
- PubMed (publishedVersion)
- Open Access System for Information Sharing (Pohang University of Science and Technology) (submittedVersion)
- Funders
- National Research Foundation of Korea (2010-0018294, 2014M3C1B2048632, 2017R1A2A1A05001090)
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Keywords
- decellularized extracellular matrix, myogenesis, myotube maturation, contact guidance, surface topography, wettability, engineered skeletal muscle, deep X-ray lithography, surface coating, tissue regeneration, drug screening
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