ACS Publications. Most Trusted. Most Cited. Most Read
Shape-Morphing Fibrous Hydrogel/Elastomer Bilayers Fabricated by a Combination of 3D Printing and Melt Electrowriting for Muscle Tissue Regeneration
My Activity

Figure 1Loading Img
    Article

    Shape-Morphing Fibrous Hydrogel/Elastomer Bilayers Fabricated by a Combination of 3D Printing and Melt Electrowriting for Muscle Tissue Regeneration
    Click to copy article linkArticle link copied!

    • Juan Uribe-Gomez
      Juan Uribe-Gomez
      Faculty of Engineering Sciences, University of Bayreuth, Thoma Strasse 36A, Bayreuth 95447, Germany
    • Andrés Posada-Murcia
      Andrés Posada-Murcia
      Faculty of Engineering Sciences, University of Bayreuth, Thoma Strasse 36A, Bayreuth 95447, Germany
    • Amit Shukla
      Amit Shukla
      Faculty of Engineering Sciences, University of Bayreuth, Thoma Strasse 36A, Bayreuth 95447, Germany
      More by Amit Shukla
    • Mert Ergin
      Mert Ergin
      Faculty of Engineering Sciences, University of Bayreuth, Thoma Strasse 36A, Bayreuth 95447, Germany
      More by Mert Ergin
    • Gissela Constante
      Gissela Constante
      Faculty of Engineering Sciences, University of Bayreuth, Thoma Strasse 36A, Bayreuth 95447, Germany
    • Indra Apsite
      Indra Apsite
      Faculty of Engineering Sciences, University of Bayreuth, Thoma Strasse 36A, Bayreuth 95447, Germany
      More by Indra Apsite
    • Dulle Martin
      Dulle Martin
      Forschungszentrum Jülich GmbH Jülich Centre for Neutron Science (JCNS-1) and Institute for Complex Systems (ICS-1), Wilhelm-Johnen-Straße, Jülich 52428, Germany
      More by Dulle Martin
    • Madeleine Schwarzer
      Madeleine Schwarzer
      Leibniz Institute of Polymer Research Dresden e. V., Hohe Straße 6, Dresden 01069, Germany
    • Anja Caspari
      Anja Caspari
      Leibniz Institute of Polymer Research Dresden e. V., Hohe Straße 6, Dresden 01069, Germany
      More by Anja Caspari
    • Alla Synytska
      Alla Synytska
      Leibniz Institute of Polymer Research Dresden e. V., Hohe Straße 6, Dresden 01069, Germany
      Faculty of Mathematics and Science, Institute of Physical Chemistry and Polymer Physics, Dresden University of Technology, Dresden 01062, Germany
    • Sahar Salehi
      Sahar Salehi
      Department of Biomaterials, University of Bayreuth, Prof.-Rüdiger-Bormann Strasse 1, 95447 Bayreuth, Germany
      More by Sahar Salehi
    • Leonid Ionov*
      Leonid Ionov
      Faculty of Engineering Sciences  and  Bavarian Polymer Institute, University of Bayreuth, Thoma Strasse 36A, Bayreuth 95447, Germany
      *Email: [email protected]
      More by Leonid Ionov
    Other Access OptionsSupporting Information (1)

    ACS Applied Bio Materials

    Cite this: ACS Appl. Bio Mater. 2021, 4, 2, 1720–1730
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsabm.0c01495
    Published January 26, 2021
    Copyright © 2021 American Chemical Society

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    This paper reports an approach for the fabrication of shape-changing bilayered scaffolds, which allow the growth of aligned skeletal muscle cells, using a combination of 3D printing of hyaluronic acid hydrogel, melt electrowriting of thermoplastic polycaprolactone-polyurethane elastomer, and shape transformation. The combination of the selected materials and fabrication methods allows a number of important advantages such as biocompatibility, biodegradability, and suitable mechanical properties (elasticity and softness of the fibers) similar to those of important components of extracellular matrix (ECM), which allow proper cell alignment and shape transformation. Myoblasts demonstrate excellent viability on the surface of the shape-changing bilayer, where they occupy space between fibers and align along them, allowing efficient cell patterning inside folded structures. The bilayer scaffold is able to undergo a controlled shape transformation and form multilayer scroll-like structures with cells encapsulated inside. Overall, the importance of this approach is the fabrication of tubular constructs with a patterned interior that can support the proliferation and alignment of muscle cells for muscle tissue regeneration.

    Copyright © 2021 American Chemical Society

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsabm.0c01495.

    • Infrared spectra of PCL-PU 121; NMR spectra of PCL-PU 121; thermogravimetric analysis of PCL-PU 121; NMR spectra of HA-MA; differential scanning calorimetry in time scale of PCL-diol 2000 kDa, PCL-PU 110, PCL-PU 121, and PCL-PU 143; C2C12 myoblast cell culture presented with detailed significant differences after quantification of cell viability after 1, 3, and 7 days of culture and cell metabolic activity after 1, 3, and 7 days of culture measured by Alamar Blue Assay (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!
    Citation Statements
    Explore this article's citation statements on scite.ai

    This article is cited by 40 publications.

    1. Danila Gorgol, Miroslav Mrlík, Filip Mikulka, Zdenka Víchová, Leona Mahelová, Markéta Ilčíková, Antonín Minařík. Smart Biopolymer Scaffolds Based on Hyaluronic Acid and Carbonyl Iron Microparticles: 3D Printing, Magneto-Responsive, and Cytotoxicity Study. ACS Applied Bio Materials 2024, 7 (11) , 7483-7493. https://doi.org/10.1021/acsabm.4c00567
    2. Hakan Berk Aydin, Altug Ozcelikkale, Ahmet Acar. Exploiting Matrix Stiffness to Overcome Drug Resistance. ACS Biomaterials Science & Engineering 2024, 10 (8) , 4682-4700. https://doi.org/10.1021/acsbiomaterials.4c00445
    3. Muthu Parkkavi Sekar, Shruthy Suresh, Allen Zennifer, Swaminathan Sethuraman, Dhakshinamoorthy Sundaramurthi. Hyaluronic Acid as Bioink and Hydrogel Scaffolds for Tissue Engineering Applications. ACS Biomaterials Science & Engineering 2023, 9 (6) , 3134-3159. https://doi.org/10.1021/acsbiomaterials.3c00299
    4. Gissela Constante, Indra Apsite, Paul Auerbach, Sebastian Aland, Dennis Schönfeld, Thorsten Pretsch, Pavel Milkin, Leonid Ionov. Smart Mechanically Tunable Surfaces with Shape Memory Behavior and Wetting-Programmable Topography. ACS Applied Materials & Interfaces 2022, 14 (17) , 20208-20219. https://doi.org/10.1021/acsami.2c01078
    5. Indra Apsite, Sahar Salehi, Leonid Ionov. Materials for Smart Soft Actuator Systems. Chemical Reviews 2022, 122 (1) , 1349-1415. https://doi.org/10.1021/acs.chemrev.1c00453
    6. Juan Uribe-Gomez, Andrés Posada-Murcia, Amit Shukla, Hanin Alkhamis, Sahar Salehi, Leonid Ionov. Soft Elastic Fibrous Scaffolds for Muscle Tissue Engineering by Touch Spinning. ACS Applied Bio Materials 2021, 4 (7) , 5585-5597. https://doi.org/10.1021/acsabm.1c00403
    7. Kunal Ranat, Hong Phan, Suhaib Ellythy, Mitchell Kenter, Adil Akkouch. Advancements in Musculoskeletal Tissue Engineering: The Role of Melt Electrowriting in 3D-Printed Scaffold Fabrication. Journal of Functional Biomaterials 2025, 16 (5) , 163. https://doi.org/10.3390/jfb16050163
    8. Waseem Kitana, Indra Apsite, Leonid Ionov. 3D (Bio) Printing Combined Fiber Fabrication Methods for Tissue Engineering Applications: Possibilities and Limitations. Advanced Functional Materials 2025, 36 https://doi.org/10.1002/adfm.202500450
    9. Alireza Sadraei, Seyed Morteza Naghib, Navid Rabiee. 4D printing chemical stimuli-responsive hydrogels for tissue engineering and localized drug delivery applications – part 2. Expert Opinion on Drug Delivery 2025, 22 (4) , 491-510. https://doi.org/10.1080/17425247.2025.2466768
    10. Piotr Stanisław Zieliński, Zhaohang Zhang, Ilaria Squillante, Guillermo Monreal Santiago, Marcus Koch, Giuseppe Portale, Marleen Kamperman, Anastasiia Krushynska, Małgorzata Katarzyna Włodarczyk‐Biegun. Designing Smartly: Understanding the Crystallinity of Melt Electrowritten Scaffolds. Engineering in Life Sciences 2025, 25 (4) https://doi.org/10.1002/elsc.70020
    11. Lorenzo Bonetti, Giulia Scalet. 4D fabrication of shape-changing systems for tissue engineering: state of the art and perspectives. Progress in Additive Manufacturing 2025, 10 (4) , 1913-1943. https://doi.org/10.1007/s40964-024-00743-5
    12. Biranche Tandon, Nasim Sabahi, Reza Farsi, Taavet Kangur, Giovanni Boero, Arnaud Bertsch, Xiaopeng Li, Juergen Brugger. Performance Comparison of Shape Memory Polymer Structures Printed by Fused Deposition Modeling and Melt Electrowriting. Advanced Materials Technologies 2025, 10 (4) https://doi.org/10.1002/admt.202400466
    13. Yunlei Yin, Hao Yang, Wenyuan Han, Cheng Guo, Qianqian Mu, Hongying Yang, Dongyi Chen. Melt Electrowriting for Biomimetic Tissue Engineering: Advances in Scaffold Design, Materials, and Multifunctional Applications. Polymers for Advanced Technologies 2025, 36 (1) https://doi.org/10.1002/pat.70067
    14. 浩哲 李. Research Progress of Shape Memory Polymers in Biomedical Applications. Hans Journal of Biomedicine 2025, 15 (03) , 489-501. https://doi.org/10.12677/hjbm.2025.153057
    15. Fucheng Zhang, Kai Cao, Ahmadreza Zaeri, Ralf Zgeib, Robert C. Chang. The Design and Fabrication of Engineered Tubular Tissue Constructs Enabled by Electrohydrodynamic Fabrication Techniques: A Review. Macromolecular Materials and Engineering 2024, 309 (9) https://doi.org/10.1002/mame.202400095
    16. Xiao Liu, Yinghan Zhao, Ku Li, Shuo Shen, Jianghua Li. Exploring the mechanism of amylose/amylopectin improving formation of yeast-soy protein high-moisture extrudates based on small and large amplitude oscillatory shear rheology. Food Hydrocolloids 2024, 153 , 110062. https://doi.org/10.1016/j.foodhyd.2024.110062
    17. Jiahui Lai, Yuwei Liu, Gang Lu, Patrick Yung, Xiaoying Wang, Rocky S. Tuan, Zhong Alan Li. 4D bioprinting of programmed dynamic tissues. Bioactive Materials 2024, 37 , 348-377. https://doi.org/10.1016/j.bioactmat.2024.03.033
    18. Paula G. Saiz, Ander Reizabal, Jose Luis Vilas‐Vilela, Paul D. Dalton, Senentxu Lanceros‐Mendez. Materials and Strategies to Enhance Melt Electrowriting Potential. Advanced Materials 2024, 36 (24) https://doi.org/10.1002/adma.202312084
    19. Brenna L. Devlin, Mark C. Allenby, Jiongyu Ren, Edmund Pickering, Travis J. Klein, Naomi C. Paxton, Maria A. Woodruff. Materials Design Innovations in Optimizing Cellular Behavior on Melt Electrowritten (MEW) Scaffolds. Advanced Functional Materials 2024, 34 (18) https://doi.org/10.1002/adfm.202313092
    20. Mathilde Grosjean, Christina Schmidleithner, Stéphane Dejean, Niels B. Larsen, Benjamin Nottelet. Degradable 4D-printed hydration-driven actuators from a single family of amphiphilic star-shaped copolymers. Materials & Design 2024, 241 , 112953. https://doi.org/10.1016/j.matdes.2024.112953
    21. Shadpour Mallakpour, Elham Azadi, Chaudhery Mustansar Hussain. Latest innovations in tissue engineering by 3D-printed hyaluronic acid-based hydrogels. 2024, 61-88. https://doi.org/10.1016/B978-0-323-95383-2.00026-3
    22. Ramisha Sajjad, Sohaib Tahir Chauhdary, Muhammad Tuoqeer Anwar, Ali Zahid, Azhar Abbas Khosa, Muhammad Imran, Muhammad Haider Sajjad. A review of 4D printing – Technologies, shape shifting, smart polymer based materials, and biomedical applications. Advanced Industrial and Engineering Polymer Research 2024, 7 (1) , 20-36. https://doi.org/10.1016/j.aiepr.2023.08.002
    23. Xiao Li, Minghao Li, Lisa Tang, Diwei Shi, Emily Lam, Jinhye Bae. 3D shape morphing of stimuli-responsive composite hydrogels. Materials Chemistry Frontiers 2023, 7 (23) , 5989-6034. https://doi.org/10.1039/D3QM00856H
    24. Jiahui Lai, Min Wang. Developments of additive manufacturing and 5D printing in tissue engineering. Journal of Materials Research 2023, 38 (21) , 4692-4725. https://doi.org/10.1557/s43578-023-01193-5
    25. Akshat Joshi, Saswat Choudhury, Vageesh Singh Baghel, Souvik Ghosh, Sumeet Gupta, Debrupa Lahiri, G. K. Ananthasuresh, Kaushik Chatterjee. 4D Printed Programmable Shape‐Morphing Hydrogels as Intraoperative Self‐Folding Nerve Conduits for Sutureless Neurorrhaphy. Advanced Healthcare Materials 2023, 12 (24) https://doi.org/10.1002/adhm.202300701
    26. Souvik Ghosh, Siddhi Chaudhuri, Partha Roy, Debrupa Lahiri. 4D Printing in Biomedical Engineering: a State-of-the-Art Review of Technologies, Biomaterials, and Application. Regenerative Engineering and Translational Medicine 2023, 9 (3) , 339-365. https://doi.org/10.1007/s40883-022-00288-5
    27. N. Pien, H. Krzyslak, S. Shastry Kallaje, J. Van Meerssche, D. Mantovani, C. De Schauwer, P. Dubruel, S. Van Vlierberghe, C.P. Pennisi. Tissue engineering of skeletal muscle, tendons and nerves: A review of manufacturing strategies to meet structural and functional requirements. Applied Materials Today 2023, 31 , 101737. https://doi.org/10.1016/j.apmt.2023.101737
    28. Han Chen, Huaqian Xue, Huanxuan Zeng, Minghai Dai, Chengxuan Tang, Liangle Liu. 3D printed scaffolds based on hyaluronic acid bioinks for tissue engineering: a review. Biomaterials Research 2023, 27 (1) https://doi.org/10.1186/s40824-023-00460-0
    29. María del Carmen De Lama-Odría, Luis J. del Valle, Jordi Puiggalí. Melt Electrospinning and Electrowriting for Pharmaceutical and Biomedical Applications. 2023, 41-70. https://doi.org/10.1007/978-3-031-26908-0_3
    30. Moqaddaseh Afzali Naniz, Mohsen Askari, Ali Zolfagharian, Mahdi Bodaghi. 4D Printing in Pharmaceutics and Biomedical Applications. 2023, 207-247. https://doi.org/10.1007/978-3-031-26908-0_9
    31. Juliane C. Kade, Ezgi Bakirci, Biranche Tandon, Danila Gorgol, Miroslav Mrlik, Robert Luxenhofer, Paul D. Dalton. The Impact of Including Carbonyl Iron Particles on the Melt Electrowriting Process. Macromolecular Materials and Engineering 2022, 307 (12) https://doi.org/10.1002/mame.202200478
    32. Moqaddaseh Afzali Naniz, Mohsen Askari, Ali Zolfagharian, Mehrdad Afzali Naniz, Mahdi Bodaghi. 4D printing: a cutting-edge platform for biomedical applications. Biomedical Materials 2022, 17 (6) , 062001. https://doi.org/10.1088/1748-605X/ac8e42
    33. Zungui Shao, Huatan Chen, Qingfeng Wang, Guoyi Kang, Jiaxin Jiang, Xiang Wang, Wenwang Li, Yifang Liu, Gaofeng Zheng. Melt Electrowriting Ordered TPU Microfibrous Mesh for On-Demand Colorimetric Wearable Sweat Detection. IEEE Sensors Journal 2022, 22 (19) , 18560-18566. https://doi.org/10.1109/JSEN.2022.3199406
    34. Hannah Haag, Paul D. Dalton, Veerle Bloemen. The Synergy of Biomimetic Design Strategies for Tissue Constructs. Advanced Functional Materials 2022, 32 (32) https://doi.org/10.1002/adfm.202201414
    35. Juan Uribe‐Gomez, Dennis Schönfeld, Andrés Posada‐Murcia, Michel‐Manuel Roland, Anja Caspari, Alla Synytska, Sahar Salehi, Thorsten Pretsch, Leonid Ionov. Fibrous Scaffolds for Muscle Tissue Engineering Based on Touch‐Spun Poly(Ester‐Urethane) Elastomer. Macromolecular Bioscience 2022, 22 (4) https://doi.org/10.1002/mabi.202100427
    36. Juliane C Kade, Biranche Tandon, Jan Weichhold, Dario Pisignano, Luana Persano, Robert Luxenhofer, Paul D Dalton. Melt electrowriting of poly(vinylidene fluoride‐ co ‐trifluoroethylene). Polymer International 2021, 70 (12) , 1725-1732. https://doi.org/10.1002/pi.6272
    37. Ju Qing Song, Xin Liang Ye, Wen Cong Chen, Li Wang, Bing Heng Lu. 3D Printing of Skeleton Muscle Tissue Engineering Scaffolds. Nano LIFE 2021, 11 (04) https://doi.org/10.1142/S1793984421410075
    38. Cathal D. O'Connell, Olivia Bridges, Cameron Everett, Natasha Antill‐O'Brien, Carmine Onofrillo, Claudia Di Bella. Electrostatic Distortion of Melt‐Electrowritten Patterns by 3D Objects: Quantification, Modeling, and Toolpath Correction. Advanced Materials Technologies 2021, 6 (11) https://doi.org/10.1002/admt.202100345
    39. Tarun Agarwal, Sung Yun Hann, Irene Chiesa, Haitao Cui, Nehar Celikkin, Simone Micalizzi, Andrea Barbetta, Marco Costantini, Timothy Esworthy, Lijie Grace Zhang, Carmelo De Maria, Tapas Kumar Maiti. 4D printing in biomedical applications: emerging trends and technologies. Journal of Materials Chemistry B 2021, 9 (37) , 7608-7632. https://doi.org/10.1039/D1TB01335A
    40. Jiahui Lai, Chong Wang, Min Wang. 3D printing in biomedical engineering: Processes, materials, and applications. Applied Physics Reviews 2021, 8 (2) https://doi.org/10.1063/5.0024177

    ACS Applied Bio Materials

    Cite this: ACS Appl. Bio Mater. 2021, 4, 2, 1720–1730
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsabm.0c01495
    Published January 26, 2021
    Copyright © 2021 American Chemical Society

    Article Views

    2362

    Altmetric

    -

    Citations

    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.