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One-Step Formation of Microporous Hydrogel Sponges Encapsulating Living Cells by Utilizing Bicontinuous Dispersion of Aqueous Polymer Solutions

  • Aruto Hori
    Aruto Hori
    Department of Applied Chemistry and Biotechnology, Graduate School of Engineering, Chiba University, 1-33 Yayoi-cho, Inage-ku, Chiba 263-8522, Japan
    More by Aruto Hori
  • Yuki Watabe
    Yuki Watabe
    Department of Applied Chemistry and Biotechnology, Graduate School of Engineering, Chiba University, 1-33 Yayoi-cho, Inage-ku, Chiba 263-8522, Japan
    More by Yuki Watabe
  • Masumi Yamada*
    Masumi Yamada
    Department of Applied Chemistry and Biotechnology, Graduate School of Engineering, Chiba University, 1-33 Yayoi-cho, Inage-ku, Chiba 263-8522, Japan
    *E-mail: [email protected]
  • Yuya Yajima
    Yuya Yajima
    Department of Applied Chemistry and Biotechnology, Graduate School of Engineering, Chiba University, 1-33 Yayoi-cho, Inage-ku, Chiba 263-8522, Japan
    More by Yuya Yajima
  • Rie Utoh
    Rie Utoh
    Department of Applied Chemistry and Biotechnology, Graduate School of Engineering, Chiba University, 1-33 Yayoi-cho, Inage-ku, Chiba 263-8522, Japan
    More by Rie Utoh
  • , and 
  • Minoru Seki
    Minoru Seki
    Department of Applied Chemistry and Biotechnology, Graduate School of Engineering, Chiba University, 1-33 Yayoi-cho, Inage-ku, Chiba 263-8522, Japan
    More by Minoru Seki
Cite this: ACS Appl. Bio Mater. 2019, 2, 5, 2237–2245
Publication Date (Web):April 24, 2019
https://doi.org/10.1021/acsabm.9b00194
Copyright © 2019 American Chemical Society

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    Abstract

    Abstract Image

    With the recent progress in three-dimensional (3D) cell culture techniques for regenerative medicine and drug development, hydrogel-based tissue engineering approaches that can precisely organize cells into functional formats have attracted increasing attention. However, challenges remain in creating continuous microconduits within hydrogels to effectively deliver oxygen and nutrients to the embedded cells. Here we propose a one-step, fully liquid state, and all-aqueous process to create porous hydrogels that can encapsulate living cells without the need for extensive processing protocols, including the incorporation and removal of sacrificial materials. An unusual bicontinuous state of aqueous two-phase dispersion was utilized, and one of the two phases, encapsulating living cells, was rapidly photo-cross-linked to form hydrogel sponges. We optimized the volumetric mixing ratio of gelatin methacrylate (GelMA)-rich and polyethylene glycol (PEG)-rich solutions and investigated the effects of the formed continuous microconduits on the cell functions by creating liver-tissue mimetic 3D constructs. The presented technology provides a facile and versatile strategy for fabricating microstructured hydrogels for cell culture and would bring new insights for the development of porous materials by fully aqueous bicontinuous dispersions.

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    Cited By

    This article is cited by 13 publications.

    1. Sai S. Patkar, Cristobal Garcia Garcia, Luisa L. Palmese, Kristi L. Kiick. Sequence-Encoded Differences in Phase Separation Enable Formation of Resilin-like Polypeptide-Based Microstructured Hydrogels. Biomacromolecules 2023, 24 (8) , 3729-3741. https://doi.org/10.1021/acs.biomac.3c00418
    2. Rina Nonogaki, Rie Utoh, Aruto Hori, Yuri Shimoda, Masumi Yamada. Fabrication of Full-thickness Skin Tissue Models Using Gelatin-based Hydrogel Sponges with Continuous Micropores. 2023, 158-161. https://doi.org/10.1109/NANOMED59780.2023.10404638
    3. Afrânio Melo, Fernando L. P. Pessoa, José Carlos Pinto. Liquid–Liquid Equilibrium in Xylene Solubles (XS) Analysis of Polypropylene. Macromolecular Reaction Engineering 2023, 17 (6) https://doi.org/10.1002/mren.202300029
    4. Ghazi Ben Messaoud, Sanja Aveic, Mattis Wachendoerfer, Horst Fischer, Walter Richtering. 3D Printable Gelatin Methacryloyl (GelMA)‐Dextran Aqueous Two‐Phase System with Tunable Pores Structure and Size Enables Physiological Behavior of Embedded Cells In Vitro. Small 2023, https://doi.org/10.1002/smll.202208089
    5. Yan Liu, Bo Zhuang, Bochuan Yuan, Hui Zhang, Jingfei Li, Wanmei Wang, Ruiteng Li, Lina Du, Pingtian Ding, Yiguang Jin. Predatory bacterial hydrogels for topical treatment of infected wounds. Acta Pharmaceutica Sinica B 2023, 13 (1) , 315-326. https://doi.org/10.1016/j.apsb.2022.05.005
    6. Cheng Wei, Pengfei Tang, Youhong Tang, Laibao Liu, Xiong Lu, Kun Yang, Qingyuan Wang, Wei Feng, Quazi T. H. Shubhra, Zhenming Wang, Hongping Zhang. Sponge‐Like Macroporous Hydrogel with Antibacterial and ROS Scavenging Capabilities for Diabetic Wound Regeneration. Advanced Healthcare Materials 2022, 11 (20) https://doi.org/10.1002/adhm.202200717
    7. Baljit Singh, Kaka Ram, Baldev Singh. Development and characterization of azadirachta indica gum-poly(2-hydroxyethyl methacrylate) crosslinked co-polymeric hydrogels for drug delivery applications. Chemical Physics Letters 2022, 792 , 139401. https://doi.org/10.1016/j.cplett.2022.139401
    8. Moon Sung Kang, Mina Kwon, So Yun Lee, Seok Hyun Lee, Hyo Jung Jo, Bongju Kim, Ki Su Kim, Dong-Wook Han. In Situ Crosslinkable Collagen-Based Hydrogels for 3D Printing of Dermis-Mimetic Constructs. ECS Journal of Solid State Science and Technology 2022, 11 (4) , 045014. https://doi.org/10.1149/2162-8777/ac6897
    9. Azadeh Mostafavi, Mohamadmahdi Samandari, Mehran Karvar, Mahsa Ghovvati, Yori Endo, Indranil Sinha, Nasim Annabi, Ali Tamayol. Colloidal multiscale porous adhesive (bio)inks facilitate scaffold integration. Applied Physics Reviews 2021, 8 (4) https://doi.org/10.1063/5.0062823
    10. Baljit Singh, Baldev Singh. Design of dietary fiber azadiracta indica gum based hydrogels for use in drug delivery. Food Hydrocolloids for Health 2021, 1 , 100011. https://doi.org/10.1016/j.fhfh.2021.100011
    11. Aruto Hori, Rie Utoh, Masumi Yamada, Minoru Seki, . Preparation of Microporous Hydrogel Sponges for 3D Perfusion Culture of Mammalian Cells. MATEC Web of Conferences 2021, 333 , 07004. https://doi.org/10.1051/matecconf/202133307004
    12. Tânia Salvador, Mariana B. Oliveira, João F. Mano. Leachable‐Free Fabrication of Hydrogel Foams Enabling Homogeneous Viability of Encapsulated Cells in Large‐Volume Constructs. Advanced Healthcare Materials 2020, 9 (20) https://doi.org/10.1002/adhm.202000543
    13. Youchuang Chao, Ho Cheung Shum. Emerging aqueous two-phase systems: from fundamentals of interfaces to biomedical applications. Chemical Society Reviews 2020, 49 (1) , 114-142. https://doi.org/10.1039/C9CS00466A

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