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Engineering Highly Vascularized Bone Tissues by 3D Bioprinting of Granular Prevascularized Spheroids

  • Yongcong Fang
    Yongcong Fang
    Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, P. R. China
    Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, P. R. China
    Biomanufacturing and Engineering Living Systems” Innovation International Talents Base (111 Base), Beijing 100084, P. R. China
  • Mengke Ji
    Mengke Ji
    Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, P. R. China
    Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, P. R. China
    Biomanufacturing and Engineering Living Systems” Innovation International Talents Base (111 Base), Beijing 100084, P. R. China
    More by Mengke Ji
  • Bingyan Wu
    Bingyan Wu
    Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, P. R. China
    Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, P. R. China
    Biomanufacturing and Engineering Living Systems” Innovation International Talents Base (111 Base), Beijing 100084, P. R. China
    More by Bingyan Wu
  • Xinxin Xu
    Xinxin Xu
    Senior Department of General Surgery, the First Medical Center, Chinese PLA General Hospital, Beijing 100853, P. R. China
    More by Xinxin Xu
  • Ge Wang
    Ge Wang
    Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, P. R. China
    Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, P. R. China
    Biomanufacturing and Engineering Living Systems” Innovation International Talents Base (111 Base), Beijing 100084, P. R. China
    More by Ge Wang
  • Yanmei Zhang
    Yanmei Zhang
    Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, P. R. China
    Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, P. R. China
    Biomanufacturing and Engineering Living Systems” Innovation International Talents Base (111 Base), Beijing 100084, P. R. China
    More by Yanmei Zhang
  • Yingkai Xia
    Yingkai Xia
    Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, P. R. China
    Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, P. R. China
    Biomanufacturing and Engineering Living Systems” Innovation International Talents Base (111 Base), Beijing 100084, P. R. China
    More by Yingkai Xia
  • Zhe Li
    Zhe Li
    Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, P. R. China
    Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, P. R. China
    Biomanufacturing and Engineering Living Systems” Innovation International Talents Base (111 Base), Beijing 100084, P. R. China
    More by Zhe Li
  • Ting Zhang
    Ting Zhang
    Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, P. R. China
    Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, P. R. China
    Biomanufacturing and Engineering Living Systems” Innovation International Talents Base (111 Base), Beijing 100084, P. R. China
    More by Ting Zhang
  • Wei Sun
    Wei Sun
    Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, P. R. China
    Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, P. R. China
    Biomanufacturing and Engineering Living Systems” Innovation International Talents Base (111 Base), Beijing 100084, P. R. China
    Department of Mechanical Engineering, Drexel University, Philadelphia, Pennsylvania 19104, United States of America
    More by Wei Sun
  • , and 
  • Zhuo Xiong*
    Zhuo Xiong
    Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, P. R. China
    Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, P. R. China
    Biomanufacturing and Engineering Living Systems” Innovation International Talents Base (111 Base), Beijing 100084, P. R. China
    *Email, [email protected]. Phone: +86-135-0111-1907.
    More by Zhuo Xiong
Cite this: ACS Appl. Mater. Interfaces 2023, 15, 37, 43492–43502
Publication Date (Web):September 11, 2023
https://doi.org/10.1021/acsami.3c08550
Copyright © 2023 American Chemical Society

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    Abstract

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    The convergence of 3D bioprinting with powerful manufacturing capability and cellular self-organization that can reproduce intricate tissue microarchitecture and function is a promising direction toward building functional tissues and has yet to be demonstrated. Here, we develop a granular aggregate-prevascularized (GAP) bioink for engineering highly vascularized bone tissues by capitalizing on the condensate-mimicking, self-organization, and angiogenic properties of prevascularized mesenchymal spheroids. The GAP bioink utilizes prevascularized aggregates as building blocks, which are embedded densely in extracellular matrices conducive to spontaneous self-organization. We printed various complex structures with high cell density (∼1.5 × 108 cells/cm3), viability (∼80%), and shape fidelity using GAP bioink. After printing, the prevascularized mesenchymal spheroids developed an interconnected vascular network through angiogenic sprouting. We printed highly vascularized bone tissues using GAP bioink and found that prevascularized spheroids were more conducive to osteogenesis and angiogenesis. We envision that the design of the GAP bioink could be further integrated with human-induced pluripotent stem cell-derived organoids, which opens new avenues to create patient-specific vascularized tissues for therapeutic applications..

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    The Supporting Information is available free of charge on the ACS Publications Web site at DOI: (input by editor). Figures S1–S14 (PDF) The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsami.3c08550.

    • In situ monitoring of HUVEC spheroid formation; immunostaining of MSC/HUVEC spheroids; formation of capillary networks within the fibrin hydrogel on day 7; preparation process for GAP bioink; cell viabilities and densities of spheroids at various volume fractions; rheological characterization of Gelbrin; mechanical characterization of printed cylinders using Gelbrin and Gap bioink; capillary formation by HUVEC self-assembly in Group #4; confocal images of samples in Group #3 on day 7; representative confocal images of samples on day 7; immunofluorescence staining on day 24; H&E, Masson’s trichrome, and Alizarin Red staining on day 17; hydroxyapatite deposition within the printed structures using the GAP bioink by SEM micrographs and EDS spectra on day 24; and osteogenic-related gene expression on day 24 (PDF)

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