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Tissue extracellular matrix hydrogels as alternatives to Matrigel for culturing gastrointestinal organoids

Author

Listed:
  • Suran Kim

    (Yonsei University)

  • Sungjin Min

    (Yonsei University)

  • Yi Sun Choi

    (Yonsei University)

  • Sung-Hyun Jo

    (Soongsil University)

  • Jae Hun Jung

    (Yonsei University College of Medicine)

  • Kyusun Han

    (Yonsei University College of Medicine)

  • Jin Kim

    (Yonsei University)

  • Soohwan An

    (Yonsei University)

  • Yong Woo Ji

    (Yonsei University College of Medicine
    National Health Insurance Service Ilsan Hospital)

  • Yun-Gon Kim

    (Soongsil University)

  • Seung-Woo Cho

    (Yonsei University
    Institute for Basic Science (IBS)
    Advanced Science Institute, Yonsei University)

Abstract

Matrigel, a mouse tumor extracellular matrix protein mixture, is an indispensable component of most organoid tissue culture. However, it has limited the utility of organoids for drug development and regenerative medicine due to its tumor-derived origin, batch-to-batch variation, high cost, and safety issues. Here, we demonstrate that gastrointestinal tissue-derived extracellular matrix hydrogels are suitable substitutes for Matrigel in gastrointestinal organoid culture. We found that the development and function of gastric or intestinal organoids grown in tissue extracellular matrix hydrogels are comparable or often superior to those in Matrigel. In addition, gastrointestinal extracellular matrix hydrogels enabled long-term subculture and transplantation of organoids by providing gastrointestinal tissue-mimetic microenvironments. Tissue-specific and age-related extracellular matrix profiles that affect organoid development were also elucidated through proteomic analysis. Together, our results suggest that extracellular matrix hydrogels derived from decellularized gastrointestinal tissues are effective alternatives to the current gold standard, Matrigel, and produce organoids suitable for gastrointestinal disease modeling, drug development, and tissue regeneration.

Suggested Citation

  • Suran Kim & Sungjin Min & Yi Sun Choi & Sung-Hyun Jo & Jae Hun Jung & Kyusun Han & Jin Kim & Soohwan An & Yong Woo Ji & Yun-Gon Kim & Seung-Woo Cho, 2022. "Tissue extracellular matrix hydrogels as alternatives to Matrigel for culturing gastrointestinal organoids," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29279-4
    DOI: 10.1038/s41467-022-29279-4
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    1. Falguni Pati & Jinah Jang & Dong-Heon Ha & Sung Won Kim & Jong-Won Rhie & Jin-Hyung Shim & Deok-Ho Kim & Dong-Woo Cho, 2014. "Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink," Nature Communications, Nature, vol. 5(1), pages 1-11, September.
    2. Björn Schwanhäusser & Dorothea Busse & Na Li & Gunnar Dittmar & Johannes Schuchhardt & Jana Wolf & Wei Chen & Matthias Selbach, 2011. "Global quantification of mammalian gene expression control," Nature, Nature, vol. 473(7347), pages 337-342, May.
    3. Toshiro Sato & Robert G. Vries & Hugo J. Snippert & Marc van de Wetering & Nick Barker & Daniel E. Stange & Johan H. van Es & Arie Abo & Pekka Kujala & Peter J. Peters & Hans Clevers, 2009. "Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche," Nature, Nature, vol. 459(7244), pages 262-265, May.
    4. So Hyun Kim & Sun-Kyoung Im & Soo-Jin Oh & Sohyeon Jeong & Eui-Sung Yoon & C. Justin Lee & Nakwon Choi & Eun-Mi Hur, 2017. "Anisotropically organized three-dimensional culture platform for reconstruction of a hippocampal neural network," Nature Communications, Nature, vol. 8(1), pages 1-16, April.
    5. Jason R. Spence & Christopher N. Mayhew & Scott A. Rankin & Matthew F. Kuhar & Jefferson E. Vallance & Kathryn Tolle & Elizabeth E. Hoskins & Vladimir V. Kalinichenko & Susanne I. Wells & Aaron M. Zor, 2011. "Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro," Nature, Nature, vol. 470(7332), pages 105-109, February.
    6. Giovanni Giuseppe Giobbe & Claire Crowley & Camilla Luni & Sara Campinoti & Moustafa Khedr & Kai Kretzschmar & Martina Maria De Santis & Elisa Zambaiti & Federica Michielin & Laween Meran & Qianjiang , 2019. "Extracellular matrix hydrogel derived from decellularized tissues enables endodermal organoid culture," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    7. Meritxell Huch & Craig Dorrell & Sylvia F. Boj & Johan H. van Es & Vivian S. W. Li & Marc van de Wetering & Toshiro Sato & Karien Hamer & Nobuo Sasaki & Milton J. Finegold & Annelise Haft & Robert G. , 2013. "In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration," Nature, Nature, vol. 494(7436), pages 247-250, February.
    8. Nikolce Gjorevski & Norman Sachs & Andrea Manfrin & Sonja Giger & Maiia E. Bragina & Paloma Ordóñez-Morán & Hans Clevers & Matthias P. Lutolf, 2016. "Designer matrices for intestinal stem cell and organoid culture," Nature, Nature, vol. 539(7630), pages 560-564, November.
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    2. Sungjin Min & Suran Kim & Woo-Sup Sim & Yi Sun Choi & Hyebin Joo & Jae-Hyun Park & Su-Jin Lee & Hyeok Kim & Mi Jeong Lee & Inhea Jeong & Baofang Cui & Sung-Hyun Jo & Jin-Ju Kim & Seok Beom Hong & Yeon, 2024. "Versatile human cardiac tissues engineered with perfusable heart extracellular microenvironment for biomedical applications," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    3. Yongcheng Jin & Ellina Mikhailova & Ming Lei & Sally A. Cowley & Tianyi Sun & Xingyun Yang & Yujia Zhang & Kaili Liu & Daniel Catarino da Silva & Luana Campos Soares & Sara Bandiera & Francis G. Szele, 2023. "Integration of 3D-printed cerebral cortical tissue into an ex vivo lesioned brain slice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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