IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45103-7.html
   My bibliography  Save this article

Chemically-defined and scalable culture system for intestinal stem cells derived from human intestinal organoids

Author

Listed:
  • Ohman Kwon

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Hana Lee

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Jaeeun Jung

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Ye Seul Son

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Sojeong Jeon

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Won Dong Yoo

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST))

  • Naeun Son

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST))

  • Kwang Bo Jung

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Eunho Choi

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST))

  • In-Chul Lee

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    KRIBB, Korea Preclinical Evaluation Center)

  • Hyung-Jun Kwon

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    KRIBB, Korea Preclinical Evaluation Center)

  • Chuna Kim

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST)
    KRIBB, Aging Convergence Research Center)

  • Mi-Ok Lee

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST))

  • Hyun-Soo Cho

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST)
    Sungkyunkwan University)

  • Dae Soo Kim

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST))

  • Mi-Young Son

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST)
    Sungkyunkwan University)

Abstract

Three-dimensional human intestinal organoids (hIO) are widely used as a platform for biological and biomedical research. However, reproducibility and challenges for large-scale expansion limit their applicability. Here, we establish a human intestinal stem cell (ISC) culture method expanded under feeder-free and fully defined conditions through selective enrichment of ISC populations (ISC3D-hIO) within hIO derived from human pluripotent stem cells. The intrinsic self-organisation property of ISC3D-hIO, combined with air-liquid interface culture in a minimally defined medium, forces ISC3D-hIO to differentiate into the intestinal epithelium with cellular diversity, villus-like structure, and barrier integrity. Notably, ISC3D-hIO is an ideal cell source for gene editing to study ISC biology and transplantation for intestinal diseases. We demonstrate the intestinal epithelium differentiated from ISC3D-hIO as a model system to study severe acute respiratory syndrome coronavirus 2 viral infection. ISC3D-hIO culture technology provides a biological tool for use in regenerative medicine and disease modelling.

Suggested Citation

  • Ohman Kwon & Hana Lee & Jaeeun Jung & Ye Seul Son & Sojeong Jeon & Won Dong Yoo & Naeun Son & Kwang Bo Jung & Eunho Choi & In-Chul Lee & Hyung-Jun Kwon & Chuna Kim & Mi-Ok Lee & Hyun-Soo Cho & Dae Soo, 2024. "Chemically-defined and scalable culture system for intestinal stem cells derived from human intestinal organoids," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45103-7
    DOI: 10.1038/s41467-024-45103-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45103-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-45103-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Rasa Elmentaite & Natsuhiko Kumasaka & Kenny Roberts & Aaron Fleming & Emma Dann & Hamish W. King & Vitalii Kleshchevnikov & Monika Dabrowska & Sophie Pritchard & Liam Bolt & Sara F. Vieira & Lira Mam, 2021. "Cells of the human intestinal tract mapped across space and time," Nature, Nature, vol. 597(7875), pages 250-255, September.
    2. Claudia Y. Janda & Luke T. Dang & Changjiang You & Junlei Chang & Wim de Lau & Zhendong A. Zhong & Kelley S. Yan & Owen Marecic & Dirk Siepe & Xingnan Li & James D. Moody & Bart O. Williams & Hans Cle, 2017. "Surrogate Wnt agonists that phenocopy canonical Wnt and β-catenin signalling," Nature, Nature, vol. 545(7653), pages 234-237, May.
    3. Shinya Sugimoto & Eiji Kobayashi & Masayuki Fujii & Yuki Ohta & Kazuya Arai & Mami Matano & Keiko Ishikawa & Kentaro Miyamoto & Kohta Toshimitsu & Sirirat Takahashi & Kosaku Nanki & Yoji Hakamata & Ta, 2021. "An organoid-based organ-repurposing approach to treat short bowel syndrome," Nature, Nature, vol. 592(7852), pages 99-104, April.
    4. 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.
    5. Kwang Bo Jung & Hana Lee & Ye Seul Son & Mi-Ok Lee & Young-Dae Kim & Soo Jin Oh & Ohman Kwon & Sunwha Cho & Hyun-Soo Cho & Dae-Soo Kim & Jung-Hwa Oh & Matthias Zilbauer & Jeong-Ki Min & Cho-Rok Jung &, 2018. "Interleukin-2 induces the in vitro maturation of human pluripotent stem cell-derived intestinal organoids," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    6. Xia Wang & Yusuke Yamamoto & Lane H. Wilson & Ting Zhang & Brooke E. Howitt & Melissa A. Farrow & Florian Kern & Gang Ning & Yue Hong & Chiea Chuen Khor & Benoit Chevalier & Denis Bertrand & Lingyan W, 2015. "Cloning and variation of ground state intestinal stem cells," Nature, Nature, vol. 522(7555), pages 173-178, June.
    7. Yusuke Yamamoto & Xia Wang & Denis Bertrand & Florian Kern & Ting Zhang & Marcin Duleba & Supriya Srivastava & Chiea Chuen Khor & Yuanyu Hu & Lane H. Wilson & Hagen Blaszyk & Daniil Rolshud & Ming Teh, 2016. "Mutational spectrum of Barrett’s stem cells suggests paths to initiation of a precancerous lesion," Nature Communications, Nature, vol. 7(1), pages 1-10, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Eun-Jung Kang & Jae-Hoon Kim & Young Eun Kim & Hana Lee & Kwang Bo Jung & Dong-Ho Chang & Youngjin Lee & Shinhye Park & Eun-Young Lee & Eun-Ji Lee & Ho Bum Kang & Moon-Young Rhyoo & Seungwoo Seo & Soh, 2024. "The secreted protein Amuc_1409 from Akkermansia muciniphila improves gut health through intestinal stem cell regulation," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Pietro Demela & Nicola Pirastu & Blagoje Soskic, 2023. "Cross-disorder genetic analysis of immune diseases reveals distinct gene associations that converge on common pathways," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Susanne Kessler & Bradly Burke & Geoffroy Andrieux & Jan Schinköthe & Lea Hamberger & Johannes Kacza & Shijun Zhan & Clara Reasoner & Taru S. Dutt & Maria Kaukab Osman & Marcela Henao-Tamayo & Julian , 2024. "Deciphering bat influenza H18N11 infection dynamics in male Jamaican fruit bats on a single-cell level," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Naomi Pode-Shakked & Megan Slack & Nambirajan Sundaram & Ruth Schreiber & Kyle W. McCracken & Benjamin Dekel & Michael Helmrath & Raphael Kopan, 2023. "RAAS-deficient organoids indicate delayed angiogenesis as a possible cause for autosomal recessive renal tubular dysgenesis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. 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.
    6. Reza Mirzazadeh & Zaneta Andrusivova & Ludvig Larsson & Phillip T. Newton & Leire Alonso Galicia & Xesús M. Abalo & Mahtab Avijgan & Linda Kvastad & Alexandre Denadai-Souza & Nathalie Stakenborg & Ale, 2023. "Spatially resolved transcriptomic profiling of degraded and challenging fresh frozen samples," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Akshaya Ramakrishnan & Aikaterini Symeonidi & Patrick Hanel & Katharina T. Schmid & Maria L. Richter & Michael Schubert & Maria Colomé-Tatché, 2023. "epiAneufinder identifies copy number alterations from single-cell ATAC-seq data," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    8. Egle Kvedaraite & Magda Lourda & Natalia Mouratidou & Tim Düking & Avinash Padhi & Kirsten Moll & Paulo Czarnewski & Indranil Sinha & Ioanna Xagoraris & Efthymia Kokkinou & Anastasios Damdimopoulos & , 2024. "Intestinal stroma guides monocyte differentiation to macrophages through GM-CSF," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    9. Feng Lin & Xia Li & Shiyu Sun & Zhongyi Li & Chenglin Lv & Jianbo Bai & Lin Song & Yizhao Han & Bo Li & Jianping Fu & Yue Shao, 2023. "Mechanically enhanced biogenesis of gut spheroids with instability-driven morphomechanics," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    10. Nannan Guo & Na Li & Li Jia & Qinyue Jiang & Mette Schreurs & Vincent Unen & Susana M. Chuva Sousa Lopes & Alexandra A. Vloemans & Jeroen Eggermont & Boudewijn Lelieveldt & Frank J. T. Staal & Noel F., 2023. "Immune subset-committed proliferating cells populate the human foetal intestine throughout the second trimester of gestation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    11. Jiarui Ding & John J. Garber & Amiko Uchida & Ariel Lefkovith & Grace T. Carter & Praveen Vimalathas & Lauren Canha & Michael Dougan & Kyle Staller & Joseph Yarze & Toni M. Delorey & Orit Rozenblatt-R, 2024. "An esophagus cell atlas reveals dynamic rewiring during active eosinophilic esophagitis and remission," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    12. Fang-Ling Zhang & Zhen Hu & Yi-Fan Wang & Wen-Juan Zhang & Bo-Wei Zhou & Qi-Shun Sun & Ze-Bin Lin & Ke-Xuan Liu, 2023. "Organoids transplantation attenuates intestinal ischemia/reperfusion injury in mice through L-Malic acid-mediated M2 macrophage polarization," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    13. Alberto Díez-Sánchez & Håvard T. Lindholm & Pia M. Vornewald & Jenny Ostrop & Rouan Yao & Andrew B. Single & Anne Marstad & Naveen Parmar & Tovah N. Shaw & Mara Martín-Alonso & Menno J. Oudhoff, 2024. "LSD1 drives intestinal epithelial maturation and controls small intestinal immune cell composition independent of microbiota in a murine model," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    14. Jia Li & Alan J. Simmons & Caroline V. Hawkins & Sophie Chiron & Marisol A. Ramirez-Solano & Naila Tasneem & Harsimran Kaur & Yanwen Xu & Frank Revetta & Paige N. Vega & Shunxing Bao & Can Cui & Regin, 2024. "Identification and multimodal characterization of a specialized epithelial cell type associated with Crohn’s disease," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    15. Carmen Aguilar & Mindaugas Pauzuolis & Malvika Pompaiah & Ehsan Vafadarnejad & Panagiota Arampatzi & Mara Fischer & Dominik Narres & Mastura Neyazi & Özge Kayisoglu & Thomas Sell & Nils Blüthgen & Mar, 2022. "Helicobacter pylori shows tropism to gastric differentiated pit cells dependent on urea chemotaxis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    16. Yue Wang & Yanbo Yu & Lixiang Li & Mengqi Zheng & Jiawei Zhou & Haifan Gong & Bingcheng Feng & Xiao Wang & Xuanlin Meng & Yanyan Cui & Yanan Xia & Shuzheng Chu & Lin Lin & Huijun Chang & Ruchen Zhou &, 2023. "Bile acid-dependent transcription factors and chromatin accessibility determine regional heterogeneity of intestinal antimicrobial peptides," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    17. James Hillier & Yuguang Zhao & Loic Carrique & Tomas Malinauskas & Reinis R. Ruza & Tao-Hsin Chang & Gangshun Yi & Helen M. E. Duyvesteyn & Jing Yu & Weixian Lu & Els Pardon & Jan Steyaert & Yanan Zhu, 2024. "Structural insights into Frizzled3 through nanobody modulators," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    18. Jie Ding & Sung-Jin Lee & Lukas Vlahos & Kanako Yuki & Cara C. Rada & Vincent Unen & Meghah Vuppalapaty & Hui Chen & Asmiti Sura & Aaron K. McCormick & Madeline Tomaske & Samira Alwahabi & Huy Nguyen , 2023. "Therapeutic blood-brain barrier modulation and stroke treatment by a bioengineered FZD4-selective WNT surrogate in mice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45103-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.