IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28226-7.html
   My bibliography  Save this article

Generation of the organotypic kidney structure by integrating pluripotent stem cell-derived renal stroma

Author

Listed:
  • Shunsuke Tanigawa

    (Kumamoto University)

  • Etsuko Tanaka

    (Kumamoto University)

  • Koichiro Miike

    (Kumamoto University)

  • Tomoko Ohmori

    (Kumamoto University)

  • Daisuke Inoue

    (Kumamoto University)

  • Chen-Leng Cai

    (Indiana University School of Medicine)

  • Atsuhiro Taguchi

    (Kumamoto University
    Max Planck Institute for Molecular Genetics)

  • Akio Kobayashi

    (Kumamoto University)

  • Ryuichi Nishinakamura

    (Kumamoto University)

Abstract

Organs consist of the parenchyma and stroma, the latter of which coordinates the generation of organotypic structures. Despite recent advances in organoid technology, induction of organ-specific stroma and recapitulation of complex organ configurations from pluripotent stem cells (PSCs) have remained challenging. By elucidating the in vivo molecular features of the renal stromal lineage at a single-cell resolution level, we herein establish an in vitro induction protocol for stromal progenitors (SPs) from mouse PSCs. When the induced SPs are assembled with two differentially induced parenchymal progenitors (nephron progenitors and ureteric buds), the completely PSC-derived organoids reproduce the complex kidney structure, with multiple types of stromal cells distributed along differentiating nephrons and branching ureteric buds. Thus, integration of PSC-derived lineage-specific stroma into parenchymal organoids will pave the way toward recapitulation of the organotypic architecture and functions.

Suggested Citation

  • Shunsuke Tanigawa & Etsuko Tanaka & Koichiro Miike & Tomoko Ohmori & Daisuke Inoue & Chen-Leng Cai & Atsuhiro Taguchi & Akio Kobayashi & Ryuichi Nishinakamura, 2022. "Generation of the organotypic kidney structure by integrating pluripotent stem cell-derived renal stroma," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28226-7
    DOI: 10.1038/s41467-022-28226-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28226-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28226-7?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. Lu Han & Praneet Chaturvedi & Keishi Kishimoto & Hiroyuki Koike & Talia Nasr & Kentaro Iwasawa & Kirsten Giesbrecht & Phillip C. Witcher & Alexandra Eicher & Lauren Haines & Yarim Lee & John M. Shanno, 2020. "Single cell transcriptomics identifies a signaling network coordinating endoderm and mesoderm diversification during foregut organogenesis," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    2. Matthew B. Buechler & Rachana N. Pradhan & Akshay T. Krishnamurty & Christian Cox & Aslihan Karabacak Calviello & Amber W. Wang & Yeqing Angela Yang & Lucinda Tam & Roger Caothien & Merone Roose-Girma, 2021. "Cross-tissue organization of the fibroblast lineage," Nature, Nature, vol. 593(7860), pages 575-579, May.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Jessica M. Vanslambrouck & Sean B. Wilson & Ker Sin Tan & Ella Groenewegen & Rajeev Rudraraju & Jessica Neil & Kynan T. Lawlor & Sophia Mah & Michelle Scurr & Sara E. Howden & Kanta Subbarao & Melissa, 2022. "Enhanced metanephric specification to functional proximal tubule enables toxicity screening and infectious disease modelling in kidney organoids," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    2. Lele Song & Qinglan Li & Lingbo Xia & Arushi Eesha Sahay & Qi Qiu & Yuanyuan Li & Haitao Li & Kotaro Sasaki & Katalin Susztak & Hao Wu & Liling Wan, 2024. "Single-cell multiomics reveals ENL mutation perturbs kidney developmental trajectory by rewiring gene regulatory landscape," Nature Communications, Nature, vol. 15(1), pages 1-26, December.

    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. Lu Han & Yongxia Wu & Kun Fang & Sean Sweeney & Ulyss K. Roesner & Melodie Parrish & Khushbu Patel & Tom Walter & Julia Piermattei & Anthony Trimboli & Julia Lefler & Cynthia D. Timmers & Xue-Zhong Yu, 2023. "The splanchnic mesenchyme is the tissue of origin for pancreatic fibroblasts during homeostasis and tumorigenesis," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Kotaro Shimizu & Junichi Kikuta & Yumi Ohta & Yutaka Uchida & Yu Miyamoto & Akito Morimoto & Shinya Yari & Takashi Sato & Takefumi Kamakura & Kazuo Oshima & Ryusuke Imai & Yu-Chen Liu & Daisuke Okuzak, 2023. "Single-cell transcriptomics of human cholesteatoma identifies an activin A-producing osteoclastogenic fibroblast subset inducing bone destruction," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. LiangYu Zhao & Sha Han & HengChuan Su & JianYing Li & ErLei Zhi & Peng Li & ChenCheng Yao & RuHui Tian & HuiXing Chen & HuiRong Chen & JiaQiang Luo & ChenKun Shi & ZhiYong Ji & JianLin Hu & Gang Wu & , 2022. "Single-cell transcriptome atlas of the human corpus cavernosum," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Ryan J. Smith & Hongpan Zhang & Shengen Shawn Hu & Theodora Yung & Roshane Francis & Lilian Lee & Mark W. Onaitis & Peter B. Dirks & Chongzhi Zang & Tae-Hee Kim, 2022. "Single-cell chromatin profiling of the primitive gut tube reveals regulatory dynamics underlying lineage fate decisions," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Fabian Peisker & Maurice Halder & James Nagai & Susanne Ziegler & Nadine Kaesler & Konrad Hoeft & Ronghui Li & Eric M. J. Bindels & Christoph Kuppe & Julia Moellmann & Michael Lehrke & Christian Stopp, 2022. "Mapping the cardiac vascular niche in heart failure," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    6. Amir Dailamy & Weiqi Lyu & Sami Nourreddine & Michael Tong & Joseph Rainaldi & Daniella McDonald & Rebecca Panwala & Alysson Muotri & Michael S. Breen & Kun Zhang & Prashant Mali, 2024. "Charting and probing the activity of ADARs in human development and cell-fate specification," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Martin Uhrbom & Lars Muhl & Guillem Genové & Jianping Liu & Henrik Palmgren & Ida Alexandersson & Fredrik Karlsson & Alex-Xianghua Zhou & Sandra Lunnerdal & Sonja Gustafsson & Byambajav Buyandelger & , 2024. "Adipose stem cells are sexually dimorphic cells with dual roles as preadipocytes and resident fibroblasts," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    8. Lucas Massier & Jutta Jalkanen & Merve Elmastas & Jiawei Zhong & Tongtong Wang & Pamela A. Nono Nankam & Scott Frendo-Cumbo & Jesper Bäckdahl & Narmadha Subramanian & Takuya Sekine & Alastair G. Kerr , 2023. "An integrated single cell and spatial transcriptomic map of human white adipose tissue," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    9. Andrea Toth & Paranthaman Kannan & John Snowball & Matthew Kofron & Joseph A. Wayman & James P. Bridges & Emily R. Miraldi & Daniel Swarr & William J. Zacharias, 2023. "Alveolar epithelial progenitor cells require Nkx2-1 to maintain progenitor-specific epigenomic state during lung homeostasis and regeneration," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    10. Karin D. Prummel & Helena L. Crowell & Susan Nieuwenhuize & Eline C. Brombacher & Stephan Daetwyler & Charlotte Soneson & Jelena Kresoja-Rakic & Agnese Kocere & Manuel Ronner & Alexander Ernst & Zahra, 2022. "Hand2 delineates mesothelium progenitors and is reactivated in mesothelioma," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    11. Kathryn Weinand & Saori Sakaue & Aparna Nathan & Anna Helena Jonsson & Fan Zhang & Gerald F. M. Watts & Majd Al Suqri & Zhu Zhu & Deepak A. Rao & Jennifer H. Anolik & Michael B. Brenner & Laura T. Don, 2024. "The chromatin landscape of pathogenic transcriptional cell states in rheumatoid arthritis," Nature Communications, Nature, vol. 15(1), pages 1-25, December.
    12. Julia M. Houthuijzen & Roebi Bruijn & Eline Burg & Anne Paulien Drenth & Ellen Wientjens & Tamara Filipovic & Esme Bullock & Chiara S. Brambillasca & Emilia M. Pulver & Marja Nieuwland & Iris Rink & F, 2023. "CD26-negative and CD26-positive tissue-resident fibroblasts contribute to functionally distinct CAF subpopulations in breast cancer," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    13. Paula Punzon-Jimenez & Alba Machado-Lopez & Raul Perez-Moraga & Jaime Llera-Oyola & Daniela Grases & Marta Galvez-Viedma & Mustafa Sibai & Elena Satorres-Perez & Susana Lopez-Agullo & Rafael Badenes &, 2024. "Effect of aging on the human myometrium at single-cell resolution," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    14. Christopher J. Hanley & Sara Waise & Matthew J. Ellis & Maria A. Lopez & Wai Y. Pun & Julian Taylor & Rachel Parker & Lucy M. Kimbley & Serena J. Chee & Emily C. Shaw & Jonathan West & Aiman Alzetani , 2023. "Single-cell analysis reveals prognostic fibroblast subpopulations linked to molecular and immunological subtypes of lung cancer," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    15. Chen Ni & Xiaohan Lou & Xiaohan Yao & Linlin Wang & Jiajia Wan & Xixi Duan & Jialu Liang & Kaili Zhang & Yuanyuan Yang & Li Zhang & Chanjun Sun & Zhenzhen Li & Ming Wang & Linyu Zhu & Dekang Lv & Zhih, 2022. "ZIP1+ fibroblasts protect lung cancer against chemotherapy via connexin-43 mediated intercellular Zn2+ transfer," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    16. Mariana A. Branco & Tiago P. Dias & Joaquim M. S. Cabral & Perpetua Pinto-do-Ó & Maria Margarida Diogo, 2022. "Human multilineage pro-epicardium/foregut organoids support the development of an epicardium/myocardium organoid," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    17. Simone Isling Pærregaard & Line Wulff & Sophie Schussek & Kristoffer Niss & Urs Mörbe & Johan Jendholm & Kerstin Wendland & Anna T. Andrusaite & Kevin F. Brulois & Robert J. B. Nibbs & Katarzyna Sitni, 2023. "The small and large intestine contain related mesenchymal subsets that derive from embryonic Gli1+ precursors," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    18. Martin Arostegui & R. Wilder Scott & Kerstin Böse & T. Michael Underhill, 2022. "Cellular taxonomy of Hic1+ mesenchymal progenitor derivatives in the limb: from embryo to adult," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    19. Joern Pezoldt & Carolin Wiechers & Mangge Zou & Maria Litovchenko & Marjan Biocanin & Michael Beckstette & Katarzyna Sitnik & Martina Palatella & Guido Mierlo & Wanze Chen & Vincent Gardeux & Stefan F, 2022. "Postnatal expansion of mesenteric lymph node stromal cells towards reticular and CD34+ stromal cell subsets," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    20. Lena Cords & Sandra Tietscher & Tobias Anzeneder & Claus Langwieder & Martin Rees & Natalie Souza & Bernd Bodenmiller, 2023. "Cancer-associated fibroblast classification in single-cell and spatial proteomics data," Nature Communications, Nature, vol. 14(1), pages 1-13, 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:13:y:2022:i:1:d:10.1038_s41467-022-28226-7. 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.