IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-44181-3.html
   My bibliography  Save this article

Unique adipose tissue invariant natural killer T cell subpopulations control adipocyte turnover in mice

Author

Listed:
  • Sang Mun Han

    (Seoul National University)

  • Eun Seo Park

    (DGIST)

  • Jeu Park

    (Seoul National University)

  • Hahn Nahmgoong

    (Seoul National University)

  • Yoon Ha Choi

    (POSTECH)

  • Jiyoung Oh

    (College of Information and Biotechnology, Ulsan National Institute of Science and Technology)

  • Kyung Min Yim

    (Seoul National University)

  • Won Taek Lee

    (Seoul National University)

  • Yun Kyung Lee

    (Seoul National University College of Medicine & Seoul National University Bundang Hospital)

  • Yong Geun Jeon

    (Seoul National University)

  • Kyung Cheul Shin

    (Seoul National University)

  • Jin Young Huh

    (Sogang University)

  • Sung Hee Choi

    (Seoul National University College of Medicine & Seoul National University Bundang Hospital)

  • Jiyoung Park

    (College of Information and Biotechnology, Ulsan National Institute of Science and Technology)

  • Jong Kyoung Kim

    (POSTECH)

  • Jae Bum Kim

    (Seoul National University)

Abstract

Adipose tissue invariant natural killer T (iNKT) cells are a crucial cell type for adipose tissue homeostasis in obese animals. However, heterogeneity of adipose iNKT cells and their function in adipocyte turnover are not thoroughly understood. Here, we investigate transcriptional heterogeneity in adipose iNKT cells and their hierarchy using single-cell RNA sequencing in lean and obese mice. We report that distinct subpopulations of adipose iNKT cells modulate adipose tissue homeostasis through adipocyte death and birth. We identify KLRG1+ iNKT cells as a unique iNKT cell subpopulation in adipose tissue. Adoptive transfer experiments showed that KLRG1+ iNKT cells are selectively generated within adipose tissue microenvironment and differentiate into a CX3CR1+ cytotoxic subpopulation in obese mice. In addition, CX3CR1+ iNKT cells specifically kill enlarged and inflamed adipocytes and recruit macrophages through CCL5. Furthermore, adipose iNKT17 cells have the potential to secrete AREG, and AREG is involved in stimulating adipose stem cell proliferation. Collectively, our data suggest that each adipose iNKT cell subpopulation plays key roles in the control of adipocyte turnover via interaction with adipocytes, adipose stem cells, and macrophages in adipose tissue.

Suggested Citation

  • Sang Mun Han & Eun Seo Park & Jeu Park & Hahn Nahmgoong & Yoon Ha Choi & Jiyoung Oh & Kyung Min Yim & Won Taek Lee & Yun Kyung Lee & Yong Geun Jeon & Kyung Cheul Shin & Jin Young Huh & Sung Hee Choi &, 2023. "Unique adipose tissue invariant natural killer T cell subpopulations control adipocyte turnover in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-44181-3
    DOI: 10.1038/s41467-023-44181-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44181-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-44181-3?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. Kirsty L. Spalding & Erik Arner & Pål O. Westermark & Samuel Bernard & Bruce A. Buchholz & Olaf Bergmann & Lennart Blomqvist & Johan Hoffstedt & Erik Näslund & Tom Britton & Hernan Concha & Moustapha , 2008. "Dynamics of fat cell turnover in humans," Nature, Nature, vol. 453(7196), pages 783-787, June.
    2. Matthew A. Cottam & Heather L. Caslin & Nathan C. Winn & Alyssa H. Hasty, 2022. "Multiomics reveals persistence of obesity-associated immune cell phenotypes in adipose tissue during weight loss and weight regain in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Margo P. Emont & Christopher Jacobs & Adam L. Essene & Deepti Pant & Danielle Tenen & Georgia Colleluori & Angelica Vincenzo & Anja M. Jørgensen & Hesam Dashti & Adam Stefek & Elizabeth McGonagle & So, 2022. "A single-cell atlas of human and mouse white adipose tissue," Nature, Nature, vol. 603(7903), pages 926-933, March.
    4. Julie Zikherman & Ramya Parameswaran & Arthur Weiss, 2012. "Endogenous antigen tunes the responsiveness of naive B cells but not T cells," Nature, Nature, vol. 489(7414), pages 160-164, September.
    5. Minji Lee & Eunmin Lee & Seong Kyu Han & Yoon Ha Choi & Dong-il Kwon & Hyobeen Choi & Kwanghwan Lee & Eun Seo Park & Min-Seok Rha & Dong Jin Joo & Eui-Cheol Shin & Sanguk Kim & Jong Kyoung Kim & You J, 2020. "Single-cell RNA sequencing identifies shared differentiation paths of mouse thymic innate T cells," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    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. Isabel Reinisch & Helene Michenthaler & Alba Sulaj & Elisabeth Moyschewitz & Jelena Krstic & Markus Galhuber & Ruonan Xu & Zina Riahi & Tongtong Wang & Nemanja Vujic & Melina Amor & Riccardo Zenezini , 2024. "Adipocyte p53 coordinates the response to intermittent fasting by regulating adipose tissue immune cell landscape," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    2. Chih-Hao Wang & Tadataka Tsuji & Li-Hong Wu & Cheng-Ying Yang & Tian Lian Huang & Mari Sato & Farnaz Shamsi & Yu-Hua Tseng, 2024. "Endothelin 3/EDNRB signaling induces thermogenic differentiation of white adipose tissue," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Shuai Yan & Anna Santoro & Micah J. Niphakis & Antonio M. Pinto & Christopher L. Jacobs & Rasheed Ahmad & Radu M. Suciu & Bryan R. Fonslow & Rachel A. Herbst-Graham & Nhi Ngo & Cassandra L. Henry & Dy, 2024. "Inflammation causes insulin resistance in mice via interferon regulatory factor 3 (IRF3)-mediated reduction in FAHFA levels," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Sanil Patel & Khatanzul Ganbold & Chung Hwan Cho & Juwairriyyah Siddiqui & Ramazan Yildiz & Njeri Sparman & Shani Sadeh & Christy M. Nguyen & Jiexin Wang & Julian P. Whitelegge & Susan K. Fried & Hiro, 2024. "Transcription factor PATZ1 promotes adipogenesis by controlling promoter regulatory loci of adipogenic factors," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. 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.
    6. Clark, Andrew E. & Etilé, Fabrice, 2011. "Happy house: Spousal weight and individual well-being," Journal of Health Economics, Elsevier, vol. 30(5), pages 1124-1136.
    7. Belot, Michèle & James, Jonathan, 2022. "Incentivizing dietary choices among children: Review of experimental evidence," Food Policy, Elsevier, vol. 111(C).
    8. Lin Qi & Marko Groeger & Aditi Sharma & Ishan Goswami & Erzhen Chen & Fenmiao Zhong & Apsara Ram & Kevin Healy & Edward C. Hsiao & Holger Willenbring & Andreas Stahl, 2024. "Adipocyte inflammation is the primary driver of hepatic insulin resistance in a human iPSC-based microphysiological system," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    9. Mikala JoAnn Simpson & Anna Minh Newen & Christopher McNees & Sukriti Sharma & Dylan Pfannenstiel & Thomas Moyer & David Stephany & Iyadh Douagi & Qiao Wang & Christian Thomas Mayer, 2024. "Peripheral apoptosis and limited clonal deletion during physiologic murine B lymphocyte development," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. Wei Perng & Mercedes Mora-Plazas & Constanza Marín & Laura S Rozek & Ana Baylin & Eduardo Villamor, 2013. "A Prospective Study of LINE-1DNA Methylation and Development of Adiposity in School-Age Children," PLOS ONE, Public Library of Science, vol. 8(4), pages 1-7, April.
    11. Heather J. Faust & Tan-Yun Cheng & Ilya Korsunsky & Gerald F. M. Watts & Shani T. Gal-Oz & William V. Trim & Suppawat Kongthong & Anna Helena Jonsson & Daimon P. Simmons & Fan Zhang & Robert Padera & , 2024. "Adipocyte associated glucocorticoid signaling regulates normal fibroblast function which is lost in inflammatory arthritis," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    12. Hongdong Wang & Yanhua Du & Shanshan Huang & Xitai Sun & Youqiong Ye & Haixiang Sun & Xuehui Chu & Xiaodong Shan & Yue Yuan & Lei Shen & Yan Bi, 2024. "Single-cell analysis reveals a subpopulation of adipose progenitor cells that impairs glucose homeostasis," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    13. Suyang Wu & Chen Qiu & Jiahao Ni & Wenli Guo & Jiyuan Song & Xingyin Yang & Yulin Sun & Yanjun Chen & Yunxia Zhu & Xiaoai Chang & Peng Sun & Chunxia Wang & Kai Li & Xiao Han, 2024. "M2 macrophages independently promote beige adipogenesis via blocking adipocyte Ets1," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    14. Benjamin M. Steiner & Abigail M. Benvie & Derek Lee & Yuwei Jiang & Daniel C. Berry, 2024. "Cxcr4 regulates a pool of adipocyte progenitors and contributes to adiposity in a sex-dependent manner," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    15. Aina Lluch & Jessica Latorre & Angela Serena-Maione & Isabel Espadas & Estefanía Caballano-Infantes & José M. Moreno-Navarrete & Núria Oliveras-Cañellas & Wifredo Ricart & María M. Malagón & Alejandro, 2023. "Impaired Plakophilin-2 in obesity breaks cell cycle dynamics to breed adipocyte senescence," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    16. Liam McAllan & Damir Baranasic & Sergio Villicaña & Scarlett Brown & Weihua Zhang & Benjamin Lehne & Marco Adamo & Andrew Jenkinson & Mohamed Elkalaawy & Borzoueh Mohammadi & Majid Hashemi & Nadia Fer, 2023. "Integrative genomic analyses in adipocytes implicate DNA methylation in human obesity and diabetes," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    17. Andreas Fønss Møller & Jesper Grud Skat Madsen, 2023. "JOINTLY: interpretable joint clustering of single-cell transcriptomes," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    18. Cheoljun Choi & Yujin L. Jeong & Koung-Min Park & Minji Kim & Sangseob Kim & Honghyun Jo & Sumin Lee & Heeseong Kim & Garam Choi & Yoon Ha Choi & Je Kyung Seong & Sik Namgoong & Yeonseok Chung & Young, 2024. "TM4SF19-mediated control of lysosomal activity in macrophages contributes to obesity-induced inflammation and metabolic dysfunction," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    19. 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.
    20. Nur Zuliani Ramli & Kok-Yong Chin & Khairul Anwar Zarkasi & Fairus Ahmad, 2019. "The Beneficial Effects of Stingless Bee Honey from Heterotrigona itama against Metabolic Changes in Rats Fed with High-Carbohydrate and High-Fat Diet," IJERPH, MDPI, vol. 16(24), pages 1-17, 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:14:y:2023:i:1:d:10.1038_s41467-023-44181-3. 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.