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Endothelial cell-derived stem cell factor promotes lipid accumulation through c-Kit-mediated increase of lipogenic enzymes in brown adipocytes

Author

Listed:
  • Hyuek Jong Lee

    (Institute for Basic Science (IBS))

  • Jueun Lee

    (Korea Basic Science Institute)

  • Myung Jin Yang

    (Institute for Basic Science (IBS)
    Korea Advanced Institute of Science and Technology (KAIST))

  • Young-Chan Kim

    (Institute for Basic Science (IBS)
    Korea Advanced Institute of Science and Technology (KAIST))

  • Seon Pyo Hong

    (Institute for Basic Science (IBS))

  • Jung Mo Kim

    (Institute for Basic Science (IBS))

  • Geum-Sook Hwang

    (Korea Basic Science Institute
    Chung-Ang University)

  • Gou Young Koh

    (Institute for Basic Science (IBS)
    Korea Advanced Institute of Science and Technology (KAIST))

Abstract

Active thermogenesis in the brown adipose tissue (BAT) facilitating the utilization of lipids and glucose is critical for maintaining body temperature and reducing metabolic diseases, whereas inactive BAT accumulates lipids in brown adipocytes (BAs), leading to BAT whitening. Although cellular crosstalk between endothelial cells (ECs) and adipocytes is essential for the transport and utilization of fatty acid in BAs, the angiocrine roles of ECs mediating this crosstalk remain poorly understood. Using single-nucleus RNA sequencing and knock-out male mice, we demonstrate that stem cell factor (SCF) derived from ECs upregulates gene expressions and protein levels of the enzymes for de novo lipogenesis, and promotes lipid accumulation by activating c-Kit in BAs. In the early phase of lipid accumulation induced by denervation or thermoneutrality, transiently expressed c-Kit on BAs increases the protein levels of the lipogenic enzymes via PI3K and AKT signaling. EC-specific SCF deletion and BA-specific c-Kit deletion attenuate the induction of the lipogenic enzymes and suppress the enlargement of lipid droplets in BAs after denervation or thermoneutrality in male mice. These data provide insight into SCF/c-Kit signaling as a regulator that promotes lipid accumulation through the increase of lipogenic enzymes in BAT when thermogenesis is inhibited.

Suggested Citation

  • Hyuek Jong Lee & Jueun Lee & Myung Jin Yang & Young-Chan Kim & Seon Pyo Hong & Jung Mo Kim & Geum-Sook Hwang & Gou Young Koh, 2023. "Endothelial cell-derived stem cell factor promotes lipid accumulation through c-Kit-mediated increase of lipogenic enzymes in brown adipocytes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38433-5
    DOI: 10.1038/s41467-023-38433-5
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    1. Tim J. Schulz & Ping Huang & Tian Lian Huang & Ruidan Xue & Lindsay E. McDougall & Kristy L. Townsend & Aaron M. Cypess & Yuji Mishina & Emanuela Gussoni & Yu-Hua Tseng, 2013. "Brown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat," Nature, Nature, vol. 495(7441), pages 379-383, March.
    2. Zan Huang & Hai-Bin Ruan & Li Xian & Weiqian Chen & Shujun Jiang & Anying Song & Qinghua Wang & Peiliang Shi & Xingxing Gu & Xiang Gao, 2014. "The stem cell factor/Kit signalling pathway regulates mitochondrial function and energy expenditure," Nature Communications, Nature, vol. 5(1), pages 1-10, September.
    3. Lei Ding & Thomas L. Saunders & Grigori Enikolopov & Sean J. Morrison, 2012. "Endothelial and perivascular cells maintain haematopoietic stem cells," Nature, Nature, vol. 481(7382), pages 457-462, January.
    4. Suoqin Jin & Christian F. Guerrero-Juarez & Lihua Zhang & Ivan Chang & Raul Ramos & Chen-Hsiang Kuan & Peggy Myung & Maksim V. Plikus & Qing Nie, 2021. "Inference and analysis of cell-cell communication using CellChat," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    5. Bo Shen & Alpaslan Tasdogan & Jessalyn M. Ubellacker & Jingzhu Zhang & Elena D. Nosyreva & Liming Du & Malea M. Murphy & Shuiqing Hu & Yating Yi & Nergis Kara & Xin Liu & Shay Guela & Yuemeng Jia & Vi, 2021. "A mechanosensitive peri-arteriolar niche for osteogenesis and lymphopoiesis," Nature, Nature, vol. 591(7850), pages 438-444, March.
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