Comprehensive analysis of intercellular communication in the thermogenic adipose niche
Abstract Brown adipose tissue (BAT) is responsible for regulating body temperature through adaptive thermogenesis. The ability of thermogenic adipocytes to dissipate chemical energy as heat counteracts weight gain and has gained considerable attention as a strategy against obesity. BAT undergoes maj...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-07-01
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| Series: | Communications Biology |
| Online Access: | https://doi.org/10.1038/s42003-023-05140-2 |
| _version_ | 1827894941865476096 |
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| author | Farnaz Shamsi Rongbin Zheng Li-Lun Ho Kaifu Chen Yu-Hua Tseng |
| author_facet | Farnaz Shamsi Rongbin Zheng Li-Lun Ho Kaifu Chen Yu-Hua Tseng |
| author_sort | Farnaz Shamsi |
| collection | DOAJ |
| description | Abstract Brown adipose tissue (BAT) is responsible for regulating body temperature through adaptive thermogenesis. The ability of thermogenic adipocytes to dissipate chemical energy as heat counteracts weight gain and has gained considerable attention as a strategy against obesity. BAT undergoes major remodeling in a cold environment. This remodeling results from changes in the number and function of brown adipocytes, expanding the network of blood vessels and sympathetic nerves, and changes in the composition and function of immune cells. Such synergistic adaptation requires extensive crosstalk between individual cells in the tissue to coordinate their responses. To understand the mechanisms of intercellular communication in BAT, we apply the CellChat algorithm to single-cell transcriptomic data of mouse BAT. We construct an integrative network of the ligand-receptor interactome in BAT and identify the major signaling inputs and outputs of each cell type. By comparing the ligand-receptor interactions in BAT of mice housed at different environmental temperatures, we show that cold exposure enhances the intercellular interactions among the major cell types in BAT, including adipocytes, adipocyte progenitors, lymphatic and vascular endothelial cells, myelinated and non-myelinated Schwann cells, and immune cells. These interactions are predicted to regulate the remodeling of the extracellular matrix, the inflammatory response, angiogenesis, and neurite growth. Together, our integrative analysis of intercellular communications in BAT and their dynamic regulation in response to housing temperatures provides a new understanding of the mechanisms underlying BAT thermogenesis. The resources presented in this study offer a valuable platform for future investigations of BAT development and thermogenesis. |
| first_indexed | 2024-03-12T22:14:35Z |
| format | Article |
| id | doaj.art-150a708469344cb095751ad474e7d761 |
| institution | Directory Open Access Journal |
| issn | 2399-3642 |
| language | English |
| last_indexed | 2024-03-12T22:14:35Z |
| publishDate | 2023-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Communications Biology |
| spelling | doaj.art-150a708469344cb095751ad474e7d7612023-07-23T11:22:37ZengNature PortfolioCommunications Biology2399-36422023-07-016111210.1038/s42003-023-05140-2Comprehensive analysis of intercellular communication in the thermogenic adipose nicheFarnaz Shamsi0Rongbin Zheng1Li-Lun Ho2Kaifu Chen3Yu-Hua Tseng4Section on Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical SchoolBasic and Translational Research Division, Department of Cardiology, Boston Children’s HospitalComputer Science and Artificial Intelligence Laboratory, Massachusetts Institute of TechnologyBasic and Translational Research Division, Department of Cardiology, Boston Children’s HospitalSection on Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical SchoolAbstract Brown adipose tissue (BAT) is responsible for regulating body temperature through adaptive thermogenesis. The ability of thermogenic adipocytes to dissipate chemical energy as heat counteracts weight gain and has gained considerable attention as a strategy against obesity. BAT undergoes major remodeling in a cold environment. This remodeling results from changes in the number and function of brown adipocytes, expanding the network of blood vessels and sympathetic nerves, and changes in the composition and function of immune cells. Such synergistic adaptation requires extensive crosstalk between individual cells in the tissue to coordinate their responses. To understand the mechanisms of intercellular communication in BAT, we apply the CellChat algorithm to single-cell transcriptomic data of mouse BAT. We construct an integrative network of the ligand-receptor interactome in BAT and identify the major signaling inputs and outputs of each cell type. By comparing the ligand-receptor interactions in BAT of mice housed at different environmental temperatures, we show that cold exposure enhances the intercellular interactions among the major cell types in BAT, including adipocytes, adipocyte progenitors, lymphatic and vascular endothelial cells, myelinated and non-myelinated Schwann cells, and immune cells. These interactions are predicted to regulate the remodeling of the extracellular matrix, the inflammatory response, angiogenesis, and neurite growth. Together, our integrative analysis of intercellular communications in BAT and their dynamic regulation in response to housing temperatures provides a new understanding of the mechanisms underlying BAT thermogenesis. The resources presented in this study offer a valuable platform for future investigations of BAT development and thermogenesis.https://doi.org/10.1038/s42003-023-05140-2 |
| spellingShingle | Farnaz Shamsi Rongbin Zheng Li-Lun Ho Kaifu Chen Yu-Hua Tseng Comprehensive analysis of intercellular communication in the thermogenic adipose niche Communications Biology |
| title | Comprehensive analysis of intercellular communication in the thermogenic adipose niche |
| title_full | Comprehensive analysis of intercellular communication in the thermogenic adipose niche |
| title_fullStr | Comprehensive analysis of intercellular communication in the thermogenic adipose niche |
| title_full_unstemmed | Comprehensive analysis of intercellular communication in the thermogenic adipose niche |
| title_short | Comprehensive analysis of intercellular communication in the thermogenic adipose niche |
| title_sort | comprehensive analysis of intercellular communication in the thermogenic adipose niche |
| url | https://doi.org/10.1038/s42003-023-05140-2 |
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