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The role of somatosensory innervation of adipose tissues

Adipose tissues communicate with the central nervous system to maintain whole-body energy homeostasis. The mainstream view is that circulating hormones secreted by the fat convey the metabolic state to the brain, which integrates peripheral information and regulates adipocyte function through noradr...

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Autores principales: Wang, Yu, Leung, Verina H., Zhang, Yunxiao, Nudell, Victoria S., Loud, Meaghan, Servin-Vences, M. Rocio, Yang, Dong, Wang, Kristina, Moya-Garzon, Maria Dolores, Li, Veronica L., Long, Jonathan Z., Patapoutian, Ardem, Ye, Li
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9477745/
https://www.ncbi.nlm.nih.gov/pubmed/36045288
http://dx.doi.org/10.1038/s41586-022-05137-7
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author Wang, Yu
Leung, Verina H.
Zhang, Yunxiao
Nudell, Victoria S.
Loud, Meaghan
Servin-Vences, M. Rocio
Yang, Dong
Wang, Kristina
Moya-Garzon, Maria Dolores
Li, Veronica L.
Long, Jonathan Z.
Patapoutian, Ardem
Ye, Li
author_facet Wang, Yu
Leung, Verina H.
Zhang, Yunxiao
Nudell, Victoria S.
Loud, Meaghan
Servin-Vences, M. Rocio
Yang, Dong
Wang, Kristina
Moya-Garzon, Maria Dolores
Li, Veronica L.
Long, Jonathan Z.
Patapoutian, Ardem
Ye, Li
author_sort Wang, Yu
collection PubMed
description Adipose tissues communicate with the central nervous system to maintain whole-body energy homeostasis. The mainstream view is that circulating hormones secreted by the fat convey the metabolic state to the brain, which integrates peripheral information and regulates adipocyte function through noradrenergic sympathetic output(1). Moreover, somatosensory neurons of the dorsal root ganglia innervate adipose tissue(2). However, the lack of genetic tools to selectively target these neurons has limited understanding of their physiological importance. Here we developed viral, genetic and imaging strategies to manipulate sensory nerves in an organ-specific manner in mice. This enabled us to visualize the entire axonal projection of dorsal root ganglia from the soma to subcutaneous adipocytes, establishing the anatomical underpinnings of adipose sensory innervation. Functionally, selective sensory ablation in adipose tissue enhanced the lipogenic and thermogenetic transcriptional programs, resulting in an enlarged fat pad, enrichment of beige adipocytes and elevated body temperature under thermoneutral conditions. The sensory-ablation-induced phenotypes required intact sympathetic function. We postulate that beige-fat-innervating sensory neurons modulate adipocyte function by acting as a brake on the sympathetic system. These results reveal an important role of the innervation by dorsal root ganglia of adipose tissues, and could enable future studies to examine the role of sensory innervation of disparate interoceptive systems.
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spelling pubmed-94777452022-09-17 The role of somatosensory innervation of adipose tissues Wang, Yu Leung, Verina H. Zhang, Yunxiao Nudell, Victoria S. Loud, Meaghan Servin-Vences, M. Rocio Yang, Dong Wang, Kristina Moya-Garzon, Maria Dolores Li, Veronica L. Long, Jonathan Z. Patapoutian, Ardem Ye, Li Nature Article Adipose tissues communicate with the central nervous system to maintain whole-body energy homeostasis. The mainstream view is that circulating hormones secreted by the fat convey the metabolic state to the brain, which integrates peripheral information and regulates adipocyte function through noradrenergic sympathetic output(1). Moreover, somatosensory neurons of the dorsal root ganglia innervate adipose tissue(2). However, the lack of genetic tools to selectively target these neurons has limited understanding of their physiological importance. Here we developed viral, genetic and imaging strategies to manipulate sensory nerves in an organ-specific manner in mice. This enabled us to visualize the entire axonal projection of dorsal root ganglia from the soma to subcutaneous adipocytes, establishing the anatomical underpinnings of adipose sensory innervation. Functionally, selective sensory ablation in adipose tissue enhanced the lipogenic and thermogenetic transcriptional programs, resulting in an enlarged fat pad, enrichment of beige adipocytes and elevated body temperature under thermoneutral conditions. The sensory-ablation-induced phenotypes required intact sympathetic function. We postulate that beige-fat-innervating sensory neurons modulate adipocyte function by acting as a brake on the sympathetic system. These results reveal an important role of the innervation by dorsal root ganglia of adipose tissues, and could enable future studies to examine the role of sensory innervation of disparate interoceptive systems. Nature Publishing Group UK 2022-08-31 2022 /pmc/articles/PMC9477745/ /pubmed/36045288 http://dx.doi.org/10.1038/s41586-022-05137-7 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Wang, Yu
Leung, Verina H.
Zhang, Yunxiao
Nudell, Victoria S.
Loud, Meaghan
Servin-Vences, M. Rocio
Yang, Dong
Wang, Kristina
Moya-Garzon, Maria Dolores
Li, Veronica L.
Long, Jonathan Z.
Patapoutian, Ardem
Ye, Li
The role of somatosensory innervation of adipose tissues
title The role of somatosensory innervation of adipose tissues
title_full The role of somatosensory innervation of adipose tissues
title_fullStr The role of somatosensory innervation of adipose tissues
title_full_unstemmed The role of somatosensory innervation of adipose tissues
title_short The role of somatosensory innervation of adipose tissues
title_sort role of somatosensory innervation of adipose tissues
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9477745/
https://www.ncbi.nlm.nih.gov/pubmed/36045288
http://dx.doi.org/10.1038/s41586-022-05137-7
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