Single-nucleus transcriptomes reveal the underlying mechanisms of dynamic whitening in thermogenic adipose tissue in goats

Abstract Background Thermogenic adipose tissue, both beige and brown, experiences whitening as animals are exposed to warmth and age, but the potential mechanisms are not fully understood. In this study, we employed single-nucleus RNA-seq to construct a cell atlas during whitening progression and id...

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Main Authors: Manman Li, Nange Ma, Shujie Luo, Yuyi Lu, Xixi Yan, Yang Li, Xinmei Li, Zhuohui Li, Zhipei Wu, Zhenyu Wei, Wei Wang, Huimei Fan, Yu Jiang, Yan Xiong, Yu Wang
Format: Article
Language:English
Published: BMC 2025-02-01
Series:Journal of Animal Science and Biotechnology
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Online Access:https://doi.org/10.1186/s40104-025-01157-1
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author Manman Li
Nange Ma
Shujie Luo
Yuyi Lu
Xixi Yan
Yang Li
Xinmei Li
Zhuohui Li
Zhipei Wu
Zhenyu Wei
Wei Wang
Huimei Fan
Yu Jiang
Yan Xiong
Yu Wang
author_facet Manman Li
Nange Ma
Shujie Luo
Yuyi Lu
Xixi Yan
Yang Li
Xinmei Li
Zhuohui Li
Zhipei Wu
Zhenyu Wei
Wei Wang
Huimei Fan
Yu Jiang
Yan Xiong
Yu Wang
author_sort Manman Li
collection DOAJ
description Abstract Background Thermogenic adipose tissue, both beige and brown, experiences whitening as animals are exposed to warmth and age, but the potential mechanisms are not fully understood. In this study, we employed single-nucleus RNA-seq to construct a cell atlas during whitening progression and identified the characteristics of thermogenic adipocytes. Results Our histological studies and bulk transcriptome gene expression analysis confirmed that both perirenal and omental adipose tissues (pAT and oAT) exhibited progressive whitening in goats. Compared to the classic brown adipocytes in mice, goat thermogenic adipocytes were more closely related in gene expression patterns to human beige adipocytes, which was also confirmed by adipocyte type- and lineage-specific marker expression analysis. Furthermore, trajectory analysis revealed beige- and white-like adipocytes deriving from a common origin, coexisting and undergoing the transdifferentiation. In addition, differences in gene expression profiles and cell communication patterns (e.g., FGF and CALCR signaling) between oAT and pAT suggested a lower thermogenic capacity of oAT than that of pAT. Conclusions We constructed a cell atlas of goat pAT and oAT and descripted the characteristics of thermogenic adipocytes during whitening progression. Altogether, our results make a significant contribution to the molecular and cellular mechanisms behind the whitening of thermogenic adipocytes, and providing new insights into obesity prevention in humans and cold adaptation in animals.
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publishDate 2025-02-01
publisher BMC
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series Journal of Animal Science and Biotechnology
spelling doaj-art-d025c9b1e0bd440db39e6882fb8729522025-02-09T12:49:05ZengBMCJournal of Animal Science and Biotechnology2049-18912025-02-0116111510.1186/s40104-025-01157-1Single-nucleus transcriptomes reveal the underlying mechanisms of dynamic whitening in thermogenic adipose tissue in goatsManman Li0Nange Ma1Shujie Luo2Yuyi Lu3Xixi Yan4Yang Li5Xinmei Li6Zhuohui Li7Zhipei Wu8Zhenyu Wei9Wei Wang10Huimei Fan11Yu Jiang12Yan Xiong13Yu Wang14Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Ministry of Education, College of Animal and Veterinary Sciences, Southwest Minzu UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Ministry of Education, College of Animal and Veterinary Sciences, Southwest Minzu UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityAbstract Background Thermogenic adipose tissue, both beige and brown, experiences whitening as animals are exposed to warmth and age, but the potential mechanisms are not fully understood. In this study, we employed single-nucleus RNA-seq to construct a cell atlas during whitening progression and identified the characteristics of thermogenic adipocytes. Results Our histological studies and bulk transcriptome gene expression analysis confirmed that both perirenal and omental adipose tissues (pAT and oAT) exhibited progressive whitening in goats. Compared to the classic brown adipocytes in mice, goat thermogenic adipocytes were more closely related in gene expression patterns to human beige adipocytes, which was also confirmed by adipocyte type- and lineage-specific marker expression analysis. Furthermore, trajectory analysis revealed beige- and white-like adipocytes deriving from a common origin, coexisting and undergoing the transdifferentiation. In addition, differences in gene expression profiles and cell communication patterns (e.g., FGF and CALCR signaling) between oAT and pAT suggested a lower thermogenic capacity of oAT than that of pAT. Conclusions We constructed a cell atlas of goat pAT and oAT and descripted the characteristics of thermogenic adipocytes during whitening progression. Altogether, our results make a significant contribution to the molecular and cellular mechanisms behind the whitening of thermogenic adipocytes, and providing new insights into obesity prevention in humans and cold adaptation in animals.https://doi.org/10.1186/s40104-025-01157-1Beige adipocytessnRNA-seqThermogenic adipose tissueWhitening
spellingShingle Manman Li
Nange Ma
Shujie Luo
Yuyi Lu
Xixi Yan
Yang Li
Xinmei Li
Zhuohui Li
Zhipei Wu
Zhenyu Wei
Wei Wang
Huimei Fan
Yu Jiang
Yan Xiong
Yu Wang
Single-nucleus transcriptomes reveal the underlying mechanisms of dynamic whitening in thermogenic adipose tissue in goats
Journal of Animal Science and Biotechnology
Beige adipocytes
snRNA-seq
Thermogenic adipose tissue
Whitening
title Single-nucleus transcriptomes reveal the underlying mechanisms of dynamic whitening in thermogenic adipose tissue in goats
title_full Single-nucleus transcriptomes reveal the underlying mechanisms of dynamic whitening in thermogenic adipose tissue in goats
title_fullStr Single-nucleus transcriptomes reveal the underlying mechanisms of dynamic whitening in thermogenic adipose tissue in goats
title_full_unstemmed Single-nucleus transcriptomes reveal the underlying mechanisms of dynamic whitening in thermogenic adipose tissue in goats
title_short Single-nucleus transcriptomes reveal the underlying mechanisms of dynamic whitening in thermogenic adipose tissue in goats
title_sort single nucleus transcriptomes reveal the underlying mechanisms of dynamic whitening in thermogenic adipose tissue in goats
topic Beige adipocytes
snRNA-seq
Thermogenic adipose tissue
Whitening
url https://doi.org/10.1186/s40104-025-01157-1
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