Single-nucleus RNA sequencing defines adipose tissue subpopulations that contribute to Tibetan pig cold adaptation
Abstract Background Thermogenic beige adipocyte displays a remarkable ability in mammals to adapt to cold environments, but the underlying cellular mechanisms remain unclear, especially in pigs that lack functional UCP1. Results Multilocular beige adipocytes were observed in both Tibetan pigs (cold-...
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2025-04-01
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| Online Access: | https://doi.org/10.1186/s12915-025-02211-0 |
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| author | Jiali Liu Yao Jiang Tianxia Liu Chuanhe Chen Linya Chui Along Cui Xueping Zhang Xiao Wang Yu Wang Chunhuai Yang Ying Zhang Tianwen Wu Shulin Yang Jiaojiao Huang Cong Tao Jianguo Zhao Yanfang Wang |
| author_facet | Jiali Liu Yao Jiang Tianxia Liu Chuanhe Chen Linya Chui Along Cui Xueping Zhang Xiao Wang Yu Wang Chunhuai Yang Ying Zhang Tianwen Wu Shulin Yang Jiaojiao Huang Cong Tao Jianguo Zhao Yanfang Wang |
| author_sort | Jiali Liu |
| collection | DOAJ |
| description | Abstract Background Thermogenic beige adipocyte displays a remarkable ability in mammals to adapt to cold environments, but the underlying cellular mechanisms remain unclear, especially in pigs that lack functional UCP1. Results Multilocular beige adipocytes were observed in both Tibetan pigs (cold-tolerant) and Bama pigs (cold-sensitive) after short-term cold exposure (4 ℃ for 3 days). Through single-nucleus RNA sequencing of adipose tissues, including subcutaneous inguinal adipose tissues (IAT) and perirenal adipose tissues (PAT), from both pig breeds at room temperature and cold treatment conditions, we discovered two cell subpopulations specific to Tibetan pigs, PDGFRα + EBF2 High in IAT and ADIPOQ + HIF1A High in both depots. PDGFRα + EBF2 High cells were characterized as potential beige precursors, while ADIPOQ + HIF1A High cells were found to express highly thermogenic-related genes. Despite the decrease of the lipogenic subpopulation and the increase of the lipolytic and the thermogenic subpopulations observed in both pig breeds upon cold treatment, Tibetan pigs exhibited stronger cellular and molecular responses compared to Bama pigs. Remarkably, cold-induced de novo beige adipogenesis and white adipocyte browning, likely occurred in Tibetan pigs, while Bama pigs relied more heavily on white browning. Moreover, BMP7, which was highly expressed in the PDGFRα + EBF2 High subpopulation, positively regulates porcine beige thermogenic capacity. Conclusions Our data offers a comprehensive and unprecedented perspective on the heterogeneity and plasticity of adipose tissues of pigs and broadens the understanding of beige fat biology in mammals. |
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| id | doaj-art-c78ba83a88e74c05979d28d4ba7bf0ef |
| institution | Kabale University |
| issn | 1741-7007 |
| language | English |
| publishDate | 2025-04-01 |
| publisher | BMC |
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| series | BMC Biology |
| spelling | doaj-art-c78ba83a88e74c05979d28d4ba7bf0ef2025-08-20T03:53:32ZengBMCBMC Biology1741-70072025-04-0123112210.1186/s12915-025-02211-0Single-nucleus RNA sequencing defines adipose tissue subpopulations that contribute to Tibetan pig cold adaptationJiali Liu0Yao Jiang1Tianxia Liu2Chuanhe Chen3Linya Chui4Along Cui5Xueping Zhang6Xiao Wang7Yu Wang8Chunhuai Yang9Ying Zhang10Tianwen Wu11Shulin Yang12Jiaojiao Huang13Cong Tao14Jianguo Zhao15Yanfang Wang16State Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS)National Animal Husbandry ServiceState Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS)College of Life Sciences, Qingdao Agricultural UniversityState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS)Abstract Background Thermogenic beige adipocyte displays a remarkable ability in mammals to adapt to cold environments, but the underlying cellular mechanisms remain unclear, especially in pigs that lack functional UCP1. Results Multilocular beige adipocytes were observed in both Tibetan pigs (cold-tolerant) and Bama pigs (cold-sensitive) after short-term cold exposure (4 ℃ for 3 days). Through single-nucleus RNA sequencing of adipose tissues, including subcutaneous inguinal adipose tissues (IAT) and perirenal adipose tissues (PAT), from both pig breeds at room temperature and cold treatment conditions, we discovered two cell subpopulations specific to Tibetan pigs, PDGFRα + EBF2 High in IAT and ADIPOQ + HIF1A High in both depots. PDGFRα + EBF2 High cells were characterized as potential beige precursors, while ADIPOQ + HIF1A High cells were found to express highly thermogenic-related genes. Despite the decrease of the lipogenic subpopulation and the increase of the lipolytic and the thermogenic subpopulations observed in both pig breeds upon cold treatment, Tibetan pigs exhibited stronger cellular and molecular responses compared to Bama pigs. Remarkably, cold-induced de novo beige adipogenesis and white adipocyte browning, likely occurred in Tibetan pigs, while Bama pigs relied more heavily on white browning. Moreover, BMP7, which was highly expressed in the PDGFRα + EBF2 High subpopulation, positively regulates porcine beige thermogenic capacity. Conclusions Our data offers a comprehensive and unprecedented perspective on the heterogeneity and plasticity of adipose tissues of pigs and broadens the understanding of beige fat biology in mammals.https://doi.org/10.1186/s12915-025-02211-0PigsnRNA-seqAdipocytesSubpopulationsCold stimulation |
| spellingShingle | Jiali Liu Yao Jiang Tianxia Liu Chuanhe Chen Linya Chui Along Cui Xueping Zhang Xiao Wang Yu Wang Chunhuai Yang Ying Zhang Tianwen Wu Shulin Yang Jiaojiao Huang Cong Tao Jianguo Zhao Yanfang Wang Single-nucleus RNA sequencing defines adipose tissue subpopulations that contribute to Tibetan pig cold adaptation BMC Biology Pig snRNA-seq Adipocytes Subpopulations Cold stimulation |
| title | Single-nucleus RNA sequencing defines adipose tissue subpopulations that contribute to Tibetan pig cold adaptation |
| title_full | Single-nucleus RNA sequencing defines adipose tissue subpopulations that contribute to Tibetan pig cold adaptation |
| title_fullStr | Single-nucleus RNA sequencing defines adipose tissue subpopulations that contribute to Tibetan pig cold adaptation |
| title_full_unstemmed | Single-nucleus RNA sequencing defines adipose tissue subpopulations that contribute to Tibetan pig cold adaptation |
| title_short | Single-nucleus RNA sequencing defines adipose tissue subpopulations that contribute to Tibetan pig cold adaptation |
| title_sort | single nucleus rna sequencing defines adipose tissue subpopulations that contribute to tibetan pig cold adaptation |
| topic | Pig snRNA-seq Adipocytes Subpopulations Cold stimulation |
| url | https://doi.org/10.1186/s12915-025-02211-0 |
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