A spatiotemporal atlas of mouse liver homeostasis and regeneration

Jiangshan Xu; Pengcheng Guo; Shijie Hao; Shuncheng Shangguan; Quan Shi; Giacomo Volpe; Keke Huang; Jing Zuo; Juan An; Yue Yuan; Mengnan Cheng; Qiuting Deng; Xiao Zhang; Guangyao Lai; Haitao Nan; Baihua Wu; Xinyi Shentu; Liang Wu; Xiaoyu Wei; Yujia Jiang; Xin Huang; Fengyu Pan; Yumo Song; Ronghai Li; Zhifeng Wang; Chuanyu Liu; Shiping Liu; Yuxiang Li; Tao Yang; Zhicheng Xu; Wensi Du; Ling Li; Tanveer Ahmed; Kai You; Zhen Dai; Li Li; Baoming Qin; Yinxiong Li; Liangxue Lai; Dajiang Qin; Junling Chen; Rong Fan; Yongyin Li; Jinlin Hou; Michael Ott; Amar Deep Sharma; Tobias Cantz; Axel Schambach; Karsten Kristiansen; Andrew P. Hutchins; Berthold Göttgens; Patrick H. Maxwell; Lijian Hui; Xun Xu; Longqi Liu; Ao Chen; Yiwei Lai; Miguel A. Esteban

doi:10.1038/s41588-024-01709-7

A spatiotemporal atlas of mouse liver homeostasis and regeneration

Jiangshan Xu, Pengcheng Guo, Shijie Hao, Shuncheng Shangguan, Quan Shi, Giacomo Volpe, Keke Huang, Jing Zuo, Juan An, Yue Yuan, Mengnan Cheng, Qiuting Deng, Xiao Zhang, Guangyao Lai, Haitao Nan, Baihua Wu, Xinyi Shentu, Liang Wu, Xiaoyu Wei, Yujia JiangXin Huang, Fengyu Pan, Yumo Song, Ronghai Li, Zhifeng Wang, Chuanyu Liu, Shiping Liu, Yuxiang Li, Tao Yang, Zhicheng Xu, Wensi Du, Ling Li, Tanveer Ahmed, Kai You, Zhen Dai, Li Li, Baoming Qin, Yinxiong Li, Liangxue Lai, Dajiang Qin, Junling Chen, Rong Fan, Yongyin Li, Jinlin Hou, Michael Ott, Amar Deep Sharma, Tobias Cantz, Axel Schambach, Karsten Kristiansen, Andrew P. Hutchins, Berthold Göttgens, Patrick H. Maxwell, Lijian Hui, Xun Xu^*, Longqi Liu, Ao Chen, Yiwei Lai, Miguel A. Esteban

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

4 Citationer (Scopus)

Abstract

The mechanism by which mammalian liver cell responses are coordinated during tissue homeostasis and perturbation is poorly understood, representing a major obstacle in our understanding of many diseases. This knowledge gap is caused by the difficulty involved with studying multiple cell types in different states and locations, particularly when these are transient. We have combined Stereo-seq (spatiotemporal enhanced resolution omics-sequencing) with single-cell transcriptomic profiling of 473,290 cells to generate a high-definition spatiotemporal atlas of mouse liver homeostasis and regeneration at the whole-lobe scale. Our integrative study dissects in detail the molecular gradients controlling liver cell function, systematically defining how gene networks are dynamically modulated through intercellular communication to promote regeneration. Among other important regulators, we identified the transcriptional cofactor TBL1XR1 as a rheostat linking inflammation to Wnt/β-catenin signaling for facilitating hepatocyte proliferation. Our data and analytical pipelines lay the foundation for future high-definition tissue-scale atlases of organ physiology and malfunction.

Originalsprog	Engelsk
Tidsskrift	Nature Genetics
Vol/bind	56
Sider (fra-til)	953-969
Antal sider	17
ISSN	1061-4036
DOI	https://doi.org/10.1038/s41588-024-01709-7
Status	Udgivet - 2024

Bibliografisk note

Funding Information:
We thank all our teams\u2019 members, Jian Zhang (Experimental Animal Center, Guangzhou Institutes of Biomedicine and Health) and the CNGB for their support. This work was supported by the National Key Research and Development Program of China (2022YFC3400400 to X.X.), National Natural Science Foundation of China (32370848 to M.A.E., 92368301, 92168202 to L.H., 32200688 to Y. Lai and 32070861 to B.Q.), National Science and Technology Innovation 2030 Major Program (2021ZD0200100 to L. Liu), Shenzhen Basic Research Project for Excellent Young Scholars (RCYX20200714114644191 to L. Liu), Guangdong Basic and Applied Basic Research Foundation (2021B1515120075 to M.A.E. and 2021A1515110180 to Y. Lai), Guangzhou Basic and Applied Basic Research Foundation (202201010408 to Y. Lai, 202201011037 to Li Li, 202201010455 to T.A.). The CNGB was supported by Guangdong Genomics Data Center (2021B1212100001).

Publisher Copyright:
© The Author(s), under exclusive licence to Springer Nature America, Inc. 2024.

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10.1038/s41588-024-01709-7

Citationsformater

A spatiotemporal atlas of mouse liver homeostasis and regeneration. / Xu, Jiangshan; Guo, Pengcheng; Hao, Shijie; Shangguan, Shuncheng; Shi, Quan; Volpe, Giacomo; Huang, Keke; Zuo, Jing; An, Juan; Yuan, Yue; Cheng, Mengnan; Deng, Qiuting; Zhang, Xiao; Lai, Guangyao; Nan, Haitao; Wu, Baihua; Shentu, Xinyi; Wu, Liang; Wei, Xiaoyu; Jiang, Yujia; Huang, Xin; Pan, Fengyu; Song, Yumo; Li, Ronghai; Wang, Zhifeng; Liu, Chuanyu; Liu, Shiping; Li, Yuxiang; Yang, Tao; Xu, Zhicheng; Du, Wensi; Li, Ling; Ahmed, Tanveer; You, Kai; Dai, Zhen; Li, Li; Qin, Baoming; Li, Yinxiong; Lai, Liangxue; Qin, Dajiang; Chen, Junling; Fan, Rong; Li, Yongyin; Hou, Jinlin; Ott, Michael; Sharma, Amar Deep; Cantz, Tobias; Schambach, Axel; Kristiansen, Karsten; Hutchins, Andrew P.; Göttgens, Berthold; Maxwell, Patrick H.; Hui, Lijian; Xu, Xun; Liu, Longqi; Chen, Ao; Lai, Yiwei; Esteban, Miguel A.

I: Nature Genetics, Bind 56, 2024, s. 953-969.

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

Xu, J, Guo, P, Hao, S, Shangguan, S, Shi, Q, Volpe, G, Huang, K, Zuo, J, An, J, Yuan, Y, Cheng, M, Deng, Q, Zhang, X, Lai, G, Nan, H, Wu, B, Shentu, X, Wu, L, Wei, X, Jiang, Y, Huang, X, Pan, F, Song, Y, Li, R, Wang, Z, Liu, C, Liu, S, Li, Y, Yang, T, Xu, Z, Du, W, Li, L, Ahmed, T, You, K, Dai, Z, Li, L, Qin, B, Li, Y, Lai, L, Qin, D, Chen, J, Fan, R, Li, Y, Hou, J, Ott, M, Sharma, AD, Cantz, T, Schambach, A, Kristiansen, K, Hutchins, AP, Göttgens, B, Maxwell, PH, Hui, L, Xu, X, Liu, L, Chen, A, Lai, Y & Esteban, MA 2024, 'A spatiotemporal atlas of mouse liver homeostasis and regeneration', Nature Genetics, bind 56, s. 953-969. https://doi.org/10.1038/s41588-024-01709-7

Xu, Jiangshan ; Guo, Pengcheng ; Hao, Shijie ; Shangguan, Shuncheng ; Shi, Quan ; Volpe, Giacomo ; Huang, Keke ; Zuo, Jing ; An, Juan ; Yuan, Yue ; Cheng, Mengnan ; Deng, Qiuting ; Zhang, Xiao ; Lai, Guangyao ; Nan, Haitao ; Wu, Baihua ; Shentu, Xinyi ; Wu, Liang ; Wei, Xiaoyu ; Jiang, Yujia ; Huang, Xin ; Pan, Fengyu ; Song, Yumo ; Li, Ronghai ; Wang, Zhifeng ; Liu, Chuanyu ; Liu, Shiping ; Li, Yuxiang ; Yang, Tao ; Xu, Zhicheng ; Du, Wensi ; Li, Ling ; Ahmed, Tanveer ; You, Kai ; Dai, Zhen ; Li, Li ; Qin, Baoming ; Li, Yinxiong ; Lai, Liangxue ; Qin, Dajiang ; Chen, Junling ; Fan, Rong ; Li, Yongyin ; Hou, Jinlin ; Ott, Michael ; Sharma, Amar Deep ; Cantz, Tobias ; Schambach, Axel ; Kristiansen, Karsten ; Hutchins, Andrew P. ; Göttgens, Berthold ; Maxwell, Patrick H. ; Hui, Lijian ; Xu, Xun ; Liu, Longqi ; Chen, Ao ; Lai, Yiwei ; Esteban, Miguel A. / A spatiotemporal atlas of mouse liver homeostasis and regeneration. I: Nature Genetics. 2024 ; Bind 56. s. 953-969.

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abstract = "The mechanism by which mammalian liver cell responses are coordinated during tissue homeostasis and perturbation is poorly understood, representing a major obstacle in our understanding of many diseases. This knowledge gap is caused by the difficulty involved with studying multiple cell types in different states and locations, particularly when these are transient. We have combined Stereo-seq (spatiotemporal enhanced resolution omics-sequencing) with single-cell transcriptomic profiling of 473,290 cells to generate a high-definition spatiotemporal atlas of mouse liver homeostasis and regeneration at the whole-lobe scale. Our integrative study dissects in detail the molecular gradients controlling liver cell function, systematically defining how gene networks are dynamically modulated through intercellular communication to promote regeneration. Among other important regulators, we identified the transcriptional cofactor TBL1XR1 as a rheostat linking inflammation to Wnt/β-catenin signaling for facilitating hepatocyte proliferation. Our data and analytical pipelines lay the foundation for future high-definition tissue-scale atlases of organ physiology and malfunction.",

author = "Jiangshan Xu and Pengcheng Guo and Shijie Hao and Shuncheng Shangguan and Quan Shi and Giacomo Volpe and Keke Huang and Jing Zuo and Juan An and Yue Yuan and Mengnan Cheng and Qiuting Deng and Xiao Zhang and Guangyao Lai and Haitao Nan and Baihua Wu and Xinyi Shentu and Liang Wu and Xiaoyu Wei and Yujia Jiang and Xin Huang and Fengyu Pan and Yumo Song and Ronghai Li and Zhifeng Wang and Chuanyu Liu and Shiping Liu and Yuxiang Li and Tao Yang and Zhicheng Xu and Wensi Du and Ling Li and Tanveer Ahmed and Kai You and Zhen Dai and Li Li and Baoming Qin and Yinxiong Li and Liangxue Lai and Dajiang Qin and Junling Chen and Rong Fan and Yongyin Li and Jinlin Hou and Michael Ott and Sharma, {Amar Deep} and Tobias Cantz and Axel Schambach and Karsten Kristiansen and Hutchins, {Andrew P.} and Berthold G{\"o}ttgens and Maxwell, {Patrick H.} and Lijian Hui and Xun Xu and Longqi Liu and Ao Chen and Yiwei Lai and Esteban, {Miguel A.}",

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AU - Volpe, Giacomo

AU - Huang, Keke

AU - Zuo, Jing

AU - An, Juan

AU - Yuan, Yue

AU - Cheng, Mengnan

AU - Deng, Qiuting

AU - Zhang, Xiao

AU - Lai, Guangyao

AU - Nan, Haitao

AU - Wu, Baihua

AU - Shentu, Xinyi

AU - Wu, Liang

AU - Wei, Xiaoyu

AU - Jiang, Yujia

AU - Huang, Xin

AU - Pan, Fengyu

AU - Song, Yumo

AU - Li, Ronghai

AU - Wang, Zhifeng

AU - Liu, Chuanyu

AU - Liu, Shiping

AU - Li, Yuxiang

AU - Yang, Tao

AU - Xu, Zhicheng

AU - Du, Wensi

AU - Li, Ling

AU - Ahmed, Tanveer

AU - You, Kai

AU - Dai, Zhen

AU - Li, Li

AU - Qin, Baoming

AU - Li, Yinxiong

AU - Lai, Liangxue

AU - Qin, Dajiang

AU - Chen, Junling

AU - Fan, Rong

AU - Li, Yongyin

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AB - The mechanism by which mammalian liver cell responses are coordinated during tissue homeostasis and perturbation is poorly understood, representing a major obstacle in our understanding of many diseases. This knowledge gap is caused by the difficulty involved with studying multiple cell types in different states and locations, particularly when these are transient. We have combined Stereo-seq (spatiotemporal enhanced resolution omics-sequencing) with single-cell transcriptomic profiling of 473,290 cells to generate a high-definition spatiotemporal atlas of mouse liver homeostasis and regeneration at the whole-lobe scale. Our integrative study dissects in detail the molecular gradients controlling liver cell function, systematically defining how gene networks are dynamically modulated through intercellular communication to promote regeneration. Among other important regulators, we identified the transcriptional cofactor TBL1XR1 as a rheostat linking inflammation to Wnt/β-catenin signaling for facilitating hepatocyte proliferation. Our data and analytical pipelines lay the foundation for future high-definition tissue-scale atlases of organ physiology and malfunction.

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