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Epigenetic regulation of cilia stability and kidney development by the chromatin remodeling SWI/SNF complex in zebrafish

Xiaoyu Cheng,  Qianshu Zhu,  Shilin Ma,  Xiaoyu Peng,  Guanliang Huang,  Guifen Liu,  Wentao Zhang,  Yong Zhang,  Cizhong Jiang,  Andong Qiu,  Ying Cao

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文章导航 > Journal of Genetics and Genomics  > 2025 > 优先出版
Xiaoyu Cheng, Qianshu Zhu, Shilin Ma, Xiaoyu Peng, Guanliang Huang, Guifen Liu, Wentao Zhang, Yong Zhang, Cizhong Jiang, Andong Qiu, Ying Cao. Epigenetic regulation of cilia stability and kidney development by the chromatin remodeling SWI/SNF complex in zebrafish[J]. 遗传学报. doi: 10.1016/j.jgg.2025.11.001
引用本文: Xiaoyu Cheng, Qianshu Zhu, Shilin Ma, Xiaoyu Peng, Guanliang Huang, Guifen Liu, Wentao Zhang, Yong Zhang, Cizhong Jiang, Andong Qiu, Ying Cao. Epigenetic regulation of cilia stability and kidney development by the chromatin remodeling SWI/SNF complex in zebrafish[J]. 遗传学报. doi: 10.1016/j.jgg.2025.11.001
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Xiaoyu Cheng, Qianshu Zhu, Shilin Ma, Xiaoyu Peng, Guanliang Huang, Guifen Liu, Wentao Zhang, Yong Zhang, Cizhong Jiang, Andong Qiu, Ying Cao. Epigenetic regulation of cilia stability and kidney development by the chromatin remodeling SWI/SNF complex in zebrafish[J]. Journal of Genetics and Genomics. doi: 10.1016/j.jgg.2025.11.001
Citation: Xiaoyu Cheng, Qianshu Zhu, Shilin Ma, Xiaoyu Peng, Guanliang Huang, Guifen Liu, Wentao Zhang, Yong Zhang, Cizhong Jiang, Andong Qiu, Ying Cao. Epigenetic regulation of cilia stability and kidney development by the chromatin remodeling SWI/SNF complex in zebrafish[J]. Journal of Genetics and Genomics. doi: 10.1016/j.jgg.2025.11.001
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Epigenetic regulation of cilia stability and kidney development by the chromatin remodeling SWI/SNF complex in zebrafish

doi: 10.1016/j.jgg.2025.11.001

  • a. State Key Laboratory of Cardiology and Medical Innovation Center, Shanghai East Hospital, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China;

  • b. Key Laboratory of Spine and Spinal Cord Injury Repair and Regeneration of Ministry of Education, Orthopaedic Department of Tongji Hospital, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China;

  • c. Department of Molecular and Cellular Biology, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China;

  • d. Medical Innovation Center, Shanghai East Hospital, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China

基金项目: 

We thank the members of the Cao lab for helpful discussions. This project was supported by grants from the National Key Research and Development Program of China (2017YFA0104600) and the National Natural Science Foundation of China (32170835 and 31970767).

详细信息
    通讯作者:

    Ying Cao,E-mail:yingcao@tongji.edu.cn

Epigenetic regulation of cilia stability and kidney development by the chromatin remodeling SWI/SNF complex in zebrafish

  • a. State Key Laboratory of Cardiology and Medical Innovation Center, Shanghai East Hospital, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China;

  • b. Key Laboratory of Spine and Spinal Cord Injury Repair and Regeneration of Ministry of Education, Orthopaedic Department of Tongji Hospital, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China;

  • c. Department of Molecular and Cellular Biology, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China;

  • d. Medical Innovation Center, Shanghai East Hospital, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China

Funds: 

We thank the members of the Cao lab for helpful discussions. This project was supported by grants from the National Key Research and Development Program of China (2017YFA0104600) and the National Natural Science Foundation of China (32170835 and 31970767).

    摘要
  • 摘要:

    Cilia are vital subcellular organelles whose assembly is regulated by master transcription factors, such as Foxj1 and Rfx. However, the mechanisms of epigenetic regulation over cilia stability remain largely unclear. Here, we investigate the epigenetic control by manipulating chromatin remodeling genes in zebrafish. We demonstrate that the depletion of multiple components of the switch/sucrose non-fermentable (SWI/SNF) chromatin remodeling complex induces ciliopathy-like phenotypes in zebrafish embryos. Specifically, the loss of Actl6a, an essential component of the SWI/SNF complex, leads to cilia disassembly and cystic kidney defects, without affecting cilia motility. Our multi-omics analyses (RNA-seq, ATAC-seq, and FitCUT&RUN) consistently reveal that in Actl6a-depleted pronephros or embryos, a critical set of cilia genes, including the master regulators foxj1a and rfx2, exhibit concordant downregulation across the transcriptional level, chromatin accessibility, and SWI/SNF binding. Consistently, the depletion of foxj1a or rfx2 causes cilia assembly defects and cystic kidney formation in zebrafish. Furthermore, overexpression of either foxj1a or rfx2 mRNA substantially rescues the cystic kidney and cilia disassembly defects observed in actl6a-/- mutant embryos. Collectively, these findings reveal that the SWI/SNF complex maintains cilia stability and kidney homeostasis by directly modulating the expression of the key ciliogenesis transcription factors foxj1a and rfx2.

    Abstract:

    Cilia are vital subcellular organelles whose assembly is regulated by master transcription factors, such as Foxj1 and Rfx. However, the mechanisms of epigenetic regulation over cilia stability remain largely unclear. Here, we investigate the epigenetic control by manipulating chromatin remodeling genes in zebrafish. We demonstrate that the depletion of multiple components of the switch/sucrose non-fermentable (SWI/SNF) chromatin remodeling complex induces ciliopathy-like phenotypes in zebrafish embryos. Specifically, the loss of Actl6a, an essential component of the SWI/SNF complex, leads to cilia disassembly and cystic kidney defects, without affecting cilia motility. Our multi-omics analyses (RNA-seq, ATAC-seq, and FitCUT&RUN) consistently reveal that in Actl6a-depleted pronephros or embryos, a critical set of cilia genes, including the master regulators foxj1a and rfx2, exhibit concordant downregulation across the transcriptional level, chromatin accessibility, and SWI/SNF binding. Consistently, the depletion of foxj1a or rfx2 causes cilia assembly defects and cystic kidney formation in zebrafish. Furthermore, overexpression of either foxj1a or rfx2 mRNA substantially rescues the cystic kidney and cilia disassembly defects observed in actl6a-/- mutant embryos. Collectively, these findings reveal that the SWI/SNF complex maintains cilia stability and kidney homeostasis by directly modulating the expression of the key ciliogenesis transcription factors foxj1a and rfx2.

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  • 收稿日期:  2025-10-29
  • 录用日期:  2025-11-04
  • 修回日期:  2025-11-04
  • 网络出版日期:  2025-11-08

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