Mechanically sensitive HSF1 is a key regulator of left-right symmetry breaking in zebrafish embryos
Summary: The left-right symmetry breaking of vertebrate embryos requires nodal flow. However, the molecular mechanisms that mediate the asymmetric gene expression regulation under nodal flow remain elusive. Here, we report that heat shock factor 1 (HSF1) is asymmetrically activated in the Kupffer’s...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-10-01
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| Series: | iScience |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004223019417 |
| _version_ | 1797647831359553536 |
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| author | Jing Du Shu-Kai Li Liu-Yuan Guan Zheng Guo Jiang-Fan Yin Li Gao Toru Kawanishi Atsuko Shimada Qiu-Ping Zhang Li-Sha Zheng Yi-Yao Liu Xi-Qiao Feng Lin Zhao Dong-Yan Chen Hiroyuki Takeda Yu-Bo Fan |
| author_facet | Jing Du Shu-Kai Li Liu-Yuan Guan Zheng Guo Jiang-Fan Yin Li Gao Toru Kawanishi Atsuko Shimada Qiu-Ping Zhang Li-Sha Zheng Yi-Yao Liu Xi-Qiao Feng Lin Zhao Dong-Yan Chen Hiroyuki Takeda Yu-Bo Fan |
| author_sort | Jing Du |
| collection | DOAJ |
| description | Summary: The left-right symmetry breaking of vertebrate embryos requires nodal flow. However, the molecular mechanisms that mediate the asymmetric gene expression regulation under nodal flow remain elusive. Here, we report that heat shock factor 1 (HSF1) is asymmetrically activated in the Kupffer’s vesicle of zebrafish embryos in the presence of nodal flow. Deficiency in HSF1 expression caused a significant situs inversus and disrupted gene expression asymmetry of nodal signaling proteins in zebrafish embryos. Further studies demonstrated that HSF1 is a mechanosensitive protein. The mechanical sensation ability of HSF1 is conserved in a variety of mechanical stimuli in different cell types. Moreover, cilia and Ca2+-Akt signaling axis are essential for the activation of HSF1 under mechanical stress in vitro and in vivo. Considering the conserved expression of HSF1 in organisms, these findings unveil a fundamental mechanism of gene expression regulation by mechanical clues during embryonic development and other physiological and pathological transformations. |
| first_indexed | 2024-03-11T15:23:17Z |
| format | Article |
| id | doaj.art-909450b7fbb444c8a3993fb727560073 |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-03-11T15:23:17Z |
| publishDate | 2023-10-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-909450b7fbb444c8a3993fb7275600732023-10-28T05:08:47ZengElsevieriScience2589-00422023-10-012610107864Mechanically sensitive HSF1 is a key regulator of left-right symmetry breaking in zebrafish embryosJing Du0Shu-Kai Li1Liu-Yuan Guan2Zheng Guo3Jiang-Fan Yin4Li Gao5Toru Kawanishi6Atsuko Shimada7Qiu-Ping Zhang8Li-Sha Zheng9Yi-Yao Liu10Xi-Qiao Feng11Lin Zhao12Dong-Yan Chen13Hiroyuki Takeda14Yu-Bo Fan15Key Laboratory for Biomechanics and Mechanobiology of Ministry of Education, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing 100083, China; Institute of Biomechanics and Medical Engineering, Department of Mechanical Engineering, School of Aerospace, Tsinghua University, Beijing 100084, China; Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo 113-0033, Japan; Corresponding authorKey Laboratory for Biomechanics and Mechanobiology of Ministry of Education, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing 100083, ChinaInstitute of Biomechanics and Medical Engineering, Department of Mechanical Engineering, School of Aerospace, Tsinghua University, Beijing 100084, ChinaKey Laboratory for Biomechanics and Mechanobiology of Ministry of Education, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing 100083, ChinaCollege of life science, Hebei Normal University, Shijiazhuang 050024, ChinaCollege of life science, Hebei Normal University, Shijiazhuang 050024, ChinaDepartment of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo 113-0033, JapanDepartment of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo 113-0033, JapanTianjin Key Laboratory of Tumor Microenvironment and Neurovascular Regulation, Department of Histology and Embryology, School of Medicine, Nankai University, Tianjin 300071, ChinaKey Laboratory for Biomechanics and Mechanobiology of Ministry of Education, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing 100083, ChinaDepartment of Biophysics, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, ChinaInstitute of Biomechanics and Medical Engineering, Department of Mechanical Engineering, School of Aerospace, Tsinghua University, Beijing 100084, ChinaTianjin Key Laboratory of Tumor Microenvironment and Neurovascular Regulation, Department of Histology and Embryology, School of Medicine, Nankai University, Tianjin 300071, ChinaTianjin Key Laboratory of Tumor Microenvironment and Neurovascular Regulation, Department of Histology and Embryology, School of Medicine, Nankai University, Tianjin 300071, China; Corresponding authorDepartment of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo 113-0033, Japan; Corresponding authorKey Laboratory for Biomechanics and Mechanobiology of Ministry of Education, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing 100083, China; Corresponding authorSummary: The left-right symmetry breaking of vertebrate embryos requires nodal flow. However, the molecular mechanisms that mediate the asymmetric gene expression regulation under nodal flow remain elusive. Here, we report that heat shock factor 1 (HSF1) is asymmetrically activated in the Kupffer’s vesicle of zebrafish embryos in the presence of nodal flow. Deficiency in HSF1 expression caused a significant situs inversus and disrupted gene expression asymmetry of nodal signaling proteins in zebrafish embryos. Further studies demonstrated that HSF1 is a mechanosensitive protein. The mechanical sensation ability of HSF1 is conserved in a variety of mechanical stimuli in different cell types. Moreover, cilia and Ca2+-Akt signaling axis are essential for the activation of HSF1 under mechanical stress in vitro and in vivo. Considering the conserved expression of HSF1 in organisms, these findings unveil a fundamental mechanism of gene expression regulation by mechanical clues during embryonic development and other physiological and pathological transformations.http://www.sciencedirect.com/science/article/pii/S2589004223019417Molecular biologyCell biologyDevelopmental biologyEmbryology |
| spellingShingle | Jing Du Shu-Kai Li Liu-Yuan Guan Zheng Guo Jiang-Fan Yin Li Gao Toru Kawanishi Atsuko Shimada Qiu-Ping Zhang Li-Sha Zheng Yi-Yao Liu Xi-Qiao Feng Lin Zhao Dong-Yan Chen Hiroyuki Takeda Yu-Bo Fan Mechanically sensitive HSF1 is a key regulator of left-right symmetry breaking in zebrafish embryos iScience Molecular biology Cell biology Developmental biology Embryology |
| title | Mechanically sensitive HSF1 is a key regulator of left-right symmetry breaking in zebrafish embryos |
| title_full | Mechanically sensitive HSF1 is a key regulator of left-right symmetry breaking in zebrafish embryos |
| title_fullStr | Mechanically sensitive HSF1 is a key regulator of left-right symmetry breaking in zebrafish embryos |
| title_full_unstemmed | Mechanically sensitive HSF1 is a key regulator of left-right symmetry breaking in zebrafish embryos |
| title_short | Mechanically sensitive HSF1 is a key regulator of left-right symmetry breaking in zebrafish embryos |
| title_sort | mechanically sensitive hsf1 is a key regulator of left right symmetry breaking in zebrafish embryos |
| topic | Molecular biology Cell biology Developmental biology Embryology |
| url | http://www.sciencedirect.com/science/article/pii/S2589004223019417 |
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