ROCK and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesis
Biomineralization had apparently evolved independently in different phyla, using distinct minerals, organic scaffolds, and gene regulatory networks (GRNs). However, diverse eukaryotes from unicellular organisms, through echinoderms to vertebrates, use the actomyosin network during biomineralization....
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2024-04-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/89080 |
| _version_ | 1797222424434966528 |
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| author | Eman Hijaze Tsvia Gildor Ronald Seidel Majed Layous Mark Winter Luca Bertinetti Yael Politi Smadar Ben-Tabou de-Leon |
| author_facet | Eman Hijaze Tsvia Gildor Ronald Seidel Majed Layous Mark Winter Luca Bertinetti Yael Politi Smadar Ben-Tabou de-Leon |
| author_sort | Eman Hijaze |
| collection | DOAJ |
| description | Biomineralization had apparently evolved independently in different phyla, using distinct minerals, organic scaffolds, and gene regulatory networks (GRNs). However, diverse eukaryotes from unicellular organisms, through echinoderms to vertebrates, use the actomyosin network during biomineralization. Specifically, the actomyosin remodeling protein, Rho-associated coiled-coil kinase (ROCK) regulates cell differentiation and gene expression in vertebrates’ biomineralizing cells, yet, little is known on ROCK’s role in invertebrates’ biomineralization. Here, we reveal that ROCK controls the formation, growth, and morphology of the calcite spicules in the sea urchin larva. ROCK expression is elevated in the sea urchin skeletogenic cells downstream of the Vascular Endothelial Growth Factor (VEGF) signaling. ROCK inhibition leads to skeletal loss and disrupts skeletogenic gene expression. ROCK inhibition after spicule formation reduces the spicule elongation rate and induces ectopic spicule branching. Similar skeletogenic phenotypes are observed when ROCK is inhibited in a skeletogenic cell culture, indicating that these phenotypes are due to ROCK activity specifically in the skeletogenic cells. Reduced skeletal growth and enhanced branching are also observed under direct perturbations of the actomyosin network. We propose that ROCK and the actomyosin machinery were employed independently, downstream of distinct GRNs, to regulate biomineral growth and morphology in Eukaryotes. |
| first_indexed | 2024-04-24T13:21:07Z |
| format | Article |
| id | doaj.art-12009aae12e4456386886e53e4b2b528 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-24T13:21:07Z |
| publishDate | 2024-04-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-12009aae12e4456386886e53e4b2b5282024-04-04T14:29:19ZengeLife Sciences Publications LtdeLife2050-084X2024-04-011210.7554/eLife.89080ROCK and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesisEman Hijaze0Tsvia Gildor1Ronald Seidel2Majed Layous3Mark Winter4https://orcid.org/0000-0003-1180-1957Luca Bertinetti5Yael Politi6Smadar Ben-Tabou de-Leon7https://orcid.org/0000-0001-9497-4938Department of Marine Biology, Leon H. Charney School of Marine Sciences, University of Haifa, Haifa, IsraelDepartment of Marine Biology, Leon H. Charney School of Marine Sciences, University of Haifa, Haifa, IsraelB CUBE Center for Molecular Bioengineering, Technische Universität Dresden, Dresden, GermanyDepartment of Marine Biology, Leon H. Charney School of Marine Sciences, University of Haifa, Haifa, IsraelDepartment of Electrical Engineering, Computer Science and Mathematics, Technische Universiteit Delft, Delft, NetherlandsB CUBE Center for Molecular Bioengineering, Technische Universität Dresden, Dresden, GermanyB CUBE Center for Molecular Bioengineering, Technische Universität Dresden, Dresden, GermanyDepartment of Marine Biology, Leon H. Charney School of Marine Sciences, University of Haifa, Haifa, IsraelBiomineralization had apparently evolved independently in different phyla, using distinct minerals, organic scaffolds, and gene regulatory networks (GRNs). However, diverse eukaryotes from unicellular organisms, through echinoderms to vertebrates, use the actomyosin network during biomineralization. Specifically, the actomyosin remodeling protein, Rho-associated coiled-coil kinase (ROCK) regulates cell differentiation and gene expression in vertebrates’ biomineralizing cells, yet, little is known on ROCK’s role in invertebrates’ biomineralization. Here, we reveal that ROCK controls the formation, growth, and morphology of the calcite spicules in the sea urchin larva. ROCK expression is elevated in the sea urchin skeletogenic cells downstream of the Vascular Endothelial Growth Factor (VEGF) signaling. ROCK inhibition leads to skeletal loss and disrupts skeletogenic gene expression. ROCK inhibition after spicule formation reduces the spicule elongation rate and induces ectopic spicule branching. Similar skeletogenic phenotypes are observed when ROCK is inhibited in a skeletogenic cell culture, indicating that these phenotypes are due to ROCK activity specifically in the skeletogenic cells. Reduced skeletal growth and enhanced branching are also observed under direct perturbations of the actomyosin network. We propose that ROCK and the actomyosin machinery were employed independently, downstream of distinct GRNs, to regulate biomineral growth and morphology in Eukaryotes.https://elifesciences.org/articles/89080biomineralizationROCKactomyosinsea urchinskeletogenesistubulogenesis |
| spellingShingle | Eman Hijaze Tsvia Gildor Ronald Seidel Majed Layous Mark Winter Luca Bertinetti Yael Politi Smadar Ben-Tabou de-Leon ROCK and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesis eLife biomineralization ROCK actomyosin sea urchin skeletogenesis tubulogenesis |
| title | ROCK and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesis |
| title_full | ROCK and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesis |
| title_fullStr | ROCK and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesis |
| title_full_unstemmed | ROCK and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesis |
| title_short | ROCK and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesis |
| title_sort | rock and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesis |
| topic | biomineralization ROCK actomyosin sea urchin skeletogenesis tubulogenesis |
| url | https://elifesciences.org/articles/89080 |
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