Dataset Information

Potassium Channel-Associated Bioelectricity of the Dermomyotome Determines Fin Patterning in Zebrafish.

ABSTRACT: The roles of bioelectric signaling in developmental patterning remain largely unknown, although recent work has implicated bioelectric signals in cellular processes such as proliferation and migration. Here, we report a mutation in the inwardly rectifying potassium channel (kir) gene, kcnj13/kir7.1, that causes elongation of the fins in the zebrafish insertional mutant Dhi2059. A viral DNA insertion into the noncoding region of kcnj13 results in transient activation and ectopic expression of kcnj13 in the somite and dermomyotome, from which the fin ray progenitors originate. We made an allele-specific loss-of-function kcnj13 mutant by CRISPR (clustered regularly interspaced short palindromic repeats) and showed that it could reverse the long-finned phenotype, but only when located on the same chromosome as the Dhi2059 viral insertion. Also, we showed that ectopic expression of kcnj13 in the dermomyotome of transgenic zebrafish produces phenocopies of the Dhi2059 mutant in a gene dosage-sensitive manner. Finally, to determine whether this developmental function is specific to kcnj13, we ectopically expressed three additional potassium channel genes: kcnj1b, kcnj10a, and kcnk9 We found that all induce the long-finned phenotype, indicating that this function is conserved among potassium channel genes. Taken together, our results suggest that dermomyotome bioelectricity is a new fin-patterning mechanism, and we propose a two-stage bioelectricity model for zebrafish fin patterning. This ion channel-regulated bioelectric developmental patterning mechanism may provide with us new insight into vertebrate morphological evolution and human congenital malformations.

SUBMITTER: Silic MR

PROVIDER: S-EPMC7404225 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Potassium Channel-Associated Bioelectricity of the Dermomyotome Determines Fin Patterning in Zebrafish.

Silic Martin R MR Wu Qiuyu Q Kim Brian H BH Golling Greg G Chen Kenny H KH Freitas Renata R Chubykin Alexander A AA Mittal Suresh K SK Zhang GuangJun G

Genetics 20200616 4

The roles of bioelectric signaling in developmental patterning remain largely unknown, although recent work has implicated bioelectric signals in cellular processes such as proliferation and migration. Here, we report a mutation in the inwardly rectifying potassium channel (kir) gene, kcnj13/kir7.1, that causes elongation of the fins in the zebrafish insertional mutant Dhi2059. A viral DNA insertion into the noncoding region of kcnj13 results in transient activation and ecto ...[more]

PMID: 32546498

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Project description:The evolution of the tetrapod limb involved an expansion and elaboration of the endoskeletal elements, while the fish fin rays were lost. Loss of fin-specific genes, and regulatory changes in key appendicular patterning genes have been identified as mechanisms of limb evolution, however their contributions to cellular organization and tissue differences between fins and limbs remains poorly understood. During early larval fin development, hoxa13a/hoxd13a-expressing fin fold mesenchyme migrate through the median and pectoral fin along actinotrichia fibrils, non-calcified skeletal elements crucial for supporting the fin fold. Fin fold mesenchyme migration defects have previously been proposed as a mechanism of fin dermal bone loss during tetrapod evolution as it has been shown they contribute directly to the fin ray osteoblast population. Using the nitroreductase/metronidazole system, we genetically ablated a subset of hoxa13a/hoxd13a-expressing fin fold mesenchyme to assess its contributions to fin development. Following the ablation of fin fold mesenchyme in larvae, the actinotrichia are unable to remain rigid and the median and pectoral fin folds collapse, resulting in a reduced fin fold size. The remaining cells following ablation are unable to migrate and show decreased actinodin1 mesenchymal reporter activity. Actinodin proteins are crucial structural component of the actinotrichia. Additionally, we show a decrease in hoxa13a, hoxd13a, fgf10a and altered shha, and ptch2 expression during larval fin development. A continuous treatment of metronidazole leads to fin ray defects at 30dpf. Fewer rays are present compared to stage-matched control larvae, and these rays are shorter and less defined. These results suggest the targeted hoxa13a/hoxd13a-expressing mesenchyme contribute to their own successful migration through their contributions to actinotrichia. Furthermore, due to their fate as fin ray osteoblasts, we propose their initial ablation, and subsequent disorganization produces truncated fin dermal bone elements during late larval stages.

Dataset Information

Potassium Channel-Associated Bioelectricity of the Dermomyotome Determines Fin Patterning in Zebrafish.

Publications

Potassium Channel-Associated Bioelectricity of the Dermomyotome Determines Fin Patterning in Zebrafish.

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