Cocurullo M et al. (2023), Molecular and Cellular Characterization of the ...

ECB-ART-51660

Cells 2023 Jan 10;122:. doi: 10.3390/cells12020272.

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Molecular and Cellular Characterization of the TH Pathway in the Sea Urchin Strongylocentrotus purpuratus.

Cocurullo M , Paganos P , Wood NJ , Arnone MI , Oliveri P .

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Thyroid Hormones (THs) are a class of signaling molecules produced by coupling iodine with tyrosine residues. In vertebrates, extensive data support their important role in a variety of processes such as metabolism, development and metamorphosis. On the other hand, in invertebrates, the synthesis and role of the THs have been, so far, poorly investigated, thus limiting our understanding of the function and evolution of this important animal signaling pathway. In sea urchins, for example, while several studies focused on the availability and function of external sources of iodotyrosines, preliminary evidence suggests that an endogenous TH pathway might be in place. Here, integrating available literature with an in silico analysis, various homologous genes of the vertebrate TH molecular toolkit have been identified in the sea urchin Strongylocentrotus purpuratus. They include genes involved in the synthesis (Sp-Pxdn), metabolism (Sp-Dios), transport (Sp-Ttrl, Sp-Mct7/8/10) and response (Sp-Thr, Sp-Rxr and Sp-Integrin αP) to thyroid hormones. To understand the cell type(s) involved in TH synthesis and/or response, we studied the spatial expression of the TH toolkit during urchin development. Exploiting single-cell transcriptomics data in conjunction with in situ hybridization and immunohistochemistry, we identified cell types that are potentially producing or responding to THs in the sea urchin. Finally, growing sea urchin embryos until the larva stage with and without a source of inorganic iodine, we provided evidence that iodine organification is important for larval skeleton growth.

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	Figure 1. Spatiotemporal expression pattern of putative sea urchin TH pathway components. (A,F,G,L,M,R) Dotplot showing the average expression and percentage of cells per cluster containing transcripts for Sp-Pxdn at 2 dpf, Sp-Pxdn at 3 dpf, Sp-DIO at 2 hpf, Sp-DIO at 3 dpf, and Sp-Thr at 2 dpf, Sp-Thr at 3 dpf, respectively. (B,B1,D,D1) Coupled FISH-IHC showing the expression of Sp-Pxdn in PMC, as indicated by the colocalization of Sp-Pxdn transcripts and the immunoreactivity-based signal of the skeletal marker Msp130 at 2 and 3 dpf. White triangles= blastocoelar cells. Green triangles= skeletogenic cells. (H,H1,J,J1) FISH showing the expression pattern of Sp-DIO at 2 and 3 dpf. (N,N1,P,P1) coupled FISH-IHC showing the expression patterns of Sp-Thr and Msp130 at 2 and 3 dpf. White triangle= blastocoelar cells. (C,E,I,K,O,Q) Schematic representations of the expression domains of Sp-Pxdn at 2 (C) and 3 (E) dpf, Sp-Dio at 2 (I) and 3 (K) dpf, and Sp-Thr at 2 (O) and 3 (Q) dpf as illustrated by the dotplots. a= anus; ae= aboral ectoderm; ane = anterior neuroectoderm; ap= apical plate; cp = coelomic pouch; es = esophagus; expl = exocrine pancreas-like; fg = forefut; I = intestine; n = neurons.
	Figure 2. Iodide accelerates skeleton growth in sea urchin larvae. (A) The phenotype of 4 dpf S. purpuratus pluteus larvae cultured in filtered artificial seawater (A1,A2) and sodium iodide (NaI) in FASW (A3,A4), respectively. (A1,A2) and (A3,A4) are different focal planes of the same larvae focusing on the right and left arms, respectively. (B) Four violin plots with box and whisker plots overlaid plotting the length of the skeleton (pixels) for the different skeletal parts in FASW (n = 42) (negative control) and sodium iodide (NaI) in FASW (n = 43), measured in larvae collected from three independent experiments. Boxes show the median, lower and upper quartiles, while the whiskers extend to the minimum and maximum data points. A student’s two-tailed t-test was performed, (p < 0.01) and * (p < 0.001), and reveals that larval skeletal parts are significantly longer when cultured in NaI FASW, with the post-oral, oral transverse, and oral distal skeletal lengths the longest and body rod a little longer. (C) Cartoon skeletons illustrating the longer skeletal lengths in the NaI FASW condition compared to normal FASW. BR, Body Rod; OD, Oral Distal; OT; Oral Transverse; PO, Post Oral; Lv, lateral view.
	Figure 3. Identification of the THs pathway components in sea urchin genome and identification of putative producing (orange) and/or receiving (blue) cells in sea urchin embryo and pluteus larva. (A) Scheme summarizing the data reported in this study. The scheme includes both the canonical and non-canonical integrin-mediated transduction cascades activated by the THs. Names in purple indicate genes belonging to the vertebrate pathway that have homologs in the sea urchin S. purpuratus genome. Purple boxes contain the proposed names for the sea urchin homologs of the genes involved in the main TH pathway. (B,C) Schematic representation of the expression patterns of Sp-Pxdn (orange), indicative of a producing cell and Sp-Thr (blue), indicative of a receiving cell. at gastrula (B) and pluteus (C) stages. Color-code is the same as shown in (A).

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