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Sci Rep
2017 Mar 08;7:43563. doi: 10.1038/srep43563.
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Troponin-I is present as an essential component of muscles in echinoderm larvae.
Yaguchi S
,
Yaguchi J
,
Tanaka H
.
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The troponin complex, composed of Troponin-I, Troponin-T and Troponin-C, is an essential mediator of the contraction of striated muscle downstream of calcium signaling in almost all bilaterians. However, in echinoderms and hemichordates, collectively termed Ambulacraria, the components of the troponin complex have never been isolated, thus suggesting that these organisms lost the troponin system during evolution. Here, by analyzing genomic information from sea urchins, we identify the troponin-I gene and isolate its complete mRNA sequence. Using this information, we reveal that the larval muscles express this gene and its translated product and that the protein is definitely a functional molecule expressed in sea urchin larvae by showing that Troponin-I morphants are unable to swallow algae. We conclude that muscular contraction in all bilaterians universally depends on a regulatory system mediated by Troponin-I, which emerged in the common ancestor of bilaterians.
Figure 1. Sea urchin has a TnI gene.(A) The phylogenic tree of TnI based on the C-terminal troponin motif indicates that the sea urchin TnI forms a sister group with chordate TnI. The number at each branch point is the bootstrap value (n = 500). In vertebrates, TnI is categorized into three groups: slow, cardiac, and fast TnIs. H. sapiens troponin-C (TnC) was used as the outgroup. Accession numbers for each TnI are listed in the Table 1. The bar indicates evolutionary distance. (B) The alignment of TnI from sea urchin, fly and zebrafish. The red square indicates the inhibitory region. The magenta and green underlines indicate the positions of the TnT binding site and of the amino acid sequence equivalent to the position of the antigen of Mesocentrotus nudus TnI, respectively. The red characters in the zebrafish sequence indicate the switch region.
Figure 2. In situ hybridization of HpTnI in 3-day-old larvae.(A) HpTnI is likely expressed around the esophagus, but the signal is not clear from the chromogenic in situ hybridization. The region outlined by the dotted square is magnified in (B). (C,D) Fluorescence in situ hybridization revealed the detailed pattern of HpTnI expression in the esophagus (E), esophageal muscle (EM), anal sphincter (AS) and pyloric sphincter (PS).
Figure 3. Expression of HpTnI protein in sea urchin larvae.(A) Schematic of muscular actin bundles in sea urchin larva. M, E, EM, PS, and AS indicate mouth, esophagus, esophageal muscles, pyloric sphincter and anal sphincter, respectively. (B) An optical section of a 60-h larva expressing HpTnI in the esophagus, esophageal region and the regions of the pyloric (PS) and anal (AS) sphincters. (C) Stacked image of a 60-h larva. HpTnI patterns are similar between 4 days (D) and 7 days (E). HpTnI expression in the ventral ectoderm is conspicuous by 4 days (D, arrowhead). (F) The anterior of the larva is at the top. HpTnI expression in the ventral ectoderm is clearly visible (arrowhead). (G) No ectodermal expression of HpTnI is visible in a Nodal morphant. (H and I) By contrast, with Nodal overexpression and in a Lefty morphant, the whole ectoderm except for the anterior and posterior ends expresses HpTnI. (J) A similar TnI pattern was observed in 72-h larvae of Temnopleurus reevesii. LV, lateral view; AV, anal view; DV, dorsal view. Bar = 20 μm.
Figure 4. HpTnI is required for swallowing food.Gastrulation and actin bundling occur normally in the HpTnI morphant (E,G), as in the control (A,C). (B,C) HpTnI in a control larva. (F,G) The morphant lacks HpTnI protein. The fluorescence of algae is observed in the stomach and intestine in a control larva (D) but only in the throat in the morphant (H, arrow). (I) Ratios of algae ingestion in the control and HpTnI morphants. p: Student’s t-test. (J) Ratios of swallowing algae in the control and HpTnI morphants. p: Student’s t-test.
Figure 5. Phylogenic tree of Troponin-C (TnC) and Calmodulin (CaM).The number at each branch point is the bootstrap value (n = 500). H. sapiens Troponin-T was used as the outgroup. Accession numbers for each gene are listed in the Table 1. The bar indicates the evolutionary distance.
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