Nizhnichenko VA et al. (2022), Muscle Regeneration in Holothurians without the...

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Int J Mol Sci 2022 Dec 16;2324:. doi: 10.3390/ijms232416037.

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Muscle Regeneration in Holothurians without the Upregulation of Muscle Genes.

Nizhnichenko VA , Boyko AV , Ginanova TT , Dolmatov IY .

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The holothurian Eupentacta fraudatrix is capable of fully restoring its muscles after transverse dissection. Although the regeneration of these structures is well studied at the cellular level, the molecular basis of the process remains poorly understood. To identify genes that may be involved in the regulation of muscle regeneration, the transcriptome of the longitudinal muscle band of E. fraudatrix has been sequenced at different time periods post-injury. An analysis of the map of biological processes and pathways has shown that most genes associated with myogenesis decrease their expression during the regeneration. The only exception is the genes united by the GO term "heart valve development". This may indicate the antiquity of mechanisms of mesodermal structure transformation, which was co-opted into various morphogeneses in deuterostomes. Two groups of genes that play a key role in the regeneration have been analyzed: transcription factors and matrix metalloproteinases. A total of six transcription factor genes (Ef-HOX5, Ef-ZEB2, Ef-RARB, Ef-RUNX1, Ef-SOX17, and Ef-ZNF318) and seven matrix metalloproteinase genes (Ef-MMP11, Ef-MMP13, Ef-MMP13-1, Ef-MMP16-2, Ef-MMP16-3, Ef-MMP24, and Ef-MMP24-1) showing differential expression during myogenesis have been revealed. The identified genes are assumed to be involved in the muscle regeneration in holothurians.

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	Figure 1. Scheme of a longitudinal section through ambulacrum at different stages after transverse cutting of a holothurian, E. fraudatrix. (a) Undamaged ambulacrum. (b) The ambulacrum immediately after cutting. (c) The ambulacrum at 2–4 dpd. (d) The ambulacrum at 10th dpd (first stage of regeneration). (e) The ambulacrum at 20th dpd (second stage of regeneration). ca, connective-tissue thickening (anlage); ce, coelomic epithelium; ct, connective tissue of the body wall; dm, destroyed muscle bundle; h, hemal lacuna; lmb, longitudinal muscle band; mb, muscle bundles; nc, radial nerve cord; nm, new muscle bundles; wv, radial water-vascular canal; w, wound.
	Figure 2. Transverse semithin sections of LMB at different stages after cutting of a holothurian, E. fraudatrix. (a) Undamaged LMB. (b) The LMB at 10th dpd (first stage of regeneration). (c) The LMB at 20th dpd (second stage of regeneration). ce, coelomic epithelium; ct, connective tissue of the body wall; h, hemal lacuna; lmb, longitudinal muscle band; nc, radial nerve cord; nm, new muscle bundles; wv, radial water-vascular canal; arrows indicate the sites of immersion of myogenic cells in the connective tissue.
	Figure 3. Correlation map of all RNA-seq samples and replicates. 10 dpd and 20 dpd—the first and second stages of regeneration, int—intact sample.
	Figure 4. Venn diagram of up- and downregulated DEGs. NR—set of sequences with hits in the NCBI non-redundant database.
	Figure 5. Phylogenetic trees showing the relationships of the TF sequences of the E. fraudatrix with homolog proteins of other animals. (a) HOX5; (b) RUNX1; (c) ZEB2; (d) SOX17; (e) RARB; (f) ZNF-318. The values on the branches indicate their length. The phylogenetic trees were constructed using the Maximum Likelihood algorithm in the MEGA11 program.
	Figure 6. TPM values of the TF genes with significant changes in the expression level compared to the intact sample during the regeneration in E. fraudatrix.
	Figure 7. Scheme of structure of the differential expressed matrix metalloproteinases in E. fraudatrix.
	Figure 8. Network of enrichment biological processes and pathways during ambulacrum regeneration in E. fraudatrix. Nodes represent biological process (gene set). Edges represent overlap between pair of gene sets. Node size and edge width depend on the number of genes. Node fill represents enrichment scores of terms at the first (right half) and second (left half) stage of regeneration relative to the intact sample. The color gradient represents an increase (red) or decrease (blue) in the level of expression (depending on the enrichment score) in the regeneration, relative to the intact tissue. 1–7—blocks associated with the regeneration of various structures of ambulacrum. The full version of the network is provided in Supplementary Figure S2.

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