Gene duplication and recruitment of a specific tropomyosin into striated muscle cells in the jellyfishPodocoryne carnea

Gröger, Hans; Callaerts, Patrick; Gehring, Walter; Schmid, Volker

doi:10.1002/(sici)1097-010x(19991215)285:4<378::aid-jez5>3.0.co;2-c

Cited by 30 publications

(5 citation statements)

References 27 publications

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“…The band 5 and 6 proteins were identified as tropomyosin isoforms comprising 242 and 246 residues and sharing 42% and 46% identity with tropomyosin-1 and tropomyosin-2, respectively, of the hydrozoan jellyfish Podocoryna carnea 34 . The two moon jelly tropomyosin isoforms share only 23% amino acid identity with each other.…”

Section: Resultsmentioning

confidence: 99%

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Smooth muscle-like Ca2+-regulation of actin–myosin interaction in adult jellyfish striated muscle

Tanaka

Ishimaru

Nagatsuka

et al. 2018

Sci Rep

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Cnidaria is an animal phylum, whose members probably have the most ancestral musculature. We prepared and characterized, for the first time to our knowledge, native actomyosin from the striated myoepithelium of the adult moon jelly Aurelia sp. The actomyosin contained myosin, paramyosin-like protein, Ser/Thr-kinase, actin, and two isoforms of tropomyosin, but not troponin, which is known to activate contraction dependent on intracellular Ca2+ signaling in almost all striated muscles of bilaterians. Notably, the myosin comprised striated muscle-type heavy chain and smooth muscle-type regulatory light chains. In the presence of Ca2+, the Mg-ATPase activity of actomyosin was stimulated and Ser21 of the regulatory light chain was concomitantly phosphorylated by the addition of calmodulin and myosin light chain kinase prepared from chicken smooth muscle. Collectively, these results suggest that, similar to smooth muscle, the contraction of jellyfish striated muscle is regulated by Ca2+-dependent phosphorylation of the myosin light chain.

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Section: Resultsmentioning

confidence: 99%

“…Gröger et al . 34 reported that tropomyosin-1 of P. carnea is a non-muscle isoform and is expressed in all tissues, whereas tropomyosin-2 is specific to the striated muscle of the subumbrella. On SDS-PAGE (Fig.…”

Section: Resultsmentioning

confidence: 99%

Smooth muscle-like Ca2+-regulation of actin–myosin interaction in adult jellyfish striated muscle

Tanaka

Ishimaru

Nagatsuka

et al. 2018

Sci Rep

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“…Of particular note is the up-regulation of a tropomyosin transcript in the gonozooids. In the hydrozoan Podocoryna carnea , a tropomyosin, tpm2 , is expressed solely in the striated muscle of the developing and adult medusa life cycle stages and not in the polyp [25], as opposed to tpm1 , which is ubiquitously expressed in both polyp and medusae stages [26]. In Hydractinia , gonophore development is greatly truncated and never reaches the medusae stage.…”

Section: Resultsmentioning

confidence: 99%

Differential gene expression between functionally specialized polyps of the colonial hydrozoan Hydractinia symbiolongicarpus (Phylum Cnidaria)

2014

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BackgroundA colony of the hydrozoan Hydractinia symbiolongicarpus comprises genetically identical yet morphologically distinct and functionally specialized polyp types. The main labor divisions are between feeding, reproduction and defense. In H. symbiolongicarpus, the feeding polyp (called a gastrozooid) has elongated tentacles and a mouth, which are absent in the reproductive polyp (gonozooid) and defensive polyp (dactylozooid). Instead, the dactylozooid has an extended body column with an abundance of stinging cells (nematocysts) and the gonozooid bears gonophores on its body column. Morphological differences between polyp types can be attributed to simple changes in their axial patterning during development, and it has long been hypothesized that these specialized polyps arose through evolutionary alterations in oral-aboral patterning of the ancestral gastrozooid.ResultsAn assembly of 66,508 transcripts (>200 bp) were generated using short-read Illumina RNA-Seq libraries constructed from feeding, reproductive, and defensive polyps of H. symbiolongicarpus. Using several different annotation methods, approximately 54% of the transcripts were annotated. Differential expression analyses were conducted between these three polyp types to isolate genes that may be involved in functional, histological, and pattering differences between polyp types. Nearly 7 K transcripts were differentially expressed in a polyp-specific manner, including members of the homeodomain, myosin, toxin and BMP gene families. We report the spatial expression of a subset of these polyp-specific transcripts to validate our differential expression analyses.ConclusionsWhile potentially originating through simple changes in patterning, polymorphic polyps in Hydractinia are the result of differentially expressed functional, structural, and patterning genes.The differentially expressed genes identified in our study provide a starting point for future investigations of the developmental patterning and functional differences that are displayed in the different polyp types that confer a division of labor within a colony of H. symbiolongicarpus.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-406) contains supplementary material, which is available to authorized users.

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“…Myosin Essential and Regulatory Light Chains, Myosin Light Chain-Kinase and Phosphatase, as well as the smooth muscle ATPase regulator Calponin are present in cnidarians genomes (Steinmetz et al, 2012) but have not been functionally characterized yet. Several Tropomyosin paralogs have also been described in cnidarians (Baader et al, 1993; López de Haro et al, 1994; Gröger et al, 1999, 2000; Fujinoki et al, 2002; Steinmetz et al, 2012), including one specific to the striated muscle cells of Podocoryna (Gröger et al, 1999, 2000). However, Troponins, important components of the striated muscle thin filaments, have to date not been found in any cnidarian genomes (Steinmetz et al, 2012).…”

Section: Molecular Characterization Of Muscles In Cnidariansmentioning

confidence: 99%

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Leclère

Röttinger

2017

Front. Cell Dev. Biol.

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The ability to perform muscle contractions is one of the most important and distinctive features of eumetazoans. As the sister group to bilaterians, cnidarians (sea anemones, corals, jellyfish, and hydroids) hold an informative phylogenetic position for understanding muscle evolution. Here, we review current knowledge on muscle function, diversity, development, regeneration and evolution in cnidarians. Cnidarian muscles are involved in various activities, such as feeding, escape, locomotion and defense, in close association with the nervous system. This variety is reflected in the large diversity of muscle organizations found in Cnidaria. Smooth epithelial muscle is thought to be the most common type, and is inferred to be the ancestral muscle type for Cnidaria, while striated muscle fibers and non-epithelial myocytes would have been convergently acquired within Cnidaria. Current knowledge of cnidarian muscle development and its regeneration is limited. While orthologs of myogenic regulatory factors such as MyoD have yet to be found in cnidarian genomes, striated muscle formation potentially involves well-conserved myogenic genes, such as twist and mef2. Although satellite cells have yet to be identified in cnidarians, muscle plasticity (e.g., de- and re-differentiation, fiber repolarization) in a regenerative context and its potential role during regeneration has started to be addressed in a few cnidarian systems. The development of novel tools to study those organisms has created new opportunities to investigate in depth the development and regeneration of cnidarian muscle cells and how they contribute to the regenerative process.

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Gene duplication and recruitment of a specific tropomyosin into striated muscle cells in the jellyfishPodocoryne carnea

Cited by 30 publications

References 27 publications

Smooth muscle-like Ca2+-regulation of actin–myosin interaction in adult jellyfish striated muscle

Smooth muscle-like Ca2+-regulation of actin–myosin interaction in adult jellyfish striated muscle

Differential gene expression between functionally specialized polyps of the colonial hydrozoan Hydractinia symbiolongicarpus (Phylum Cnidaria)

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

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