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Mesodermal origin of median fin mesenchyme and tail muscle in amphibian larvae.

Taniguchi Y, Kurth T, Medeiros DM, Tazaki A, Ramm R, Epperlein HH - Sci Rep (2015)

Bottom Line: Mesenchyme is an embryonic precursor tissue that generates a range of structures in vertebrates including cartilage, bone, muscle, kidney, and the erythropoietic system.Because ectodermal and mesodermal mesenchyme can form in close proximity and give rise to similar derivatives, the embryonic origin of many mesenchyme-derived tissues is still unclear.Using similar strategies in the Mexican axolotl (Ambystoma mexicanum), and the South African clawed toad (Xenopus laevis), we traced the origins of fin mesenchyme and tail muscle in amphibians.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Anatomy, Technische Universität Dresden, Fetscherstrasse 74, D-01307 Dresden, Germany [2] Center for Regenerative Therapies, Technische Universität Dresden, Fetscherstrasse 105, D-01307 Dresden, Germany.

ABSTRACT
Mesenchyme is an embryonic precursor tissue that generates a range of structures in vertebrates including cartilage, bone, muscle, kidney, and the erythropoietic system. Mesenchyme originates from both mesoderm and the neural crest, an ectodermal cell population, via an epithelial to mesenchymal transition (EMT). Because ectodermal and mesodermal mesenchyme can form in close proximity and give rise to similar derivatives, the embryonic origin of many mesenchyme-derived tissues is still unclear. Recent work using genetic lineage tracing methods have upended classical ideas about the contributions of mesodermal mesenchyme and neural crest to particular structures. Using similar strategies in the Mexican axolotl (Ambystoma mexicanum), and the South African clawed toad (Xenopus laevis), we traced the origins of fin mesenchyme and tail muscle in amphibians. Here we present evidence that fin mesenchyme and striated tail muscle in both animals are derived solely from mesoderm and not from neural crest. In the context of recent work in zebrafish, our experiments suggest that trunk neural crest cells in the last common ancestor of tetrapods and ray-finned fish lacked the ability to form ectomesenchyme and its derivatives.

No MeSH data available.


Related in: MedlinePlus

Expression of molecular markers for epidermis, mesoderm, and neural crest.In situ hybridization of axolotl neurulae (stage 15) with keratin (A, A’), sox2 (B, B’ and B”), brachyury (C, C’ and C”) and tfap2a (D, D’ and D”) riboprobes. A–D, dorsal views of whole embryos. A’–D’, posterior views of whole embryos. A”–D”, posterior aspects of anterior halves of bisected embryos. Sectioning planes are indicated by dashed lines and run through the middle of region 3 fold/plate (A’, C’ and D’) or through region 2 (B). Red double-dashed lines indicate neural folds; prospective epidermis is lateral and neural plate medial to the folds. E, fate of plate/fold region3 based on in situ hybridization with brachyury (bra), sox2 and tfap2a riboprobes (neurula stage 15). Brachyury: positive in the centre of plate region 3; tfap2a: positive.in cranial and trunk neural folds until the anterior part of fold region 3; sox2: positive in cranial and region 2 plate. F and G, transverse sections through neural fold/plate (stage 15) in region 1–2 (F) and middle of region3 (G). Axial differences of neural plate and neural crest potential become evident (neuroectoderm vs. mesoderm and neural crest vs. neural fold, respectively). These data and the indication of the distribution of the tfap2-, sox2- and bra-zones in E are based on in situ hybridization (see above). nc in F, prospective neural crest; nfo in G, tfap2a-negative neural fold tissue, probably mesoderm. Number of experiments: about 20 for each riboprobe. White arrowheads in A‘-D‘ point to blastopore. Abbreviations: not, notochord; nfo, neural fold; cr. nfo, cranial neurl fold; npl, neural plate; ax, axial mesoderm; pax, paraxial mesoderm. Scale bars, 500 μm (D’) and 200 μm (D”).
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f6: Expression of molecular markers for epidermis, mesoderm, and neural crest.In situ hybridization of axolotl neurulae (stage 15) with keratin (A, A’), sox2 (B, B’ and B”), brachyury (C, C’ and C”) and tfap2a (D, D’ and D”) riboprobes. A–D, dorsal views of whole embryos. A’–D’, posterior views of whole embryos. A”–D”, posterior aspects of anterior halves of bisected embryos. Sectioning planes are indicated by dashed lines and run through the middle of region 3 fold/plate (A’, C’ and D’) or through region 2 (B). Red double-dashed lines indicate neural folds; prospective epidermis is lateral and neural plate medial to the folds. E, fate of plate/fold region3 based on in situ hybridization with brachyury (bra), sox2 and tfap2a riboprobes (neurula stage 15). Brachyury: positive in the centre of plate region 3; tfap2a: positive.in cranial and trunk neural folds until the anterior part of fold region 3; sox2: positive in cranial and region 2 plate. F and G, transverse sections through neural fold/plate (stage 15) in region 1–2 (F) and middle of region3 (G). Axial differences of neural plate and neural crest potential become evident (neuroectoderm vs. mesoderm and neural crest vs. neural fold, respectively). These data and the indication of the distribution of the tfap2-, sox2- and bra-zones in E are based on in situ hybridization (see above). nc in F, prospective neural crest; nfo in G, tfap2a-negative neural fold tissue, probably mesoderm. Number of experiments: about 20 for each riboprobe. White arrowheads in A‘-D‘ point to blastopore. Abbreviations: not, notochord; nfo, neural fold; cr. nfo, cranial neurl fold; npl, neural plate; ax, axial mesoderm; pax, paraxial mesoderm. Scale bars, 500 μm (D’) and 200 μm (D”).

Mentions: Since we showed that both neural plate and neural fold in region 3 form tail muscle and fin mesenchyme, we decided to compare the relative contributions of the two regions to these derivatives. First we tested the effect of ablating region 3 neural plate and region 3 neural fold on tail morphology. We found that while ablation of region 3 neural plate results in severe tail malformation (Fig. S3A), ablation of region 3 neural fold leads to only limited defects (Fig. S3B). We then tested if neural plate region 3 was capable of organizing the formation of fin mesenchyme or a full tail at a heterotopic site where axial mesoderm and neural crest are present. We grafted region 3 plate into the position of region 1 plate and found that an almost complete ectopic tail, with fin mesenchyme, muscle, and spinal cord derived from the GFP+ graft was formed, and with notochord derived from the host (Fig. 4), as reported previously for Xenopus22. Both the mesodermal homo- and heterotopic plate region 3 grafts might contain marginal ectodermal and NC cells. To rule out any contribution of NC, we isolated only the central part of the posterior region 3 plate and grafted it homo- and heterotopically to white hosts. We observed GFP+ striated muscle and fin mesenchyme in both cases (Fig. 5). Due to its topography and as evidenced by in situ hybridization this central region consists definitely only of mesoderm (Fig. 6). Taken together, these experiments suggest that the posterior neural plate and neural folds (region 3) are the main source of tail fin mesenchyme and tail muscle.


Mesodermal origin of median fin mesenchyme and tail muscle in amphibian larvae.

Taniguchi Y, Kurth T, Medeiros DM, Tazaki A, Ramm R, Epperlein HH - Sci Rep (2015)

Expression of molecular markers for epidermis, mesoderm, and neural crest.In situ hybridization of axolotl neurulae (stage 15) with keratin (A, A’), sox2 (B, B’ and B”), brachyury (C, C’ and C”) and tfap2a (D, D’ and D”) riboprobes. A–D, dorsal views of whole embryos. A’–D’, posterior views of whole embryos. A”–D”, posterior aspects of anterior halves of bisected embryos. Sectioning planes are indicated by dashed lines and run through the middle of region 3 fold/plate (A’, C’ and D’) or through region 2 (B). Red double-dashed lines indicate neural folds; prospective epidermis is lateral and neural plate medial to the folds. E, fate of plate/fold region3 based on in situ hybridization with brachyury (bra), sox2 and tfap2a riboprobes (neurula stage 15). Brachyury: positive in the centre of plate region 3; tfap2a: positive.in cranial and trunk neural folds until the anterior part of fold region 3; sox2: positive in cranial and region 2 plate. F and G, transverse sections through neural fold/plate (stage 15) in region 1–2 (F) and middle of region3 (G). Axial differences of neural plate and neural crest potential become evident (neuroectoderm vs. mesoderm and neural crest vs. neural fold, respectively). These data and the indication of the distribution of the tfap2-, sox2- and bra-zones in E are based on in situ hybridization (see above). nc in F, prospective neural crest; nfo in G, tfap2a-negative neural fold tissue, probably mesoderm. Number of experiments: about 20 for each riboprobe. White arrowheads in A‘-D‘ point to blastopore. Abbreviations: not, notochord; nfo, neural fold; cr. nfo, cranial neurl fold; npl, neural plate; ax, axial mesoderm; pax, paraxial mesoderm. Scale bars, 500 μm (D’) and 200 μm (D”).
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f6: Expression of molecular markers for epidermis, mesoderm, and neural crest.In situ hybridization of axolotl neurulae (stage 15) with keratin (A, A’), sox2 (B, B’ and B”), brachyury (C, C’ and C”) and tfap2a (D, D’ and D”) riboprobes. A–D, dorsal views of whole embryos. A’–D’, posterior views of whole embryos. A”–D”, posterior aspects of anterior halves of bisected embryos. Sectioning planes are indicated by dashed lines and run through the middle of region 3 fold/plate (A’, C’ and D’) or through region 2 (B). Red double-dashed lines indicate neural folds; prospective epidermis is lateral and neural plate medial to the folds. E, fate of plate/fold region3 based on in situ hybridization with brachyury (bra), sox2 and tfap2a riboprobes (neurula stage 15). Brachyury: positive in the centre of plate region 3; tfap2a: positive.in cranial and trunk neural folds until the anterior part of fold region 3; sox2: positive in cranial and region 2 plate. F and G, transverse sections through neural fold/plate (stage 15) in region 1–2 (F) and middle of region3 (G). Axial differences of neural plate and neural crest potential become evident (neuroectoderm vs. mesoderm and neural crest vs. neural fold, respectively). These data and the indication of the distribution of the tfap2-, sox2- and bra-zones in E are based on in situ hybridization (see above). nc in F, prospective neural crest; nfo in G, tfap2a-negative neural fold tissue, probably mesoderm. Number of experiments: about 20 for each riboprobe. White arrowheads in A‘-D‘ point to blastopore. Abbreviations: not, notochord; nfo, neural fold; cr. nfo, cranial neurl fold; npl, neural plate; ax, axial mesoderm; pax, paraxial mesoderm. Scale bars, 500 μm (D’) and 200 μm (D”).
Mentions: Since we showed that both neural plate and neural fold in region 3 form tail muscle and fin mesenchyme, we decided to compare the relative contributions of the two regions to these derivatives. First we tested the effect of ablating region 3 neural plate and region 3 neural fold on tail morphology. We found that while ablation of region 3 neural plate results in severe tail malformation (Fig. S3A), ablation of region 3 neural fold leads to only limited defects (Fig. S3B). We then tested if neural plate region 3 was capable of organizing the formation of fin mesenchyme or a full tail at a heterotopic site where axial mesoderm and neural crest are present. We grafted region 3 plate into the position of region 1 plate and found that an almost complete ectopic tail, with fin mesenchyme, muscle, and spinal cord derived from the GFP+ graft was formed, and with notochord derived from the host (Fig. 4), as reported previously for Xenopus22. Both the mesodermal homo- and heterotopic plate region 3 grafts might contain marginal ectodermal and NC cells. To rule out any contribution of NC, we isolated only the central part of the posterior region 3 plate and grafted it homo- and heterotopically to white hosts. We observed GFP+ striated muscle and fin mesenchyme in both cases (Fig. 5). Due to its topography and as evidenced by in situ hybridization this central region consists definitely only of mesoderm (Fig. 6). Taken together, these experiments suggest that the posterior neural plate and neural folds (region 3) are the main source of tail fin mesenchyme and tail muscle.

Bottom Line: Mesenchyme is an embryonic precursor tissue that generates a range of structures in vertebrates including cartilage, bone, muscle, kidney, and the erythropoietic system.Because ectodermal and mesodermal mesenchyme can form in close proximity and give rise to similar derivatives, the embryonic origin of many mesenchyme-derived tissues is still unclear.Using similar strategies in the Mexican axolotl (Ambystoma mexicanum), and the South African clawed toad (Xenopus laevis), we traced the origins of fin mesenchyme and tail muscle in amphibians.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Anatomy, Technische Universität Dresden, Fetscherstrasse 74, D-01307 Dresden, Germany [2] Center for Regenerative Therapies, Technische Universität Dresden, Fetscherstrasse 105, D-01307 Dresden, Germany.

ABSTRACT
Mesenchyme is an embryonic precursor tissue that generates a range of structures in vertebrates including cartilage, bone, muscle, kidney, and the erythropoietic system. Mesenchyme originates from both mesoderm and the neural crest, an ectodermal cell population, via an epithelial to mesenchymal transition (EMT). Because ectodermal and mesodermal mesenchyme can form in close proximity and give rise to similar derivatives, the embryonic origin of many mesenchyme-derived tissues is still unclear. Recent work using genetic lineage tracing methods have upended classical ideas about the contributions of mesodermal mesenchyme and neural crest to particular structures. Using similar strategies in the Mexican axolotl (Ambystoma mexicanum), and the South African clawed toad (Xenopus laevis), we traced the origins of fin mesenchyme and tail muscle in amphibians. Here we present evidence that fin mesenchyme and striated tail muscle in both animals are derived solely from mesoderm and not from neural crest. In the context of recent work in zebrafish, our experiments suggest that trunk neural crest cells in the last common ancestor of tetrapods and ray-finned fish lacked the ability to form ectomesenchyme and its derivatives.

No MeSH data available.


Related in: MedlinePlus