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Molecular footprinting of skeletal tissues in the catshark Scyliorhinus canicula and the clawed frog Xenopus tropicalis identifies conserved and derived features of vertebrate calcification.

Enault S, Muñoz DN, Silva WT, Borday-Birraux V, Bonade M, Oulion S, Ventéo S, Marcellini S, Debiais-Thibaud M - Front Genet (2015)

Bottom Line: Understanding the evolutionary emergence and subsequent diversification of the vertebrate skeleton requires a comprehensive view of the diverse skeletal cell types found in distinct developmental contexts, tissues, and species.To date, our knowledge of the molecular nature of the shark calcified extracellular matrix, and its relationships with osteichthyan skeletal tissues, remain scarce.Finally, we uncover a striking parallel, from a molecular and histological perspective, between the vertebral cartilage calcification of both species and discuss the evolutionary origin of endochondral ossification.

View Article: PubMed Central - PubMed

Affiliation: Institut des Sciences de l'Evolution de Montpellier, UMR5554, Université Montpellier, Centre National de la Recherche Scientifique, IRD, EPHE Montpellier, France.

ABSTRACT
Understanding the evolutionary emergence and subsequent diversification of the vertebrate skeleton requires a comprehensive view of the diverse skeletal cell types found in distinct developmental contexts, tissues, and species. To date, our knowledge of the molecular nature of the shark calcified extracellular matrix, and its relationships with osteichthyan skeletal tissues, remain scarce. Here, based on specific combinations of expression patterns of the Col1a1, Col1a2, and Col2a1 fibrillar collagen genes, we compare the molecular footprint of endoskeletal elements from the chondrichthyan Scyliorhinus canicula and the tetrapod Xenopus tropicalis. We find that, depending on the anatomical location, Scyliorhinus skeletal calcification is associated to cell types expressing different subsets of fibrillar collagen genes, such as high levels of Col1a1 and Col1a2 in the neural arches, high levels of Col2a1 in the tesserae, or associated to a drastic Col2a1 downregulation in the centrum. We detect low Col2a1 levels in Xenopus osteoblasts, thereby revealing that the osteoblastic expression of this gene was significantly reduced in the tetrapod lineage. Finally, we uncover a striking parallel, from a molecular and histological perspective, between the vertebral cartilage calcification of both species and discuss the evolutionary origin of endochondral ossification.

No MeSH data available.


Related in: MedlinePlus

Comparison of the Col1a1, Col1a2, and Col2a1 expression patterns during Xenopustropicalis hindlimb development. Stage NF54 (top panel) or NF60 (bottom panel) hindlimbs were examined by whole mount Alizarin red staining (insets), sectioned along the proximo-distal axis and stained with HES, (A–C, M–O) or processed by in situ hybridization for the Xt-Col1a1, Xt-Col1a2, and Xt-Col2a1 probes, (D–L, P–X). Results are shown for the whole skeletal element (left column, scale bar: 500 μm) and higher magnifications of the diaphysis (middle column, scale bar: 50 μm) and epiphysis (right column, scale bar: 50 μm). Arrows and arrowheads show osteoblasts and osteocytes, respectively. In situ hybridization signal is light to dark blue, and brown endogenous X.t. pigment cells are visible on most sections. Legend: Bo, bone; Ch, chondrocytes; Me, medulla; Pe, perichondrium; Sm, striated muscles.
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Figure 3: Comparison of the Col1a1, Col1a2, and Col2a1 expression patterns during Xenopustropicalis hindlimb development. Stage NF54 (top panel) or NF60 (bottom panel) hindlimbs were examined by whole mount Alizarin red staining (insets), sectioned along the proximo-distal axis and stained with HES, (A–C, M–O) or processed by in situ hybridization for the Xt-Col1a1, Xt-Col1a2, and Xt-Col2a1 probes, (D–L, P–X). Results are shown for the whole skeletal element (left column, scale bar: 500 μm) and higher magnifications of the diaphysis (middle column, scale bar: 50 μm) and epiphysis (right column, scale bar: 50 μm). Arrows and arrowheads show osteoblasts and osteocytes, respectively. In situ hybridization signal is light to dark blue, and brown endogenous X.t. pigment cells are visible on most sections. Legend: Bo, bone; Ch, chondrocytes; Me, medulla; Pe, perichondrium; Sm, striated muscles.

Mentions: We examined the expression of Xt-Col1a1, Xt-Col1a2, and Xt-Col2a1 in the diaphysis and epiphysis of X.t. hindlimbs both before (stage NF54, Figures 3A–C) and after (stage NF60, Figures 3M–O) ossification. At stage NF54, Xt-Col1a1, and Xt-Col1a2 are most strongly expressed in perichondral cells of developing long bones (Figures 3D–I). At stage NF60, Xt-Col1a1, and Xt-Col1a2 transcripts are robustly detected in osteoblasts and in some osteocytes, albeit more weakly (Figures 3P–U). Finally, Xt-Col2a1 is expressed in all chondrocytes of NF54 non-calcified cartilaginous elements (Figures 3J–L), and is restricted to the epiphyseal chondrocytes at stage NF60 (Figures 3V–X).


Molecular footprinting of skeletal tissues in the catshark Scyliorhinus canicula and the clawed frog Xenopus tropicalis identifies conserved and derived features of vertebrate calcification.

Enault S, Muñoz DN, Silva WT, Borday-Birraux V, Bonade M, Oulion S, Ventéo S, Marcellini S, Debiais-Thibaud M - Front Genet (2015)

Comparison of the Col1a1, Col1a2, and Col2a1 expression patterns during Xenopustropicalis hindlimb development. Stage NF54 (top panel) or NF60 (bottom panel) hindlimbs were examined by whole mount Alizarin red staining (insets), sectioned along the proximo-distal axis and stained with HES, (A–C, M–O) or processed by in situ hybridization for the Xt-Col1a1, Xt-Col1a2, and Xt-Col2a1 probes, (D–L, P–X). Results are shown for the whole skeletal element (left column, scale bar: 500 μm) and higher magnifications of the diaphysis (middle column, scale bar: 50 μm) and epiphysis (right column, scale bar: 50 μm). Arrows and arrowheads show osteoblasts and osteocytes, respectively. In situ hybridization signal is light to dark blue, and brown endogenous X.t. pigment cells are visible on most sections. Legend: Bo, bone; Ch, chondrocytes; Me, medulla; Pe, perichondrium; Sm, striated muscles.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4584932&req=5

Figure 3: Comparison of the Col1a1, Col1a2, and Col2a1 expression patterns during Xenopustropicalis hindlimb development. Stage NF54 (top panel) or NF60 (bottom panel) hindlimbs were examined by whole mount Alizarin red staining (insets), sectioned along the proximo-distal axis and stained with HES, (A–C, M–O) or processed by in situ hybridization for the Xt-Col1a1, Xt-Col1a2, and Xt-Col2a1 probes, (D–L, P–X). Results are shown for the whole skeletal element (left column, scale bar: 500 μm) and higher magnifications of the diaphysis (middle column, scale bar: 50 μm) and epiphysis (right column, scale bar: 50 μm). Arrows and arrowheads show osteoblasts and osteocytes, respectively. In situ hybridization signal is light to dark blue, and brown endogenous X.t. pigment cells are visible on most sections. Legend: Bo, bone; Ch, chondrocytes; Me, medulla; Pe, perichondrium; Sm, striated muscles.
Mentions: We examined the expression of Xt-Col1a1, Xt-Col1a2, and Xt-Col2a1 in the diaphysis and epiphysis of X.t. hindlimbs both before (stage NF54, Figures 3A–C) and after (stage NF60, Figures 3M–O) ossification. At stage NF54, Xt-Col1a1, and Xt-Col1a2 are most strongly expressed in perichondral cells of developing long bones (Figures 3D–I). At stage NF60, Xt-Col1a1, and Xt-Col1a2 transcripts are robustly detected in osteoblasts and in some osteocytes, albeit more weakly (Figures 3P–U). Finally, Xt-Col2a1 is expressed in all chondrocytes of NF54 non-calcified cartilaginous elements (Figures 3J–L), and is restricted to the epiphyseal chondrocytes at stage NF60 (Figures 3V–X).

Bottom Line: Understanding the evolutionary emergence and subsequent diversification of the vertebrate skeleton requires a comprehensive view of the diverse skeletal cell types found in distinct developmental contexts, tissues, and species.To date, our knowledge of the molecular nature of the shark calcified extracellular matrix, and its relationships with osteichthyan skeletal tissues, remain scarce.Finally, we uncover a striking parallel, from a molecular and histological perspective, between the vertebral cartilage calcification of both species and discuss the evolutionary origin of endochondral ossification.

View Article: PubMed Central - PubMed

Affiliation: Institut des Sciences de l'Evolution de Montpellier, UMR5554, Université Montpellier, Centre National de la Recherche Scientifique, IRD, EPHE Montpellier, France.

ABSTRACT
Understanding the evolutionary emergence and subsequent diversification of the vertebrate skeleton requires a comprehensive view of the diverse skeletal cell types found in distinct developmental contexts, tissues, and species. To date, our knowledge of the molecular nature of the shark calcified extracellular matrix, and its relationships with osteichthyan skeletal tissues, remain scarce. Here, based on specific combinations of expression patterns of the Col1a1, Col1a2, and Col2a1 fibrillar collagen genes, we compare the molecular footprint of endoskeletal elements from the chondrichthyan Scyliorhinus canicula and the tetrapod Xenopus tropicalis. We find that, depending on the anatomical location, Scyliorhinus skeletal calcification is associated to cell types expressing different subsets of fibrillar collagen genes, such as high levels of Col1a1 and Col1a2 in the neural arches, high levels of Col2a1 in the tesserae, or associated to a drastic Col2a1 downregulation in the centrum. We detect low Col2a1 levels in Xenopus osteoblasts, thereby revealing that the osteoblastic expression of this gene was significantly reduced in the tetrapod lineage. Finally, we uncover a striking parallel, from a molecular and histological perspective, between the vertebral cartilage calcification of both species and discuss the evolutionary origin of endochondral ossification.

No MeSH data available.


Related in: MedlinePlus