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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

Histology of the developing Xenopus tropicalis vertebrae. (A) Schematic drawing of transverse sections running through the lateral or the dorsal region of the neural arches. (B) Color code used to represent the distinct skeletal tissues of the X.t. vertebrae in (F,I,N,T,P,V). (C) Whole mount Alizarin red staining of stage NF54 vertebral column (lateral view, anterior to the left). (D–I) Histology of the stage NF54 vertebrae examined with HES (D,E,G,H). (J) Whole mount Alizarin red staining of stage NF57 vertebral columns (lateral view, anterior to the left). (K–V) Histology of the stage NF57 vertebrae examined with HES (K,O,Q,U), Alcian blue (L,R) and Alizarin red (M,S). Insets in D, G, K and Q are shown in F, I, P and V, respectively. Panels E, H, K, O, Q and U are schematized in F, I, N, P, T and V, respectively. Abbreviations: nt, neural tube; ntc, notochord. Scale bars: 1 mm in (C,J); 250 μm in (D,G); 50 μm in (E,F) and (H,I); 500 μm in (K–N) and (Q–T); and 50 μm in (O,P,U,V).
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Figure 4: Histology of the developing Xenopus tropicalis vertebrae. (A) Schematic drawing of transverse sections running through the lateral or the dorsal region of the neural arches. (B) Color code used to represent the distinct skeletal tissues of the X.t. vertebrae in (F,I,N,T,P,V). (C) Whole mount Alizarin red staining of stage NF54 vertebral column (lateral view, anterior to the left). (D–I) Histology of the stage NF54 vertebrae examined with HES (D,E,G,H). (J) Whole mount Alizarin red staining of stage NF57 vertebral columns (lateral view, anterior to the left). (K–V) Histology of the stage NF57 vertebrae examined with HES (K,O,Q,U), Alcian blue (L,R) and Alizarin red (M,S). Insets in D, G, K and Q are shown in F, I, P and V, respectively. Panels E, H, K, O, Q and U are schematized in F, I, N, P, T and V, respectively. Abbreviations: nt, neural tube; ntc, notochord. Scale bars: 1 mm in (C,J); 250 μm in (D,G); 50 μm in (E,F) and (H,I); 500 μm in (K–N) and (Q–T); and 50 μm in (O,P,U,V).

Mentions: Because of the complex shape of the X.t. vertebrae, transverse sections either run through the lateral (Figures 4A,D–F,K–P) or the dorsal (Figures 4A,G–I,Q–V) region of the non-calcified (stage NF54, see Figures 4B–I) and calcified (stage NF57, see Figures 4J–V) neural arches protecting the neural tube. At stage NF57, the cartilage matrix is abundant (Figures 4L,R) and displays a pronounced HES and Alizarin red staining co-localizing at the level of the dorsal region underlying the notochord, and within the lateral and dorsal neural arches (see Figures 4K,M,N,Q,S,T). In addition, cartilage calcification and periosteal bone develop in contact to each other (Figures 4O,P,U,V).


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)

Histology of the developing Xenopus tropicalis vertebrae. (A) Schematic drawing of transverse sections running through the lateral or the dorsal region of the neural arches. (B) Color code used to represent the distinct skeletal tissues of the X.t. vertebrae in (F,I,N,T,P,V). (C) Whole mount Alizarin red staining of stage NF54 vertebral column (lateral view, anterior to the left). (D–I) Histology of the stage NF54 vertebrae examined with HES (D,E,G,H). (J) Whole mount Alizarin red staining of stage NF57 vertebral columns (lateral view, anterior to the left). (K–V) Histology of the stage NF57 vertebrae examined with HES (K,O,Q,U), Alcian blue (L,R) and Alizarin red (M,S). Insets in D, G, K and Q are shown in F, I, P and V, respectively. Panels E, H, K, O, Q and U are schematized in F, I, N, P, T and V, respectively. Abbreviations: nt, neural tube; ntc, notochord. Scale bars: 1 mm in (C,J); 250 μm in (D,G); 50 μm in (E,F) and (H,I); 500 μm in (K–N) and (Q–T); and 50 μm in (O,P,U,V).
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Figure 4: Histology of the developing Xenopus tropicalis vertebrae. (A) Schematic drawing of transverse sections running through the lateral or the dorsal region of the neural arches. (B) Color code used to represent the distinct skeletal tissues of the X.t. vertebrae in (F,I,N,T,P,V). (C) Whole mount Alizarin red staining of stage NF54 vertebral column (lateral view, anterior to the left). (D–I) Histology of the stage NF54 vertebrae examined with HES (D,E,G,H). (J) Whole mount Alizarin red staining of stage NF57 vertebral columns (lateral view, anterior to the left). (K–V) Histology of the stage NF57 vertebrae examined with HES (K,O,Q,U), Alcian blue (L,R) and Alizarin red (M,S). Insets in D, G, K and Q are shown in F, I, P and V, respectively. Panels E, H, K, O, Q and U are schematized in F, I, N, P, T and V, respectively. Abbreviations: nt, neural tube; ntc, notochord. Scale bars: 1 mm in (C,J); 250 μm in (D,G); 50 μm in (E,F) and (H,I); 500 μm in (K–N) and (Q–T); and 50 μm in (O,P,U,V).
Mentions: Because of the complex shape of the X.t. vertebrae, transverse sections either run through the lateral (Figures 4A,D–F,K–P) or the dorsal (Figures 4A,G–I,Q–V) region of the non-calcified (stage NF54, see Figures 4B–I) and calcified (stage NF57, see Figures 4J–V) neural arches protecting the neural tube. At stage NF57, the cartilage matrix is abundant (Figures 4L,R) and displays a pronounced HES and Alizarin red staining co-localizing at the level of the dorsal region underlying the notochord, and within the lateral and dorsal neural arches (see Figures 4K,M,N,Q,S,T). In addition, cartilage calcification and periosteal bone develop in contact to each other (Figures 4O,P,U,V).

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