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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

An evolutionary scenario for cartilage calcification in jawed vertebrates. Expression patterns and cartilage matrix calcification were mapped onto a simplified vertebrate phylogenetic tree to deduce ancestral states and polarize evolutionary change. We propose that, in the last vertebrate common ancestor, the expression of Col2a1 experienced a strong downregulation in maturing, non-calcified, cartilaginous regions. This downregulation was subsequently inherited by distinct vertebrate lineages, and is associated to hard cartilage in cyclostomes and to calcified cartilage in jawed vertebrates. The chondrichthyan and osteichthyan representatives analyzed in this study display a calcified Col2a1-negative vertebral cartilage, a likely jawed vertebrate synapomorphy. Tesserae calcification, a recent chondrichthyan innovation, occurs in the absence of Col2a1 downregulation. Perichondrium and bone have been omitted for the sake of simplicity. See text for details.
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Figure 7: An evolutionary scenario for cartilage calcification in jawed vertebrates. Expression patterns and cartilage matrix calcification were mapped onto a simplified vertebrate phylogenetic tree to deduce ancestral states and polarize evolutionary change. We propose that, in the last vertebrate common ancestor, the expression of Col2a1 experienced a strong downregulation in maturing, non-calcified, cartilaginous regions. This downregulation was subsequently inherited by distinct vertebrate lineages, and is associated to hard cartilage in cyclostomes and to calcified cartilage in jawed vertebrates. The chondrichthyan and osteichthyan representatives analyzed in this study display a calcified Col2a1-negative vertebral cartilage, a likely jawed vertebrate synapomorphy. Tesserae calcification, a recent chondrichthyan innovation, occurs in the absence of Col2a1 downregulation. Perichondrium and bone have been omitted for the sake of simplicity. See text for details.

Mentions: Another site of calcification in S.c. corresponds to the developing tesserae embedded in Meckel's cartilage, a process classically described to occur at the surface of the cartilaginous skeletal piece (Kemp and Westrin, 1979; Dean et al., 2009). As we show here, the onset of this type of calcification takes place in a Col2-positive context, within the cartilaginous scaffold (Figures 1, 6). We failed to detect Col1a1/Col1a2 expression in the chondrocytes neighboring the mineralized matrix, suggesting that the cellular processes involved in matrix calcification are very different from what has been described in osteichthyan bone or chondroid bone (Mizoguchi et al., 1997). This type of calcification is well developed in extant batoid and selachimorph species, and is also known in fossil holocephalan species (Grogan and Lund, 2000; Finarelli and Coates, 2014) and, therefore, is considered to be an early evolutionary innovation of the chondrichthyan lineage (Figure 7).


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)

An evolutionary scenario for cartilage calcification in jawed vertebrates. Expression patterns and cartilage matrix calcification were mapped onto a simplified vertebrate phylogenetic tree to deduce ancestral states and polarize evolutionary change. We propose that, in the last vertebrate common ancestor, the expression of Col2a1 experienced a strong downregulation in maturing, non-calcified, cartilaginous regions. This downregulation was subsequently inherited by distinct vertebrate lineages, and is associated to hard cartilage in cyclostomes and to calcified cartilage in jawed vertebrates. The chondrichthyan and osteichthyan representatives analyzed in this study display a calcified Col2a1-negative vertebral cartilage, a likely jawed vertebrate synapomorphy. Tesserae calcification, a recent chondrichthyan innovation, occurs in the absence of Col2a1 downregulation. Perichondrium and bone have been omitted for the sake of simplicity. See text for details.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 7: An evolutionary scenario for cartilage calcification in jawed vertebrates. Expression patterns and cartilage matrix calcification were mapped onto a simplified vertebrate phylogenetic tree to deduce ancestral states and polarize evolutionary change. We propose that, in the last vertebrate common ancestor, the expression of Col2a1 experienced a strong downregulation in maturing, non-calcified, cartilaginous regions. This downregulation was subsequently inherited by distinct vertebrate lineages, and is associated to hard cartilage in cyclostomes and to calcified cartilage in jawed vertebrates. The chondrichthyan and osteichthyan representatives analyzed in this study display a calcified Col2a1-negative vertebral cartilage, a likely jawed vertebrate synapomorphy. Tesserae calcification, a recent chondrichthyan innovation, occurs in the absence of Col2a1 downregulation. Perichondrium and bone have been omitted for the sake of simplicity. See text for details.
Mentions: Another site of calcification in S.c. corresponds to the developing tesserae embedded in Meckel's cartilage, a process classically described to occur at the surface of the cartilaginous skeletal piece (Kemp and Westrin, 1979; Dean et al., 2009). As we show here, the onset of this type of calcification takes place in a Col2-positive context, within the cartilaginous scaffold (Figures 1, 6). We failed to detect Col1a1/Col1a2 expression in the chondrocytes neighboring the mineralized matrix, suggesting that the cellular processes involved in matrix calcification are very different from what has been described in osteichthyan bone or chondroid bone (Mizoguchi et al., 1997). This type of calcification is well developed in extant batoid and selachimorph species, and is also known in fossil holocephalan species (Grogan and Lund, 2000; Finarelli and Coates, 2014) and, therefore, is considered to be an early evolutionary innovation of the chondrichthyan lineage (Figure 7).

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