Limits...
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 bone formation and perichondral calcification in jawed vertebrates. Bone/perichondrium histology and gene expression patterns were mapped onto a simplified vertebrate phylogenetic tree to deduce ancestral states and polarize evolutionary change. We propose that the ancestral Clade A fibrillar collagen gene (i.e., before the duplications that produced the distinct member of this family) was expressed in the non-calcified perichondrium. This expression pattern was inherited by the unique cyclostome fibrillar collagen gene which is more closely related to the Col2a1 subgroup. In jawed vertebrates, perichondral cells and osteoblasts maintained high levels of Col1a1 and Col1a2 while the Col2a1 osteoblastic expression was dramatically reduced in most (but not all) lineages. The presence of bone in placoderms and tetrapods supports the idea that the calcified fibrous perichondrium observed in some chondrichthyan species either represents bone evolutionary remnants (Hypothesis 1) or a secondary gain of calcification (Hypothesis 2). Osteocytes have been omitted for the sake of simplicity. See text for details.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4584932&req=5

Figure 6: An evolutionary scenario for bone formation and perichondral calcification in jawed vertebrates. Bone/perichondrium histology and gene expression patterns were mapped onto a simplified vertebrate phylogenetic tree to deduce ancestral states and polarize evolutionary change. We propose that the ancestral Clade A fibrillar collagen gene (i.e., before the duplications that produced the distinct member of this family) was expressed in the non-calcified perichondrium. This expression pattern was inherited by the unique cyclostome fibrillar collagen gene which is more closely related to the Col2a1 subgroup. In jawed vertebrates, perichondral cells and osteoblasts maintained high levels of Col1a1 and Col1a2 while the Col2a1 osteoblastic expression was dramatically reduced in most (but not all) lineages. The presence of bone in placoderms and tetrapods supports the idea that the calcified fibrous perichondrium observed in some chondrichthyan species either represents bone evolutionary remnants (Hypothesis 1) or a secondary gain of calcification (Hypothesis 2). Osteocytes have been omitted for the sake of simplicity. See text for details.

Mentions: We detected X.t. Col2a1 transcripts in osteoblasts of the vertebrae, albeit they displayed a weaker in situ hybridization signal than hypertrophic chondrocytes present on the same section (Figures 5I,L), which is consistent with expression results obtained with primary cultures of X.t. osteoblasts (Bertin et al., 2015). While Col2a1 is traditionally considered to be a chondrocyte-specific marker (Kobayashi and Kronenberg, 2005; Hartmann, 2009), its robust osteoblastic expression has been reported in embryos from several species of actinopterygian fishes (Benjamin and Ralphs, 1991; Albertson et al., 2010; Eames et al., 2012). The moderate Col2a1 expression levels described in the clawed frog (this study), chick (Abzhanov et al., 2007) and mouse (Hilton et al., 2007) therefore support the idea that the osteogenic transcription of Col2a1 was significantly reduced in the tetrapod lineage, and almost completely abolished in mammals (Figure 6).


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 bone formation and perichondral calcification in jawed vertebrates. Bone/perichondrium histology and gene expression patterns were mapped onto a simplified vertebrate phylogenetic tree to deduce ancestral states and polarize evolutionary change. We propose that the ancestral Clade A fibrillar collagen gene (i.e., before the duplications that produced the distinct member of this family) was expressed in the non-calcified perichondrium. This expression pattern was inherited by the unique cyclostome fibrillar collagen gene which is more closely related to the Col2a1 subgroup. In jawed vertebrates, perichondral cells and osteoblasts maintained high levels of Col1a1 and Col1a2 while the Col2a1 osteoblastic expression was dramatically reduced in most (but not all) lineages. The presence of bone in placoderms and tetrapods supports the idea that the calcified fibrous perichondrium observed in some chondrichthyan species either represents bone evolutionary remnants (Hypothesis 1) or a secondary gain of calcification (Hypothesis 2). Osteocytes 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 6: An evolutionary scenario for bone formation and perichondral calcification in jawed vertebrates. Bone/perichondrium histology and gene expression patterns were mapped onto a simplified vertebrate phylogenetic tree to deduce ancestral states and polarize evolutionary change. We propose that the ancestral Clade A fibrillar collagen gene (i.e., before the duplications that produced the distinct member of this family) was expressed in the non-calcified perichondrium. This expression pattern was inherited by the unique cyclostome fibrillar collagen gene which is more closely related to the Col2a1 subgroup. In jawed vertebrates, perichondral cells and osteoblasts maintained high levels of Col1a1 and Col1a2 while the Col2a1 osteoblastic expression was dramatically reduced in most (but not all) lineages. The presence of bone in placoderms and tetrapods supports the idea that the calcified fibrous perichondrium observed in some chondrichthyan species either represents bone evolutionary remnants (Hypothesis 1) or a secondary gain of calcification (Hypothesis 2). Osteocytes have been omitted for the sake of simplicity. See text for details.
Mentions: We detected X.t. Col2a1 transcripts in osteoblasts of the vertebrae, albeit they displayed a weaker in situ hybridization signal than hypertrophic chondrocytes present on the same section (Figures 5I,L), which is consistent with expression results obtained with primary cultures of X.t. osteoblasts (Bertin et al., 2015). While Col2a1 is traditionally considered to be a chondrocyte-specific marker (Kobayashi and Kronenberg, 2005; Hartmann, 2009), its robust osteoblastic expression has been reported in embryos from several species of actinopterygian fishes (Benjamin and Ralphs, 1991; Albertson et al., 2010; Eames et al., 2012). The moderate Col2a1 expression levels described in the clawed frog (this study), chick (Abzhanov et al., 2007) and mouse (Hilton et al., 2007) therefore support the idea that the osteogenic transcription of Col2a1 was significantly reduced in the tetrapod lineage, and almost completely abolished in mammals (Figure 6).

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