Limits...
On the evolutionary relationship between chondrocytes and osteoblasts.

Gómez-Picos P, Eames BF - Front Genet (2015)

Bottom Line: Emphasizing an embryological and evolutionary transcriptomic view, we hypothesize that the Runx2 GRN underlying bone formation was co-opted from mature cartilage.We discuss how modern molecular genetic experiments, such as comparative transcriptomics, can test this hypothesis directly, meanwhile permitting levels of constraint and adaptation to be evaluated quantitatively.Therefore, comparative transcriptomics may revolutionize understanding of not only the clade-specific evolution of skeletal cells, but also the generation of evolutionary novelties, providing a modern paradigm for the evolutionary process.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Cell Biology, University of Saskatchewan, Saskatoon, SK Canada.

ABSTRACT
Vertebrates are the only animals that produce bone, but the molecular genetic basis for this evolutionary novelty remains obscure. Here, we synthesize information from traditional evolutionary and modern molecular genetic studies in order to generate a working hypothesis on the evolution of the gene regulatory network (GRN) underlying bone formation. Since transcription factors are often core components of GRNs (i.e., kernels), we focus our analyses on Sox9 and Runx2. Our argument centers on three skeletal tissues that comprise the majority of the vertebrate skeleton: immature cartilage, mature cartilage, and bone. Immature cartilage is produced during early stages of cartilage differentiation and can persist into adulthood, whereas mature cartilage undergoes additional stages of differentiation, including hypertrophy and mineralization. Functionally, histologically, and embryologically, these three skeletal tissues are very similar, yet unique, suggesting that one might have evolved from another. Traditional studies of the fossil record, comparative anatomy and embryology demonstrate clearly that immature cartilage evolved before mature cartilage or bone. Modern molecular approaches show that the GRNs regulating differentiation of these three skeletal cell fates are similar, yet unique, just like the functional and histological features of the tissues themselves. Intriguingly, the Sox9 GRN driving cartilage formation appears to be dominant to the Runx2 GRN of bone. Emphasizing an embryological and evolutionary transcriptomic view, we hypothesize that the Runx2 GRN underlying bone formation was co-opted from mature cartilage. We discuss how modern molecular genetic experiments, such as comparative transcriptomics, can test this hypothesis directly, meanwhile permitting levels of constraint and adaptation to be evaluated quantitatively. Therefore, comparative transcriptomics may revolutionize understanding of not only the clade-specific evolution of skeletal cells, but also the generation of evolutionary novelties, providing a modern paradigm for the evolutionary process.

No MeSH data available.


Related in: MedlinePlus

Similarities and differences among immature cartilage, mature cartilage, and bone suggest that these three skeletal tissues share an evolutionary history.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4585068&req=5

Figure 1: Similarities and differences among immature cartilage, mature cartilage, and bone suggest that these three skeletal tissues share an evolutionary history.

Mentions: An introductory look at the similarities and differences among cartilage and bone suggests that the underlying GRNs may be related. Cartilage and bone are specialized connective tissues that provide form and structural support to the body, protect vital organs, and play a crucial role in locomotion through muscle attachments (Gray and Williams, 1989). Despite these similarities, they also have distinct functions (Figure 1). Cartilage typically offers a flexible structure to support soft tissues and also to serve as a load-bearing surface between bones. On the other hand, bone is a hard, rigid structure that protects vital organs and acts as a storage site for minerals, such as calcium and phosphorus (Smith and Hall, 1990; Volkmann and Baluska, 2006). Also unlike cartilage, which has almost no capacity for regeneration, bone is a highly dynamic structure that undergoes constant remodeling, preserving bone strength and regulating calcium homeostasis (Datta et al., 2008). Perhaps related to regenerative capacity, these tissues differ in vascularity. Bone is highly vascularized, but cartilage typically is avascular. However, important exceptions to cartilage vascularization occur. Mature cartilage in tetrapods often is invaded by vasculature as it degrades, creating the marrow cavity (Johnson, 1980; Roach, 1997; Stricker et al., 2002; Ortega et al., 2004; Moriishi et al., 2005), and even immature cartilage is highly vascularized near articulating surfaces in some avian and mammalian species (Ytrehus et al., 2004; Blumer et al., 2005). When cartilage extracellular matrix (ECM) undergoes mineralization, its functions change. In some vertebrates, such as sharks, mineralized cartilage can serve as the major rigid structural support for the body, meanwhile providing a mineral reservoir (Daniel, 1934; Kemp and Westrin, 1979; Eames et al., 2007). In most extant vertebrates, however, mineralized cartilage mainly serves as a scaffold during endochondral ossification, outlined below.


On the evolutionary relationship between chondrocytes and osteoblasts.

Gómez-Picos P, Eames BF - Front Genet (2015)

Similarities and differences among immature cartilage, mature cartilage, and bone suggest that these three skeletal tissues share an evolutionary history.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4585068&req=5

Figure 1: Similarities and differences among immature cartilage, mature cartilage, and bone suggest that these three skeletal tissues share an evolutionary history.
Mentions: An introductory look at the similarities and differences among cartilage and bone suggests that the underlying GRNs may be related. Cartilage and bone are specialized connective tissues that provide form and structural support to the body, protect vital organs, and play a crucial role in locomotion through muscle attachments (Gray and Williams, 1989). Despite these similarities, they also have distinct functions (Figure 1). Cartilage typically offers a flexible structure to support soft tissues and also to serve as a load-bearing surface between bones. On the other hand, bone is a hard, rigid structure that protects vital organs and acts as a storage site for minerals, such as calcium and phosphorus (Smith and Hall, 1990; Volkmann and Baluska, 2006). Also unlike cartilage, which has almost no capacity for regeneration, bone is a highly dynamic structure that undergoes constant remodeling, preserving bone strength and regulating calcium homeostasis (Datta et al., 2008). Perhaps related to regenerative capacity, these tissues differ in vascularity. Bone is highly vascularized, but cartilage typically is avascular. However, important exceptions to cartilage vascularization occur. Mature cartilage in tetrapods often is invaded by vasculature as it degrades, creating the marrow cavity (Johnson, 1980; Roach, 1997; Stricker et al., 2002; Ortega et al., 2004; Moriishi et al., 2005), and even immature cartilage is highly vascularized near articulating surfaces in some avian and mammalian species (Ytrehus et al., 2004; Blumer et al., 2005). When cartilage extracellular matrix (ECM) undergoes mineralization, its functions change. In some vertebrates, such as sharks, mineralized cartilage can serve as the major rigid structural support for the body, meanwhile providing a mineral reservoir (Daniel, 1934; Kemp and Westrin, 1979; Eames et al., 2007). In most extant vertebrates, however, mineralized cartilage mainly serves as a scaffold during endochondral ossification, outlined below.

Bottom Line: Emphasizing an embryological and evolutionary transcriptomic view, we hypothesize that the Runx2 GRN underlying bone formation was co-opted from mature cartilage.We discuss how modern molecular genetic experiments, such as comparative transcriptomics, can test this hypothesis directly, meanwhile permitting levels of constraint and adaptation to be evaluated quantitatively.Therefore, comparative transcriptomics may revolutionize understanding of not only the clade-specific evolution of skeletal cells, but also the generation of evolutionary novelties, providing a modern paradigm for the evolutionary process.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Cell Biology, University of Saskatchewan, Saskatoon, SK Canada.

ABSTRACT
Vertebrates are the only animals that produce bone, but the molecular genetic basis for this evolutionary novelty remains obscure. Here, we synthesize information from traditional evolutionary and modern molecular genetic studies in order to generate a working hypothesis on the evolution of the gene regulatory network (GRN) underlying bone formation. Since transcription factors are often core components of GRNs (i.e., kernels), we focus our analyses on Sox9 and Runx2. Our argument centers on three skeletal tissues that comprise the majority of the vertebrate skeleton: immature cartilage, mature cartilage, and bone. Immature cartilage is produced during early stages of cartilage differentiation and can persist into adulthood, whereas mature cartilage undergoes additional stages of differentiation, including hypertrophy and mineralization. Functionally, histologically, and embryologically, these three skeletal tissues are very similar, yet unique, suggesting that one might have evolved from another. Traditional studies of the fossil record, comparative anatomy and embryology demonstrate clearly that immature cartilage evolved before mature cartilage or bone. Modern molecular approaches show that the GRNs regulating differentiation of these three skeletal cell fates are similar, yet unique, just like the functional and histological features of the tissues themselves. Intriguingly, the Sox9 GRN driving cartilage formation appears to be dominant to the Runx2 GRN of bone. Emphasizing an embryological and evolutionary transcriptomic view, we hypothesize that the Runx2 GRN underlying bone formation was co-opted from mature cartilage. We discuss how modern molecular genetic experiments, such as comparative transcriptomics, can test this hypothesis directly, meanwhile permitting levels of constraint and adaptation to be evaluated quantitatively. Therefore, comparative transcriptomics may revolutionize understanding of not only the clade-specific evolution of skeletal cells, but also the generation of evolutionary novelties, providing a modern paradigm for the evolutionary process.

No MeSH data available.


Related in: MedlinePlus