Divergent Expression of SPARC, SPARC-L, and SCPP Genes During Jawed Vertebrate Cartilage Mineralization.

Adrian Romero,Nicolas Leurs,Sylvain Marcellini,Mélanie Debiais-Thibaud,David Muñoz

doi:10.3389/fgene.2021.788346

Abstract

While cartilage is an ancient tissue found both in protostomes and deuterostomes, its mineralization evolved more recently, within the vertebrate lineage. SPARC, SPARC-L, and the SCPP members (Secretory Calcium-binding PhosphoProtein genes which evolved from SPARC-L) are major players of dentine and bone mineralization, but their involvement in the emergence of the vertebrate mineralized cartilage remains unclear. We performed in situ hybridization on mineralizing cartilaginous skeletal elements of the frog Xenopus tropicalis (Xt) and the shark Scyliorhinus canicula (Sc) to examine the expression of SPARC (present in both species), SPARC-L (present in Sc only) and the SCPP members (present in Xt only). We show that while mineralizing cartilage expresses SPARC (but not SPARC-L) in Sc, it expresses the SCPP genes (but not SPARC) in Xt, and propose two possible evolutionary scenarios to explain these opposite expression patterns. In spite of these genetic divergences, our data draw the attention on an overlooked and evolutionarily conserved peripheral cartilage subdomain expressing SPARC or the SCPP genes and exhibiting a high propensity to mineralize.

Highlights

The evolution of a mineralized skeleton occurred in early vertebrates, in a variety of tissues including superficial dermal scales and teeth, together with internal cartilages, and perichondral bones (Ørvig, 1951; Donoghue and Sansom, 2002)
SCPP genes become activated at late stages of hypertrophy, when the cartilage matrix becomes replaced by bone marrow at the mammalian diaphysis (Chen et al, 1991; Fujikawa et al, 2015)
In Xenopus tropicalis (Xt), Dentin matrix protein 1 (DMP1) is exclusively expressed at the diaphysis (Figure 3F), and SCPPA2 exhibits a much stronger expression at the diaphysis than the epiphysis region (Figures 3G,G9)

Summary

Introduction

The evolution of a mineralized skeleton occurred in early vertebrates, in a variety of tissues including superficial dermal scales and teeth, together with internal cartilages, and perichondral bones (Ørvig, 1951; Donoghue and Sansom, 2002). Several cell types are associated with biomineralization, and the most studied cell model in mammalian organisms is the osteoblast active in the endochondral ossification process (Long and Ornitz, 2013) These osteoblasts are derived from periosteal tissues or from hypertrophic transdifferentiated chondrocytes (Tsang et al, 2015). Evolution of Cartilage Mineralization et al, 2015; Paul et al, 2016; Pears et al, 2020; Berio et al, 2021) Even though both perichondral bones and cartilaginous tissues displayed mineralization in the earliest forms of mineralized internal skeletons (Ørvig, 1951; Min and Janvier, 1998; Donoghue et al, 2006; Johanson et al, 2010, 2012; Pears et al, 2020), mineralizing cartilages have been understudied from a genetic and evolutionary perspective in extant vertebrates. A better understanding of the genetic underpinning of the mineralizing chondrocytes is necessary to understand the early steps of the evolution of endoskeletal mineralization in vertebrates

Methods

Results

Conclusion