Gene Duplication and the Evolution of Vertebrate Skeletal Mineralization

Kawasaki, Kazuhiko; Buchanan, Anne V.; Weiss, Kenneth M.

doi:10.1159/000102678

Cited by 65 publications

(84 citation statements)

References 237 publications

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“…As SPARCL1 has been lost in amphibians [20,21], we focused on the D. rerio and M. musculus orthologues. In zebrafish, restricted SPARCL1 expression is first detected in 24 hpf stage embryos in the lens, the brain and at a lower rspb.royalsocietypublishing.org Proc R Soc B 280: 20122963 level in the notochord (figure 2s).…”

Section: (B) Synteny Conservation Analysismentioning

confidence: 99%

A dynamic history of gene duplications and losses characterizes the evolution of the SPARC family in eumetazoans

et al. 2013

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The vertebrates share the ability to produce a skeleton made of mineralized extracellular matrix. However, our understanding of the molecular changes that accompanied their emergence remains scarce. Here, we describe the evolutionary history of the SPARC (secreted protein acidic and rich in cysteine) family, because its vertebrate orthologues are expressed in cartilage, bones and teeth where they have been proposed to bind calcium and act as extracellular collagen chaperones, and because further duplications of specific SPARC members produced the small calcium-binding phosphoproteins (SCPP) family that is crucial for skeletal mineralization to occur. Both phylogeny and synteny conservation analyses reveal that, in the eumetazoan ancestor, a unique ancestral gene duplicated to give rise to SPARC and SPARCB described here for the first time. Independent losses have eliminated one of the two paralogues in cnidarians, protostomes and tetrapods. Hence, only non-tetrapod deuterostomes have conserved both genes. Remarkably, SPARC and SPARCB paralogues are still linked in the amphioxus genome. To shed light on the evolution of the SPARC family members in chordates, we performed a comprehensive analysis of their embryonic expression patterns in amphioxus, tunicates, teleosts, amphibians and mammals. Our results show that in the chordate lineage SPARC and SPARCB family members were recurrently recruited in a variety of unrelated tissues expressing collagen genes. We propose that one of the earliest steps of skeletal evolution involved the co-expression of SPARC paralogues with collagenous proteins.

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Section: (B) Synteny Conservation Analysismentioning

confidence: 99%

A dynamic history of gene duplications and losses characterizes the evolution of the SPARC family in eumetazoans

et al. 2013

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“…This consists of osteopontin (OPN), bone sialoprotein (BSP (IBSP)), dentin matrix protein 1 (DMP1), dentin sialophosphoprotein (DSPP) and matrix extracellular phosphoglycoprotein (MEPE). It is likely that this protein family arose from the secretory calcium-binding phosphoprotein family by gene duplication due to their apparent common evolutionary heritage, as is elegantly reviewed by Kawasaki & Weiss (2006), Kawasaki et al (2007), Kawasaki (2011) and Rowe (2012). It is therefore somewhat surprising that the SIBLING proteins have little intrinsic sequence homology and yet they share the following characteristics: i) all are located to a 375 kb region on the human chromosome 4q21 and mouse chromosome 5q, ii) display similar exon structures, iii) display an Arg-Gly-Asp (RGD) motif that mediates cell attachment/signalling and iv) are principally expressed in bone and dentin and are secreted into the ECM during osteoid formation and subsequent mineralisation.…”

Section: Introductionmentioning

confidence: 99%

The importance of the SIBLING family of proteins on skeletal mineralisation and bone remodelling

Staines¹,

MacRae²,

Farquharson³

2012

Journal of Endocrinology

187

109

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The small integrin-binding ligand N-linked glycoprotein (SIBLING) family consists of osteopontin, bone sialoprotein, dentin matrix protein 1, dentin sialophosphoprotein and matrix extracellular phosphoglycoprotein. These proteins share many structural characteristics and are primarily located in bone and dentin. Accumulating evidence has implicated the SIBLING proteins in matrix mineralisation. Therefore, in this review, we discuss the individual role that each of the SIBLING proteins has in this highly orchestrated process. In particular, we emphasise how the nature and extent of their proteolytic processing and post-translational modification affect their functional role. Finally, we describe the likely roles of the SIBLING proteins in clinical disorders of hypophosphataemia and their potential therapeutic use.

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“…In accordance with this interpretation, he regarded the capping layer of heterostracans as enamel (Moss, 1968a). However, true enamel is genetically and developmentally distinct from 'enameloid' present in living teleosts or chondricthyans (Poole, 1967;Sasagawa, 2002;Kawasaki et al, 2004;Kawasaki and Weiss, 2006;Kawasaki et al, 2007) and is restricted to osteichthyans (Donoghue, 2001).…”

Section: Historical Reviewmentioning

confidence: 99%

Histology of the heterostracan dermal skeleton: Insight into the origin of the vertebrate mineralised skeleton

Keating

Marquart

Donoghue

2015

Journal of Morphology

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Living vertebrates are divided into those that possess a fully formed and fully mineralised skeleton (gnathostomes) versus those that possess only unmineralised cartilaginous rudiments (cyclostomes). As such, extinct phylogenetic intermediates of these living lineages afford unique insights into the evolutionary assembly of the vertebrate mineralised skeleton and its canonical tissue types. Extinct jawless and jawed fishes assigned to the gnathostome stem evidence the piecemeal assembly of skeletal systems, revealing that the dermal skeleton is the earliest manifestation of a homologous mineralised skeleton. Yet the nature of the primitive dermal skeleton, itself, is poorly understood. This is principally because previous histological studies of early vertebrates lacked a phylogenetic framework required to derive evolutionary hypotheses. Nowhere is this more apparent than within Heterostraci, a diverse clade of primitive jawless vertebrates. To this end, we surveyed the dermal skeletal histology of heterostracans, inferred the plesiomorphic heterostracan skeleton and, through histological comparison to other skeletonising vertebrate clades, deduced the ancestral nature of the vertebrate dermal skeleton. Heterostracans primitively possess a fourlayered skeleton, comprising a superficial layer of odontodes composed of dentine and enameloid; a compact layer of acellular parallel-fibred bone containing a network of vascular canals that supply the pulp canals (L1); a trabecular layer consisting of intersecting radial walls composed of acellular parallel-fibred bone, showing osteon-like development (L2); and a basal layer of isopedin (L3). A three layered skeleton, equivalent to the superficial layer L2 and L3 and composed of enameloid, dentine and acellular bone, is possessed by the ancestor of heterostracans 1 jawed vertebrates. We conclude that an osteogenic component is plesiomorphic with respect to the vertebrate dermal skeleton. Consequently, we interpret the dermal skeleton of denticles in chondrichthyans and jawless thelodonts as independently and secondarily simplified. J.

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Gene Duplication and the Evolution of Vertebrate Skeletal Mineralization

Cited by 65 publications

References 237 publications

A dynamic history of gene duplications and losses characterizes the evolution of the SPARC family in eumetazoans

A dynamic history of gene duplications and losses characterizes the evolution of the SPARC family in eumetazoans

The importance of the SIBLING family of proteins on skeletal mineralisation and bone remodelling

Histology of the heterostracan dermal skeleton: Insight into the origin of the vertebrate mineralised skeleton

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