Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans

Kawasaki, Kazuhiko; Keating, Joseph N.; Nakatomi, Mitsushiro; Welten, Monique; Mikami, Masato; Sasagawa, Ichiro; Puttick, Mark N.; Donoghue, Philip C. J.; Ishiyama, Mikio

doi:10.1016/j.isci.2020.102023

Cited by 30 publications

(71 citation statements)

References 55 publications

(50 reference statements)

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“…3 , Supplementary Data 1 and Supplementary Note 7 ). Similar to gar 7 , 50 , 51 , the bowfin possesses ganoin-forming SCPP genes enamelin ( enam ), ameloblastin ( ambn ) and scpp5 (Fig. 3 ).…”

Section: Resultsmentioning

confidence: 99%

The bowfin genome illuminates the developmental evolution of ray-finned fishes

et al. 2021

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The bowfin (Amia calva) is a ray-finned fish that possesses a unique suite of ancestral and derived phenotypes, which are key to understanding vertebrate evolution. The phylogenetic position of bowfin as a representative of neopterygian fishes, its archetypical body plan and its unduplicated and slowly evolving genome make bowfin a central species for the genomic exploration of ray-finned fishes. Here we present a chromosome-level genome assembly for bowfin that enables gene-order analyses, settling long-debated neopterygian phylogenetic relationships. We examine chromatin accessibility and gene expression through bowfin development to investigate the evolution of immune, scale, respiratory and fin skeletal systems and identify hundreds of gene-regulatory loci conserved across vertebrates. These resources connect developmental evolution among bony fishes, further highlighting the bowfin’s importance for illuminating vertebrate biology and diversity in the genomic era.

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Section: Resultsmentioning

confidence: 99%

The bowfin genome illuminates the developmental evolution of ray-finned fishes

et al. 2021

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“…We detected robust enam and weak scpp5 expression, but not ambn in SFCs (Fig 2C). These transcripts are not typically found in osteoblasts, including the cells that generate attachment bone underlying the tooth-like scales of the gar (Kawasaki et al, 2021).…”

Section: A Heterogenous Population Of Epidermal and Dermal Cells Contributes To Scale Plate Formationmentioning

confidence: 94%

“…Transcripts of sparc (Osteonectin), most often associated with mineralized matrix formation, were expressed broadly in skin (Fig 2C), raising the possibility of additional roles beyond assembly of calcified matrix (Rosset and Bradshaw, 2016). Transcripts considered diagnostic for mammalian odontoblasts, Dmp1 (Dentin Matrix Protein 1) and Dspp (Dentinogenesis and Dentin Sialophosphoprotein), are not present in Actinopterygian genomes (MacDougall et al, 1996;Jia et al, 2015;Kawasaki et al, 2021).…”

Section: A Heterogenous Population Of Epidermal and Dermal Cells Contributes To Scale Plate Formationmentioning

confidence: 99%

“…In all overtly tooth-like protuberances of vertebrates, calcified matrices are deposited by two cooperating cell types, mesenchymal cells of dermal or neural crest origin that form dentin, bone or both, and overlying epithelial cells of epidermal origin that produce hypermineralized matrices like enamel (Sire, 1990;Sire and Huysseune, 2003). Hypothesizing that epidermis of zebrafish retains vestiges of this ancient function, we predicted that a subset of epidermal cells should express transcripts encoding enamel matrix proteins (EMPs) a conserved family of non-collagen matrix proteins that underly hypermineralization (Kawasaki, 2011;Kawasaki et al, 2021).…”

Section: A Heterogenous Population Of Epidermal and Dermal Cells Contributes To Scale Plate Formationmentioning

confidence: 99%

“…Actinopterygian fish, including zebrafish, are known already to synthesize a hypermineralized enameloid that is similar in hardness and matrix composition to the true enamel of tetrapod teeth. This material is associated with expression of conserved EMP genes, ambn (encoding Ameloblastin), enam (Enamelin) and scpp5 (Secretory calcium-binding phosphoprotein 5), which facilitate the ordered formation of calcium hydroxyapatite crystals (Kawasaki, 2011;Braasch et al, 2016;Kawasaki et al, 2021). We therefore analyzed the distribution of these transcripts across the whole skin, predicting such cells might be found among basal epidermal cells, as the zebrafish scale plate forms at the interface between these cells and underlying dermal cells (Fig 2A,B; Fig 2 -S1) (Sire and Akimenko, 2004).…”

Section: A Heterogenous Population Of Epidermal and Dermal Cells Contributes To Scale Plate Formationmentioning

confidence: 99%

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Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin

Aman

Saunders

Carr³

et al. 2021

Preprint

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Regulation of neural crest derived pigment cells and dermal cells that form skin appendages is broadly similar across vertebrate taxa. In zebrafish, organized pigment stripes and an array of calcified scales form simultaneously in the skin during post-embryonic development. Understanding mechanisms that regulate stripe patterning and dermal morphogenesis may lead to discovery of fundamental mechanisms that govern development of animal form. To learn about cell types and potential signaling interactions that govern skin patterning and morphogenesis we generated and analyzed single cell transcriptomes of skin with genetic or induced defects in pigmentation and squamation. These data reveal a previously undescribed population of ameloblast-like epidermal cells, suggest hormonal control of epithelial-mesenchymal signaling, clarify the signaling network that governs scale papillae development, and identify the hypodermis as a crucial pigment cell support environment. These analyses provide new insights into the development of skin and pigmentation and highlight the utility of zebrafish for uncovering essential features of post-embryonic development in vertebrates.

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Enam expression is regulated by Msx2

Ruspita

Das

Miyoshi

et al. 2023

Developmental Dynamics

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BackgroundThe precise formation of mineralized dental tissues such as enamel and/or dentin require tight transcriptional control of the secretion of matrix proteins. Here, we have investigated the transcriptional regulation of the second most prominent enamel matrix protein, enamelin, and its regulation through the major odontogenic transcription factor, MSX2.ResultsUsing in vitro and in vivo approaches, we identified that (a) Enam expression is reduced in the Msx2 mouse mutant pre‐secretory and secretory ameloblasts, (b) Enam is an early response gene whose expression is under the control of Msx2, (c) Msx2 binds to Enam promoter in vitro, suggesting that enam is a direct target for Msx2 and that (d) Msx2 alone represses Enam gene expression.ConclusionsCollectively, these results illustrate that Enam gene expression is controlled by Msx2 in a spatio‐temporal manner. They also suggest that Msx2 may interact with other transcription factors to control spatial and temporal expression of Enam and hence amelogenesis and enamel biomineralization.

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Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans

Cited by 30 publications

References 55 publications

The bowfin genome illuminates the developmental evolution of ray-finned fishes

The bowfin genome illuminates the developmental evolution of ray-finned fishes

Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin

Enam expression is regulated by Msx2

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