Identification of a Parathyroid Hormone in the Fish <i>Fugu rubripes</i>

Danks, Janine A.; Ho, Patricia M W; Notini, Amanda J.; Katsis, Frosa; Hoffmann, Peter; Kemp, Bruce E.; Martın, Thomas; Zajac, Jeffrey D

doi:10.1359/jbmr.2003.18.7.1326

Cited by 63 publications

(38 citation statements)

References 22 publications

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“…4B). These results are in keeping with another recent study that similarly identified two PTH genes in zebrafish and fugu that are shown to be fully active (13,14). We have further analyzed the tissues expression of the zebrafish PTH genes, and we find that these genes are expressed by the gills (Fig.…”

Section: Gcm-2 Is Required For the Elaboration Of The Internal Gill Bsupporting

confidence: 91%

“…Thus, Gcm-2 likely serves a conserved function across the gnathostomes with respect to the elaboration of pharyngeal pouches into internal gill buds and parathyroid. It is known that calcium uptake is a particularly important function of the gills (15), and we also show that fish do possess PTH genes, which have been shown by others to generate fully active peptides (13,14), and that this gene is expressed in the gills. Thus, both the tetrapod parathyroid gland and the gills of fish contribute to the regulation of extracellular calcium levels.…”

Section: Discussionsupporting

confidence: 77%

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The origin of the parathyroid gland

Okabe

Graham

2004

Proc. Natl. Acad. Sci. U.S.A.

149

128

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It has long been held that the parathyroid glands and parathyroid hormone evolved with the emergence of the tetrapods, reflecting a need for new controls on calcium homeostasis in terrestrial, rather than aquatic, environments. Developmentally, the parathyroid gland is derived from the pharyngeal pouch endoderm, and studies in mice have shown that its formation is under the control of a key regulatory gene, Gcm-2. We have used a phylogenetic analysis of Gcm-2 to probe the evolutionary origins of the parathyroid gland. We show that in chicks, as in mice, Gcm-2 is expressed in the pharyngeal pouches and the forming parathyroid gland. We find that Gcm-2 is present not only in tetrapods but also in teleosts and chondrichthyans, and that in these species, Gcm-2 is expressed within the pharyngeal pouches and internal gill buds that derive from them in zebrafish (Danio rerio), a teleost, and dogfish (Scyliorhinus canicula), a chondrichthyan. We further demonstrate that Gcm-2 is required for the formation of the internal gill buds in zebrafish. We also have identified parathyroid hormone 1͞2-encoding genes in fish and show that these genes are expressed by the gills. We further show that the gills express the calcium-sensing receptor, which is used in tetrapods to monitor serum calcium levels. These results indicate that the tetrapod parathyroid gland and the gills of fish are evolutionarily related structures, and that the parathyroid likely came into being as a result of the transformation of the gills during tetrapod evolution.pharyngeal endoderm ͉ vertebrate evolution ͉ Gcm-2 ͉ gills I n tetrapods, the parathyroid glands play a pivotal role in regulating extracellular calcium homeostasis, which is important to many physiological processes such as muscle contraction, blood coagulation, and synaptic activity. These glands detect changes in the levels of calcium in blood by means of the calcium-sensing receptor (CasR), which in turn modulates the secretion of parathyroid hormone (PTH), which acts to release calcium from internal stores such as bone and modulates renal ion transport (1). Developmentally, the parathyroid glands arise from the endodermal pharyngeal pouches; in humans and chickens, from the third and fourth pouches, and in mice, from the third pouch only. Importantly, studies in mice have demonstrated that the transcription factor encoded by Gcm-2 is a key regulator of parathyroid gland development. The expression of this gene is restricted to the parathyroid glands, and if this gene is mutated, the parathyroid glands fail to form (2-4).Fish, however, have been believed to lack parathyroid glands and PTH, and unlike tetrapods, the majority of calcium uptake in fish is from external sources. These differences are believed to reflect the fact that with the evolution of the tetrapods and the shift from an aquatic to a terrestrial environment, new controls for regulating calcium homeostasis had to be put in place, and thus the evolution of the parathyroid glands and PTH was a key event in facilitating this tra...

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Section: Gcm-2 Is Required For the Elaboration Of The Internal Gill Bsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 77%

The origin of the parathyroid gland

Okabe

Graham

2004

Proc. Natl. Acad. Sci. U.S.A.

149

128

View full text Add to dashboard Cite

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“…9% NaCl) or either Fugu PTHrP (1-34; Danks et al 2003) or the recombinant full length sea bream PTHrP (sbPTHrP 1-125). For both the forms, the dose was 10 ng/g BW.…”

Section: Physiologymentioning

confidence: 99%

“…The array of endocrines involved in the calcemic control in fish includes PTH-related protein (PTHrP), a key in calcium balance in fish ); more recently, PTH genes have been demonstrated in zebrafish (Danks et al 2003) and pufferfish (Gensure et al 2004), but our understanding of the role of the peptides coded by these genes in the calcium physiology of fishes awaits further study . A relationship between PTHrP and calcitriol in calcemic control was recently established for sea bream ; it was shown that a decrease of plasma calcitriol levels, due to dietary vitamin D 3 deficiency, result in an adjustment of (hypercalcemic) PTHrP activities in gills and pituitary cells.…”

Section: Introductionmentioning

confidence: 99%

CYP27A1 expression in gilthead sea bream (Sparus auratus, L.): effects of calcitriol and parathyroid hormone-related protein

Bevelander

Pinto

Canário

et al. 2007

Journal of Endocrinology

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Little is known about vitamin D metabolism in fishes. Several reports have shown hydroxylase activities in various organs to produce vitamin D metabolites, but the enzymes involved have not been isolated or characterized. We isolated and characterized a renal mitochondrial hydroxylase, CYP27A1, that governs vitamin D metabolism in gilthead sea bream, Sparus auratus. The enzyme is highly expressed in kidney and to a far lesser extent in liver. When treated with 25-hydroxy vitamin D or calcitriol, the kidney responded differentially and time dependently with CYP27A1 mRNA expression levels. This response substantiates a role for CYP27A1 in fish vitamin D metabolism. This notion is strengthened by upregulation of CYP27A1 in sea bream treated with parathyroid hormone-related protein (PTHrP), and suggests an original role for PTHrP in calcitriol-regulated processes n fish similar to the role of PTH in mammalian vitamin D-dependent processes.

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“…However, surprisingly, Pth was identified in a ray-finned fish, fugu, (Fugu rubripes). (3) Subsequently, a second fugu Pth gene and two zebrafish (Danio rerio) Pth genes (4) have been identified.…”

Section: Introductionmentioning

confidence: 99%

Parathyroid hormone gene family in a cartilaginous fish, the elephant shark (Callorhinchus milii)

Liu¹,

Ibrahim²,

Tay³

et al. 2010

Journal of Bone and Mineral Research

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The development of bone was a major step in the evolution of vertebrates. A bony skeleton provided structural support and a calcium reservoir essential for the movement from an aquatic to a terrestrial environment. Cartilaginous fishes are the oldest living group of jawed vertebrates. In this study we have identified three members of the parathyroid hormone (Pth) gene family in a cartilaginous fish, the elephant shark (Callorhinchus milii). The three genes include two Pth genes, designated as Pth1 and Pth2, and a Pthrp gene. Phylogenetic analysis suggested that elephant shark Pth2 is an ancient gene whose orthologue is lost in bony vertebrates. The Pth1 and Pth2 genes have the same structure as the Pth gene in bony vertebrates, whereas the structure of the Pthrp gene is more complex in tetrapods compared with elephant shark. The three elephant shark genes showed distinct patterns of expression, with Pth2 being expressed only in the brain and spleen. This contrasts with localization of the corresponding proteins, which showed considerable overlap in their distribution. There were conserved sites of localization for Pthrp between elephant shark and mammals, including tissues such as kidney, skin, skeletal and cardiac muscle, pancreas, and cartilage. The elephant shark Pth1(1-34) and Pthrp(1-34) peptides were able to stimulate cAMP accumulation in mammalian UMR106.01 cells. However, Pth2(1-34) peptide did not show such PTH-like biologic activity. The presence of Pth and Pthrp genes in the elephant shark indicates that these genes played fundamental roles before their recruitment to bone development in bony jawed vertebrates. ß

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Identification of a Parathyroid Hormone in the Fish Fugu rubripes

Cited by 63 publications

References 22 publications

The origin of the parathyroid gland

The origin of the parathyroid gland

CYP27A1 expression in gilthead sea bream (Sparus auratus, L.): effects of calcitriol and parathyroid hormone-related protein

Parathyroid hormone gene family in a cartilaginous fish, the elephant shark (Callorhinchus milii)

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