Expression and Localization of Prohormone Convertase PC1 in the Calcitonin-producing Cells of the Bullfrog Ultimobranchial Gland

Yaoi, Yuichi; Suzuki, Masakazu; Tomura, Hideaki; Kurabuchi, Shingo; Sasayama, Yuichi; Tanaka, Shigeyasu

doi:10.1177/002215540305101106

Cited by 5 publications

(6 citation statements)

References 25 publications

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“…These findings suggest that the endostyle is an ancestral or precursor organ of the vertebrate thyroid gland 41 . Furthermore, the expression of PC2 and some peptides including calcitonin (CT), somatostatin, and ghrelin was observed in the thyroid gland of mammals and the ultimobranchial gland of non-mammalian vertebrates (the counterpart for mammalian thyroid glands) 43,44 . A main function of peptidergic system in the thyroid gland and ultimobranchial gland is calcium homeostasis that is controlled by CT 45 .…”

Section: Distribution Of Peptidergic Cells In the Endostylementioning

confidence: 99%

The ventral peptidergic system of the adult ascidian Ciona robusta (Ciona intestinalis Type A) insights from a transgenic animal model

Osugi

Sasakura

Satake

2020

Sci Rep

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Ascidians are the sister group of vertebrates and occupy a critical position in explorations of the evolution of the endocrine and nervous systems of chordates. Here, we describe the complete ventral peptidergic system in adult transgenic Ciona robusta (Ciona intestinalis type A) which expresses the Kaede reporter gene driven by the prohormone convertase 2 (PC2) gene promoter. Numerous PC2 promoter-driven fluorescent (Kaede-positive) non-neural cells were distributed in the blood sinus located at the anterior end of the pharynx, suggesting the acquisition of a peptidergic circulatory system in Ciona. Kaede-positive ciliated columnar cells, rounded cells, and tall ciliated cells were observed in the alimentary organs, including the endostyle, pharynx, esophagus, stomach, and intestine, suggesting that digestive functions are regulated by multiple peptidergic systems. in the heart, Kaede-positive neurons were located in the ring-shaped plexus at both ends of the myocardium. Nerve fiber-like tracts ran along the raphe and appeared to be connected with the plexuses. Such unique structures suggest a role for the peptidergic system in cardiac function. collectively, the present anatomic analysis revealed the major framework of the ventral peptidergic system of adult Ciona, which could facilitate investigations of peptidergic regulation of the pharynx, endostyle, alimentary tissues, and heart.

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Section: Distribution Of Peptidergic Cells In the Endostylementioning

confidence: 99%

The ventral peptidergic system of the adult ascidian Ciona robusta (Ciona intestinalis Type A) insights from a transgenic animal model

Osugi

Sasakura

Satake

2020

Sci Rep

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“…The apical portions of the secretory cells directly border on the luminal cavity. The follicular epithelium of bullfrogs is immunoreactive for calcitonin and calcitonin gene‐related peptide (CGRP) (Yaoi et al, ). Unmyelinated nerve fibers are distributed in the ultimobranchial parenchyma of Rana pipiens (Robertson, ).…”

Section: Phylogenic Analysis Of the Ultimobranchial Glandmentioning

confidence: 99%

“…Similar to mammalian thyroid C cells, the ultimobranchial gland of many nonmammalian vertebrates, including the ray, trout, zebrafish, goldfish, bullfrog, newt, chicken, quail, macaw, and grass parakeet is immunoreactive for calcitonin (McMillan et al, ; Sasayama et al, ; Yaoi et al, ; Hidaka and Suzuki, ; Yamada et al, ; Kameda et al, ). Thyroid C cells of dogs and rats have been demonstrated to react sensitively to changes in concentration of serum calcium (Kameda, ).…”

Section: Function Of the Ultimobranchial Gland In Lower Vertebratesmentioning

confidence: 99%

Morphological and molecular evolution of the ultimobranchial gland of nonmammalian vertebrates, with special reference to the chicken C cells

Kameda

2017

Developmental Dynamics

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This review summarizes the current understanding of the nonmammalian ultimobranchial gland from morphological and molecular perspectives. Ultimobranchial anlage of all animal species develops from the last pharyngeal pouch. The genes involved in the development of pharyngeal pouches are well conserved across vertebrates. The ultimobranchial anlage of nonmammalian vertebrates and monotremes does not merge with the thyroid, remaining as an independent organ throughout adulthood. Although C cells of all animal species secrete calcitonin, the shape, cellular components and location of the ultimobranchial gland vary from species to species. Avian ultimobranchial gland is unique in several phylogenic aspects; the organ is located between the vagus and recurrent laryngeal nerves at the upper thorax and is densely innervated by branches emanating from them. In chick embryos, TuJ1-, HNK-1-, and PGP 9.5-immunoreactive cells that originate from the distal vagal (nodose) ganglion, colonize the ultimobranchial anlage and differentiate into C cells; neuronal cells give rise to C cells. Like C cells of mammals, the cells of fishes, amphibians, reptiles, and also a subset of C cells of birds, appear to be derived from the endodermal epithelium forming ultimobranchial anlage. Thus, the avian ultimobranchial C cells may have dual origins, neural progenitors and endodermal epithelium. Developmental Dynamics 246:719-739, 2017. V C 2017 Wiley Periodicals, Inc.

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“…After treatment of 20 g of total RNA with DNase (4 U; Takara, Kyoto, Japan), a 10-g aliquot of the total RNA was reverse-transcribed in 20 l of reaction buffer containing a 1-mM concentration of each dNTP, 9.9 U of RNase inhibitor (Toyobo; Osaka, Japan), and 7.5 mM oligo-dT(19) primer (Life Technologies) at 42C for 1 hr and then at 52C for 30 min. PCR was then performed basically by the same method as described previously (Yaoi et al 2003a), using the following homologous primers: otoconin-22 sense, 5 Ј -CTGTGACTCAGACATACCGCTTCTA-3 Ј (247-271 b); otoconin-22 antisense, 5 Ј -CATCGCACT-CACAGACCATCTT-3 Ј (324-345 b). Bullfrog ␤ -actin was used as an internal standard during detection of otoconin-22 mRNA expression.…”

Section: Rt-pcr Of Developing Embryosmentioning

confidence: 99%

“…Bullfrog ␤ -actin was used as an internal standard during detection of otoconin-22 mRNA expression. The ␤ -actin cDNA was amplified by using a set of primers designed to amplify a ␤ -actin fragment of 96 bp (Yaoi et al 2003a). The RT-PCR products were analyzed on a 2% agarose gel containing ethidium bromide (EtBr; 0.5 g/ml) with Marker 6 ( /Sty1 digest; Wako Pure Chemicals, Osaka, Japan) molecular weight markers.…”

Section: Rt-pcr Of Developing Embryosmentioning

confidence: 99%

Developmental Expression of Otoconin-22 in the Bullfrog Endolymphatic Sac and Inner Ear

Yaoi

Onda

Hidaka

et al. 2004

J Histochem Cytochem.

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S U M M A R YIn amphibians, calcium carbonate crystals are present in the endolymphatic sac and the inner ear. The formation of these crystals is considered to be facilitated by a protein called otoconin-22. We examined the spatial and temporal expression of otoconin-22 during the development of the bullfrog ( Rana catesbeiana ) using RT-PCR, in situ hybridization (ISH), and immunofluorescence techniques. By RT-PCR, otoconin-22 mRNA was first detected in embryos at Shumway stage 20, and this expression pattern continues in late stages. The first otoconin-22 mRNA-positive reaction was detected in stage 22 embryos in the placode of the endolymphatic sac. Otoconin-22 protein was observed in the epithelial cells of the endolymphatic sac at stage 24. On the other hand, a whole-mount ISH technique showed the first expression of otoconin-22 mRNA in the inner ear, in addition to the endolymphatic sac, at the mid-phase of Shumway stage 25. We discuss the role of otoconin-22 in the formation of calcium carbonate crystals in the endolymphatic sac and inner ear. O rganisms produce hard tissues in a process called biomineralization. Hard tissue includes bones, teeth, calculus, and otoliths, which are present in many vertebrates, in scales in fish, and in eggshell in birds. In invertebrates, examples of hard tissue are the shells of mollusks and diatoms, the ossicles of sea urchins, the exoskeletons of crustaceans, and the coccoliths of coccolithophriods. Recently, several cDNAs encoding proteins involved in the formation of ear stones have been cloned and sequenced, otoconin-90 (also called otoconin-95) in mammals (Wang et al. 1998;Verpy et al. 1999;Thalmann et al. 2001) and otolith matrix protein-1 (Murayama et al. 2000) and otolin-1 (Murayama et al. 2002) in teleosts. Analysis of the molecular mechanism of the ear stone formation has advanced rapidly. In most vertebrates the endolymphatic sac, which arises as the endolymphatic duct from the junction of the utriculus and the sacculus, terminates in a small blind-ending vesicle within the braincase, whereas the amphibian endolymphatic sac not only enlarges to form processes around the brain but also extends caudally along the vertebral canal and protrudes between the vertebrae, where it is referred to as the paravertebral lime sac. The lumen of these sacs contains many tiny crystals consisting of calcium carbonate, which are formed by otoconin-22 protein. In a previous study, we found that otoconin-22 protein is present in the endolymphatic sac surrounding the pituitary gland and the paravertebral lime sac in the bullfrog (Yaoi et al. 2001). Later, we cloned and sequenced a cDNA encoding bullfrog otoconin-22 and found that calcitonin regulates the expression of otoconin-22 mRNA in the endolymphatic sac, thereby stimulating the formation of calcium crystals in the lumen of the endolymphatic sac (Yaoi et al. 2003b). Furthermore, we noted that the inner ear expressed otoconin-22 mRNA but not calcitonin receptor mRNA, although the receptor mRNA was expressed in the endolymphatic...

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Expression and Localization of Prohormone Convertase PC1 in the Calcitonin-producing Cells of the Bullfrog Ultimobranchial Gland

Cited by 5 publications

References 25 publications

The ventral peptidergic system of the adult ascidian Ciona robusta (Ciona intestinalis Type A) insights from a transgenic animal model

The ventral peptidergic system of the adult ascidian Ciona robusta (Ciona intestinalis Type A) insights from a transgenic animal model

Morphological and molecular evolution of the ultimobranchial gland of nonmammalian vertebrates, with special reference to the chicken C cells

Developmental Expression of Otoconin-22 in the Bullfrog Endolymphatic Sac and Inner Ear

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