Expression of the gene for ancestral glycoprotein hormone β subunit in the nerve cord of amphioxus

Tando, Yukiko; Kubokawa, Kaoru

doi:10.1016/j.ygcen.2009.04.015

Cited by 40 publications

(23 citation statements)

References 34 publications

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“…Interestingly, the hagfish GPHα forms a clade with the gnathostome GPHαs. For the β-subunits, we propose that an ancestral GPB5 further diverged into vertebrate GPHβ (LHβ, FSHβ, and TSHβ) and GPB5 (18). The hagfish GPHβ forms a clade with the TSHβs; however, the bootstrap values are low and hagfishes evolved before the gnathostomes (Fig.…”

Section: Resultsmentioning

confidence: 95%

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Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish

Uchida

Moriyama

Chiba

et al. 2010

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

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Hagfish, which lack both jaws and vertebrae, are considered the most primitive vertebrate known, living or extinct. Hagfish have long been the enigma of vertebrate evolution not only because of their evolutionary position, but also because of our lack of knowledge on fundamental processes. Key elements of the reproductive endocrine system in hagfish have yet to be elucidated. Here, the presence and identity of a functional glycoprotein hormone (GPH) have been elucidated from the brown hagfish Paramyxine atami. The hagfish GPH consists of two subunits, α and β, which are synthesized and colocalized in the same cells of the adenohypophysis. The cellular and transcriptional activities of hagfish GPHα and -β were significantly correlated with the developmental stages of the gonad. The purified native GPH induced the release of gonadal sex steroids in vitro. From our phylogenetic analysis, we propose that ancestral glycoprotein α-subunit 2 (GPA2) and β-subunit 5 (GPB5) gave rise to GPHα and GPHβ of the vertebrate glycoprotein hormone family, respectively. The identified hagfish GPHα and -β subunits appear to be the typical gnathostome GPHα and -β subunits based on the sequence and phylogenetic analyses. We hypothesize that the identity of a single functional GPH of the hagfish, hagfish GTH, provides critical evidence for the existence of a pituitary-gonadal system in the earliest divergent vertebrate that likely evolved from an ancestral, prevertebrate exclusively neuroendocrine mechanism by gradual emergence of a previously undescribed control level, the pituitary, which is not found in the Protochordates.

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Section: Resultsmentioning

confidence: 95%

“…S1) (14). The basal lineage of chordates, such as tunicates and amphioxus, contains GPA2 and GPA5 in their genome but not GPHα and GPHβ (16)(17)(18)(19). Lamprey may also have GPA2 and GPB5, in addition to the canonical GTHβ-like protein (1,3).…”

mentioning

confidence: 99%

Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish

Uchida

Moriyama

Chiba

et al. 2010

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

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“…Finally, amphioxian GPB5 is 40% homologous to the human form. Th e molecular phylogenetic tree demonstrates how GPB5 is the most ancestral GPB gene, using the neighbor-joining method (Figure 3) (Tando and Kubokawa 2009a).…”

Section: Evolutionary Perspectivementioning

confidence: 99%

“…Numbers upon branching represent bootstrap probabilities for 1000 replication trials, and the evolutionary distance (p-distance) is shown by the scale bar. Th is tree was created using the neighbor-joining method by Tando and Kubokawa (2009a). Abbreviations: TGFβ -tumor growth factor beta, BRP-1 -beta related protein 1 fully been developed yet, a yeast two-hybrid assay has been performed to identify the presence of the molecule along with a radioimmunoassay to assess the intracellular signaling through the cAMP .…”

Section: Th E Functional Role Of Thyrostimulinmentioning

confidence: 99%

The role of thyrostimulin and its potential clinical significance

Karponis

Ananth

2017

Endocrine Regulations

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Th yrostimulin is a glycoprotein heterodimer of GPA2 and GPB5, fi rst described in 2002. It is involved in the physiological function of several tissues. Moreover, evidence points towards the ability of thyrostimulin's individual monomers to induce a biological eff ect, which could denote the circulatory/systemic eff ects of the molecule when found in higher concentrations. From the evolutionary point of view, thyrostimulin shares a binding epitope with the thyroid-stimulating hormone for the thyroid stimulating hormone receptor, whilst possessing affi nity for another unique binding site on the same receptor. Although thyrostimulin can be involved in the hypothalamicpituitary-thyroid axis, its presence in various tissues in an eclectic array of diff erent species renders it multifunctional. From weight loss via increasing metabolic rate to progression of cancer in human ovaries, it is certainly not a signaling molecule to overlook. Furthermore, thyrostimulin has been implicated in bone metabolism, acute illness, and reproductive function. In summary, to our knowledge, this is the fi rst review dealing with the physiological role of thyrostimulin and its potential applications in the clinical practice.

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“…With the discovery of GPA2 and glycoprotein β-subunit 5 (GPB5, thyrostimulin beta) homologs not only in other vertebrates but invertebrates including fly, nematode, and sea urchin (40,41), it is proposed that ancestral glycoprotein existed before the divergence of vertebrates/invertebrates, and that later gene duplication events in vertebrates produced the thyrostimulin (GPA2 and GPB5) and GTH/TSH [GPHα and GPHβ (LHβ/FSHβ/TSHβ)] (40) (Figure 1). The basal lineage of chordates such as tunicates and amphioxus contains GPA2 and GPA5 in their genome but not GPHα or GPHβ (2,(42)(43)(44)(45). Lamprey also has GPA2 and GPB5 genes in addition to the canonical GTHβ (1,33,34,42).…”

Section: Glycoprotein Hormone Familymentioning

confidence: 99%

The hagfish heart

Davison¹

2015

Hagfish Biology

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The hypothalamic-pituitary system is considered to be a seminal event that emerged prior to or during the differentiation of the ancestral agnathans (jawless vertebrates). Hagfishes as one of the only two extant members of the class of agnathans are considered the most primitive vertebrates known, living or extinct. Accordingly, studies on their reproduction are important for understanding the evolution and phylogenetic aspects of the vertebrate reproductive endocrine system. In gnathostomes (jawed vertebrates), the hormones of the hypothalamus and pituitary have been extensively studied and shown to have well-defined roles in the control of reproduction. In hagfish, it was thought that they did not have the same neuroendocrine control of reproduction as gnathostomes, since it was not clear whether the hagfish pituitary gland contained tropic hormones of any kind. This review highlights the recent findings of the hypothalamic-pituitary-gonadal endocrine system in the hagfish. In contrast to gnathostomes that have two gonadotropins (GTH: luteinizing hormone and follicle-stimulating hormone), only one pituitary GTH has been identified in the hagfish. Immunohistochemical and functional studies confirmed that this hagfish GTH was significantly correlated with the developmental stages of the gonads and showed the presence of a steroid (estradiol) feedback system at the hypothalamic-pituitary levels. Moreover, while the identity of hypothalamic gonadotropin-releasing hormone (GnRH) has not been determined, immunoreactive (ir) GnRH has been shown in the hagfish brain including seasonal changes of ir-GnRH corresponding to gonadal reproductive stages. In addition, a hagfish PQRFamide peptide was identified and shown to stimulate the expression of hagfish GTHβ mRNA in the hagfish pituitary. These findings provide evidence that there are neuroendocrine-pituitary hormones that share common structure and functional features compared to later evolved vertebrates.

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Expression of the gene for ancestral glycoprotein hormone β subunit in the nerve cord of amphioxus

Cited by 40 publications

References 34 publications

Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish

Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish

The role of thyrostimulin and its potential clinical significance

The hagfish heart

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