The Kiss2 receptor (Kiss2r) gene in Southern Bluefin Tuna, Thunnus maccoyii and in Yellowtail Kingfish, Seriola lalandi – Functional analysis and isolation of transcript variants

Nocillado, Josephine; Biran, Jakob; Lee, Y.Y.; Levavi‐Sivan, Berta; Mechaly, Alejandro S.; Zohar, Yonathan; Elizur, Abigail

doi:10.1016/j.mce.2012.06.024

Cited by 45 publications

(23 citation statements)

References 46 publications

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“…The ability of fish Kiss to activate the PKA pathway has been identified by several groups (24,29,55). In the present study, we found that Bjgpr54L-1 could activate both PKC and PKA pathways, supporting the conclusion in fish.…”

Section: Signaling Pathway Activated By Amphioxus Kissrsupporting

confidence: 87%

Demonstration of a Functional Kisspeptin/Kisspeptin Receptor System in Amphioxus With Implications for Origin of Neuroendocrine Regulation

Wang

et al. 2017

Endocrinology

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Amphioxus belongs to the Cephalochordata, which is the most basal subphylum of the chordates. Despite many studies on the endocrine system of amphioxus, key information about its regulation remains ambiguous. Here we clearly demonstrate the presence of a functional kisspeptin/kisspeptin receptor (Kiss-Kissr) system, which is involved in the regulation of reproduction in amphioxus. Evolutionary analyses revealed large expansion of Kiss and Kissr (gpr54) genes in amphioxus, and they might represent the ancestral type of the Kiss/gpr54 genes in chordates. Amphioxus Kiss was obviously expression at the cerebral vesicle and the Hatschek pit, whereas amphioxus gpr54 messenger RNA (mRNA) was abundantly present in nerve cord, ovary, and testes. Amphioxus GPR54-Like1 (GPR54L-1) was shown to be located on the cell membrane. The synthetic amphioxus Kiss-like (KissL) peptides were capable of activating the amphioxus GPR54L-1 with different potencies, hinting the interaction between Kiss and GPR54. Moreover, the expression of amphioxus gpr54 mRNA was significantly decreased during low or high temperature extremes. Importantly, the injection of amphioxus KissL could cause an elevation of zebrafish blood luteinizing hormone level and induce the expression of amphioxus gpb5, a gene encoding the ancestral type of vertebrate pituitary glycoprotein hormones. Also, the expression levels of BjkissL-2 or Bjgpr54L-1 were downregulated after spermiation or spawning. Collectively, the amphioxus Kiss-Kissr system has a correlation with the regulation of reproduction. Our studies provide insights into the functional roles and evolutionary history of the Kiss-Kissr system, as well as the origin of the vertebrate neuroendocrine axis for controlling reproduction.

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Section: Signaling Pathway Activated By Amphioxus Kissrsupporting

confidence: 87%

Demonstration of a Functional Kisspeptin/Kisspeptin Receptor System in Amphioxus With Implications for Origin of Neuroendocrine Regulation

Wang

et al. 2017

Endocrinology

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“…Similarly, Nocillado et al (2012) showed that Southern bluefin tuna KissR2 and yellowtail kingfish KissR2 preferentially transduced via the PKC than PKA pathways (Nocillado et al 2012). In zebrafish, which possesses two Kiss (Kiss1 and Kiss2) and two KissR (Kiss1Ra and Kiss1RbZKissR2 and KissR3 in our nomenclature, respectively), differential activation of signaling pathways has been observed using COS cells transfected with zebrafish KissR and SRE-/CRE-reporters (Biran et al 2008).…”

Section: Signaling Pathways In Mammalsmentioning

confidence: 76%

“…The existence of kissr mRNA splicing isoforms has been reported in several teleost species including the senegalese sole (two KissR2 isoforms) (Mechaly et al 2009), the yellowtail kingfish (five KissR2 isoforms) and Southern bluefin tuna (two kissr2 isoforms) (Nocillado et al 2012), the zebrafish (five kissr3 isoforms) (Onuma & Duan 2012), and the European eel (three kissr3 isoforms) (Pasquier et al 2012a). The splicing variants can result from the retention of an intron as in the senegalese sole (Mechaly et al 2009), yellowtail kingfish and bluefin tuna (Nocillado et al 2012), or they can result from the deletion of exonic sequence as in the zebrafish (Onuma & Duan 2012), yellowtail kingfish (Nocillado et al 2012), and European eel (Pasquier et al 2012a).…”

Section: Kissr Gene Structurementioning

confidence: 98%

“…The splicing variants can result from the retention of an intron as in the senegalese sole (Mechaly et al 2009), yellowtail kingfish and bluefin tuna (Nocillado et al 2012), or they can result from the deletion of exonic sequence as in the zebrafish (Onuma & Duan 2012), yellowtail kingfish (Nocillado et al 2012), and European eel (Pasquier et al 2012a). So far, these splicing variants are considered to give rise to non-functional proteins except for one of the zebrafish truncated isoforms (KRBDP3), which has been located in the nucleus and could exert a transactivation effect upon kisspeptin binding (Onuma & Duan 2012).…”

Section: Kissr Gene Structurementioning

confidence: 99%

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MOLECULAR EVOLUTION OF GPCRS: Kisspeptin/kisspeptin receptors

Pasquier¹,

Kamech²,

Lafont³

et al. 2014

Journal of Molecular Endocrinology

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Following the discovery of kisspeptin (Kiss) and its receptor (GPR54 or KissR) in mammals, phylogenetic studies revealed up to three Kiss and four KissR paralogous genes in other vertebrates. The multiplicity of Kiss and KissR types in vertebrates probably originated from the two rounds of whole-genome duplication (1R and 2R) that occurred in early vertebrates. This review examines compelling recent advances on molecular diversity and phylogenetic evolution of vertebrate Kiss and KissR. It also addresses, from an evolutionary point of view, the issues of the structure-activity relationships and interaction of Kiss with KissR and of their signaling pathways. Independent gene losses, during vertebrate evolution, have shaped the repertoire of Kiss and KissR in the extant vertebrate species. In particular, there is no conserved combination of a given Kiss type with a KissR type, across vertebrate evolution. The striking conservation of the biologically active ten-amino-acid C-terminal sequence of all vertebrate kisspeptins, probably allowed this evolutionary flexibility of Kiss/KissR pairs. KissR mutations, responsible for hypogonadotropic hypogonadism in humans, mostly occurred at highly conserved amino acid positions among vertebrate KissR. This further highlights the key role of these amino acids in KissR function. In contrast, less conserved KissR regions, notably in the intracellular C-terminal domain, may account for differential intracellular signaling pathways between vertebrate KissR. Cross talk between evolutionary and biomedical studies should contribute to further understanding of the Kiss/KissR structure-activity relationships and biological functions.

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“…These findings are in close agreement with previous data in zebrafish, where it was demonstrated that synthetic Kiss1 and Kiss2 peptides activate Kiss receptors with different potencies, the Kissr2 form exhibiting higher sensitivity toward Kiss1-derived peptides than Kiss2-derived peptides ). In the southern bluefin tuna (Thunnus maccoyii) and in yellowtail kingfish (Seriola lalandi), Kissr3 showed a higher response to Kiss2-10 than to Kiss1-10, with stronger transduction via the PKC than PKA pathway (Nocillado et al 2012). Conversely, in goldfish, according to Li et al (2009), Kiss1-10 enhances the PKC pathway through Kissr3 activation, while Kiss2-10 exhibits higher preference for Kissr2 and the ability to activate both PKC and PKA pathways.…”

Section: Discussionmentioning

confidence: 99%

Differential activation of kiss receptors by Kiss1 and Kiss2 peptides in the sea bass

et al. 2015

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Two forms of kiss gene (kiss1 and kiss2) have been described in the teleost sea bass. This study assesses the cloning and characterization of two Kiss receptor genes, namely kissr2 and kissr3 (known as gpr54-1b and gpr54-2b, respectively), and their signal transduction pathways in response to Kiss1 and Kiss2 peptides. Phylogenetic and synteny analyses indicate that these paralogs originated by duplication of an ancestral gene before teleost specific duplication. The kissr2 and kissr3 mRNAs encode proteins of 368 and 378 amino acids, respectively, and share 53.1% similarity in amino acid sequences. In silico analysis of the putative promoter regions of the sea bass Kiss receptor genes revealed conserved flanking regulatory sequences among teleosts. Both kissr2 and kissr3 are predominantly expressed in brain and gonads of sea bass, medaka and zebrafish. In the testis, the expression levels of sea bass kisspeptins and Kiss receptors point to a significant variation during the reproductive cycle. In vitro functional analyses revealed that sea bass Kiss receptor signals are transduced both via the protein kinase C and protein kinase A pathway. Synthetic sea bass Kiss1-15 and Kiss2-12 peptides activated Kiss receptors with different potencies, indicating a differential ligand selectivity. Our data suggest that Kissr2 and Kissr3 have a preference for Kiss1 and Kiss2 peptides, respectively, thus providing the basis for future studies aimed at establishing their physiologic roles in sea bass. . To date, a single ligand (Kiss) and receptor (Gpr54 or Kissr) have been demonstrated to exist in placental mammals (human, opossum) and reptiles, while mammalian monotrems (platypus) possess two forms of Kiss and Kissr genes. Contrasting situations are found in other tetrapodes, such as amphibians, which have three kiss and kissr genes, whereas the kisspeptin system is absent in birds, although a recent investigation into the kisspeptin system in avian lineages provides molecular evidence of the presence of a kiss2-like gene that degenerated and lost its function (Pasquier et al. 2014b). All in all, advances in genome sequencing and comparative genomics in several groups occupying relevant phylogenetic positions have led to the identification of four kissr and three kiss genes in the coelacanth (Sarcopterygian), while in teleosts at least one kiss and kissr is known to be present in all the species investigated to date. Nevertheless, a second gene for kisspeptin and its receptor has been observed in the genomes of other fish species (Biran et al. 2008, Akazome et al. 2010, Oakley et al. 2010, Um et al. 2010, Zohar et al. 2010, Kim et al. 2012, Pasquier et al. 2012a,b, Tena-Sempere et al. 2012. So far, the occurrence of three kissr and two kiss paralogous genes has been reported in an early group of teleosts, the Elopomorphs (European eel, Anguilla anguilla) (Pasquier et al. 2012a,b). In the spotted gar, Lepisosteus oculatus (Actinopterygian, Ginglymode), four kissr and two kiss have been identified, while four kiss but n...

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The Kiss2 receptor (Kiss2r) gene in Southern Bluefin Tuna, Thunnus maccoyii and in Yellowtail Kingfish, Seriola lalandi – Functional analysis and isolation of transcript variants

Cited by 45 publications

References 46 publications

Demonstration of a Functional Kisspeptin/Kisspeptin Receptor System in Amphioxus With Implications for Origin of Neuroendocrine Regulation

Demonstration of a Functional Kisspeptin/Kisspeptin Receptor System in Amphioxus With Implications for Origin of Neuroendocrine Regulation

MOLECULAR EVOLUTION OF GPCRS: Kisspeptin/kisspeptin receptors

Differential activation of kiss receptors by Kiss1 and Kiss2 peptides in the sea bass

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