Characterization of Gonadotropin-Releasing Hormone (GnRH) Genes From Cartilaginous Fish: Evolutionary Perspectives

Gaillard, Anne Laure; Tay, Boon Hui; Sirkin, Daniela I. Pérez; Lafont, Anne Gaëlle; Flori, Céline De; Vissio, Paula Gabriela; Mazan, Sylvie; Dufour, Sylvie; Venkatesh, Byrappa; Tostivint, Hervé

doi:10.3389/fnins.2018.00607

Cited by 27 publications

(27 citation statements)

References 49 publications

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“…The main aim of the present study was to determine the repertoire of the SST gene family in cartilaginous fish. For this purpose, the genome and/or transcriptome databases from three representative chondrichthyan species were examined, namely the small-spotted catshark S. canicula (unpublished, see Gaillard et al 2018 for more details), the whale shark, R. typus (Read et al 2017) and the elephant shark C. milii (Venkatesh et al 2014). In S. canicula, two new SST genes, named SSTd and STTe were found, in addition to the three SST genes, SSTa, SSTb and SSTc, previoulsly identified .…”

Section: Discussionmentioning

confidence: 99%

Revisiting the evolution of the somatostatin family: Already five genes in the gnathostome ancestor

Tostivint¹,

Gaillard²,

Mazan

et al. 2019

General and Comparative Endocrinology

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The somatostatin (SST) family members are a group of neuropeptides that are best known for their role in the regulation of growth, development and metabolism. The occurrence of six paralogous SST genes named SST1, SST2, SST3, SST4, SST5 and SST6 has been reported in vertebrates. It has been proposed that SST1, SST2 and SST5 arose in 2R from a common ancestral gene. SST3 and SST6 would have been subsequently generated by tandem duplications of the SST1 and SST2 genes respectively, at the base of the actinopterygian lineage. SST4 is thought to have appeared more recently from SST1, in teleost-specific 3R. In order to gain more insights into the SST gene family in vertebrates, we sought to identify which paralogs of this family are present in cartilaginous fish. For this purpose, we first searched the recently available genome and transcriptome databases from the catshark Scyliorhinus canicula. In a previous study, three S. canicula SST genes, called at that time SSTa, SSTb and SSTc, were identified and proposed to correspond to SST1, SST5 and SST2 respectively. In the present work, two additional SST genes, called SSTd and SSTe, were found in S. canicula plus two other chondrichtyan species, elephant shark (Callorhinchus milii) and whale shark (Rhincodon typus). Phylogeny and synteny analyses were then carried out in order to reveal the evolutionary relationships of SSTd and SSTe with other vertbrates SSTs. We showed that SSTd and SSTe correspond to SST2 and SST3 respectively, while SSTc corresponds to SST6 and not to SST2 as initially proposed. Our investigations in other vertebrate species also led us to find that the so-called SST2 gene in chicken, lungfish, sturgeons and teleosts actually corresponds to SST6. Conversely, the so-called SST6 gene in actinopterygians corresponds to SST2. Taken together, our results suggest that: i) SST3 and SST6 were already present in the gnathostome ancestor, much earlier than previously thought; ii) SST6 was also present in the tetrapod ancestor and still occurs in living birds; with this respect, it is likely that SST6 was independently lost several times during evolution: in euteleosts, amphibians, squamates and mammals; iii) SST2, SST3 and SST5 were probably lost in euteleosts, sarcopterygians and tetrapods, respectively. whale shark, Rhincodon typus (Read et al. 2017) and the elephant shark, C. milii (Venkatesh et al. 2014). We found two novel S. canicula SST genes that we propose to provisionally call SSTd and SSTe (according to the nomenclature initially proposed in Quan et al. 2013). S. canicula SSTd was shown to be the ortholog of the L. erinacea and C. milii atypical SST-like gene abovementioned, while S. canicula SSTe appeared as a totally new SST gene. In both R. typus and C. milii, four SST genes were found that correspond SSTa, SSTc, SSTd and SSTe. Taking advantage of the genome assembly of various representative species from other vertebrate groups, we then carried out phylogeny and synteny analyses in order to reveal the evolutionary relationships of chondrichthy...

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Section: Discussionmentioning

confidence: 99%

Revisiting the evolution of the somatostatin family: Already five genes in the gnathostome ancestor

Tostivint¹,

Gaillard²,

Mazan

et al. 2019

General and Comparative Endocrinology

Self Cite

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“…It is now widely recognized that while less evolved teleost species such as salmonids and cyprinids possess two Gnrh isoforms, the brain of most teleost species, including Perciformes, Pleuronectiformes and many other fish orders, exhibit three distinct forms of Gnrh (Kah et al, 2007;Zohar et al, 2010;Choi, 2018). Interestingly, three isoforms of Gnrh were found in the superclass Agnatha and also recently across the non-teleost, cartilaginous fish (Gaillard et al, 2018).…”

Section: The Discovery Of Gnrh Isoformsmentioning

confidence: 99%

“…For example, the GnRH1 genes of both medaka and human lie adjacent to a gene for a potassium channel tetramerization domain containing 9 (KCTD9) and GnRH2 genes are adjacent to a gene for protein tyrosine phosphatase A (PTPRA) (Okubo et al 2002). The syntenies in the GnRH gene loci are also preserved in several other vertebrate species, including chimpanzees, mice, chickens, the pufferfish Tetraodon nigroviridis and Takifugu rubripes, zebrafish, lamprey and sharks (Morgan and Millar, 2004;Kuo et al, 2005;Ikemoto and Park, 2006;Tostivint, 2011;Decatur et al 2013;Gaillard et al, 2018). It is now suggested that GnRH1, GnRH2 and GnRH3 genes represent three paralogous genes resulting from the two rounds (2R) of tetraploidization that took place early in vertebrate evolution, followed by two separate deletion events (Figure 2) (Kim et al 2011;Tostivint, 2011;Roch et al, 2014).…”

Section: Evolution Of Gnrh Isoformsmentioning

confidence: 99%

The gonadotropin-releasing hormones: Lessons from fish

Muñoz‐Cueto

Zmora

Paullada-Salmerón

et al. 2020

General and Comparative Endocrinology

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Fish have been of paramount importance to our understanding of vertebrate comparative neuroendocrinology and the mechanisms underlying the physiology and evolution of gonadotropin-releasing hormones (GnRH) and their genes. This review integrates past and recent knowledge on the Gnrh system in the fish model. Multiple Gnrh isoforms (two or three forms) are present in all teleosts, as well as multiple Gnrh receptors (up to five types), which differ in neuroanatomical localization, pattern of projections, ontogeny and functions. The role of the different Gnrh forms in reproduction seems to also differ in teleost models possessing two versus three Gnrh forms, Gnrh3 being the main hypophysiotropic hormone in the former and Gnrh1 in the latter. Functions of the non-hypothalamic Gnrh isoforms are still unclear, although under suboptimal physiological conditions (e.g. fasting), Gnrh2 may increase in the pituitary to ensure the integrity of reproduction under these conditions. Recent developments in transgenesis and mutagenesis in fish models have permitted the generation of fish lines expressing fluorophores in Gnrh neurons and to elucidate the dynamics of the elaborate innervations of the different neuronal populations, thus enabling a more accurate delineation of their reproductive roles and regulations. Moreover, in combination with neuronal electrophysiology, these lines have clarified the Gnrh mode of actions in modulating Lh and Fsh activities. While loss of function and genome editing studies had the premise to elucidate the exact roles of the multiple Gnrhs in reproduction and other processes, they have instead evoked an ongoing debate about these roles and opened new avenues of research that will no doubt lead to new discoveries regarding the not-yet-fully-understood Gnrh system.

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“…GnRH is a decapeptide produced in the hypothalamus with a regulatory function in the reproductive system (32)(33)(34). Different analogs of GnRH with different half-life exist (22).…”

Section: Discussionmentioning

confidence: 99%

Design, production and purification of a novel recombinant gonadotropin-releasing hormone associated peptide as a spawning inducing agent for fish

Mohammadzadeh

Moradian

Falahatkar

et al. 2020

Protein Expression and Purification

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GnRH is a neuropeptide known to regulate reproduction in vertebrates. The purpose of this study was to design and produce recombinant gonadotropin-releasing hormone associated peptide (rGnRH/GAP) as an alternative of the previous GnRHs and native extracted hormone from tissue, to induce final maturation in fish. Decapeptide as well as GAP area sequences were compared between GnRH1, GnRH2, and mGnRH from Acipenser sp and Huso huso, respectively. Considering the conserved amino acids and the replacement of unstable amino acids with those that were more stable against proteolytic digestion as well as had a longer halflife, the sequence was designed. The sequences of decapeptide and GAP region were synthesized and then cloned on pET28a expression vector and transformed into expression host Escherichia coli BL21(DE3). The supernatant of cultured recombinant bacteria was used for purification using TALON Metal affinity resin. The purity of the GnRH/GAP was confirmed by single 8 kDa band on SDS-PAGE and western blot. Bioinformatics studies were performed for evaluation of homology between GnRH protein sequences and prediction of 3D protein structure using Swiss Model. The result showed that the structure prediction of the recombinant GnRH decapeptide was relatively similar to decapeptide of GnRH2 from Beluga (Huso huso). The GAP structure was similar to GAP1 of Nile tilapia (Oreochromis niloticus) and sturgeon and GnRH2 of Chinese sturgeon (Acipenser sinensis). The mass analysis showed that the sequence was exactly the same as designated sequence. Biology activity of rGnRH/GAP was tested in mature goldfish (Carassius auratus) and results showed that rGnRH/GAP had a positive effect in final maturation. Indeed 17α, 20β-dihydroxy-4-pregnen-3-one (DHP) was increased 17 h and 24h after injection with rGnRH/GAP and spawning stemmed from that injection. These novel findings introduce the potential of utilizing rGnRH/GAP in aquaculture.

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Characterization of Gonadotropin-Releasing Hormone (GnRH) Genes From Cartilaginous Fish: Evolutionary Perspectives

Cited by 27 publications

References 49 publications

Revisiting the evolution of the somatostatin family: Already five genes in the gnathostome ancestor

Revisiting the evolution of the somatostatin family: Already five genes in the gnathostome ancestor

The gonadotropin-releasing hormones: Lessons from fish

Design, production and purification of a novel recombinant gonadotropin-releasing hormone associated peptide as a spawning inducing agent for fish

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