Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives

The neuropeptide gonadotropin-releasing hormone (GnRH) plays an important role in the control of reproductive functions. Vertebrates possess multiple GnRH forms that are classified into three main groups, namely GnRH1, GnRH2, and GnRH3. In order to gain more insights into the GnRH gene family in ver...

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Autores principales: Gaillard, A.-L., Tay, B.-H., Sirkin, D.I.P., Lafont, A.-G., De Flori, C., Vissio, P.G., Mazan, S., Dufour, S., Venkatesh, B., Tostivint, H.
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Acceso en línea:http://hdl.handle.net/20.500.12110/paper_16624548_v12_nSEP_p_Gaillard
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spelling todo:paper_16624548_v12_nSEP_p_Gaillard2023-10-03T16:28:44Z Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives Gaillard, A.-L. Tay, B.-H. Sirkin, D.I.P. Lafont, A.-G. De Flori, C. Vissio, P.G. Mazan, S. Dufour, S. Venkatesh, B. Tostivint, H. Cartilaginous fish Elasmobranchii Evolution Gonadotropin-releasing hormone Holocephali Multigenic family Neuropeptides Vertebrates gonadorelin gonadorelin associated peptide helix loop helix protein messenger RNA protein GAP1a protein GAP1b protein GAP3 unclassified drug animal tissue Article Callorhinchus milii cartilaginous fish controlled study diencephalon enzyme activity female gene gene dosage gene expression gene identification gene structure genetic trait genome GnRH gene GnRH1 gene GnRH1a gene GnRH1b gene GnRH2 gene GnRH3 gene Holocephali male mesencephalon nerve cell nonhuman nucleotide sequence phylogeny prediction protein structure reverse transcription polymerase chain reaction Rhincodon typus Scyliorhinus canicula shark synteny telencephalon transcriptomics The neuropeptide gonadotropin-releasing hormone (GnRH) plays an important role in the control of reproductive functions. Vertebrates possess multiple GnRH forms that are classified into three main groups, namely GnRH1, GnRH2, and GnRH3. In order to gain more insights into the GnRH gene family in vertebrates, we sought to identify which paralogs of this family are present in cartilaginous fish. For this purpose, we searched the genomes and/or transcriptomes of three representative species of this group, the small-spotted catshark, Scyliorhinus canicula, the whale shark, Rhincodon typus and the elephant shark Callorhinchus milii. In each species, we report the identification of three GnRH genes. In catshark and whale shark, phylogenetic and synteny analysis showed that these three genes correspond to GnRH1, GnRH2, and GnRH3. In both species, GnRH1 was found to encode a novel form of GnRH whose primary structure was determined as follows: QHWSFDLRPG. In elephant shark, the three genes correspond to GnRH1a and GnRH1b, two copies of the GnRH1 gene, plus GnRH2. 3D structure prediction of the chondrichthyan GnRH-associated peptides (GAPs) revealed that catshark GAP1, GAP2, and elephant shark GAP2 peptides exhibit a helix-loop-helix (HLH) structure. This structure observed for many osteichthyan GAP1 and GAP2, may convey GAP biological activity. This HLH structure could not be observed for elephant shark GAP1a and GAP1b. As for all other GAP3 described so far, no typical 3D HLH structure was observed for catshark nor whale shark GAP3. RT-PCR analysis revealed that GnRH1, GnRH2, and GnRH3 genes are differentially expressed in the catshark brain. GnRH1 mRNA appeared predominant in the diencephalon while GnRH2 and GnRH3 mRNAs seemed to be most abundant in the mesencephalon and telencephalon, respectively. Taken together, our results show that the GnRH gene repertoire of the vertebrate ancestor was entirely conserved in the chondrichthyan lineage but that the GnRH3 gene was probably lost in holocephali. They also suggest that the three GnRH neuronal systems previously described in the brain of bony vertebrates are also present in cartilaginous fish. © 2018 Gaillard, Tay, Pérez Sirkin, Lafont, De Flori, Vissio, Mazan, Dufour, Venkatesh and Tostivint. JOUR info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_16624548_v12_nSEP_p_Gaillard
institution Universidad de Buenos Aires
institution_str I-28
repository_str R-134
collection Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA)
topic Cartilaginous fish
Elasmobranchii
Evolution
Gonadotropin-releasing hormone
Holocephali
Multigenic family
Neuropeptides
Vertebrates
gonadorelin
gonadorelin associated peptide
helix loop helix protein
messenger RNA
protein GAP1a
protein GAP1b
protein GAP3
unclassified drug
animal tissue
Article
Callorhinchus milii
cartilaginous fish
controlled study
diencephalon
enzyme activity
female
gene
gene dosage
gene expression
gene identification
gene structure
genetic trait
genome
GnRH gene
GnRH1 gene
GnRH1a gene
GnRH1b gene
GnRH2 gene
GnRH3 gene
Holocephali
male
mesencephalon
nerve cell
nonhuman
nucleotide sequence
phylogeny
prediction
protein structure
reverse transcription polymerase chain reaction
Rhincodon typus
Scyliorhinus canicula
shark
synteny
telencephalon
transcriptomics
spellingShingle Cartilaginous fish
Elasmobranchii
Evolution
Gonadotropin-releasing hormone
Holocephali
Multigenic family
Neuropeptides
Vertebrates
gonadorelin
gonadorelin associated peptide
helix loop helix protein
messenger RNA
protein GAP1a
protein GAP1b
protein GAP3
unclassified drug
animal tissue
Article
Callorhinchus milii
cartilaginous fish
controlled study
diencephalon
enzyme activity
female
gene
gene dosage
gene expression
gene identification
gene structure
genetic trait
genome
GnRH gene
GnRH1 gene
GnRH1a gene
GnRH1b gene
GnRH2 gene
GnRH3 gene
Holocephali
male
mesencephalon
nerve cell
nonhuman
nucleotide sequence
phylogeny
prediction
protein structure
reverse transcription polymerase chain reaction
Rhincodon typus
Scyliorhinus canicula
shark
synteny
telencephalon
transcriptomics
Gaillard, A.-L.
Tay, B.-H.
Sirkin, D.I.P.
Lafont, A.-G.
De Flori, C.
Vissio, P.G.
Mazan, S.
Dufour, S.
Venkatesh, B.
Tostivint, H.
Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives
topic_facet Cartilaginous fish
Elasmobranchii
Evolution
Gonadotropin-releasing hormone
Holocephali
Multigenic family
Neuropeptides
Vertebrates
gonadorelin
gonadorelin associated peptide
helix loop helix protein
messenger RNA
protein GAP1a
protein GAP1b
protein GAP3
unclassified drug
animal tissue
Article
Callorhinchus milii
cartilaginous fish
controlled study
diencephalon
enzyme activity
female
gene
gene dosage
gene expression
gene identification
gene structure
genetic trait
genome
GnRH gene
GnRH1 gene
GnRH1a gene
GnRH1b gene
GnRH2 gene
GnRH3 gene
Holocephali
male
mesencephalon
nerve cell
nonhuman
nucleotide sequence
phylogeny
prediction
protein structure
reverse transcription polymerase chain reaction
Rhincodon typus
Scyliorhinus canicula
shark
synteny
telencephalon
transcriptomics
description The neuropeptide gonadotropin-releasing hormone (GnRH) plays an important role in the control of reproductive functions. Vertebrates possess multiple GnRH forms that are classified into three main groups, namely GnRH1, GnRH2, and GnRH3. In order to gain more insights into the GnRH gene family in vertebrates, we sought to identify which paralogs of this family are present in cartilaginous fish. For this purpose, we searched the genomes and/or transcriptomes of three representative species of this group, the small-spotted catshark, Scyliorhinus canicula, the whale shark, Rhincodon typus and the elephant shark Callorhinchus milii. In each species, we report the identification of three GnRH genes. In catshark and whale shark, phylogenetic and synteny analysis showed that these three genes correspond to GnRH1, GnRH2, and GnRH3. In both species, GnRH1 was found to encode a novel form of GnRH whose primary structure was determined as follows: QHWSFDLRPG. In elephant shark, the three genes correspond to GnRH1a and GnRH1b, two copies of the GnRH1 gene, plus GnRH2. 3D structure prediction of the chondrichthyan GnRH-associated peptides (GAPs) revealed that catshark GAP1, GAP2, and elephant shark GAP2 peptides exhibit a helix-loop-helix (HLH) structure. This structure observed for many osteichthyan GAP1 and GAP2, may convey GAP biological activity. This HLH structure could not be observed for elephant shark GAP1a and GAP1b. As for all other GAP3 described so far, no typical 3D HLH structure was observed for catshark nor whale shark GAP3. RT-PCR analysis revealed that GnRH1, GnRH2, and GnRH3 genes are differentially expressed in the catshark brain. GnRH1 mRNA appeared predominant in the diencephalon while GnRH2 and GnRH3 mRNAs seemed to be most abundant in the mesencephalon and telencephalon, respectively. Taken together, our results show that the GnRH gene repertoire of the vertebrate ancestor was entirely conserved in the chondrichthyan lineage but that the GnRH3 gene was probably lost in holocephali. They also suggest that the three GnRH neuronal systems previously described in the brain of bony vertebrates are also present in cartilaginous fish. © 2018 Gaillard, Tay, Pérez Sirkin, Lafont, De Flori, Vissio, Mazan, Dufour, Venkatesh and Tostivint.
format JOUR
author Gaillard, A.-L.
Tay, B.-H.
Sirkin, D.I.P.
Lafont, A.-G.
De Flori, C.
Vissio, P.G.
Mazan, S.
Dufour, S.
Venkatesh, B.
Tostivint, H.
author_facet Gaillard, A.-L.
Tay, B.-H.
Sirkin, D.I.P.
Lafont, A.-G.
De Flori, C.
Vissio, P.G.
Mazan, S.
Dufour, S.
Venkatesh, B.
Tostivint, H.
author_sort Gaillard, A.-L.
title Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives
title_short Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives
title_full Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives
title_fullStr Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives
title_full_unstemmed Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives
title_sort characterization of gonadotropin-releasing hormone (gnrh) genes from cartilaginous fish: evolutionary perspectives
url http://hdl.handle.net/20.500.12110/paper_16624548_v12_nSEP_p_Gaillard
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