Functional and Evolutionary Analysis of Flatfish Gonadotropin Receptors Reveals Cladal- and Lineage-Level Divergence of the Teleost Glycoprotein Receptor Family
Chauvigné, Francois; Tingaud-Sequeira, Angele; Agulleiro, Maria Jet al.
[en] Pituitary gonadotropins, follicle-stimulating hormone (FSH),
and luteinizing hormone (LH) act via their cognate glycoprotein
hormone receptors (GpHRs), FSH receptor (FSHR), and LH/
choriogonadotropin receptor (LHCGR) to regulate gonad physiology.
Here, we show that the flatfish Senegalese sole (Solea
senegalensis) expresses functional isoforms of fshr and lhcgr, but
the genomic origin, ligand activation, and tissue distribution of
the receptor transcripts are more complex than expected. By
integrating the molecular phylogeny of GpHRs with the syntenic
loci of vertebrate orthologs, and by subsequently characterizing
the physical maps with the phylogeny of flanking genes, we
found that vertebrate GpHRs have undergone a divergent
evolution. In Teleostei, fshr genes have a common descent and
can be classified as fshra, whereas lhcgrb genes exist as
alternatively coded genes even in closely related species.
Structural analyses of the receptors revealed that Fshra has an
elongated ligand-binding domain, containing an extra leucinerich
repeat that specifically arose in the Acanthomorpha
because of exon duplication. Ectopic expression in Xenopus
laevis oocytes demonstrated that sole Fshra responded to piscine
Fsh and Lh, whereas Lhcgrba was preferentially activated by its
cognate hormone. The expression pattern of sole fshra and
lhcgrba in gonads during the reproductive cycle was consistent
with earlier observations wherein Fshra regulates ovarian
growth and spermatogenesis and Lhcgrb triggers gamete
maturation, respectively. However, contrary to observations in
other teleosts, fshra was localized exclusively in Sertoli cells of
the testis, whereas lhcgrba was expressed in Leydig cells as well as in spermatids. These results demonstrate the presence of
alternatively coded lhcgr isoforms (lhcgrba and lhcgrbb) in
teleosts and suggest a role of the lhcgrba receptor in the
differentiation of spermatids into spermatozoa in Senegalese
sole.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Chauvigné, Francois
Tingaud-Sequeira, Angele
Agulleiro, Maria J
Calusinska, Magdalena ; Université de Liège - ULiège > Centre d'ingénierie des protéines
Gomez, Ana
Finn, Roderick Nigel
Cerda, Joan
Language :
English
Title :
Functional and Evolutionary Analysis of Flatfish Gonadotropin Receptors Reveals Cladal- and Lineage-Level Divergence of the Teleost Glycoprotein Receptor Family
Alternative titles :
[en] Functional and Evolutionary Analysis of Flatfish Gonadotropin Receptors Reveals Cladal- and Lineage-Level Divergence of the Teleost Glycoprotein Receptor Family
Publication date :
03 March 2010
Journal title :
Biology of Reproduction
ISSN :
0006-3363
eISSN :
1529-7268
Publisher :
Society for the Study of Reproduction, Madison, United States - Wisconsin
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