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Molecular cloning and pharmacological characterization of two novel GnRH receptors in the lamprey (Petromyzon marinus).

ABSTRACT: This paper reports the identification, expression, binding kinetics, and functional studies of two novel type III lamprey GnRH receptors (lGnRH-R-2 and lGnRH-R-3) in the sea lamprey, a basal vertebrate. These novel GnRH receptors share the structural features and amino acid motifs common to other known gnathostome GnRH receptors. The ligand specificity and activation of intracellular signaling studies showed ligands lGnRH-II and -III induced an inositol phosphate (IP) response at lGnRH-R-2 and lGnRH-R-3, whereas the ligand lGnRH-I did not stimulate an IP response. lGnRH-II was a more potent activator of lGnRH-R-3 than lGnRH-III. Stimulation of lGnRH-R-2 and lGnRH-R-3 testing all three lGnRH ligands did not elicit a cAMP response. lGnRH-R-2 has a higher binding affinity in response to lGnRH-III than lGnRH-II, whereas lGnRH-R-3 has a higher binding affinity in response to lGnRH-II than IGnRH-III. lGnRH-R-2 precursor transcript was detected in a wide variety of tissues including the pituitary whereas lGnRH-R-3 precursor transcript was not as widely expressed and primarily expressed in the brain and eye of male and female lampreys. From our phylogenetic analysis, we propose that lGnRH-R-1 evolved from a common ancestor of all vertebrate GnRH receptors and lGnRH-R-2 and lGnRH-R-3 likely occurred due to a gene duplication within the lamprey lineage. In summary, we propose from our findings of receptor subtypes in the sea lamprey that the evolutionary recruitment of specific pituitary GnRH receptor subtypes for particular physiological functions seen in later evolved vertebrates was an ancestral character that first arose in a basal vertebrate.

SUBMITTER: Joseph NT

PROVIDER: S-EPMC3380312 | biostudies-literature | 2012 Jul

REPOSITORIES: biostudies-literature

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Project description:The sea lamprey, Petromyzon marinus, is an anadromous, semelparous species that is vulnerable to endangered in parts of its native range due in part to loss of spawning habitat because of man-made barriers. The ability of lampreys to return to the ocean or estuary and search out alternative spawning river systems would be limited by their osmoregulatory ability in seawater. A reduction in tolerance to salinity has been documented in migrants, although the underlying mechanisms have not been characterized. We examined the capacity for marine osmoregulation in upstream spawning migrants by characterizing the physiological effects of salinity challenge from a molecular perspective. Estuarine-captured migrants held in freshwater (FW) for ∼1 week (short-term acclimation) or 2 months (long-term acclimation) underwent an incremental salinity challenge until loss of equilibrium occurred and upper thresholds of 25 and 17.5, respectively, occurred. Regardless of salinity tolerance, all lamprey downregulated FW ion-uptake mechanisms [gill transcripts of Na(+):Cl(-) cotransporter (NCC/slc12a3) and epithelial Na(+) channel (ENaC/scnn1) and kidney Na(+)/K(+)-ATPase (NKA) protein and activity but not transcript]. At their respective salinity limits, lamprey displayed a clear osmoregulatory failure and were unable to regulate [Na(+)] and [Cl(-)] in plasma and intestinal fluid within physiological limits, becoming osmocompromised. A >90% drop in haematocrit indicated haemolysis, and higher plasma concentrations of the cytosolic enzymes alanine aminotransferase, aspartate aminotransferase and lactate dehydrogenase indicated damage to other tissues, including liver. However, >80% of short-term FW-acclimated fish were able to osmoregulate efficiently, with less haemolysis and tissue damage. This osmoregulatory ability was correlated with significant upregulation of the secretory form of Na(+):K(+):2Cl(-) cotransporter (NKCC1/slc12a2) transcript levels and the re-emergence of seawater-type ionocytes detected through immunohistochemical NKA immunoreactivity in the gill, the central ionoregulatory organ. This work sheds light on the molecular and physiological limits to the potential return to seawater for lampreys searching for alternative FW systems in which to spawn.

Project description:BackgroundRetinoic acid (RA) signaling controls many developmental processes in chordates, from early axis specification to late organogenesis. The functions of RA are chiefly mediated by a subfamily of nuclear hormone receptors, the retinoic acid receptors (RARs), that act as ligand-activated transcription factors. While RARs have been extensively studied in jawed vertebrates (that is, gnathostomes) and invertebrate chordates, very little is known about the repertoire and developmental roles of RARs in cyclostomes, which are extant jawless vertebrates. Here, we present the first extensive study of cyclostome RARs focusing on three different lamprey species: the European freshwater lamprey, Lampetra fluviatilis, the sea lamprey, Petromyzon marinus, and the Japanese lamprey, Lethenteron japonicum.ResultsWe identified four rar paralogs (rar1, rar2, rar3, and rar4) in each of the three lamprey species, and phylogenetic analyses indicate a complex evolutionary history of lamprey rar genes including the origin of rar1 and rar4 by lineage-specific duplication after the lamprey-hagfish split. We further assessed their expression patterns during embryonic development by in situ hybridization. The results show that lamprey rar genes are generally characterized by dynamic and highly specific expression domains in different embryonic tissues. In particular, lamprey rar genes exhibit combinatorial expression domains in the anterior central nervous system (CNS) and the pharyngeal region.ConclusionsOur results indicate that the genome of lampreys encodes at least four rar genes and suggest that the lamprey rar complement arose from vertebrate-specific whole genome duplications followed by a lamprey-specific duplication event. Moreover, we describe a combinatorial code of lamprey rar expression in both anterior CNS and pharynx resulting from dynamic and highly specific expression patterns during embryonic development. This 'RAR code' might function in regionalization and patterning of these two tissues by differentially modulating the expression of downstream effector genes during development.

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Molecular cloning and pharmacological characterization of two novel GnRH receptors in the lamprey (Petromyzon marinus).

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