Gene structure and seasonal expression of carp fish prolactin short receptor isoforms

Abstract

The complex adaptive mechanisms that eurythermal fish have evolved in response to the seasonal changes of the environment include the transduction of the physical parameter variations into neuroendocrine signals. Studies in carp (Cyprinus carpio) have indicated that prolactin (PRL) and growth hormone (GH) expression is associated with acclimatization, suggesting that the pituitary gland is a relevant physiological node in this adaptive process. Also, the distinctive pattern of expression that carp prolactin receptor (PRLr) protein depicts upon seasonal acclimatization supports the hypothesis that PRL and its receptor clearly are involved in the new homeostatic stage that the eurythermal fish needs to survive during the cyclical changes of its habitat. Here, we characterize the first prolactin receptor gene in a teleost and show that its expression is not associated with alternative promoters, unlike in humans and rodents. Using the regulatory region to direct the transcription of green fluorescent protein (GFP) in zebrafish embryos, we mapped the appearance of this hormone receptor during fish development. This is the first report identifying a fish prolactin receptor gene expressing transcript isoforms encoding for short forms of the protein (45 kDa). These have been found in osmoregulatory tissues of the carp and are regulated in connection with the seasonal acclimatization of the fish.

A novel tilapia prolactin receptor is functionally distinct from its paralog

“…It is possible that additional splice variants of OmPRLR2 are expressed that were not detected in this study because they lack the antigenic region detected by our OmPRLR2 antibody. The presence of shorter PRLR variants is a common feature in mammals but was only recently described in fish when alternatively spliced PRLR1 forms having a truncated ICD were detected in carp (San Martin et al, 2007). Carp variations resemble human PRLR splice variants but are different from the short OmPRLR2 variant found in this study, where the ICD remains constant compared with the full-length variant.…”

Cloning and expression of a unique short form of the porcine prolactin receptor

“…The porcine PRLR long form (LF) containing full-length exon 10 has been characterized (Trott et al 2007), where the LF transduces both mitogenic and differentiative signals in all species studied to date (Lesueur et al 1991, O'Neal & Yu-Lee 1994, Jabbour et al 1998, Llovera et al 2000. Recently, we identified two short isoforms of the human PRLR (hPRLR-short form (SF); Trott et al 2003), generated by alternative splicing to exon 11, that extends its observation in other species including the rat (Boutin et al 1988), mouse (Davis & Linzer 1989), sheep and goat (Bignon et al 1997), cow , and carp (San Martin et al 2007). The PRLR-SF share common features including a truncated intracellular domain, and function either as heterodimers with the PRLR-LF or as PRLR-SF homodimers.…”

“…These data are consistent with our observations. A discrepency between PRLR-SF mRNA levels and protein levels has also been observed in carp, where the PRLR-SF is the predominant protein even though the PRLR-LF mRNA is more abundant than the PRLR-SF mRNA (San Martin et al 2004Martin et al , 2007. The discrepancy between pPRLR-SF mRNA and protein levels could be due to increased stability of the mRNA or protein relative to the pPRLR-LF.…”

“…7). However, this strategy is different from that of ruminants (Bignon et al 1997) and carp (San Martin et al 2007). The PRL gene for primates, rodents, and ruminants/pigs diverged from each other at least 75 million years ago, while the pig PRL gene diverged from the ruminant PRL gene only 55 million years ago (Wallis 2000).…”

“…Comparison of the evolution of splicing strategies used to generate short isoforms of the prolactin receptor with the evolution of PRLR-LF sequences in different species. (A) The PRLR-LF in most species is generated by splicing together coding exons 3-10; in many fish species the long isoform comprises coding exons 2-9 (San Martin et al 2007, Fiol et al 2009). In all species studied to date, the final exon is the longest.…”