Cloning and expression of the rat prolactin receptor, a member of the growth hormone/prolactin receptor gene family

doi:10.1016/0092-8674(88)90488-6

Cell

Volume 53, Issue 1, 8 April 1988, Pages 69-77

https://doi.org/10.1016/0092-8674(88)90488-6 Get rights and content

Abstract

The primary structure of the rat liver prolactin receptor has been deduced from a single complementary DNA clone. The sequence begins with a putative 19 amino acid signal peptide followed by the 291 amino acid receptor that includes a single 24 amino acid transmembrane segment. In spite of the fact that the prolactin receptor has a much shorter cytoplasmic region than the growth hormone receptor, there is strong localized sequence identity between these two receptors in both the extracellular and cytoplasmic domains, suggesting that the two receptors originated from a common ancestor.

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Prolactin potentiates the activity of acid-sensing ion channels in female rat primary sensory neurons
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Citation Excerpt :
PRLRs may mediate PRL enhancing effect of ASIC currents in DRG neurons, since the potentiation of PRL was blocked by Δ1-9-G129R-hPRL, a full PRLR antagonist. Two natural PRLR isoforms, short (PRLR-S) and long (PRLR-L), are generated by alternative splicing of the same gene in rats (Boutin et al., 1988; Shirota et al., 1990). Recent data from in situ hybridization and immunohistochemistry indicate that the patterns of PRLR-S and PRLR-L expression are different in sensory neurons in normal conditions (Belugin et al., 2013).
Prolactin (PRL) is a polypeptide hormone produced and released from the pituitary and extrapituitary tissues. It regulates activity of nociceptors and causes hyperalgesia in pain conditions, but little is known the molecular mechanism. We report here that PRL can exert a potentiating effect on the functional activity of acid-sensing ion channels (ASICs), key sensors for extracellular protons. First, PRL dose-dependently increased the amplitude of ASIC currents with an EC₅₀ of (5.89 ± 0.28) × 10⁻⁸ M. PRL potentiation of ASIC currents was also pH dependent. Second, PRL potentiation of ASIC currents was blocked by Δ1-9-G129R-hPRL, a PRL receptor antagonist, and removed by intracellular dialysis of either protein kinase C inhibitor GF109203X, protein interacting with C-kinase 1(PICK1) inhibitor FSC-231, or PI3K inhibitor AS605240. Third, PRL altered acidosis-evoked membrane excitability of DRG neurons and caused a significant increase in the amplitude of the depolarization and the number of spikes induced by acid stimuli. Four, PRL exacerbated nociceptive responses to injection of acetic acid in female rats. Finally, PRL displayed a stronger effect on ASIC mediated-currents and nociceptive behavior in intact female rats than OVX female and male rats and thus modulation of PRL may be gender-dependent. These results suggest that PRL up-regulates the activity of ASICs and enhances ASIC mediated nociceptive responses in female rats, which reveal a novel peripheral mechanism underlying PRL involvement in hyperalgesia.
Prolactin and teleost ionocytes: New insights into cellular and molecular targets of prolactin in vertebrate epithelia
2014, General and Comparative Endocrinology
The peptide hormone prolactin is a functionally versatile hormone produced by the vertebrate pituitary. Comparative studies over the last six decades have revealed that a conserved function for prolactin across vertebrates is the regulation of ion and water transport in a variety of tissues including those responsible for whole-organism ion homeostasis. In teleost fishes, prolactin was identified as the “freshwater-adapting hormone”, promoting ion-conserving and water-secreting processes by acting on the gill, kidney, gut and urinary bladder. In mammals, prolactin is known to regulate renal, intestinal, mammary and amniotic epithelia, with dysfunction linked to hypogonadism, infertility, and metabolic disorders. Until recently, our understanding of the cellular mechanisms of prolactin action in fishes has been hampered by a paucity of molecular tools to define and study ionocytes, specialized cells that control active ion transport across branchial and epidermal epithelia. Here we review work in teleost models indicating that prolactin regulates ion balance through action on ion transporters, tight-junction proteins, and water channels in ionocytes, and discuss recent advances in our understanding of ionocyte function in the genetically and embryonically accessible zebrafish (Danio rerio). Given the high degree of evolutionary conservation in endocrine and osmoregulatory systems, these studies in teleost models are contributing novel mechanistic insight into how prolactin participates in the development, function, and dysfunction of osmoregulatory systems across the vertebrate lineage.
Reproductive actions of prolactin mediated through short and long receptor isoforms
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Citation Excerpt :
This membrane-anchored protein is composed of an extracellular ligand-binding domain, a single pass transmembrane chain and an intracellular domain responsible for the signal transduction. PRLR was first cloned and characterized in rodents (Boutin et al., 1988; Kelly et al., 1989; Davis and Linzer, 1989, 1990), and almost simultaneously described in human (Boutin et al., 1989), rabbit (Edery et al., 1989), and later in bovine (Scott et al., 1992), chicken (Zhou et al., 1996), frog (Yamamoto et al., 2000), and rainbow trout (Prunet et al., 2000). Although it codes for a single gene product, alternative splicing of its primary transcript or post-translational cleavage can generate multiple variants of the receptor.
Prolactin (PRL) is a polypeptide hormone with a wide range of physiological functions, and is critical for female reproduction. PRL exerts its action by binding to membrane bound receptor isoforms broadly classified as the long form and the short form receptors. Both receptor isoforms are highly expressed in the ovary as well as in the uterus. Although signaling through the long form is believed to be more predominant, it remains unclear whether activation of this isoform alone is sufficient to support reproductive functions or whether both types of receptor are required. The generation of transgenic mice selectively expressing either the short or the long form of PRL receptor has provided insight into the differential signaling mechanisms and physiological functions of these receptors. This review describes the essential finding that both long and short receptor isoforms are crucial for ovarian functions and female fertility, and highlights novel mechanisms of action for these receptors.
Sex-dependent roles of prolactin and prolactin receptor in postoperative pain and hyperalgesia in mice
2013, Neuroscience
Citation Excerpt :
Nevertheless, the elevation of local and systemic PRL levels seen in females, but not males, may be sufficient to both sensitize TRPV1 nociceptors and to stimulate the immune system and these combined effects could help explain the mechanism by which the PRL system is capable of producing sex-dependent thermal (heat and cold) hyperalgesia after hindpaw incision. PRL is a member of the family of class I cytokines (Boutin et al., 1988). Its actions are mediated by the PRL-R, which has two forms, short and long (Kelly et al., 1991; Ginsburg et al., 2012).
Although surgical trauma activates the anterior pituitary gland and elicits an increase in prolactin (PRL) serum levels that can modulate nociceptive responses, the role of PRL and the PRL-receptor (PRL-R) in thermal and mechanical hyperalgesia in postoperative pain is unknown. Acute postoperative pain condition was generated with the use of the hindpaw plantar incision model. Results showed endogenous PRL levels were significantly increased in serum, operated hindpaw and spinal cords of male and female rats 24 h after incision. These alterations were especially pronounced in females. We then examined the role of the PRL system in thermal and mechanical hyperalgesia in male and female mice 3–168 h after plantar incision with the use of knock-out (KO) mice with PRL or PRL-R gene ablations and in wild-type (WT) mice. WT mice showed postoperative cold hyperalgesia in a sex-dependent manner (only in females), but with no effect on heat hyperalgesia or mechanical allodynia in either sex. Studies in KO mice showed no effect of PRL and PRL-R gene ablation on heat and cold hyperalgesia in male mice, while heat hyperlgesia were reduced 3–72 h post-surgery in female PRL and PRL-R KO mice. In contrast, PRL and PRL-R ablations significantly attenuated mechanical allodynia 3–72 h post-surgery in both male and female mice. Overall, we found elevated PRL levels in serum, hindpaws and spinal cords after incision, and identify a contributory role for the PRL system in postoperative pain responses to thermal stimuli in females and to mechanical stimuli in both males and females.
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Cell

Cloning and expression of the rat prolactin receptor, a member of the growth hormone/prolactin receptor gene family

Abstract

J. Biol. Chem.

Biochem. Biophys. Res. Commun.

Cell

Cell

Anal. Biochem.

Gene

J. Biol. Chem.

J. Biol. Chem.

J. Dairy Sci.

Cell

Anal. Biochem.

Mol. Cell. Endocrinol.

Cell

J. Mol. Biol.

J. Biol. Chem.

Cell

J. Biol. Chem.

Cell

Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose

Plasmids for the cloning and expression of full-length double-stranded cDNAs under control of the SV40 early or late gene promoter

Nucl. Acids Res.

Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease

Biochemistry

Translation of eukaryotic messenger RNA in Xenopus oocytes

Molecular cloning of the chicken progesterone receptor

Science

Evolution of prolactin receptors in rabbit mammary gland during pregnancy and lactation

Endocrinology

Protein export in prokaryotes and eukaryotes: indications of a difference in the mechanism of exportation

J. Mol. Evol.

Primary structure and expression of a functional human glucocorticoid receptor cDNA

Nature

Prolactin binding components in rabbit mammary gland: characterization by partial purification and affinity labelling

Endocrinology