Endocrine regulation of prolactin cell function and modulation of osmoreception in the Mozambique tilapia
Introduction
The structure and function of the macromolecules that carry on the business of life are maintained by weak forces, that is, hydrogen bonds and hydrophobic interactions. For this reason, they are highly vulnerable to small changes in their osmotic environment. The ability to detect and respond to changes in osmolality is, therefore, foundational to life for both unicellular and multicellular organisms. Endocrine osmoreceptors are typically controlled directly by the parameter they regulate: solute concentration (Grau and Borski, 1994, Seale et al., 2012c, Verbalis, 2007). In euryhaline teleost fish, such as Mozambique tilapia (Oreochromis mossambicus), this osmotic reflex is exemplified by the regulation of prolactin (PRL). Prolactin activates target cells by interacting with a pair of single-transmembrane domain receptors that are linked to the Janus kinase/signal transducers and activators of transcription (JAK/STAT) pathway (Brooks, 2012, Freeman et al., 2000). In tilapia, there are two PRL isoforms that are the sole products of the cells of the rostral pars distalis (RPD) of the pituitary gland, hereafter referred to as PRL cells, which are encoded by separate genes (Rentier-Delrue et al., 1989, Specker et al., 1985, Yamaguchi et al., 1988). The two PRLs, designated PRL177 and PRL188, possess similar activity in an osmoregulation-based bioassay (Specker et al., 1985) but have been found to be differentially osmosensitive, with PRL188 responding more robustly to a fall in extracellular osmolality than PRL177 (Borski et al., 1992, Seale et al., 2002a). Furthermore, PRL177, but not PRL188, possesses somatotropic activity (Shepherd et al., 1997). While PRL expression has also been described in peripheral tissues of several teleosts (Imaoka et al., 2000, Sakamoto et al., 2005, Santos et al., 1999, Zhang et al., 2004), including the Mozambique tilapia (Yada et al., 2002), the regulation and relative contribution of non-pituitary PRL to physiological processes in fish remain to be fully investigated. On the other hand, the importance of pituitary PRL for survival in fresh water (FW), is clear and was first determined by Pickford and Phillips (1959) who found that PRL injection prevented death in FW fish after hypophysectomy. Such restorative ability, which is also found in Mozambique tilapia (Breves et al., 2010c, Dharmamba, 1970, Young et al., 1988), has been largely attributed to PRL’s hyperosmoregulatory actions on epithelial cells (Brown and Brown, 1987, Hirano, 1986, McCormick and Bradshaw, 2006). In branchial ionocytes, PRL induces ionic uptake via the Na+/Cl− co-transporter (NCC) (Breves et al., 2010c). Prolactin cells are directly sensitive to small, physiologically relevant, changes in extracellular osmolality in vitro (Grau and Borski, 1994, Grau et al., 1981, Nagahama et al., 1975, Seale et al., 2002b, Seale et al., 2005). Circulating levels of PRL are elevated in FW tilapia, a response that does not require hypothalamic mediation (Seale et al., 2012a, Seale et al., 2012b, Shepherd et al., 1999, Yada et al., 1994). In vitro, small, physiologically appropriate, decreases in extracellular osmolality elicit significant changes in PRL release from intact pituitaries and dispersed PRL cells alike (Grau et al., 1981, Seale et al., 2002b, Seale et al., 2006a). In a hyposmotic environment, the osmotic gradient across the cell membrane leads to a rise in PRL cell volume via a membrane-bound aquaporin channel (AQP3) (Watanabe et al., 2009, Weber et al., 2004). This rise initiates an influx of extracellular Ca2+ through the stretch-activated channel, transient receptor potential vanilloid 4 (TRPV4), producing an increase in intracellular Ca2+ which stimulates PRL release (Seale et al., 2003a, Seale et al., 2003b, Seale et al., 2004, Seale et al., 2012b, Watanabe et al., 2012). Thus, the tilapia PRL cell is an osmoreceptor by virtue of its intrinsic osmosensitivity and its ability to transduce a change in extracellular osmolality into the release of a hormone that is critical to FW osmoregulation (Grau and Helms, 1990, Grau and Borski, 1994, Sakamoto et al., 2005, Seale et al., 2006b, Seale et al., 2012c). The response of PRL cells to a fall in extracellular osmolality and to endocrine modulation, and the actions of both PRLs on target cells, are summarized in Fig. 1.
Other cell types share the characteristics that define osmoreceptors, but experimental approaches involving other osmoreceptors of known cellular identity and measurable output have been limited by virtue of their complex morphology and anatomical arrangement (e.g., vasopressinergic neurons (Bourque and Oliet, 1997, Oliet and Bourque, 1993). Studies investigating the mechanisms underlying PRL cell osmoreception in tilapia have greatly benefited by their anatomical arrangement: PRL cells can be easily isolated and studied in vitro (Grau and Helms, 1989, Seale et al., 2005), as they are located in a homogeneous tissue comprising >99% of the RPD of the pituitary (Nishioka et al., 1988). Furthermore, the tilapia PRL cell model allows the estimation of gene expression and hormone secretion simultaneously (Seale et al., 2012a).
We have recently reported that PRL cell responsiveness is directly sensitive to salinity (Seale et al., 2012a). Hyposmotically-induced PRL release is more robust in cells of fish acclimated to FW than in those from tilapia acclimated to seawater (SW). For reasons that will be discussed below, PRL mRNA levels are only found to rise during hyposmotic stimulation in SW-acclimated fish (Seale et al., 2012a, Seale et al., 2012c). Expression of TRPV4 is also osmosensitive, increasing as extracellular osmolality rises (Seale et al., 2012b). Prolactin’s actions are not limited to salt and water homeostasis, and its control is not limited to environmental factors. Over 300 distinct actions of PRL have been described among vertebrates (Manzon, 2002). Although the dependence on PRL for FW osmoregulation varies among teleosts according to life history (Bentley, 1998), in Mozambique tilapia and other euryhaline teleost fishes, the indispensable action of PRL is osmoregulation (Brown and Brown, 1987, Clarke and Bern, 1980, Hirano, 1986, Manzon, 2002, McCormick, 2001, McCormick and Bradshaw, 2006, Sakamoto and McCormick, 2006). Additional roles of PRL seen in tilapia include parental behavior (Blum and Fiedler, 1965, Summers and Zhu, 2008), sexual maturation (Tacon et al., 2000) and growth (Shepherd et al., 1997). The functional versatility of this hormone across vertebrate species or within a given species suggests a highly complex pattern of regulation. In fact, direct innervation of the RPD by hypothalamic neurons attests to a high degree of control exercised by the brain (Bern et al., 1975, Grau et al., 1985). Not surprisingly then, a multitude of neuroendocrine factors have been shown to modulate PRL release in tilapia (reviewed in Kawauchi et al. (2009)). To date, twenty hormonal modulators, of hypothalamic and extra-hypothalamic origin, have been shown to affect PRL release or PRL mRNA levels of Mozambique tilapia (Table 1). The regulation of PRL cells, therefore, is likely to result from the intricate interaction between direct osmotic and endocrine control of PRL synthesis and release.
Section snippets
Peptides
A hypothalamic factor that specifically stimulates the release of PRL, PRL-releasing peptide (PrRP), was first identified in mammals as an endogenous ligand for a G protein-coupled receptor (GPCR) (Hinuma et al., 1998). The two isoforms of this peptide, PrRP20 and PrRP31, are effective in increasing plasma PRL levels and stimulating PRL release from dispersed pituitary cells of rats (Hinuma et al., 1998, Matsumoto et al., 1999, Tokita et al., 1999). A homologue of PrRP20, designated Carassius
Extra-hypothalamic factors
Angiotensin II (ANG II), a potent dipsogenic and hypertensive hormone, and the principal biologically active product of the renin-angiotensin system (RAS) in all vertebrates (Kobayashi and Takei, 1996, Takei, 2000), has a multiplicity of actions. It is a potent pressor agent acting directly through vasoconstrictor actions and through the stimulation of the sympathoadrenal system, both centrally and peripherally, as well as through inhibition of vagal control of heart rate. While ANG II appears
Cross-talk between osmoreception and the hormonal regulation of tilapia PRL cells
As described above, tilapia PRL cells are regulated by a variety of factors involved in physiological processes including hydromineral balance, growth and metabolism, stress and immune responses, and reproduction. The presence of multiple regulators of PRL synthesis and release underlines the pervasive importance of this hormone in vertebrate physiology and suggests a diversity of signal transduction pathways available in this cell type.
Because the tilapia PRL cell is an osmoreceptor, which
Acknowledgments
Over the course of more than 30 years the work of the Grau laboratory referenced herein was funded by grants from the National Science Foundation (NSF), including IOS-0517769, OISE-0852518 and IOS-1119693, Essential support has also been provided by numerous grants from the Edwin W. Pauley Foundation, The University of Hawaii Sea Grant College Program, The Binational Agricultural Research Development Fund, and the United States Department of Agriculture’s (USDA) Agriculture and Food Research
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