Prolactin and teleost ionocytes: New insights into cellular and molecular targets of prolactin in vertebrate epithelia

Abstract

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.

Hormonal regulation of aquaporin 3: opposing actions of prolactin and cortisol in tilapia gill

“…In the pituitary, cortisol inhibits Prl release within minutes via nongenomic mechanisms (Borski et al 1991). Recent advances in our understanding of how the teleost gill operates at the molecular level have provided the fodder for identifying novel, and conserved, hormone targets (Breves et al 2014a, Guh et al 2015. For example, the connection between Prl and Ncc first identified in the tilapia gill has been recently found to operate in mouse and rat kidney.…”

clc-2c is regulated by salinity, prolactin and extracellular osmolality in tilapia gill

“…Only recently have gene targets of Prl been identified which underlie discreet solute and water handling processes. These transcriptional targets encode ion transporters/channels, Na + /K + -ATPase subunits, aquaporins and tight-junction proteins (Breves et al 2014a). …”

Histological and hormonal changes in the European eel (Anguilla anguilla) after exposure to environmental cocaine concentration

“…In teleosts, prolactin (PRL) plays an important role in osmotic regulation in fresh water. It regulates ion and water movements in intestine, skin, gills, kidney and urinary bladder and stimulates mucus secretion by skin, intestine and gill (Norris ; Breves, McCormick & Karlstrom ). Moreover, in fish, PRL is involved in epithelial cell proliferation (Sakamoto & McCormick ; Takahashi, Takahashi & Sakamoto ; Takahashi et al .…”