Urotensin II and its receptor in the killifish gill: regulators of NaCl extrusion

Abstract

SUMMARYThe peptide urotensin II (UII) and its receptor (UT) mediate cardiovascular and renal effects in both mammals and fishes. In both groups, vasopressor and diuretic responses predominate, although, in mammals, some secondary vasodilatation is found, mediated by secondary release of nitric oxide or prostacyclin. In fishes, gill extrusion of NaCl is inhibited by UII, but a single study has determined that UT is expressed in gill vasculature, not on the epithelium that mediates the transport. To begin to clarify the pathways involved in UII inhibition of gill transport, we have cloned the cDNA encoding UII and UT from the euryhaline killifish (Fundulus heteroclitus L.) gill and spinal cord, quantified UT mRNA expression in various tissues and measured relative expression in gill tissue from fish acclimated to seawater (SW) vs fresh water (FW). We have also localized UT in the gill epithelium, and measured the effect of UII on ion transport across the opercular epithelium. We found that both UII and UT are synthesized in the gill of F. heteroclitus and that gill UT mRNA levels are ~80% higher in SW-vs FW-acclimated individuals. In addition, UII inhibits NaCl transport across the opercular epithelium in a concentration-dependent manner, and this inhibition is at least partially mediated by both nitric oxide and a prostanoid. Supplementary material available online at

International Union of Basic and Clinical Pharmacology. XCII. Urotensin II, Urotensin II–Related Peptide, and Their Receptor: From Structure to Function

“…In the European flounder and the killfish Fundulus heteroclitus, UT mRNA is expressed in heart, ovary, bladder, kidney, pituitary, and gill (Lu et al, 2006;Evans et al, 2011). In the flounder and the grouper, UT-like immunoreactivity is evident in vascular elements irrigating osmoregulatory tissues such as kidney glomeruli and collecting ducts and the primary and secondary lamellae of the gill (Lu et al, 2006;Sun et al, 2014).…”

AVT and IT regulate ion transport across the opercular epithelium of killifish (Fundulus heteroclitus) and gilthead sea bream (Sparus aurata)

“…When the membrane is removed and mounted in Ussing chambers, the short circuit current is equivalent to Cl − secretion rates and provides an accessible model to circumvent gill cell culture. In this way, the regulatory action of several endocrine/neuroendocrine factors (stimulatory actions of atriopeptin II (Scheide and Zadunaisky, 1988), as well as inhibitory actions of urotensin II (Marshall and Bern, 1979;Evans et al, 2011), nitric oxide (Evans et al, 2004) or cathecholamines (Marshall et al, 1993)) has been established using the opercular membrane of killifish.…”

UII and UT in grouper: cloning and effects on the transcription of hormones related to growth control

“…In mammals, both UII and UT are widely expressed in the CNS and various peripheral tissues (Onan et al 2004, Malagon et al 2008. UII has been cloned from many fish species, such as flounder (Lu et al 2006), killifish (Evans et al 2011), and eels (Nobata et al 2011). Although the caudal neurosecretory system (CNSS) is the major site of UII expression, as in mammals, UII is also widely expressed in the CNS, such as in the optic nerve, different parts of the brain, hypothalamus, pituitary, and spinal cord, and in peripheral tissues, including gill, head kidney, kidney, bladder, stomach, intestine, rectum, heart, spleen, liver, and ovary (Lu et al 2006, Evans et al 2011.…”

“…UII has been cloned from many fish species, such as flounder (Lu et al 2006), killifish (Evans et al 2011), and eels (Nobata et al 2011). Although the caudal neurosecretory system (CNSS) is the major site of UII expression, as in mammals, UII is also widely expressed in the CNS, such as in the optic nerve, different parts of the brain, hypothalamus, pituitary, and spinal cord, and in peripheral tissues, including gill, head kidney, kidney, bladder, stomach, intestine, rectum, heart, spleen, liver, and ovary (Lu et al 2006, Evans et al 2011. The mRNA expression of UT has been identified in the CNSS, CNS, and different peripheral tissues of fish (Lu et al 2006, Evans et al 2011.…”

“…Although UII was first isolated from fish more than 30 years ago (Pearson et al 1980), the study of the physiological functions of the UII/UT system in fish is far behind that in mammals. In addition to the studies on the roles of UII in smooth-muscle contraction (Bern et al 1985), cardiovascular activity (Le Mevel et al 2008, Nobata et al 2011, and locomotor activity (Le Mevel et al 2008), most of the studies on fish have focused on its osmoregulatory functions (Vaudry et al 2010), such as its inhibitory effects on prolactin release in tilapia (Seale et al 2013) and NaCl transport across the opercular epithelium in killifish (Evans et al 2011). However, to the best of our knowledge, a study similar to that conducted on the role of UII as an autocrine/paracrine growth factor in mammals has not been carried out yet in fish.…”