Claudins of sea lamprey (Petromyzon marinus) – organ‐specific expression and transcriptional responses to water of varying ion content

Abstract

The role of lamprey epithelium tight junctions (TJs) in the regulation of salt and water balance is poorly understood. This study reported on claudin (Cldn) TJ protein transcripts of pre‐metamorphic larval and post‐metamorphic juvenile sea lamprey (Petromyzon marinus) and the transcriptional response of genes encoding Cldns to changed environmental ion levels. Transcripts encoding Cldn‐3b, ‐4, ‐5, ‐10, ‐14, ‐18 and ‐19 were identified, and mRNA expression profiles revealed the organ‐specific presence of cldn‐5 and ‐14, broad expression of cldn‐3b, ‐4, ‐10, ‐18 and ‐19 and spatial differences in the mRNA abundance of cldn‐4, ‐3b and ‐14 along the ammocoete intestine. Expression profiles were qualitatively similar in ammocoetes and juvenile fishes. Transcript abundance of genes encoding Cldns in osmoregulatory organs (gill, kidney, intestine and skin) was subsequently investigated after exposure of ammocoetes to ion‐poor water (IPW) and juveniles to hyperosmotic conditions [60% sea water (SW)]. IPW‐acclimated ammocoetes increased mRNA abundance of nearly all cldns in the gill. Simultaneously, cldn‐10 abundance increased in the skin, whereas cldn‐4, ‐14 and ‐18 decreased in the kidney. Ammocoete cldn mRNA abundance in the intestine was altered in a region‐specific manner. In contrast, cldn transcript abundance was mostly downregulated in osmoregulatory organs of juvenile fish acclimated to SW – cldn‐3b, ‐10 and ‐19 in the gill; cldn‐3b, ‐4, ‐10 and ‐19 in the skin; cldn‐3b in the kidney; and cldn‐3b and ‐14 in the intestine. Data support the idea that Cldn TJ proteins play an important role in the osmoregulatory physiology of pre‐ and post‐metamorphic sea lamprey and that Cldn participation can occur across organs, in an organ‐specific manner, as well as differ spatially within organs, which contributes to the regulation of salt and water balance in these fishes.

11-Deoxycortisol controls hydromineral balance in the most basal osmoregulating vertebrate, sea lamprey (Petromyzon marinus)

“…It is known that tight junction (TJ) complexes dynamically control paracellular permeability in many vertebrate epithelia, including changes in gill epithelium of teleost fishes from “tight” in FW to “leaky” in SW 35 . A functional role for TJ complex proteins has more recently been elucidated in the sea lamprey 35 – 38 . Several studies have demonstrated putative corticosteroid control of TJ proteins in cultured teleost fish gill epithelia 24 , 39 , 40 , and it is possible that S may thus also control TJ complexing and paracellular permeability in the sea lamprey gill, in addition to its role in controlling active ion transport.…”

Genomic insights into the seawater adaptation in Cyprinidae

“…3A). Previous studies have provided evidence identifying the ocln gene as an osmoregulation-related gene in Acipenser baerii [51], while the cldn19 gene played significant roles in osmoregulatory physiology of Petromyzon marinus [52]. Moreover, the PSG cldn10, which predominantly expressed in osmoregulatory organs of teleost fishes [38,53], was found have two specific AA replacements in the two Pseudaspius species (Additional file 2: Figure S6A).…”

Transport and Barrier Functions in Rainbow Trout Trunk Skin Are Regulated by Environmental Salinity

“…Certain claudin-10 isoforms are thought to provide the paracellular pathway with cation selective pores, which facilitate ion efflux in SW (Marshall et al, 2018). However, Kolosov et al (2020) recently demonstrated that claudin-10 is downregulated following SW acclimation in the lamprey, indicating that the contribution of claudins to epithelial barrier function may be species dependent.…”