The vertebrate Aqp14 water channel is a neuropeptide-regulated polytransporter

François Chauvigné,Alba Ferré,Joan Cerdà,Per Gunnar Fjelldal,Roderick Nigel Finn,Roderick Nigel Finn,Ozlem Yilmaz

doi:10.1038/s42003-019-0713-y

Abstract

Water channels (aquaporins) were originally discovered in mammals with fourteen subfamilies now identified (AQP0-13). Here we show that a functional Aqp14 subfamily phylogenetically related to AQP4-type channels exists in all vertebrate lineages except hagfishes and eutherian mammals. In contrast to the water-selective classical aquaporins, which have four aromatic-arginine constriction residues, Aqp14 proteins present five non-aromatic constriction residues and facilitate the permeation of water, urea, ammonia, H2O2 and glycerol. Immunocytochemical assays suggest that Aqp14 channels play important osmoregulatory roles in piscine seawater adaptation. Our data indicate that Aqp14 intracellular trafficking is tightly regulated by the vasotocinergic/isotocinergic neuropeptide and receptor systems, whereby protein kinase C and A transduction pathways phosphorylate highly conserved C-terminal residues to control channel plasma membrane insertion. The neuropeptide regulation of Aqp14 channels thus predates the vasotocin/vasopressin regulation of AQP2-5-6 orthologs observed in tetrapods. These findings demonstrate that vertebrate Aqp14 channels represent an ancient subfamily of neuropeptide-regulated polytransporters.

Highlights

Water channels were originally discovered in mammals with fourteen subfamilies identified (AQP0-13)
Since we have previously shown that its genome retains the AQP13 ortholog found in Amphibia, and each of the other subfamilies reported for tetrapods, except AQP10
With the exception of AQP16, which is an Aqp8-type channel (AQP8)-type channel identified in amphibians, turtles and crocodylians, the platypus and zebrafish display each of the major divisions of aquaporin subfamilies (AQP0-15) that are representative for the two major lineages of osteichthyan vertebrates (Sarcopterygii and Actinopterygii) with the highest aquaporin gene copy numbers[16,19,20,29]

Summary

Introduction

Water channels (aquaporins) were originally discovered in mammals with fourteen subfamilies identified (AQP0-13). The vertebrate aquaporin superfamily is currently comprised of 17 subfamilies (AQP0 – 16) that are phylogenetically classified into four grades that can be traced to basal metazoan or parazoan lineages including Cnidaria (jelly fish and corals) or Porifera (sponges) This includes: classical aquaporins (AQP0, −1, −2, −4, −5, −6, −14 and 15) that primarily transport water, Aqp8-type aquaporins (AQP8 and −16) that primarily transport water, urea, ammonia and peroxide, aquaglyceroporins (AQP3, −7, −9, 10 and −13) that primarily function as water, urea and polyol transporters, and the intracellular unorthodox aquaporins (AQP11 and −12), for which functional data are mostly lacking, except for AQP11 which seems to transport water and glycerol[17,18,19,20]. No functional data exist for the novel aqp[14] gene subfamily, which has no specific annotation in available genome databases, yet is suggested to exist in a broad range of vertebrates[16]

Methods

Results

Conclusion