117 research outputs found
Subcellular Localization of Selectively Permeable Aquaporins in the Male Germ Line of a Marine Teleost Reveals Spatial Redistribution in Activated Spermatozoa
No full textIn oviparous vertebrates such as the marine teleost gilthead seabream, water and
fluid homeostasis associated with testicular physiology and the external activation of
spermatozoa is potentially mediated by multiple aquaporins. To test this hypothesis, we
isolated five novel members of the aquaporin superfamily from gilthead seabream and
developed paralog-specific antibodies to localize the cellular sites of protein expression in
the male reproductive tract. Together with phylogenetic classification, functional ..
Aquaporin splice variation differentially modulates channel function during marine teleost egg hydration
No full text22 pages, 8 figures, supporting information https://doi.org/10.1371/journal.pone.0294814.-- Data Availability: The full-length cDNAs for SaAqp1ab1-WT, HhAqp1ab1-WT and SsAqp1ab2-WT are available in GenBank under accession numbers AY626938, MW960022 and DQ889223, respectively. The full-length transcripts of SaAqp1ab1_v1, SaAqp1ab1_v2, HhAqp1ab1_v1, SsAqp1ab2_v1 and SsAqp1ab2_v2 were deposited in GenBank under accession numbers OR498208, OR498209, OR498210, OR498211 and OR498212, respectively. All relevant data are within the paper and its Supporting information filesAquaporin-mediated oocyte hydration is a developmentally regulated adaptive mechanism that co-occurs with meiosis resumption in marine teleosts. It provides the early embryos with vital water until osmoregulatory systems develop, and in the majority of marine teleosts causes their eggs to float. Recent studies have shown that the subdomains of two water channels (Aqp1ab1 and Aqp1ab2) encoded in a teleost-specific aquaporin-1 cluster (TSA1C) co-evolved with duplicated Ywhaz-like (14-3-3ζ-like) binding proteins to differentially control their membrane trafficking for maximal egg hydration. Here, we report that in species that encode the full TSA1C, in-frame intronic splice variants of Aqp1ab1 result in truncated proteins that cause dominant-negative inhibition of the canonical channel trafficking to the plasma membrane. The inhibition likely occurs through hetero-oligomerization and retention in the endoplasmic reticulum (ER) and ultimate degradation. Conversely, in species that only encode the Aqp1ab2 channel we found an in-frame intronic splice variant that results in an intact protein with an extended extracellular loop E, and an out-of frame intronic splice variant with exon readthrough that results in a truncated protein. Both isoforms cause dominant-negative enhancement of the degradation pathway. However, the extended and truncated Aqp1ab2-type variants can also partially escape from the ER to reach the oocyte plasma membrane, where they dominantly-negatively inhibit water flux. The ovarian follicular expression ratios of the Aqp1ab2 isoforms in relation to the canonical channel are lowest during oocyte hydration, but subsequently highest when the canonical channel is recycled, thus leaving the eggs endowed with >90% water. These findings suggest that the expression of inhibitory isoforms of Aqp1ab1 and Aqp1ab2 may represent a new regulatory mechanism through which the cell-surface expression and the activity of the canonical channels can be physiologically modulated during oocyte hydration in marine teleostsThis work was supported by the Spanish Ministry of Science and Innovation (MCIN/AEI/10.13039/501100011033), and the European Regional Development Fund (ERDF) “A way of making Europe" (European Union), Grant no. AGL2016-76802-R (to J.C.). A.F. was recipient of a predoctoral contract from Spanish MCIN (BES-2014-068745). R.N.F. was supported by the University of Bergen (Norway)With the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S)Peer reviewe
Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
No full text20 pages, 8 figures, supplementary material https://doi.org/10.1093/molbev/msad071.-- Data Availability: Data underlying this article are available in the article and in its online Supplementary materialAquaporin-mediated oocyte hydration is considered important for the evolution of pelagic eggs and the radiative success of marine teleosts. However, the molecular regulatory mechanisms controlling this vital process are not fully understood. Here, we analyzed >400 piscine genomes to uncover a previously unknown teleost-specific aquaporin-1 cluster (TSA1C) comprised of tandemly arranged aqp1aa-aqp1ab2-aqp1ab1 genes. Functional evolutionary analysis of the TSA1C reveals a ∼300-million-year history of downstream aqp1ab-type gene loss, neofunctionalization, and subfunctionalization, but with marine species that spawn highly hydrated pelagic eggs almost exclusively retaining at least one of the downstream paralogs. Unexpectedly, one-third of the modern marine euacanthomorph teleosts selectively retain both aqp1ab-type channels and co-evolved protein kinase-mediated phosphorylation sites in the intracellular subdomains together with teleost-specific Ywhaz-like (14-3-3ζ-like) binding proteins for co-operative membrane trafficking regulation. To understand the selective evolutionary advantages of these mechanisms, we show that a two-step regulated channel shunt avoids competitive occupancy of the same plasma membrane space in the oocyte and accelerates hydration. These data suggest that the evolution of the adaptive molecular regulatory features of the TSA1C facilitated the rise of pelagic eggs and their subsequent geodispersal in the oceanic currentsThis work was supported by the Spanish Ministry of Science and Innovation (MCIN/AEI/10.13039/501100011033), the European Regional Development Fund (ERDF) “A way of making Europe” (European Union), Grant no. AGL2016-76802-R (to J.C.), and the Norwegian Research Council (RCN) Grant no. 294768/E40 (to R.N.F). F.C. and A.F. were supported, respectively, by the “Ramon y Cajal” programe (RYC-2015-17103) and a predoctoral (BES-2014-068745) contract from Spanish MCIN. R.N.F. was also supported by the University of Bergen (Norway)With the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S)Peer reviewe
Raw RT-PCR gels images.
No full textAquaporin-mediated oocyte hydration is a developmentally regulated adaptive mechanism that co-occurs with meiosis resumption in marine teleosts. It provides the early embryos with vital water until osmoregulatory systems develop, and in the majority of marine teleosts causes their eggs to float. Recent studies have shown that the subdomains of two water channels (Aqp1ab1 and Aqp1ab2) encoded in a teleost-specific aquaporin-1 cluster (TSA1C) co-evolved with duplicated Ywhaz-like (14-3-3ζ-like) binding proteins to differentially control their membrane trafficking for maximal egg hydration. Here, we report that in species that encode the full TSA1C, in-frame intronic splice variants of Aqp1ab1 result in truncated proteins that cause dominant-negative inhibition of the canonical channel trafficking to the plasma membrane. The inhibition likely occurs through hetero-oligomerization and retention in the endoplasmic reticulum (ER) and ultimate degradation. Conversely, in species that only encode the Aqp1ab2 channel we found an in-frame intronic splice variant that results in an intact protein with an extended extracellular loop E, and an out-of frame intronic splice variant with exon readthrough that results in a truncated protein. Both isoforms cause dominant-negative enhancement of the degradation pathway. However, the extended and truncated Aqp1ab2-type variants can also partially escape from the ER to reach the oocyte plasma membrane, where they dominantly-negatively inhibit water flux. The ovarian follicular expression ratios of the Aqp1ab2 isoforms in relation to the canonical channel are lowest during oocyte hydration, but subsequently highest when the canonical channel is recycled, thus leaving the eggs endowed with >90% water. These findings suggest that the expression of inhibitory isoforms of Aqp1ab1 and Aqp1ab2 may represent a new regulatory mechanism through which the cell-surface expression and the activity of the canonical channels can be physiologically modulated during oocyte hydration in marine teleosts.</div
The Adaptive Evolution of Arthropod and Vertebrate Aquaporins: Deciphering the Differential Basis of Water Homeostasis, 2015
No full textThe epizootic caused by the Atlantic salmon louse, a caligid ectoparasitic crustacean, is a severe threat to wild and domestic salmonids. Novel therapeutic approaches to dealing with this pest are needed. The project provides an combination of molecular genetics, evolution, and potential drug targeting of invertebrate aquaporin's. For further information about ”The Adaptive Evolution of Arthropod and Vertebrate Aquaporins: Deciphering the Differential Basis of Water Homeostasis, 2015”, please contact the principal investigator
Comprehensive Transcriptome Analysis of Artemia franciscana Across Developmental Stages Using Illumina and Nanopore Sequencing [Dataset]
No full textExtremophiles evolved capacities to survive extended exposure to harsh environmental conditions such as complete desiccation (anhydrobiosis) and freezing (cryobiosis). Accumulation of the three-carbon polyhydric alcohol glycerol is commonly observed in anhydrobiotic organisms, although it is considered to preferentially enhance cryobiosis rather than anhydrobiosis. Here, using dormant stages of the halophilic extremophile crustacean Artemia franciscana, we show that this role is reversed. We find that A. franciscana and related branchiopods evolved co-opted entomoglyceroporin (Eglp)-like aquaporin-type channels previously only characterized in hexapods. Phylogenomic and site-directed mutagenesis analyses indicate that EglpL orthologs likely evolved during the early Cambrian in the common ancestor of the Pancrustacea. RNAi-mediated knockdown experiments show that the A. franciscana EglpL glycerol transporter is subfunctionally co-regulated with canonical aquaglyceroporins (Glps) to mediate glycerol accumulation in the diapause cysts. Termination of diapause using either desiccation or hydrogen peroxide and further exposure of the cysts to freezing suggest that the acquired glycerol plays a more critical role in anhydrobiosis rather than cryobiosis. These findings uncover the essential role of evolutionary divergent aquaporin-type glycerol channels in the accrual of glycerol in an anhydrobiotic organism and reveal a previously overlooked function of this polyol for desiccation toleranceSpanish Ministry of Science, Innovation and Universities (MICIU/AEI/https://doi.org/10.13039/501100011033) and the European Regional Development Fund (ERDF) “A way of making Europe” (European Union), Grant no. PID2019-103868RB-I00 (to J.C.) and PID2019-104483GB-I00 (to J.L.M.)
Agency for Management of University and Research Grants (Government of Catalonia) Grant 2021 SGR 00068 (to J.C.).
Spanish MICIU (PRE2020-092214).
University of Bergen (Norway).
Institutional support to CNAG was from the Spanish MICIU and Generalitat de Catalunya through the Departament de Recerca i Universitats and Departament de Salut.
“Severo Ochoa Centre of Excellence” accreditation (CEX2019-000928-S) funded by the Spanish Agencia Estatal de Investigación (AEI)https://doi.org/10.13039/501100011033Raw Data (FASTQ files) from samples. Count and Normalized expression matrices. DNA sequences. ERX13367886 Illumina NovaSeq 6000 paired end sequencing; ERX13367887 Illumina NovaSeq 6000 paired end sequencing; ERX13367888 Illumina NovaSeq 6000 paired end sequencing; ERX13367889 Illumina NovaSeq 6000 paired end sequencing; ERX13367891 Illumina NovaSeq 6000 paired end sequencing; ERX13367893 Illumina NovaSeq 6000 paired end sequencing; ERX13367894 Illumina NovaSeq 6000 paired end sequencing; ERX13383215 GridION sequencing; ERX13383216 GridION sequencing; ERX13383217 GridION sequencing; ERX13367896 Illumina NovaSeq 6000 paired end sequencing; ERX13367897 Illumina NovaSeq 6000 paired end sequencing; ERX13367890 Illumina NovaSeq 6000 paired end sequencing; ERX13367892 Illumina NovaSeq 6000 paired end sequencing; ERX13367895 Illumina NovaSeq 6000 paired end sequencingPeer reviewe
Aquaporin evolution in fishes
No full textAquaporins represent a primordial group of transmembrane solvent channels that have been documented throughout the living biota. This facet alone emphasizes the positive selection pressure for proteins associated with intracellular fluid homeostasis. Amongst extant Eukaryota the highest gene copy number can be found in plants and teleosts, a feature that reflects the genomic duplication history in both groups. In this minireview we discuss the discovery, structure, duplication, and diversification of the aquaporin superfamily. We focus on teleosts as the main models, but include data available for other organisms to provide a broader perspective
Vertebrate Vitellogenin Gene Duplication in Relation to the ‘‘3R Hypothesis’’: Correlation to the Pelagic Egg and the Oceanic Radiation of Teleosts
No full textThe spiny ray-finned teleost fishes (Acanthomorpha) are the most successful group of vertebrates in terms of species diversity. Their meteoric radiation and speciation in the oceans during the late Cretaceous and Eocene epoch is unprecedented in vertebrate history, occurring in one third of the time for similar diversity to appear in the birds and mammals. The success of marine teleosts is even more remarkable considering their long freshwater ancestry, since it implies solving major physiological challenges when freely broadcasting their eggs in the hyper-osmotic conditions of seawater. Most extant marine teleosts spawn highly hydrated pelagic eggs, due to differential proteolysis of vitellogenin (Vtg)-derived yolk proteins. The maturational degradation of Vtg involves depolymerization of mainly the lipovitellin heavy chain (LvH) of one form of Vtg to generate a large pool of free amino acids (FAA 150–200 mM). This organic osmolyte pool drives hydration of the ooctye while still protected within the maternal ovary. In the present contribution, we have used Bayesian analysis to examine the evolution of vertebrate Vtg genes in relation to the ‘‘3R hypothesis’’ of whole genome duplication (WGD) and the functional end points of LvH degradation during oocyte maturation. We find that teleost Vtgs have experienced a post-R3 lineage-specific gene duplication to form paralogous clusters that correlate to the pelagic and benthic character of the eggs. Neo-functionalization allowed one paralogue to be proteolyzed to FAA driving hydration of the maturing oocytes, which pre-adapts them to the marine environment and causes them to float. The timing of these events matches the appearance of the Acanthomorpha in the fossil record. We discuss the significance of these adaptations in relation to ancestral physiological features, and propose that the neo-functionalization of duplicated Vtg genes was a key event in the evolution and success of the teleosts in the oceanic environment
Genetic adaptations for the oceanic success of fish eggs
No full textGenetic adaptations of organisms living in extreme environments are fundamental to our understanding of where life can evolve. Water is the single limiting parameter in this regard, yet when released in the oceans, the single-celled eggs of marine bony fishes (teleosts) have no means of acquiring it. They are strongly hyposmotic to seawater and lack osmoregulatory systems. Paradoxically, modern teleosts successfully release vast quantities of eggs in the extreme saline environment and recorded the most explosive radiation in vertebrate history. Here, we highlight key genetic adaptations that evolved to solve this paradox by filling the pre-ovulated eggs with water. The degree of water acquisition is uniquely prevalent to marine teleosts, permitting the survival and oceanic dispersal of their eggs
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