Plasma proteome profiling of freshwater and seawater life stages of rainbow trout (Oncorhynchus mykiss)

Morro, Bernat; Doherty, Mary K.; Balseiro, Pablo; Handeland, Sigurd O.; Mackenzie, Simon; Sveier, Harald; Albalat, Amaya

doi:10.1371/journal.pone.0227003

Cited by 18 publications

(8 citation statements)

References 117 publications

(132 reference statements)

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“…( 17 )). Recent work has applied such approaches in salmonids ( 18 ), including to document changes in plasma protein abundance during sea water adaptation in rainbow trout ( 19 ). Such approaches require a comprehensive protein database for the target species and enable simultaneous identification and quantification of hundreds to thousands of proteins per experiment ( 20 – 23 ).…”

Section: Introductionmentioning

confidence: 99%

Plasma Proteome Responses in Salmonid Fish Following Immunization

et al. 2020

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Vaccination plays a critical role in the protection of humans and other animals from infectious diseases. However, the same vaccine often confers different protection levels among individuals due to variation in genetics and/or immunological histories. While this represents a well-recognized issue in humans, it has received little attention in fish. Here we address this knowledge gap in a proteomic study of rainbow trout ( Oncorhynchus mykiss , Walbaum), using non-lethal repeated blood sampling to establish the plasma protein response of individual fish following immunization. Six trout were immunized with adjuvanted hen egg-white lysozyme (HEL) and peripheral blood sampled at ten time points from day 0 to day 84 post-injection. We confirm that an antigen-specific antibody response to HEL was raised, showing differences in timing and magnitude among individuals. Using label-free liquid chromatography-mass spectrometry, we quantified the abundance of 278 plasma proteins across the timecourse. As part of the analysis, we show that this approach can distinguish many (but not all) duplicated plasma proteins encoded by paralogous genes retained from the salmonid-specific whole genome duplication event. Global variation in the plasma proteome was predominantly explained by individual differences among fish. However, sampling day explained a major component of variation in abundance for a statistically defined subset of 41 proteins, representing 15% of those detected. These proteins clustered into five groups showing distinct temporal responses to HEL immunization at the population level, and include classical immune (e.g. complement system members) and acute phase molecules (e.g. apolipoproteins, haptoglobins), several enzymes and other proteins supporting the immune response, in addition to evolutionarily conserved molecules that are as yet uncharacterized. Overall, this study improves our understanding of the fish plasma proteome, provides valuable marker proteins for different phases of the immune response, and has implications for vaccine development and the design of immune challenge experiments.

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Section: Introductionmentioning

confidence: 99%

Plasma Proteome Responses in Salmonid Fish Following Immunization

et al. 2020

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“…Even if previous studies have shown gene expression changes when fish adapt to water salinity change (e.g. migration, precipitation) for salmonids (Morro, 2020;Norman et al, 2014) and other species (Fiol, 2006;Pujante, 2018), evidence of such an impact of low water salinity on the overall ovulatory process were, to our knowledge, previously unreported. This raises the question of how low water salinity can inhibit the overall ovulatory process and not only osmotic exchanges.…”

Section: Inflammation-related Genes Are Under-expressed In Low Salinity Watermentioning

confidence: 68%

Effect of a low water concentration in chloride, sodium and potassium on oocyte maturation, oocyte hydration, ovulation and egg quality in rainbow trout

Segret

Cardona

Skiba‐Cassy

et al. 2021

Preprint

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Water salinity is an important environmental factor known to have detrimental effects on salmonid reproduction, mostly when migrating female broodfish are held in sea water. In contrast, data obtained in freshwater are scarce and the impact of low water salinity during reproduction in freshwater is currently unknown. For this reason, and because ion and water fluxes are critical for the final steps of the female gamete formation, including oocyte hydration and ovulation, the aim of the present study was to investigate the impact of low salinity water on final oocyte maturation, ovulation and, ultimately, on egg quality, using rainbow trout as a physiological model and relevant aquaculture species. Fish from the same commercial strain were raised throughout their lifecycle either in a site characterized by low concentrations of Na+, K+, and Cl- ions in the water or in a closely located control site exhibiting standard salinity levels. Egg quality and duration of final oocyte maturation were investigated using innovative phenotyping tools such as automatic assessment of egg viability using the VisEgg system and non-invasive echograph-based monitoring of final oocyte maturation duration, respectively. Oocyte hydration during final oocyte maturation and after ovulation was also investigated. Finally, molecular phenotyping was performed using real-time PCR-based monitoring of several key players of final oocyte maturation and ovulation associated with ion and water transport, inflammation, proteolytic activity, and coagulation. Oocyte hydration and gene expression data were analyzed in the light of the duration of final oocyte maturation. Here we show that low water salinity negatively influences final oocyte maturation, ovulation and, ultimately, egg quality. Low water salinity triggers delayed ovulation and lower oocyte viability. When investigating the impact of low water salinity on final oocyte maturation duration, individuals presenting the most severe phenotypes exhibited impaired oocyte hydration and abnormally reduced gene expression levels of several key players of the ovulatory process. While the under expression of water (e.g., aquaporins) and ion (e.g., solute carriers) transporters is consistent with impaired oocyte hydration, our observations also indicate that the entire ovulatory gene expression program is disrupted. Our results raise the question of the mechanisms underlying the negative influence of low salinity water on the dynamics of the preovulatory phase, on the control of the oocyte homeostasis, including hydration, and on the overall success of the maturation-ovulation process.

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“…To overcome these limitations, in this study we applied MS-based proteomics to nurse shark plasma to identify the proteins present and quantify abundance changes following immunization. Most proteomic studies rely upon an annotated, species-matched genome as the reference database for protein identification (e.g., 13 , 14 , 27 ). As the nurse shark genome has yet to be sequenced, we compared two alternate approaches for protein identification.…”

Section: Discussionmentioning

confidence: 99%

“…Our previous immunization study on rainbow trout ( Oncorhynchus mykiss ), also using LC-MS/MS proteomics ( 14 ), identified abundance changes in 278 plasma proteins, including both classical immune proteins (e.g., complement components) and proteins not usually associated with immune responses in mammals (e.g., apolipoproteins). A separate study by Morro and colleagues ( 27 ) identified a greater number of plasma proteins (1822) in rainbow trout using LC-MS/MS label-free proteomics in combination with enrichment of low abundance proteins. We therefore hypothesized that the approach used in our previous study would yield similar results in terms of the number and types of immune proteins detected in nurse shark.…”

Section: Introductionmentioning

confidence: 99%

Exploration of the Nurse Shark (Ginglymostoma cirratum) Plasma Immunoproteome Using High-Resolution LC-MS/MS

et al. 2022

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Many animals of scientific importance lack species-specific reagents (e.g., monoclonal antibodies) for in-depth studies of immune proteins. Mass spectrometry (MS)-based proteomics has emerged as a useful method for monitoring changes in protein abundance and modifications in non-model species. It can be used to quantify hundreds of candidate immune molecules simultaneously without the generation of new reagents. Here, we used MS-based proteomics to identify and quantify candidate immune proteins in the plasma of the nurse shark (Ginglymostoma cirratum), a cartilaginous fish and representative of the most basal extant vertebrate lineage with an immunoglobulin-based immune system. Mass spectrometry-based LC-MS/MS was performed on the blood plasma of nurse sharks immunized with human serum albumin (n=4) or sham immunized (n=1), and sampled at days 0 (baseline control), 1, 2, 3, 5, 7, 14, 21, 28, 25, 42 and 49. An antigen-specific antibody response was experimentally confirmed post-immunization. To provide a high-quality reference to identify proteins, we assembled and annotated a multi-tissue de novo transcriptome integrating long- and short-read sequence data. This comprised 62,682 contigs containing open reading frames (ORFs) with a length >80 amino acids. Using this transcriptome, we reliably identified 626 plasma proteins which were broadly categorized into coagulation, immune, and metabolic functional groups. To assess the feasibility of performing LC-MS/MS proteomics in nurse shark in the absence of species-specific protein annotations, we compared the results to an alternative strategy, mapping peptides to proteins predicted in the genome assembly of a related species, the whale shark (Rhincodon typus). This approach reliably identified 297 proteins, indicating that useful data on the plasma proteome may be obtained in many instances despite the absence of a species-specific reference protein database. Among the plasma proteins defined against the nurse shark transcriptome, fifteen showed consistent changes in abundance across the immunized shark individuals, indicating a role in the immune response. These included alpha-2-macroglobulin (A2M) and a novel protein yet to be characterized in diverse vertebrate lineages. Overall, this study enhances genetic and protein-level resources for nurse shark research and vastly improves our understanding of the elasmobranch plasma proteome, including its remodelling following immune stimulation.

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Plasma proteome profiling of freshwater and seawater life stages of rainbow trout (Oncorhynchus mykiss)

Cited by 18 publications

References 117 publications

Plasma Proteome Responses in Salmonid Fish Following Immunization

Plasma Proteome Responses in Salmonid Fish Following Immunization

Effect of a low water concentration in chloride, sodium and potassium on oocyte maturation, oocyte hydration, ovulation and egg quality in rainbow trout

Exploration of the Nurse Shark (Ginglymostoma cirratum) Plasma Immunoproteome Using High-Resolution LC-MS/MS

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