Expansion of fish CCL20_like chemokines by genome and local gene duplication: Characterisation and expression analysis of 10 CCL20_like chemokines in rainbow trout (Oncorhynchus mykiss)

Liu, Fuguo; Wang, Tingyu; Hu, Yeh-Fang; Tian, Guangming; Secombes, Christopher J.; Wang, Tiehui

doi:10.1016/j.dci.2019.103502

Cited by 21 publications

(4 citation statements)

References 67 publications

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“…Many of the genes present in the high diversity regions belong to the innate immune system, an observation consistent with the fact that in fish, defense mechanisms against pathogens are skewed towards innate immunity (Magnadóttir 2006; Uribe et al 2011), while in mammals, adaptive immune responses are more important for immune protection (Litman et al 2010; Han et al 2020b). Previous studies have also noted lineage/species-specific gene family expansions of genes involved in innate immunity in teleosts relative to other vertebrates, and related these expansions to the evolutionary success of the teleost lineage; this includes genes for complement factors (Najafpour et al 2020), toll-like receptors ( TLR ) (Star et al 2011; Solbakken et al 2016), novel immune-type receptor ( NITR ) (Desai et al 2008; Ferraresso et al 2009), NACHT-domain and leucine-rich-repeat-containing ( NLR ) (Howe et al 2016; Suurväli et al 2022), tripartite motif proteins ( TRIM ) (Boudinot et al 2011; Suurväli et al 2022), CC chemokines (Liu, Tingyu Wang, et al 2020) and interferons (Liu, Tiehui Wang, et al 2020). Our observations demonstrate that immune-related gene families also have experienced rapid and dynamic evolution in the two sister species of herring studied here.…”

Section: Discussionmentioning

confidence: 99%

Copy number variation and elevated genetic diversity at immune trait loci in Atlantic and Pacific herring

Mohamadnejad Sangdehi,

Jamsandekar,

Enbody

et al. 2023

Preprint

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Atlantic and Pacific herring are sister species that diverged about 2 million years ago. Here we describe a genome comparison of the two species that reveal high genome-wide differentiation as expected for two distinct species but with islands of remarkably low genetic differentiation as measured by anFSTanalysis. However, this is not caused by low interspecies sequence divergence but an exceptionally high estimated intraspecies nucleotide diversity. These high diversity regions are not enriched for repeats but are highly enriched for immune trait-related genes. This enrichment includes classical immunity genes, such as immunoglobulin, T-cell receptor and major histocompatibility complex genes, but also a substantial number of genes with a role in the innate immune system. An analysis of long-read based assemblies from two Atlantic herring individuals revealed extensive copy number variation at these genomic regions, indicating that the elevated intraspecies nucleotide diversities was partially due to the cross-mapping of short reads. This study demonstrates that copy number expansion and variation is a characteristic feature of immune trait loci in herring and that this genetic diversity is likely to contribute to resistance to infectious diseases in extremely abundant species, such as the Atlantic and Pacific herring. Another important implication is that these loci are blind spots in classical genome-wide screens for genetic differentiation using short-read data, not only in herring, likely also in other species harboring qualitatively similar variation at immune trait loci.SignificanceThis study has revealed an extensive copy number variation and high nucleotide diversity at genes related to the immune system in Atlantic herring. Our analysis of previously published data in teleost species indicate that this is probably a widespread pattern among vertebrates. We also document that population genetic parameters estimated using short-read sequencing data are unreliable for these regions due to their complexity. They will also appear as blind spots in genome scans for regions of genetic differentiation based onFSTstatistics due to the very high within population nucleotide diversity. We show how long-read data can be used to decipher the gene organization and genetic diversity at these regions.

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Section: Discussionmentioning

confidence: 99%

Copy number variation and elevated genetic diversity at immune trait loci in Atlantic and Pacific herring

Mohamadnejad Sangdehi,

Jamsandekar,

Enbody

et al. 2023

Preprint

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“…ccl19 is a chemokine known to orchestrate the migration of dendritic cells (DCs) and T cells into lymphoid tissue or vaccination sites and is also involved in immune tolerance and inflammatory responses [ 74 , 75 ]. ccl20 attracts lymphocytes and DCs towards epithelial cells to mucosal immune sites under inflammatory conditions [ 76 ]. In orally immunized compared to larvae who had been orally mock immunized, there was a significant increase in levels of ccl19 and ccl20 at 2 wpi, while there was a significant decrease in ccl20 levels at 4 wpi ( Figure 5 B and Figure S7B ).…”

Section: Discussionmentioning

confidence: 99%

Oral Immunization of Larvae and Juvenile of Lumpfish (Cyclopterus lumpus) against Vibrio anguillarum Does Not Influence Systemic Immunity

et al. 2021

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Vibrio anguillarum, a marine bacterial pathogen that causes vibriosis, is a recurrent pathogen of lumpfish (Cyclopterus lumpus). Lumpfish is utilized as a cleaner fish in the Atlantic salmon (Salmo salar) aquaculture in the North Atlantic region because of its ability to visualize and prey on the ectoparasite sea lice (Lepeophtheirus salmonis) on the skin of Atlantic salmon, and its performance in cold environments. Lumpfish immunity is critical for optimal performance and sea lice removal. Oral vaccine delivery at a young age is the desired method for fish immunization because is easy to use, reduces fish stress during immunization, and can be applied on a large scale while the fish are at a young age. However, the efficacy of orally delivered inactivated vaccines is controversial. In this study, we evaluated the effectiveness of a V. anguillarum bacterin orally delivered to cultured lumpfish and contrasted it to an intraperitoneal (i.p.) boost delivery. We bio-encapsulated V. anguillarum bacterin in Artemia salina live-feed and orally immunized lumpfish larvae. Vaccine intake and immune response were evaluated by microscopy and quantitative polymerase chain reaction (qPCR) analysis, respectively. qPCR analyses showed that the oral immunization of lumpfish larvae resulted in a subtle stimulation of canonical immune transcripts such as il8b, il10, igha, ighmc, ighb, ccl19, ccl20, cd8a, cd74, ifng, and lgp2. Nine months after oral immunization, one group was orally boosted, and a second group was both orally and i.p. boosted. Two months after boost immunization, lumpfish were challenged with V. anguillarum (7.8 × 105 CFU dose−1). Orally boosted fish showed a relative percentage of survival (RPS) of 2%. In contrast, the oral and i.p. boosted group showed a RPS of 75.5% (p < 0.0001). V. anguillarum bacterin that had been orally delivered was not effective in lumpfish, which is in contrast to the i.p. delivered bacterin that protected the lumpfish against vibriosis. This suggests that orally administered V. anguillarum bacterin did not reach the deep lymphoid tissues, either in the larvae or juvenile fish, therefore oral immunization was not effective. Oral vaccines that are capable of crossing the epithelium and reach deep lymphoid tissues are required to confer an effective protection to lumpfish against V. anguillarum

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“…Ccl19 is a regulator of the induction of T-cell activation, immune tolerance, and in ammatory responses during continuous immune surveillance, homeostasis, and development (Bjørgen et al, 2019). Teleosts ccl20 molecules generally highly expressed in mucosal related tissues and involved in mucosal immunity (Liu et al, 2020). Chemokine receptors CXCR4 and CXCR5 are indispensable to reactions of germinal centers in humans , which are the sites of antibody-mediated adaptative immunity (Weber, 2018).…”

Section: Immune Response To Hypoxia Challenge In Gillsmentioning

confidence: 99%

Mechanisms of acclimation to chronic intermittent hypoxia in the gills of Largemouth bass (Micropterus salmoides)

Liu,

Wang,

et al. 2023

Preprint

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Anthropogenically induced hypoxia in water bodies has been a stressor for fish for many years and is expected to persist in the future. In order to investigate the acclimation response of fish gills to chronic intermittent hypoxia (CIH) stress, we conducted a study using largemouth bass (Micropterus salmoides) exposed to intermittent hypoxia (dissolved oxygen level: 2.0 mg·L− 1) for either one or three hours per day, over a period of 8 weeks. Our findings indicate that exposure to CIH induced remodeling of the gills and an increase in gill surface area. We also observed significant up-regulation of genes related to glycolysis (fba, pgam1, pepck, atp-pfk, pfk-2, g6pi, gapd-1, and pk), while genes associated with cholesterol synthesis (3β-hsd, cyp51, dsdr-x1, dsdr, and dhcr7) were down-regulated following CIH exposure. Furthermore, we observed the presence of elongated megamitochondria in mitochondria-rich cells within the gills of fish exposed to hypoxia. Additionally, numerous genes involved in calcium signaling pathways were up-regulated in the gills of largemouth bass, suggesting an enhanced sensitivity of gills to environmental cues in hypoxia conditions. However, the expression levels of certain genes related to innate and adaptive immune responses were inhibited following CIH exposure. Moreover, the number of mucous cells decreased, potentially making the gills more susceptible to pathogen infections. These findings highlight the potential vulnerability of gills to pathogenic organisms in the presence of CIH. Overall, our study contributes to a better understanding of how fish acclimate to CIH.

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Expansion of fish CCL20_like chemokines by genome and local gene duplication: Characterisation and expression analysis of 10 CCL20_like chemokines in rainbow trout (Oncorhynchus mykiss)

Cited by 21 publications

References 67 publications

Copy number variation and elevated genetic diversity at immune trait loci in Atlantic and Pacific herring

Copy number variation and elevated genetic diversity at immune trait loci in Atlantic and Pacific herring

Oral Immunization of Larvae and Juvenile of Lumpfish (Cyclopterus lumpus) against Vibrio anguillarum Does Not Influence Systemic Immunity

Mechanisms of acclimation to chronic intermittent hypoxia in the gills of Largemouth bass (Micropterus salmoides)

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