Identification of the salmonid IL-17A/F1a/b, IL-17A/F2b, IL-17A/F3 and IL-17N genes and analysis of their expression following in vitro stimulation and infection

Wang, Tiehui; Jiang, Yousheng; Wang, Alex; Husain, Mansourah; Xu, Qiaoqing

doi:10.1007/s00251-015-0838-1

Cited by 56 publications

(50 citation statements)

References 55 publications

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“…Thus, spleen leukocytes from control and infected fish were isolated 4 dpi and sorted into four lymphocyte populations, CD4 DP, CD4-2 SP, CD8α + , and CD4-1 − /CD4-2 − /CD8α − lymphocytes (Neg). In line with previous reports (29, 46), whole spleen leukocytes (WSLs) in infected fish showed higher expression levels of il-2 , il-10 , ifng , il-17a/f-1a , il-21b , and il-22 cytokines when compared to those in control fish, whereas the expression levels of il-4/13a and il-21a remained unchanged (Fig. 5).…”

Section: Resultssupporting

confidence: 92%

Novel Teleost CD4-Bearing Cell Populations Provide Insights into the Evolutionary Origins and Primordial Roles of CD4+ Lymphocytes and CD4+ Macrophages

Takizawa

Magadán

Parra

et al. 2016

The Journal of Immunology

103

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Tetrapods contain a single CD4 co-receptor with four immunoglobulin domains that likely arose from a primordial two-domain ancestor. Notably, teleost fish contain two CD4 genes. Like tetrapod CD4, CD4-1 of rainbow trout includes four immunoglobulin domains while CD4-2 contains only two. Since CD4-2 is reminiscent of the prototypic two-domain CD4 co-receptor, we hypothesized that by characterizing the cell types bearing CD4-1 and CD4-2, we would shed light into the evolution and primordial roles of CD4-bearing cells. Using newly established monoclonal antibodies against CD4-1 and CD4-2, we identified two bona fide CD4+ T-cell populations, a predominant lymphocyte population co-expressing surface CD4-1 and CD4-2 (CD4 DP), and a minor subset expressing only CD4-2 (CD4-2 SP). While both subsets produced equivalent levels of Th1, Th17, and Treg cytokines upon bacterial infection, CD4-2 SP lymphocytes were less proliferative and displayed a more restricted TCRβ repertoire. These data suggest that CD4-2 SP cells represent a functionally distinct population and may embody a vestigial CD4+ T cell subset, the roles of which reflect those of primeval CD4+ T cells. Importantly, we also describe the first CD4+ monocyte/macrophage population in a non-mammalian species. Of all myeloid subsets, we found the CD4+ population to be the most phagocytic, while CD4+ lymphocytes lacked this capacity. This study fills in an important gap in the knowledge of teleost CD4-bearing leukocytes thus revealing critical insights into the evolutionary origins and primordial roles of CD4+ lymphocytes and CD4+ monocyte/macrophages.

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Section: Resultssupporting

confidence: 92%

Novel Teleost CD4-Bearing Cell Populations Provide Insights into the Evolutionary Origins and Primordial Roles of CD4+ Lymphocytes and CD4+ Macrophages

Takizawa

Magadán

Parra

et al. 2016

The Journal of Immunology

103

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“…Purified Atlantic salmon GALT leucocytes obtained using protocol-3, were suspended in RPMI-1640 containing P/S and 10% FBS, then plated at 2x10 6 cells /well into 12 well plates and cultured at 20 o C. The cells, from individual fish, were then stimulated with 10 μg /ml phytohaemagglutinin from Phaseolus vulgaris (PHA, Sigma), 50 μg /ml LPS, 100 μg /ml polyinosinic acid: polycytidylic acid (poly I:C, Sigma), 100 ng /ml recombinant flagellin from Yersinia ruckeri (rYRF, [26], 25 ng /ml IL-1β1 [27], 100 ng /ml IL-2B [28], 100 ng /ml IL-6 [29], 200 ng /ml IL-21 [30] and 20 ng /ml IFN-α2/IFN2 [31]. All doses used were previously shown to be optimal for trout and Atlantic salmon cells [32,33,34], and the cytokine paralogues chosen have known bioactivity on leucocytes from other tissues. Untreated cells were included as controls.…”

Section: Atlantic Salmon Galt Leucocyte Analysismentioning

confidence: 99%

Gene expression analysis of isolated salmonid GALT leucocytes in response to PAMPs and recombinant cytokines

Attaya

Wang

Zou

et al. 2018

Fish & Shellfish Immunology

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Increased knowledge of the immune response of the intestine, a physiologically critical organ involved in absorption, secretion and homeostasis in a non-sterile environment, is needed to better understand the mechanisms involved in the induction of long-lasting immunity and, subsequently, the development of efficacious gastrointestinal immunization approaches. To this end, analysis of isolated gut cells will give an insight into the cell types present and their immune capability. Hence, in this study we first optimised a method for salmonid gut leucocyte isolation and characterised the cells on the basis of their expression of a range of selected cell markers associated with T & B cells and dendritic cells. The GALT leucocytes were then stimulated with a variety of PAMPs, recombinant cytokines and PHA, as a means to help characterise the diversity of the immune repertoire present in such cells. The stimulants tested were designed to examine the nature of the antibacterial, antiviral and T cell type responses in the cells (at the transcript level) using a panel of genes relevant to innate and adaptive immunity. The results showed distinct responses to the stimulants, with a clear delineation seen between the stimulant used (eg viral or bacterial PAMP) and the pathway elicited. The changes in the expression patterns of the immune genes in these cells indicates that the salmonid intestine contains a good repertoire of competent immune cells able to respond to different pathogen types. Such information may aid the development of efficient priming by oral vaccination in salmonids.

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“…It has been reported that expression levels of IL-17A/F1, 2, and 3 genes fluctuate at the mRNA level during bacterial infection in multiple fish species. Yersinia ruckeri upregulates salmonid IL-17A/F1, 2, and 3 in the spleen (22), whereas Aeromonas hydrophila up-regulates large yellow croaker counterparts in the head, kidney, and gill (23). However, details regarding the mechanism of fish IL-17A/F gene regulation of the intestinal tract microbiome are unknown.…”

Section: Introductionmentioning

confidence: 99%

Interleukin-17A/F1 Deficiency Reduces Antimicrobial Gene Expression and Contributes to Microbiome Alterations in Intestines of Japanese medaka (Oryzias latipes)

et al. 2020

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In mammals, interleukin (IL)-17A and F are hallmark inflammatory cytokines that play key roles in protection against infection and intestinal mucosal immunity. In the gastrointestinal tract (GI), the induction of antimicrobial peptide (AMP) production via Paneth cells is a fundamental role of IL-17A and F in maintaining homeostasis of the GI microbiome and health. Although mammalian IL-17A and F homologs (referred to as IL-17A/F1-3) have been identified in several fish species, their function in the intestine is poorly understood. Additionally, the fish intestine lacks Paneth cells, and its GI structure is very different from that of mammals. Therefore, the GI microbiome modulatory mechanism via IL-17A/F genes has not been fully elucidated. In this study, Japanese medaka (Oryzias latipes) were used as a teleost model, and IL-17A/F1-knockout (IL-17A/F1-KO) medaka were established using the CRISPR/Cas9 genome editing technique. Furthermore, two IL-17A/F1-deficient medaka strains were generated, including one strain containing a 7-bp deletion (-7) and another with an 11-bp addition (+11). After establishing F2 homozygous KO medaka, transcriptome analysis (RNA-seq) was conducted to elucidate IL-17A/F1-dependent gene induction in the intestine. Results of RNA-seq and real-time PCR (qPCR) demonstrated down-regulation of immune-related genes, including interleukin-1β (IL-1β), complement 1q subunit C (C1qc), transferrin a (Tfa), and G-type lysozyme (LyzG), in IL-17A/F1-KO medaka. Interestingly, protein and lipid digestive enzyme genes, including phospholipase A2, group IB (pla2g1b), and elastase-1-like (CELA1), were also downregulated in the intestines of IL-17A/F1-KO medaka. Furthermore, to reveal the influence of these downregulated genes on the gut microbiome in IL-17A/F1-KO, 16S rRNA-based metagenomic sequencing analysis was conducted to analyze the microbiome constitution. Under a non-exposed state, the Okamura et al. Role of IL-17A/F1 in Teleost Intestineintestinal microbiome of IL-17A/F1-KO medaka differed at the phylum level from wild-type, with significantly higher levels of Verrucomicrobia and Planctomycetes. Additionally, at the operational taxonomic unit (OTU) level of the human and fish pathogens, the Enterobacteriaceae Plesiomonas shigelloides was the dominant species in IL-17A/F1-KO medaka. These findings suggest that IL-17A/F1 is involved in the maintenance of a healthy gut microbiome.

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Identification of the salmonid IL-17A/F1a/b, IL-17A/F2b, IL-17A/F3 and IL-17N genes and analysis of their expression following in vitro stimulation and infection

Cited by 56 publications

References 55 publications

Novel Teleost CD4-Bearing Cell Populations Provide Insights into the Evolutionary Origins and Primordial Roles of CD4+ Lymphocytes and CD4+ Macrophages

Novel Teleost CD4-Bearing Cell Populations Provide Insights into the Evolutionary Origins and Primordial Roles of CD4+ Lymphocytes and CD4+ Macrophages

Gene expression analysis of isolated salmonid GALT leucocytes in response to PAMPs and recombinant cytokines

Interleukin-17A/F1 Deficiency Reduces Antimicrobial Gene Expression and Contributes to Microbiome Alterations in Intestines of Japanese medaka (Oryzias latipes)

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