Differential Transcriptomic Response in the Spleen and Head Kidney Following Vaccination and Infection of Asian Seabass with Streptococcus iniae

Abstract

Vaccination is an important strategy in the protection of aquaculture species from major diseases. However, we still do not have a good understanding of the mechanisms underlying vaccine-induced disease resistance. This is further complicated by the presence of several lymphoid organs that play different roles when mounting an immune response. In this study, we attempt to elucidate some of these mechanisms using a microarray-based approach. Asian seabass (Lates calcarifer) were vaccinated against Streptococcus iniae and the transcriptomic changes within the spleen and head kidney at one and seven days post-vaccination were profiled. We subsequently challenged the seabass at three weeks post-vaccination with live S. iniae and similarly profiled the transcriptomes of the two organs after the challenge. We found that vaccination induced an early, but transient transcriptomic change in the spleens and a delayed response in the head kidneys, which became more similar to one another compared to un-vaccinated ones. When challenged with the pathogen, the spleen, but not the head kidneys, responded transcriptomically at 25–29 hours post-challenge. A unique set of genes, in particular those involved in the activation of NF-κB signaling, was up-regulated in the vaccinated spleens upon pathogen challenge but not in the un-vaccinated spleens. A semi-quantitative PCR detection of S. iniae using metagenomic DNA extracted from the water containing the seabass also revealed that vaccination resulted in reduction of pathogen shedding. This result indicated that vaccination not only led to a successful immune defense against the infection, but also reduced the chances for horizontal transmission of the pathogen. In conclusion, we have provided a transcriptomic analysis of how the teleost spleen and head kidneys responded to vaccination and subsequent infection. The different responses from the two organs are suggestive of their unique roles in establishing a vaccine-induced disease resistance.

Vaccine-induced modulation of gene expression in turbot peritoneal cells. A microarray approach

“…We also observe a decrease in the expression of genes coding for proteins expressed in B cells, such as B-cell CLL/lymphoma 11Ab, immunoglobulin heavy variable 4-31, immunoglobulin gamma 2A chain, lymphocyte antigen 6 complex, locus G6F, B-cell receptor CD22, immunoglobulin mu heavy chain, and B-cell antigen receptor complex-associated protein alpha chain. These results indicate that genes related to B and T lymphocyte activity and migration were inhibited in peritoneal cells after injection of vaccine and contrast with those found in the spleen of Asian sea bass, where up-regulation of genes related to lymphocytes was observed on days one and seven after vaccination (Jiang et al, 2014). It has been shown that the peritoneal cavity of vaccinated turbot has low levels of lymphocytes in comparison with other cell types (Folgueira et al, 2015).…”

Distribution, properties, and inhibitor sensitivity of zebrafish catechol-O-methyl transferases (COMT)

“…Zebrafish spleen is likely to be the target of adrenergic regulation, similar to that reported in other fish [63], but MAO content in this organ is very low [64] and therefore COMT may be required for the inactivation of the neurotransmitters involved in adrenergic signaling. Moreover, zebrafish COMT present in the spleen may be involved in the regulation of immune response, as reported for mice [37] and fish (sea bass) [40]. COMT protein is present in the spleen of mice [7] and rats [59].…”

“…The zebrafish kidney showed comt gene expression and rather high COMT enzyme activity, similarly to the kidneys of other fish [40] and mammals [4]. The functions of COMT in the kidney may include both the regulation of dopamine levels to control salt homeostasis, as demonstrated for rats [4], and the degradation of excess adrenaline synthesized by scattered cells in the anterior part of the kidney [65] that serve as the adrenal glands in teleost fish.…”

“…The comt gene of stinging catfish was expressed in multiple tissues, including the brain, liver, and ovary, where the enzyme regulated egg development through inactivating catechol estrogens [39]. The comt gene of sea bass was apparently involved in immune response, since the expression of this gene in fish spleen was significantly downregulated upon vaccination and bacterial challenge [40]. COMT enzymatic activity was detected in trout gills, and the gills were supposed to take part in the inactivation of circulating catecholamine neurotransmitters [41].…”

Transcriptome Survey of a Marine Food Fish: Asian Seabass (Lates calcarifer)

“…The transcriptome will be useful for the annotation of the genome, and can also be utilized for gene expression studies through the design of microarrays, as we have done for the Asian seabass [46], or by means of RNA-seq experiments [9,47,48]. In these RNA-seq studies, the transcriptome served as a reference for read mapping and quantification of differential expression.…”