The importance of the Atlantic salmon peritoneal cavity B cell response: Local IgM secreting cells are predominant upon Piscirickettsia salmonis infection

Wal, Yorick Andreas van der; Jenberie, Shiferaw; Nordli, Henriette; Greiner-Tollersrud, Linn; Kool, Jaap; Jensen, Ingvill; Jørgensen, Jorunn B.

doi:10.1016/j.dci.2021.104125

Cited by 15 publications

(9 citation statements)

References 49 publications

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“…Our results indicated that, upon an intraperitoneal injection with a TI antigen, the AT is one of the tissues that harbors antigen-specific IgM-secreting cells for long time periods, at levels similar to those of systemic immune tissues such as the spleen or the head kidney. As reported before ( 19 , 48 ), the peritoneal cavity contained a very high frequency of B cells secreting TNP-specific IgMs, which seemed to be retained in this location for long time periods. Thus, in our study, while these cells started to decrease between days 14 and 28 post-immunization in the AT, they were still increasing at the peritoneal cavity during this time period.…”

Section: Discussionsupporting

confidence: 79%

“…In Atlantic salmon ( Salmo salar L.), a recent study, also reported transcriptional changes in the AT after an intraperitoneal challenge with Piscirickettsia salmonis . The changes observed in the levels of transcription of marker genes for different adaptive cell types led the authors to hypothesize that the AT is a site for antigen presentation and B cell activation ( 19 ). In this context, it seemed adequate to thoroughly characterize the different B cell populations present in teleost AT and investigate their response to immune stimulation, and this is what we have undertaken in the current study using the rainbow trout as a model.…”

Section: Introductionmentioning

confidence: 99%

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Functional and Phenotypic Characterization of B Cells in the Teleost Adipose Tissue

et al. 2022

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The immune response of the adipose tissue (AT) has been neglected in most animal models until investigations in human and mice linked obesity to chronic inflammation, highlighting the immune nature of this tissue. Despite this, in teleost fish, only a few studies have addressed the immune role of the AT. These studies have mostly focused on reporting transcriptional changes in the AT in response to diverse intraperitoneally delivered stimuli. Although the presence of B cells within the AT was also previously revealed, these cells have never been phenotypically or functionally characterized and this is what we have addressed in the current study. Initially, the B cell populations present in the rainbow trout (Oncorhynchus mykiss) AT were characterized in comparison to B cells from other sources. As occurs in other rainbow trout tissues, IgM+IgD+, IgM+IgD- and IgD+IgM- B cell subsets were identified in the AT. Interestingly, AT IgM+IgD- B cells showed a transcriptional profile that agrees with that of cells that have committed to plasmablasts/plasma cells, being this profile much more pronounced towards a differentiation state than that of blood IgM+IgD- B cells. Accordingly, the IgM-secreting capacity of AT B cells is significantly higher than that of blood B cells. Additionally, AT IgM+IgD+ B cells also showed specific phenotypic traits when compared to their counterparts in other tissues. Finally, we established how these B cell subsets responded when rainbow trout were intraperitoneally injected with a model antigen. Our results demonstrate that the AT hosts plasmablasts/plasma cells that secrete specific IgMs, as happens in the peritoneal cavity and systemic immune tissues. Although the presence of these antigen-specific IgM-secreting cells was more abundant in the peritoneal cavity, these specific differentiated B cells were detected in the AT for long time periods at levels similar to those of spleen and head kidney. Our results provide new evidence regarding the immune role of the teleost AT, indicating that it functions as a secondary lymphoid organ that promotes immunity to peritoneal antigens.

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Section: Discussionsupporting

confidence: 79%

Section: Introductionmentioning

confidence: 99%

Functional and Phenotypic Characterization of B Cells in the Teleost Adipose Tissue

et al. 2022

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“…The intraperitoneal route is usually chosen for the administration of vaccines in salmon, but there is little knowledge about its immune response. Recently, a significant increase in leukocytes, total IgM antibody-secreting cells (ASCs) and P. salmonis -specific ASCs in the peritoneal cavity at 3 and 6 weeks after infection with P. salmonis has been described ( 157 ). Hence, the authors suggest a putative role for adipose tissue in the peritoneal cavity immune response.…”

Section: Vaccination Against P Salmonis : Mission ...mentioning

confidence: 99%

Why Does Piscirickettsia salmonis Break the Immunological Paradigm in Farmed Salmon? Biological Context to Understand the Relative Control of Piscirickettsiosis

Rozas‐Serri¹

2022

Front. Immunol.

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Piscirickettsiosis (SRS) has been the most important infectious disease in Chilean salmon farming since the 1980s. It was one of the first to be described, and to date, it continues to be the main infectious cause of mortality. How can we better understand the epidemiological situation of SRS? The catch-all answer is that the Chilean salmon farming industry must fight year after year against a multifactorial disease, and apparently only the environment in Chile seems to favor the presence and persistence of Piscirickettsia salmonis. This is a fastidious, facultative intracellular bacterium that replicates in the host’s own immune cells and antigen-presenting cells and evades the adaptive cell-mediated immune response, which is why the existing vaccines are not effective in controlling it. Therefore, the Chilean salmon farming industry uses a lot of antibiotics—to control SRS—because otherwise, fish health and welfare would be significantly impaired, and a significantly higher volume of biomass would be lost per year. How can the ever-present risk of negative consequences of antibiotic use in salmon farming be balanced with the productive and economic viability of an animal production industry, as well as with the care of the aquatic environment and public health and with the sustainability of the industry? The answer that is easy, but no less true, is that we must know the enemy and how it interacts with its host. Much knowledge has been generated using this line of inquiry, however it remains insufficient. Considering the state-of-the-art summarized in this review, it can be stated that, from the point of view of fish immunology and vaccinology, we are quite far from reaching an effective and long-term solution for the control of SRS. For this reason, the aim of this critical review is to comprehensively discuss the current knowledge on the interaction between the bacteria and the host to promote the generation of more and better measures for the prevention and control of SRS.

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“…Fish have mammalian-like T and B lymphocytes. Different subpopulations of fish T cells have not been well characterized, but homologs of CD8 and CD4 have been reported, while B lymphocytes were also found to have phagocytic activity ( 300 , 301 ). Fish MHC I, TCR and TCR co-receptor CD8 are homologous to mammals, suggesting similarities in the antigen presentation process, i.e., antigens presented by MHC are recognized by TCR and activate immune responses.…”

Section: Mechanism Of Aquatic Vaccinesmentioning

confidence: 99%

Current status and development prospects of aquatic vaccines

Liu

et al. 2022

Front. Immunol.

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Diseases are a significant impediment to aquaculture’s sustainable and healthy growth. The aquaculture industry is suffering significant financial losses as a result of the worsening water quality and increasing frequency of aquatic disease outbreaks caused by the expansion of aquaculture. Drug control, immunoprophylaxis, ecologically integrated control, etc. are the principal control strategies for fish infections. For a long time, the prevention and control of aquatic diseases have mainly relied on the use of various antibiotics and chemical drugs. However, long-term use of chemical inputs not only increases pathogenic bacteria resistance but also damages the fish and aquaculture environments, resulting in drug residues in aquatic products, severely impeding the development of the aquaculture industry. The development and use of aquatic vaccines are the safest and most effective ways to prevent aquatic animal diseases and preserve the health and sustainability of aquaculture. To give references for the development and implementation of aquatic vaccines, this study reviews the development history, types, inoculation techniques, mechanisms of action, development prospects, and challenges encountered with aquatic vaccines.

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The importance of the Atlantic salmon peritoneal cavity B cell response: Local IgM secreting cells are predominant upon Piscirickettsia salmonis infection

Cited by 15 publications

References 49 publications

Functional and Phenotypic Characterization of B Cells in the Teleost Adipose Tissue

Functional and Phenotypic Characterization of B Cells in the Teleost Adipose Tissue

Why Does Piscirickettsia salmonis Break the Immunological Paradigm in Farmed Salmon? Biological Context to Understand the Relative Control of Piscirickettsiosis

Current status and development prospects of aquatic vaccines

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