Erling O Koppang’s research while affiliated with Norwegian University of Life Sciences and other places

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Publications (75)


Organisation of the Atlantic salmon (Salmo salar) thymus and its content of Ig-expressing cells
  • Article

May 2024

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16 Reads

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1 Citation

Fish & Shellfish Immunology

Håvard Bjørgen

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Fran Barac

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[...]

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Erling O. Koppang

Correction to: Cellular heterogeneity in red and melanized focal muscle changes in farmed Atlantic salmon (Salmo salar) visualized by spatial transcriptomics
  • Article
  • Full-text available

December 2023

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24 Reads

Cell and Tissue Research

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Red focal changes (RFCs) (a) and melanized focal changes (MFCs) (b) in Atlantic salmon fillet
Hematoxylin and eosin stain of a RFC and b MFC
UMAP clustering of all spots with different spatial barcodes on the spatial gene expression slide, based on complete gene expression profiles
Spatially resolved cell populations as defined by SNN clustering for RFC samples 1 and 2 and MFC samples 1 and 2 (a, b, c, and d) and corresponding histology images (a’, b’, c’, and d’)
Chord diagram showing the extent of overlap in genes defining the different cell populations (RFCs versus MFCs; up- and downregulated genes combined)

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Cellular heterogeneity in red and melanized focal muscle changes in farmed Atlantic salmon (Salmo salar) visualized by spatial transcriptomics

December 2023

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89 Reads

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3 Citations

Cell and Tissue Research

Spatial transcriptomics is a technique that provides insight into gene expression profiles in tissue sections while retaining structural information. We have employed this method to study the pathological conditions related to red and melanized focal changes in farmed Atlantic salmon (Salmo salar). Our findings support a model where similar molecular mechanisms are involved in both red and melanized filet discolorations and genes associated with several relevant pathways show distinct expression patterns in both sample types. Interestingly, there appears to be significant cellular heterogeneity in the foci investigated when looking at gene expression patterns. Some of the genes that show differential spatial expression are involved in cellular processes such as hypoxia and immune responses, providing new insight into the nature of muscle melanization in Atlantic salmon.



Identification of a pharyngeal mucosal lymphoid organ in zebrafish and other teleosts: Tonsils in fish?

November 2023

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96 Reads

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16 Citations

Science Advances

The constant exposure of the fish branchial cavity to aquatic pathogens causes local mucosal immune responses to be extremely important for their survival. Here, we used a marker for T lymphocytes/natural killer (NK) cells (ZAP70) and advanced imaging techniques to investigate the lymphoid architecture of the zebrafish branchial cavity. We identified a sub-pharyngeal lymphoid organ, which we tentatively named “Nemausean lymphoid organ” (NELO). NELO is enriched in T/NK cells, plasma/B cells, and antigen-presenting cells embedded in a network of reticulated epithelial cells. The presence of activated T cells and lymphocyte proliferation, but not V(D)J recombination or hematopoiesis, suggests that NELO is a secondary lymphoid organ. In response to infection, NELO displays structural changes including the formation of T/NK cell clusters. NELO and gill lymphoid tissues form a cohesive unit within a large mucosal lymphoid network. Collectively, we reveal an unreported mucosal lymphoid organ reminiscent of mammalian tonsils that evolved in multiple teleost fish families.




Identification of a new pharyngeal mucosal lymphoid organ in zebrafish and other teleosts: tonsils in fish?

April 2023

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150 Reads

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1 Citation

The constant exposure of the fish branchial cavity to aquatic pathogens must have driven local mucosal immune responses to be extremely important for their survival. In this study, we used a universal marker for T lymphocytes/natural killer cells (ZAP70) and advanced imaging techniques to investigate the lymphoid architecture of the zebrafish branchial cavity. We identified a new lymphoid organ, which we tentatively named “Nemausean Lymphoid Organ” (NEMO), situated below the pharynx, and closely associated with gill lymphoid tissues. Besides T/NK cells, NEMO is enriched in plasma/B cells and antigen-presenting cells embedded in a network of reticulated epithelial cells. Presence of activated T cells and lymphocyte proliferation but not V(D)J recombination or hematopoiesis, suggests a function as secondary lymphoid organ. In response to infection, NEMO displays structural changes including the formation of T/NK cells clusters. NEMO and gill lymphoid aggregates form a cohesive unit within a lymphoid network that extends throughout the pharyngo-respiratory area. Collectively, our findings reveal a new mucosal lymphoid organ reminiscent of mammalian tonsils that evolved in fish. Importantly, NEMO could clearly be identified in multiple teleost fish families. One sentence summary A previously unreported lymphoid organ has been identified within the pharyngo-respiratory tract of the zebrafish, and other teleost fish, providing new insights into the immune system of teleost fish and the evolution of vertebrate immunology.


The teleost polymeric Ig receptor counterpart in ballan wrasse (Labrus bergylta) differs from pIgR in higher vertebrates

May 2022

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71 Reads

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10 Citations

Veterinary Immunology and Immunopathology

As mucosal barriers in fish are the main sites where pathogens are encountered, mucosal immunity is crucial to avoid infection in the aquatic environment. In teleost fish, immunoglobulins are present in gut, gill and skin mucus, although not in the same amounts as in higher vertebrates. In mammals, the poly-Ig receptor (pIgR) is synthesized in epithelial cells and mediates the active transport of poly-immunoglobulins (pIgs) across the epithelium. During transport, a component of the pIgR, the secretory component (SC), is covalently bound to pIgs secreted into the mucus providing protection against proteases and avoiding degradation. The teleost pIgR gene does not show synteny to higher vertebrates, the overall structure of the protein is different (comprising two Ig domains) and its functional mechanisms remain unclear. The J-chain which is essential for pIgR-mediated transport of IgA and IgM in higher vertebrates is absent in teleost fish. The aim of the present study was to characterize the ballan wrasse (Labrus bergylta) pIgR and use it as a marker for further studies of mucosal immunity in this species. The pIgR gene was unambiguously identified. Unexpectedly, reverse transcription real time PCR (RT-qPCR) revealed highest abundance of pIgR mRNA in liver and significantly lower expression in mucosal organs such as foregut, hindgut, and skin. In situ hybridization showed pIgR-positive cells dispersed in the lamina propria while it was undetectable in epithelial cells of foregut and hindgut of ballan wrasse. A similar pattern was observed in Atlantic salmon. Liquid Chromatography-Mass Spectrometry (LC-MS/MS) analysis of IgM enriched mucus samples from gut, gill, skin, and bile gave relatively few matches to wrasse pIgR. Notably, the matching peptides were from the transmembrane (TM) and cytoplasmatic (Cy) region as well as the putative SC, indicating leakage from lysed cells rather than covalent bonds between IgM and SC. Altogether, the results indicate that pIgR has another (or at least an additional) function in wrasse. Another pIgR-like molecule (pIgRL) in ballan wrasse (comprising three Ig domains) was analyzed to see if this could be an alternative functional pIgR homolog. However, the presence of pIgRL mRNA in blood leukocytes and a relatively high expression in immune organs like spleen and head kidney pointed to a receptor function on a circulating leukocyte population. As significant amounts of IgM were found in bile of ballan wrasse further studies should consider the hepato-biliary route regarding IgM delivery to the gut lumen.


High-Resolution, 3D Imaging of the Zebrafish Gill-Associated Lymphoid Tissue (GIALT) Reveals a Novel Lymphoid Structure, the Amphibranchial Lymphoid Tissue

November 2021

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445 Reads

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28 Citations

The zebrafish is extensively used as an animal model for human and fish diseases. However, our understanding of the structural organization of its immune system remains incomplete, especially the mucosa-associated lymphoid tissues (MALTs). Teleost MALTs are commonly perceived as diffuse and scattered populations of immune cells throughout the mucosa. Yet, structured MALTs have been recently discovered in Atlantic salmon (Salmo salar L.), including the interbranchial lymphoid tissue (ILT) in the gills. The existence of the ILT was only recently identified in zebrafish and other fish species, highlighting the need for in-depth characterizations of the gill-associated lymphoid tissue (GIALT) in teleosts. Here, using 3-D high-resolution microscopy, we analyze the GIALT of adult zebrafish with an immuno-histology approach that reveals the organization of lymphoid tissues via the labeling of T/NK cells with an antibody directed to a highly conserved epitope on the kinase ZAP70. We show that the GIALT in zebrafish is distributed over at least five distinct sub-regions, an organization found in all pairs of gill arches. The GIALT is diffuse in the pharyngeal part of the gill arch, the interbranchial septum and the filaments/lamellae, and structured in two sub-regions: the ILT, and a newly discovered lymphoid structure located along each side of the gill arch, which we named the Amphibranchial Lymphoid Tissue (ALT). Based on RAG2 expression, neither the ILT nor the ALT constitute additional thymi. The ALT shares several features with the ILT such as presence of abundant lymphoid cells and myeloid cells embedded in a network of reticulated epithelial cells. Further, the ILT and the ALT are also a site for T/NK cell proliferation. Both ILT and ALT show structural changes after infection with Spring Viraemia of Carp Virus (SVCV). Together, these data suggest that ALT and ILT play an active role in immune responses. Comparative studies show that whereas the ILT seems absent in most neoteleosts (“Percomorphs”), the ALT is widely present in cyprinids, salmonids and neoteleosts, suggesting that it constitutes a conserved tissue involved in the protection of teleosts via the gills.


Citations (53)


... However, in pathological conditions such as RFCs/MFCs, oxygen availability is constrained, and recently, hypoxia has been proposed as a factor involved in the pathogenesis of MFCs . Using spatial transcriptomic analysis, Bjørgen et al. (2023) showed that the hypoxia-inducible factor 1 (HIF-1) pathway was markedly upregulated in several cell populations in both RFCs and MFCs from Atlantic salmon. HIF complexes serve as major transcriptional regulators, eliciting cell-specific responses to hypoxia in vertebrates (Masoud & Li, 2015;Pelster & Egg, 2018). ...

Reference:

Deciphering the pathogenesis of melanized focal changes in the white skeletal muscle of farmed Atlantic salmon (Salmo salar)
Cellular heterogeneity in red and melanized focal muscle changes in farmed Atlantic salmon (Salmo salar) visualized by spatial transcriptomics

Cell and Tissue Research

... Therefore, based on observations in ballan wrasse (Figs. 2 and 3), the transport of IgM produced by PC in the pancreatic tissue toward the veins and into the blood stream mediated by endothelial pIgR seems unlikely. However, the scenario where transport of Igs occurs in the opposite direction, from blood and into pancreatic tissue also seems rather unlikely as ballan wrasse has abundant IgM + cells within the pancreatic tissue ( Fig. 3A and B), also within the abdominal exocrine pancreas where acinar cells are not organized around veins as observed in the liver [91]. Thus, it is more likely that wrasse IgM + cells localized in the pancreas release IgM towards the pancreatic ducts, supported by a weak pIgR staining of acinar cells (Fig. 2B). ...

The ontogeny of lymphoid organs and IgM+ B-cells in ballan wrasse (Labrus bergylta) reveals a potential site for extrarenal B-cell lymphopoiesis: The pancreas

Fish & Shellfish Immunology

... For teleost fish, the development of a proper thymus occurs from the pharyngeal pouches between the branchial arches (Chilmonczyk 1992). Since 2008, subsequent research has revealed a series of additional lymphoid organs in this region, some directly associated with the gills (Dalum et al. 2021;Haugarvoll et al. 2008;Koppang et al. 2010;Resseguier et al. 2023). However, the exact participation of these structures in gill immune functions remains unknown. ...

Identification of a pharyngeal mucosal lymphoid organ in zebrafish and other teleosts: Tonsils in fish?
  • Citing Article
  • November 2023

Science Advances

... The first investigated pIgR gene among teleosts was in fugu (Takifugu rubripes) [8]. Subsequently, numerous species were investigated, as reviewed in Rombout et al. [13], and reports in several species have emerged in the last decade [1,10,21,23,26,29,[54][55][56]. The teleost pIgR has been found to exhibit only two Ig domains where the first seems to correspond to mammalian D1 [3,5,57], while Hamuro et al. [8] suggested that the second Ig domain might be an ancestral domain of mammalian D5 and it is therefore often referred to as D5. ...

The teleost polymeric Ig receptor counterpart in ballan wrasse (Labrus bergylta) differs from pIgR in higher vertebrates

Veterinary Immunology and Immunopathology

... For teleost fish, the development of a proper thymus occurs from the pharyngeal pouches between the branchial arches (Chilmonczyk 1992). Since 2008, subsequent research has revealed a series of additional lymphoid organs in this region, some directly associated with the gills (Dalum et al. 2021;Haugarvoll et al. 2008;Koppang et al. 2010;Resseguier et al. 2023). However, the exact participation of these structures in gill immune functions remains unknown. ...

High-Resolution, 3D Imaging of the Zebrafish Gill-Associated Lymphoid Tissue (GIALT) Reveals a Novel Lymphoid Structure, the Amphibranchial Lymphoid Tissue

... The virus infects host cells using its surface protein (S), which binds to angiotensin-converting enzyme 2 (ACE2). ACE2 is a membrane-bound peptidase expressed in the heart, lungs, gastrointestinal tract and kidneys, playing an important role in immune pathways [4][5][6]. Common symptoms of infection include respiratory symptoms, fever, cough, shortness of breath and breathing difficulties. In more severe cases, infection can cause pneumonia, acute respiratory syndrome, kidney failure and even death [7][8][9]. ...

Immune protection is dependent on the gut microbiome in a lethal mouse gammaherpesviral infection

... This is not limited to the pharyngeal region; it extends to the cloaca, where significant structures like the bursa of Fabricius form in birds. Its piscine structural equivalent has been identified in the Atlantic salmon (Løken et al. 2020). In the pharyngeal region of fish, thymus-like structures were present in the gills of lampreys (Bajoghli et al. 2011). ...

A teleost structural analogue to the avian bursa of Fabricius

Journal of Anatomy

... The upregulation of mhc1 induced by yeast in this study may be of advantage in boosting the immune system before SWT. However, the upregulation of mhc1 was followed by a slight downregulation on d56 in SW in the Yeast group, suggesting an immune system depression post SWT that is consistent with the findings by Johansson et al. (2016) and Jarungsriapisit et al. (2018). Nevertheless, the immune suppression responses at the transcriptome level were not as pronounced as reported previously. ...

Time after seawater transfer influences immune cell abundance and responses to SAV3 infection in Atlantic salmon

Journal of Fish Diseases

... Hence, disease, growing to a larger slaughtering weight and more energy spent for maintenance could explain the difference in mean FCR and TGC between the two locations (FCR fjord: 1.24, FCR coast: 1.04, TGC fjord: 2,87, TGC coast 3,70). Previous studies have hypothesized that inflammation and the formation of ectopic goblet cells in Atlantic salmon worsens with long-term exposure to a challenging plant-based feed ingredient (Bjørgen et al., 2018;Dale et al., 2009). The DI RNAseq and histological assessment of the present study support this hypothesis. ...

Ectopic epithelial cell clusters in salmonid intestine are associated with inflammation

Journal of Fish Diseases

... Our results suggest that the expression of MHCII is not limited to immune cell types, but is also evident in the superficial keratinocytes. This is consistent with similar observations of MHCII expression in human keratinocytes [146,147] and may explain previous observations of MHCII expression in Atlantic salmon epidermis in response to sea lice [25,148]. Our results support the potential importance of superficial keratinocytes for sensing pathogens via antigen presentation and initiating immune and inflammatory responses [149]. ...

Contrasting expression of immune genes in scaled and scaleless skin of Atlantic salmon infected with young stages of Lepeophtheirus salmonis
  • Citing Article
  • October 2016

Developmental & Comparative Immunology