Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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A role for CXC chemokines and their receptors in stress axis regulation of common carp
Pijanowski, Lukasz ; Verburg-van Kemenade, Lidy ; Chadzinska, Magdalena - \ 2019
General and Comparative Endocrinology 280 (2019). - ISSN 0016-6480 - p. 194 - 199.
Carp - CXC chemokines - CXC receptors - Stress

Although chemokines mainly function to activate leukocytes and to direct their migration, novel evidence indicates non-immune functions for chemokines within the nervous and endocrine systems. These include development of the nervous system, neuromodulation, neuroendocrine regulation and direct neurotransmitter-like actions. In order to clarify a potential role for chemokines and their receptors in the stress response of fish, we studied changes in the expression patterns of CXC ligands and their receptors in the stress axis organs of carp, during a restraint stress procedure. We showed that stress down-regulated the gene expression of CXCL9-11 (CXCb1 and CXCb2)in stress axis organs and up-regulated expression of CXCR4 chemokine receptor in NPO and pituitary. Moreover, upon stress, reduced gene expression of CXCL12a and CXCL14 was observed in the head kidney. Our results imply that in teleost fish, CXC chemokines and their receptors are involved in neuroendocrine regulation. The active regulation of their expression in stress axis organs during periods of restraint indicates a significant role in the stress response.

Stress differentially affects the systemic and leukocyte estrogen network in common carp
Szwejser, Ewa ; Pijanowski, Lukasz ; Maciuszek, Magdalena ; Ptak, Anna ; Wartalski, Kamil ; Duda, Malgorzata ; Segner, Helmut ; Kemenade, Lidy van; Chadzinska, Magdalena - \ 2017
Fish and Shellfish Immunology 68 (2017). - ISSN 1050-4648 - p. 190 - 201.
17β-estradiol - Aromatase - Carp - Estrogen receptors - Leukocytes - Stress

Both systemic and locally released steroid hormones, such as cortisol and estrogens, show immunomodulatory actions. This research gives evidence that circulating and leukocyte-derived estrogens can be involved in the regulation of the immune response in common carp, during homeostasis and upon restraining stress. It was found that stress reduced level of blood 17β-estradiol (E2) and down-regulated the gene expression of components of the “classical” estrogen system: the nuclear estrogen receptors and the aromatase CYP19, in the hypothalamus, the pituitary and in the ovaries. In contrast, higher gene expression of the nuclear estrogen receptors and cyp19a was found in the head kidney of stressed animals. Moreover, stress induced changes in the E2 level and in the estrogen sensitivity at local/leukocyte level. For the first time in fish, we showed the presence of physiologically relevant amounts of E2 and the substrates for its conversion (estrone – E1 and testosterone – T) in head kidney monocytes/macrophages and found that its production is modulated upon stress. Moreover, stress reduced the sensitivity of leukocytes towards estrogens, by down-regulation the expression of the erb and cyp19 genes in carp phagocytes. In contrast, era expression was up-regulated in the head kidney monocytes/macrophages and in PBLs derived from stressed animals. We hypothesize that, the increased expression of ERα, that was observed during stress, can be important for the regulation of leukocyte differentiation, maturation and migration. In conclusion, these results indicate that, in fish, the estrogen network can be actively involved in the regulation of the systemic and local stress response and the immune response.

Stress-induced adaptation of neutrophilic granulocyte activity in K and R3 carp lines
Pijanowski, L. ; Verburg-van Kemenade, B.M.L. ; Irnazarow, I. ; Chadzinska, M. - \ 2015
Fish and Shellfish Immunology 47 (2015)2. - ISSN 1050-4648 - p. 886 - 892.
Common carp - IL-10 - NET formation - Neutrophilic granulocytes - Respiratory burst - Stress

Both in mammals and fish, stress induces remarkable changes in the immune response. We focused on stress-induced changes in the activity of neutrophilic granulocytes in the R3 and K lines of common carp, which showed differential stress responses. Our study clearly demonstrates that a prolonged restraint stress differentially affects the activity of K and R3 carp neutrophils. In the K line, stress decreased the respiratory burst, while in the R3 line it reduced the release of extracellular DNA. Surprisingly, the stress-induced changes in ROS production and NET formation did not correlate with changes in gene expression of the inflammatory mediators and GR receptors. In neutrophilic granulocytes from K carp, gene expression of the stress-sensitive cortisol GR1 receptor was significantly higher than in neutrophils from R3 fish, which will make these cells more sensitive to high levels of cortisol. Moreover, upon stress, neutrophilic granulocytes of K carp up-regulated gene expression of the anti-inflammatory cytokine IL-10 while this was not observed in neutrophilic granulocytes of R3 carp.Therefore, we can hypothesize that, in contrast to R3 neutrophils, the more cortisol sensitive neutrophils from K carp respond to stress with up-regulation of IL-10 and consequently reduction of ROS production. Most probably the ROS-independent NET formation in K carp is not regulated by this anti-inflammatory cytokine. These data may indicate a predominantly ROS-independent formation of NETs by carp neutrophilic granulocytes. Moreover, they underline the important role of IL-10 in stress-induced immunoregulation.

Mechanisms involved in the formation of extracellular traps in granuloctyes and macrophages of common carp
Pijanowski, L. ; Verburg-van Kemenade, B.M.L. ; Chadzinska, M.K. - \ 2015
A role for melatonin in maintaining the pro- and anti-inflammatory balance by influencing leukocyte migration and apoptosis in carp
Kepka, M. ; Szwejser, E. ; Pijanowski, L. ; Verburg-van Kemenade, B.M.L. ; Chadzinska, M.K. - \ 2015
Developmental and Comparative Immunology 53 (2015). - ISSN 0145-305X - p. 179 - 190.
coupled receptor dimerization - messenger-rna expression - pineal hormone melatonin - innate immune parameters - common carp - dna-damage - in-vitro - neutrophilic granulocytes - glucocorticoid-receptor - phagocytic-activity
Melatonin is responsible for the synchronization of many physiological processes, including the immune response. Here we focus on the expression of melatonin MT1 receptors in/on leukocytes, and on the effects of melatonin administration on the inflammatory processes of carp. For the first time, we showed that fish leukocytes express MT1 receptors, implicating direct responsiveness to melatonin stimulation. Moreover, both in vitro and in vivo, melatonin modulated the immune response. The most potent effects of melatonin concerned the regulation of leukocyte migration. Melatonin reduced chemotaxis of leukocytes towards CXC chemokines in vitro. In vivo, during zymosan induced peritonitis, i.p. administration of melatonin reduced the number of neutrophils. This correlated with a melatonin-induced decrease of gene expression of the CXCa chemokine. Moreover, melatonin induced a decrease of the respiratory burst in inflammatory leukocytes. Although these data do suggest a potent anti-inflammatory function for this hormone, melatonin-induced inhibition of leukocyte apoptosis clearly indicates towards a dual function. These results show that also in carp, melatonin performs a pleiotropic and extra-pineal function that is important in maintaining the delicate pro- and anti-inflammatory balance during infection. They furthermore demonstrate that neuroendocrine–immune interaction via melatonin is evolutionary conserved.
Activity of the hypothalamus-pituitary-interrenal axis (HPI axis) and immune response in carp lines with different susceptibility to disease
Pijanowski, L. ; Jurecka, P.M. ; Irnazarow, I. ; Kepka, M. ; Szwejser, E. ; Verburg-van Kemenade, B.M.L. ; Chadzinska, M.K. - \ 2015
Fish Physiology and Biochemistry 41 (2015)5. - ISSN 0920-1742 - p. 1261 - 1278.
The stress response transmitted by the HPA axis is one of the best examples of neuroendocrine–immune interactions that are critical for survival. Analogous to the situation in mammals, the stress response in fish is characterized by the activation of the hypothalamo–pituitary–interrenal axis (HPI). Effects of cortisol on the fish immune system comply with findings in mammals and suggest that the differences in sensitivity to stress will influence the immune response and as a consequence of survival. Therefore, we studied the stress response and its immunity-related effects in four different carp lines (R3, R3xR8, K and R2) that display a differential pathogen susceptibility. Previous studies indicate that R3xR8 and R3 carp are susceptible to bacterial and parasite infection, while R2 and K are relatively resistant to infection. Interestingly, the most striking effect of stress on leukocyte composition and activity was observed in the pathogen-resistant K carp, even though no robust changes in gene expression of stress-involved factors were observed. In contrast, R3 carp showed no spectacular stress-induced changes in their immunological parameters with concurrent significant activation of the HPI axis. Upon stress, the R3 carp showed up-regulation of crf, pomc and gr2 gene expression in the hypothalamus. Furthermore in R3 carp, at all levels of the HPI axis, stress induced the highest up-regulation of il-1ß gene expression. Although we are aware of the complexity of the interactions between stress and pathogen susceptibility and of the risk of interpretation based on correlations, it is noteworthy that the fish more susceptible to infection also exhibited the highest response to stress.
Production of inflammatory mediators and extracellular traps by carp macrophages and neutrophils in response to lipopolysaccharide and/or interferon-¿2
Pijanowski, L. ; Scheer, M.H. ; Verburg-van Kemenade, B.M.L. ; Chadzinska, M.K. - \ 2015
Fish and Shellfish Immunology 42 (2015)2. - ISSN 1050-4648 - p. 473 - 482.
toll-like receptors - cyprinus-carpio - signaling pathways - expression analysis - escherichia-coli - immune-response - lps recognition - gene-expression - fish - l.
Neutrophilic granulocytes and macrophages are crucial for the innate immune response against infections. They migrate into the focus of inflammation, where they efficiently bind, engulf and kill bacteria by proteolytic enzymes, antimicrobial peptides, reactive oxygen (ROS) and nitrogen (RNS) species. Moreover, activated neutrophils and macrophages can form extracellular traps (ETs). Fish neutrophils and macrophages are morphologically, histochemically, and functionally similar to their mammalian counterparts, but their significance for regulation of inflammatory responses and pathogen killing needs further elucidation. We compared the activity of head kidney monocytes/macrophages and neutrophilic granulocytes of common carp and established that upon lipopolysaccharide stimulation, not only neutrophils, but also carp monocytes/macrophages release extracellular DNA and are capable to form macrophage extracellular traps (METs). To clarify whether many specific LPS functions reported for piscine phagocytes might be due to impurities in the commonly used LPS preparations we studied expression of inflammatory mediators, release of DNA, ROS and RNS in cells stimulated with LPS or its highly purified form (pLPS). Also IFN-¿2 stimulation and its synergism with LPS/pLPS in stimulating expression of pro-inflammatory mediators was studied. Results substantiate that a classical stimulation of TLR4 by LPS may indeed be absent in carp as most of the classically reported LPS effects are abolished or diminished when pLPS is used. Interestingly, we also observed a potent IL-10 expression in neutrophilic granulocytes upon LPS stimulation, which, apart from their pro-inflammatory function, clearly indicates a role in restrictive control of the inflammatory reaction.
Melatonin affects migration and apoptosis of carp inflammatory leukocytes
Kepka, M. ; Pijanowski, L. ; Verburg-van Kemenade, B.M.L. ; Chadzinska, M.K. - \ 2014
In: 27th conference of european comparative endocrinologists (CECE) 2014 abstracts & programme. - - p. 96 - 96.
Stress response and activity of the hypothalamus-pituitary-interrenal axis (HPI axis) in carp lines with different susceptibility to disease
Pijanowski, L. ; Jurecka, P.M. ; Irnazarow, I. ; Kepka, M. ; Verburg-van Kemenade, B.M.L. ; Chadzinska, M.K. - \ 2014
In: Proceedings of the 27th conference of european comparative endocrinologists (CECE) 2014 abstracts & programme. - - p. 107 - 107.
The stress response is one of the best examples of neuroendocrine-immune interactions. Analogue to the HPA axis in mammals, the stress response in fish is characterized by activation the hypothalamo-pituitary-interrenal (HPI) axis, activation of which starts in the hypothalamic nucleus preopticus (NPO) releasing corticotropic releasing hormone (CRH). CRH stimulates the pituitary to release adrenocorticotropic hormone (ACTH) which is cleaved from pro-opiomelanocortin (POMC). ACTH stimulates release of cortisol from the head kidney. Interestingly, also the crucial pro-inflammatory cytokine IL-1b is involved in both immune and endocrine signalling during stress. Like in mammals, fish leukocytes express receptors for cortisol (GR) and effects of cortisol on the fish immune system generally comply with findings in mammals. This implies that a differential sensitivity to stress may influence the immune response and as a consequence survival. Therefore we studied the stress response in different carp lines that display a differential pathogen susceptibility (R3xR8 and R3 carp are susceptible to bacterial and parasite infection, while R2 and K are relatively resistant). After a stress paradigm of prolonged restraining glucose and cortisol levels were determined, as well as expression of genes involved in HPI axis activity. Stress induced significant increase of serum cortisol levels in all fish lines studied. Both basal and stress-stimulated cortisol levels were higher in the R3xR8 line than in R2, K and R3 fish. In R3 fish we observed stress-induced up-regulation of POMC and GR2 gene expression in the NPO, while in K fish restraining stress slightly down-regulated expression of POMC and GR genes both in NPO and pituitary. Furthermore, both in NPO and pituitary of R3 fish the highest up-regulation of IL- 1b gene expression was observed. Although we are aware of the complexity of the network of connections between stress and susceptibility to pathogens it is striking that the fish more susceptible to infection also exhibit a higher expression of stress related genes.
Characterization and expression analysis of an interferon-y2 induced chemokine receptor CXCR3 in common carp (Cyprinus carpio L.)
Chadzinska, M.K. ; Golbach, L.A. ; Pijanowski, L. ; Scheer, M.H. ; Verburg-van Kemenade, B.M.L. - \ 2014
Developmental and Comparative Immunology 47 (2014)1. - ISSN 0145-305X - p. 68 - 76.
central-nervous-system - rheumatoid-arthritis - t-cells - monoclonal-antibodies - molecular evolution - endothelial-cells - phagocytic-cells - teleost fish - b-cells - inflammation
Chemokine and chemokine receptor signalling pairs play a crucial role in regulation of cell migration, morphogenesis, and cell activation. Expressed in mammals on activated T and NK cells, chemokine receptor CXCR3 binds interferon-¿ inducible chemokines CXCL9–11 and CCL21. Here we sequenced the carp CXCR3 chemokine receptor and showed its relationship to CXCR3a receptors found in other teleosts. We found high expression of the CXCR3 gene in most of the organs and tissues of the immune system and in immune-related tissues such as gills and gut, corroborating a predominantly immune-related function. The very high expression in gill and gut moreover indicates a role for CXCR3 in cell recruitment during infection. High in vivo expression of CXCR3 at later stages of inflammation, as well as its in vitro sensitivity to IFN-¿2 stimulation indicate that in carp, CXCR3 is involved in macrophage-mediated responses. Moreover, as expression of the CXCR3 and CXCb genes coincides in the focus of inflammation and as both the CXCb chemokines and the CXCR3 receptor are significantly up-regulated upon IFN-¿ stimulation it is hypothesized that CXCb chemokines may be putative ligands for CXCR3.
ROS involvement in the formation of neutrophil extracellular traps in common carp
Pijanowski, L. ; Golbach, L.A. ; Kepka, M. ; Verburg-van Kemenade, B.M.L. ; Chadzinska, M.K. - \ 2013
Fish and Shellfish Immunology 34 (2013)6. - ISSN 1050-4648 - p. 1729 - 1729.
Carp neutrophilic granulocyes form extracellular traps via ROS-dependent and independent pathways
Pijanowski, L. ; Golbach, L.A. ; Kolaczkowska, E. ; Scheer, M.H. ; Verburg-van Kemenade, B.M.L. ; Chadzinska, M.K. - \ 2013
Fish and Shellfish Immunology 34 (2013)5. - ISSN 1050-4648 - p. 1244 - 1252.
differential expression - net formation - teleost fish - myeloperoxidase - bacterial - immunity - genes - l. - matrix-metalloproteinase-9 - streptococcus
Neutrophil extracellular traps (NETs) have recently been described as an important innate defense mechanism that leads to immobilization and killing of invading pathogens. NETs have been identified in several species, but the mechanisms involved in NET formation and their role in infection have not been well determined yet. Here we show that upon in vitro stimulation with different immunostimulants of bacterial, fungal or viral origin, carp neutrophilic granulocytes rapidly release NET structures. We analyzed the composition of these structures and the kinetics of their formation by confocal microscopy, by quantifying the levels of extracellular DNA and the release of enzymes originating from neutrophilic granules: myeloperoxidase, neutrophil elastase and matrix metalloproteinase 9 (MMP-9). Profiles of NET release by carp neutrophils as well as their enzyme composition are stimulus- and time-dependent. This study moreover provides evidence for a stimulus-dependent selective requirement of reactive oxygen species in the process of NET formation. Collectively the results support an evolutionary conserved and strictly regulated mechanism of NET formation in teleost fish.
Neutrophil extracellular traps in carp
Pijanowski, L. ; Golbach, L.A. ; Verburg-van Kemenade, B.M.L. ; Kolaczkowska, E. ; Chadzinska, M.K. - \ 2012
In: The 12th congress of ISDCI program and abstracts, Fukuoka, Japan, 9-13 July 2012. - - p. 68 - 68.
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