Evolutionarily conserved mechanisms regulating stress-induced neutrophil redistribution in fish
IntroductionStress may pose a serious challenge to immune homeostasis. Stress however also may prepare the immune system for challenges such as wounding or infection, which are likely to happen during a fight or flight stress response.MethodsIn common carp (Cyprinus carpio L.) we studied the stress-...
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| Format: | Article |
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Frontiers Media S.A.
2024-03-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1330995/full |
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| author | Katarzyna Klak Katarzyna Klak Magdalena Maciuszek Lukasz Pijanowski Magdalena Marcinkowska Magdalena Marcinkowska Joanna Homa B. M. Lidy Verburg-van Kemenade Krzysztof Rakus Magdalena Chadzinska |
| author_facet | Katarzyna Klak Katarzyna Klak Magdalena Maciuszek Lukasz Pijanowski Magdalena Marcinkowska Magdalena Marcinkowska Joanna Homa B. M. Lidy Verburg-van Kemenade Krzysztof Rakus Magdalena Chadzinska |
| author_sort | Katarzyna Klak |
| collection | DOAJ |
| description | IntroductionStress may pose a serious challenge to immune homeostasis. Stress however also may prepare the immune system for challenges such as wounding or infection, which are likely to happen during a fight or flight stress response.MethodsIn common carp (Cyprinus carpio L.) we studied the stress-induced redistribution of neutrophils into circulation, and the expression of genes encoding CXC chemokines known to be involved in the regulation of neutrophil retention (CXCL12) and redistribution (CXCL8), and their receptors (CXCR4 and CXCR1-2, respectively) in blood leukocytes and in the fish hematopoietic organ – the head kidney. The potential involvement of CXC receptors and stress hormone receptors in stress-induced neutrophil redistribution was determined by an in vivo study with selective CXCR inhibitors and antagonists of the receptors involved in stress regulation: glucocorticoid/mineralocorticoid receptors (GRs/MRs), adrenergic receptors (ADRs) and the melanocortin 2 receptor (MC2R).ResultsThe stress-induced increase of blood neutrophils was accompanied by a neutrophil decrease in the hematopoietic organs. This increase was cortisol-induced and GR-dependent. Moreover, stress upregulated the expression of genes encoding CXCL12 and CXCL8 chemokines, their receptors, and the receptor for granulocytes colony-stimulation factor (GCSFR) and matrix metalloproteinase 9 (MMP9). Blocking of the CXCR4 and CXCR1 and 2 receptors with selective inhibitors inhibited the stress-induced neutrophil redistribution and affected the expression of genes encoding CXC chemokines and CXCRs as well as GCSFR and MMP9.DiscussionOur data demonstrate that acute stress leads to the mobilization of the immune system, characterized by neutrophilia. CXC chemokines and CXC receptors are involved in this stress-induced redistribution of neutrophils from the hematopoietic tissue into the peripheral blood. This phenomenon is directly regulated by interactions between cortisol and the GR/MR. Considering the pivotal importance of neutrophilic granulocytes in the first line of defense, this knowledge is important for aquaculture, but will also contribute to the mechanisms involved in the stress-induced perturbation in neutrophil redistribution as often observed in clinical practice. |
| first_indexed | 2024-03-07T14:03:12Z |
| format | Article |
| id | doaj.art-96439813d68a4d9e8ab60da28090086c |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-03-07T14:03:12Z |
| publishDate | 2024-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-96439813d68a4d9e8ab60da28090086c2024-03-07T04:41:26ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-03-011510.3389/fimmu.2024.13309951330995Evolutionarily conserved mechanisms regulating stress-induced neutrophil redistribution in fishKatarzyna Klak0Katarzyna Klak1Magdalena Maciuszek2Lukasz Pijanowski3Magdalena Marcinkowska4Magdalena Marcinkowska5Joanna Homa6B. M. Lidy Verburg-van Kemenade7Krzysztof Rakus8Magdalena Chadzinska9Department of Evolutionary Immunology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, PolandDoctoral School of Exact and Natural Sciences, Jagiellonian University, Krakow, PolandDepartment of Evolutionary Immunology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, PolandDepartment of Evolutionary Immunology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, PolandDepartment of Evolutionary Immunology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, PolandDoctoral School of Exact and Natural Sciences, Jagiellonian University, Krakow, PolandDepartment of Evolutionary Immunology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, PolandCell Biology and Immunology Group, Department of Animal Sciences, Wageningen University, Wageningen, NetherlandsDepartment of Evolutionary Immunology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, PolandDepartment of Evolutionary Immunology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, PolandIntroductionStress may pose a serious challenge to immune homeostasis. Stress however also may prepare the immune system for challenges such as wounding or infection, which are likely to happen during a fight or flight stress response.MethodsIn common carp (Cyprinus carpio L.) we studied the stress-induced redistribution of neutrophils into circulation, and the expression of genes encoding CXC chemokines known to be involved in the regulation of neutrophil retention (CXCL12) and redistribution (CXCL8), and their receptors (CXCR4 and CXCR1-2, respectively) in blood leukocytes and in the fish hematopoietic organ – the head kidney. The potential involvement of CXC receptors and stress hormone receptors in stress-induced neutrophil redistribution was determined by an in vivo study with selective CXCR inhibitors and antagonists of the receptors involved in stress regulation: glucocorticoid/mineralocorticoid receptors (GRs/MRs), adrenergic receptors (ADRs) and the melanocortin 2 receptor (MC2R).ResultsThe stress-induced increase of blood neutrophils was accompanied by a neutrophil decrease in the hematopoietic organs. This increase was cortisol-induced and GR-dependent. Moreover, stress upregulated the expression of genes encoding CXCL12 and CXCL8 chemokines, their receptors, and the receptor for granulocytes colony-stimulation factor (GCSFR) and matrix metalloproteinase 9 (MMP9). Blocking of the CXCR4 and CXCR1 and 2 receptors with selective inhibitors inhibited the stress-induced neutrophil redistribution and affected the expression of genes encoding CXC chemokines and CXCRs as well as GCSFR and MMP9.DiscussionOur data demonstrate that acute stress leads to the mobilization of the immune system, characterized by neutrophilia. CXC chemokines and CXC receptors are involved in this stress-induced redistribution of neutrophils from the hematopoietic tissue into the peripheral blood. This phenomenon is directly regulated by interactions between cortisol and the GR/MR. Considering the pivotal importance of neutrophilic granulocytes in the first line of defense, this knowledge is important for aquaculture, but will also contribute to the mechanisms involved in the stress-induced perturbation in neutrophil redistribution as often observed in clinical practice.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1330995/fullstressneutrophil redistributioncortisolCXC chemokinesCXC receptorsGCSFR |
| spellingShingle | Katarzyna Klak Katarzyna Klak Magdalena Maciuszek Lukasz Pijanowski Magdalena Marcinkowska Magdalena Marcinkowska Joanna Homa B. M. Lidy Verburg-van Kemenade Krzysztof Rakus Magdalena Chadzinska Evolutionarily conserved mechanisms regulating stress-induced neutrophil redistribution in fish Frontiers in Immunology stress neutrophil redistribution cortisol CXC chemokines CXC receptors GCSFR |
| title | Evolutionarily conserved mechanisms regulating stress-induced neutrophil redistribution in fish |
| title_full | Evolutionarily conserved mechanisms regulating stress-induced neutrophil redistribution in fish |
| title_fullStr | Evolutionarily conserved mechanisms regulating stress-induced neutrophil redistribution in fish |
| title_full_unstemmed | Evolutionarily conserved mechanisms regulating stress-induced neutrophil redistribution in fish |
| title_short | Evolutionarily conserved mechanisms regulating stress-induced neutrophil redistribution in fish |
| title_sort | evolutionarily conserved mechanisms regulating stress induced neutrophil redistribution in fish |
| topic | stress neutrophil redistribution cortisol CXC chemokines CXC receptors GCSFR |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1330995/full |
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