Q51279071
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INTRODUCTION: Red blood cells (RBCs), also known as erythrocytes, are underestimated in their role in the immune system. In mammals, erythrocytes undergo maturation that involves the loss of nuclei, resulting in limited transcription and protein synthesis capabilities. However, the nucleated nature of non-mammalian RBCs is challenging this conventional understanding of RBCs. Notably, in bony fishes, research indicates that RBCs are not only susceptible to pathogen attacks but express immune receptors and effector molecules. However, given the abundance of RBCs and their interaction with every physiological system, we postulate that they act in surveillance as sentinels, rapid responders, and messengers. METHODS: We performed a series of in vitro experiments with Cyprinus carpio RBCs exposed to Aeromonas hydrophila, as well as in vivo laboratory infections using different concentrations of bacteria. RESULTS: qPCR revealed that RBCs express genes of several inflammatory cytokines. Using cyprinid-specific antibodies, we confirmed that RBCs secreted tumor necrosis factor alpha (TNFα) and interferon gamma (IFNγ). In contrast to these indirect immune mechanisms, we observed that RBCs produce reactive oxygen species and, through transmission electron and confocal microscopy, that RBCs can engulf particles. Finally, RBCs expressed and upregulated several putative toll-like receptors, including tlr4 and tlr9, in response to A. hydrophila infection in vivo. DISCUSSION: Overall, the RBC repertoire of pattern recognition receptors, their secretion of effector molecules, and their swift response make them immune sentinels capable of rapidly detecting and signaling the presence of foreign pathogens. By studying the interaction between a bacterium and erythrocytes, we provide novel insights into how the latter may contribute to overall innate and adaptive immune responses of teleost fishes.
- MeSH
- Aeromonas hydrophila * imunologie MeSH
- cytokiny * metabolismus imunologie MeSH
- erytrocyty * imunologie metabolismus MeSH
- fagocytóza imunologie MeSH
- gramnegativní bakteriální infekce * imunologie MeSH
- kapři * imunologie mikrobiologie MeSH
- nemoci ryb * imunologie mikrobiologie MeSH
- PAMP struktury imunologie MeSH
- přirozená imunita MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
The myxozoan parasite Tetracapsuloides bryosalmonae is the causative agent of proliferative kidney disease (PKD)-a disease of salmonid fishes, notably of the commercially farmed rainbow trout Oncorhynchus mykiss. Both wild and farmed salmonids are threatened by this virulent/deadly disease, a chronic immunopathology characterized by massive lymphocyte proliferation and hyperplasia, which manifests as swollen kidneys in susceptible hosts. Studying the immune response towards the parasite helps us understand the causes and consequences of PKD. While examining the B cell population during a seasonal outbreak of PKD, we unexpectedly detected the B cell marker immunoglobulin M (IgM) on red blood cells (RBCs) of infected farmed rainbow trout. Here, we studied the nature of this IgM and this IgM+ cell population. We verified the presence of surface IgM via parallel approaches: flow cytometry, microscopy, and mass spectrometry. The levels of surface IgM (allowing complete resolution of IgM- RBCs from IgM+ RBCs) and frequency of IgM+ RBCs (with up to 99% of RBCs being positive) have not been described before in healthy fishes nor those suffering from disease. To assess the influence of the disease on these cells, we profiled the transcriptomes of teleost RBCs in health and disease. Compared to RBCs originating from healthy fish, PKD fundamentally altered RBCs in their metabolism, adhesion, and innate immune response to inflammation. In summary, RBCs play a larger role in host immunity than previously appreciated. Specifically, our findings indicate that the nucleated RBCs of rainbow trout interact with host IgM and contribute to the immune response in PKD.
- MeSH
- B-lymfocyty MeSH
- erytrocyty MeSH
- imunoglobulin M MeSH
- nemoci ledvin * MeSH
- Oncorhynchus mykiss * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Myxozoa is a group of endoparasitic cnidarians covering almost 2600 species but merely 53 species, mostly from the genus Chloromyxum, have been reported from sharks, rays, and skates (Elasmobranchii). Elasmobranchs play a key role in the study of evolutionary trajectories of myxozoans as they represent ancestral vertebrate hosts. Our study provides new data on Chloromyxum spp. from 57 elasmobranchs, covering 20 species from geographical regions and host groups not previously investigated, such as Lamniformes and Hexanchiformes, the most basal phylogenetic shark lineage. In total, 28% of elasmobranchs were infected with Chloromyxum spp., indicating high diversity. Of the seven distinguished species, six are formally described based on morphological, morphometric, and genetic (18S rDNA) data. Comprehensive co-phylogenetic analyses and ancestral state reconstruction revealed that parasite and host phylogenies are clearly correlated, resulting in a distinct phylogenetic separation of chloromyxids from selachid (shark) vs. batoid (ray and skate) hosts. Species infecting the most ancient elasmobranchs formed a sublineage, branching off in the middle of the Chloromyxum sensu stricto clade. Our findings indicate that chloromyxids likely invaded an ancestral elasmobranch prior the time of divergence of shark and batoid lineages. Our analyses did not show a clear phylogeographic pattern of Chloromyxum parasites, probably due to the cosmopolitan distribution and migratory behaviour of many elasmobranch hosts, but geographical sampling must be extended to confirm or refute this observation. This study provides a complex view on species diversity, phylogeny, evolution, host-parasite co-phylogeny, and the phylogeographic origin of Chloromyxum species from elasmobranchs. Our results highlight the importance of adding missing data from previously un- or undersampled geographical regions and host species which results in a more accurate estimate of myxozoan biodiversity and a better understanding of the evolution of this parasite group in their hosts and in the different oceans of our planet.
- MeSH
- Elasmobranchii * genetika parazitologie MeSH
- fylogeneze MeSH
- Myxozoa * genetika MeSH
- paraziti * MeSH
- ryby parazitologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Poly lactic-co-glycolic acid (PLGA) particles safely and effectively deliver pharmaceutical ingredients, with many applications approved for clinical use in humans. In fishes, PLGA particles are being considered as carriers of therapeutic drugs and vaccine antigens. However, existing studies focus mainly on vaccine antigens, the endpoint immune responses to these (e.g., improved antibody titres), without deeper understanding of whether fishes react to the carrier. To test whether or not PLGA are recognized by or interact at all with the immune system of a teleost fish, we prepared, characterized and injected PLGA microparticles intraperitoneally into common carp. The influx, phenotype of inflammatory leukocytes, and their capacity to produce reactive oxygen species and phagocytose PLGA microparticles were tested by flow cytometry, qPCR, and microscopy. PLGA microparticles were indeed recognized. However, they induced only transient recruitment of inflammatory leukocytes that was resolved 4 days later whereas only the smallest μm-sized particles were phagocytosed. The overall response resembled that described in mammals against foreign materials. Given the similarities between our findings and those described in mammals, PLGA particles can be adapted to play a dual role as both antigen and drug carriers in fishes, depending on the administered dose and their design.
Myxozoans are microscopic, metazoan, obligate parasites, belonging to the phylum Cnidaria. In contrast to the free-living lifestyle of most members of this taxon, myxozoans have complex life cycles alternating between vertebrate and invertebrate hosts. Vertebrate hosts are primarily fish, although they are also reported from amphibians, reptiles, trematodes, mollusks, birds and mammals. Invertebrate hosts include annelids and bryozoans. Most myxozoans are not overtly pathogenic to fish hosts, but some are responsible for severe economic losses in fisheries and aquaculture. In both scenarios, the interaction between the parasite and the host immune system is key to explain such different outcomes of this relationship. Innate immune responses contribute to the resistance of certain fish strains and species, and the absence or low levels of some innate and regulatory factors explain the high pathogenicity of some infections. In many cases, immune evasion explains the absence of a host response and allows the parasite to proliferate covertly during the first stages of the infection. In some infections, the lack of an appropriate regulatory response results in an excessive inflammatory response, causing immunopathological consequences that are worse than inflicted by the parasite itself. This review will update the available information about the immune responses against Myxozoa, with special focus on T and B lymphocyte and immunoglobulin responses, how these immune effectors are modulated by different biotic and abiotic factors, and on the mechanisms of immune evasion targeting specific immune effectors. The current and future design of control strategies for myxozoan diseases is based on understanding this myxozoan-fish interaction, and immune-based strategies such as improvement of innate and specific factors through diets and additives, host genetic selection, passive immunization and vaccination, are starting to be considered.
- MeSH
- adaptivní imunita * MeSH
- antiparazitární látky farmakologie MeSH
- B-lymfocyty imunologie metabolismus parazitologie MeSH
- imunitní únik MeSH
- imunoglobuliny imunologie metabolismus MeSH
- interakce hostitele a parazita MeSH
- Myxozoa účinky léků imunologie patogenita MeSH
- nemoci ryb imunologie metabolismus parazitologie prevence a kontrola MeSH
- parazitární nemoci u zvířat imunologie metabolismus parazitologie prevence a kontrola MeSH
- přirozená imunita * MeSH
- ryby imunologie metabolismus parazitologie MeSH
- T-lymfocyty imunologie metabolismus parazitologie MeSH
- vakcíny farmakologie MeSH
- vodní hospodářství MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
BACKGROUND: Lineage-specific gene expansions represent one of the driving forces in the evolutionary dynamics of unique phylum traits. Myxozoa, a cnidarian subphylum of obligate parasites, are evolutionarily altered and highly reduced organisms with a simple body plan including cnidarian-specific organelles and polar capsules (a type of nematocyst). Minicollagens, a group of structural proteins, are prominent constituents of nematocysts linking Myxozoa and Cnidaria. Despite recent advances in the identification of minicollagens in Myxozoa, the evolutionary history and diversity of minicollagens in Myxozoa and Cnidaria remain elusive. RESULTS: We generated new transcriptomes of two myxozoan species using a novel pipeline for filtering of closely related contaminant species in RNA-seq data. Mining of our transcriptomes and published omics data confirmed the existence of myxozoan Ncol-4, reported only once previously, and revealed a novel noncanonical minicollagen, Ncol-5, which is exclusive to Myxozoa. Phylogenetic analyses support a close relationship between myxozoan Ncol-1-3 with minicollagens of Polypodium hydriforme, but suggest independent evolution in the case of the myxozoan minicollagens Ncol-4 and Ncol-5. Additional genome- and transcriptome-wide searches of cnidarian minicollagens expanded the dataset to better clarify the evolutionary trajectories of minicollagen. CONCLUSIONS: The development of a new approach for the handling of next-generation data contaminated by closely related species represents a useful tool for future applications beyond the field of myxozoan research. This data processing pipeline allowed us to expand the dataset and study the evolution and diversity of minicollagen genes in Myxozoa and Cnidaria. We identified a novel type of minicollagen in Myxozoa (Ncol-5). We suggest that the large number of minicollagen paralogs in some cnidarians is a result of several recent large gene multiplication events. We revealed close juxtaposition of minicollagens Ncol-1 and Ncol-4 in myxozoan genomes, suggesting their common evolutionary history. The unique gene structure of myxozoan Ncol-5 suggests a specific function in the myxozoan polar capsule or tubule. Despite the fact that myxozoans possess only one type of nematocyst, their gene repertoire is similar to those of other cnidarians.
- MeSH
- fylogeneze MeSH
- genom MeSH
- Myxozoa * genetika MeSH
- paraziti * MeSH
- životní styl MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Myxozoans are highly diverse and globally distributed cnidarian endoparasites in freshwater and marine habitats. They have adopted a heteroxenous life cycle, including invertebrate and fish hosts, and have been associated with diseases in aquaculture and wild fish stocks. Despite their importance, genomic resources of myxozoans have proven difficult to obtain due to their miniaturized and derived genome character and close associations with fish tissues. The first 'omic' datasets have now become the main resource for a better understanding of host-parasite interactions, virulence, and diversity, but also the evolutionary history of myxozoans. In this review, we discuss recent genomic advances in the field and outline outstanding questions to be answered with continuous and improved efforts of generating myxozoan genomic data.
- MeSH
- genom genetika MeSH
- genomika trendy MeSH
- Myxozoa klasifikace genetika patogenita MeSH
- parazitární nemoci parazitologie přenos MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
Myxozoans are a diverse group of cnidarian parasites, including important pathogens in different aquaculture species, without effective legalized treatments for fish destined for human consumption. We tested the effect of natural feed additives on immune parameters of common carp and in the course of a controlled laboratory infection with the myxozoan Sphaerospora molnari. Carp were fed a base diet enriched with 0.5% curcumin or 0.12% of a multi-strain yeast fraction, before intraperitoneal injection with blood stages of S. molnari. We demonstrate the impact of these treatments on respiratory burst, phagocytosis, nitric oxide production, adaptive IgM+ B cell responses, S. molnari-specific antibody titers, and on parasite numbers. Both experimental diets enriched B cell populations prior to infection and postponed initial parasite proliferation in the blood. Curcumin-fed fish showed a decrease in reactive oxygen species, nitric oxide production and B cell density at late-stage infection, likely due to its anti-inflammatory properties, favoring parasite propagation. In contrast, multi-strain yeast fraction (MsYF)-fed fish harbored the highest S. molnari-specific antibody titer, in combination with the overall lowest parasite numbers. The results demonstrate that yeast products can be highly beneficial for the outcome of myxozoan infections and could be used as effective feed additives in aquaculture.
- Publikační typ
- časopisecké články MeSH
AIMS: As the most abundant cell population in the blood, erythrocytes represent an attractive source of nutrients and a protective niche to a number of pathogens. Previously, we observed the attachment of the myxozoan parasite Sphaerospora molnari to erythrocytes of its host, common carp (Cyprinus carpio), raising a number of questions about the nature of this interaction. METHODS AND RESULTS: We elucidated the impact of S molnari on the number of erythrocytes in healthy and immunocompromised fish, over a period of 6 weeks. While we observed only a mild decrease in RBC numbers in healthy individuals, we witnessed gradual and finally severe haemolytic anaemia in immunosuppressed fish. Accompanying this overt loss was increased erythropoiesis as represented by an increase of erythroblasts in the blood. In vitro, we demonstrated the uptake of host proteins from CFSE-labelled erythrocytes, ultimately inducing death of host RBCs, likely for nutrient gain of the parasite. Nevertheless, the results do not exclude a possible role of erythrocyte-derived proteins in immune evasion. CONCLUSION: Overall, the obtained data provide first evidence for the previously unknown appetite of myxozoan parasites for host erythrocytes and create an important framework for future investigations into the molecular mechanisms underlining this interaction.
- MeSH
- erytrocyty parazitologie MeSH
- erytropoéza fyziologie MeSH
- fylogeneze MeSH
- hemolytické anemie parazitologie MeSH
- kapři parazitologie MeSH
- Myxozoa fyziologie MeSH
- nemoci ryb parazitologie MeSH
- stravovací zvyklosti fyziologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Myxobolus pseudodispar Gorbunova, 1936 (Myxozoa) was originally described as a parasite of common roach, Rutilus rutilus (Linnaeus), with developing stages in muscles and spores disseminated in macrophage centres of different organs and tissues. Later, this parasite was described from several other cyprinids, but with relatively large intraspecific differences based on SSU rDNA gene sequences. Within our long-term study on myxozoan biodiversity, we performed a broad microscopic and molecular screening of various freshwater fish species (over 450 specimens, 36 species) from different localities. We investigated the cryptic species status of M. pseudodispar. Our analysis revealed four new unique SSU rDNA sequences of M. pseudodispar as well as an infection in new fish host species. Myxobolus pseudodispar sequence analysis showed clear phylogenetic grouping according to fish host criterion forming 13 well-recognised clades. Using 1% SSU rDNA-based genetic distance criterion, at least ten new species of Myxobolus Bütschli, 1882 may be recognised in the group of M. pseudodispar sequences. Our analysis showed the paraphyletic character of M. pseudodispar sequences and the statistical tests rejected hypothetical tree topology with the monophyletic status of the M. pseudodispar group. Myxobolus pseudodispar represents a species complex and it is a typical example of myxozoan hidden diversity phenomenon confirming myxozoans as an evolutionary very successful group of parasites with a great ability to adapt to a new hosts with subsequent speciation events.
- MeSH
- biodiverzita * MeSH
- biologická evoluce MeSH
- hostitelská specificita * MeSH
- interakce hostitele a parazita * MeSH
- Myxobolus klasifikace fyziologie MeSH
- parazitární nemoci u zvířat parazitologie MeSH
- ribozomální DNA analýza MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
