Differences in inflammatory responses of rainbow trout infected by two genotypes of the myxozoan parasite Ceratonova shasta
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.
Grantová podpora
R01 GM085207
NIGMS NIH HHS - United States
PubMed
32846161
PubMed Central
PMC7655565
DOI
10.1016/j.dci.2020.103829
PII: S0145-305X(20)30384-0
Knihovny.cz E-zdroje
- Klíčová slova
- Cytokine, Fish disease, Immunoglobulin, Intestine, Salmonid,
- MeSH
- cytokiny genetika metabolismus MeSH
- genotyp * MeSH
- imunoglobulin M krev MeSH
- imunoglobuliny krev MeSH
- interakce hostitele a parazita MeSH
- Myxozoa genetika patogenita MeSH
- nemoci ryb imunologie MeSH
- Oncorhynchus mykiss imunologie MeSH
- parazitární nemoci u zvířat imunologie MeSH
- parazitární zátěž MeSH
- pohyb buněk MeSH
- rybí proteiny krev MeSH
- sliznice imunologie MeSH
- virulence MeSH
- zánět imunologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Názvy látek
- cytokiny MeSH
- immunoglobulin T, teleost MeSH Prohlížeč
- imunoglobulin M MeSH
- imunoglobuliny MeSH
- rybí proteiny MeSH
Two genotypes of the intestinal parasite Ceratonova shasta infect Oncorhynchus mykiss: genotype 0 results in a chronic infection with low mortality while genotype IIR causes disease with high mortality. We determined parasite load and the relative expression of six immune factors (IgT, IgM, IL-6, IL-8, IL-10, IFNG) in fish infected with either genotype over 29 days post-exposure. In genotype IIR infections the host responded with upregulation of inflammatory and regulatory cytokines. In contrast, genotype 0 infection did not elicit an inflammatory response and expression of IFNG and IL-10 was lower. Antibody expression was upregulated in both infections but appeared to have limited efficacy in the virulent genotype IIR infections. Histologically, in genotype 0 infections the parasite migrated through the tissue layers causing inflammation but minimal damage to the mucosal epithelium, which contrasts with the severe pathology found in genotype IIR infections.
Department of Biomedical Sciences 106 Dryden Hall Oregon State University Corvallis OR 97331 USA
Department of Microbiology 226 Nash Hall Oregon State University Corvallis OR 97331 USA
Faculty of Marine Science and Technology Fukui Prefectural University Obama Fukui Japan
Zobrazit více v PubMed
Abós B, Wang T, Castro R, Granja AG, Leal E, Havixbeck J, Luque A, Barreda DR, Secombes CJ, Tafalla C, 2016. Distinct differentiation programs triggered by IL-6 and LPS in teleost IgM+ B cells in the absence of germinal centers. Sci. Rep 6, 30004 10.1038/srep30004 PubMed DOI PMC
Abós B, Estensoro I, Perdiguero P, Faber M, Hu Y, Díaz Rosales P, Granja AG, Secombes CJ, Holland JW, Tafalla C, 2018. Dysregulation of B cell activity during proliferative kidney disease in rainbow trout. Front. Immunol 9 10.3389/fimmu.2018.01203 PubMed DOI PMC
Alama-Bermejo G, Holzer AS, Bartholomew JL, 2019. Myxozoan adhesion and virulence: Ceratonova shasta on the move. Microorganisms 7, 397 10.3390/microorganisms7100397 PubMed DOI PMC
Alama-Bermejo G, Meyer E, Atkinson SD, Holzer AS, Wísniewska MM, Kolísko M, Bartholomew JL, 2020. Transcriptome-wide comparisons and virulence gene polymorphisms of host-associated genotypes of the cnidarian parasite Ceratonova shasta in salmonids. Genome Biol. Evoln evaa109 10.1093/gbe/evaa109 PubMed DOI PMC
Atkinson SD, Bartholomew JL, 2010a. Disparate infection patterns of Ceratomyxa shasta (Myxozoa) in rainbow trout (Oncorhynchus mykiss) and Chinook salmon (Oncorhynchus tshawytscha) correlate with internal transcribed spacer-1 sequence variation in the parasite. Int. J. Parasitol 40, 599–604. 10.1016/j.ijpara.2009.10.010 PubMed DOI
Atkinson SD, Bartholomew JL, 2010b. Spatial, temporal and host factors structure the Ceratomyxa shasta (Myxozoa) population in the Klamath River basin. Infect. Genet. Evol 10, 1019–1026. 10.1016/j.meegid.2010.06.013 PubMed DOI
Atkinson SD, Hallett SL, Bartholomew JL, 2018. Genotyping of individual Ceratonova shasta (Cnidaria: Myxosporea) myxospores reveals intra-spore ITS-1 variation and invalidates the distinction of genotypes II and III. Parasitology 1–6. 10.1017/S0031182018000422 PubMed DOI
Bartholomew JL, 1998. Host resistance to infection by the myxosporean parasite Ceratomyxa shasta: a review. J. Aquat. Anim. Health 10, 112–120. 10.1577/1548-8667(1998)010<0112:HRTIBT>2.0.CO;2 DOI
Bartholomew JL, Ray E, Torell B, Whipple MJ, Heidel JR, 2004. Monitoring Ceratomyxa shasta infection during a hatchery rearing cycle: comparison of molecular, serological and histological methods. Dis. Aquat. Organ 62, 85–92. 10.3354/dao062085 PubMed DOI
Bartholomew JL, Smith CE, Rohovec JS, Fryer JL, 1989. Characterization of a host response to the myxosporean parasite, Ceratomyxa shasta (Noble), by histology, scanning electron microscopy and immunological techniques. J. Fish Dis 12, 509–522. 10.1111/j.1365-2761.1989.tb00561.x DOI
Bjork SJ, Bartholomew JL, 2010. Invasion of Ceratomyxa shasta (Myxozoa) and comparison of migration to the intestine between susceptible and resistant fish hosts. Int. J. Parasitol 40, 1087–1095. 10.1016/j.ijpara.2010.03.005 PubMed DOI
Bjork SJ, Bartholomew JL, 2009. Effects of Ceratomyxa shasta dose on a susceptible strain of rainbow trout and comparatively resistant Chinook and coho salmon. Dis. Aquat. Organ 86, 29–37. 10.3354/dao02092 PubMed DOI
Bjork SJ, Zhang Y-A, Hurst CN, Alonso-Naveiro ME, Alexander JD, Sunyer JO, Bartholomew JL, 2014. Defenses of susceptible and resistant Chinook salmon (Onchorhynchus tshawytscha) against the myxozoan parasite Ceratomyxa shasta. Fish Shellfish Immunol. 37, 87–95. 10.1016/j.fsi.2013.12.024 PubMed DOI PMC
Braden LM, Rasmussen KJ, Purcell SL, Ellis L, Mahony A, Cho S, Whyte SK, Jones SRM, Fast MD, 2018. Acquired protective immunity in Atlantic salmon Salmo salar against the myxozoan Kudoa thyrsites involves induction of MHIIβ+ CD83+ antigen-presenting cells. Infect. Immun 86, e00556–17. 10.1128/IAI.00556-17 PubMed DOI PMC
Cope A, Le Friec G, Cardone J, Kemper C, 2011. The Th1 life cycle: molecular control of IFN-γ to IL-10 switching. Trends Immunol. 32, 278–286. 10.1016/j.it.2011.03.010 PubMed DOI
Deloffre LAM, Andrade A, Filipe AI, Canario AVM, 2012. Reference genes to quantify gene expression during oogenesis in a teleost fish. Gene 506, 69–75. 10.1016/j.gene.2012.06.047 PubMed DOI
Fujiwara M, Mohr MS, Greenberg A, Foott JS, Bartholomew JL, 2011. Effects of ceratomyxosis on population dynamics of Klamath fall-run Chinook salmon. Trans. Am. Fish. Soc 140, 1380–1391. 10.1080/00028487.2011.621811 DOI
Gorgoglione B, Wang T, Secombes CJ, Holland JW, 2013. Immune gene expression profiling of Proliferative Kidney Disease in rainbow trout Oncorhynchus mykiss reveals a dominance of anti-inflammatory, antibody and T helper cell-like activities. Vet. Res 44, 55 10.1186/1297-9716-44-55 PubMed DOI PMC
Hallett SL, Bartholomew JL, 2006. Application of a real-time PCR assay to detect and quantify the myxozoan parasite Ceratomyxa shasta in river water samples. Dis. Aquat. Organ 71, 109–18. 10.3354/dao071109 PubMed DOI
Hallett SL, Ray RA, Hurst CN, Holt RA, Buckles GR, Atkinson SD, Bartholomew JL, 2012. Density of the waterborne parasite Ceratomyxa shasta and its biological effects on salmon. Appl. Environ. Microbiol 78, 3724–31. 10.1128/AEM.07801-11 PubMed DOI PMC
Hurst CN, Alexander JD, Dolan BP, Jia L, Bartholomew JL, 2019. Outcome of within-host competition demonstrates that parasite virulence doesn’t equal success in a myxozoan model system. Int. J. Parasitol. Parasites Wildl, 9, 25–35. 10.1016/j.ijppaw.2019.03.008 PubMed DOI PMC
Hurst CN, Bartholomew JL, 2012. Ceratomyxa shasta genotypes cause differential mortality in their salmonid hosts. J. Fish Dis 35, 725–732. 10.1111/j.1365-2761.2012.01407.x PubMed DOI
Pérez-Cordón G, Estensoro I, Benedito-Palos L, Calduch-Giner JA, Sitjà-Bobadilla A, Pérez-Sánchez J, 2014. Interleukin gene expression is strongly modulated at the local level in a fish–parasite model. Fish Shellfish Immunol. 37, 201–208. 10.1016/j.fsi.2014.01.022 PubMed DOI
Piazzon MC, Galindo-Villegas J, Pereiro P, Estensoro I, Calduch-Giner JA, Gómez-Casado E, Novoa B, Mulero V, Sitjà-Bobadilla A, Pérez-Sánchez J, 2016. Differential modulation of IgT and IgM upon parasitic, bacterial, viral, and dietary challenges in a perciform fish. Front. Immunol 7 10.3389/fimmu.2016.00637 PubMed DOI PMC
Ratliff DE, 1981. Ceratomyxa shasta: Epizootiology in Chinook Salmon of Central Oregon. Transactions of the American Fisheries Society 110, 507–513. 10.1577/1548-8659(1981)110<507:CS>2.0.CO;2 DOI
Ronza P, Robledo D, Bermúdez R, Losada AP, Pardo BG, Sitjà-Bobadilla A, Quiroga MI, Martínez P, 2016. RNA-seq analysis of early enteromyxosis in turbot (Scophthalmus maximus): new insights into parasite invasion and immune evasion strategies. Int. J. Parasitol 46, 507–517. 10.1016/j.ijpara.2016.03.007 PubMed DOI
Schmittgen TD, Livak KJ, 2008. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc 3, 1101–1108. 10.1038/nprot.2008.73 PubMed DOI
Sitjà-Bobadilla A, Diamant A, Palenzuela O, Alvarez-Pellitero P, 2007. Effect of host factors and experimental conditions on the horizontal transmission of Enteromyxum leei (Myxozoa) to gilthead sea bream, Sparus aurata L., and European sea bass, Dicentrarchus labrax (L.). J. Fish Dis 30, 243–250. 10.1111/j.1365-2761.2007.00804.x PubMed DOI
Soares MP, Teixeira L, Moita LF, 2017. Disease tolerance and immunity in host protection against infection. Nat. Rev. Immunol 17, 83–96. 10.1038/nri.2016.136 PubMed DOI
Stinson MET, Atkinson SD, Bartholomew JL, 2018. Host-specific genotypes of Ceratonova shasta (Cnidaria:Myxosporea) are widespread in the Pacific Northwest of North America. J. Parasitol 104, 645–650. 10.1645/18-79 PubMed DOI
Stinso MET, Bartholomew JL, 2012. Predicted redistribution of Ceratomyxa shasta genotypes with salmonid passage in the Deschutes River, Oregon. J. Aquat. Anim. Health 24, 274–280. 10.1080/08997659.2012.716012 PubMed DOI
Stocking RW, Holt RA, Foott JS, Bartholomew JL, 2006. Spatial and temporal occurrence of the salmonid parasite Ceratomyxa shasta in the Oregon–California Klamath River Basin. J. Aquat. Anim. Health 18, 194–202. 10.1577/H05-036.1 DOI
Zhang Y-A, Salinas I, Li J, Parra D, Bjork S, Xu Z, LaPatra SE, Bartholomew J, Sunyer JO, 2010. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol 11, 827–835. 10.1038/ni.1913 PubMed DOI PMC