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Erschienen in: Archives of Virology 7/2020

12.05.2020 | Original Article

Studies on the clinical symptoms, virus distribution, and mRNA expression of several antiviral immunity-related genes in grass carp after infection with genotype II grass carp reovirus

Erschienen in: Archives of Virology | Ausgabe 7/2020

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Abstract

The viral hemorrhage disease caused by grass carp reovirus (GCRV) is a serious contagious disease of grass carp that mainly infects fingerlings and yearlings. Epidemiological studies have shown that GCRV genotype II is currently the prominent genotype. However, little is known about the histopathological characteristics, virus distribution, and expression of immunity-related genes in grass carp infected by GCRV genotype II. In this study, we found that grass carp infected by GCRV genotype II lost appetite, swam alone, and rolled, and their fins, eyes, operculum, oral cavity, abdomen, intestine, and muscles showed pronounced punctate hemorrhage. Congestion, swelling, deformation, thinning of membranes, dilatation and darkened color of nucleoli, cathepsis, erythrocyte infiltration, and vacuole formation were observed in some infected tissues. A qRT-PCR test showed that the 11 genome segments of GCRV had similar expression patterns in different tissues. The S8 segment, with unknown function and no homologous sequences, had the highest expression level, while the most conserved segment, L2, had the lowest expression level. GCRV particles were distributed in different tissues, especially in the intestine. In the infected intestine, the expression of various receptors and adaptor molecules was modulated at different levels. Pro-inflammatory cytokine interleukin-1β (IL-1β) expression was 2160.9 times higher than that in the control group. The upregulation of immunity-related genes activated the antiviral immunity pathways. Therefore, the intestine might play a dual role in mediating GCRV infection and the antiviral immune response. This study provides detailed information about the pathogenicity of GCRV and expression of immunity-related genes, laying the foundation for further research on virus control and treatment.
Literatur
1.
Zurück zum Zitat Fang Q, Shah S, Liang YY, Zhou HZ (2005) 3D reconstruction and capsid protein characterization of grass carp reovirus. Sci China Ser C: Life Sci 48(6):593–600CrossRef Fang Q, Shah S, Liang YY, Zhou HZ (2005) 3D reconstruction and capsid protein characterization of grass carp reovirus. Sci China Ser C: Life Sci 48(6):593–600CrossRef
2.
Zurück zum Zitat Wang Q, Zeng WW, Liu C, Zhang C, Wang YY, Shi CB, Wu SQ (2012) Complete genome sequence of a reovirus isolated from grass carp, indicating different genotypes of GCRV in China. J Virol 86(22):12466PubMedPubMedCentralCrossRef Wang Q, Zeng WW, Liu C, Zhang C, Wang YY, Shi CB, Wu SQ (2012) Complete genome sequence of a reovirus isolated from grass carp, indicating different genotypes of GCRV in China. J Virol 86(22):12466PubMedPubMedCentralCrossRef
3.
Zurück zum Zitat Tang YF, Zeng WW, Wang YY, Wang Q, Yin JY, Li YY, Wang CB, Bergmann SM, Gao CX, Hu HZ (2020) Comparison of the blood parameters and histopathology between grass carp infected with a virulent and avirulent isolates of genotype II grass carp reovirus. Microb Pathog 139:103859PubMedCrossRef Tang YF, Zeng WW, Wang YY, Wang Q, Yin JY, Li YY, Wang CB, Bergmann SM, Gao CX, Hu HZ (2020) Comparison of the blood parameters and histopathology between grass carp infected with a virulent and avirulent isolates of genotype II grass carp reovirus. Microb Pathog 139:103859PubMedCrossRef
4.
Zurück zum Zitat Wang T, Li JL, Lu LQ (2013) Quantitative in vivo and in vitro characterization of co-infection by two genetically distant grass carp reoviruses. J Gen Virol 94:1301–1309PubMedCrossRef Wang T, Li JL, Lu LQ (2013) Quantitative in vivo and in vitro characterization of co-infection by two genetically distant grass carp reoviruses. J Gen Virol 94:1301–1309PubMedCrossRef
5.
Zurück zum Zitat Wu ML, Cui K, Li HY, He JX, Chen HL, Jiang YY, Ren J (2016) Genomic characterization and evolution analysis of a mutant reovirus isolated from grass carp in Anhui. Arch Virol 161(5):1385–1387PubMedCrossRef Wu ML, Cui K, Li HY, He JX, Chen HL, Jiang YY, Ren J (2016) Genomic characterization and evolution analysis of a mutant reovirus isolated from grass carp in Anhui. Arch Virol 161(5):1385–1387PubMedCrossRef
6.
Zurück zum Zitat Pei C, Ke F, Chen ZY, Zhang QY (2014) Complete genome sequence and comparative analysis of grass carp reovirus strain 109 (GCReV-109) with other grass carp reovirus strains reveals no significant correlation with regional distribution. Arch Virol 159(9):2435–2440PubMedCrossRef Pei C, Ke F, Chen ZY, Zhang QY (2014) Complete genome sequence and comparative analysis of grass carp reovirus strain 109 (GCReV-109) with other grass carp reovirus strains reveals no significant correlation with regional distribution. Arch Virol 159(9):2435–2440PubMedCrossRef
7.
Zurück zum Zitat Zhang C, Wang Q, Shi CB, Zeng WW, Liu YK, Wu SQ (2010) Molecular analysis of grass carp reovirus HZ08 genome segments 1-3 and 5-6. Virus Genes 41:102–104PubMedCrossRef Zhang C, Wang Q, Shi CB, Zeng WW, Liu YK, Wu SQ (2010) Molecular analysis of grass carp reovirus HZ08 genome segments 1-3 and 5-6. Virus Genes 41:102–104PubMedCrossRef
8.
Zurück zum Zitat Wu H, Zhang YY, Lu XY, Xiao J, Feng PH, Hao F (2019) STAT1a and STAT1b of black carp play important roles in the innate immune defense against GCRV. Fish Shellfish Immunol 87:386–394PubMedCrossRef Wu H, Zhang YY, Lu XY, Xiao J, Feng PH, Hao F (2019) STAT1a and STAT1b of black carp play important roles in the innate immune defense against GCRV. Fish Shellfish Immunol 87:386–394PubMedCrossRef
9.
Zurück zum Zitat Su JG, Zhu ZY, Wang YP, Zou J, Wang N, Jang SH (2009) Grass carp reovirus activates RNAi pathway in rare minnow. Gobiocypris rarus. Aquaculture 289(1–2):1–5 Su JG, Zhu ZY, Wang YP, Zou J, Wang N, Jang SH (2009) Grass carp reovirus activates RNAi pathway in rare minnow. Gobiocypris rarus. Aquaculture 289(1–2):1–5
10.
11.
Zurück zum Zitat Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124(4):783–801PubMedCrossRef Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124(4):783–801PubMedCrossRef
12.
Zurück zum Zitat Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449(7164):819–826PubMedCrossRef Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449(7164):819–826PubMedCrossRef
14.
Zurück zum Zitat Li S, Lu LF, Wang ZX, Chen DD, Zhang YA (2016) Fish IRF6 is a positive regulator of IFN expression and involved in both of the MyD88 and TBK1 pathways. Fish Shellfish Immunol 57:262–268PubMedCrossRef Li S, Lu LF, Wang ZX, Chen DD, Zhang YA (2016) Fish IRF6 is a positive regulator of IFN expression and involved in both of the MyD88 and TBK1 pathways. Fish Shellfish Immunol 57:262–268PubMedCrossRef
15.
Zurück zum Zitat Fernández-Trujillo MA, Novel P, Manchado M, Sepulcre MP, Mulero V, Borrego JJ, Álvarez MC, Béjar J (2011) Three Mx genes with differential response to VNNV infection have been identified in gilthead seabream (Sparus aurata). Mol Immunol 48(9–10):1216–1223PubMedCrossRef Fernández-Trujillo MA, Novel P, Manchado M, Sepulcre MP, Mulero V, Borrego JJ, Álvarez MC, Béjar J (2011) Three Mx genes with differential response to VNNV infection have been identified in gilthead seabream (Sparus aurata). Mol Immunol 48(9–10):1216–1223PubMedCrossRef
16.
Zurück zum Zitat Rao YL, Su JG, Yang CR, Peng LM, Feng XL, Li QM (2013) Characterizations of two grass carp Ctenopharyngodon idella HMGB2 genes and potential roles in innate immunity. Dev Comp Immunol 41(2):164–177PubMedCrossRef Rao YL, Su JG, Yang CR, Peng LM, Feng XL, Li QM (2013) Characterizations of two grass carp Ctenopharyngodon idella HMGB2 genes and potential roles in innate immunity. Dev Comp Immunol 41(2):164–177PubMedCrossRef
17.
Zurück zum Zitat Rao YL, Su JG (2015) Insights into the antiviral immunity against grass carp (Ctenopharyngodon idella) reovirus (GCRV) in grass carp. J Immunol Res 2015:670437PubMedPubMedCentralCrossRef Rao YL, Su JG (2015) Insights into the antiviral immunity against grass carp (Ctenopharyngodon idella) reovirus (GCRV) in grass carp. J Immunol Res 2015:670437PubMedPubMedCentralCrossRef
18.
Zurück zum Zitat Tafalla C, Saint-Jean SR, Pérez-Prieto S (2006) Immunological consequences of the coinfection of brown trout (Salmo trutta) with infectious hematopoietic necrosis virus (IHNV) and infectious pancreatic necrosis virus (IPNV). Aquaculture 256:15–22CrossRef Tafalla C, Saint-Jean SR, Pérez-Prieto S (2006) Immunological consequences of the coinfection of brown trout (Salmo trutta) with infectious hematopoietic necrosis virus (IHNV) and infectious pancreatic necrosis virus (IPNV). Aquaculture 256:15–22CrossRef
19.
Zurück zum Zitat Zhang XS, Xu XY, Shen YB, Fang Y, Zhang Jh, Bai YL, Gu ST, Wang RQ, Chen TS, Li JL (2019) Myeloid differentiation factor 88 (Myd88) is involved in the innate immunity of black carp (Mylopharyngodon piceus) defense against pathogen infection. Fish Shellfish Immunol 94:220–229PubMedCrossRef Zhang XS, Xu XY, Shen YB, Fang Y, Zhang Jh, Bai YL, Gu ST, Wang RQ, Chen TS, Li JL (2019) Myeloid differentiation factor 88 (Myd88) is involved in the innate immunity of black carp (Mylopharyngodon piceus) defense against pathogen infection. Fish Shellfish Immunol 94:220–229PubMedCrossRef
20.
Zurück zum Zitat Pasare C, Medzhitov R (2004) Toll-like receptors and acquired immunity. Semin Immunol 16:23–26PubMedCrossRef Pasare C, Medzhitov R (2004) Toll-like receptors and acquired immunity. Semin Immunol 16:23–26PubMedCrossRef
21.
Zurück zum Zitat Lin YF, He J, Zeng RY, Li ZM, Luo ZY, Pan WQ, Weng SP, Guo CJ, He JG (2019) Deletion of the infectious spleen and kidney necrosis virus ORF069L reduces virulence to Mandarin fish Siniperca chuatsi. Fish Shellfish Immunol 95:328–335PubMedCrossRef Lin YF, He J, Zeng RY, Li ZM, Luo ZY, Pan WQ, Weng SP, Guo CJ, He JG (2019) Deletion of the infectious spleen and kidney necrosis virus ORF069L reduces virulence to Mandarin fish Siniperca chuatsi. Fish Shellfish Immunol 95:328–335PubMedCrossRef
22.
Zurück zum Zitat Guo CJ, He J, He JG (2019) The immune evasion strategies of fish viruses. Fish Shellfish Immunol 86:772–784PubMedCrossRef Guo CJ, He J, He JG (2019) The immune evasion strategies of fish viruses. Fish Shellfish Immunol 86:772–784PubMedCrossRef
23.
Zurück zum Zitat Wang B, Du HH, Huang HQ, Xian JA, Xia ZH, Hu YH (2019) Major histocompatibility complex class I (MHC Iα) of Japanese flounder (Paralichthys olivaceus) plays a critical role in defense against intracellular pathogen infection. Fish Shellfish Immunol 94:122–131PubMedCrossRef Wang B, Du HH, Huang HQ, Xian JA, Xia ZH, Hu YH (2019) Major histocompatibility complex class I (MHC Iα) of Japanese flounder (Paralichthys olivaceus) plays a critical role in defense against intracellular pathogen infection. Fish Shellfish Immunol 94:122–131PubMedCrossRef
24.
Zurück zum Zitat Su JG, Zhang RF, Dong J, Yang CR (2011) Evaluation of internal control genes for qRT-PCR normalization in tissues and cell culture for antiviral studies of grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 30(3):830–835PubMedCrossRef Su JG, Zhang RF, Dong J, Yang CR (2011) Evaluation of internal control genes for qRT-PCR normalization in tissues and cell culture for antiviral studies of grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 30(3):830–835PubMedCrossRef
25.
Zurück zum Zitat Liang B, Su JG (2019) Inducible nitric oxide synthase (iNOS) mediates vascular endothelial cell apoptosis in grass carp reovirus (GCRV)-induced hemorrhage. Int J Mol Sci 20(24):6335PubMedCentralCrossRef Liang B, Su JG (2019) Inducible nitric oxide synthase (iNOS) mediates vascular endothelial cell apoptosis in grass carp reovirus (GCRV)-induced hemorrhage. Int J Mol Sci 20(24):6335PubMedCentralCrossRef
26.
Zurück zum Zitat Attoui H, Becnel J, Belaganahalli S, Bergoin M, Brussaard CP, Chappell JD, Ciarlet M, del Vas M, Dermody TS, Dormitzer PR, Duncan R, Fang Q, Graham R, Guglielmi KM, Harding RM, Hillman B, Makkay A, Marzachi AC, Matthijnssens J, Mertens PPC, Milne RG, Mohd Jaafar F, Mori H, Noordeloos AA, Omura T, Patton JT, Rao S, Maan M, Stoltz D, Suzuki N, Upadhyaya NM, Wei C, Zhou H (2012) Part II-the double stranded RNA viruses. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Family Reoviridae. Elsevier Academic Press, San Diego, pp 541–637 Attoui H, Becnel J, Belaganahalli S, Bergoin M, Brussaard CP, Chappell JD, Ciarlet M, del Vas M, Dermody TS, Dormitzer PR, Duncan R, Fang Q, Graham R, Guglielmi KM, Harding RM, Hillman B, Makkay A, Marzachi AC, Matthijnssens J, Mertens PPC, Milne RG, Mohd Jaafar F, Mori H, Noordeloos AA, Omura T, Patton JT, Rao S, Maan M, Stoltz D, Suzuki N, Upadhyaya NM, Wei C, Zhou H (2012) Part II-the double stranded RNA viruses. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Family Reoviridae. Elsevier Academic Press, San Diego, pp 541–637
27.
Zurück zum Zitat Ng KKS, Arnold JJ, Cameron CE (2008) Structure-function relationships among RNA-dependent RNA polymerases. Curr Top Microbiol Immunol 320:137–156PubMedPubMedCentral Ng KKS, Arnold JJ, Cameron CE (2008) Structure-function relationships among RNA-dependent RNA polymerases. Curr Top Microbiol Immunol 320:137–156PubMedPubMedCentral
28.
Zurück zum Zitat Kim J, Tao Y, Reinisch KM, Harrison SC, Nibert ML (2004) Orthoreovirus and Aquareovirus core proteins: conserved enzymatic surfaces, but not protein-protein interfaces. Virus Res 101(1):15–28PubMedCrossRef Kim J, Tao Y, Reinisch KM, Harrison SC, Nibert ML (2004) Orthoreovirus and Aquareovirus core proteins: conserved enzymatic surfaces, but not protein-protein interfaces. Virus Res 101(1):15–28PubMedCrossRef
29.
30.
Zurück zum Zitat Parker JS, Broering TJ, Kim J, Higgins DE, Nibert ML (2002) Reovirus core protein μ2 determines the filamentous morphology of viral inclusion bodies by interacting with and stabilizing microtubules. J Virol 76(9):4483–4496PubMedPubMedCentralCrossRef Parker JS, Broering TJ, Kim J, Higgins DE, Nibert ML (2002) Reovirus core protein μ2 determines the filamentous morphology of viral inclusion bodies by interacting with and stabilizing microtubules. J Virol 76(9):4483–4496PubMedPubMedCentralCrossRef
31.
Zurück zum Zitat Zhang FX, Guo H, Zhang J, Yan LM, Chen QX, Yan SC, Fang Q (2015) VP5 autocleavage is required for efficient infection by in vitro recoated aquareovirus particles. J Gen Virol 96(7):1795–1800PubMedCrossRef Zhang FX, Guo H, Zhang J, Yan LM, Chen QX, Yan SC, Fang Q (2015) VP5 autocleavage is required for efficient infection by in vitro recoated aquareovirus particles. J Gen Virol 96(7):1795–1800PubMedCrossRef
32.
Zurück zum Zitat Chen QX, Guo H, Zhang FX, Fang Q (2018) N-terminal myristoylated VP5 is required for penetrating cell membrane and promoting infectivity in Aquareoviruses. Virol Sin 33:287–290PubMedPubMedCentralCrossRef Chen QX, Guo H, Zhang FX, Fang Q (2018) N-terminal myristoylated VP5 is required for penetrating cell membrane and promoting infectivity in Aquareoviruses. Virol Sin 33:287–290PubMedPubMedCentralCrossRef
33.
Zurück zum Zitat Odegard AL, Chandran K, Zhang X, Parker JS, Baker TS, Nibert ML (2004) Putative autocleavage of outer capsid protein μ1, allowing release of myristoylated peptide μ1N during particle uncoating, is critical for cell entry by reovirus. J Virol 78(16):8732–8745PubMedPubMedCentralCrossRef Odegard AL, Chandran K, Zhang X, Parker JS, Baker TS, Nibert ML (2004) Putative autocleavage of outer capsid protein μ1, allowing release of myristoylated peptide μ1N during particle uncoating, is critical for cell entry by reovirus. J Virol 78(16):8732–8745PubMedPubMedCentralCrossRef
34.
Zurück zum Zitat Liemann S, Chandran K, Baker TS, Nibert ML, Harrison SC (2002) Structure of the reovirus membrane-penetration protein, μ1, in a complex with its protector protein, σ3. Cell 108(2):283–295PubMedPubMedCentralCrossRef Liemann S, Chandran K, Baker TS, Nibert ML, Harrison SC (2002) Structure of the reovirus membrane-penetration protein, μ1, in a complex with its protector protein, σ3. Cell 108(2):283–295PubMedPubMedCentralCrossRef
35.
Zurück zum Zitat Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275(5304):1320–1323PubMedCrossRef Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275(5304):1320–1323PubMedCrossRef
36.
Zurück zum Zitat Gomatos PJ, Prakash O, Stamatos NM (1981) Small reovirus particles composed solely of sigma NS with specificity for binding different nucleic acids. J Virol 39(1):115–124PubMedPubMedCentralCrossRef Gomatos PJ, Prakash O, Stamatos NM (1981) Small reovirus particles composed solely of sigma NS with specificity for binding different nucleic acids. J Virol 39(1):115–124PubMedPubMedCentralCrossRef
37.
Zurück zum Zitat Key T, Read J, Nibert ML, Duncan R (2013) Piscine reovirus encodes a cytotoxic, non-fusogenic, integral membrane protein and previously unrecognized virion outer-capsid proteins. J Gen Virol 94:1039–1050PubMedCrossRef Key T, Read J, Nibert ML, Duncan R (2013) Piscine reovirus encodes a cytotoxic, non-fusogenic, integral membrane protein and previously unrecognized virion outer-capsid proteins. J Gen Virol 94:1039–1050PubMedCrossRef
38.
Zurück zum Zitat Hamming I, Timens W, Bulthuis MLC, Lely AT, Navis GJ, van Goor H (2004) Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol 203:631–637PubMedPubMedCentralCrossRef Hamming I, Timens W, Bulthuis MLC, Lely AT, Navis GJ, van Goor H (2004) Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol 203:631–637PubMedPubMedCentralCrossRef
39.
Zurück zum Zitat Aoki T, Hikima JI, Hwang SD, Jung TS (2013) Innate immunity of finfish: primordial conservation and function of viral RNA sensors in teleosts. Fish Shellfish Immunol 35(6):1689–1702PubMedCrossRef Aoki T, Hikima JI, Hwang SD, Jung TS (2013) Innate immunity of finfish: primordial conservation and function of viral RNA sensors in teleosts. Fish Shellfish Immunol 35(6):1689–1702PubMedCrossRef
40.
Zurück zum Zitat Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140(6):805–820PubMedCrossRef Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140(6):805–820PubMedCrossRef
41.
Zurück zum Zitat Yanai H, Ban T, Taniguchi T (2012) High-mobility group box family of proteins: ligand and sensor for innate immunity. Trends Immunol 33(12):633–640PubMedCrossRef Yanai H, Ban T, Taniguchi T (2012) High-mobility group box family of proteins: ligand and sensor for innate immunity. Trends Immunol 33(12):633–640PubMedCrossRef
42.
Zurück zum Zitat Bianchi ME, Celona B (2010) Ancient news: HMGBs are universal sentinels. J Mol Cell Biol 2(3):116–117PubMedCrossRef Bianchi ME, Celona B (2010) Ancient news: HMGBs are universal sentinels. J Mol Cell Biol 2(3):116–117PubMedCrossRef
43.
Zurück zum Zitat Goubau D, Deddouche S, Reis e Sousa C (2013) Cytosolic Sensing of Viruses. Immun 38(5):855–869CrossRef Goubau D, Deddouche S, Reis e Sousa C (2013) Cytosolic Sensing of Viruses. Immun 38(5):855–869CrossRef
44.
Zurück zum Zitat Palti Y (2011) Toll-like receptors in bony fish: from genomics to function. Dev Comp Immunol 35(12):1263–1272PubMedCrossRef Palti Y (2011) Toll-like receptors in bony fish: from genomics to function. Dev Comp Immunol 35(12):1263–1272PubMedCrossRef
45.
Zurück zum Zitat Verrier ER, Langevin C, Benmansour A, Boudinot P (2011) Early antiviral response and virus-induced genes in fish. Dev Comp Immunol 35(12):1204–1214PubMedCrossRef Verrier ER, Langevin C, Benmansour A, Boudinot P (2011) Early antiviral response and virus-induced genes in fish. Dev Comp Immunol 35(12):1204–1214PubMedCrossRef
46.
Zurück zum Zitat Yang CR, Chen LJ, Su JG, Feng XL, Rao YL (2013) Two novel homologs of high mobility group box 3 gene in grass carp (Ctenopharyngodon idella): potential roles in innate immune responses. Fish Shellfish Immunol 35(5):1501–1510PubMedCrossRef Yang CR, Chen LJ, Su JG, Feng XL, Rao YL (2013) Two novel homologs of high mobility group box 3 gene in grass carp (Ctenopharyngodon idella): potential roles in innate immune responses. Fish Shellfish Immunol 35(5):1501–1510PubMedCrossRef
47.
Zurück zum Zitat Yang CR, Peng LM, Su JG (2013) Two HMGB1 genes from grass carp Ctenopharyngodon idella mediate immune responses to viral/bacterial PAMPs and GCRV challenge. Dev Comp Immunol 39(3):133–146PubMedCrossRef Yang CR, Peng LM, Su JG (2013) Two HMGB1 genes from grass carp Ctenopharyngodon idella mediate immune responses to viral/bacterial PAMPs and GCRV challenge. Dev Comp Immunol 39(3):133–146PubMedCrossRef
48.
Zurück zum Zitat Yang CR, Su JG, Huang T, Zhang RF, Peng LM (2011) Identifcation of a retinoic acid-inducible gene I from grass carp (Ctenopharyngodon idella) and expression analysis in vivo and in vitro. Fish Shellfish Immunol 30(3):936–943PubMedCrossRef Yang CR, Su JG, Huang T, Zhang RF, Peng LM (2011) Identifcation of a retinoic acid-inducible gene I from grass carp (Ctenopharyngodon idella) and expression analysis in vivo and in vitro. Fish Shellfish Immunol 30(3):936–943PubMedCrossRef
49.
Zurück zum Zitat Dinarello CA (1988) Interleukin-1. Adv Pharmacol 6(1):51–95 Dinarello CA (1988) Interleukin-1. Adv Pharmacol 6(1):51–95
50.
Zurück zum Zitat Puhlmann M, Weinreich DM, Farma JM, Carroll NM, Turner EM, Alexander HR Jr (2005) Interleukin-1β induced vascular permeability is dependent on induction of endothelial tissue factor (TF) activity. J Transl Med 3:37PubMedPubMedCentralCrossRef Puhlmann M, Weinreich DM, Farma JM, Carroll NM, Turner EM, Alexander HR Jr (2005) Interleukin-1β induced vascular permeability is dependent on induction of endothelial tissue factor (TF) activity. J Transl Med 3:37PubMedPubMedCentralCrossRef
52.
Zurück zum Zitat Hakanpaa L, Kiss EA, Jacquemet G, Miinalainen I, Lerche M, Guzmán C, Mervaalad E, Eklunde L, Ivaskab J, Saharinen P (2018) Targeting β1-integrin inhibits vascular leakage in endotoxemia. Proc Natl Acad Sci USA 115(28):E6467–E6476PubMedCrossRef Hakanpaa L, Kiss EA, Jacquemet G, Miinalainen I, Lerche M, Guzmán C, Mervaalad E, Eklunde L, Ivaskab J, Saharinen P (2018) Targeting β1-integrin inhibits vascular leakage in endotoxemia. Proc Natl Acad Sci USA 115(28):E6467–E6476PubMedCrossRef
53.
Zurück zum Zitat Shui YM, Lu SY, Guo X, Liu XL, Fu BQ, Hu P, Qu LL, Liu NN, Li YS, Wang LL, Zhai FF, Ju DD, Liu ZS, Zhou Y, Ren HL (2018) Molecular characterization and differential expression analysis of interleukin 1β from Ovis aries. Microb Pathog 116:180–188PubMedCrossRef Shui YM, Lu SY, Guo X, Liu XL, Fu BQ, Hu P, Qu LL, Liu NN, Li YS, Wang LL, Zhai FF, Ju DD, Liu ZS, Zhou Y, Ren HL (2018) Molecular characterization and differential expression analysis of interleukin 1β from Ovis aries. Microb Pathog 116:180–188PubMedCrossRef
54.
Zurück zum Zitat Ochsenbein AF, Fehr T, Lutz C, Suter M, Brombacher F, Hengartner H, Zinkernagel RM (1999) Control of early viral and bacterial distribution and disease by natural antibodies. Science 286(5447):2156–2159PubMedCrossRef Ochsenbein AF, Fehr T, Lutz C, Suter M, Brombacher F, Hengartner H, Zinkernagel RM (1999) Control of early viral and bacterial distribution and disease by natural antibodies. Science 286(5447):2156–2159PubMedCrossRef
Metadaten
Titel
Studies on the clinical symptoms, virus distribution, and mRNA expression of several antiviral immunity-related genes in grass carp after infection with genotype II grass carp reovirus
Publikationsdatum
12.05.2020
Erschienen in
Archives of Virology / Ausgabe 7/2020
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-020-04654-y

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