Mechanisms of circovirus immunosuppression and pathogenesis with a focus on porcine circovirus 2: a review

References

• Abadie J, Nguyen F, Groizeleau C, Amenna N, Fernandez B, Guereaud C, Guigand L, Robart P, Lefebvre B, Wyers M. 2001. Pigeon circovirus infection: pathological observations and suggested pathogenesis. Avian Pathol. 30(2):149–158. doi: 10.1080/03079450124811.
   PubMed Web of Science ®Google Scholar
• Ablasser A, Hur S. 2020. Regulation of cGAS- and RLR-mediated immunity to nucleic acids. Nat Immunol. 21(1):17–29. doi: 10.1038/s41590-019-0556-1.
   PubMed Web of Science ®Google Scholar
• Allan GM, McNeilly F, Ellis J, Krakowka S, Meehan B, McNair I, Walker I, Kennedy S. 2000. Experimental infection of colostrum deprived piglets with porcine circovirus 2 (PCV2) and porcine reproductive and respiratory syndrome virus (PRRSV) potentiates PCV2 replication. Arch Virol. 145(11):2421–2429. doi: 10.1007/s007050070031.
   PubMed Web of Science ®Google Scholar
• Allan GM, McNeilly F, Kennedy S, Daft B, Clarke EG, Ellis JA, Haines DM, Meehan BM, Adair BM. 1998. Isolation of porcine circovirus-like viruses from pigs with a wasting disease in the USA and Europe. J Vet Diagn Invest. 10(1):3–10. doi: 10.1177/104063879801000102.
   PubMed Web of Science ®Google Scholar
• Amoroso MG, Serra F, Esposito C, D’Alessio N, Ferrara G, Cioffi B, Anzalone A, Pagnini U, De Carlo E, Fusco G, et al. 2021. Prevalence of infection with porcine circovirus types 2 and 3 in the wild boar population in the campania region (Southern Italy). Animals (Basel). 11(11):3215. doi: 10.3390/ani11113215.
   PubMedGoogle Scholar
• Anderson A, Hartmann K, Leutenegger CM, Proksch AL, Mueller RS, Unterer S. 2017. Role of canine circovirus in dogs with acute haemorrhagic diarrhoea. Vet Rec. 180(22):542. doi: 10.1136/vr.103926.
   PubMed Web of Science ®Google Scholar
• Balmelli C, Steiner E, Moulin H, Peduto N, Herrmann B, Summerfield A, McCullough K. 2011. Porcine circovirus type 2 DNA influences cytoskeleton rearrangements in plasmacytoid and monocyte-derived dendritic cells. Immunology. 132(1):57–65. doi: 10.1111/j.1365-2567.2010.03339.x.
   PubMed Web of Science ®Google Scholar
• Borghetti P, Morganti M, Saleri R, Ferrari L, De Angelis E, Cavalli V, Cacchioli A, Corradi A, Martelli P. 2013. Innate pro-inflammatory and adaptive immune cytokines in PBMC of vaccinated and unvaccinated pigs naturally exposed to porcine circovirus type 2 (PCV2) infection vary with the occurrence of the disease and the viral burden. Vet Microbiol. 163(1-2):42–53. doi: 10.1016/j.vetmic.2012.12.007.
   PubMed Web of Science ®Google Scholar
• Cao J, Lin C, Wang H, Wang L, Zhou N, Jin Y, Liao M, Zhou J. 2015. Circovirus transport proceeds via direct interaction of the cytoplasmic dynein IC1 subunit with the viral capsid protein. J Virol. 89(5):2777–2791. doi: 10.1128/JVI.03117-14.
   PubMed Web of Science ®Google Scholar
• Cao L, Sun W, Lu H, Tian M, Xie C, Zhao G, Han J, Wang W, Zheng M, Du R, et al. 2018. Genetic variation analysis of PCV1 strains isolated from Guangxi Province of China in 2015. BMC Vet Res. 14(1):43. doi: 10.1186/s12917-018-1345-z.
   PubMed Web of Science ®Google Scholar
• Cao S, Zhang X, Edwards JP, Mosser DM. 2006. NF-kappaB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J Biol Chem. 281(36):26041–26050. doi: 10.1074/jbc.M602222200.
   PubMed Web of Science ®Google Scholar
• Cecere TE, Todd SM, Leroith T. 2012. Regulatory T cells in arterivirus and coronavirus infections: do they protect against disease or enhance it? Viruses. 4(5):833–846. doi: 10.3390/v4050833.
   PubMed Web of Science ®Google Scholar
• Chang HW, Jeng CR, Lin TL, Liu JJ, Chiou MT, Tsai YC, Chia MY, Jan TR, Pang VF. 2006. Immunopathological effects of porcine circovirus type 2 (PCV2) on swine alveolar macrophages by in vitro inoculation. Vet Immunol Immunopathol. 110(3–4):207–219. doi: 10.1016/j.vetimm.2005.09.016.
   PubMed Web of Science ®Google Scholar
• Chen M, Han J, Zhang Y, Duan D, Zhang S. 2016. Porcine circovirus type 2 induces type I interferon production via MyD88-IKKalpha-IRFs signaling rather than NF-kappaB in porcine alveolar macrophages in vitro. Res Vet Sci. 104:188–194. doi: 10.1016/j.rvsc.2015.12.016.
   PubMed Web of Science ®Google Scholar
• Choi CY, Choi YC, Park IB, Lee CH, Kang SJ, Chun T. 2018. The ORF5 protein of porcine circovirus type 2 enhances viral replication by dampening type I interferon expression in porcine epithelial cells. Vet Microbiol. 226:50–58. doi: 10.1016/j.vetmic.2018.10.005.
   PubMed Web of Science ®Google Scholar
• Choi CY, Oh HN, Jun Lee S, Chun T. 2015. ORF2 protein of porcine circovirus type 2 promotes phagocytic activity of porcine macrophages by inhibiting proteasomal degradation of complement component 1, q subcomponent binding protein (C1QBP) through physical interaction. J Gen Virol. 96(11):3294–3301. doi: 10.1099/jgv.0.000282.
   PubMed Web of Science ®Google Scholar
• Circella E, Legretto M, Pugliese N, Caroli A, Bozzo G, Accogli G, Lavazza A, Camarda A. 2014. Psittacine beak and feather disease-like illness in Gouldian finches (Chloebia gouldiae). Avian Dis. 58(3):482–487. doi: 10.1637/10745-121113Case.1.
   PubMed Web of Science ®Google Scholar
• Cui Y, Hou L, Pan Y, Feng X, Zhou J, Wang D, Guo J, Liu C, Shi Y, Sun T, et al. 2022. Reconstruction of the evolutionary origin, phylodynamics, and phylogeography of the porcine circovirus type 3. Front Microbiol. 13:898212. doi: 10.3389/fmicb.2022.898212.
   PubMed Web of Science ®Google Scholar
• Dankaona W, Mongkholdej E, Satthathum C, Piewbang C, Techangamsuwan S. 2022. Epidemiology, genetic diversity, and association of canine circovirus infection in dogs with respiratory disease. Sci Rep. 12(1):15445. doi: 10.1038/s41598-022-19815-z.
   PubMed Web of Science ®Google Scholar
• Darwich L, Balasch M, Plana-Duran J, Segales J, Domingo M, Mateu E. 2003a. Cytokine profiles of peripheral blood mononuclear cells from pigs with postweaning multisystemic wasting syndrome in response to mitogen, superantigen or recall viral antigens. J Gen Virol. 84(Pt 12):3453–3457. doi: 10.1099/vir.0.19364-0.
   PubMed Web of Science ®Google Scholar
• Darwich L, Mateu E. 2012. Immunology of porcine circovirus type 2 (PCV2). Virus Res. 164(1-2):61–67. doi: 10.1016/j.virusres.2011.12.003.
   PubMed Web of Science ®Google Scholar
• Darwich L, Pie S, Rovira A, Segales J, Domingo M, Oswald IP, Mateu E. 2003b. Cytokine mRNA expression profiles in lymphoid tissues of pigs naturally affected by postweaning multisystemic wasting syndrome. J Gen Virol. 84(Pt 8):2117–2125. doi: 10.1099/vir.0.19124-0.
   PubMed Web of Science ®Google Scholar
• Darwich L, Segales J, Mateu E. 2004. Pathogenesis of postweaning multisystemic wasting syndrome caused by Porcine circovirus 2: an immune riddle. Arch Virol. 149(5):857–874. doi: 10.1007/s00705-003-0280-9.
   PubMed Web of Science ®Google Scholar
• Darwich L, Segales J, Resendes A, Balasch M, Plana-Duran J, Mateu E. 2008. Transient correlation between viremia levels and IL-10 expression in pigs subclinically infected with porcine circovirus type 2 (PCV2). Res Vet Sci. 84(2):194–198. doi: 10.1016/j.rvsc.2007.04.005.
   PubMed Web of Science ®Google Scholar
• Deim Z, Dencső L, Erdélyi I, Valappil SK, Varga C, Pósa A, Makrai L, Rákhely G. 2019. Porcine circovirus type 3 detection in a Hungarian pig farm experiencing reproductive failures. Vet Rec. 185(3):84. doi: 10.1136/vr.104784.
   PubMed Web of Science ®Google Scholar
• Deng Z, Sun R, Han X, Zhang Y, Zhou Y, Shan Y, Xu J, Li X, He F, Fang W. 2022. Porcine circovirus 2 activates the PERK-reactive oxygen species axis to induce p53 phosphorylation with subsequent cell cycle arrest at s phase in favor of its replication. J Virol. 96(22):e0127422. doi: 10.1128/jvi.01274-22.
   PubMed Web of Science ®Google Scholar
• Dong VH, Tu PY, Tsai PC, Lin YH, Chang HL, Kuo TY, Chiou MT, Lin CN, Chung WB. 2015. Expression of Toll-like receptor signaling-related genes in pigs co-infected with porcine reproductive and respiratory syndrome virus and porcine circovirus type 2. Res Vet Sci. 101:180–186. doi: 10.1016/j.rvsc.2015.05.006.
   PubMed Web of Science ®Google Scholar
• Driessler F, Venstrom K, Sabat R, Asadullah K, Schottelius AJ. 2004. Molecular mechanisms of interleukin-10-mediated inhibition of NF-kappaB activity: a role for p50. Clin Exp Immunol. 135(1):64–73. doi: 10.1111/j.1365-2249.2004.02342.x.
   PubMed Web of Science ®Google Scholar
• Duan D, Zhang S, Li X, Guo H, Chen M, Zhang Y, Han J, Lv Y. 2014. Activation of the TLR/MyD88/NF-kappaB signal pathway contributes to changes in IL-4 and IL-12 production in piglet lymphocytes infected with porcine circovirus type 2 in vitro. PLoS One. 9(5):e97653. doi: 10.1371/journal.pone.0097653.
   PubMed Web of Science ®Google Scholar
• Du Q, Huang Y, Wang T, Zhang X, Chen Y, Cui B, Li D, Zhao X, Zhang W, Chang L, et al. 2016. Porcine circovirus type 2 activates PI3K/Akt and p38 MAPK pathways to promote interleukin-10 production in macrophages via Cap interaction of gC1qR. Oncotarget. 7(14):17492–17507. doi: 10.18632/oncotarget.7362.
   PubMedGoogle Scholar
• Du Q, Wu X, Wang T, Yang X, Wang Z, Niu Y, Zhao X, Liu SL, Tong D, Huang Y. 2018. Porcine circovirus Type 2 suppresses IL-12p40 induction via Capsid/gC1qR-mediated MicroRNAs and signalings. J Immunol. 201(2):533–547. doi: 10.4049/jimmunol.1800250.
   PubMed Web of Science ®Google Scholar
• Du Q, Zhang H, He M, Zhao X, He J, Cui B, Yang X, Tong D, Huang Y. 2019. Interleukin-10 promotes porcine circovirus type 2 persistent infection in mice and aggravates the tissue lesions by suppression of T cell infiltration. Front Microbiol. 10:2050. doi: 10.3389/fmicb.2019.02050.
   PubMed Web of Science ®Google Scholar
• Eaglesham JB, Kranzusch PJ. 2020. Conserved strategies for pathogen evasion of cGAS-STING immunity. Curr Opin Immunol. 66:27–34. doi: 10.1016/j.coi.2020.04.002.
   PubMed Web of Science ®Google Scholar
• Ellis J, Hassard L, Clark E, Harding J, Allan G, Willson P, Strokappe J, Martin K, McNeilly F, Meehan B, et al. 1998. Isolation of circovirus from lesions of pigs with postweaning multisystemic wasting syndrome. Can Vet J. 39(1):44–51.
   PubMed Web of Science ®Google Scholar
• Fanelli A, Pellegrini F, Camero M, Catella C, Buonavoglia D, Fusco G, Martella V, Lanave G. 2022. Genetic diversity of porcine circovirus types 2 and 3 in wild boar in Italy. Animals (Basel. 12(8):953. doi: 10.3390/ani12080953.
   PubMedGoogle Scholar
• Feher E, Kaszab E, Bali K, Hoitsy M, Sos E, Banyai K. 2022. Novel circoviruses from birds share common evolutionary roots with fish origin circoviruses. Life (Basel. 12(3):368. doi: 10.3390/life12030368.
   PubMed Web of Science ®Google Scholar
• Gao Z, Dong Q, Jiang Y, Opriessnig T, Wang J, Quan Y, Yang Z. 2014b. ORF4-protein deficient PCV2 mutants enhance virus-induced apoptosis and show differential expression of mRNAs in vitro. Virus Res. 183:56–62. doi: 10.1016/j.virusres.2014.01.024.
   PubMed Web of Science ®Google Scholar
• Gao F, Xie JL, Jia CW, Ren HY, Zhou SH. 2014a. Effects of porcine circovirus type 2 and pseudorabies vaccine co-inoculation on regulatory cytokine mRNA expression in pig peripheral blood mononuclear cells. Genet Mol Res. 13(1):1540–1547. doi: 10.4238/2014.March.12.6.
   PubMed Web of Science ®Google Scholar
• Garcia-Sastre A. 2017. Ten strategies of interferon evasion by viruses. Cell Host Microbe. 22(2):176–184. doi: 10.1016/j.chom.2017.07.012.
   PubMed Web of Science ®Google Scholar
• Geng SC, Li XL, Fang WH. 2020. Porcine circovirus 3 capsid protein induces autophagy in HEK293T cells by inhibiting phosphorylation of the mammalian target of rapamycin. J Zhejiang Univ Sci B. 21(7):560–570. doi: 10.1631/jzus.B1900657.
   PubMed Web of Science ®Google Scholar
• Gilpin DF, McCullough K, Meehan BM, McNeilly F, McNair I, Stevenson LS, Foster JC, Ellis JA, Krakowka S, Adair BM, et al. 2003. In vitro studies on the infection and replication of porcine circovirus type 2 in cells of the porcine immune system. Vet Immunol Immunopathol. 94(3–4):149–161. doi: 10.1016/s0165-2427(03)00087-4.
   PubMed Web of Science ®Google Scholar
• Guo J, Tian J, Tan X, Yu H, Ding S, Sun H, Yu X. 2011. Pathological observations of an experimental infection of geese with goose circovirus. Avian Pathol. 40(1):55–61. doi: 10.1080/03079457.2010.538371.
   PubMed Web of Science ®Google Scholar
• Guo K, Xu L, Wu M, Hou Y, Jiang Y, Lv J, Xu P, Fan Z, Zhang R, Xing F, et al. 2018. A host factor GPNMB restricts porcine circovirus type 2 (PCV2) replication and interacts with PCV2 ORF5 protein. Front Microbiol. 9:3295. doi: 10.3389/fmicb.2018.03295.
   PubMed Web of Science ®Google Scholar
• Hansoongnern P, Phecharat N, Wasanasuk K, Tommeurd W, Chankeeree P, Lekcharoensuk C, Semkum P, Pinitkiatisakul S, Lekcharoensuk P. 2022. Encapsidated-CpG ODN enhances immunogenicity of porcine circovirus type 2 virus-like particles. Vet Microbiol. 275:109583. doi: 10.1016/j.vetmic.2022.109583.
   PubMed Web of Science ®Google Scholar
• Hasslung FC, Berg M, Allan GM, Meehan BM, McNeilly F, Fossum C. 2003. Identification of a sequence from the genome of porcine circovirus type 2 with an inhibitory effect on IFN-alpha production by porcine PBMCs. J Gen Virol. 84(Pt 11):2937–2945. doi: 10.1099/vir.0.19362-0.
   PubMed Web of Science ®Google Scholar
• Hayden MS, Ghosh S. 2014. Regulation of NF-kappaB by TNF family cytokines. Semin Immunol. 26(3):253–266. doi: 10.1016/j.smim.2014.05.004.
   PubMed Web of Science ®Google Scholar
• He J, Cao J, Zhou N, Jin Y, Wu J, Zhou J. 2013. Identification and functional analysis of the novel ORF4 protein encoded by porcine circovirus type 2. J Virol. 87(3):1420–1429. doi: 10.1128/JVI.01443-12.
   PubMed Web of Science ®Google Scholar
• Hong YT, Kang M, Jang HK. 2018. Pathogenesis of duck circovirus genotype 1 in experimentally infected Pekin ducks. Poult Sci. 97(9):3050–3057. doi: 10.3382/ps/pey177.
   PubMed Web of Science ®Google Scholar
• Hu X, Chen Z, Li Y, Ding Z, Zeng Q, Wan T, Wu H. 2022. Detection of porcine circovirus 1/2/3 and genetic analysis of porcine circovirus 2 in wild boar from Jiangxi Province of China. Animals (Basel. 12(16):2021. doi: 10.3390/ani12162021.
   PubMedGoogle Scholar
• Huang YL, Castaneda OA, Thongchan D, Khatri-Chhetri R, Tsai SS, Wu HY. 2017b. Pigeon circovirus infection in disqualified racing pigeons from Taiwan. Avian Pathol. 46(4):359–366. doi: 10.1080/03079457.2017.1284305.
   PubMed Web of Science ®Google Scholar
• Huang B, Li J, Zhang X, Zhao Q, Lu M, Lv Y. 2017a. RIG-1 and MDA-5 signaling pathways contribute to IFN-beta production and viral replication in porcine circovirus virus type 2-infected PK-15 cells in vitro. Vet Microbiol. 211:36–42. doi: 10.1016/j.vetmic.2017.09.022.
   PubMed Web of Science ®Google Scholar
• Huang HY, Silva BBI, Tsai SP, Tsai CY, Tyan YC, Lin TC, Flores RJD, Chuang KP. 2021. Immunogenicity and protective activity of pigeon circovirus recombinant capsid protein virus-like particles (PiCV rCap-VLPs) in pigeons (Columba livia) experimentally infected with PiCV. Vaccines (Basel). 9(2):98. doi: 10.3390/vaccines9020098.
   PubMed Web of Science ®Google Scholar
• Huang B, Zhang L, Lu M, Li J, Lv Y. 2018. PCV2 infection activates the cGAS/STING signaling pathway to promote IFN-beta production and viral replication in PK-15 cells. Vet Microbiol. 227:34–40. doi: 10.1016/j.vetmic.2018.10.027.
   PubMed Web of Science ®Google Scholar
• Igriczi B, Denes L, Biksi I, Albert E, Revesz T, Balka G. 2022. High prevalence of porcine circovirus 3 in hungarian pig herds: results of a systematic sampling protocol. Viruses. 14(6):1219. doi: 10.3390/v14061219.
   PubMed Web of Science ®Google Scholar
• Iizuka N, Kohara M, Hagino-Yamagishi K, Abe S, Komatsu T, Tago K, Arita M, Nomoto A. 1989. Construction of less neurovirulent polioviruses by introducing deletions into the 5’ noncoding sequence of the genome. J Virol. 63(12):5354–5363. doi: 10.1128/JVI.63.12.5354-5363.1989.
   PubMed Web of Science ®Google Scholar
• Jiang H, Wei L, Wang D, Wang J, Zhu S, She R, Liu T, Tian J, Quan R, Hou L, et al. 2020. ITRAQ-based quantitative proteomics reveals the first proteome profiles of piglets infected with porcine circovirus type 3. J Proteomics. 212:103598. doi: 10.1016/j.jprot.2019.103598.
   PubMed Web of Science ®Google Scholar
• Kaszab E, Lengyel G, Marton S, Dan A, Banyai K, Feher E. 2020. Occurrence and genetic diversity of CRESS DNA viruses in wild birds: a Hungarian study. Sci Rep. 10(1):7036. doi: 10.1038/s41598-020-63795-x.
   PubMed Web of Science ®Google Scholar
• Kekarainen T, Montoya M, Dominguez J, Mateu E, Segales J. 2008a. Porcine circovirus type 2 (PCV2) viral components immunomodulate recall antigen responses. Vet Immunol Immunopathol. 124(1-2):41–49. doi: 10.1016/j.vetimm.2008.01.031.
   PubMed Web of Science ®Google Scholar
• Kekarainen T, Montoya M, Mateu E, Segales J. 2008b. Porcine circovirus type 2-induced interleukin-10 modulates recall antigen responses. J Gen Virol. 89(Pt 3):760–765. doi: 10.1099/vir.0.83354-0.
   PubMed Web of Science ®Google Scholar
• Kim J, Ha Y, Chae C. 2006. Potentiation of porcine circovirus 2-induced postweaning multisystemic wasting syndrome by porcine parvovirus is associated with excessive production of tumor necrosis factor-alpha. Vet Pathol. 43(5):718–725. doi: 10.1354/vp.43-5-718.
   PubMed Web of Science ®Google Scholar
• Kim SH, Park JY, Jung JY, Kim HY, Park YR, Lee KK, Lyoo YS, Yeo SG, Park CK. 2018. Detection and genetic characterization of porcine circovirus 3 from aborted fetuses and pigs with respiratory disease in Korea. J Vet Sci. 19(5):721–724. doi: 10.4142/jvs.2018.19.5.721.
   PubMed Web of Science ®Google Scholar
• Kozdruń W, Woźniakowski G, Samorek-Salamonowicz E, Czekaj H. 2012. Viral infections in goose flocks in Poland. Pol J Vet Sci. 15(3):525–530. doi: 10.2478/v10181-012-0080-9.
   PubMed Web of Science ®Google Scholar
• Kroeger M, Temeeyasen G, Pineyro PE. 2022. Five years of porcine circovirus 3: what have we learned about the clinical disease, immune pathogenesis, and diagnosis. Virus Res. 314:198764. doi: 10.1016/j.virusres.2022.198764.
   PubMed Web of Science ®Google Scholar
• Lee AJ, Ashkar AA. 2018. The dual nature of type I and type II interferons. Front Immunol. 9:2061. doi: 10.3389/fimmu.2018.02061.
   PubMed Web of Science ®Google Scholar
• Li X, Chen S, Zhang L, Niu G, Zhang X, Yang L, Ji W, Ren L. 2022. Coinfection of porcine circovirus 2 and pseudorabies virus enhances immunosuppression and inflammation through NF-kappaB, JAK/STAT, MAPK, and NLRP3 pathways. IJMS. 23(8):4469. doi: 10.3390/ijms23084469.
   Web of Science ®Google Scholar
• Li J, Lu M, Huang B, Lv Y. 2018. Porcine circovirus type 2 inhibits inter-beta expression by targeting Karyopherin alpha-3 in PK-15 cells. Virology. 520:75–82. doi: 10.1016/j.virol.2018.05.008.
   PubMed Web of Science ®Google Scholar
• Liu J, Bai J, Zhang L, Jiang Z, Wang X, Li Y, Jiang P. 2013. Hsp70 positively regulates porcine circovirus type 2 replication in vitro. Virology. 447(1–2):52–62. doi: 10.1016/j.virol.2013.08.025.
   PubMed Web of Science ®Google Scholar
• Liu J, Chen I, Du Q, Chua H, Kwang J. 2006. The ORF3 protein of porcine circovirus type 2 is involved in viral pathogenesis in vivo. J Virol. 80(10):5065–5073. doi: 10.1128/JVI.80.10.5065-5073.2006.
   PubMed Web of Science ®Google Scholar
• Liu J, Chen I, Kwang J. 2005. Characterization of a previously unidentified viral protein in porcine circovirus type 2-infected cells and its role in virus-induced apoptosis. J Virol. 79(13):8262–8274. doi: 10.1128/JVI.79.13.8262-8274.2005.
   PubMed Web of Science ®Google Scholar
• Liu X, Shen H, Zhang X, Liang T, Ban Y, Yu L, Zhang L, Liu Y, Dong J, Zhang P, et al. 2021. Porcine circovirus type 3 capsid protein induces NF-kappaB activation and upregulates pro-inflammatory cytokine expression in HEK-293T cells. Arch Virol. 166(8):2141–2149. doi: 10.1007/s00705-021-05104-z.
   PubMed Web of Science ®Google Scholar
• Liu X, Wang Y, Han C, Li Q, Hou X, Song Q, Zhou S, Li H. 2022. TGF-beta from the porcine intestinal cell line IPEC-J2 induced by porcine circovirus 2 increases the frequency of treg cells via the activation of ERK (in CD4(+) T Cells) and NF-kappaB (in IPEC-J2). Viruses. 14(11):2466. doi: 10.3390/v14112466.
   PubMed Web of Science ®Google Scholar
• Li XD, Wu J, Gao D, Wang H, Sun L, Chen ZJ. 2013. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science. 341(6152):1390–1394. doi: 10.1126/science.1244040.
   PubMed Web of Science ®Google Scholar
• Luka PD, Adedeji AJ, Jambol AR, Ifende IV, Luka HG, Choji ND, Weka R, Settypalli TBK, Achenbach JE, Cattoli G, et al. 2022. Coinfections of African swine fever virus, porcine circovirus 2 and 3, and porcine parvovirus 1 in swine in Nigeria. Arch Virol. 167(12):2715–2722. doi: 10.1007/s00705-022-05593-6.
   PubMed Web of Science ®Google Scholar
• Lv Q, Guo K, Xu H, Wang T, Zhang Y. 2015. Identification of putative ORF5 protein of porcine circovirus type 2 and functional analysis of GFP-Fused ORF5 protein. PLoS One. 10(6):e0127859. doi: 10.1371/journal.pone.0127859.
   PubMed Web of Science ®Google Scholar
• Lv QZ, Guo KK, Zhang YM. 2014. Current understanding of genomic DNA of porcine circovirus type 2. Virus Genes. 49(1):1–10. doi: 10.1007/s11262-014-1099-z.
   PubMed Web of Science ®Google Scholar
• Lv J, Jiang Y, Feng Q, Fan Z, Sun Y, Xu P, Hou Y, Zhang X, Fan Y, Xu X, et al. 2020. Porcine circovirus type 2 ORF5 protein induces autophagy to promote viral replication via the PERK-eIF2alpha-ATF4 and mTOR-ERK1/2-AMPK signaling pathways in PK-15 cells. Front Microbiol. 11:320. doi: 10.3389/fmicb.2020.00320.
   PubMed Web of Science ®Google Scholar
• Ma X, Yan W, Zheng H, Du Q, Zhang L, Ban Y, Li N, Wei F. 2015. Regulation of IL-10 and IL-12 production and function in macrophages and dendritic cells. F1000Res. 4:1465. doi: 10.12688/f1000research.7010.1.
   Google Scholar
• Maizels RM, Smith KA. 2011. Regulatory T cells in infection. Adv Immunol. 112:73–136. doi: 10.1016/B978-0-12-387827-4.00003-6.
   PubMed Web of Science ®Google Scholar
• Meerts P, Misinzo G, Nauwynck HJ. 2005a. Enhancement of porcine circovirus 2 replication in porcine cell lines by IFN-gamma before and after treatment and by IFN-alpha after treatment. J Interferon Cytokine Res. 25(11):684–693. doi: 10.1089/jir.2005.25.684.
   PubMed Web of Science ®Google Scholar
• Meerts P, Van Gucht S, Cox E, Vandebosch A, Nauwynck HJ. 2005b. Correlation between type of adaptive immune response against porcine circovirus type 2 and level of virus replication. Viral Immunol. 18(2):333–341. doi: 10.1089/vim.2005.18.333.
   PubMed Web of Science ®Google Scholar
• Misinzo G, Delputte PL, Lefebvre DJ, Nauwynck HJ. 2009. Porcine circovirus 2 infection of epithelial cells is clathrin-, caveolae- and dynamin-independent, actin and Rho-GTPase-mediated, and enhanced by cholesterol depletion. Virus Res. 139(1):1–9. doi: 10.1016/j.virusres.2008.09.005.
   PubMed Web of Science ®Google Scholar
• Misinzo G, Delputte PL, Meerts P, Lefebvre DJ, Nauwynck HJ. 2006. Porcine circovirus 2 uses heparan sulfate and chondroitin sulfate B glycosaminoglycans as receptors for its attachment to host cells. J Virol. 80(7):3487–3494. doi: 10.1128/JVI.80.7.3487-3494.2006.
   PubMed Web of Science ®Google Scholar
• Misinzo G, Meerts P, Bublot M, Mast J, Weingartl HM, Nauwynck HJ. 2005. Binding and entry characteristics of porcine circovirus 2 in cells of the porcine monocytic line 3D4/31. J Gen Virol. 86(Pt 7):2057–2068. doi: 10.1099/vir.0.80652-0.
   PubMed Web of Science ®Google Scholar
• Mutthi P, Theerawatanasirikul S, Roytrakul S, Paemanee A, Lekcharoensuk C, Hansoongnern P, Petcharat N, Thangthamniyom N, Lekcharoensuk P. 2018. Interferon gamma induces cellular protein alteration and increases replication of porcine circovirus type 2 in PK-15 cells. Arch Virol. 163(11):2947–2957. doi: 10.1007/s00705-018-3944-1.
   PubMed Web of Science ®Google Scholar
• Nayar GP, Hamel A, Lin L. 1997. Detection and characterization of porcine circovirus associated with postweaning multisystemic wasting syndrome in pigs. Can Vet J. 38(6):385–386.
   PubMed Web of Science ®Google Scholar
• Niu G, Zhang X, Ji W, Chen S, Li X, Yang L, Zhang L, Ouyang H, Li C, Ren L. 2022. Porcine circovirus 4 rescued from an infectious clone is replicable and pathogenic in vivo. Transbound Emerg Dis. 69(5):e1632–e1641. doi: 10.1111/tbed.14498.
   PubMed Web of Science ®Google Scholar
• Opriessnig T, Karuppannan AK, Castro A, Xiao CT. 2020. Porcine circoviruses: current status, knowledge gaps and challenges. Virus Res. 286:198044. doi: 10.1016/j.virusres.2020.198044.
   PubMed Web of Science ®Google Scholar
• Ouyang T, Zhang X, Liu X, Ren L. 2019. Co-infection of swine with porcine circovirus type 2 and other swine viruses. Viruses. 11(2):185. doi: 10.3390/v11020185.
   PubMed Web of Science ®Google Scholar
• Palinski R, Pineyro P, Shang P, Yuan F, Guo R, Fang Y, Byers E, Hause BM. 2017. A novel porcine circovirus distantly related to known circoviruses is associated with porcine dermatitis and nephropathy syndrome and reproductive failure. J Virol. 91(1):e01879–16. doi: 10.1128/JVI.01879-16.
   PubMed Web of Science ®Google Scholar
• Pan Y, Li P, Jia R, Wang M, Yin Z, Cheng A. 2018. Regulation of apoptosis during porcine circovirus type 2 infection. Front Microbiol. 9:2086. doi: 10.3389/fmicb.2018.02086.
   PubMed Web of Science ®Google Scholar
• Phan TG, Giannitti F, Rossow S, Marthaler D, Knutson TP, Li L, Deng X, Resende T, Vannucci F, Delwart E. 2016. Detection of a novel circovirus PCV3 in pigs with cardiac and multi-systemic inflammation. Virol J. 13(1):184. doi: 10.1186/s12985-016-0642-z.
   PubMed Web of Science ®Google Scholar
• Ramamoorthy S, Huang FF, Huang YW, Meng XJ. 2009. Interferon-mediated enhancement of in vitro replication of porcine circovirus type 2 is influenced by an interferon-stimulated response element in the PCV2 genome. Virus Res. 145(2):236–243. doi: 10.1016/j.virusres.2009.07.009.
   PubMed Web of Science ®Google Scholar
• Raue R, Schmidt V, Freick M, Reinhardt B, Johne R, Kamphausen L, Kaleta EF, Muller H, Krautwald-Junghanns ME. 2005. A disease complex associated with pigeon circovirus infection, young pigeon disease syndrome. Avian Pathol. 34(5):418–425. doi: 10.1080/03079450500267825.
   PubMed Web of Science ®Google Scholar
• Richmond O, Cecere TE, Erdogan E, Meng XJ, Pineyro P, Subramaniam S, Todd SM, LeRoith T. 2015. The PD-L1/CD86 ratio is increased in dendritic cells co-infected with porcine circovirus type 2 and porcine reproductive and respiratory syndrome virus, and the PD-L1/PD-1 axis is associated with anergy, apoptosis, and the induction of regulatory T-cells in porcine lymphocytes. Vet Microbiol. 180(3–4):223–229. doi: 10.1016/j.vetmic.2015.09.014.
   PubMed Web of Science ®Google Scholar
• Ritchie BW, Niagro FD, Lukert PD, Steffens WL, 3rd, Latimer KS. 1989. Characterization of a new virus from cockatoos with psittacine beak and feather disease. Virology. 171(1):83–88. doi: 10.1016/0042-6822(89)90513-8.
   PubMed Web of Science ®Google Scholar
• Robino P, Grego E, Rossi G, Bert E, Tramuta C, Stella MC, Bertoni P, Nebbia P. 2014. Molecular analysis and associated pathology of beak and feather disease virus isolated in Italy from young Congo African grey parrots (Psittacus erithacus) with an "atypical peracute form" of the disease. Avian Pathol. 43(4):333–344. doi: 10.1080/03079457.2014.934660.
   PubMed Web of Science ®Google Scholar
• Rojas JM, Alejo A, Martin V, Sevilla N. 2021. Viral pathogen-induced mechanisms to antagonize mammalian interferon (IFN) signaling pathway. Cell Mol Life Sci. 78(4):1423–1444. doi: 10.1007/s00018-020-03671-z.
   PubMed Web of Science ®Google Scholar
• Rosario K, Breitbart M, Harrach B, Segales J, Delwart E, Biagini P, Varsani A. 2017. Revisiting the taxonomy of the family Circoviridae: establishment of the genus Cyclovirus and removal of the genus Gyrovirus. Arch Virol. 162(5):1447–1463. doi: 10.1007/s00705-017-3247-y.
   PubMed Web of Science ®Google Scholar
• Rosell C, Segales J, Plana-Duran J, Balasch M, Rodriguez-Arrioja GM, Kennedy S, Allan GM, McNeilly F, Latimer KS, Domingo M. 1999. Pathological, immunohistochemical, and in-situ hybridization studies of natural cases of postweaning multisystemic wasting syndrome (PMWS) in pigs. J Comp Pathol. 120(1):59–78. doi: 10.1053/jcpa.1998.0258.
   PubMed Web of Science ®Google Scholar
• Rovira A, Balasch M, Segales J, Garcia L, Plana-Duran J, Rosell C, Ellerbrok H, Mankertz A, Domingo M. 2002. Experimental inoculation of conventional pigs with porcine reproductive and respiratory syndrome virus and porcine circovirus 2. J Virol. 76(7):3232–3239. doi: 10.1128/jvi.76.7.3232-3239.2002.
   PubMed Web of Science ®Google Scholar
• Sahindokuyucu I, Turkmen MB, Sumer T, Elhag AE, Alcigir ME, Yazici Z, Barry G, Gulbahar MY, Kul O. 2022. First detection and molecular characterisation of a pigeon aviadenovirus A and pigeon circovirus co-infection associated with Young Pigeon Disease Syndrome (YPDS) in Turkish pigeons (Columba livia domestica). Vet Med Sci. 8(1):139–149. doi: 10.1002/vms3.662.
   PubMed Web of Science ®Google Scholar
• Saikumar G, Das T. 2019. Porcine circovirus. In: Malik Y, Singh R, Yadav M, editors. Recent advances in animal virology. Singapore: Springer; p. 171–195. doi: 10.1007/978-981-13-9073-9_10.
   Google Scholar
• Schmidt V, Schlomer J, Luken C, Johne R, Biere B, Muller H, Krautwald-Junghanns ME. 2008. Experimental infection of domestic pigeons with pigeon circovirus. Avian Dis. 52(3):380–386. doi: 10.1637/8188-120407-Reg.
   PubMed Web of Science ®Google Scholar
• Schneider WM, Chevillotte MD, Rice CM. 2014. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol. 32:513–545. doi: 10.1146/annurev-immunol-032713-120231.
   PubMed Web of Science ®Google Scholar
• Schroder K, Hertzog PJ, Ravasi T, Hume DA. 2004. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol. 75(2):163–189. doi: 10.1189/jlb.0603252.
   PubMed Web of Science ®Google Scholar
• Shen H, Liu X, Zhang P, Wang S, Liu Y, Zhang L, Song C. 2020. Porcine circovirus 3 Cap inhibits type I interferon signaling through interaction with STAT2. Virus Res. 275:197804. doi: 10.1016/j.virusres.2019.197804.
   PubMed Web of Science ®Google Scholar
• Shi KC, Guo X, Ge XN, Liu Q, Yang HC. 2010. Cytokine mRNA expression profiles in peripheral blood mononuclear cells from piglets experimentally co-infected with porcine reproductive and respiratory syndrome virus and porcine circovirus type 2. Vet Microbiol. 140(1–2):155–160. doi: 10.1016/j.vetmic.2009.07.021.
   PubMed Web of Science ®Google Scholar
• Shivaprasad HL, Hill D, Todd D, Smyth JA. 2004. Circovirus infection in a Gouldian finch (Chloebia gouldiae). Avian Pathol. 33(5):525–529. doi: 10.1080/03079450400003585.
   PubMed Web of Science ®Google Scholar
• Sinha A, Shen HG, Schalk S, Beach NM, Huang YW, Meng XJ, Halbur PG, Opriessnig T. 2011. Porcine reproductive and respiratory syndrome virus (PRRSV) influences infection dynamics of porcine circovirus type 2 (PCV2) subtypes PCV2a and PCV2b by prolonging PCV2 viremia and shedding. Vet Microbiol. 152(3–4):235–246. doi: 10.1016/j.vetmic.2011.05.005.
   PubMed Web of Science ®Google Scholar
• Sipos W, Duvigneau JC, Willheim M, Schilcher F, Hartl RT, Hofbauer G, Exel B, Pietschmann P, Schmoll F. 2004. Systemic cytokine profile in feeder pigs suffering from natural postweaning multisystemic wasting syndrome (PMWS) as determined by semiquantitative RT-PCR and flow cytometric intracellular cytokine detection. Vet Immunol Immunopathol. 99(1–2):63–71. doi: 10.1016/j.vetimm.2004.01.001.
   PubMed Web of Science ®Google Scholar
• Sirisereewan C, Thanawongnuwech R, Kedkovid R. 2022. Current understanding of the pathogenesis of porcine circovirus 3. Pathogens. 11(1):64. doi: 10.3390/pathogens11010064.
   PubMed Web of Science ®Google Scholar
• Soike D, Kohler B, Albrecht K. 1999. A circovirus-like infection in geese related to a runting syndrome. Avian Pathol. 28(2):199–202. doi: 10.1080/03079459994939.
   PubMed Web of Science ®Google Scholar
• Song J, Hou L, Wang D, Wei L, Zhu S, Wang J, Quan R, Jiang H, Shi R, Liu J. 2021. Nucleolar phosphoprotein NPM1 interacts with porcine circovirus type 3 cap protein and facilitates viral replication. Front Microbiol. 12:679341. doi: 10.3389/fmicb.2021.679341.
   PubMed Web of Science ®Google Scholar
• Stanifer ML, Guo C, Doldan P, Boulant S. 2020. Importance of type I and III interferons at respiratory and intestinal barrier surfaces. Front Immunol. 11:608645. doi: 10.3389/fimmu.2020.608645.
   PubMed Web of Science ®Google Scholar
• Steiner E, Balmelli C, Herrmann B, Summerfield A, McCullough K. 2008. Porcine circovirus type 2 displays pluripotency in cell targeting. Virology. 378(2):311–322. doi: 10.1016/j.virol.2008.06.009.
   PubMed Web of Science ®Google Scholar
• Stenzel T, Dziewulska D, Śmiałek M, Tykałowski B, Kowalczyk J, Koncicki A. 2019. Comparison of the immune response to vaccination with pigeon circovirus recombinant capsid protein (PiCV rCP) in pigeons uninfected and subclinically infected with PiCV. PLoS One. 14(6):e0219175. doi: 10.1371/journal.pone.0219175.
   PubMed Web of Science ®Google Scholar
• Stenzel T, Dziewulska D, Tykałowski B, Koncicki A. 2020. The clinical infection with pigeon circovirus (PiCV) leads to lymphocyte B apoptosis but has no effect on lymphocyte T subpopulation. Pathogens. 9(8):632. doi: 10.3390/pathogens9080632.
   PubMed Web of Science ®Google Scholar
• Stenzel T, Koncicki A. 2017. The epidemiology, molecular characterization and clinical pathology of circovirus infections in pigeons - current knowledge. Vet Q. 37(1):166–174. doi: 10.1080/01652176.2017.1325972.
   PubMed Web of Science ®Google Scholar
• Stevenson LS, McCullough K, Vincent I, Gilpin DF, Summerfield A, Nielsen J, McNeilly F, Adair BM, Allan GM. 2006. Cytokine and C-reactive protein profiles induced by porcine circovirus type 2 experimental infection in 3-week-old piglets. Viral Immunol. 19(2):189–195. doi: 10.1089/vim.2006.19.189.
   PubMed Web of Science ®Google Scholar
• Sun R, Deng Z, Han X, Zhang Y, Zhou Y, Shan Y, Fang W, Li X. 2021. Porcine circovirus 2 manipulates the PERK-ERO1alpha axis of the endoplasmic reticulum to favor its replication by derepressing viral DNA from HMGB1 sequestration within nuclei. J Virol. 95(19):e0100921. doi: 10.1128/JVI.01009-21.
   PubMed Web of Science ®Google Scholar
• Sydler T, Bragger S, Handke M, Hartnack S, Lewis FI, Sidler X, Brugnera E. 2016. Latent porcine circovirus type 2-infected domestic pigs: a potential infection model for the effective development of vaccines against latent or chronic virus induced diseases. Vaccine. 34(8):1047–1053. doi: 10.1016/j.vaccine.2016.01.005.
   PubMed Web of Science ®Google Scholar
• Tang Q, Li S, Zhang H, Wei Y, Wu H, Liu J, Wang Y, Liu D, Zhang Z, Liu C. 2013. Correlation of the cyclin A expression level with porcine circovirus type 2 propagation efficiency. Arch Virol. 158(12):2553–2560. doi: 10.1007/s00705-013-1785-5.
   PubMed Web of Science ®Google Scholar
• Temeeyasen G, Lierman S, Arruda BL, Main R, Vannucci F, Gimenez-Lirola LG, Pineyro PE. 2020. Pathogenicity and immune response against porcine circovirus type 3 infection in caesarean-derived, colostrum-deprived pigs. J Gen Virol. 102(11):001502. doi: 10.1099/jgv.0.001502.
   Web of Science ®Google Scholar
• Tischer I, Rasch R, Tochtermann G. 1974. Characterization of papovavirus-and picornavirus-like particles in permanent pig kidney cell lines. Zentralbl Bakteriol Orig A. 226(2):153–167.
   PubMedGoogle Scholar
• Todd D, Scott AN, Fringuelli E, Shivraprasad HL, Gavier-Widen D, Smyth JA. 2007. Molecular characterization of novel circoviruses from finch and gull. Avian Pathol. 36(1):75–81. doi: 10.1080/03079450601113654.
   PubMed Web of Science ®Google Scholar
• Todd D, Weston J, Ball NW, Borghmans BJ, Smyth JA, Gelmini L, Lavazza A. 2001. Nucleotide sequence-based identification of a novel circovirus of canaries. Avian Pathol. 30(4):321–325. doi: 10.1080/03079450120066322.
   PubMed Web of Science ®Google Scholar
• Tu PY, Tsai PC, Lin YH, Liu PC, Chang HL, Kuo TY, Chung WB. 2015. Expression profile of Toll-like receptor mRNA in pigs co-infected with porcine reproductive and respiratory syndrome virus and porcine circovirus type 2. Res Vet Sci. 98:134–141. doi: 10.1016/j.rvsc.2014.12.003.
   PubMed Web of Science ®Google Scholar
• Vargas-Bermudez DS, Mogollon JD, Jaime J. 2022. The prevalence and genetic diversity of PCV3 and PCV2 in Colombia and PCV4 survey during 2015-2016 and 2018-2019. Pathogens. 11(6):633. doi: 10.3390/pathogens11060633.
   PubMed Web of Science ®Google Scholar
• Vincent IE, Balmelli C, Meehan B, Allan G, Summerfield A, McCullough KC. 2007. Silencing of natural interferon producing cell activation by porcine circovirus type 2 DNA. Immunology. 120(1):47–56. doi: 10.1111/j.1365-2567.2006.02476.x.
   PubMed Web of Science ®Google Scholar
• Vincent IE, Carrasco CP, Guzylack-Piriou L, Herrmann B, McNeilly F, Allan GM, Summerfield A, McCullough KC. 2005. Subset-dependent modulation of dendritic cell activity by circovirus type 2. Immunology. 115(3):388–398. doi: 10.1111/j.1365-2567.2005.02165.x.
   PubMed Web of Science ®Google Scholar
• Vincent IE, Carrasco CP, Herrmann B, Meehan BM, Allan GM, Summerfield A, McCullough KC. 2003. Dendritic cells harbor infectious porcine circovirus type 2 in the absence of apparent cell modulation or replication of the virus. J Virol. 77(24):13288–13300. doi: 10.1128/jvi.77.24.13288-13300.2003.
   PubMed Web of Science ®Google Scholar
• Walker FC, Sridhar PR, Baldridge MT. 2021. Differential roles of interferons in innate responses to mucosal viral infections. Trends Immunol. 42(11):1009–1023. doi: 10.1016/j.it.2021.09.003.
   PubMed Web of Science ®Google Scholar
• Wang Z, Chen J, Wu X, Ma D, Zhang X, Li R, Han C, Liu H, Yin X, Du Q, et al. 2021b. PCV2 targets cGAS to inhibit type I interferon induction to promote other DNA virus infection. PLoS Pathog. 17(9):e1009940. doi: 10.1371/journal.ppat.1009940.
   PubMed Web of Science ®Google Scholar
• Wang Z, Chen J, Zhang QG, Huang K, Ma D, Du Q, Tong D, Huang Y. 2022c. Porcine circovirus type 2 infection inhibits the activation of type I interferon signaling via capsid protein and host gC1qR. Vet Microbiol. 266:109354. doi: 10.1016/j.vetmic.2022.109354.
   PubMed Web of Science ®Google Scholar
• Wang T, Du Q, Niu Y, Zhang X, Wang Z, Wu X, Yang X, Zhao X, Liu SL, Tong D, et al. 2019. Cellular p32 is a critical regulator of porcine circovirus type 2 nuclear egress. J Virol. 93(23): doi: 10.1128/JVI.00979-19.
   Web of Science ®Google Scholar
• Wang T, Du Q, Wu X, Niu Y, Guan L, Wang Z, Zhao X, Liu SL, Tong D, Huang Y. 2018. Porcine MKRN1 modulates the replication and pathogenesis of porcine circovirus type 2 by inducing capsid protein ubiquitination and degradation. J Virol. 92(21):e00100–00118. doi: 10.1128/JVI.00100-18.
   PubMed Web of Science ®Google Scholar
• Wang X, Li L, Shang H, Zhou F, Wang C, Zhang S, Gao P, Guo P, Zhu R, Sun Z, et al. 2022b. Effects of duck circovirus on immune function and secondary infection of Avian Pathogenic Escherichia coli. Poult Sci. 101(5):101799. doi: 10.1016/j.psj.2022.101799.
   PubMed Web of Science ®Google Scholar
• Wang S, Li C, Sun P, Shi J, Wu X, Liu C, Peng Z, Han H, Xu S, Yang Y, et al. 2021a. PCV2 triggers PK-15 cell apoptosis through the PLC-IP3R-Ca(2+) signaling pathway. Front Microbiol. 12:674907. doi: 10.3389/fmicb.2021.674907.
   PubMed Web of Science ®Google Scholar
• Wang D, Mai J, Yang Y, Xiao CT, Wang N. 2022a. Current knowledge on epidemiology and evolution of novel porcine circovirus 4. Vet Res. 53(1):38. doi: 10.1186/s13567-022-01053-w.
   PubMed Web of Science ®Google Scholar
• Wang S, Ren X, Li J, Lin C, Zhou J, Zhou J, Gu J., 2020. NAP1L4 inhibits porcine circovirus type 2 replication via IFN-beta signaling pathway. Vet Microbiol. 246:108692. doi: 10.1016/j.vetmic.2020.108692.
   PubMed Web of Science ®Google Scholar
• Wei L, Kwang J, Wang J, Shi L, Yang B, Li Y, Liu J. 2008. Porcine circovirus type 2 induces the activation of nuclear factor kappa B by IkappaBalpha degradation. Virology. 378(1):177–184. doi: 10.1016/j.virol.2008.05.013.
   PubMed Web of Science ®Google Scholar
• Wei R, Trus I, Yang B, Huang L, Nauwynck HJ. 2018. Breed differences in PCV2 uptake and disintegration in porcine monocytes. Viruses. 10(10):562. doi: 10.3390/v10100562.
   PubMed Web of Science ®Google Scholar
• Wei, R., Van Renne, N., Nauwynck, H.J., 2019. Strain-dependent porcine circovirus type 2 (PCV2) entry and replication in T-lymphoblasts. Viruses, 911, 813. doi: 10.3390/v11090813.
   PubMed Web of Science ®Google Scholar
• Wei L, Zhu S, Wang J, Liu J. 2012. Activation of the phosphatidylinositol 3-kinase/Akt signaling pathway during porcine circovirus type 2 infection facilitates cell survival and viral replication. J Virol. 86(24):13589–13597. doi: 10.1128/JVI.01697-12.
   PubMed Web of Science ®Google Scholar
• Wei L, Zhu Z, Wang J, Liu J. 2009. JNK and p38 mitogen-activated protein kinase pathways contribute to porcine circovirus type 2 infection. J Virol. 83(12):6039–6047. doi: 10.1128/JVI.00135-09.
   PubMed Web of Science ®Google Scholar
• Wikstrom FH, Meehan BM, Berg M, Timmusk S, Elving J, Fuxler L, Magnusson M, Allan GM, McNeilly F, Fossum C. 2007. Structure-dependent modulation of alpha interferon production by porcine circovirus 2 oligodeoxyribonucleotide and CpG DNAs in porcine peripheral blood mononuclear cells. J Virol. 81(10):4919–4927. doi: 10.1128/JVI.02797-06.
   PubMed Web of Science ®Google Scholar
• Wu H, Hou C, Wang Z, Meng P, Chen H, Cao H. 2022. First complete genomic sequence analysis of porcine circovirus type 4 (PCV4) in wild boars. Vet Microbiol. 273:109547. doi: 10.1016/j.vetmic.2022.109547.
   PubMed Web of Science ®Google Scholar
• Wu X, Wang Z, Qiao D, Yuan Y, Han C, Yang N, Li R, Du Q, Tong D, Huang Y. 2021. Porcine circovirus type 2 infection attenuates the K63-linked ubiquitination of STING to inhibit IFN-beta induction via p38-MAPK pathway. Vet Microbiol. 258:109098. doi: 10.1016/j.vetmic.2021.109098.
   PubMed Web of Science ®Google Scholar
• Wu X, Wang X, Shi T, Luo L, Qiao D, Wang Z, Han C, Du Q, Tong D, Huang Y. 2019. Porcine Circovirus Type 2 Rep Enhances IL-10 Production in Macrophages via Activation of p38-MAPK Pathway. Viruses. 11(12):1141. doi: 10.3390/v11121141.
   PubMed Web of Science ®Google Scholar
• Xiang QW, Wang X, Xie ZJ, Sun YN, Zhu YL, Wang SJ, Liu HJ, Jiang SJ. 2012. ORF3 of duck circovirus: a novel protein with apoptotic activity. Vet Microbiol. 159(1-2):251–256. doi: 10.1016/j.vetmic.2012.03.045.
   PubMed Web of Science ®Google Scholar
• Xu T, Chen XM, Fu Y, Ai Y, Wang DM, Wei ZY, Li XS, Zheng LL, Chen HY. 2022. Cross-species transmission of an emerging porcine circovirus (PCV4): First molecular detection and retrospective investigation in dairy cows. Vet Microbiol. 273:109528. doi: 10.1016/j.vetmic.2022.109528.
   PubMed Web of Science ®Google Scholar
• Yang K, Jiao Z, Zhou D, Guo R, Duan Z, Tian Y. 2019. Development of a multiplex PCR to detect and discriminate porcine circoviruses in clinical specimens. BMC Infect Dis. 19(1):778. doi: 10.1186/s12879-019-4398-0.
   PubMed Web of Science ®Google Scholar
• Yang Z, Marthaler DG, Rovira A. 2022. Frequency of porcine circovirus 3 detection and histologic lesions in clinical samples from swine in the United States. J Vet Diagn Invest. 34(4):602–611. doi: 10.1177/10406387221099538.
   PubMed Web of Science ®Google Scholar
• Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, Hanada T, Takeda K, Akira S, Hoshijima M, et al. 2003. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol. 4(6):551–556. doi: 10.1038/ni938.
   PubMed Web of Science ®Google Scholar
• Zhang HH, Hu WQ, Li JY, Liu TN, Zhou JY, Opriessnig T, Xiao CT. 2020a. Novel circovirus species identified in farmed pigs designated as Porcine circovirus 4, Hunan province, China. Transbound Emerg Dis. 67(3):1057–1061. doi: 10.1111/tbed.13446.
   PubMed Web of Science ®Google Scholar
• Zhang H, Liu C, Cheng S, Wang X, Li W, Charreyre C, Audonnet JC, He Q. 2013. Porcine CD74 is involved in the inflammatory response activated by nuclear factor kappa B during porcine circovirus type 2 (PCV-2) infection. Arch Virol. 158(11):2285–2295. doi: 10.1007/s00705-013-1750-3.
   PubMed Web of Science ®Google Scholar
• Zhang L, Qiu S, Lu M, Huang C, Lv Y. 2020b. Nuclear transporter karyopherin subunit alpha 3 levels modulate Porcine circovirus type 2 replication in PK-15 cells. Virology. 548:31–38. doi: 10.1016/j.virol.2020.06.003.
   PubMed Web of Science ®Google Scholar
• Zhang P, Shen H, Liu X, Wang S, Liu Y, Xu Z, Song C. 2020c. Porcine circovirus type 3 cap inhibits type i interferon induction through interaction with G3BP1. Front Vet Sci. 7:594438. doi: 10.3389/fvets.2020.594438.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Sun R, Geng S, Shan Y, Li X, Fang W. 2019. Porcine circovirus type 2 induces ORF3-independent mitochondrial apoptosis via PERK activation and elevation of cytosolic calcium. J Virol. 93(7):e01784–01718. doi: 10.1128/JVI.01784-18.
   PubMed Web of Science ®Google Scholar
• Zhou J, Dai Y, Lin C, Zhang Y, Feng Z, Dong W, Jin Y, Yan Y, Zhou J, Gu J. 2020. Nucleolar protein NPM1 is essential for circovirus replication by binding to viral capsid. Virulence. 11(1):1379–1393. doi: 10.1080/21505594.2020.1832366.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Qi B, Gu Y, Xu F, Du H, Li X, Fang W. 2016. Porcine circovirus 2 deploys PERK pathway and GRP78 for its enhanced replication in PK-15 cells. Viruses. 8(2):56. doi: 10.3390/v8020056.
   PubMed Web of Science ®Google Scholar
• Zhu X, Bai J, Liu P, Wang X, Jiang P. 2016. Suppressor of cytokine signaling 3 plays an important role in porcine circovirus type 2 subclinical infection by downregulating proinflammatory responses. Sci Rep. 6:32538. doi: 10.1038/srep32538.
   PubMed Web of Science ®Google Scholar
• Zhu B, Zhou Y, Xu F, Shuai J, Li X, Fang W. 2012. Porcine circovirus type 2 induces autophagy via the AMPK/ERK/TSC2/mTOR signaling pathway in PK-15 cells. J Virol. 86(22):12003–12012. doi: 10.1128/JVI.01434-12.
   PubMed Web of Science ®Google Scholar