Identification of key proteins of cytopathic biotype bovine viral diarrhoea virus involved in activating NF-κB pathway in BVDV-induced inflammatory response

References

• Machado G, Egocheaga RMF, Hein HE, et al. Bovine viral diarrhoea virus (BVDV) in dairy cattle: a matched case-control study. Transbound Emerg Dis. 2016;63:e1–13.
   PubMed Web of Science ®Google Scholar
• Lanyon SR, Hill FI, Reichel MP, et al. Bovine viral diarrhoea: pathogenesis and diagnosis. Vet J. 2014;199:201–209.
   PubMed Web of Science ®Google Scholar
• Richter V, Lebl K, Baumgartner W, et al. A systematic worldwide review of the direct monetary losses in cattle due to bovine viral diarrhoea virus infection. Vet J. 2017;220:80–87.
   PubMed Web of Science ®Google Scholar
• Collett MS, Larson R, Belzer SK, et al. Proteins encoded by bovine viral diarrhea virus: the genomic organization of a pestivirus. Virology. 1988;165:200–208.
   PubMed Web of Science ®Google Scholar
• Tautz N, Elbers K, Stoll D, et al. Serine protease of pestiviruses: determination of cleavage sites. J Virol. 1997;71:5415–5422.
   PubMed Web of Science ®Google Scholar
• Su A, Fu YG, Meens J, et al. Infection of polarized bovine respiratory epithelial cells by bovine viral diarrhea virus (BVDV). Virulence. 2021;12:177–187.
   PubMed Web of Science ®Google Scholar
• Wang Y, Feng B, Niu C, et al. Dendritic cell targeting of bovine viral diarrhea virus E2 protein expressed by Lactobacillus casei effectively induces antigen-specific immune responses via oral vaccination. Viruses. 2019;11:575.
   PubMed Web of Science ®Google Scholar
• Jia S, Huang X, Li H, et al. Immunogenicity evaluation of recombinant Lactobacillus casei W56 expressing bovine viral diarrhea virus E2 protein in conjunction with cholera toxin B subunit as an adjuvant. Microb Cell Fact. 2020;19:186.
   PubMedGoogle Scholar
• Karin M, Cao Y, Greten FR, et al. NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer. 2002;2:301–310.
   PubMed Web of Science ®Google Scholar
• Karin M, Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol. 2002;3:221–227.
   PubMed Web of Science ®Google Scholar
• Li Q, Verma IM. NF-kappaB regulation in the immune system. Nat Rev Immunol. 2002;2:725–734.
   PubMed Web of Science ®Google Scholar
• Siggers T, Chang AB, Teixeira A, et al. Principles of dimer-specific gene regulation revealed by a comprehensive characterization of NF-κB family DNA binding. Nat Immunol. 2011;13:95–102.
   PubMed Web of Science ®Google Scholar
• Smale ST. Dimer-specific regulatory mechanisms within the NF-κB family of transcription factors. Immunol Rev. 2012;246:193–204.
   PubMed Web of Science ®Google Scholar
• Zheng C, Yin Q, Wu H. Structural studies of NF-κB signaling. Cell Res. 2011;21:183–195.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Lenardo MJ, Baltimore D. 30 years of NF-kB: a blossoming of relevance to human pathobiology. Cell. 2017;168:37–57.
   PubMed Web of Science ®Google Scholar
• Zhang G, Ghosh S. Toll-like receptor-mediated NF-κB activation: a phylogenetically conserved paradigm in innate immunity. J Clin Invest. 2001;107:13–19.
   PubMed Web of Science ®Google Scholar
• Scherer DC, Brockman JA, Chen A, et al. Signal-induced degradation of IκBα requires site-specific ubiquitination. Proc Natl Acad Sci, USA. 1995;92:11259–11263.
   PubMed Web of Science ®Google Scholar
• Jimi E, Fei H, Nakatomi C. NF-κB signaling regulates physiological and pathological chondrogenesis. Int J Mol Sci. 2019;20:6275.
   PubMed Web of Science ®Google Scholar
• Yang F, Sheng X, Huang X, et al. Interactions between Salmonella and host macrophages—dissecting NF-κB signaling pathway responses. Microb Pathog. 2021;154:104846.
   PubMed Web of Science ®Google Scholar
• Xiao G, Harhaj EW, Sun SC. NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100. Mol Cell. 2001;7:401–409.
   PubMed Web of Science ®Google Scholar
• Sun SC. Non-canonical NF-κB signaling pathway. Cell Res. 2011;21:71–85.
   PubMed Web of Science ®Google Scholar
• Zarnegar BJ, Wang Y, Mahoney DJ, et al. Noncanonical NF-kappaB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol. 2008;9:1371–1378.
   PubMed Web of Science ®Google Scholar
• Wietek C, O’Neill LA. Diversity and regulation in the NF-kappaB system. Trends Biochem Sci. 2007;32:311–319.
   PubMed Web of Science ®Google Scholar
• Wang L, Qiao XY, Zhang SJ, et al. Porcine transmissible gastroenteritis virus nonstructural protein 2 contributes to inflammation via NF-κB activation. Virulence. 2018;9:1685–1698.
   PubMed Web of Science ®Google Scholar
• Santoro MG, Rossi A, Amici C. NF-kappaB and virus infection: who controls whom? Embo J. 2003;22:2552–2560.
   PubMed Web of Science ®Google Scholar
• Ma YY, Wang L, Jiang XX, et al. Integrative transcriptomics and proteomics analysis provide a deep insight into bovine viral diarrhea virus-host interactions during BVDV infection. Front Immunol. 2022;13:862828.
   PubMed Web of Science ®Google Scholar
• Gao X, Niu C, Wang Z, et al. Comprehensive analysis of lncRNA expression profiles in cytopathic biotype BVDV-infected MDBK cells provides an insight into biological contexts of host-BVDV interactions. Virulence. 2021;12:20–34.
   PubMed Web of Science ®Google Scholar
• Coates BM, Staricha KL, Nandini R, et al. Inhibition of the NOD-like receptor protein 3 inflammasome is protective in juvenile influenza a virus infection. Front Immunol. 2017;8:782.
   PubMed Web of Science ®Google Scholar
• Luan J, Zhang X, Wang S, et al. NOD-like receptor protein 3 inflammasome- dependent IL-1β accelerated conA-induced hepatitis. Front Immunol. 2018;9:758.
   PubMed Web of Science ®Google Scholar
• Oem JK, Jackel-Cram C, Li YP, et al. Hepatitis C virus non-structural protein-2 activates CXCL-8 transcription through NF-κB. Arch Virol. 2008;153:293–301.
   PubMed Web of Science ®Google Scholar
• Liu SQ, Gao X, Xie Y, et al. Rabies viruses of different virulence regulates inflammatory responses both in vivo and in vitro via MAPK and NF-κB pathway. Mol Immunol. 2020;125:70–82.
   PubMed Web of Science ®Google Scholar
• Lai FW, Stephenson KB, Mahony J, et al. Human coronavirus OC43 nucleocapsid protein binds microRNA and potentiates NF-κB activation. J Virol. 2014;88:54–65.
   PubMed Web of Science ®Google Scholar
• Cao L, Ge X, Gao Y, et al. Porcine epidemic diarrhea virus infection induces NF-κB activation through the TLR2, TLR3 and TLR9 pathways in porcine intestinal epithelial cells. J Gen Virol. 2015;96:1757–1767.
   PubMed Web of Science ®Google Scholar
• Merwaiss F, Czibener C, Alvarez DE. Cell-to-cell transmission is the main mechanism supporting bovine viral diarrhea virus spread in cell culture. J Virol. 2019;93. e01776-18. DOI:10.1128/JVI.01776-18.
   PubMed Web of Science ®Google Scholar
• Fredericksen F, Carrasco G, Villalba M, et al. Cytopathic BVDV-1 strain induces immune marker production in bovine cells through the NF-κB signaling pathway. Mol Immunol. 2015;68:213–222.
   PubMed Web of Science ®Google Scholar
• Maldonado N, Fredericksen F, Espiñeira C, et al. BVDV-1 induces interferon-beta gene expression through a pathway involving IRF1, IRF7, and NF-κB activation. Mol Immunol. 2020;128:33–40.
   PubMed Web of Science ®Google Scholar
• Daniels BP, Holman DW, Cruz-Orengo L, et al. Viral pathogen-associated molecular patterns regulate blood-brain barrier integrity via competing innate cytokine signals. MBio. 2014;5:e01476.
   PubMed Web of Science ®Google Scholar
• Ernandes MJ, Kagan JC, Cossart PF. Interferon-independent restriction of RNA virus entry and replication by a class of damage-associated molecular patterns. MBio. 2021;12. e00584-21. DOI:10.1128/mBio.00584-21.
   PubMed Web of Science ®Google Scholar
• Zhang C, Qin J, Zhang S, et al. ADP/P2Y1 aggravates inflammatory bowel disease through ERK5-mediated NLRP3 inflammasome activation. Mucosal Immunol. 2020;213:2931–2945.
   Google Scholar
• Lawrence TM, Hudacek AW, Zoete M, et al. Rabies virus is recognized by the NLRP3 inflammasome and activates interleukin-1β release in murine dendritic cells. J Virol. 2013;87:5848–5857.
   PubMed Web of Science ®Google Scholar
• Ito M, Yanagi Y, Ichinohe T, et al. Encephalomyocarditis virus viroporin 2B activates NLRP3 inflammasome. Plos Pathg. 2012;8:e1002857.
   PubMed Web of Science ®Google Scholar
• Ichinohe T, Pang IK, Iwasaki A. Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat Immunol. 2010;11:404–410.
   PubMed Web of Science ®Google Scholar
• Fan S, Jin Y, Deng S, et al. Activation of interleukin-1β release by the classical swine fever virus is dependent on the NLRP3 inflammasome, which affects virus growth in monocytes. Front Cell Infect Microbiol. 2018;8:225.
   PubMed Web of Science ®Google Scholar
• Chen W, Xu Y, Li H, et al. HCV genomic RNA activates the NLRP3 inflammasome in human myeloid cells. PLoS One. 2014;9:e84953.
   PubMed Web of Science ®Google Scholar
• Botto S, Abraham J, Mizuno N, et al. Human cytomegalovirus immediate early 86-kDa protein blocks transcription and induces degradation of the immature interleukin-1β protein during virion-mediated activation of the AIM2 inflammasome. MBio. 2019;10:e02510–18.
   PubMed Web of Science ®Google Scholar
• Hassan M, Selimovic D, Ghozlan H, et al. Induction of high-molecular-weight (HMW) tumor necrosis factor (TNF) alpha by hepatitis C virus (HCV) non-structural protein 3 (NS3) in liver cells is AP-1 and NF-κB-dependent activation. Cell Signal. 2007;19:301–311.
   PubMed Web of Science ®Google Scholar
• Subramaniam S, Kwon B, Beura LK, et al. Porcine reproductive and respiratory syndrome virus non-structural protein 1 suppresses tumor necrosis factor-alpha promoter activation by inhibiting NF-κB and Sp1. Virology. 2010;406:270–279.
   PubMed Web of Science ®Google Scholar
• Reed KE, Gorbalenya AE, Rice CM. The NS5A/NS5 proteins of viruses from three genera of the family Flaviviridae are phosphorylated by associated serine/threonine kinases. J Virol. 1998;72:6199–6206.
   PubMed Web of Science ®Google Scholar
• Brass V, Pal Z, Sapay N, et al. Conserved determinants for membrane association of nonstructural protein 5A from hepatitis C virus and related viruses. J Virol. 2007;81:2745–2757.
   PubMed Web of Science ®Google Scholar
• Gong G, Waris G, Tanveer R, et al. Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates STAT-3 and NF-kappa B. Proc Nat Acad Sci USA. 2001;98:9599–9604.
   PubMed Web of Science ®Google Scholar
• Park KJ, Choi SH, Lee SY, et al. Nonstructural 5A protein of hepatitis C virus modulates tumor necrosis factor alpha-stimulated nuclear factor kappa B activation. J Biol Chem. 2002;277:13122–13128.
   PubMed Web of Science ®Google Scholar
• Cheng D, Zhao L, Zhang L, et al. P53 controls hepatitis C virus non-structural protein 5A-mediated downregulation of GADD45a expression via the NF-kB and PI3K–Akt pathways. J Gen Virol. 2013;94:326–335.
   PubMed Web of Science ®Google Scholar
• Zhang JJ, Liu Q, Qiao L. HCV NS5A promotes cholesterol synthesis in the mouse hepatocytes by inhibiting AMPK phosphorylation and up-regulating SREBP-2 and HMG-CoA reductase. Chin J Biochem Mol Biol. 2017;33:1152–1160. (in Chinese).
   Google Scholar
• Aye ILMH, Waddell BJ, Mark PJ, et al. Oxysterols exert proinflammatory effects in placental trophoblasts via TLR4-dependent, cholesterol-sensitive activation of NF-κB. Mol Hum Reprod. 2012;18:341–353.
   PubMed Web of Science ®Google Scholar
• He M, Zhang W, Dong Y, et al. Pro-inflammation NF-κB signaling triggers a positive feedback via enhancing cholesterol accumulation in liver cancer cells. J Exp Clin Cancer Res. 2017;36:15.
   PubMed Web of Science ®Google Scholar
• Qi L, Hou J. GW28-e0163 cholesterol loading induces VSMCs apoptosis and monocytes adhesion via NF/kB pathway. J Am Coll Cardiol. 2017;70:C4.
   Web of Science ®Google Scholar
• Tall AR, Yvan-Charvet L. Cholesterol, inflammation and innate immunity. Nat Rev Immunol. 2015;15:104–116.
   PubMed Web of Science ®Google Scholar
• Yuan Q, Zhang QM. Cholesterol induces endothelial cells injury by increasing production of reactive oxygen species and activation NF-κB. Chin J Pathophysiol. 2010;26:1521–1526. (in Chinese).
   Google Scholar
• Zahoor MA, Yamane D, Mohamed YM, et al. Bovine viral diarrhea virus non-structural protein 5A interacts with NIK- and IKKβ-binding protein. J Gen Virol. 2010;91:1939–1948.
   PubMed Web of Science ®Google Scholar
• Rajamäki K, Lappalainen J, Oörni K, et al. Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation. PLoS One. 2010;5:e11765.
   PubMed Web of Science ®Google Scholar
• Silva GB, Gierman LM, Rakner JJ, et al. Cholesterol crystals and NLRP3 mediated inflammation in the uterine wall decidua in normal and preeclamptic pregnancies. Front Immunol. 2020;11:564712.
   PubMed Web of Science ®Google Scholar