CLC number:
On-line Access: 2024-03-01
Received: 2023-02-28
Revision Accepted: 2023-08-03
Crosschecked: 2024-03-06
Cited: 0
Clicked: 909
Fulong NAN, Wenlong NAN, Xin YAN, Hui WANG, Shasha JIANG, Shuyun ZHANG, Zhongjie YU, Xianjuan ZHANG, Fengjun LIU, Jun LI, Xiaoqiong ZHOU, Delei NIU, Yiquan LI, Wei WANG, Ning SHI, Ningyi JIN, Changzhan XIE, Xiaoni CUI, He ZHANG, Bin WANG, Huijun LU. Newcastle disease virus suppresses antigen presentation via inhibiting IL-12 expression in dendritic cells[J]. Journal of Zhejiang University Science B, 2024, 25(3): 254-270.
@article{title="Newcastle disease virus suppresses antigen presentation via inhibiting IL-12 expression in dendritic cells",
author="Fulong NAN, Wenlong NAN, Xin YAN, Hui WANG, Shasha JIANG, Shuyun ZHANG, Zhongjie YU, Xianjuan ZHANG, Fengjun LIU, Jun LI, Xiaoqiong ZHOU, Delei NIU, Yiquan LI, Wei WANG, Ning SHI, Ningyi JIN, Changzhan XIE, Xiaoni CUI, He ZHANG, Bin WANG, Huijun LU",
journal="Journal of Zhejiang University Science B",
volume="25",
number="3",
pages="254-270",
year="2024",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2300134"
}
%0 Journal Article
%T Newcastle disease virus suppresses antigen presentation via inhibiting IL-12 expression in dendritic cells
%A Fulong NAN
%A Wenlong NAN
%A Xin YAN
%A Hui WANG
%A Shasha JIANG
%A Shuyun ZHANG
%A Zhongjie YU
%A Xianjuan ZHANG
%A Fengjun LIU
%A Jun LI
%A Xiaoqiong ZHOU
%A Delei NIU
%A Yiquan LI
%A Wei WANG
%A Ning SHI
%A Ningyi JIN
%A Changzhan XIE
%A Xiaoni CUI
%A He ZHANG
%A Bin WANG
%A Huijun LU
%J Journal of Zhejiang University SCIENCE B
%V 25
%N 3
%P 254-270
%@ 1673-1581
%D 2024
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2300134
TY - JOUR
T1 - Newcastle disease virus suppresses antigen presentation via inhibiting IL-12 expression in dendritic cells
A1 - Fulong NAN
A1 - Wenlong NAN
A1 - Xin YAN
A1 - Hui WANG
A1 - Shasha JIANG
A1 - Shuyun ZHANG
A1 - Zhongjie YU
A1 - Xianjuan ZHANG
A1 - Fengjun LIU
A1 - Jun LI
A1 - Xiaoqiong ZHOU
A1 - Delei NIU
A1 - Yiquan LI
A1 - Wei WANG
A1 - Ning SHI
A1 - Ningyi JIN
A1 - Changzhan XIE
A1 - Xiaoni CUI
A1 - He ZHANG
A1 - Bin WANG
A1 - Huijun LU
J0 - Journal of Zhejiang University Science B
VL - 25
IS - 3
SP - 254
EP - 270
%@ 1673-1581
Y1 - 2024
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2300134
Abstract: As a potential vectored vaccine, newcastle disease virus (NDV) has been subject to various studies for vaccine development, while relatively little research has outlined the immunomodulatory effect of the virus in antigen presentation. To elucidate the key inhibitory factor in regulating the interaction of infected dendritic cells (DCs) and t cells, DCs were pretreated with the NDV vaccine strain LaSota as an inhibitor and stimulated with lipopolysaccharide (LPS) for further detection by enzyme-linked immunosorbent assay (ELISA), flow cytometry, immunoblotting, and quantitative real-time polymerase chain reaction (qRT-PCR). The results revealed that NDV infection resulted in the inhibition of interleukin (IL)-12p40 in DCs through a p38 mitogen-activated protein kinase (MAPK)-dependent manner, thus inhibiting the synthesis of IL-12p70, leading to the reduction in T cell proliferation and the secretion of interferon-γ (IFN-γ), tumor necrosis factor-α (TNF-α), and IL-6 induced by DCs. Consequently, downregulated cytokines accelerated the infection and viral transmission from DCs to t cells. Furthermore, several other strains of NDV also exhibited inhibitory activity. The current study reveals that NDV can modulate the intensity of the innate‒adaptive immune cell crosstalk critically toward viral invasion improvement, highlighting a novel mechanism of virus-induced immunosuppression and providing new perspectives on the improvement of NDV-vectored vaccine.
[1]AyasoufiK, PfallerCK, 2020. Seek and hide: the manipulating interplay of measles virus with the innate immune system. Curr Opin Virol, 41:18-30.
[2]BaratinM, ForayC, DemariaO, et al., 2015. Homeostatic NF-κB signaling in steady-state migratory dendritic cells regulates immune homeostasis and tolerance. Immunity, 42(4):627-639.
[3]BradyMT, MacDonaldAJ, RowanAG, et al., 2003. Hepatitis C virus non-structural protein 4 suppresses Th1 responses by stimulating IL-10 production from monocytes. Eur J Immunol, 33(12):3448-3457.
[4]CardoneM, IkedaKN, VaranoB, et al., 2015. HIV-1-induced impairment of dendritic cell cross talk with γδ T lymphocytes. J Virol, 89(9):4798-4808.
[5]ChenDJ, LiuXW, XuSK, et al., 2019. TNF-α induced by porcine reproductive and respiratory syndrome virus inhibits the replication of classical swine fever virus C-strain. Vet Microbiol, 234:25-33.
[6]CoughlinMM, BelliniWJ, RotaPA, 2013. Contribution of dendritic cells to measles virus induced immunosuppression. Rev Med Virol, 23(2):126-138.
[7]de WitteL, de VriesRD, van der VlistM, et al., 2008. DC-SIGN and CD150 have distinct roles in transmission of measles virus from dendritic cells to T-lymphocytes. PLoS Pathog, 4(4):e1000049.
[8]DienzO, RudJG, EatonSM, et al., 2012. Essential role of IL-6 in protection against H1N1 influenza virus by promoting neutrophil survival in the lung. Mucosal Immunol, 5(3):258-266.
[9]DuraiV, MurphyKM, 2016. Functions of murine dendritic cells. Immunity, 45(4):719-736.
[10]GaoHW, LiuX, SunW, et al., 2017. Total tanshinones exhibits anti-inflammatory effects through blocking TLR4 dimerization via the MyD88 pathway. Cell Death Dis, 8(8):e3004.
[11]GatelyMK, DesaiBB, WolitzkyAG, et al., 1991. Regulation of human lymphocyte proliferation by a heterodimeric cytokine, IL-12 (cytotoxic lymphocyte maturation factor). J Immunol, 147(3):874-882.
[12]GhilasS, AmbrosiniM, CancelJC, et al., 2021. Natural killer cells and dendritic epidermal γδ T cells orchestrate type 1 conventional DC spatiotemporal repositioning toward CD8+ T cells. iScience, 24(9):103059-103083.
[13]GuptaM, LoMK, SpiropoulouCF, 2013. Activation and cell death in human dendritic cells infected with Nipah virus. Virology, 441(1):49-56.
[14]HilliganKL, RoncheseF, 2020. Antigen presentation by dendritic cells and their instruction of CD4+ T helper cell responses. Cell Mol Immunol, 17(6):587-599.
[15]JiangKF, GuoS, YangC, et al., 2018. Barbaloin protects against lipopolysaccharide (LPS)-induced acute lung injury by inhibiting the ROS-mediated PI3K/AKT/NF-κB pathway. Int Immunopharmacol, 64:140-150.
[16]KürtenCHL, DeußE, LeiYL, et al., 2020. Stimulierende und inhibierende Signalwege der APZ- und T-Zell-Interaktion sowie Einfluss von TLR-Agonisten auf APZ. HNO, 68(12):916-921 (in German).
[17]LiYC, WuQX, HuangLL, et al., 2018. An alternative pathway of enteric PEDV dissemination from nasal cavity to intestinal mucosa in swine. Nat Commun, 9:3811.
[18]MenonMB, GropengießerJ, FischerJ, et al., 2017. P38MAPK/MK2-dependent phosphorylation controls cytotoxic RIPK1 signalling in inflammation and infection. Nat Cell Biol, 19(10):1248-1259.
[19]NanFL, ZhangH, NanWL, et al., 2021a. Lentogenic NDV V protein inhibits IFN responses and represses cell apoptosis. Vet Microbiol, 261:109181.
[20]NanFL, ZhengW, NanWL, et al., 2021b. Newcastle disease virus inhibits the proliferation of T cells induced by dendritic cells in vitro and in vivo. Front Immunol, 11:619829.
[21]NieY, WangZ, ChaiG, et al., 2019. Dehydrocostus lactone suppresses LPS-induced acute lung injury and macrophage activation through NF-κB signaling pathway mediated by p38 MAPK and Akt. Molecules, 24(8):1510.
[22]ParkJG, OladunniFS, RohaimMA, et al., 2021. Immunogenicity and protective efficacy of an intranasal live-attenuated vaccine against SARS-CoV-2. iScience, 24(9):102941.
[23]PulendranB, 2015. The varieties of immunological experience: of pathogens, stress, and dendritic cells. Annu Rev Immunol, 33:563-606.
[24]QianG, LiYW, MaH, et al., 2018. Peiminine protects against lipopolysaccharide-induced mastitis by inhibiting the AKT/NF-κB, ERK1/2 and p38 signaling pathways. Int J Mol Sci, 19(9):2637.
[25]QiuX, FuQ, MengC, et al., 2016. Newcastle disease virus V protein targets phosphorylated STAT1 to block IFN-I signaling. PLoS ONE, 11(2):e0148560.
[26]RajmaniRS, GuptaSK, SinghPK, et al., 2016. HN protein of Newcastle disease virus sensitizes HeLa cells to TNF-αinduced apoptosis by downregulating NF-κB expression. Arch Virol, 161(9):2395-2405.
[27]RescignoM, 2002. Dendritic cells and the complexity of microbial infection. Trends Microbiol, 10(9):425-431.
[28]Romanets-KorbutO, KovalevskaLM, SeyaT, et al., 2016. Measles virus hemagglutinin triggers intracellular signaling in CD150-expressing dendritic cells and inhibits immune response. Cell Mol Immunol, 13(6):828-838.
[29]RonetC, Hauyon-La TorreY, Revaz-BretonM, et al., 2010. Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. J Immunol, 184(2):886-894.
[30]SchönrichG, RafteryMJ, 2015. Dendritic cells as Achilles’ heel and Trojan horse during varicella zoster virus infection. Front Microbiol, 6:417.
[31]SchulzO, EdwardsAD, SchitoM, et al., 2000. CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity, 13(4):453-462.
[32]ShresthaB, YouDH, SaraviaJ, et al., 2017. IL-4Rα on dendritic cells in neonates and Th2 immunopathology in respiratory syncytial virus infection. J Leukoc Biol, 102(1):153-161.
[33]SunWN, LiuYH, AmanatF, et al., 2021. A Newcastle disease virus expressing a stabilized spike protein of SARS-CoV-2 induces protective immune responses. Nat Commun, 12:6197.
[34]SunYJ, ZhengH, YuSQ, et al., 2019. Newcastle disease virus V protein degrades mitochondrial antiviral signaling protein to inhibit host type I interferon production via E3 ubiquitin ligase RNF5. J Virol, 93(18):e00322-19.
[35]TanL, ZhangYQ, QiaoCT, et al., 2018. NDV entry into dendritic cells through macropinocytosis and suppression of T lymphocyte proliferation. Virology, 518:126-135.
[36]van PanhuysN, 2016. TCR signal strength alters T-DC activation and interaction times and directs the outcome of differentiation. Front Immunol, 7:6.
[37]WonderlichER, WuWC, NormolleDP, et al., 2015. Macrophages and myeloid dendritic cells lose T cell-stimulating function in simian immunodeficiency virus infection associated with diminished IL-12 and IFN-α production. J Immunol, 195(7):3284-3292.
[38]YangX, ArslanM, LiuXJ, et al., 2020. IFN-γ establishes interferon-stimulated gene-mediated antiviral state against Newcastle disease virus in chicken fibroblasts. Acta Biochim Biophys Sin, 52(3):268-280.
[39]YoshimuraS, BondesonJ, FoxwellBMJ, et al., 2001. Effective antigen presentation by dendritic cells is NF-κB dependent: coordinate regulation of MHC, co-stimulatory molecules and cytokines. Int Immunol, 13(5):675-683.
[40]ZhangH, NanFL, LiZX, et al., 2019. Construction and immunological evaluation of recombinant Newcastle disease virus vaccines expressing highly pathogenic porcine reproductive and respiratory syndrome virus GP3/GP5 proteins in pigs. Vet Microbiol, 239:108490.
[41]ZhangHL, ChenS, ZengMC, et al., 2018. Apelin-13 administration protects against LPS-induced acute lung injury by inhibiting NF-κB pathway and NLRP3 inflammasome activation. Cell Physiol Biochem, 49(5):1918-1932.
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