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01-07-2020 | Arthritis | Original Article

The Vif protein of caprine arthritis encephalitis virus inhibits interferon production

Authors: Yali Fu, Dong Lu, Yanxin Su, Heng Chi, Jiashun Wang, Jinhai Huang

Published in: Archives of Virology | Issue 7/2020

Abstract

Caprine arthritis-encephalitis (CAE) is a chronic progressive infectious disease caused by caprine arthritis-encephalitis virus (CAEV) that seriously threatens the goat industry. Chronic infection and life-long multi-tissue inflammation are the typical features of the disease. Innate antiviral immunity is essential for the host defense system that rapidly recognizes and eliminates invading viruses. Interferon β (IFN-β) is important for innate immunity and regulates immunity against a broad spectrum of viruses. To investigate the details of the IFN-β response to CAEV infection, the effects of six viral proteins and the molecular mechanisms by which they affect IFN-β production were analyzed. Overexpression of DU and Vif promote virus proliferation and inhibit the production of IFN-β. qRT-PCR and luciferase reporter assays showed that overexpression of Vif inhibits the expression of luciferase under the control of the ISRE, NF-κB or IFN-β promoter but does not affect the expression of IFN-β activated by IRF3, indicating that Vif negatively regulates IFN-β production by affecting upstream signal transduction of IRF3. Amino acids 149-164 of Vif were found to be necessary for the inhibitory effect of IFN-β production. Our results indicate that CAEV evades surveillance and clearance by intracellular innate immunity by downregulating IFN-β production.

O’Sullivan BM, Eaves FW, Baxendell SA, Rowan KJ (1978) Leucoencephalomyelitis of goat kids. Aust Vet J 54:479–483PubMedCrossRef

Adams DS, Crawford TB, Klevjer-Anderson P (1980) A pathogenetic study of the early connective tissue lesions of viral caprine arthritis–encephalitis. Am J Pathol 99:257–278PubMedPubMedCentral

Crawford TB, Adams DS, Cheevers WP, Cork LC (1980) Chronic arthritis in goats caused by a retrovirus. Science 207:997–999PubMedCrossRef

Lamara A, Fieni F, Chatagnon G, Larrat M, Dubreil L, Chebloune Y (2013) Caprine arthritis encephalitis virus (CAEV) replicates productively in cultured epididymal cells from goats. Comp Immunol Microbiol Infect Dis 36:397–404PubMedCrossRef

Li Y, Zhou F, Li X, Wang J, Zhao X, Huang J (2013) Development of TaqMan-based qPCR method for detection of caprine arthritis-encephalitis virus (CAEV) infection. Arch Virol 158:2135–2141PubMedCrossRefPubMedCentral

Crawford TB, Adams DS (1981) Caprine arthritis–encephalitis: clinical features and presence of antibody in selected goat populations. J Am Vet Med Assoc 178:713–719PubMed

Tageldin MH, Johnson EH, Al-Busaidi RM, Al-Habsi KR, Al-Habsi SS (2012) Serological evidence of caprine arthritis-encephalitis virus (CAEV) infection in indigenous goats in the Sultanate of Oman. Trop Anim Health Prod 44:1–3PubMedCrossRef

Tu PA, Shiu JS, Lee SH, Pang VF, Wang DC, Wang PH (2017) Development of a recombinase polymerase amplification lateral flow dipstick (RPA-LFD) for the field diagnosis of caprine arthritis–encephalitis virus (CAEV) infection. J Virol Methods 243:98–104PubMedCrossRef

Michiels R, Van Mael E, Quinet C, Welby S, Cay AB, De Regge N (2018) Seroprevalence and risk factors related to small ruminant lentivirus infections in Belgian sheep and goats. Prev Vet Med 151:13–20PubMedCrossRef

10.

Adedeji AO, Barr B, Gomez-Lucia E, Murphy B (2013) A polytropic caprine arthritis encephalitis virus promoter isolated from multiple tissues from a sheep with multisystemic lentivirus-associated inflammatory disease. Viruses 5:2005–2018PubMedCrossRefPubMedCentral

11.

Hess JL, Pyper JM, Clements JE (1986) Nucleotide sequence and transcriptional activity of the caprine arthritis–encephalitis virus long terminal repeat. J Virol 60:385–393PubMedCrossRefPubMedCentral

12.

Barros SC, Andresdottir V, Fevereiro M (2005) Cellular specificity and replication rate of Maedi Visna virus in vitro can be controlled by LTR sequences. Arch Virol 150:201–213PubMedCrossRef

13.

Oskarsson T, Hreggvidsdottir HS, Agnarsdottir G, Matthiasdottir S, Ogmundsdottir MH, Jonsson SR, Georgsson G, Ingvarsson S, Andresson OS, Andresdottir V (2007) Duplicated sequence motif in the long terminal repeat of maedi-visna virus extends cell tropism and is associated with neurovirulence. J Virol 81:4052–4057PubMedCrossRefPubMedCentral

14.

L’Homme Y, Leboeuf A, Arsenault J, Fras M (2015) Identification and characterization of an emerging small ruminant lentivirus circulating recombinant form (CRF). Virology 475:159–171PubMedCrossRef

15.

Valas S, Benoit C, Baudry C, Perrin G, Mamoun RZ (2000) Variability and immunogenicity of caprine arthritis–encephalitis virus surface glycoprotein. J Virol 74:6178–6185PubMedCrossRefPubMedCentral

16.

Harmache A, Russo P, Guiguen F, Vitu C, Vignoni M, Bouyac M, Hieblot C, Pepin M, Vigne R, Suzan M (1996) Requirement of caprine arthritis encephalitis virus vif gene for in vivo replication. Virology 224:246–255PubMedCrossRef

17.

Schoborg RV, Saltarelli MJ, Clements JE (1994) A Rev protein is expressed in caprine arthritis encephalitis virus (CAEV)-infected cells and is required for efficient viral replication. Virology 202:1–15PubMedCrossRef

18.

Korb J, Travnicek M, Riman J (1976) The oncornavirus maturation process: quantitative correlation between morphological changes and conversion of genomic virion RNA. Intervirology 7:211–224PubMedCrossRef

19.

Lamara A, Fieni F, Mselli-Lakhal L, Chatagnon G, Bruyas JF, Tainturier D, Battut I, Fornazero C, Chebloune Y (2002) Early embryonic cells from in vivo-produced goat embryos transmit the caprine arthritis-encephalitis virus (CAEV). Theriogenology 58:1153–1163PubMedCrossRef

20.

Lamara A, Fieni F, Mselli-Lakhal L, Tainturier D, Chebloune Y (2001) Efficient replication of caprine arthritis-encephalitis virus in goat granulosa cells. Virus Res 79:165–172PubMedCrossRef

21.

Cardinaux L, Zahno ML, Deubelbeiss M, Zanoni R, Vogt HR, Bertoni G (2013) Virological and phylogenetic characterization of attenuated small ruminant lentivirus isolates eluding efficient serological detection. Vet Microbiol 162:572–581PubMedCrossRef

22.

Blacklaws BA (2012) Small ruminant lentiviruses: immunopathogenesis of visna-maedi and caprine arthritis and encephalitis virus. Comp Immunol Microbiol Infect Dis 35:259–269PubMedCrossRef

23.

Jarczak J, Kaba J, Reczynska D, Bagnicka E (2016) Impaired expression of cytokines as a result of viral infections with an emphasis on small ruminant lentivirus infection in goats. Viruses 8(186):1–12CrossRefPubMedCentral

24.

Medin CL, Rothman AL (2006) Cell type-specific mechanisms of interleukin-8 induction by dengue virus and differential response to drug treatment. J Infect Dis 193:1070–1077PubMedCrossRef

25.

Tanji T, Ip YT (2005) Regulators of the Toll and Imd pathways in the Drosophila innate immune response. Trends Immunol 26:193–198PubMedCrossRef

26.

Bourgeois C, Majer O, Frohner IE, Lesiak-Markowicz I, Hildering KS, Glaser W, Stockinger S, Decker T, Akira S, Muller M, Kuchler K (2011) Conventional dendritic cells mount a type I IFN response against Candida spp. requiring novel phagosomal TLR7-mediated IFN-beta signaling. J Immunol 186:3104–3112PubMedCrossRef

27.

Li J, Liu Y, Zhang X (2010) Murine coronavirus induces type I interferon in oligodendrocytes through recognition by RIG-I and MDA5. J Virol 84:6472–6482PubMedCrossRefPubMedCentral

28.

Meylan E, Tschopp J, Karin M (2006) Intracellular pattern recognition receptors in the host response. Nature 442:39–44PubMedCrossRef

29.

Belgnaoui SM, Paz S, Samuel S, Goulet ML, Sun Q, Kikkert M, Iwai K, Dikic I, Hiscott J, Lin R (2012) Linear ubiquitination of NEMO negatively regulates the interferon antiviral response through disruption of the MAVS–TRAF3 complex. Cell Host Microbe 12:211–222PubMedCrossRef

30.

Liu X, Wang Q, Pan Y, Wang C (2015) Sensing and responding to cytosolic viruses invasions: an orchestra of kaleidoscopic ubiquitinations. Cytokine Growth Factor Rev 26:379–387PubMedCrossRef

31.

Thanos D, Maniatis T (1995) Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell 83:1091–1100PubMedCrossRef

32.

Shi P, Su Y, Li R, Liang Z, Dong S, Huang J (2019) PEDV nsp16 negatively regulates innate immunity to promote viral proliferation. Virus Res 265:57–66PubMedCrossRefPubMedCentral

33.

Cheevers WP, Beyer JC, Hotzel I (2001) Plasmid DNA encoding caprine interferon gamma inhibits antibody response to caprine arthritis-encephalitis virus (CAEV) surface protein encoded by a co-administered plasmid expressing CAEV env and tat genes. Vaccine 19:3209–3215PubMedCrossRef

34.

Hariya Y, Yokosawa N, Yonekura N, Kohama G, Fuji N (2013) Mumps virus can suppress the effective augmentation of HPC-induced apoptosis by IFN-gamma through disruption of IFN signaling in U937 cells. Microbiol Immunol 44:537–541CrossRef

35.

Peng Q, Lan X, Wang C, Ren Y, Yue N, Wang J, Zhong B, Zhu Q (2017) Kobuvirus VP3 protein restricts the IFN-β-triggered signaling pathway by inhibiting STAT2–IRF9 and STAT2–STAT2 complex formation. Virology 507:161PubMedCrossRef

36.

Murphy B, Hillman C, Castillo D, Vapniarsky N, Rowe J (2012) The presence or absence of the gamma-activated site determines IFN gamma-mediated transcriptional activation in CAEV promoters cloned from the mammary gland and joint synovium of a single CAEV-infected goat. Virus Res 163:537–545PubMedCrossRef

37.

White-Ziegler CA, Low DA (1992) Thermoregulation of the pap operon: evidence for the involvement of RimJ, the N-terminal acetylase of ribosomal protein S5. J Bacteriol 174:7003PubMedCrossRefPubMedCentral

38.

Turelli P, Guiguen F, Mornex JF, Vigne R, Querat G (1997) dUTPase-minus caprine arthritis-encephalitis virus is attenuated for pathogenesis and accumulates G-to-A substitutions. J Virol 71:4522–4530PubMedCrossRefPubMedCentral

39.

Carruth LM, Hardwick JM, Morse BA, Clements JE (1994) Visna virus Tat protein: a potent transcription factor with both activator and suppressor domains. J Virol 68:6137–6146PubMedCrossRefPubMedCentral

40.

Li R, Chen C, He J, Zhang L, Zhang L, Guo Y, Zhang W, Tan K, Huang J (2019) E3 ligase ASB8 promotes porcine reproductive and respiratory syndrome virus proliferation by stabilizing the viral Nsp1alpha protein and degrading host IKKbeta kinase. Virology 532:55–68PubMedCrossRef

41.

Shi P, Su Y, Li R, Zhang L, Chen C, Zhang L, Faaberg K, Huang J (2018) Dual regulation of host TRAIP post-translation and nuclear/plasma distribution by porcine reproductive and respiratory syndrome virus non-structural protein 1alpha promotes viral proliferation. Front Immunol 9:3023PubMedCrossRefPubMedCentral

42.

Pulido MR, Sáiz M (2017) Molecular mechanisms of foot-and-mouth disease virus targeting the host antiviral response. Front Cell Infect Microbiol 7:252CrossRef

43.

Zhang HL, Ye HQ, Liu SQ, Deng CL, Li XD, Shi PY, Zhang B (2017) West Nile virus NS1 antagonizes interferon-Î² production by targeting RIG-I and MDA5. J Virol 91:JVI.02396-16CrossRef

44.

Okumura A, Alce T, Lubyova B, Ezelle H, Strebel K, Pitha PM (2008) HIV-1 accessory proteins VPR and Vif modulate antiviral response by targeting IRF-3 for degradation. Virology 373:85–97PubMedCrossRef

45.

Park SY, Waheed AA, Zhang ZR, Freed EO, Bonifacino JS (2014) HIV-1 Vpu accessory protein induces caspase-mediated cleavage of IRF3 transcription factor. J Biol Chem 289:35102–35110PubMedCrossRefPubMedCentral

46.

Bose D, Gagnon J, Chebloune Y (2015) Comparative analysis of tat-dependent and tat-deficient natural lentiviruses. Vet Sci 2:293–348PubMedCrossRefPubMedCentral

47.

Rathinam VA, Fitzgerald KA (2011) Cytosolic surveillance and antiviral immunity. Curr Opin Virol 1:455–462PubMedCrossRefPubMedCentral

48.

Killip MJ, Fodor E, Randall RE (2015) Influenza virus activation of the interferon system. Virus Res 209:11–22PubMedCrossRefPubMedCentral

49.

Harmache A, Bouyac M, Audoly G, Hieblot C, Peveri P, Vigne R, Suzan M (1995) The vif gene is essential for efficient replication of caprine arthritis encephalitis virus in goat synovial membrane cells and affects the late steps of the virus replication cycle. J Virol 69:3247–3257PubMedCrossRefPubMedCentral

50.

Seroude V, Audoly G, Gluschankof P, Suzan M (2001) Tryptophan 95, an amino acid residue of the Caprine arthritis encephalitis virus vif protein which is essential for virus replication. Virology 280:232–242PubMedCrossRef

51.

Sauter D, Kirchhoff F (2018) Multilayered and versatile inhibition of cellular antiviral factors by HIV and SIV accessory proteins. Cytokine Growth Factor Rev 40:3–12PubMedCrossRef

Title: The Vif protein of caprine arthritis encephalitis virus inhibits interferon production
Authors: Yali Fu
Dong Lu
Yanxin Su
Heng Chi
Jiashun Wang
Jinhai Huang
Publication date: 01-07-2020
Publisher: Springer Vienna
Keywords: Arthritis
Encephalitis
Interferon
Published in: Archives of Virology / Issue 7/2020
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-020-04637-z

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