Journal of Veterinary Science

The Korean Society of Veterinary Science (대한수의학회)
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Annexin A2 gene interacting with viral matrix protein to promote bovine ephemeral fever virus release

  • Chen, Lihui (Ruminant Diseases Research Center, College of Life Sciences, Shandong Normal University) ;
  • Li, Xingyu (Ruminant Diseases Research Center, College of Life Sciences, Shandong Normal University) ;
  • Wang, Hongmei (Ruminant Diseases Research Center, College of Life Sciences, Shandong Normal University) ;
  • Hou, Peili (Ruminant Diseases Research Center, College of Life Sciences, Shandong Normal University) ;
  • He, Hongbin (Ruminant Diseases Research Center, College of Life Sciences, Shandong Normal University)
  • Received : 2019.09.03
  • Accepted : 2019.12.30
  • Published : 2020.03.31
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Abstract

Bovine ephemeral fever virus (BEFV) causes bovine ephemeral fever, which can produce considerable economic damage to the cattle industry. However, there is limited experimental evidence regarding the underlying mechanisms of BEFV. Annexin A2 (AnxA2) is a calcium and lipid-conjugated protein that binds phospholipids and the cytoskeleton in a Ca2+-dependent manner, and it participates in various cellular functions, including vesicular trafficking, organization of membrane domains, and virus proliferation. The role of the AnxA2 gene during virus infection has not yet been reported. In this study, we observed that AnxA2 gene expression was up-regulated in BHK-21 cells infected with the virus. Additionally, overexpression of the AnxA2 gene promoted the release of mature virus particles, whereas BEFV replication was remarkably inhibited after reducing AnxA2 gene expression by using the small interfering RNA (siRNA). For viral proteins, overexpression of the Matrix (M) gene promotes the release of mature virus particles. Moreover, the AnxA2 protein interaction with the M protein of BEFV was confirmed by GST pull-down and co-immunoprecipitation assays. Experimental results indicate that the C-terminal domain (268-334 aa) of AxnA2 contributes to this interaction. An additional mechanistic study showed that AnxA2 protein interacts with M protein and mediates the localization of the M protein at the plasma membrane. Furthermore, the absence of the AnxA2-V domain could attenuate the effect of AnxA2 on BEFV replication. These findings can contribute to elucidating the regulation of BEFV replication and may have implications for antiviral strategy development.

Keywords

Acknowledgement

This study was partially supported by grants from the National Natural Science Fund of China (31872490, 31672556), the Primary Research & Development Plan of Shandong Province (2018GNC113011), and a fund earmarked for the Taishan Scholar Project (Hongbin He).

References

  1. Walker PJ, Klement E. Epidemiology and control of bovine ephemeral fever. Vet Res (Faisalabad) 2015;46:124. https://doi.org/10.1186/s13567-015-0262-4
  2. Hayama Y, Moriguchi S, Yanase T, Suzuki M, Niwa T, Ikemiyagi K, Nitta Y, Yamamoto T, Kobayashi S, Murai K, Tsutsui T. Epidemiological analysis of bovine ephemeral fever in 2012-2013 in the subtropical islands of Japan. BMC Vet Res 2016;12:47. https://doi.org/10.1186/s12917-016-0673-0
  3. Du X, Zhou J. Application of biosensors to detection of epidemic diseases in animals. Res Vet Sci 2018;118:444-448. https://doi.org/10.1016/j.rvsc.2018.04.011
  4. Hou P, Zhao G, He C, Wang H, He H. Biopanning of polypeptides binding to bovine ephemeral fever virus G1 protein from phage display peptide library. BMC Vet Res 2018;14:3. https://doi.org/10.1186/s12917-017-1315-x
  5. He CQ, Liu YX, Wang HM, Hou PL, He HB, Ding NZ. New genetic mechanism, origin and population dynamic of bovine ephemeral fever virus. Vet Microbiol 2016;182:50-56. https://doi.org/10.1016/j.vetmic.2015.10.029
  6. Jayakar HR, Jeetendra E, Whitt MA. Rhabdovirus assembly and budding. Virus Res 2004;106:117-132. https://doi.org/10.1016/j.virusres.2004.08.009
  7. Zan J, Liu J, Zhou JW, Wang HL, Mo KK, Yan Y, Xu YB, Liao M, Su S, Hu RL, Zhou JY. Rabies virus matrix protein induces apoptosis by targeting mitochondria. Exp Cell Res 2016;347:83-94. https://doi.org/10.1016/j.yexcr.2016.07.008
  8. Jayakar HR, Murti KG, Whitt MA. Mutations in the PPPY motif of vesicular stomatitis virus matrix protein reduce virus budding by inhibiting a late step in virion release. J Virol 2000;74:9818-9827. https://doi.org/10.1128/JVI.74.21.9818-9827.2000
  9. Gerke V, Moss SE. Annexins: from structure to function. Physiol Rev 2002;82:331-371. https://doi.org/10.1152/physrev.00030.2001
  10. Mirsaeidi M, Gidfar S, Vu A, Schraufnagel D. Annexins family: insights into their functions and potential role in pathogenesis of sarcoidosis. J Transl Med 2016;14:89. https://doi.org/10.1186/s12967-016-0843-7
  11. Raynal P, Pollard HB. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim Biophys Acta 1994;1197:63-93. https://doi.org/10.1016/0304-4157(94)90019-1
  12. Aliyu IA, Ling KH, Md Hashim N, Chee HY. Annexin A2 extracellular translocation and virus interaction: A potential target for antivirus-drug discovery. Rev Med Virol 2019;29:e2038. https://doi.org/10.1002/rmv.2038
  13. Solbak SM, Abdurakhmanov E, Vedeler A, Danielson UH. Characterization of interactions between hepatitis C virus NS5B polymerase, annexin A2 and RNA - effects on NS5B catalysis and allosteric inhibition. Virol J 2017;14:236. https://doi.org/10.1186/s12985-017-0904-4
  14. Woodham AW, Taylor JR, Jimenez AI, Skeate JG, Schmidt T, Brand HE, Da Silva DM, Kast WM. Small molecule inhibitors of the annexin A2 heterotetramer prevent human papillomavirus type 16 infection. J Antimicrob Chemother 2015;70:1686-1690. https://doi.org/10.1093/jac/dkv045
  15. Wang J, Song J, Clark G, Roux SJ. ANN1 and ANN2 function in post-phloem sugar transport in root tips to affect primary root growth. Plant Physiol 2018;178:390-401. https://doi.org/10.1104/pp.18.00713
  16. Luo S, Xie C, Wu P, He J, Tang Y, Xu J, Zhao S. Annexin A2 is an independent prognostic biomarker for evaluating the malignant progression of laryngeal cancer. Exp Ther Med 2017;14:6113-6118.
  17. Shaker MK, Abdel Fattah HI, Sabbour GS, Montasser IF, Abdelhakam SM, El Hadidy E, Yousry R, El Dorry AK. Annexin A2 as a biomarker for hepatocellular carcinoma in Egyptian patients. World J Hepatol 2017;9:469-476. https://doi.org/10.4254/wjh.v9.i9.469
  18. Taylor JR, Skeate JG, Kast WM. Annexin A2 in virus infection. Front Microbiol 2018;9:2954. https://doi.org/10.3389/fmicb.2018.02954
  19. Nazmi AR, Ozorowski G, Pejic M, Whitelegge JP, Gerke V, Luecke H. N-terminal acetylation of annexin A2 is required for S100A10 binding. Biol Chem 2012;393:1141-1150. https://doi.org/10.1515/hsz-2012-0179
  20. Woodham AW, Da Silva DM, Skeate JG, Raff AB, Ambroso MR, Brand HE, Isas JM, Langen R, Kast WM. The S100A10 subunit of the annexin A2 heterotetramer facilitates L2-mediated human papillomavirus infection. PLoS One 2012;7:e43519. https://doi.org/10.1371/journal.pone.0043519
  21. Grindheim AK, Saraste J, Vedeler A. Protein phosphorylation and its role in the regulation of Annexin A2 function. Biochim Biophys Acta, Gen Subj 2017;1861:2515-2529. https://doi.org/10.1016/j.bbagen.2017.08.024
  22. Filipenko NR, MacLeod TJ, Yoon CS, Waisman DM. Annexin A2 is a novel RNA-binding protein. J Biol Chem 2004;279:8723-8731. https://doi.org/10.1074/jbc.M311951200
  23. Mickleburgh I, Burtle B, Hollas H, Campbell G, Chrzanowska-Lightowlers Z, Vedeler A, Hesketh J. Annexin A2 binds to the localization signal in the 3' untranslated region of c-myc mRNA. FEBS J 2005;272:413-421. https://doi.org/10.1111/j.1742-4658.2004.04481.x
  24. Wright JF, Kurosky A, Wasi S. An endothelial cell-surface form of annexin II binds human cytomegalovirus. Biochem Biophys Res Commun 1994;198:983-989. https://doi.org/10.1006/bbrc.1994.1140
  25. Wright JF, Kurosky A, Pryzdial EL, Wasi S. Host cellular annexin II is associated with cytomegalovirus particles isolated from cultured human fibroblasts. J Virol 1995;69:4784-4791. https://doi.org/10.1128/jvi.69.8.4784-4791.1995
  26. Backes P, Quinkert D, Reiss S, Binder M, Zayas M, Rescher U, Gerke V, Bartenschlager R, Lohmann V. Role of annexin A2 in the production of infectious hepatitis C virus particles. J Virol 2010;84:5775-5789. https://doi.org/10.1128/JVI.02343-09
  27. LeBouder F, Morello E, Rimmelzwaan GF, Bosse F, Pechoux C, Delmas B, Riteau B. Annexin II incorporated into influenza virus particles supports virus replication by converting plasminogen into plasmin. J Virol 2008;82:6820-6828. https://doi.org/10.1128/JVI.00246-08
  28. Ma Y, Sun J, Gu L, Bao H, Zhao Y, Shi L, Yao W, Tian G, Wang X, Chen H. Annexin A2 (ANXA2) interacts with nonstructural protein 1 and promotes the replication of highly pathogenic H5N1 avian influenza virus. BMC Microbiol 2017;17:191. https://doi.org/10.1186/s12866-017-1097-0
  29. Liu Y, Gao P. Modulation of hepatitis B surface antigen secretion by annexin II expressed in hepatitis B virus-producing hepatoma cells. Mol Med Rep 2014;10:3113-3117. https://doi.org/10.3892/mmr.2014.2602
  30. Sheng C, Liu X, Jiang Q, Xu B, Zhou C, Wang Y, Chen J, Xiao M. Annexin A2 is involved in the production of classical swine fever virus infectious particles. J Gen Virol 2015;96:1027-1032. https://doi.org/10.1099/vir.0.000048
  31. Hou P, Wang H, Zhao G, He C, He H. Rapid detection of infectious bovine Rhinotracheitis virus using recombinase polymerase amplification assays. BMC Vet Res 2017;13:386. https://doi.org/10.1186/s12917-017-1284-0
  32. Wang X, Ju Z, Huang J, Hou M, Zhou L, Qi C, Zhang Y, Gao Q, Pan Q, Li G, Zhong J, Wang C. The relationship between the variants of the bovine MBL2 gene and milk production traits, mastitis, serum MBL-C levels and complement activity. Vet Immunol Immunopathol 2012;148:311-319. https://doi.org/10.1016/j.vetimm.2012.06.017
  33. Chang XB, Yang YQ, Gao JC, Zhao K, Guo JC, Ye C, Jiang CG, Tian ZJ, Cai XH, Tong GZ, An TQ. Annexin A2 binds to vimentin and contributes to porcine reproductive and respiratory syndrome virus multiplication. Vet Res (Faisalabad) 2018;49:75. https://doi.org/10.1186/s13567-018-0571-5
  34. Wang XG, Huang JM, Feng MY, Ju ZH, Wang CF, Yang GW, Yuan JD, Zhong JF. Regulatory mutations in the A2M gene are involved in the mastitis susceptibility in dairy cows. Anim Genet 2014;45:28-37. https://doi.org/10.1111/age.12099
  35. Li S, van Os GM, Ren S, Yu D, Ketelaar T, Emons AM, Liu CM. Expression and functional analyses of EXO70 genes in Arabidopsis implicate their roles in regulating cell type-specific exocytosis. Plant Physiol 2010;154:1819-1830. https://doi.org/10.1104/pp.110.164178
  36. Lv L, Zhao G, Wang H, He H. Cholesterol 25-Hydroxylase inhibits bovine parainfluenza virus type 3 replication through enzyme activity-dependent and -independent ways. Vet Microbiol 2019;239:108456. https://doi.org/10.1016/j.vetmic.2019.108456
  37. Hou P, Zhao M, He W, He H, Wang H. Cellular microRNA bta-miR-2361 inhibits bovine herpesvirus 1 replication by directly targeting EGR1 gene. Vet Microbiol 2019;233:174-183. https://doi.org/10.1016/j.vetmic.2019.05.004
  38. Ma W, Wang H, He H. Bovine herpesvirus 1 tegument protein UL41 suppresses antiviral innate immune response via directly targeting STAT1. Vet Microbiol 2019;239:108494. https://doi.org/10.1016/j.vetmic.2019.108494
  39. Liang J, Sagum CA, Bedford MT, Sidhu SS, Sudol M, Han Z, Harty RN. Chaperone-mediated autophagy protein BAG3 negatively regulates ebola and marburg VP40-mediated egress. PLoS Pathog 2017;13:e1006132. https://doi.org/10.1371/journal.ppat.1006132
  40. Koga R, Kubota M, Hashiguchi T, Yanagi Y, Ohno S. Annexin A2 mediates the localization of measles virus matrix protein at the plasma membrane. J Virol 2018;92:92.
  41. Dziduszko A, Ozbun MA. Annexin A2 and S100A10 regulate human papillomavirus type 16 entry and intracellular trafficking in human keratinocytes. J Virol 2013;87:7502-7515. https://doi.org/10.1128/JVI.00519-13
  42. Yang SL, Chou YT, Wu CN, Ho MS. Annexin II binds to capsid protein VP1 of enterovirus 71 and enhances viral infectivity. J Virol 2011;85:11809-11820. https://doi.org/10.1128/JVI.00297-11
  43. Li J, Guo D, Huang L, Yin M, Liu Q, Wang Y, Yang C, Liu Y, Zhang L, Tian Z, Cai X, Yu L, Weng C. The interaction between host Annexin A2 and viral Nsp9 is beneficial for replication of porcine reproductive and respiratory syndrome virus. Virus Res 2014;189:106-113. https://doi.org/10.1016/j.virusres.2014.05.015
  44. Kwak H, Park MW, Jeong S. Annexin A2 binds RNA and reduces the frameshifting efficiency of infectious bronchitis virus. PLoS One 2011;6:e24067. https://doi.org/10.1371/journal.pone.0024067
  45. Lai CK, Jeng KS, Machida K, Lai MM. Association of hepatitis C virus replication complexes with microtubules and actin filaments is dependent on the interaction of NS3 and NS5A. J Virol 2008;82:8838-8848. https://doi.org/10.1128/JVI.00398-08
  46. Saxena V, Lai CK, Chao TC, Jeng KS, Lai MM. Annexin A2 is involved in the formation of hepatitis C virus replication complex on the lipid raft. J Virol 2012;86:4139-4150. https://doi.org/10.1128/JVI.06327-11
  47. Soh TK, Whelan SP. Tracking the fate of genetically distinct vesicular stomatitis virus matrix proteins highlights the role for late domains in assembly. J Virol 2015;89:11750-11760. https://doi.org/10.1128/JVI.01371-15
  48. Hollas H, Aukrust I, Grimmer S, Strand E, Flatmark T, Vedeler A. Annexin A2 recognises a specific region in the 3'-UTR of its cognate messenger RNA. Biochim Biophys Acta 2006;1763:1325-1334. https://doi.org/10.1016/j.bbamcr.2006.08.043
  49. Santos-Valencia JC, Cancio-Lonches C, Trujillo-Uscanga A, Alvarado-Hernandez B, Lagunes-Guillen A, Gutierrez-Escolano AL. Annexin A2 associates to feline calicivirus RNA in the replication complexes from infected cells and participates in an efficient viral replication. Virus Res 2019;261:1-8. https://doi.org/10.1016/j.virusres.2018.12.003