Rab18 binds to classical swine fever virus NS5A and mediates viral replication and assembly in swine umbilical vein endothelial cells

References

• Moennig V. The control of classical swine fever in wild boar. Front Microbiol. 2015;6:1211.
   PubMed Web of Science ®Google Scholar
• Rossi S, Staubach C, Blome S, et al. Controlling of CSFV in European wild boar using oral vaccination: a review. Front Microbiol. 2015;6:1141.
   PubMed Web of Science ®Google Scholar
• Ji W, Guo Z, Ding NZ, et al. Studying classical swine fever virus: making the best of a bad virus. Virus Res. 2014;197:35–47.
   PubMed Web of Science ®Google Scholar
• Lin Z, Liang W, Kang K, et al. Classical swine fever virus and p7 protein induce secretion of IL-1β in macrophages. J Gen Virol. 2014;95(12):2693–2699.
   PubMedGoogle Scholar
• Luo Y, Ji S, Liu Y, et al. Isolation and characterization of a moderately virulent classical swine fever virus emerging in China. Transbound Emerg Dis. 2017;64(6):1848–1857.
   PubMed Web of Science ®Google Scholar
• He L, Zhang YM, Lin Z, et al. Classical swine fever virus NS5A protein localizes to endoplasmic reticulum and induces oxidative stress in vascular endothelial cells. Virus Genes. 2012;45(2):274–282.
   PubMed Web of Science ®Google Scholar
• Tellinghuisen TL, Marcotrigiano J, Gorbalenya AE, et al. The NS5A protein of hepatitis C virus is a zinc metalloprotein. J Biol Chem. 2004;279(47):48576–48587.
   PubMed Web of Science ®Google Scholar
• Tellinghuisen TL, Marcotrigiano J, Rice CM. Structure of the zinc-binding domain of an essential component of the hepatitis C virus replicase. Nature. 2005;435(7040):374–379.
   PubMed Web of Science ®Google Scholar
• Tellinghuisen TL, Paulson MS, Rice CM. The NS5A protein of bovine viral diarrhea virus contains an essential zinc-binding site similar to that of the Hepatitis C virus NS5A protein. J Virol. 2006;80(15):7450–7458.
   PubMed Web of Science ®Google Scholar
• Sheng C, Zhu Z, Yu J, et al. Characterization of NS3, NS5A and NS5B of classical swine fever virus through mutation and complementation analysis. Vet Microbiol. 2010;140(1–2):72–80.
   PubMed Web of Science ®Google Scholar
• Risager PC, Fahnøe U, Gullberg M, et al. Analysis of classical swine fever virus RNA replication determinants using replicons. J Gen Virol. 2013;94(8):1739–1748.
   PubMedGoogle Scholar
• Sheng C, Kou S, Jiang Q, et al. Characterization of the C-terminal sequence of NS5A necessary for the assembly and production of classical swine fever virus infectious particles. Res Vet Sci. 2014;97(2):449–454.
   PubMed Web of Science ®Google Scholar
• Chen Y, Xiao J, Xiao J, et al. Classical swine fever virus NS5A regulates viral RNA replication through binding to NS5B and 3ʹUTR. Virology. 2012;432(2):376–388.
   PubMed Web of Science ®Google Scholar
• Sheng C, Wang J, Xiao J, et al. Classical swine fever virus NS5B protein suppresses the inhibitory effect of NS5A on viral translation by binding to NS5A. J Gen Virol. 2012;93(5):939–950.
   PubMedGoogle Scholar
• Liu X, Sheng C, Zhou C, et al. Annexin A2 is involved in the production of classical swine fever virus infectious particles. J Gen Virol. 2015;96(5):1027–1032.
   PubMedGoogle Scholar
• Zhang C, Kang K, Ning P, et al. Heat shock protein 70 is associated with CSFV NS5A protein and enhances viral RNA replication. Virology. 2015;482:9–18.
   PubMed Web of Science ®Google Scholar
• Lin J, Wang C, Liang W, et al. Rab1A is required for assembly of classical swine fever virus particle. Virology. 2017;514:18.
   PubMed Web of Science ®Google Scholar
• Bhuin T, Roy JK. Rab proteins: the key regulators of intracellular vesicle transport. Exp Cell Res. 2014;328(1):1–19.
   PubMed Web of Science ®Google Scholar
• Müller MP, Goody RS. Molecular control of Rab activity by GEFs, GAPs and GDI. Small GTPases. 2018;9(1–2):5–21.
   PubMedGoogle Scholar
• Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol. 2009;10(8):513–525.
   PubMed Web of Science ®Google Scholar
• Martin S, Driessen K, Nixon SJ, et al. Regulated localization of Rab18 to lipid droplets. J Biol Chem. 2005;280(51):42325–42335.
   PubMed Web of Science ®Google Scholar
• Dejgaard SY, Murshid A, Erman A, et al. Rab18 and Rab43 have key roles in ER-Golgi trafficking. J Cell Sci. 2008;121(16):2768–2781.
   PubMed Web of Science ®Google Scholar
• Ozeki S. Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J Cell Sci. 2005;118(12):2601–2611.
   PubMed Web of Science ®Google Scholar
• Wu Q, Sun X, Yue W, et al. RAB18, a protein associated with Warburg Micro syndrome, controls neuronal migration in the developing cerebral cortex. Mol Brain. 2016;9(1):19.
   PubMedGoogle Scholar
• Wu B, Qi R, Liu X, et al. Rab18 overexpression promotes proliferation and chemoresistance through regulation of mitochondrial function in human gastric cancer. Onco Targets Ther. 2018;11:7805.
   PubMed Web of Science ®Google Scholar
• Dansako H, Hiramoto H, Ikeda M, et al. Rab18 is required for viral assembly of hepatitis C virus through trafficking of the core protein to lipid droplets. Virology. 2014;462:166–174.
   PubMed Web of Science ®Google Scholar
• Salloum S, Wang H, Ferguson C, et al. Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets. PLoS Pathog. 2013;9(8):e1003513.
   PubMed Web of Science ®Google Scholar
• Zhao L, Imperiale MJ, Duprex WP. Identification of Rab18 as an essential host factor for BK polyomavirus infection using a whole-genome RNA interference screen. mSphere. 2017;2(4):e00291–17.
   PubMed Web of Science ®Google Scholar
• Tang WC, Lin RJ, Liao CL, et al. Rab18 facilitates dengue virus infection by targeting fatty acid synthase to sites of viral replication. J Virol. 2014;88(12):6793–6804.
   PubMed Web of Science ®Google Scholar
• Shi BJ, Liu CC, Zhou J, et al. Entry of classical swine fever virus into PK-15 cells via a pH-, dynamin-, and cholesterol-dependent, clathrin-mediated endocytic pathway that requires Rab5 and Rab7. J Virol. 2016;90(20):9194–9208.
   PubMed Web of Science ®Google Scholar
• Hong HX, Zhang YM, Xu H, et al. Immortalization of swine umbilical vein endothelial cells with human telomerase reverse transcriptase. Mol Cells. 2007;24(3):358–363.
   PubMed Web of Science ®Google Scholar
• Liang W, Zheng M, Bao C, et al. CSFV proliferation is associated with GBF1 and Rab2. J Biosci. 2016;42(1):1–14.
   Web of Science ®Google Scholar
• Dejgaard SY, Presley JF. Rab18: new insights into the function of an essential protein. Cell Mol Life Sci. 2019;76(10):1935‐1945.
   PubMed Web of Science ®Google Scholar
• Spearman P. Viral interactions with host cell Rab GTPases. Small GTPases. 2018;9(1–2):192–201.
   PubMedGoogle Scholar
• Vazquez-Martinez R, Cruz-Garcia D, Duran-Prado M, et al. Rab18 inhibits secretory activity in neuroendocrine cells by interacting with secretory granules. Traffic. 2007;8(7):867–882.
   PubMed Web of Science ®Google Scholar
• Feldmann A, Bekbulat F, Huesmann H, et al. The RAB GTPase RAB18 modulates macroautophagy and proteostasis. Biochem Biophys Res Commun. 2017;486(3):738–743.
   PubMed Web of Science ®Google Scholar
• Hsu NY, Ilnytska O, Belov G, et al. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell. 2010;141(5):799–811.
   PubMed Web of Science ®Google Scholar
• Takacs CN, Andreo U, Dao Thi VL, et al. Differential regulation of lipoprotein and hepatitis c virus secretion by Rab1b. Cell Rep. 2017;21(2):431–441.
   PubMed Web of Science ®Google Scholar
• Inoue J, Krueger EW, Chen J, et al. HBV secretion is regulated through the activation of endocytic and autophagic compartments mediated by Rab7 stimulation. J Cell Sci. 2015;128(9):1696–1706.
   PubMed Web of Science ®Google Scholar
• Caillet M, Janvier K, Pelchen–Matthews A, et al. Rab7A is required for efficient production of infectious HIV-1. PLoS Pathog. 2011;7(11):e1002347.
   Web of Science ®Google Scholar
• Zhang J, Zhang X, Liu G, et al. Intracellular trafficking network of protein nanocapsules: endocytosis, exocytosis and autophagy. Theranostics. 2016;6(12):2099–2113.
   PubMed Web of Science ®Google Scholar
• Blanchard E, Belouzard S, Goueslain L, et al. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J Virol. 2006;80(14):6964–6972.
   PubMed Web of Science ®Google Scholar
• Lecot S, Belouzard S, Dubuisson J, et al. Bovine viral diarrhea virus entry is dependent on clathrin-mediated endocytosis. J Virol. 2005;79(16):10826–10829.
   PubMed Web of Science ®Google Scholar
• Zhang YN, Liu YY, Xiao FC, et al. Rab5, Rab7, and Rab11 are required for caveolae-dependent endocytosis of classic swine fever virus in porcine alveolar macrophages. J Virol. 2018;JVI.00797–18. DOI:https://doi.org/10.1128/JVI.00797-18.
   Google Scholar
• Ning P, Gao L, Zhou Y, et al. Caveolin-1-mediated endocytic pathway is involved in classical swine fever virus Shimen infection of porcine alveolar macrophages. Vet Microbiol. 2016;195:81–86.
   PubMed Web of Science ®Google Scholar
• Chen TC, Hsieh CH, Sarnow P. Supporting role for GTPase Rab27a in hepatitis C virus RNA replication through a novel miR-122-mediated effect. PLoS Pathog. 2015;11(8):e1005116.
   Web of Science ®Google Scholar
• Alexandrov K, Horiuchi H, Steele-Mortimer O, et al. Rab escort protein-1 is a multifunctional protein that accompanies newly prenylated Rab proteins to their target membranes. Embo J. 1994;13(22):5262–5273.
   PubMed Web of Science ®Google Scholar
• Leung KF, Baron R, Seabra MC. Thematic review series: lipid posttranslational modifications. geranylgeranylation of Rab GTPases. J Lipid Res. 2006;47(3):467–475.
   PubMed Web of Science ®Google Scholar
• Wu YW, Tan KT, Waldmann H, et al. Interaction analysis of prenylated Rab GTPase with Rab escort protein and GDP dissociation inhibitor explains the need for both regulators. Proc Natl Acad Sci U S A. 2007;104(30):2294–12299.
   Web of Science ®Google Scholar
• Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev. 2011;91(1):119–149.
   PubMed Web of Science ®Google Scholar