Skip to main content

Advertisement

SpringerLink
Log in

The Restrictome of Flaviviruses

  • REVIEW
  • Published:
Virologica Sinica

Abstract

Flaviviruses are a genus of mostly arthropod-borne RNA viruses that cause a range of pathologies in humans. Basic knowledge on flaviviruses is rapidly expanding, partly due to their status as frequent emerging or re-emerging pathogens. Flaviviruses include the dengue, Zika, West Nile, tick-borne encephalitis and yellow fever viruses (DENV, ZIKV, WNV, TBEV and YFV, respectively). As is the case with other families of viruses, the success of productive infection of human cells by flaviviruses depends in part on the antiviral activity of a heterogeneous group of cellular antiviral proteins called restriction factors. Restriction factors are the effector proteins of the cell-autonomous innate response against viruses, an immune pathway that also includes virus sensors as well as intracellular and extracellular signal mediators such as type I interferons (IFN-I). In this review, I summarize recent progress toward the identification and characterization of flavivirus restriction factors. In particular, I focus on IFI6, Schlafen 11, FMRP, OAS-RNase L, RyDEN, members of the TRIM family of proteins (TRIM5α, TRIM19, TRIM56, TRIM69 and TRIM79α) and a new mechanism of action proposed for viperin. Recent and future studies on this topic will lead to a more complete picture of the flavivirus restrictome, defined as the ensemble of cellular factors with demonstrated anti-flaviviral activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Aguirre S, Maestre AM, Pagni S, Patel JR, Savage T, Gutman D, Maringer K, Bernal-Rubio D, Shabman RS, Simon V, Rodriguez-Madoz JR, Mulder LC, Barber GN, Fernandez-Sesma A (2012) DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog 8:e1002934

    PubMed  PubMed Central  Google Scholar 

  • Aktepe TE, Mackenzie JM (2018) Shaping the flavivirus replication complex: It is curvaceous! Cell Microbiol 20:e12884

    PubMed  PubMed Central  Google Scholar 

  • Arakawa M, Morita E (2019) Flavivirus replication organelle biogenesis in the endoplasmic reticulum: comparison with other single-stranded positive-sense RNA viruses. Int J Mol Sci 20:2336

    PubMed Central  CAS  Google Scholar 

  • Augustine AD, Cassetti MC, Ennis FA, Harris E, Hildebrand WH, Repik PM (2010) NIAID workshop on Flavivirus immunity. Viral Immunol 23:235–240

    PubMed  PubMed Central  CAS  Google Scholar 

  • Balinsky CA, Schmeisser H, Wells AI, Ganesan S, Jin T, Singh K, Zoon KC (2017) IRAV (FLJ11286), an interferon-stimulated gene with antiviral activity against dengue virus, interacts with MOV10. J Virol 91:e01606

    PubMed  PubMed Central  CAS  Google Scholar 

  • Banerjee S, Gusho E, Gaughan C, Dong B, Gu X, Holvey-Bates E, Talukdar M, Li Y, Weiss SR, Sicheri F, Saunthararajah Y, Stark GR, Silverman RH (2019) OAS-RNase L innate immune pathway mediates the cytotoxicity of a DNA-demethylating drug. Proc Natl Acad Sci USA 116:5071–5076

    PubMed  CAS  PubMed Central  Google Scholar 

  • Best SM (2016) Flaviviruses. Curr Biol 26:R1258–R1260

    PubMed  CAS  Google Scholar 

  • Brasil P, Pereira JP Jr, Moreira ME, Ribeiro Nogueira RM, Damasceno L, Wakimoto M, Rabello RS, Valderramos SG, Halai UA, Salles TS, Zin AA, Horovitz D, Daltro P, Boechat M, Raja Gabaglia C, Carvalho de Sequeira P, Pilotto JH, Medialdea-Carrera R, Cotrim da Cunha D, Abreu de Carvalho LM, Pone M, Machado Siqueira A, Calvet GA, Rodrigues Baiao AE, Neves ES, Nassar de Carvalho PR, Hasue RH, Marschik PB, Einspieler C, Janzen C, Cherry JD, Bispo de Filippis AM, Nielsen-Saines K (2016) Zika virus infection in pregnant women in Rio de Janeiro. N Engl J Med 375:2321–2334

    PubMed  PubMed Central  Google Scholar 

  • Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, Ryan BJ, Weyer JL, van der Weyden L, Fikrig E, Adams DJ, Xavier RJ, Farzan M, Elledge SJ (2009) The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139:1243–1254

    PubMed  PubMed Central  Google Scholar 

  • Campbell EM, Perez O, Anderson JL, Hope TJ (2008) Visualization of a proteasome-independent intermediate during restriction of HIV-1 by rhesus TRIM5alpha. J Cell Biol 180:549–561

    PubMed  PubMed Central  CAS  Google Scholar 

  • Carthagena L, Bergamaschi A, Luna JM, David A, Uchil PD, Margottin-Goguet F, Mothes W, Hazan U, Transy C, Pancino G, Nisole S (2009) Human TRIM gene expression in response to interferons. PLoS ONE 4:e4894

    PubMed  PubMed Central  Google Scholar 

  • Chan YL, Chang TH, Liao CL, Lin YL (2008) The cellular antiviral protein viperin is attenuated by proteasome-mediated protein degradation in Japanese encephalitis virus-infected cells. J Virol 82:10455–10464

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chen E, Sharma MR, Shi X, Agrawal RK, Joseph S (2014) Fragile X mental retardation protein regulates translation by binding directly to the ribosome. Mol Cell 54:407–417

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chin KC, Cresswell P (2001) Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc Natl Acad Sci USA 98:15125–15130

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chiramel AI, Meyerson NR, McNally KL, Broeckel RM, Montoya VR, Mendez-Solis O, Robertson SJ, Sturdevant GL, Lubick KJ, Nair V, Youseff BH, Ireland RM, Bosio CM, Kim K, Luban J, Hirsch VM, Taylor RT, Bouamr F, Sawyer SL, Best SM (2019) TRIM5alpha restricts flavivirus replication by targeting the viral protease for proteasomal degradation. Cell Rep 27(3269–3283):e3266

    Google Scholar 

  • Courtney SC, Di H, Stockman BM, Liu H, Scherbik SV, Brinton MA (2012) Identification of novel host cell binding partners of Oas1b, the protein conferring resistance to flavivirus-induced disease in mice. J Virol 86:7953–7963

    PubMed  PubMed Central  CAS  Google Scholar 

  • Daffis S, Szretter KJ, Schriewer J, Li J, Youn S, Errett J, Lin TY, Schneller S, Zust R, Dong H, Thiel V, Sen GC, Fensterl V, Klimstra WB, Pierson TC, Buller RM, Gale M Jr, Shi PY, Diamond MS (2010) 2’-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468:452–456

    PubMed  PubMed Central  CAS  Google Scholar 

  • Davis JK, Broadie K (2017) Multifarious functions of the fragile X mental retardation protein. Trends Genet 33:703–714

    PubMed  PubMed Central  CAS  Google Scholar 

  • De La Cruz Hernandez SI, Puerta-Guardo H, Flores-Aguilar H, Gonzalez-Mateos S, Lopez-Martinez I, Ortiz-Navarrete V, Ludert JE, Del Angel RM (2014) A strong interferon response correlates with a milder dengue clinical condition. J Clin Virol 60:196–199

    Google Scholar 

  • Deo S, Patel TR, Dzananovic E, Booy EP, Zeid K, McEleney K, Harding SE, McKenna SA (2014) Activation of 2’ 5’-oligoadenylate synthetase by stem loops at the 5’-end of the West Nile virus genome. PLoS ONE 9:e92545

    PubMed  PubMed Central  Google Scholar 

  • Diamond MS (2009) Mechanisms of evasion of the type I interferon antiviral response by flaviviruses. J Interferon Cytokine Res 29:521–530

    PubMed  CAS  Google Scholar 

  • Diamond MS, Roberts TG, Edgil D, Lu B, Ernst J, Harris E (2000) Modulation of dengue virus infection in human cells by alpha, beta, and gamma interferons. J Virol 74:4957–4966

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ding Q, Gaska JM, Douam F, Wei L, Kim D, Balev M, Heller B, Ploss A (2018) Species-specific disruption of STING-dependent antiviral cellular defenses by the Zika virus NS2B3 protease. Proc Natl Acad Sci USA 115:E6310–E6318

    PubMed  CAS  PubMed Central  Google Scholar 

  • D’Ortenzio E, Matheron S, Yazdanpanah Y, de Lamballerie X, Hubert B, Piorkowski G, Maquart M, Descamps D, Damond F, Leparc-Goffart I (2016) Evidence of sexual transmission of Zika virus. N Engl J Med 374:2195–2198

    PubMed  Google Scholar 

  • Dukhovny A, Lamkiewicz K, Chen Q, Fricke M, Jabrane-Ferrat N, Marz M, Jung JU, Sklan EH (2019) A CRISPR activation screen identifies genes that protect against Zika virus infection. J Virol 93:e00211

    PubMed  PubMed Central  CAS  Google Scholar 

  • Duschene KS, Broderick JB (2010) The antiviral protein viperin is a radical SAM enzyme. FEBS Lett 584:1263–1267

    PubMed  PubMed Central  CAS  Google Scholar 

  • Everett RD, Parada C, Gripon P, Sirma H, Orr A (2008) Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J Virol 82:2661–2672

    PubMed  CAS  Google Scholar 

  • Fensterl V, Sen GC (2015) Interferon-induced Ifit proteins: their role in viral pathogenesis. J Virol 89:2462–2468

    PubMed  Google Scholar 

  • Fink J, Gu F, Ling L, Tolfvenstam T, Olfat F, Chin KC, Aw P, George J, Kuznetsov VA, Schreiber M, Vasudevan SG, Hibberd ML (2007) Host gene expression profiling of dengue virus infection in cell lines and patients. PLoS Negl Trop Dis 1:e86

    PubMed  PubMed Central  Google Scholar 

  • Fitzgerald KA (2011) The interferon inducible gene: viperin. J Interferon Cytokine Res 31:131–135

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ganser-Pornillos BK, Pornillos O (2019) Restriction of HIV-1 and other retroviruses by TRIM5. Nat Rev Microbiol 17:546–556

    PubMed  CAS  PubMed Central  Google Scholar 

  • Giovannoni F, Damonte EB, Garcia CC (2015) Cellular promyelocytic leukemia protein is an important dengue virus restriction factor. PLoS ONE 10:e0125690

    PubMed  PubMed Central  Google Scholar 

  • Gizzi AS, Grove TL, Arnold JJ, Jose J, Jangra RK, Garforth SJ, Du Q, Cahill SM, Dulyaninova NG, Love JD, Chandran K, Bresnick AR, Cameron CE, Almo SC (2018) A naturally occurring antiviral ribonucleotide encoded by the human genome. Nature 558:610–614

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gorman MJ, Poddar S, Farzan M, Diamond MS (2016) The interferon-stimulated gene Ifitm3 restricts West Nile virus infection and pathogenesis. J Virol 90:8212–8225

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gotovtseva EP, Kapadia AS, Smolensky MH, Lairson DR (2008) Optimal frequency of imiquimod (aldara) 5% cream for the treatment of external genital warts in immunocompetent adults: a meta-analysis. Sex Transm Dis 35:346–351

    PubMed  CAS  Google Scholar 

  • Gould EA, Solomon T (2008) Pathogenic flaviviruses. Lancet 371:500–509

    PubMed  CAS  Google Scholar 

  • Grotzinger T, Sternsdorf T, Jensen K, Will H (1996) Interferon-modulated expression of genes encoding the nuclear-dot-associated proteins Sp100 and promyelocytic leukemia protein (PML). Eur J Biochem 238:554–560

    PubMed  CAS  Google Scholar 

  • Gunther T, Schreiner S, Dobner T, Tessmer U, Grundhoff A (2014) Influence of ND10 components on epigenetic determinants of early KSHV latency establishment. PLoS Pathog 10:e1004274

    PubMed  PubMed Central  Google Scholar 

  • Gusho E, Baskar D, Banerjee S (2016) New advances in our understanding of the “unique” RNase L in host pathogen interaction and immune signaling. Cytokine. https://doi.org/10.1016/j.cyto.2016.08.009

    Article  PubMed  PubMed Central  Google Scholar 

  • Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, Hunsperger E, Kroeger A, Margolis HS, Martinez E, Nathan MB, Pelegrino JL, Simmons C, Yoksan S, Peeling RW (2010) Dengue: a continuing global threat. Nat Rev Microbiol 8:S7–16

    PubMed  PubMed Central  CAS  Google Scholar 

  • Han R, Wang R, Zhao Q, Han Y, Zong S, Miao S, Song W, Wang L (2016) Trim69 regulates zebrafish brain development by ap-1 pathway. Sci Rep 6:24034

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hatakeyama S (2017) TRIM family proteins: roles in autophagy, immunity, and carcinogenesis. Trends Biochem Sci 42:297–311

    PubMed  CAS  Google Scholar 

  • Helbig KJ, Lau DT, Semendric L, Harley HA, Beard MR (2005) Analysis of ISG expression in chronic hepatitis C identifies viperin as a potential antiviral effector. Hepatology 42:702–710

    PubMed  CAS  Google Scholar 

  • Helbig KJ, Carr JM, Calvert JK, Wati S, Clarke JN, Eyre NS, Narayana SK, Fiches GN, McCartney EM, Beard MR (2013) Viperin is induced following dengue virus type-2 (DENV-2) infection and has anti-viral actions requiring the C-terminal end of viperin. PLoS Negl Trop Dis 7:e2178

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hinson ER, Cresswell P (2009a) The antiviral protein, viperin, localizes to lipid droplets via its N-terminal amphipathic alpha-helix. Proc Natl Acad Sci USA 106:20452–20457

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hinson ER, Cresswell P (2009b) The N-terminal amphipathic alpha-helix of viperin mediates localization to the cytosolic face of the endoplasmic reticulum and inhibits protein secretion. J Biol Chem 284:4705–4712

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hotter D, Sauter D, Kirchhoff F (2013) Emerging role of the host restriction factor tetherin in viral immune sensing. J Mol Biol 425:4956–4964

    PubMed  CAS  Google Scholar 

  • Jiang D, Weidner JM, Qing M, Pan XB, Guo H, Xu C, Zhang X, Birk A, Chang J, Shi PY, Block TM, Guo JT (2010) Identification of five interferon-induced cellular proteins that inhibit west nile virus and dengue virus infections. J Virol 84:8332–8341

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kim YE, Ahn JH (2015) Positive role of promyelocytic leukemia protein in type I interferon response and its regulation by human cytomegalovirus. PLoS Pathog 11:e1004785

    PubMed  PubMed Central  Google Scholar 

  • Kimura T, Katoh H, Kayama H, Saiga H, Okuyama M, Okamoto T, Umemoto E, Matsuura Y, Yamamoto M, Takeda K (2013) Ifit1 inhibits Japanese encephalitis virus replication through binding to 5’ capped 2’-O unmethylated RNA. J Virol 87:9997–10003

    PubMed  PubMed Central  CAS  Google Scholar 

  • Konermann S, Brigham MD, Trevino AE, Joung J, Abudayyeh OO, Barcena C, Hsu PD, Habib N, Gootenberg JS, Nishimasu H, Nureki O, Zhang F (2015) Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517:583–588

    PubMed  CAS  Google Scholar 

  • Krishnan MN, Ng A, Sukumaran B, Gilfoy FD, Uchil PD, Sultana H, Brass AL, Adametz R, Tsui M, Qian F, Montgomery RR, Lev S, Mason PW, Koski RA, Elledge SJ, Xavier RJ, Agaisse H, Fikrig E (2008) RNA interference screen for human genes associated with West Nile virus infection. Nature 455:242–245

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lallemand-Breitenbach V, de The H (2018) PML nuclear bodies: from architecture to function. Curr Opin Cell Biol 52:154–161

    PubMed  CAS  Google Scholar 

  • Lewy TG, Grabowski JM, Bloom ME (2017) BiP: master regulator of the unfolded protein response and crucial factor in flavivirus biology. Yale J Biol Med 90:291–300

    PubMed  PubMed Central  CAS  Google Scholar 

  • Li M, Kao E, Gao X, Sandig H, Limmer K, Pavon-Eternod M, Jones TE, Landry S, Pan T, Weitzman MD, David M (2012) Codon-usage-based inhibition of HIV protein synthesis by human schlafen 11. Nature 491:125–128

    PubMed  PubMed Central  CAS  Google Scholar 

  • Li J, Ding SC, Cho H, Chung BC, Gale M Jr, Chanda SK, Diamond MS (2013) A short hairpin RNA screen of interferon-stimulated genes identifies a novel negative regulator of the cellular antiviral response. MBio 4:e00385-00313

    Google Scholar 

  • Lin RJ, Chang BL, Yu HP, Liao CL, Lin YL (2006) Blocking of interferon-induced Jak-Stat signaling by Japanese encephalitis virus NS5 through a protein tyrosine phosphatase-mediated mechanism. J Virol 80:5908–5918

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lin RJ, Yu HP, Chang BL, Tang WC, Liao CL, Lin YL (2009) Distinct antiviral roles for human 2’,5’-oligoadenylate synthetase family members against dengue virus infection. J Immunol 183:8035–8043

    PubMed  CAS  Google Scholar 

  • Liu SY, Sanchez DJ, Cheng G (2011) New developments in the induction and antiviral effectors of type I interferon. Curr Opin Immunol 23:57–64

    PubMed  Google Scholar 

  • Liu B, Li NL, Wang J, Shi PY, Wang T, Miller MA, Li K (2014) Overlapping and distinct molecular determinants dictating the antiviral activities of TRIM56 against flaviviruses and coronavirus. J Virol 88:13821–13835

    PubMed  PubMed Central  Google Scholar 

  • Lopez-Gonzalez M, Meza-Sanchez D, Garcia-Cordero J, Bustos-Arriaga J, Velez-Del Valle C, Marsch-Moreno M, Castro-Jimenez T, Flores-Romo L, Santos-Argumedo L, Gutierrez-Castaneda B, Cedillo-Barron L (2018) Human keratinocyte cultures (HaCaT) can be infected by DENV, triggering innate immune responses that include IFNlambda and LL37. Immunobiology 223:608–617

    PubMed  CAS  Google Scholar 

  • Malone D, Lardelli RM, Li M, David M (2019) Dephosphorylation activates the interferon-stimulated schlafen family member 11 in the DNA damage response. J Biol Chem. https://doi.org/10.1074/jbc.RA118.006588

    Article  PubMed  PubMed Central  Google Scholar 

  • Manokaran G, Finol E, Wang C, Gunaratne J, Bahl J, Ong EZ, Tan HC, Sessions OM, Ward AM, Gubler DJ, Harris E, Garcia-Blanco MA, Ooi EE (2015) Dengue subgenomic RNA binds TRIM25 to inhibit interferon expression for epidemiological fitness. Science 350:217–221

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mark KE, Corey L, Meng TC, Magaret AS, Huang ML, Selke S, Slade HB, Tyring SK, Warren T, Sacks SL, Leone P, Bergland VA, Wald A (2007) Topical resiquimod 0.01% gel decreases herpes simplex virus type 2 genital shedding: a randomized, controlled trial. J Infect Dis 195:1324–1331

    PubMed  CAS  Google Scholar 

  • Martinot AJ, Abbink P, Afacan O, Prohl AK, Bronson R, Hecht JL, Borducchi EN, Larocca RA, Peterson RL, Rinaldi W, Ferguson M, Didier PJ, Weiss D, Lewis MG, De La Barrera RA, Yang E, Warfield SK, Barouch DH (2018) Fetal neuropathology in Zika virus-infected pregnant female rhesus monkeys. Cell 173(1111–1122):e1110

    Google Scholar 

  • Mashimo T, Lucas M, Simon-Chazottes D, Frenkiel MP, Montagutelli X, Ceccaldi PE, Deubel V, Guenet JL, Despres P (2002) A nonsense mutation in the gene encoding 2’-5’-oligoadenylate synthetase/L1 isoform is associated with West Nile virus susceptibility in laboratory mice. Proc Natl Acad Sci USA 99:11311–11316

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mashimo T, Glaser P, Lucas M, Simon-Chazottes D, Ceccaldi PE, Montagutelli X, Despres P, Guenet JL (2003) Structural and functional genomics and evolutionary relationships in the cluster of genes encoding murine 2’,5’-oligoadenylate synthetases. Genomics 82:537–552

    PubMed  CAS  Google Scholar 

  • Masroori N, Merindol N, Berthoux L (2016) The interferon-induced antiviral protein PML (TRIM19) promotes the restriction and transcriptional silencing of lentiviruses in a context-specific, isoform-specific fashion. Retrovirology 13:19

    PubMed  PubMed Central  Google Scholar 

  • Mavrommatis E, Fish EN, Platanias LC (2013) The schlafen family of proteins and their regulation by interferons. J Interferon Cytokine Res 33:206–210

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mazeaud C, Freppel W, Chatel-Chaix L (2018) The multiples fates of the flavivirus RNA genome during pathogenesis. Front Genet 9:595

    PubMed  PubMed Central  CAS  Google Scholar 

  • Merindol N, El-Far M, Sylla M, Masroori N, Dufour C, Li JX, Cherry P, Plourde MB, Tremblay C, Berthoux L (2018) HIV-1 capsids from B27/B57+ elite controllers escape Mx2 but are targeted by TRIM5alpha, leading to the induction of an antiviral state. PLoS Pathog 14:e1007398

    PubMed  PubMed Central  Google Scholar 

  • Miner JJ, Cao B, Govero J, Smith AM, Fernandez E, Cabrera OH, Garber C, Noll M, Klein RS, Noguchi KK, Mysorekar IU, Diamond MS (2016) Zika virus infection during pregnancy in mice causes placental damage and fetal demise. Cell 165:1081–1091

    PubMed  PubMed Central  CAS  Google Scholar 

  • Miorin L, Maestre AM, Fernandez-Sesma A, Garcia-Sastre A (2017) Antagonism of type I interferon by flaviviruses. Biochem Biophys Res Commun 492:587–596

    PubMed  PubMed Central  CAS  Google Scholar 

  • Munoz-Jordan JL, Sanchez-Burgos GG, Laurent-Rolle M, Garcia-Sastre A (2003) Inhibition of interferon signaling by dengue virus. Proc Natl Acad Sci USA 100:14333–14338

    PubMed  CAS  PubMed Central  Google Scholar 

  • Neil SJ, Zang T, Bieniasz PD (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425–430

    PubMed  CAS  Google Scholar 

  • Ozato K, Shin DM, Chang TH, Morse HC 3rd (2008) TRIM family proteins and their emerging roles in innate immunity. Nat Rev Immunol 8:849–860

    PubMed  PubMed Central  CAS  Google Scholar 

  • Padmanabhan R, Mueller N, Reichert E, Yon C, Teramoto T, Kono Y, Takhampunya R, Ubol S, Pattabiraman N, Falgout B, Ganesh VK, Murthy K (2006) Multiple enzyme activities of flavivirus proteins. Novartis Found Symp 277:74–84 discussion 84–76, 251–253

    PubMed  CAS  Google Scholar 

  • Panayiotou C, Lindqvist R, Kurhade C, Vonderstein K, Pasto J, Edlund K, Upadhyay AS, Overby AK (2018) Viperin restricts Zika virus and tick-borne encephalitis virus replication by targeting NS3 for proteasomal degradation. J Virol 92:e02054

    PubMed  PubMed Central  CAS  Google Scholar 

  • Perelygin AA, Scherbik SV, Zhulin IB, Stockman BM, Li Y, Brinton MA (2002) Positional cloning of the murine flavivirus resistance gene. Proc Natl Acad Sci USA 99:9322–9327

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, Bisiaux A, Albert ML, Strambio-De-Castillia C, Mothes W, Pizzato M, Grutter MG, Luban J (2011) TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472:361–365

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pestka S, Krause CD, Walter MR (2004) Interferons, interferon-like cytokines, and their receptors. Immunol Rev 202:8–32

    PubMed  CAS  Google Scholar 

  • Peterson E, Shippee E, Brinton MA, Kaur P (2019) Biochemical characterization of the mouse ABCF3 protein, a partner of the flavivirus-resistance protein OAS1B. J Biol Chem. https://doi.org/10.1074/jbc.RA119.008477

    Article  PubMed  PubMed Central  Google Scholar 

  • Reymond A, Meroni G, Fantozzi A, Merla G, Cairo S, Luzi L, Riganelli D, Zanaria E, Messali S, Cainarca S, Guffanti A, Minucci S, Pelicci PG, Ballabio A (2001) The tripartite motif family identifies cell compartments. EMBO J 20:2140–2151

    PubMed  PubMed Central  CAS  Google Scholar 

  • Richardson RB, Ohlson MB, Eitson JL, Kumar A, McDougal MB, Boys IN, Mar KB, De La Cruz-Rivera PC, Douglas C, Konopka G, Xing C, Schoggins JW (2018) A CRISPR screen identifies IFI6 as an ER-resident interferon effector that blocks flavivirus replication. Nat Microbiol 3:1214–1223

    PubMed  PubMed Central  CAS  Google Scholar 

  • Rivieccio MA, Suh HS, Zhao Y, Zhao ML, Chin KC, Lee SC, Brosnan CF (2006) TLR3 ligation activates an antiviral response in human fetal astrocytes: a role for viperin/cig5. J Immunol 177:4735–4741

    PubMed  CAS  Google Scholar 

  • Roa A, Hayashi F, Yang Y, Lienlaf M, Zhou J, Shi J, Watanabe S, Kigawa T, Yokoyama S, Aiken C, Diaz-Griffero F (2012) RING domain mutations uncouple TRIM5alpha restriction of HIV-1 from inhibition of reverse transcription and acceleration of uncoating. J Virol 86:1717–1727

    PubMed  PubMed Central  CAS  Google Scholar 

  • Rodriguez W, Srivastav K, Muller M (2019) C19ORF66 broadly escapes virus-induced endonuclease cleavage and restricts Kaposi’s Sarcoma-Associated Herpesvirus. J Virol 93:e00373

    PubMed  PubMed Central  CAS  Google Scholar 

  • Rogozin IB, Aravind L, Koonin EV (2003) Differential action of natural selection on the N and C-terminal domains of 2’-5’ oligoadenylate synthetases and the potential nuclease function of the C-terminal domain. J Mol Biol 326:1449–1461

    PubMed  CAS  Google Scholar 

  • Saitoh T, Satoh T, Yamamoto N, Uematsu S, Takeuchi O, Kawai T, Akira S (2011) Antiviral protein viperin promotes Toll-like receptor 7- and Toll-like receptor 9-mediated type I interferon production in plasmacytoid dendritic cells. Immunity 34:352–363

    PubMed  CAS  Google Scholar 

  • Samuel MA, Diamond MS (2005) Alpha/beta interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival. J Virol 79:13350–13361

    PubMed  PubMed Central  CAS  Google Scholar 

  • Samuel MA, Whitby K, Keller BC, Marri A, Barchet W, Williams BR, Silverman RH, Gale M Jr, Diamond MS (2006) PKR and RNase L contribute to protection against lethal West Nile virus infection by controlling early viral spread in the periphery and replication in neurons. J Virol 80:7009–7019

    PubMed  PubMed Central  CAS  Google Scholar 

  • Savidis G, Perreira JM, Portmann JM, Meraner P, Guo Z, Green S, Brass AL (2016) The IFITMs Inhibit Zika virus replication. Cell Rep 15:2323–2330

    PubMed  CAS  Google Scholar 

  • Sawyer SL, Wu LI, Emerman M, Malik HS (2005) Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci USA 102:2832–2837

    PubMed  CAS  PubMed Central  Google Scholar 

  • Scherer M, Stamminger T (2016) Emerging role of PML nuclear bodies in innate immune signaling. J Virol 90:5850–5854

    PubMed  PubMed Central  CAS  Google Scholar 

  • Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481–485

    PubMed  PubMed Central  CAS  Google Scholar 

  • Schoggins JW, Dorner M, Feulner M, Imanaka N, Murphy MY, Ploss A, Rice CM (2012) Dengue reporter viruses reveal viral dynamics in interferon receptor-deficient mice and sensitivity to interferon effectors in vitro. Proc Natl Acad Sci USA 109:14610–14615

    PubMed  CAS  PubMed Central  Google Scholar 

  • Shan C, Muruato AE, Nunes BTD, Luo H, Xie X, Medeiros DBA, Wakamiya M, Tesh RB, Barrett AD, Wang T, Weaver SC, Vasconcelos PFC, Rossi SL, Shi PY (2017) A live-attenuated Zika virus vaccine candidate induces sterilizing immunity in mouse models. Nat Med 23:763–767

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sheehy AM, Gaddis NC, Choi JD, Malim MH (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646–650

    PubMed  CAS  Google Scholar 

  • Short KM, Cox TC (2006) Subclassification of the RBCC/TRIM superfamily reveals a novel motif necessary for microtubule binding. J Biol Chem 281:8970–8980

    PubMed  CAS  Google Scholar 

  • Silverman RH (2007) Viral encounters with 2’,5’-oligoadenylate synthetase and RNase L during the interferon antiviral response. J Virol 81:12720–12729

    PubMed  PubMed Central  CAS  Google Scholar 

  • Simmons CP, Popper S, Dolocek C, Chau TN, Griffiths M, Dung NT, Long TH, Hoang DM, Chau NV, le Thao TT, Hien TT, Relman DA, Farrar J (2007) Patterns of host genome-wide gene transcript abundance in the peripheral blood of patients with acute dengue hemorrhagic fever. J Infect Dis 195:1097–1107

    PubMed  PubMed Central  CAS  Google Scholar 

  • Soto-Acosta R, Xie X, Shan C, Baker CK, Shi PY, Rossi SL, Garcia-Blanco MA, Bradrick S (2018) Fragile X mental retardation protein is a Zika virus restriction factor that is antagonized by subgenomic flaviviral RNA. Elife 7:e39023

    PubMed  PubMed Central  Google Scholar 

  • Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J (2004) The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427:848–853

    PubMed  CAS  Google Scholar 

  • Suzuki Y, Chin WX, Han Q, Ichiyama K, Lee CH, Eyo ZW, Ebina H, Takahashi H, Takahashi C, Tan BH, Hishiki T, Ohba K, Matsuyama T, Koyanagi Y, Tan YJ, Sawasaki T, Chu JJ, Vasudevan SG, Sano K, Yamamoto N (2016) Characterization of RyDEN (C19orf66) as an interferon-stimulated cellular inhibitor against dengue virus replication. PLoS Pathog 12:e1005357

    PubMed  PubMed Central  Google Scholar 

  • Szretter KJ, Brien JD, Thackray LB, Virgin HW, Cresswell P, Diamond MS (2011) The interferon-inducible gene viperin restricts West Nile virus pathogenesis. J Virol 85:11557–11566

    PubMed  PubMed Central  CAS  Google Scholar 

  • Szretter KJ, Daniels BP, Cho H, Gainey MD, Yokoyama WM, Gale M Jr, Virgin HW, Klein RS, Sen GC, Diamond MS (2012) 2’-O methylation of the viral mRNA cap by West Nile virus evades ifit1-dependent and -independent mechanisms of host restriction in vivo. PLoS Pathog 8:e1002698

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tabachnick WJ (2016) Climate change and the Arboviruses: lessons from the evolution of the dengue and yellow fever viruses. Annu Rev Virol 3:125–145

    PubMed  CAS  Google Scholar 

  • Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140:805–820

    PubMed  CAS  Google Scholar 

  • Taylor RT, Lubick KJ, Robertson SJ, Broughton JP, Bloom ME, Bresnahan WA, Best SM (2011) TRIM79alpha, an interferon-stimulated gene product, restricts tick-borne encephalitis virus replication by degrading the viral RNA polymerase. Cell Host Microbe 10:185–196

    PubMed  PubMed Central  CAS  Google Scholar 

  • Upadhyay AS, Vonderstein K, Pichlmair A, Stehling O, Bennett KL, Dobler G, Guo JT, Superti-Furga G, Lill R, Overby AK, Weber F (2014) Viperin is an iron-sulfur protein that inhibits genome synthesis of tick-borne encephalitis virus via radical SAM domain activity. Cell Microbiol 16:834–848

    PubMed  CAS  Google Scholar 

  • Usami Y, Wu Y, Gottlinger HG (2015) SERINC3 and SERINC5 restrict HIV-1 infectivity and are counteracted by Nef. Nature 526:218–223

    PubMed  PubMed Central  CAS  Google Scholar 

  • Valdez F, Salvador J, Palermo PM, Mohl JE, Hanley KA, Watts D, Llano M (2019) Schlafen 11 restricts flavivirus replication. J Virol 93:e00104

    PubMed  PubMed Central  CAS  Google Scholar 

  • van Gent M, Sparrer KMJ, Gack MU (2018) TRIM proteins and their roles in antiviral host defenses. Annu Rev Virol 5:385–405

    PubMed  PubMed Central  Google Scholar 

  • Vanwalscappel B, Tada T, Landau NR (2018) Toll-like receptor agonist R848 blocks Zika virus replication by inducing the antiviral protein viperin. Virology 522:199–208

    PubMed  CAS  Google Scholar 

  • von Kleist M, Metzner P, Marquet R, Schutte C (2012) HIV-1 polymerase inhibition by nucleoside analogs: cellular- and kinetic parameters of efficacy, susceptibility and resistance selection. PLoS Comput Biol 8:e1002359

    Google Scholar 

  • Vonderstein K, Nilsson E, Hubel P, Nygard Skalman L, Upadhyay A, Pasto J, Pichlmair A, Lundmark R, Overby AK (2018) Viperin targets flavivirus virulence by inducing assembly of noninfectious capsid particles. J Virol 92:e01751

    PubMed  Google Scholar 

  • Wang X, Hinson ER, Cresswell P (2007) The interferon-inducible protein viperin inhibits influenza virus release by perturbing lipid rafts. Cell Host Microbe 2:96–105

    PubMed  CAS  Google Scholar 

  • Wang J, Liu B, Wang N, Lee YM, Liu C, Li K (2011) TRIM56 is a virus- and interferon-inducible E3 ubiquitin ligase that restricts pestivirus infection. J Virol 85:3733–3745

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang K, Zou C, Wang X, Huang C, Feng T, Pan W, Wu Q, Wang P, Dai J (2018) Interferon-stimulated TRIM69 interrupts dengue virus replication by ubiquitinating viral nonstructural protein 3. PLoS Pathog 14:e1007287

    PubMed  PubMed Central  Google Scholar 

  • Whelan JN, Li Y, Silverman RH, Weiss SR (2019) Zika virus production is resistant to RNase L antiviral activity. J Virol 93:e00313–00319

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wilkins C, Gale M Jr (2010) Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 22:41–47

    PubMed  PubMed Central  CAS  Google Scholar 

  • Xu D, Holko M, Sadler AJ, Scott B, Higashiyama S, Berkofsky-Fessler W, McConnell MJ, Pandolfi PP, Licht JD, Williams BR (2009) Promyelocytic leukemia zinc finger protein regulates interferon-mediated innate immunity. Immunity 30:802–816

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yan N, Chen ZJ (2012) Intrinsic antiviral immunity. Nat Immunol 13:214–222

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yang JY, Deng XY, Li YS, Ma XC, Feng JX, Yu B, Chen Y, Luo YL, Wang X, Chen ML, Fang ZX, Zheng FX, Li YP, Zhong Q, Kang TB, Song LB, Xu RH, Zeng MS, Chen W, Zhang H, Xie W, Gao S (2018) Structure of Schlafen13 reveals a new class of tRNA/rRNA- targeting RNase engaged in translational control. Nat Commun 9:1165

    PubMed  PubMed Central  Google Scholar 

  • Yang D, Li NL, Wei D, Liu B, Guo F, Elbahesh H, Zhang Y, Zhou Z, Chen GY, Li K (2019) The E3 ligase TRIM56 is a host restriction factor of Zika virus and depends on its RNA-binding activity but not miRNA regulation, for antiviral function. PLoS Negl Trop Dis 13:e0007537

    PubMed  PubMed Central  Google Scholar 

  • Yockey LJ, Varela L, Rakib T, Khoury-Hanold W, Fink SL, Stutz B, Szigeti-Buck K, Van den Pol A, Lindenbach BD, Horvath TL, Iwasaki A (2016) Vaginal exposure to Zika virus during pregnancy leads to fetal brain infection. Cell 166(1247–1256):e1244

    Google Scholar 

Download references

Acknowledgements

I apologize to colleagues whose excellent works I did not include in this review.

Author information

Authors and Affiliations

  1. Department of Medical Biology, Université du Québec à Trois-Rivières, Trois-Rivières, QC, Canada

    Lionel Berthoux

Authors
  1. Lionel Berthoux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lionel Berthoux.

Ethics declarations

Conflict of interest

The author declares that he has no conflict of interest.

Animal and Human Rights Statement

This article does not contain any studies with human or animal subjects performed by the author.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Berthoux, L. The Restrictome of Flaviviruses. Virol. Sin. 35, 363–377 (2020). https://doi.org/10.1007/s12250-020-00208-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12250-020-00208-3

Keywords

Search

Navigation