4gv6 › Citations

Structures of arenaviral nucleoproteins with triphosphate dsRNA reveal a unique mechanism of immune suppression.

FIGURE 1.
FIGURE 2.
FIGURE 3.
Jiang X, Huang Q, Wang W, Dong H, Ly H, Liang Y, Dong C
OpenAccess logo J Biol Chem 288 16949-16959 (2013)
Related entries: 4g9z, 4gv3, 4gv9, 4gve

Cited: 63 times
EuropePMC logo PMID: 23615902

Abstract

A hallmark of severe Lassa fever is the generalized immune suppression, the mechanism of which is poorly understood. Lassa virus (LASV) nucleoprotein (NP) is the only known 3'-5' exoribonuclease that can suppress type I interferon (IFN) production possibly by degrading immune-stimulatory RNAs. How this unique enzymatic activity of LASV NP recognizes and processes RNA substrates is unknown. We provide an atomic view of a catalytically active exoribonuclease domain of LASV NP (LASV NP-C) in the process of degrading a 5' triphosphate double-stranded (ds) RNA substrate, a typical pathogen-associated molecular pattern molecule, to induce type I IFN production. Additionally, we provide for the first time a high-resolution crystal structure of an active exoribonuclease domain of Tacaribe arenavirus (TCRV) NP. Coupled with the in vitro enzymatic and cell-based interferon suppression assays, these structural analyses strongly support a unified model of an exoribonuclease-dependent IFN suppression mechanism shared by all known arenaviruses. New knowledge learned from these studies should aid the development of therapeutics against pathogenic arenaviruses that can infect hundreds of thousands of individuals and kill thousands annually.

Articles - 4gv6 mentioned but not cited (2)

  1. Structures of arenaviral nucleoproteins with triphosphate dsRNA reveal a unique mechanism of immune suppression. Jiang X, Huang Q, Wang W, Dong H, Ly H, Liang Y, Dong C. J Biol Chem 288 16949-16959 (2013)
  2. Inhibition of Arenaviridae nucleoprotein exonuclease by bisphosphonate. Nguyen THV, Yekwa E, Selisko B, Canard B, Alvarez K, Ferron F. IUCrJ 9 468-479 (2022)


Reviews citing this publication (26)

  1. Pattern Recognition and Signaling Mechanisms of RIG-I and MDA5. Reikine S, Nguyen JB, Modis Y. Front Immunol 5 342 (2014)
  2. Immunobiology of Ebola and Lassa virus infections. Prescott JB, Marzi A, Safronetz D, Robertson SJ, Feldmann H, Best SM. Nat Rev Immunol 17 195-207 (2017)
  3. To sense or not to sense viral RNA--essentials of coronavirus innate immune evasion. Kindler E, Thiel V. Curr Opin Microbiol 20 69-75 (2014)
  4. Strategies of highly pathogenic RNA viruses to block dsRNA detection by RIG-I-like receptors: hide, mask, hit. Zinzula L, Tramontano E. Antiviral Res 100 615-635 (2013)
  5. Transcription and replication mechanisms of Bunyaviridae and Arenaviridae L proteins. Ferron F, Weber F, de la Torre JC, Reguera J. Virus Res 234 118-134 (2017)
  6. Comparative analysis of disease pathogenesis and molecular mechanisms of New World and Old World arenavirus infections. McLay L, Liang Y, Ly H. J Gen Virol 95 1-15 (2014)
  7. Hemorrhagic Fever-Causing Arenaviruses: Lethal Pathogens and Potent Immune Suppressors. Brisse ME, Ly H. Front Immunol 10 372 (2019)
  8. Structural perspective on the formation of ribonucleoprotein complex in negative-sense single-stranded RNA viruses. Zhou H, Sun Y, Guo Y, Lou Z. Trends Microbiol 21 475-484 (2013)
  9. Cytosolic Innate Immune Sensing and Signaling upon Infection. Radoshevich L, Dussurget O. Front Microbiol 7 313 (2016)
  10. Human hemorrhagic Fever causing arenaviruses: molecular mechanisms contributing to virus virulence and disease pathogenesis. Shao J, Liang Y, Ly H. Pathogens 4 283-306 (2015)
  11. Sensing microbial RNA in the cytosol. Vabret N, Blander JM. Front Immunol 4 468 (2013)
  12. Vaccine platforms for the prevention of Lassa fever. Purushotham J, Lambe T, Gilbert SC. Immunol Lett 215 1-11 (2019)
  13. Current research for a vaccine against Lassa hemorrhagic fever virus. Warner BM, Safronetz D, Stein DR. Drug Des Devel Ther 12 2519-2527 (2018)
  14. Segmented negative strand RNA virus nucleoprotein structure. Reguera J, Cusack S, Kolakofsky D. Curr Opin Virol 5 7-15 (2014)
  15. Vaccine platforms to control Lassa fever. Lukashevich IS, Pushko P. Expert Rev Vaccines 15 1135-1150 (2016)
  16. Differential Immune Responses to Hemorrhagic Fever-Causing Arenaviruses. Mantlo E, Paessler S, Huang C. Vaccines (Basel) 7 E138 (2019)
  17. Functional and structural insights into the piRNA factor Maelstrom. Sato K, Siomi MC. FEBS Lett 589 1688-1693 (2015)
  18. The mechanism of genome replication and transcription in bunyaviruses. Malet H, Williams HM, Cusack S, Rosenthal M. PLoS Pathog 19 e1011060 (2023)
  19. What can pestiviral endonucleases teach us about innate immunotolerance? Lussi C, Schweizer M. Cytokine Growth Factor Rev 29 53-62 (2016)
  20. Differential Immune Responses to New World and Old World Mammalian Arenaviruses. Ly H. Int J Mol Sci 18 E1040 (2017)
  21. Brothers in Arms: Structure, Assembly and Function of Arenaviridae Nucleoprotein. Papageorgiou N, Spiliopoulou M, Nguyen TV, Vaitsopoulou A, Laban EY, Alvarez K, Margiolaki I, Canard B, Ferron F. Viruses 12 E772 (2020)
  22. Distinct Molecular Mechanisms of Host Immune Response Modulation by Arenavirus NP and Z Proteins. Stott RJ, Strecker T, Foster TL. Viruses 12 E784 (2020)
  23. Host Cell Restriction Factors of Bunyaviruses and Viral Countermeasures. Lerolle S, Freitas N, Cosset FL, Legros V. Viruses 13 784 (2021)
  24. The Virus-Host Interplay in Junín Mammarenavirus Infection. Gallo GL, López N, Loureiro ME. Viruses 14 1134 (2022)
  25. The COVID-19 Impact on the Trends in Yellow Fever and Lassa Fever Infections in Nigeria. Opara NU, Nwagbara UI, Hlongwana KW. Infect Dis Rep 14 932-941 (2022)
  26. Protection of eIF2B from inhibitory phosphorylated eIF2: A viral strategy to maintain mRNA translation during the PKR-triggered integrated stress response. Ito T, Wuerth JD, Weber F. J Biol Chem 299 105287 (2023)

Articles citing this publication (35)

  1. Remdesivir and SARS-CoV-2: Structural requirements at both nsp12 RdRp and nsp14 Exonuclease active-sites. Shannon A, Le NT, Selisko B, Eydoux C, Alvarez K, Guillemot JC, Decroly E, Peersen O, Ferron F, Canard B. Antiviral Res 178 104793 (2020)
  2. Mutagenesis of Coronavirus nsp14 Reveals Its Potential Role in Modulation of the Innate Immune Response. Becares M, Pascual-Iglesias A, Nogales A, Sola I, Enjuanes L, Zuñiga S. J Virol 90 5399-5414 (2016)
  3. The Z proteins of pathogenic but not nonpathogenic arenaviruses inhibit RIG-I-like receptor-dependent interferon production. Xing J, Ly H, Liang Y. J Virol 89 2944-2955 (2015)
  4. Structure and dynamics of SARS-CoV-2 proofreading exoribonuclease ExoN. Moeller NH, Shi K, Demir Ö, Belica C, Banerjee S, Yin L, Durfee C, Amaro RE, Aihara H. Proc Natl Acad Sci U S A 119 e2106379119 (2022)
  5. Structural basis of mismatch recognition by a SARS-CoV-2 proofreading enzyme. Liu C, Shi W, Becker ST, Schatz DG, Liu B, Yang Y. Science 373 1142-1146 (2021)
  6. Exonuclease domain of the Lassa virus nucleoprotein is critical to avoid RIG-I signaling and to inhibit the innate immune response. Reynard S, Russier M, Fizet A, Carnec X, Baize S. J Virol 88 13923-13927 (2014)
  7. In vitro and in vivo characterizations of pichinde viral nucleoprotein exoribonuclease functions. Huang Q, Shao J, Lan S, Zhou Y, Xing J, Dong C, Liang Y, Ly H. J Virol 89 6595-6607 (2015)
  8. Crystal structure of Schmallenberg orthobunyavirus nucleoprotein-RNA complex reveals a novel RNA sequestration mechanism. Dong H, Li P, Böttcher B, Elliott RM, Dong C. RNA 19 1129-1136 (2013)
  9. A Novel Live Pichinde Virus-Based Vaccine Vector Induces Enhanced Humoral and Cellular Immunity after a Booster Dose. Dhanwani R, Zhou Y, Huang Q, Verma V, Dileepan M, Ly H, Liang Y. J Virol 90 2551-2560 (2015)
  10. Interactome analysis of the lymphocytic choriomeningitis virus nucleoprotein in infected cells reveals ATPase Na+/K+ transporting subunit Alpha 1 and prohibitin as host-cell factors involved in the life cycle of mammarenaviruses. Iwasaki M, Minder P, Caì Y, Kuhn JH, Yates JR, Torbett BE, de la Torre JC. PLoS Pathog 14 e1006892 (2018)
  11. High-resolution structure of the N-terminal endonuclease domain of the Lassa virus L polymerase in complex with magnesium ions. Wallat GD, Huang Q, Wang W, Dong H, Ly H, Liang Y, Dong C. PLoS One 9 e87577 (2014)
  12. Differential Inhibition of Macrophage Activation by Lymphocytic Choriomeningitis Virus and Pichinde Virus Is Mediated by the Z Protein N-Terminal Domain. Xing J, Chai Z, Ly H, Liang Y. J Virol 89 12513-12517 (2015)
  13. Preparation by alkaline treatment and detailed characterisation of empty hepatitis B virus core particles for vaccine and gene therapy applications. Strods A, Ose V, Bogans J, Cielens I, Kalnins G, Radovica I, Kazaks A, Pumpens P, Renhofa R. Sci Rep 5 11639 (2015)
  14. The exonuclease domain of Lassa virus nucleoprotein is involved in antigen-presenting-cell-mediated NK cell responses. Russier M, Reynard S, Carnec X, Baize S. J Virol 88 13811-13820 (2014)
  15. Crystal structure of Junin virus nucleoprotein. Zhang Y, Li L, Liu X, Dong S, Wang W, Huo T, Guo Y, Rao Z, Yang C. J Gen Virol 94 2175-2183 (2013)
  16. Lymphocytic Choriomeningitis Virus Differentially Affects the Virus-Induced Type I Interferon Response and Mitochondrial Apoptosis Mediated by RIG-I/MAVS. Pythoud C, Rothenberger S, Martínez-Sobrido L, de la Torre JC, Kunz S. J Virol 89 6240-6250 (2015)
  17. Arenaviral Nucleoproteins Suppress PACT-Induced Augmentation of RIG-I Function To Inhibit Type I Interferon Production. Shao J, Huang Q, Liu X, Di D, Liang Y, Ly H. J Virol 92 e00482-18 (2018)
  18. Lassa Virus, but Not Highly Pathogenic New World Arenaviruses, Restricts Immunostimulatory Double-Stranded RNA Accumulation during Infection. Mateer EJ, Maruyama J, Card GE, Paessler S, Huang C. J Virol 94 e02006-19 (2020)
  19. Comparison of the Innate Immune Responses to Pathogenic and Nonpathogenic Clade B New World Arenaviruses. Moreno H, Möller R, Fedeli C, Gerold G, Kunz S. J Virol 93 e00148-19 (2019)
  20. Structure of the LCMV nucleoprotein provides a template for understanding arenavirus replication and immunosuppression. West BR, Hastie KM, Saphire EO. Acta Crystallogr D Biol Crystallogr 70 1764-1769 (2014)
  21. The S Genome Segment Is Sufficient to Maintain Pathogenicity in Intra-Clade Lassa Virus Reassortants in a Guinea Pig Model. Welch SR, Scholte FEM, Albariño CG, Kainulainen MH, Coleman-McCray JD, Guerrero LW, Chakrabarti AK, Klena JD, Nichol ST, Spengler JR, Spiropoulou CF. Front Cell Infect Microbiol 8 240 (2018)
  22. Activation of the RLR/MAVS Signaling Pathway by the L Protein of Mopeia Virus. Zhang LK, Xin QL, Zhu SL, Wan WW, Wang W, Xiao G. J Virol 90 10259-10270 (2016)
  23. Differential contributions of tacaribe arenavirus nucleoprotein N-terminal and C-terminal residues to nucleocapsid functional activity. D'Antuono A, Loureiro ME, Foscaldi S, Marino-Buslje C, Lopez N. J Virol 88 6492-6505 (2014)
  24. Activity inhibition and crystal polymorphism induced by active-site metal swapping. Yekwa E, Khourieh J, Canard B, Papageorgiou N, Ferron F. Acta Crystallogr D Struct Biol 73 641-649 (2017)
  25. Crystal structures of Lymphocytic choriomeningitis virus endonuclease domain complexed with diketo-acid ligands. Saez-Ayala M, Yekwa EL, Carcelli M, Canard B, Alvarez K, Ferron F. IUCrJ 5 223-235 (2018)
  26. The Antiviral Effect of the Chemical Compounds Targeting DED/EDh Motifs of the Viral Proteins on Lymphocytic Choriomeningitis Virus and SARS-CoV-2. Ngwe Tun MM, Morita K, Ishikawa T, Urata S. Viruses 13 1220 (2021)
  27. Effect of Strain Variations on Lassa Virus Z Protein-Mediated Human RIG-I Inhibition. Huang Q, Liu X, Brisse M, Ly H, Liang Y. Viruses 12 E907 (2020)
  28. Influence of RNA Binding on the Structure and Dynamics of the Lassa Virus Nucleoprotein. Pattis JG, May ER. Biophys J 110 1246-1254 (2016)
  29. Isolation of Reconstructed Functional Ribonucleoprotein Complexes of Machupo Virus. Pyle JD, Whelan SPJ. J Virol 95 e0105421 (2021)
  30. The Protein Kinase Receptor Modulates the Innate Immune Response against Tacaribe Virus. Moreno H, Kunz S. Viruses 13 1313 (2021)
  31. A dsRNA-binding mutant reveals only a minor role of exonuclease activity in interferon antagonism by the arenavirus nucleoprotein. Bohn P, Waßmann I, Wendt L, Leske A, Hoenen T, Tews BA, Groseth A. PLoS Pathog 19 e1011049 (2023)
  32. Evaluating the Biological Role of Lassa Viral Z Protein-Mediated RIG-I Inhibition Using a Replication-Competent Trisegmented Pichinde Virus System in an Inducible RIG-IN Expression Cell Line. Di D, Huang Q, Ly H, Liang Y. J Virol 96 e0075422 (2022)
  33. Nuclease Activity of the Junín Virus Nucleoprotein C-Terminal Domain. Sierra AA, Loureiro ME, Esperante S, Borkosky SS, Gallo GL, de Prat Gay G, Lopez N. Viruses 15 1818 (2023)
  34. Structure of the Spring Viraemia of Carp Virus Ribonucleoprotein Complex Reveals Its Assembly Mechanism and Application in Antiviral Drug Screening. Wang ZX, Liu B, Yang T, Yu D, Zhang C, Zheng L, Xie J, Liu B, Liu M, Peng H, Lai L, Ouyang Q, Ouyang S, Zhang YA. J Virol 97 e0182922 (2023)
  35. editorial Virulence profile: Hinh Ly. Ly H. Virulence 7 895-897 (2016)


Quick links