HIV-1 blocks the signaling adaptor MAVS to evade antiviral host defense after sensing of abortive HIV-1 RNA by the host helicase DDX3

Nature Immunology

Volumn 18, Issue 2, 2017, Pages 225-235

  Gringhuis, Sonja I ^a   Hertoghs, Nina ^a   Kaptein, Tanja M ^a   Zijlstra Willems, Esther M ^a   Sarrami Fooroshani, Ramin ^a   Sprokholt, Joris K ^a   Van Teijlingen, Nienke H ^a   Kootstra, Neeltje A ^a   Booiman, Thijs ^a   Van Dort, Karel A ^a   Ribeiro, Carla M S ^a   Drewniak, Agata ^a   Geijtenbeek, Teunis B H ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; BETA INTERFERON; CD209 ANTIGEN; I KAPPA B KINASE EPSILON; INTERFERON REGULATORY FACTOR 3; ISG15 PROTEIN; MACROPHAGE ACTIVATING FACTOR; MAVS PROTEIN; MESSENGER RNA; MX2 PROTEIN; PEPTIDES AND PROTEINS; POLO LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE; RAF PROTEIN; RNA HELICASE; RNA HELICASE DDX3; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TBK1 PROTEIN; TRIPARTITE MOTIF PROTEIN; TRIPARTITE MOTIF PROTEIN 22; TRIPARTITE MOTIF PROTEIN 5; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UNCLASSIFIED DRUG; VIRUS RNA; CELL EXTRACT; DDX3X PROTEIN, HUMAN; DEAD BOX PROTEIN; PATTERN RECOGNITION RECEPTOR; VISA PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ARTICLE; CELL ACTIVATION; CELL MATURATION; COHORT ANALYSIS; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; HOST RESISTANCE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN TISSUE; IMMUNE ACTIVATION; IMMUNE EVASION; IMMUNITY; IMMUNOSURVEILLANCE; INNATE IMMUNITY; MALE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; SENSOR; SIGNAL TRANSDUCTION; VIRUS LOAD; VIRUS REPLICATION; BLOOD; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; MACROPHAGE; METABOLISM; PHYSIOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; VIROLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL EXTRACTS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; COHORT STUDIES; DEAD-BOX RNA HELICASES; DENDRITIC CELLS; GENE EXPRESSION REGULATION, VIRAL; HEK293 CELLS; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; IMMUNITY; INTERFERON-BETA; MACROPHAGES; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, PATTERN RECOGNITION; RNA, VIRAL; SIGNAL TRANSDUCTION; VIRAL LOAD;

EID: 85007090147     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3647     Document Type: Article

References (43)

1. Steinman, R.M. Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 30, 1-22 (2012).
2. Miller, E. & Bhardwaj, N. Dendritic cell dysregulation during HIV-1 infection. Immunol. Rev. 254, 170-189 (2013).
3. Goujon, C. et al. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 502, 559-562 (2013).
4. Kane, M. et al. MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 502, 563-566 (2013).
5. Yan, N. & Chen, Z.J. Intrinsic antiviral immunity. Nat. Immunol. 13, 214-222 (2012).
6. Simmons, D.P. et al. Type I IFN drives a distinctive dendritic cell maturation phenotype that allows continued class II MHC synthesis and antigen processing. J. Immunol. 188, 3116-3126 (2012).
7. González-Navajas, J.M., Lee, J., David, M. & Raz, E. Immunomodulatory functions of type I interferons. Nat. Rev. Immunol. 12, 125-135 (2012).
8. Sandler, N.G. et al. Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression. Nature 511, 601-605 (2014).
9. Gringhuis, S.I. et al. C-Type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1-kinase-dependent acetylation of transcription factor NF-κB. Immunity 26, 605-616 (2007).
10. Gringhuis, S.I., den Dunnen, J., Litjens, M., van der Vlist, M. & Geijtenbeek, T.B.H. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1, and Helicobacter pylori. Nat. Immunol. 10, 1081-1088 (2009).
11. Solis, M. et al. RIG-I-mediated antiviral signaling is inhibited in HIV-1 infection by a protease-mediated sequestration of RIG-I. J. Virol. 85, 1224-1236 (2011).
12. Gringhuis, S.I. et al. HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat. Immunol. 11, 419-426 (2010).
13. Kao, S.Y., Calman, A.F., Luciw, P.A. & Peterlin, B.M. Anti-Termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature 330, 489-493 (1987).
14. Yedavalli, V.S., Neuveut, C., Chi, Y.H., Kleiman, L. & Jeang, K.T. Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell 119, 381-392 (2004).
15. Naji, S. et al. Host cell interactome of HIV-1 Rev includes RNA helicases involved in multiple facets of virus production. Mol. Cell. Proteomics 11, 015313 (2012).
16. Soto-Rifo, R. et al. DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs. EMBO J. 31, 3745-3756 (2012).
17. Soto-Rifo, R., Rubilar, P.S. & Ohlmann, T. The DEAD-box helicase DDX3 substitutes for the cap-binding protein eIF4E to promote compartmentalized translation initiation of the HIV-1 genomic RNA. Nucleic Acids Res. 41, 6286-6299 (2013).
18. Goubau, D., Deddouche, S. & Reis e Sousa, C. Cytosolic sensing of viruses. Immunity 38, 855-869 (2013).
19. Gao, D. et al. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341, 903-906 (2013).
20. Yan, N., Regalado-Magdos, A.D., Stiggelbout, B., Lee-Kirsch, M.A. & Lieberman, J. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat. Immunol. 11, 1005-1013 (2010).
21. Lahouassa, H. et al. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat. Immunol. 13, 223-228 (2012).
22. Hertoghs, N. et al. SAMHD1 degradation enhances active suppression of dendritic cell maturation by HIV-1. J. Immunol. 194, 4431-4437 (2015).
23. Hou, F. et al. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146, 448-461 (2011).
24. Clark, K., Plater, L., Peggie, M. & Cohen, P. Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IκB kinase epsilon: A distinct upstream kinase mediates Ser172 phosphorylation and activation. J. Biol. Chem. 284, 14136-14146 (2009).
25. Saha, S.K. et al. Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif. EMBO J. 25, 3257-3263 (2006).
26. Vitour, D. et al. Polo-like kinase 1 (PLK1) regulates interferon (IFN) induction by MAVS. J. Biol. Chem. 284, 21797-21809 (2009).
27. Elia, A.E. et al. The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 115, 83-95 (2003).
28. Ji, J.H. et al. Purification and proteomic identification of putative upstream regulators of polo-like kinase 1 from mitotic cell extracts. FEBS Lett. 584, 4299-4305 (2010).
29. Rabizadeh, S. et al. The scaffold protein CNK1 interacts with the tumor suppressor RASSF1A and augments RASSF1A-induced cell death. J. Biol. Chem. 279, 29247-29254 (2004).
30. Praskova, M., Khoklatchev, A., Ortiz-Vega, S. & Avruch, J. Regulation of the MST1 kinase by autophosphorylation, by the growth inhibitory proteins RASSF1 and NORE1, and by Ras. Biochem. J. 381, 453-462 (2004).
31. de Roda Husman, A.M. et al. Association between CCR5 genotype and the clinical course of HIV-1 infection. Ann. Intern. Med. 127, 882-890 (1997).
32. Pothlichet, J. et al. A loss-of-function variant of the antiviral molecule MAVS is associated with a subset of systemic lupus patients. EMBO Mol. Med. 3, 142-152 (2011).
33. Pertel, T., Reinhard, C. & Luban, J. Vpx rescues HIV-1 transduction of dendritic cells from the antiviral state established by type 1 interferon. Retrovirology 8, 49 (2011).
34. Manel, N. et al. A cryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 467, 214-217 (2010).
35. Adams, M. et al. Cellular latency in human-immunodeficiency-virus-infected individuals with high CD4 levels can be detected by the presence of promoter-proximal transcripts. Proc. Natl. Acad. Sci. USA 91, 3862-3866 (1994).
36. Luban, J. Innate immune sensing of HIV-1 by dendritic cells. Cell Host Microbe 12, 408-418 (2012).
37. Archambault, V. & Glover, D.M. Polo-like kinases: conservation and divergence in their functions and regulation. Nat. Rev. Mol. Cell Biol. 10, 265-275 (2009).
38. Li, S., Zhang, Y. & Xu, W. Developments of polo-like kinase 1 (Plk1) inhibitors as anticancer agents. Mini Rev. Med. Chem. 13, 2014-2025 (2013).
39. Hunt, P.W. et al. Gut epithelial barrier dysfunction and innate immune activation predict mortality in treated HIV infection. J. Infect. Dis. 210, 1228-1238 (2014).
40. Roberts, L. et al. Genital tract inflammation during early HIV-1 infection predicts higher plasma viral load set point in women. J. Infect. Dis. 205, 194-203 (2012).
41. Fernandez, S. et al. CD4+ T cell deficiency in HIV patients responding to antiretroviral therapy is associated with increased expression of interferon-stimulated genes in CD4+ T cells. J. Infect. Dis. 204, 1927-1935 (2011).
42. Fraietta, J.A. et al. Type I interferon upregulates Bak and contributes to T cell loss during human immunodeficiency virus (HIV) infection. PLoS Pathog. 9, e1003658 (2013).
43. Wheeler, L.A. et al. TREX1 knockdown induces an interferon response to HIV that delays viral infection in humanized mice. Cell Rep. 15, 1715-1727 (2016).