Genomic HIV RNA induces innate immune responses through RIG-I-dependent sensing of secondary-structured RNA

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Berg, Randi K ^a   Melchjorsen, Jesper ^a   Rintahaka, Johanna ^b   Diget, Elisabeth ^a   Søby, Stine ^a   Horan, Kristy A ^c   Gorelick, Robert J ^d   Matikainen, Sampsa ^b   Larsen, Carsten S ^a   Ostergaard, Lars ^a   Paludan, Søren R ^c   Mogensen, Trine H ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b FINNISH INSTITUTE OF OCCUPATIONAL HEALTH   (Finland)

^c AARHUS UNIVERSITY   (Denmark)

^d SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; GENOMIC RNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN MAVS; RETINOIC ACID INDUCIBLE PROTEIN I; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS RNA; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN; INTERFERON REGULATORY FACTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; OLIGORIBONUCLEOTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VIRUS PROTEIN; VISA PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE; GENE ACTIVATION; GENE LOCATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOSTIMULATION; INNATE IMMUNITY; INTERFERON GENE; INTERFERON TYPE 1 GENE; MACROPHAGE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PEROXISOME; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA ANALYSIS; RNA GENE; RNA STRUCTURE; SIGNAL TRANSDUCTION; VIRUS GENOME; ANIMAL; C57BL MOUSE; CHEMISTRY; CONFORMATION; CYTOLOGY; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; PROTEIN TRANSPORT; TUMOR CELL LINE; VIROLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL LINE, TUMOR; DEAD-BOX RNA HELICASES; GENOME, VIRAL; HIV-1; HUMANS; IMMUNITY, INNATE; INTERFERON REGULATORY FACTORS; LEUKOCYTES, MONONUCLEAR; MICE; MICE, INBRED C57BL; NF-KAPPA B; NUCLEIC ACID CONFORMATION; OLIGORIBONUCLEOTIDES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEROXISOMES; PROTEIN TRANSPORT; RNA, VIRAL; SIGNAL TRANSDUCTION; VIRAL PROTEINS;

EID: 84855301478     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029291     Document Type: Article

References (55)

1. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, et al. (1983) Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220: 868-871.
2. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, et al. (2004) CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200: 749-759.
3. Guadalupe M, Reay E, Sankaran S, Prindiville T, Flamm J, et al. (2003) Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J Virol 77: 11708-11717.
4. Ho DD, Neumann AU, Perelson AS, Chen W, Leonard JM, et al. (1995) Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373: 123-126.
5. Douek DC, Roederer M, Koup RA, (2009) Emerging concepts in the immunopathogenesis of AIDS. Annu Rev Med 60: 471-484.
6. Lempicki RA, Kovacs JA, Baseler MW, Adelsberger JW, Dewar RL, et al. (2000) Impact of HIV-1 infection and highly active antiretroviral therapy on the kinetics of CD4+ and CD8+ T cell turnover in HIV-infected patients. Proc Natl Acad Sci U S A 97: 13778-13783.
7. Tilling R, Kinloch S, Goh LE, Cooper D, Perrin L, et al. (2002) Parallel decline of CD8+/CD38++ T cells and viraemia in response to quadruple highly active antiretroviral therapy in primary HIV infection. AIDS 16: 589-596.
8. Medzhitov R, Littman D, (2008) HIV immunology needs a new direction. Nature 455: 591.
9. Iwasaki A, Medzhitov R, (2010) Regulation of adaptive immunity by the innate immune system. Science 327: 291-295.
10. Janeway CA Jr, (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54 Pt 1: 1-13.
11. Kawai T, Akira S, (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373-384.
12. Mogensen TH, (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22: 240-73 Table.
13. Mogensen TH, Melchjorsen J, Larsen CS, Paludan SR, (2010) Innate immune recognition and activation during HIV infection. Retrovirology 7: 54.
14. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA, (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
15. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa, (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
16. Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, et al. (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303: 1526-1529.
17. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, et al. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
18. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5: 730-737.
19. Schlee M, Roth A, Hornung V, Hagmann CA, Wimmenauer V, et al. (2009) Recognition of 5′ triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 31: 25-34.
20. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, et al. (2006) 5′-Triphosphate RNA is the ligand for RIG-I. Science 314: 994-997.
21. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, et al. (2008) Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 205: 1601-1610.
22. Pichlmair A, Schulz O, Tan CP, Rehwinkel J, Kato H, et al. (2009) Activation of MDA5 requires higher-order RNA structures generated during virus infection. J Virol 83: 10761-10769.
23. Takaoka A, Wang Z, Choi MK, Yanai H, Negishi H, et al. (2007) DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448: 501-505.
24. Ablasser A, Bauernfeind F, Hartmann G, Latz E, Fitzgerald KA, et al. (2009) RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat Immunol 10: 1065-1072.
25. Chiu YH, Macmillan JB, Chen ZJ, (2009) RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138: 576-591.
26. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, et al. (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458: 514-518.
27. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, et al. (2010) IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11: 997-1004.
28. Greene WC, Peterlin BM, (2002) Charting HIV's remarkable voyage through the cell: Basic science as a passport to future therapy. Nat Med 8: 673-680.
29. Meier A, Alter G, Frahm N, Sidhu H, Li B, et al. (2007) MyD88-dependent immune activation mediated by human immunodeficiency virus type 1-encoded Toll-like receptor ligands. J Virol 81: 8180-8191.
30. Beignon AS, McKenna K, Skoberne M, Manches O, DaSilva I, et al. (2005) Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest 115: 3265-3275.
31. Baenziger S, Heikenwalder M, Johansen P, Schlaepfer E, Hofer U, et al. (2009) Triggering TLR7 in mice induces immune activation and lymphoid system disruption, resembling HIV-mediated pathology. Blood 113: 377-388.
32. Lepelley A, Louis S, Sourisseau M, Law HK, Pothlichet J, et al. (2011) Innate Sensing of HIV-Infected Cells. PLoS Pathog 7: e1001284.
33. Brown JN, Kohler JJ, Coberley CR, Sleasman JW, Goodenow MM, (2008) HIV-1 activates macrophages independent of Toll-like receptors. PLoS ONE 3: e3664.
34. Solis M, Nakhaei P, Jalalirad M, Lacoste J, Douville R, et al. (2011) RIG-I-Mediated Antiviral Signaling Is Inhibited in HIV-1 Infection by a Protease-Mediated Sequestration of RIG-I. J Virol 85: 1224-1236.
35. Stetson DB, Ko JS, Heidmann T, Medzhitov R, (2008) Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134: 587-598.
36. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J, (2010) The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat Immunol 11: 1005-1013.
37. Manel N, Hogstad B, Wang Y, Levy DE, Unutmaz D, et al. (2010) A cryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 467: 214-217.
38. Watts JM, Dang KK, Gorelick RJ, Leonard CW, Bess JW Jr, et al. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460: 711-716.
39. Seth RB, Sun L, Ea CK, Chen ZJ, (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682.
40. Ishikawa H, Barber GN, (2008) STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455: 674-678.
41. Dixit E, Boulant S, Zhang Y, Lee AS, Odendall C, et al. (2010) Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141: 668-681.
42. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR, (2006) Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 80: 5059-5064.
43. Kikuchi M, Zhu C, Senoo T, Obara Y, Joyce NC, (2006) p27kip1 siRNA induces proliferation in corneal endothelial cells from young but not older donors. Invest Ophthalmol Vis Sci 47: 4803-4809.
44. Blight KJ, Kolykhalov AA, Rice CM, (2000) Efficient initiation of HCV RNA replication in cell culture. Science 290: 1972-1974.
45. Chang JJ, Altfeld M, (2010) Innate immune activation in primary HIV-1 infection. J Infect Dis 202 (Suppl 2): S297-S301.
46. Zhong B, Yang Y, Li S, Wang YY, Li Y, et al. (2008) The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29: 538-550.
47. Breckpot K, Escors D, Arce F, Lopes L, Karwacz K, et al. (2010) HIV-1 lentiviral vector immunogenicity is mediated by Toll-like receptor 3 (TLR3) and TLR7. J Virol 84: 5627-5636.
48. Bochud PY, Hersberger M, Taffe P, Bochud M, Stein CM, et al. (2007) Polymorphisms in Toll-like receptor 9 influence the clinical course of HIV-1 infection. AIDS 21: 441-446.
49. Lee HK, Lund JM, Ramanathan B, Mizushima N, Iwasaki A, (2007) Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315: 1398-1401.
50. Doehle BP, Hladik F, McNevin JP, McElrath MJ, Gale M Jr, (2009) Human immunodeficiency virus type 1 mediates global disruption of innate antiviral signaling and immune defenses within infected cells. J Virol 83: 10395-10405.
51. Murray SM, Down CM, Boulware DR, Stauffer WM, Cavert WP, et al. (2010) Reduction of immune activation with chloroquine therapy during chronic HIV infection. J Virol 84: 12082-12086.
52. Melchjorsen J, Siren J, Julkunen I, Paludan SR, Matikainen S, (2006) Induction of cytokine expression by herpes simplex virus in human monocyte-derived macrophages and dendritic cells is dependent on virus replication and is counteracted by ICP27 targeting NF-kappaB and IRF-3. J Gen Virol 87: 1099-1108.
53. Ott DE, Coren LV, Johnson DG, Sowder RC, Arthur LO, et al. (1995) Analysis and localization of cyclophilin A found in the virions of human immunodeficiency virus type 1 MN strain. AIDS Res Hum Retroviruses 11: 1003-1006.
54. Melchjorsen J, Rintahaka J, Soby S, Horan KA, Poltajainen A, et al. (2010) Early innate recognition of herpes simplex virus in human primary macrophages is mediated via the MDA5/MAVS-dependent and MDA5/MAVS/RNA polymerase III-independent pathways. J Virol 84: 11350-11358.
55. Rintahaka J, Wiik D, Kovanen PE, Alenius H, Matikainen S, (2008) Cytosolic antiviral RNA recognition pathway activates caspases 1 and 3. J Immunol 180: 1749-1757.