Innate sensing of HIV-infected cells

PLoS Pathogens

Volumn 7, Issue 2, 2011, Pages

  Lepelley, Alice ^a   Louis, Stéphanie ^a   Sourisseau, Marion ^a   Law, Helen K W ^b   Pothlichet, Julien ^b   Schilte, Clémentine ^b   Chaperot, Laurence ^c   Plumas, Joël ^c   Randall, Richard E ^d   Si Tahar, Mustapha ^b   Mammano, Fabrizio ^a   Albert, Matthew L ^b   Schwartz, Olivier ^a  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

^c UNIV GRENOBLE ALPES   (France)

^d UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRASE; INTERFERON; INTERFERON REGULATORY FACTOR 3; NUCLEOCAPSID PROTEIN; RNA DIRECTED DNA POLYMERASE; TOLL LIKE RECEPTOR 7; ALPHA INTERFERON; GLYCOPROTEIN; IRF3 PROTEIN, HUMAN; MESSENGER RNA; TLR7 PROTEIN, HUMAN;

ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL DIVISION; CELL TYPE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOPLASM; DONOR; ENDOSOME; GENE MUTATION; GENE SILENCING; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INNATE IMMUNITY; INNATE SENSING; NONHUMAN; PLASMACYTOID DENDRITIC CELL; VIRION; VIRUS ENVELOPE; VIRUS NUCLEOCAPSID; WILD TYPE; CELL CULTURE; DENDRITIC CELL; GENETICS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOLOGY; LYMPHOCYTE; METABOLISM; PATHOGENICITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY; VIRUS REPLICATION; WESTERN BLOTTING;

HUMAN IMMUNODEFICIENCY VIRUS 1; REPLICATION DEFECTIVE VIRUSES;

BLOTTING, WESTERN; CELLS, CULTURED; DENDRITIC CELLS; GLYCOPROTEINS; HEMATOPOIETIC STEM CELLS; HIV; HIV INFECTIONS; HIV SEROPOSITIVITY; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON-ALPHA; LYMPHOCYTES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TOLL-LIKE RECEPTOR 7; VIRION; VIRUS REPLICATION;

EID: 79952217825     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001284     Document Type: Article

References (80)

1. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF, (2010) The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol 10: 11-23.
2. Haase AT, (2010) Targeting early infection to prevent HIV-1 mucosal transmission. Nature 464: 217-223.
3. Brenchley JM, Silvestri G, Douek DC, (2010) Nonprogressive and progressive primate immunodeficiency lentivirus infections. Immunity 32: 737-742.
4. Sodora DL, Allan JS, Apetrei C, Brenchley JM, Douek DC, et al. (2009) Toward an AIDS vaccine: lessons from natural simian immunodeficiency virus infections of African nonhuman primate hosts. Nat Med 15: 861-865.
5. Li Q, Estes JD, Schlievert PM, Duan L, Brosnahan AJ, et al. (2009) Glycerol monolaurate prevents mucosal SIV transmission. Nature 458: 1034-1038.
6. Mandl JN, Barry AP, Vanderford TH, Kozyr N, Chavan R, et al. (2008) Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med 14: 1077-1087.
7. Jacquelin B, Mayau V, Targat B, Liovat AS, Kunkel D, et al. (2009) Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest 119: 3544-3555.
8. Bosinger SE, Li Q, Gordon SN, Klatt NR, Duan L, et al. (2009) Global genomic analysis reveals rapid control of a robust innate response in SIV-infected sooty mangabeys. J Clin Invest 119: 3556-3572.
9. Harris LD, Tabb B, Sodora DL, Paiardini M, Klatt NR, et al. (2010) Downregulation of Robust Acute Type I Interferon Responses Distinguishes Nonpathogenic Simian Immunodeficiency Virus (SIV) Infection of Natural Hosts from Pathogenic SIV Infection of Rhesus Macaques. J Virol 84: 7886-7891.
10. Gilliet M, Cao W, Liu YJ, (2008) Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol 8: 594-606.
11. McCartney SA, Colonna M, (2009) Viral sensors: diversity in pathogen recognition. Immunol Rev 227: 87-94.
12. Hosmalin A, Lebon P, (2006) Type I interferon production in HIV-infected patients. J Leukoc Biol 80: 984-993.
13. Fitzgerald-Bocarsly P, Jacobs ES, (2010) Plasmacytoid dendritic cells in HIV infection: striking a delicate balance. J Leukoc Biol 87: 609-20.
14. Fonteneau JF, Larsson M, Beignon AS, McKenna K, Dasilva I, et al. (2004) Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J Virol 78: 5223-5232.
15. 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.
16. Manches O, Munn D, Fallahi A, Lifson J, Chaperot L, et al. (2008) HIV-activated human plasmacytoid DCs induce Tregs through an indoleamine 2,3-dioxygenase-dependent mechanism. J Clin Invest 118: 3431-3439.
17. Audige A, Urosevic M, Schlaepfer E, Walker R, Powell D, et al. (2006) Anti-HIV state but not apoptosis depends on IFN signature in CD4+ T cells. J Immunol 177: 6227-6237.
18. Herbeuval JP, Hardy AW, Boasso A, Anderson SA, Dolan MJ, et al. (2005) Regulation of TNF-related apoptosis-inducing ligand on primary CD4+ T cells by HIV-1: role of type I IFN-producing plasmacytoid dendritic cells. Proc Natl Acad Sci U S A 102: 13974-13979.
19. Capobianchi MR, Ankel H, Ameglio F, Paganelli R, Pizzoli PM, et al. (1992) Recombinant glycoprotein 120 of human immunodeficiency virus is a potent interferon inducer. AIDS Res Hum Retroviruses 8: 575-579.
20. Martinelli E, Cicala C, Van Ryk D, Goode DJ, Macleod K, et al. (2007) HIV-1 gp120 inhibits TLR9-mediated activation and IFN-{alpha} secretion in plasmacytoid dendritic cells. Proc Natl Acad Sci U S A 104: 3396-3401.
21. Del Corno M, Gauzzi MC, Penna G, Belardelli F, Adorini L, et al. (2005) Human immunodeficiency virus type 1 gp120 and other activation stimuli are highly effective in triggering alpha interferon and CC chemokine production in circulating plasmacytoid but not myeloid dendritic cells. J Virol 79: 12597-12601.
22. Haupt S, Donhauser N, Chaipan C, Schuster P, Puffer B, et al. (2008) CD4 binding affinity determines human immunodeficiency virus type 1-induced alpha interferon production in plasmacytoid dendritic cells. J Virol 82: 8900-8905.
23. Garcia-Sastre A, Biron CA, (2006) Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312: 879-882.
24. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, et al. (2006) RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314: 997-1001.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. Doitsh G, Cavrois M, Lassen KG, Zepeda O, Yang Z, et al. (2010) Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 143: 789-801.
32. 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.
33. Ankel H, Capobianchi MR, Frezza F, Castilletti C, Dianzani F, (1996) Interferon induction by HIV-1-infected cells: a possible role of sulfatides or related glycolipids. Virology 221: 113-119.
34. Schmidt B, Ashlock BM, Foster H, Fujimura SH, Levy JA, (2005) HIV-infected cells are major inducers of plasmacytoid dendritic cell interferon production, maturation, and migration. Virology 343: 256-266.
35. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C, (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
36. Haller O, Stertz S, Kochs G, (2007) The Mx GTPase family of interferon-induced antiviral proteins. Microbes Infect 9: 1636-1643.
37. 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.
38. Vendrame D, Sourisseau M, Perrin V, Schwartz O, Mammano F, (2009) Partial inhibition of human immunodeficiency virus replication by type I interferons: impact of cell-to-cell viral transfer. J Virol 83: 10527-10537.
39. Turville SG, Cameron PU, Handley A, Lin G, Pohlmann S, et al. (2002) Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol 3: 975-983.
40. Nobile C, Petit C, Moris A, Skrabal K, Abastado JP, et al. (2005) Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J Virol 79: 5386-5399.
41. Vollmer J, Krieg AM, (2009) Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists. Adv Drug Deliv Rev 61: 195-204.
42. Maréchal V, Clavel F, Heard JM, Schwartz O, (1998) Cytosolic Gag p24 as an index of productive entry of Human Immunodeficiency Virus type 1. J Virol 72: 2208-2212.
43. Hardy AW, Graham DR, Shearer GM, Herbeuval JP, (2007) HIV turns plasmacytoid dendritic cells (pDC) into TRAIL-expressing killer pDC and down-regulates HIV coreceptors by Toll-like receptor 7-induced IFN-alpha. Proc Natl Acad Sci U S A 104: 17453-17458.
44. Thomas JA, Bosche WJ, Shatzer TL, Johnson DG, Gorelick RJ, (2008) Mutations in human immunodeficiency virus type 1 nucleocapsid protein zinc fingers cause premature reverse transcription. J Virol 82: 9318-9328.
45. Schwartz O, Alizon M, Heard JM, Danos O, (1994) Impairment of T cell receptor-dependent stimulation in CD4+ lymphocytes after contact with membrane-bound HIV-1 envelope glycoprotein. Virology 198: 360-365.
46. Chaperot L, Blum A, Manches O, Lui G, Angel J, et al. (2006) Virus or TLR agonists induce TRAIL-mediated cytotoxic activity of plasmacytoid dendritic cells. J Immunol 176: 248-255.
47. Di Domizio J, Blum A, Gallagher-Gambarelli M, Molens JP, Chaperot L, et al. (2009) TLR7 stimulation in human plasmacytoid dendritic cells leads to the induction of early IFN-inducible genes in the absence of type I IFN. Blood 114: 1794-1802.
48. Patterson S, Rae A, Hockey N, Gilmour J, Gotch F, (2001) Plasmacytoid dendritic cells are highly susceptible to human immunodeficiency virus type 1 infection and release infectious virus. J Virol 75: 6710-6713.
49. Sourisseau M, Sol-Foulon N, Porrot F, Blanchet F, Schwartz O, (2007) Inefficient human immunodeficiency virus replication in mobile lymphocytes. J Virol 81: 1000-1012.
50. Rudnicka D, Feldmann J, Porrot F, Wietgrefe S, Guadagnini S, et al. (2009) Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses. J Virol 83: 6234-6246.
51. Hornung V, Rothenfusser S, Britsch S, Krug A, Jahrsdorfer B, et al. (2002) Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 168: 4531-4537.
52. Melchjorsen J, Jensen SB, Malmgaard L, Rasmussen SB, Weber F, et al. (2005) Activation of innate defense against a paramyxovirus is mediated by RIG-I and TLR7 and TLR8 in a cell-type-specific manner. J Virol 79: 12944-12951.
53. 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.
54. Strahle L, Marq JB, Brini A, Hausmann S, Kolakofsky D, et al. (2007) Activation of the beta interferon promoter by unnatural Sendai virus infection requires RIG-I and is inhibited by viral C proteins. J Virol 81: 12227-12237.
55. Hiscott J, (2007) Triggering the innate antiviral response through IRF-3 activation. J Biol Chem 282: 15325-15329.
56. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, et al. (2005) IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6: 981-988.
57. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, et al. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167-1172.
58. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, et al. (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19: 727-740.
59. George TC, Fanning SL, Fitzgerald-Bocarsly P, Medeiros RB, Highfill S, et al. (2006) Quantitative measurement of nuclear translocation events using similarity analysis of multispectral cellular images obtained in flow. J Immunol Methods 311: 117-129.
60. Fanning SL, George TC, Feng D, Feldman SB, Megjugorac NJ, et al. (2006) Receptor cross-linking on human plasmacytoid dendritic cells leads to the regulation of IFN-alpha production. J Immunol 177: 5829-5839.
61. Riddell JR, Wang XY, Minderman H, Gollnick SO, (2010) Peroxiredoxin 1 stimulates secretion of proinflammatory cytokines by binding to TLR4. J Immunol 184: 1022-1030.
62. Sattentau Q, (2008) Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 6: 815-826.
63. Ruggiero E, Bona R, Muratori C, Federico M, (2008) Virological consequences of early events following cell-cell contact between human immunodeficiency virus type 1-infected and uninfected CD4+ cells. J Virol 82: 7773-7789.
64. Hubner W, McNerney GP, Chen P, Dale BM, Gordon RE, et al. (2009) Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323: 1743-1747.
65. Nobile C, Moris A, Porrot F, Sol-Foulon N, Schwartz O, (2003) Inhibition of Human Immunodeficiency Virus Type 1 Env-Mediated Fusion by DC-SIGN. J Virol 77: 5313-5323.
66. Herschke F, Plumet S, Duhen T, Azocar O, Druelle J, et al. (2007) Cell-cell fusion induced by measles virus amplifies the type I interferon response. J Virol 81: 12859-12871.
67. Vodicka MA, Goh WC, Wu LI, Rogel ME, Bartz SR, et al. (1997) Indicator cell lines for detection of primary strains of human and simian immunodeficiency viruses. Virology 233: 193-198.
68. Thomas JA, Ott DE, Gorelick RJ, (2007) Efficiency of human immunodeficiency virus type 1 postentry infection processes: evidence against disproportionate numbers of defective virions. J Virol 81: 4367-4370.
69. Schlee M, Hartmann E, Coch C, Wimmenauer V, Janke M, et al. (2009) Approaching the RNA ligand for RIG-I? Immunol Rev 227: 66-74.
70. Rehwinkel J, Reis e Sousa C, (2010) RIGorous detection: exposing virus through RNA sensing. Science 327: 284-286.
71. 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.
72. Stetson DB, Ko JS, Heidmann T, Medzhitov R, (2008) Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134: 587-598.
73. Moris A, Pajot A, Blanchet F, Guivel-Benhassine F, Salcedo M, et al. (2006) Dendritic cells and HIV-specific CD4+ T cells: HIV antigen presentation, T cell activation, viral transfer. Blood 108: 1643-1651.
74. Gorelick RJ, Gagliardi TD, Bosche WJ, Wiltrout TA, Coren LV, et al. (1999) Strict conservation of the retroviral nucleocapsid protein zinc finger is strongly influenced by its role in viral infection processes: characterization of HIV-1 particles containing mutant nucleocapsid zinc-coordinating sequences. Virology 256: 92-104.
75. Petit C, Schwartz O, Mammano F, (1999) Oligomerization within virions and subcellular localization of Human Immunodeficiency Virus type 1 integrase. J Virol 73: 5079-5088.
76. Sol-Foulon N, Sourisseau M, Porrot F, Thoulouze MI, Trouillet C, et al. (2007) ZAP-70 kinase regulates HIV cell-to-cell spread and virological synapse formation. Embo J 26: 516-526.
77. Hilton L, Moganeradj K, Zhang G, Chen YH, Randall RE, et al. (2006) The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. J Virol 80: 11723-11732.
78. Decalf J, Fernandes S, Longman R, Ahloulay M, Audat F, et al. (2007) Plasmacytoid dendritic cells initiate a complex chemokine and cytokine network and are a viable drug target in chronic HCV patients. J Exp Med 204: 2423-2437.
79. Uze G, Di Marco S, Mouchel-Vielh E, Monneron D, Bandu MT, et al. (1994) Domains of interaction between alpha interferon and its receptor components. J Mol Biol 243: 245-257.
80. Le Goffic R, Pothlichet J, Vitour D, Fujita T, Meurs E, et al. (2007) Cutting Edge: Influenza A virus activates TLR3-dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells. J Immunol 178: 3368-3372.