Hiv delays IFN-α production from human plasmacytoid dendritic cells and is associated with SYK phosphorylation

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Lo, Calvin C ^a   Schwartz, Jordan A ^a   Johnson, Dylan J ^a   Yu, Monica ^a   Aidarus, Nasra ^a   Mujib, Shariq ^a   Benko, Erika ^a,b   Hyrcza, Martin ^a   Kovacs, Colin ^a,b   Ostrowski, Mario A ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b MAPLE LEAF MEDICAL CLINIC   (Canada)

^c ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CD83 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; PROTEIN KINASE SYK; PROTEIN TYROSINE KINASE; SIGNAL PEPTIDE;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DISEASE ASSOCIATION; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFLUENZA; INNATE IMMUNITY; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PROTEIN PHOSPHORYLATION; SENDAI VIRUS; SIGNAL TRANSDUCTION; UPREGULATION; VIRUS INDUCTION; VIRUS REPLICATION; BIOSYNTHESIS; DENDRITIC CELL; IMMUNOLOGY; METABOLISM; ORTHOMYXOVIRUS; PHOSPHORYLATION; PHYSIOLOGY; SPECIES DIFFERENCE; TIME; VIROLOGY;

HUMAN HERPESVIRUS 2;

DENDRITIC CELLS; HIV; HUMANS; INTERFERON-ALPHA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ORTHOMYXOVIRIDAE; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; SPECIES SPECIFICITY; TIME FACTORS; VIRUS REPLICATION;

EID: 84861664983     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037052     Document Type: Article

References (57)

1. Samuel CE, (2001) Antiviral actions of interferons. Clin Microbiol Rev 14 778-809, table of contents.
2. Der SD, Zhou A, Williams BR, Silverman RH, (1998) Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci U S A 95: 15623-15628.
3. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD, (1998) How cells respond to interferons. Annu Rev Biochem 67: 227-264.
4. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, et al. (2005) Cell type-specific involvement of RIG-I in antiviral response. Immunity 23: 19-28.
5. 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.
6. Liu YJ, (2005) IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 23: 275-306.
7. Izaguirre A, Barnes BJ, Amrute S, Yeow WS, Megjugorac N, et al. (2003) Comparative analysis of IRF and IFN-αlpha expression in human plasmacytoid and monocyte-derived dendritic cells. J Leukoc Biol 74: 1125-1138.
8. Dai J, Megjugorac NJ, Amrute SB, Fitzgerald-Bocarsly P, (2004) Regulation of IFN regulatory factor-7 and IFN-αlpha production by enveloped virus and lipopolysaccharide in human plasmacytoid dendritic cells. J Immunol 173: 1535-1548.
9. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, et al. (2005) IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434: 772-777.
10. Osawa Y, Iho S, Takauji R, Takatsuka H, Yamamoto S, et al. (2006) Collaborative action of NF-kappaB and p38 MAPK is involved in CpG DNA-induced IFN-αlpha and chemokine production in human plasmacytoid dendritic cells. J Immunol 177: 4841-4852.
11. Sato M, Hata N, Asagiri M, Nakaya T, Taniguchi T, et al. (1998) Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS Lett 441: 106-110.
12. Kawai T, Sato S, Ishii KJ, Coban C, Hemmi H, et al. (2004) Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat Immunol 5: 1061-1068.
13. Guiducci C, Coffman RL, Barrat FJ, (2009) Signalling pathways leading to IFN-alpha production in human plasmacytoid dendritic cell and the possible use of agonists or antagonists of TLR7 and TLR9 in clinical indications. J Intern Med 265: 43-57.
14. Cox K, North M, Burke M, Singhal H, Renton S, et al. (2005) Plasmacytoid dendritic cells (PDC) are the major DC subset innately producing cytokines in human lymph nodes. J Leukoc Biol 78: 1142-1152.
15. Penna G, Vulcano M, Roncari A, Facchetti F, Sozzani S, et al. (2002) Cutting edge: differential chemokine production by myeloid and plasmacytoid dendritic cells. J Immunol 169: 6673-6676.
16. Krug A, Towarowski A, Britsch S, Rothenfusser S, Hornung V, et al. (2001) Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12. European Journal of Immunology 31: 3026-3037.
17. Matsui T, Connolly JE, Michnevitz M, Chaussabel D, Yu CI, et al. (2009) CD2 distinguishes two subsets of human plasmacytoid dendritic cells with distinct phenotype and functions. J Immunol 182: 6815-6823.
18. Asselin-Paturel C, Trinchieri G, (2005) Production of type I interferons: plasmacytoid dendritic cells and beyond. J Exp Med 202: 461-465.
19. 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.
20. Li Q, Estes JD, Schlievert PM, Duan L, Brosnahan AJ, et al. (2009) Glycerol monolaurate prevents mucosal SIV transmission. Nature 458: 1034-1038.
21. 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.
22. 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.
23. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD, (1996) HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271: 1582-1586.
24. Markowitz M, Louie M, Hurley A, Sun E, Di Mascio M, et al. (2003) A novel antiviral intervention results in more accurate assessment of human immunodeficiency virus type 1 replication dynamics and T-cell decay in vivo. J Virol 77: 5037-5038.
25. Ribeiro RM, Qin L, Chavez LL, Li D, Self SG, et al. (2010) Estimation of the initial viral growth rate and basic reproductive number during acute HIV-1 infection. J Virol 84: 6096-6102.
26. Baccam P, Beauchemin C, Macken CA, Hayden FG, Perelson AS, (2006) Kinetics of influenza A virus infection in humans. J Virol 80: 7590-7599.
27. Donhauser N, Helm M, Pritschet K, Schuster P, Ries M, et al. (2010) Differential effects of P-class versus other CpG oligodeoxynucleotide classes on the impaired innate immunity of plasmacytoid dendritic cells in HIV type 1 infection. AIDS Res Hum Retroviruses 26: 161-171.
28. 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.
29. Sadaka C, Marloie-Provost MA, Soumelis V, Benaroch P, (2009) Developmental regulation of MHC II expression and transport in human plasmacytoid-derived dendritic cells. Blood 113: 2127-2135.
30. Gibson SJ, Lindh JM, Riter TR, Gleason RM, Rogers LM, et al. (2002) Plasmacytoid dendritic cells produce cytokines and mature in response to the TLR7 agonists, imiquimod and resiquimod. Cell Immunol 218: 74-86.
31. 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.
32. Cao W, Bover L, Cho M, Wen X, Hanabuchi S, et al. (2009) Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. J Exp Med 206: 1603-1614.
33. Cao W, Rosen DB, Ito T, Bover L, Bao M, et al. (2006) Plasmacytoid dendritic cell-specific receptor ILT7-Fc epsilonRI gamma inhibits Toll-like receptor-induced interferon production. J Exp Med 203: 1399-1405.
34. Dzionek A, Sohma Y, Nagafune J, Cella M, Colonna M, et al. (2001) BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon alpha/beta induction. J Exp Med 194: 1823-1834.
35. 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.
36. Rock J, Schneider E, Grun JR, Grutzkau A, Kuppers R, et al. (2007) CD303 (BDCA-2) signals in plasmacytoid dendritic cells via a BCR-like signalosome involving Syk, Slp65 and PLCgamma2. Eur J Immunol 37: 3564-3575.
37. Zhang Z, Schuler T, Zupancic M, Wietgrefe S, Staskus KA, et al. (1999) Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. Science 286: 1353-1357.
38. Miller CJ, Li Q, Abel K, Kim EY, Ma ZM, et al. (2005) Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus. J Virol 79: 9217-9227.
39. Cohen MS, Shaw GM, McMichael AJ, Haynes BF, (2011) Acute HIV-1 Infection. N Engl J Med 364: 1943-1954.
40. Sheth PM, Danesh A, Sheung A, Rebbapragada A, Shahabi K, et al. (2006) Disproportionately high semen shedding of HIV is associated with compartmentalized cytomegalovirus reactivation. J Infect Dis 193: 45-48.
41. Baeten JM, Kahle E, Lingappa JR, Coombs RW, Delany-Moretlwe S, et al. (2011) Genital HIV-1 RNA predicts risk of heterosexual HIV-1 transmission. Sci Transl Med 3: 77ra29.
42. Megjugorac NJ, Young HA, Amrute SB, Olshalsky SL, Fitzgerald-Bocarsly P, (2004) Virally stimulated plasmacytoid dendritic cells produce chemokines and induce migration of T and NK cells. J Leukoc Biol 75: 504-514.
43. Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, et al. (2002) IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J Immunol 168: 3195-3204.
44. Lane BR, King SR, Bock PJ, Strieter RM, Coffey MJ, et al. (2003) The C-X-C chemokine IP-10 stimulates HIV-1 replication. Virology 307: 122-134.
45. Benlahrech A, Patterson S, (2011) HIV-1 infection and induction of interferon alpha in plasmacytoid dendritic cells. Curr Opin HIV AIDS 6: 373-378.
46. 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.
47. Gondois-Rey F, Dental C, Halfon P, Baumert TF, Olive D, et al. (2009) Hepatitis C virus is a weak inducer of interferon alpha in plasmacytoid dendritic cells in comparison with influenza and human herpesvirus type-1. PLoS One 4: e4319.
48. O'Brien M, Manches O, Sabado RL, Baranda SJ, Wang Y, et al. (2011) Spatiotemporal trafficking of HIV in human plasmacytoid dendritic cells defines a persistently IFN-αlpha-producing and partially matured phenotype. J Clin Invest 121: 1088-1101.
49. Porcu P, Gaddy J, Broxmeyer HE, (1998) Alloantigen-induced unresponsiveness in cord blood T lymphocytes is associated with defective activation of Ras. Proc Natl Acad Sci U S A 95: 4538-4543.
50. 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.
51. Ghedin E, Sengamalay NA, Shumway M, Zaborsky J, Feldblyum T, et al. (2005) Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature 437: 1162-1166.
52. Ratner L, Haseltine W, Patarca R, Livak KJ, Starcich B, et al. (1985) Complete nucleotide sequence of the AIDS virus, HTLV-III. Nature 313: 277-284.
53. Cao W, Zhang L, Rosen DB, Bover L, Watanabe G, et al. (2007) BDCA2/Fc epsilon RI gamma complex signals through a novel BCR-like pathway in human plasmacytoid dendritic cells. PLoS Biol 5: e248.
54. Xu Y, Hu Y, Shi B, Zhang X, Wang J, et al. (2009) HBsAg inhibits TLR9-mediated activation and IFN-αlpha production in plasmacytoid dendritic cells. Mol Immunol 46: 2640-2646.
55. Dobson-Belaire WN, Rebbapragada A, Malott RJ, Yue FY, Kovacs C, et al. (2010) Neisseria gonorrhoeae effectively blocks HIV-1 replication by eliciting a potent TLR9-dependent interferon-alpha response from plasmacytoid dendritic cells. Cell Microbiol.
56. Pal R, Venzon D, Letvin NL, Santra S, Montefiori DC, et al. (2002) ALVAC-SIV-gag-pol-env-based vaccination and macaque major histocompatibility complex class I (A*01) delay simian immunodeficiency virus SIVmac-induced immunodeficiency. J Virol 76: 292-302.
57. Spackman E, Suarez DL, (2008) Type A influenza virus detection and quantitation by real-time RT-PCR. Methods Mol Biol 436: 19-26.