HIV infection of dendritic cells subverts the IFN induction pathway via IRF-1 and inhibits type 1 IFN production

Blood

Volumn 118, Issue 2, 2011, Pages 298-308

  Harman, Andrew N ^a   Lai, Joey ^a   Turville, Stuart ^a   Samarajiwa, Shamith ^b   Gray, Lachlan ^c,d   Marsden, Valerie ^a   Mercier, Sarah ^a   Jones, Kate ^c,d   Nasr, Najla ^a   Rustagi, Arjun ^e   Cumming, Helen ^b   Donaghy, Heather ^a   Mak, Johnson ^c,d   Gale Jr , Michael ^e   Churchill, Melissa ^c   Hertzog, Paul ^b   Cunningham, Anthony L ^a  

^a WESTMEAD HOSPITAL   (Australia)

^b HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c BURNET INSTITUTE   (Australia)

^d MONASH UNIVERSITY   (Australia)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; GAG PROTEIN; INTERFERON; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 7;

ARTICLE; BINDING SITE; CELL DIVISION; CONTROLLED STUDY; DELETION MUTANT; DENDRITIC CELL; HERPES SIMPLEX VIRUS 2; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; INTERFERON PRODUCTION; LONG TERMINAL REPEAT; MONOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; UPREGULATION; VIRUS MUTANT;

EID: 79957998255     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-07-297721     Document Type: Article

References (55)

1. Hu J, Gardner MB, Miller CJ. Simian immunodeficiency virus rapidly penetrates the cervicovaginal mucosa after intravaginal inoculation and infects intraepithelial dendritic cells. J Virol. 2000;74(13):6087-6095. (Pubitemid 30412980)
2. Sewell AK, Price DA. Dendritic cells and transmission of HIV-1. Trends Immunol. 2001;22(4):173-175.
3. Knight SC. Dendritic cells and HIV infection: immunity with viral transmission versus compromised cellular immunity? Immunobiology. 2001;204(5):614-621. (Pubitemid 34134175)
4. Turville SG, Cameron PU, Arthos J. Bitter-sweet symphony: defining the role of dendritic cell gp120 receptors in HIV infection. J Clin Virol. 2001;22(3):229-239. (Pubitemid 32846553)
5. Harman AN, Wilkinson J, Bye CR, et al. HIV induces maturation of monocyte-derived dendritic cells and Langerhans cells. J Immunol. 2006;177(10):7103-7113. (Pubitemid 44715078)
6. de Witte L, Nabatov A, Pion M, et al. Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat Med. 2007;13(3):367-371.
7. Kawamura T, Koyanagi Y, Nakamuara Y, et al. Significant virus replication in Langerhans cells following application of HIV to abraded skin: relevance to occupational transmission of HIV. J Immunol. 2008;180(5):3297-3304.
8. Turville SG, Arthos J, Donald KM, et al. HIV gp120 receptors on human dendritic cells. Blood. 2001;98(8):2482-2488.
9. Sugaya M, Lore K, Koup RA, Douek DC, Blauvelt A. HIV-infected Langerhans cells preferentially transmit virus to proliferating autologous CD4+ memory T cells located within Langerhans cell-T cell clusters. J Immunol. 2004;172(4):2219-2224. (Pubitemid 38182369)
10. Turville SG, Santos JJ, Frank I, et al. Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood. 2004;103(6):2170-2179. (Pubitemid 38326235)
11. Hladik F, Sakchalathorn P, Ballweber L, et al. Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity. 2007;26(2):257-70, 2007.
12. McDonald D, Wu L, Bohks SM, KewelRamani VN, Unutmaz D, Hope TJ. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science. 2003;300(5623):1295-1297. (Pubitemid 36618241)
13. Weissman D, Rabin RL, Arthos J, et al. Macrophage-tropic HIV and SIV envelope proteins induce a signal through the CCR5 chemokine receptor. Nature. 1997;389(6654):981-985. (Pubitemid 27485691)
14. Sodhi A, Montaner S, Gutkind JS. Viral hijacking of G-protein-coupled- receptor signalling networks. Nat Rev Mol Cell Biol. 2004;5(12):998-1012. (Pubitemid 39611536)
15. Harman AN, Kraus M, Bye CR, et al. HIV-1-infected dendritic cells show 2 phases of gene expression changes, with lysosomal enzyme activity decreased during the second phase. Blood. 2009;114(1):85-94.
16. Doehle BP, Hladik F, McNevin JP, et al. Human immunodeficiency virus type 1 mediates global disruption of innate antiviral signaling and immune defenses within infected cells. J Virol. 2009;83(20):10395-10405.
17. Okumura A, Alce T, Lubyova B, Ezelle H, Strebel K, Pitha PM. HIV-1 accessory proteins VPR and Vif modulate antiviral response by targeting IRF-3 for degradation. Virology. 2008;373(1):85-97.
18. Ball TB, Ji H, Kimani J, et al. Polymorphisms in IRF-1 associated with resistance to HIV-1 infection in highly exposed uninfected Kenyan sex workers. AIDS. 2007;21(9):1091-1101. (Pubitemid 46763279)
19. Chertova E, Bess JW Jr, Crise BJ, et al. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J Virol. 2002;76(11):5315-5325. (Pubitemid 34517882)
20. Koup RA, Ho DD, Poli G, Fauci AS. Isolation and quantitation of HIV in peripheral blood. Curr Protoc Immunol. 2001;Chapter 12:Unit 12 2.
21. Zeichner SL, Kim JY, Alwine JC. Linker-scanning mutational analysis of the transcriptional activity of the human immunodeficiency virus type 1 long terminal repeat. J Virol. 1991;65(5):2436-2444.
22. Donaghy H, Bosnjak L, Harman AN, et al. A role for plasmacytoid dendritic cells in the immune control of human recurrent herpes simplex. J Virol. 2009;83(4):1952-1961.
23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402-408. (Pubitemid 34164012)
24. Watson S, Mercier S, Bye C, Wilkinson J, Cunningham AL, Hraman AN. Determination of suitable housekeeping genes for normalisation of quantitative real time PCR analysis of cells infected with human immunodeficiency virus and herpes viruses. Virol J. 2007;4:130.
25. Genome Bioinformatics Group of UC Santa Cruz. UCSC Genome Browser. http://www.genome.ucsc.edu. Accessed August 2008.
26. European Bioinformatics Institute and Wellcome Trust Sanger Institute. Ensembl Genome Browser http://www.ensembl.org. Accessed August 2008.
27. Samarajiwa SA, Forster S, Auchettl K, Hertzog PJ. INTERFEROME: the database of interferon regulated genes. Nucleic Acids Res. 2008;37(Database issue):D852-D857.
28. Wingender E, Chen X, Fricke E, et al. The TRANSFAC system on gene expression regulation. Nucleic Acids Res. 2001;29(1):281-283. (Pubitemid 32054469)
29. Swiss Institute of Bioinformatics. Eukaryotic Promoter Database. http://www.epd.isb-sib.ch/. Accessed August 2008.
30. Aerts S Van Loo P, Thijs G, et al. TOUCAN 2: the all-inclusive open source workbench for regulatory sequence analysis. Nucleic Acids Res. 2005;33(Web Server issue):W393-W396.
31. Turville SG, Aravantinou M, Stossel H, Romani N, Robbiani M. Resolution of de novo HIV production and trafficking in immature dendritic cells. Nat Methods. 2008;5(1):75-85.
32. Gough DJ, Messina NL, Hii L, et al. Functional crosstalk between type I and II interferon through the regulated expression of STAT1. PLoS Biol. 2010;8(4):e1000361.
33. Marsili G, Remoli AL, Sqarbanti M, Battistina A. Role of acetylases and deacetylase inhibitors in IRF-1-mediated HIV-1 long terminal repeat transcription. Ann N Y Acad Sci. 2004;1030:636-643. (Pubitemid 40378963)
34. Sgarbanti M, Borsetti A, Moscufo N, et al. Modulation of human immunodeficiency virus 1 replication by interferon regulatory factors. J Exp Med. 2002;195(10):1359-1370. (Pubitemid 34564337)
35. Sgarbanti M, Marsili G, Remoli AL, et al. Analysis of the signal transduction pathway leading to human immunodeficiency virus-1-induced interferon regulatory factor-1 upregulation. Ann N Y Acad Sci. 2004;1030:187-195. (Pubitemid 40378913)
36. Loo YM, Fornek J, Crochet N, et al. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol. 2008;82(1):335-345. (Pubitemid 350309149)
37. Coberley CR, Kohler JJ, Brown JN, et al. Impact on genetic networks in human macrophages by a CCR5 strain of human immunodeficiency virus type 1. J Virol. 2004;78(21):11477-11486. (Pubitemid 39390735)
38. Geiss GK, Bumgarner RE, An MC, et al. Large-scale monitoring of host cell gene expression during HIV-1 infection using cDNA microarrays. Virology. 2000;266(1):8-16.
39. Izmailova E, Bertley FM, Huang Q, et al. HIV-1 Tat reprograms immature dendritic cells to express chemoattractants for activated T cells and macrophages. Nat Med. 2003;9(2):191-197. (Pubitemid 36227721)
40. van 't Wout AB, Lehrman GK, Mikheeva SA, et al. Cellular gene expression upon human immunodeficiency virus type 1 infection of CD4(+)-T-cell lines. J Virol. 2003;77(2):1392-1402.
41. Harada H, Willison K, Sakakibara J, Miyamoto M, Fujita T, Taniquchi T. Absence of the type I IFN system in EC cells: transcriptional activator (IRF-1) and repressor (IRF-2) genes are developmentally regulated. Cell. 1990;63(2):303-312.
42. Hida S, Ogasawara K, Sato K, et al. CD8(+) T cell-mediated skin disease in mice lacking IRF-2, the transcriptional attenuator of interferon-alpha/beta signaling. Immunity. 2000;13(5):643-655.
43. Pollara G, Jones M, Handley ME, et al. Herpes simplex virus type-1-induced activation of myeloid dendritic cells: the roles of virus cell interaction and paracrine type I IFN secretion. J Immunol. 2004;173(6):4108- 4119. (Pubitemid 39280776)
44. Schacker T, Zeh J, Hu H, Shaughnessy M, Corey L. Changes in plasma human immunodeficiency virus type 1 RNA associated with herpes simplex virus reactivation and suppression. J Infect Dis. 2002;186(12):1718-1725. (Pubitemid 35463503)
45. Nakaya T, Sata M, Hata N, et al. Gene induction pathways mediated by distinct IRFs during viral infection. Biochem Biophys Res Commun. 2001;283(5):1150-1156. (Pubitemid 32912888)
46. Ogawa S, Lozach J, Benner C, et al. Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell. 2005;122(5):707-721. (Pubitemid 41242636)
47. Stirnweiss A, Ksienzyk A, Klages K, et al. IFN regulatory factor-1 bypasses IFN-mediated antiviral effects through viperin gene induction. J Immunol. 2010;184(9):5179-5185.
48. Van Lint C, Amella CA, Emiliani S, John M, Jie T, Verdin E. Transcription factor binding sites downstream of the human immunodeficiency virus type 1 transcription start site are important for virus infectivity. J Virol. 1997;71(8):6113-6127.
49. Sgarbanti M, Remoli AL, Marsili G, et al. IRF-1 is required for full NF-kappaB transcriptional activity at the human immunodeficiency virus type 1 long terminal repeat enhancer. J Virol. 2008;82(7):3632-3641. (Pubitemid 351429939)
50. Su RC, Sivro A. Kimani J, Jaoko W, Plummer FA, Ball TB. Epigenetic control of IRF1 responses in HIV-exposed seronegative versus HIV-susceptible individuals. Blood. Prepublished on January 3, 2011, as DOI 10.1182/blood-2010- 10-312462.
51. (Now available as Blood. 2011;117(9):2649-2657).
52. Warke RV, Becerra A, Zawadzka A, et al. Efficient dengue virus (DENV) infection of human muscle satellite cells upregulates type I interferon response genes and differentially modulates MHC I expression on bystander and DENV-infected cells. J Gen Virol. 2008;89(Pt 7):1605-1615.
53. Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nat Rev Immunol. 2008;8(7):559-568.
54. Trapp S, Derby NR, Singer R, et al. Double-stranded RNA analog poly(I:C) inhibits human immunodeficiency virus amplification in dendritic cells via type I interferon-mediated activation of APOBEC3G. J Virol. 2009;83(2):884-895.
55. Pion M, Granelli-Piperno A, Mangeat B, et al. APOBEC3G/3F mediates intrinsic resistance of monocyte-derived dendritic cells to HIV-1 infection. J Exp Med. 2006;203(13):2887-2893. (Pubitemid 46026166)