Interferon-α Is the Primary Plasma Type-I IFN in HIV-1 Infection and Correlates with Immune Activation and Disease Markers

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Hardy, Gareth A D ^a   Sieg, Scott ^a   Rodriguez, Benigno ^a   Anthony, Donald ^a,b   Asaad, Robert ^a   Jiang, Wei ^a   Mudd, Joseph ^a   Schacker, Timothy ^c   Funderburg, Nicholas T ^a   Pilch Cooper, Heather A ^a   Debernardo, Robert ^d   Rabin, Ronald L ^e   Lederman, Michael M ^a   Harding, Clifford V ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^e CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CD38 ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON; MESSENGER RNA; OMEGA INTERFERON; RIBAVIRIN; UNCLASSIFIED DRUG; VIRUS RNA;

ANTIVIRAL THERAPY; ARTICLE; BIOASSAY; BIOLOGICAL ACTIVITY; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE MARKER; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOSTIMULATION; LOCAL LYMPH NODE ASSAY; MAJOR CLINICAL STUDY; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN BLOOD LEVEL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANTIVIRAL AGENTS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; HEPACIVIRUS; HEPATITIS C; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, ACTIVE; INTERFERON-ALPHA; LYMPH NODES; RIBAVIRIN;

EID: 84874280676     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056527     Document Type: Article

References (36)

1. Kadowaki N, Liu YJ, (2002) Natural type I interferon-producing cells as a link between innate and adaptive immunity. Hum Immunol 63: 1126-1132.
2. Santini SM, Di Pucchio T, Lapenta C, Parlato S, Logozzi M, et al. (2002) The natural alliance between type I interferon and dendritic cells and its role in linking innate and adaptive immunity. J Interferon Cytokine Res 22: 1071-1080.
3. Honda K, Sakaguchi S, Nakajima C, Watanabe A, Yanai H, et al. (2003) Selective contribution of IFN-alpha/beta signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc Natl Acad Sci USA 100: 10872-10877.
4. Colonna M, Trinchieri G, Liu YJ, (2004) Plasmacytoid dendritic cells in immunity. Nat Immunol 5: 1219-1226.
5. Siegal FP, Kadowaki N, Shodell M, Fitzgerald-Bocarsly PA, Shah K, et al. (1999) The nature of the principal type 1 interferon-producing cells in human blood. Science 284: 1835-1837.
6. Kadowaki N, Antonenko S, Lau JY, Liu YJ, (2000) Natural interferon alpha/beta-producing cells link innate and adaptive immunity. J Exp Med 192: 219-226.
7. Stylianou E, Aukrust P, Bendtzen K, Muller F, Froland SS, (2000) Interferons and interferon (IFN)-inducible protein 10 during highly active anti-retroviral therapy (HAART)-possible immunosuppressive role of IFN-alpha in HIV infection. Clin Exp Immunol 119: 479-485.
8. Sedaghat AR, German J, Teslovich TM, Cofrancesco J Jr, Jie CC, et al. (2008) Chronic CD4+ T-cell activation and depletion in human immunodeficiency virus type 1 infection: type I interferon-mediated disruption of T-cell dynamics. J Virol 82: 1870-1883.
9. DeStefano E, Friedman RM, Friedman-Kien AE, Goedert JJ, Henriksen D, et al. (1982) Acid-labile human leukocyte interferon in homosexual men with Kaposi's sarcoma and lymphadenopathy. J Infect Dis 146: 451-459.
10. Kontsek P, Borecky L, Novak M, (1991) Are the acid-labile interferon alpha and interferon omega-1 identical? Virology 181: 416-418.
11. Minagawa T, Mizuno K, Hirano S, Asano M, Numata A, et al. (1989) Detection of high levels of immunoreactive human beta-1 interferon in sera from HIV-infected patients. Life Sci 45: iii-vii.
12. von Sydow M, Sonnerborg A, Gaines H, Strannegard O, (1991) Interferon-alpha and tumor necrosis factor-alpha in serum of patients in various stages of HIV-1 infection. AIDS Res Hum Retroviruses 7: 375-380.
13. Jones GJ, Watera C, Patterson S, Rutebemberwa A, Kaleebu P, et al. (2001) Comparative loss and maturation of peripheral blood dendritic cell subpopulations in African and non-African HIV-1-infected patients. Aids 15: 1657-1663.
14. Donaghy H, Pozniak A, Gazzard B, Qazi N, Gilmour J, et al. (2001) Loss of blood CD11c(+) myeloid and CD11c(-) plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Blood 98: 2574-2576.
15. Feldman S, Stein D, Amrute S, Denny T, Garcia Z, et al. (2001) Decreased interferon-alpha production in HIV-infected patients correlates with numerical and functional deficiencies in circulating type 2 dendritic cell precursors. Clin Immunol 101: 201-210.
16. Chehimi J, Campbell DE, Azzoni L, Bacheller D, Papasavvas E, et al. (2002) Persistent decreases in blood plasmacytoid dendritic cell number and function despite effective highly active antiretroviral therapy and increased blood myeloid dendritic cells in HIV-infected individuals. J Immunol 168: 4796-4801.
17. Nascimbeni M, Perie L, Chorro L, Diocou S, Kreitmann L, et al. (2009) Plasmacytoid dendritic cells accumulate in spleens from chronically HIV-infected patients but barely participate in interferon-alpha expression. Blood 113: 6112-6119.
18. Herbeuval JP, Nilsson J, Boasso A, Hardy AW, Kruhlak MJ, et al. (2006) Differential expression of IFN-alpha and TRAIL/DR5 in lymphoid tissue of progressor versus nonprogressor HIV-1-infected patients. Proc Natl Acad Sci USA 103: 7000-7005.
19. Tilton JC, Johnson AJ, Luskin MR, Manion MM, Yang J, et al. (2006) Diminished production of monocyte proinflammatory cytokines during human immunodeficiency virus viremia is mediated by type I interferons. J Virol 80: 11486-11497.
20. Hardy GA, Sieg SF, Rodriguez B, Jiang W, Asaad R, et al. (2009) Desensitization to type I interferon in HIV-1 infection correlates with markers of immune activation and disease progression. Blood 113: 5497-5505.
21. McCune JM, (2001) The dynamics of CD4+ T-cell depletion in HIV disease. Nature 410: 974-979.
22. Manion M, Rodriguez B, Medvik K, Hardy G, Harding CV, et al. (2012) Interferon-Alpha Administration Enhances CD8+ T Cell Activation in HIV Infection. PLoS ONE 7: e30306.
23. 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.
24. Lederman MM, Calabrese L, Funderburg NT, Clagett B, Medvik K, et al. (2011) Immunologic failure despite suppressive antiretroviral therapy is related to activation and turnover of memory CD4 cells. J Infect Dis 204: 1217-1226.
25. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
26. Mehandru S, Poles MA, Tenner-Racz K, Jean-Pierre P, Manuelli V, et al. (2006) Lack of mucosal immune reconstitution during prolonged treatment of acute and early HIV-1 infection. PLoS Med 3: e484.
27. Benito JM, Lopez M, Lozano S, Ballesteros C, Capa L, et al. (2005) CD4+ T cell recovery beyond the first year of complete suppression of viral replication during highly active antiretroviral therapy is not influenced by CD8+ T cell activation. J Infect Dis 192: 2142-2146.
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. 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.
30. 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.
31. 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.
32. Hazenberg MD, Hamann D, Schuitemaker H, Miedema F, (2000) T cell depletion in HIV-1 infection: how CD4+ T cells go out of stock. Nat Immunol 1: 285-289.
33. Liu Z, Cumberland WG, Hultin LE, Prince HE, Detels R, et al. (1997) Elevated CD38 antigen expression on CD8+ T cells is a stronger marker for the risk of chronic HIV disease progression to AIDS and death in the Multicenter AIDS Cohort Study than CD4+ cell count, soluble immune activation markers, or combinations of HLA-DR and CD38 expression. J Acquir Immune Defic Syndr Hum Retrovirol 16: 83-92.
34. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, et al. (1999) Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis 179: 859-870.
35. Rodriguez B, Lederman MM, Jiang W, Bazdar DA, Garate K, et al. (2006) Interferon-alpha differentially rescues CD4 and CD8 T cells from apoptosis in HIV infection. AIDS 20: 1379-1389.
36. Izaguirre A, Barnes BJ, Amrute S, Yeow WS, Megjugorac N, et al. (2003) Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J Leukoc Biol 74: 1125-1138.