Chronic immune activation in HIV-1 infection contributes to reduced interferon alpha production via enhanced CD40:CD40 ligand interaction

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Donhauser, Norbert ^a   Pritschet, Kathrin ^a   Helm, Martin ^b   Harrer, Thomas ^c   Schuster, Philipp ^a   Ries, Moritz ^a   Bischof, Georg ^a   Vollmer, Jörg ^d   Smola, Sigrun ^e   Schmidt, Barbara ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b Praxis Dr G Abelein/Dr M Helm   (Germany)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^d PFIZER INC   (United States)

^e SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ANTIRETROVIRUS AGENT; CD40 ANTIGEN; CD40 LIGAND; CPG OLIGODEOXYNUCLEOTIDE; INTERLEUKIN 6; INTERLEUKIN 8; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; OLIGONUCLEOTIDE; TOLL LIKE RECEPTOR;

ADULT; AGED; ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CD4 LYMPHOCYTE COUNT; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOSTIMULATION; MAJOR CLINICAL STUDY; MALE; MOLECULAR INTERACTION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMACYTOID DENDRITIC CELL; PROTEIN BLOOD LEVEL; UPREGULATION; VIRUS LOAD; ANIMAL; CELL LINE; CHRONIC DISEASE; DRUG EFFECT; GENE EXPRESSION REGULATION; HAMSTER; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADULT; AGED; ANIMALS; ANTI-HIV AGENTS; ANTIGENS, CD40; CD40 LIGAND; CELL LINE; CHRONIC DISEASE; CRICETINAE; FEMALE; GENE EXPRESSION REGULATION; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON-ALPHA; INTERLEUKIN-6; INTERLEUKIN-8; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; OLIGONUCLEOTIDES; TOLL-LIKE RECEPTORS;

EID: 84858697429     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033925     Document Type: Article

References (49)

1. Kirchhoff F, (2009) Is the high virulence of HIV-1 an unfortunate coincidence of primate lentiviral evolution? Nat Rev Microbiol 7: 467-476.
2. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, et al. (1999) Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nature Medicine 5: 919-923.
3. 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.
4. 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.
5. Fong L, Mengozzi M, Abbey NW, Herndier BG, Engleman EG, (2002) Productive infection of plasmacytoid dendritic cells with human immunodeficiency virus type 1 is triggered by CD40 ligation. J Virol 76: 11033-11041.
6. 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.
7. Herbeuval JP, Grivel JC, Boasso A, Hardy AW, Chougnet C, et al. (2005) CD4+ T-cell death induced by infectious and noninfectious HIV-1: role of type 1 interferon-dependent, TRAIL/DR5-mediated apoptosis. Blood 106: 3524-3531.
8. 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 U S A 103: 7000-7005.
9. Meyers JH, Justement JS, Hallahan CW, Blair ET, Sun YA, et al. (2007) Impact of HIV on cell survival and antiviral activity of plasmacytoid dendritic cells. PLoS One 2: e458.
10. 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.
11. 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. Clinical Immunology 101: 201-210.
12. Finke JS, Shodell M, Shah K, Siegal FP, Steinman RM, (2004) Dendritic cell numbers in the blood of HIV-1 infected patients before and after changes in antiretroviral therapy. J Clin Immunol 24: 647-652.
13. Martinson JA, Tenorio AR, Montoya CJ, Al Harthi L, Gichinga CN, et al. (2007) Impact of class A, B and C CpG-oligodeoxynucleotides on in vitro activation of innate immune cells in human immunodeficiency virus-1 infected individuals. Immunology 120: 526-535.
14. Siegal FP, Fitzgerald-Bocarsly P, Holland BK, Shodell M, (2001) Interferon-alpha generation and immune reconstitution during antiretroviral therapy for human immunodeficiency virus infection. AIDS 15: 1603-1612.
15. Tilton JC, Manion MM, Luskin MR, Johnson AJ, Patamawenu AA, et al. (2008) Human immunodeficiency virus viremia induces plasmacytoid dendritic cell activation in vivo and diminished alpha interferon production in vitro. J Virol 82: 3997-4006.
16. Schmidt B, Scott I, Whitmore RG, Foster H, Fujimura S, et al. (2004) Low-level HIV infection of plasmacytoid dendritic cells: onset of cytopathic effects and cell death after PDC maturation. Virology 329: 280-288.
17. van Kooten C, Banchereau J, (2000) CD40-CD40 ligand. J Leukoc Biol 67: 2-17.
18. Hsu YM, Lucci J, Su L, Ehrenfels B, Garber E, et al. (1997) Heteromultimeric complexes of CD40 ligand are present on the cell surface of human T lymphocytes. J Biol Chem 272: 911-915.
19. Mazzei GJ, Edgerton MD, Losberger C, Lecoanet-Henchoz S, Graber P, et al. (1995) Recombinant soluble trimeric CD40 ligand is biologically active. J Biol Chem 270: 7025-7028.
20. Barron MA, Blyveis N, Palmer BE, MaWhinney S, Wilson CC, (2003) Influence of plasma viremia on defects in number and immunophenotype of blood dendritic cell subsets in human immunodeficiency virus 1-infected individuals. J Infect Dis 187: 26-37.
21. Lore K, Sonnerborg A, Brostrom C, Goh LE, Perrin L, et al. (2002) Accumulation of DC-SIGN+CD40+ dendritic cells with reduced CD80 and CD86 expression in lymphoid tissue during acute HIV-1 infection. AIDS 16: 683-692.
22. Dillon SM, Robertson KB, Pan SC, MaWhinney S, Meditz AL, et al. (2008) Plasmacytoid and myeloid dendritic cells with a partial activation phenotype accumulate in lymphoid tissue during asymptomatic chronic HIV-1 infection. J Acquir Immune Defic Syndr 48: 1-12.
23. Sipsas NV, Sfikakis PP, Kontos A, Kordossis T, (2002) Levels of soluble CD40 ligand (CD154) in serum are increased in human immunodeficiency virus type 1-infected patients and correlate with CD4(+) T-cell counts. Clin Diagn Lab Immunol 9: 558-561.
24. Sui Z, Sniderhan LF, Schifitto G, Phipps RP, Gelbard HA, et al. (2007) Functional synergy between CD40 ligand and HIV-1 Tat contributes to inflammation: implications in HIV type 1 dementia. J Immunol 178: 3226-3236.
25. Sousa AE, Chaves AF, Doroana M, Antunes F, Victorino RM, (1999) Early reduction of the over-expression of CD40L, OX40 and Fas on T cells in HIV-1 infection during triple anti-retroviral therapy: possible implications for lymphocyte traffic and functional recovery. Clin Exp Immunol 116: 307-315.
26. von Hentig N, Forster AK, Kuczka K, Klinkhardt U, Klauke S, et al. (2008) Platelet-leucocyte adhesion markers before and after the initiation of antiretroviral therapy with HIV protease inhibitors. J Antimicrob Chemother 62: 1118-1121.
27. O'Gorman MR, DuChateau B, Paniagua M, Hunt J, Bensen N, et al. (2001) Abnormal CD40 ligand (CD154) expression in human immunodeficiency virus-infected children. Clin Diagn Lab Immunol 8: 1104-1109.
28. Vanham G, Penne L, Devalck J, Kestens L, Colebunders R, et al. (1999) Decreased CD40 ligand induction in CD4 T cells and dysregulated IL-12 production during HIV infection. Clin Exp Immunol 117: 335-342.
29. Zhang R, Lifson JD, Chougnet C, (2006) Failure of HIV-exposed CD4+ T cells to activate dendritic cells is reversed by restoration of CD40/CD154 interactions. Blood 107: 1989-1995.
30. Subauste CS, Subauste A, Wessendarp M, (2007) Role of CD40-dependent down-regulation of CD154 in impaired induction of CD154 in CD4(+) T cells from HIV-1-infected patients. J Immunol 178: 1645-1653.
31. 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.
32. Nusslein HG, Frosch KH, Woith W, Lane P, Kalden JR, et al. (1996) Increase of intracellular calcium is the essential signal for the expression of CD40 ligand. Eur J Immunol 26: 846-850.
33. McDougal JS, Cort SP, Kennedy MS, Cabridilla CD, Feorino PM, et al. (1985) Immunoassay for the detection and quantitation of infectious human retrovirus, lymphadenopathy-associated virus (LAV). J Immunol Methods 76: 171-183.
34. Hess S, Engelmann H, (1996) A novel function of CD40: induction of cell death in transformed cells. J Exp Med 183: 159-167.
35. Samulowitz U, Weber M, Weeratna R, Uhlmann E, Noll B, et al. (2010) A novel class of immune-stimulatory CpG oligodeoxynucleotides unifies high potency in type I interferon induction with preferred structural properties. Oligonucleotides 20: 93-101.
36. Grouard G, Rissoan MC, Filgueira L, Durand I, Banchereau J, et al. (1997) The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med 185: 1101-1111.
37. Killian MS, Norris PJ, Rawal BD, Lebedeva M, Hecht FM, et al. (2006) The effects of early antiretroviral therapy and its discontinuation on the HIV-specific antibody response. AIDS Res Hum Retroviruses 22: 640-647.
38. Schmidt B, Fujimura SH, Martin JN, Levy JA, (2006) Variations in Plasmacytoid Dendritic Cell (PDC) and Myeloid Dendritic Cell (MDC) Levels in HIV-Infected Subjects on and off Antiretroviral Therapy. J Clin Immunol 26: 55-64.
39. 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.
40. Bai F, Tincati C, Merlini E, Pacioni C, Sinigaglia E, et al. (2012) Reduced Central Memory CD4+ T Cells and Increased T-Cell Activation Characterise Treatment-Naive Patients Newly Diagnosed at Late Stage of HIV Infection. AIDS Res Treat 2012: 314849.
41. Fox PA, Nathan M, Francis N, Singh N, Weir J, et al. (2010) A double-blind, randomized controlled trial of the use of imiquimod cream for the treatment of anal canal high-grade anal intraepithelial neoplasia in HIV-positive MSM on HAART, with long-term follow-up data including the use of open-label imiquimod. AIDS 24: 2331-2335.
42. Lepelley A, Louis S, Sourisseau M, Law HK, Pothlichet J, et al. (2011) Innate sensing of HIV-infected cells. PLoS Pathog 7: e1001284.
43. Ries M, Pritschet K, Schmidt B, (2012) Blocking Type I Interferon Production: A New Therapeutic Option to Reduce the HIV-1-Induced Immune Activation. Clin Dev Immunol 2012: 534929.
44. Chehimi J, Papasavvas E, Tomescu C, Gekonge B, Abdulhaqq S, et al. (2010) Inability of plasmacytoid dendritic cells to directly lyse HIV-infected autologous CD4+ T cells despite induction of tumor necrosis factor-related apoptosis-inducing ligand. J Virol 84: 2762-2773.
45. Palefsky J, (2008) Human papillomavirus and anal neoplasia. Curr HIV/AIDS Rep 5: 78-85.
46. Pham LV, Tamayo AT, Yoshimura LC, Lin-Lee YC, Ford RJ, (2005) Constitutive NF-kappaB and NFAT activation in aggressive B-cell lymphomas synergistically activates the CD154 gene and maintains lymphoma cell survival. Blood 106: 3940-3947.
47. Ratnam I, Chiu C, Kandala NB, Easterbrook PJ, (2006) Incidence and risk factors for immune reconstitution inflammatory syndrome in an ethnically diverse HIV type 1-infected cohort. Clin Infect Dis 42: 418-427.
48. Graham SM, Masese L, Gitau R, Richardson BA, Mandaliya K, et al. (2011) Genital ulceration does not increase HIV-1 shedding in cervical or vaginal secretions of women taking antiretroviral therapy. Sex Transm Infect 87: 114-117.
49. Maurais E, Cantin R, Tremblay MJ, (2009) Human immunodeficiency virus type 1-anchored CD40 ligand induces secretion of the chemokine interleukin-8 by human primary macrophages. Virology 385: 227-232.