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PMID: 22701674 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Influence of cytokines on HIV-specific antibody-dependent cellular cytotoxicity activation profile of natural killer cells.

PloS one ·Vol. 7 ·No. 6 ·2012-00-00 ·Pages e38580

Wren L, Parsons MS, Isitman G, Center RJ, Kelleher AD, Stratov I, Bernard NF, Kent SJ

Abstract

There is growing interest in HIV-specific antibody-dependent cellular cytotoxicity (ADCC) as an effective immune response to prevent or control HIV infection. ADCC relies on innate immune effector cells, particularly NK cells, to mediate control of virus-infected cells. The activation of NK cells (i.e., expression of cytokines and/or degranulation) by ADCC antibodies in serum is likely subject to the influence of other factors that are also present. We observed that the HIV-specific ADCC antibodies, within serum samples from a panel of HIV-infected individuals induced divergent activation profiles of NK cells from the same donor. Some serum samples primarily induced NK cell cytokine expression (i.e., IFNγ), some primarily initiated NK cell expression of a degranulation marker (CD107a) and others initiated a similar magnitude of responses across both effector functions. We therefore evaluated a number of HIV-relevant soluble factors for their influence on the activation of NK cells by HIV-specific ADCC antibodies. Key findings were that the cytokines IL-15 and IL-10 consistently enhanced the ability of NK cells to respond to HIV-specific ADCC antibodies. Furthermore, IL-15 was demonstrated to potently activate "educated" KIR3DL1(+) NK cells from individuals carrying its HLA-Bw4 ligand. The cytokine was also demonstrated to activate "uneducated" KIR3DL1(+) NK cells from HLA-Bw6 homozygotes, but to a lesser extent. Our results show that cytokines influence the ability of NK cells to respond to ADCC antibodies in vitro. Manipulating the immunological environment to enhance the potency of NK cell-mediated HIV-specific ADCC effector functions could be a promising immunotherapy or vaccine strategy.

MeSH Terms
Antibody-Dependent Cell Cytotoxicity/immunology Cytokines/immunology Enzyme-Linked Immunosorbent Assay HIV Antibodies/immunology HIV Infections/immunology,prevention & control HLA-B Antigens/metabolism Humans Interleukin-10/immunology Interleukin-15/immunology Killer Cells, Natural/immunology,metabolism New South Wales Receptors, KIR3DL1/metabolism Statistics, Nonparametric
Chemicals
Cytokines HIV Antibodies HLA-B Antigens HLA-Bw4 antigen Interleukin-15 KIR3DL1 protein, human Receptors, KIR3DL1 Interleukin-10
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Wren Leia
Department of Microbiology and Immunology, University of Melbourne, Victoria, Australia.
Parsons Matthew S
Isitman Gamze
Center Robert J
Kelleher Anthony D
Stratov Ivan
Bernard Nicole F
Kent Stephen J
References (57)
57 references, click to expand
  1. Effect of interleukin (IL)-12 and IL-15 on activated natural killer (ANK) and antibody-dependent cellular cytotoxicity (ADCC) in HIV infection.
    J Clin Immunol. 1998 Sep;18(5):335-45 PMID: 9793826
  2. Robust NK cell-mediated human immunodeficiency virus (HIV)-specific antibody-dependent responses in HIV-infected subjects.
    J Virol. 2008 Jun;82(11):5450-9 PMID: 18353957
  3. IL-10 enhances NK cell proliferation, cytotoxicity and production of IFN-gamma when combined with IL-18.
    Eur J Immunol. 1999 Sep;29(9):2658-65 PMID: 10508240
  4. Heterogeneous neutralizing antibody and antibody-dependent cell cytotoxicity responses in HIV-1 elite controllers.
    AIDS. 2009 May 15;23(8):897-906 PMID: 19414990
  5. IL-10 stimulatory effects on human NK cells explored by gene profile analysis.
    Genes Immun. 2004 Dec;5(8):621-30 PMID: 15573087
  6. High concentrations of interleukin 15 in breast milk are associated with protection against postnatal HIV transmission.
    J Infect Dis. 2009 Nov 15;200(10):1498-502 PMID: 19835475
  7. HIV protective KIR3DL1 and HLA-B genotypes influence NK cell function following stimulation with HLA-devoid cells.
    J Immunol. 2010 Feb 15;184(4):2057-64 PMID: 20061407
  8. Rapid degranulation of NK cells following activation by HIV-specific antibodies.
    J Immunol. 2009 Jan 15;182(2):1202-10 PMID: 19124764
  9. Increased production of IL-7 accompanies HIV-1-mediated T-cell depletion: implications for T-cell homeostasis.
    Nat Med. 2001 Jan;7(1):73-9 PMID: 11135619
  10. Education of hyporesponsive NK cells by cytokines.
    Eur J Immunol. 2009 Sep;39(9):2548-55 PMID: 19701893
  11. Interleukin-15 enhances rituximab-dependent cytotoxicity against chronic lymphocytic leukemia cells and overcomes transforming growth factor beta-mediated immunosuppression.
    Exp Hematol. 2011 Nov;39(11):1064-71 PMID: 21864486
  12. Cutting edge: increased NK cell activity in HIV-1-exposed but uninfected Vietnamese intravascular drug users.
    J Immunol. 2003 Dec 1;171(11):5663-7 PMID: 14634071
  13. Elevated plasma lipopolysaccharide is not sufficient to drive natural killer cell activation in HIV-1-infected individuals.
    AIDS. 2009 Jan 2;23(1):29-34 PMID: 19050383
  14. Immune escape from HIV-specific antibody-dependent cellular cytotoxicity (ADCC) pressure.
    Proc Natl Acad Sci U S A. 2011 May 3;108(18):7505-10 PMID: 21502492
  15. Pol as a target for antibody dependent cellular cytotoxicity responses in HIV-1 infection.
    Virology. 2011 Mar 30;412(1):110-6 PMID: 21269655
  16. IgG isotype, glycosylation, and EGFR expression determine the induction of antibody-dependent cellular cytotoxicity in vitro by cetuximab.
    Hum Antibodies. 2010;19(4):89-99 PMID: 21178280
  17. Mind the gap: lack of association between KIR3DL1*004/HLA‐Bw4-induced natural killer cell function and protection from HIV infection.
    J Infect Dis. 2010 Nov 1;202 Suppl 3:S356-60 PMID: 20887224
  18. NK cell function and antibodies mediating ADCC in HIV-1-infected viremic and controller patients.
    Viral Immunol. 2011 Oct;24(5):359-68 PMID: 21958370
  19. Killer cell immunoglobulin-like receptor 3DL1 licenses CD16-mediated effector functions of natural killer cells.
    J Leukoc Biol. 2010 Nov;88(5):905-12 PMID: 20664023
  20. Induction of HIV-1 subtype B and AE-specific neutralizing antibodies in mice and macaques with DNA prime and recombinant gp140 protein boost regimens.
    Vaccine. 2009 Nov 5;27(47):6605-12 PMID: 19712773
  21. The activation of natural killer cell effector functions by cetuximab-coated, epidermal growth factor receptor positive tumor cells is enhanced by cytokines.
    Clin Cancer Res. 2007 Nov 1;13(21):6419-28 PMID: 17962339
  22. HIV Vaccine efficacy trial: glimmers of hope and the potential role of antibody-dependent cellular cytotoxicity.
    Hum Vaccin. 2011 Apr;7(4):466-73 PMID: 21389779
  23. IL-12 synergizes with IL-2 to induce lymphokine-activated cytotoxicity and perforin and granzyme gene expression in fresh human NK cells.
    Cell Immunol. 1995 Oct 1;165(1):33-43 PMID: 7671323
  24. Interleukin-15 in HIV infection: immunological and virological interactions in antiretroviral-naive and -treated patients.
    AIDS. 2002 Jan 25;16(2):181-8 PMID: 11807301
  25. Enhancement of natural killer and antibody-dependent cytolytic activities of the peripheral blood mononuclear cells of HIV-infected patients by recombinant IL-15.
    J Acquir Immune Defic Syndr Hum Retrovirol. 1997 Nov 1;16(3):137-45 PMID: 9390564
  26. Increased levels of interferon-gamma (IFN-gamma), IL-4 and transforming growth factor-beta (TGF-beta) mRNA expressing blood mononuclear cells in human HIV infection.
    Clin Exp Immunol. 1994 Apr;96(1):59-63 PMID: 8149667
  27. Short communication: CD8(+) T cell polyfunctionality profiles in progressive and nonprogressive pediatric HIV type 1 infection.
    AIDS Res Hum Retroviruses. 2011 Sep;27(9):1005-12 PMID: 21288139
  28. Preclinical safety evaluation of recombinant human interleukin-10.
    Regul Toxicol Pharmacol. 2002 Feb;35(1):56-71 PMID: 11846636
  29. Blockade of immunosuppressive cytokines restores NK cell antiviral function in chronic hepatitis B virus infection.
    PLoS Pathog. 2010 Dec 16;6(12):e1001227 PMID: 21187913
  30. The strength of inhibitory input during education quantitatively tunes the functional responsiveness of individual natural killer cells.
    Blood. 2009 Mar 12;113(11):2434-41 PMID: 18974374
  31. Vaccine-elicited SIV and HIV envelope-specific IgA and IgG memory B cells in rhesus macaque peripheral blood correlate with functional antibody responses and reduced viremia.
    Vaccine. 2011 Apr 12;29(17):3310-9 PMID: 21382487
  32. Toward an AIDS vaccine.
    Science. 2008 May 9;320(5877):760-4 PMID: 18467582
  33. IL-10 is up-regulated in multiple cell types during viremic HIV infection and reversibly inhibits virus-specific T cells.
    Blood. 2009 Jul 9;114(2):346-56 PMID: 19365081
  34. The interleukin-12-mediated pathway of immune events is dysfunctional in human immunodeficiency virus-infected individuals.
    Blood. 1999 Aug 1;94(3):1003-11 PMID: 10419892
  35. HIV disease progression: immune activation, microbes, and a leaky gut.
    Top HIV Med. 2007 Aug-Sep;15(4):114-7 PMID: 17720995
  36. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand.
    N Engl J Med. 2009 Dec 3;361(23):2209-20 PMID: 19843557
  37. A combined genotype of KIR3DL1 high expressing alleles and HLA-B*57 is associated with a reduced risk of HIV infection.
    AIDS. 2008 Jul 31;22(12):1487-91 PMID: 18614872
  38. HIV-1 gp120-specific antibody-dependent cell-mediated cytotoxicity correlates with rate of disease progression.
    J Immunol. 1996 Sep 1;157(5):2168-73 PMID: 8757343
  39. Fc receptor but not complement binding is important in antibody protection against HIV.
    Nature. 2007 Sep 6;449(7158):101-4 PMID: 17805298
  40. Serum interleukin-6 concentrations are elevated and associated with elevated tumor necrosis factor-alpha and immunoglobulin G and A concentrations in children with HIV infection.
    AIDS. 1991 Nov;5(11):1319-25 PMID: 1768380
  41. Antiviral NK cell responses in HIV infection: II. viral strategies for evasion and lessons for immunotherapy and vaccination.
    J Leukoc Biol. 2008 Jul;84(1):27-49 PMID: 18388299
  42. HIV infection abrogates the functional advantage of natural killer cells educated through KIR3DL1/HLA-Bw4 interactions to mediate anti-HIV antibody-dependent cellular cytotoxicity.
    J Virol. 2012 Apr;86(8):4488-95 PMID: 22345455
  43. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections.
    J Virol. 2009 Apr;83(8):3719-33 PMID: 19176632
  44. Extended IL10 haplotypes and their association with HIV progression to AIDS.
    Genes Immun. 2009 Jun;10(4):309-22 PMID: 19295541
  45. Human NK cell education by inhibitory receptors for MHC class I.
    Immunity. 2006 Aug;25(2):331-42 PMID: 16901727
  46. Antibody-dependent cell-mediated cytotoxic responses in participants enrolled in a phase I/II ALVAC-HIV/AIDSVAX B/E prime-boost HIV-1 vaccine trial in Thailand.
    Vaccine. 2005 Mar 31;23(19):2522-9 PMID: 15752839
  47. Granulocyte-macrophage colony-stimulating factor and tumor necrosis factor alpha in patients with human immunodeficiency virus (HIV) type 1 infection.
    Microbiol Immunol. 1993;37(10):785-92 PMID: 7904721
  48. IL-15 treatment during acute simian immunodeficiency virus (SIV) infection increases viral set point and accelerates disease progression despite the induction of stronger SIV-specific CD8+ T cell responses.
    J Immunol. 2008 Jan 1;180(1):350-60 PMID: 18097036
  49. Current perspectives of natural killer cell education by MHC class I molecules.
    Nat Rev Immunol. 2010 Oct;10(10):724-34 PMID: 20818413
  50. Protection against simian/human immunodeficiency virus (SHIV) 89.6P in macaques after coimmunization with SHIV antigen and IL-15 plasmid.
    Proc Natl Acad Sci U S A. 2007 Nov 20;104(47):18648-53 PMID: 18000037
  51. Increase in plasma IL-10 levels and rapid loss of CD4+ T cells among HIV-infected individuals in south India.
    Int J STD AIDS. 2000 Jan;11(1):49-51 PMID: 10667901
  52. Plasma cytokine levels during acute HIV-1 infection predict HIV disease progression.
    AIDS. 2010 Mar 27;24(6):819-31 PMID: 20224308
  53. Education of human natural killer cells by activating killer cell immunoglobulin-like receptors.
    Blood. 2010 Feb 11;115(6):1166-74 PMID: 19903900
  54. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1.
    Nat Genet. 2007 Jun;39(6):733-40 PMID: 17496894
  55. Antibody-dependent cell-mediated cytotoxicity in simian immunodeficiency virus-infected rhesus monkeys.
    J Virol. 2011 Jul;85(14):6906-12 PMID: 21593181
  56. Genetic association of IL-10 gene promoter polymorphism and HIV-1 infection in North Indians.
    J Clin Immunol. 2009 Jan;29(1):71-7 PMID: 18683035
  57. Activation of NK cells by ADCC antibodies and HIV disease progression.
    J Acquir Immune Defic Syndr. 2011 Oct 1;58(2):127-31 PMID: 21792067
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2012-00-00
Epub
2012-00-11
Pages
e38580
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC3372512
Subset
IM
Grants
NIAID NIH HHS · R21 AI081541 · United States
NIAID NIH HHS · R21AI081541 · United States
CIHR · Canada
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