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Monocytes and T lymphocytes in HIV-1-positive patients express HLA-G molecule

Lozano, José M.a; González, Rafaela; Kindelán, José M.b; Rouas-Freiss, Nathaliec; Caballos, Rafaela; Dausset, Jeanc; Carosella, Edgardo D.c; Peña, Joséa

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Author Information

From the aService of Immunology and bInfectious Unit, Reina Sofía University Hospital, University of Cordoba, School of Medicine, Cordoba, Spain; and cService de Recherches en Hemato-immunologie CEA, Hospital Saint-Louis, IUH, Paris, France.

Correspondence to: Professor José Peña, Department of Immunology, Hospital Universitario Reina Sofía. C/. Menendez Pidal s/n, 14004 Cordoba, Spain. Tel and fax: +34 957 011628; e-mail: fi1pemaj@uco.es

Received: 2 February 2001;

revised: 18 September 2001; accepted: 24 September 2001.

Sponsorship: This work was supported by grants SAF 96-0259 and SAF00/0060 (to J.P.) from the Spanish Ministry of Education.

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Abstract

Objective: To study the expression of HLA-G on peripheral blood mononuclear cells (PBMC) from HIV-1-infected individuals in order to determine whether this molecule is induced as a consequence of HIV-1 infection.

Design: A total of 23 HIV-positive individuals in different stages of the disease were studied.

Methods: Flow cytometric analysis and Western blot were used to measure HLA-G expression on PBMC obtained from HIV-positive and control individuals.

Results: Most of the monocytes obtained from HIV-1-infected individuals express HLA-G, whereas only a very low proportion of monocytes from healthy individuals express this molecule. When T lymphocytes from HIV-1 infections were studied, it was found that 30% of them express HLA-G, whereas only 1% were HLA-G-positive in healthy individuals. HLA-G expression was also confirmed by Western blot using specific anti-HLA-G monoclonal antibodies.

Conclusion: The synthesis of HLA-G is increased in monocytes and certain T lymphocytes from HIV-1-infected individuals.

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Introduction

HIV-1 uses various strategies to avoid destruction by the immune system [1–3]. In some cases the virus protects infected cells from recognition and destruction by modifying the surface expression of histocompatibility molecules (HLA). It has thus been reported that the selective downregulation of HLA class I molecules (HLA-A, B and C), without affecting the levels of the non-classic histocompatibility molecule HLA-E by HIV-1, protects HIV-infected cells from natural killer (NK) cells [4]. The antigen-specific induction of non-classic HLA-G in activated macrophages by cytomegalovirus infection has also been reported [5].

HLA-G is a non-classic major histocompatibility class I molecule, which is characterized by limited polymorphism and tissue-restricted distribution: fetal extravillous cytotrophoblast and thymic epithelial cells [6–9]. Functionally, HLA-G is recognized by some killing inhibitory receptors [10–13]; it inhibits both NK and T cell-mediated cytolysis, as well as allogenic proliferative responses. It has been described that HLA-G proteins are involved in maternal–fetal tolerance, heart graft-acceptance and tumour immunosurveillance [7,14], although some of these functions are presently under discussion [15,16]. We have studied the expression of HLA-G on the surface of monocytes and T lymphocytes from HIV-1-infected individuals in order to determine whether this molecule is induced as a consequence of HIV-1 infection.

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Materials and methods

Blood from HIV-infected individuals was obtained during their routine follow-up visits to the Infectious Unit of the Reina Sofia University Hospital. All subjects gave informed consent under the auspices of the appropriate Hospital's Research and Ethics Committees. A total of 23 HIV-1-positive patients were eligible for analysis of cytometry, 20 of whom were receiving highly active antiretroviral therapy (HAART), whereas three were not receiving any treatment. Cells from 10 healthy individuals and the human choriocarcinoma cell line, JEG-3, were used as negative and positive controls, respectively. Peripheral blood mononuclear cells (PBMC) were obtained by density gradient centrifugation (Lymphoprep, Nycomed Pharma, Oslo, Norway). Stable transfectant cells, namely M8-HLA-G1 and K562-HLA-G1 (transfected with HLA-G1 complementary DNA) and M8-pcDNA and K562-pcDNA (transfected with the control vector alone), were obtained as previously described [17].

HLA-G expression was studied in monocytes, T lymphocytes, JEG-3, M8 and K562 HLA-G transfected cell lines by indirect immunofluorescence, as previously described [18]. Cells were incubated on ice for 30 min using monoclonal antibody (mAb) anti-HLA-G as the first antibody (MEM-G/9; EXBIO, Prague) or mAb 87G, kindly provided by Daniel Geraghty, Fred Hutchinson Cancer Reseach, Seatttle, WA, USA [19]. After thorough washing, they were then incubated with goat anti-mouse IgG (Caltag, Cambridge, USA) as the second mAb. Monocytes and T lymphocytes were evaluated by direct immunofluorescence using the mAb Leu-M3 (anti-CD14) and Leu-4 (anti-CD3), respectively, obtained from Becton-Dickinson (San Jose, California ). An isotype matched-control was used to detect non-specific binding, and no labelling was detected using negative control antibody. HLA-G levels were measured by flow cytometry in a Becton-Dickinson FACSort. The flow cytometer was appropriately compensated with Cali-Brite beads (Becton-Dickinson) and acquired cells were selectively gated by forward- and side-scatter parameters.

Western immunoblotting was performed using PBMC separated by centrifugation on ficoll gradient. Cells were lysed with Brij-97 lysing buffer, separated by sodium dodecylsulphate–polyacrylamide gel electrophoresis (10% polyacrylamide gels, reducing conditions) and electrotransferred to Hybond-P hydrophobic polyvinylidene difluoride membranes (Amersham, Bucks, UK). HLA-G was probed on Hybond-P polyvinylidene difluoride membranes using 0.1 μg/ml of the MEM-G/1 mAb from EXBIO (Prague), which is able to recognize HLA-G molecules in Western blot assay. After that they were incubated with horseradish peroxidase-labelled goat anti-mouse as the second antibody (Transduction Laboratories, Lexington, KY, USA). The blot was developed by chemiluminescence (ECLTM; Amersham). PBMC from seven HIV-1 individuals were analysed. JEG-3 and M8 transfected with HLA-G1 were used as positive controls, whereas PBMC from healthy individuals were used as negative controls.

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Results

To control the specificity of the mAb MEM-G/9, the cell line JEG-3 was used to analyse the expression of HLA-G, which resulted in the reactivity found with this mAb being equivalent to the reactivity found with 87G (Fig. 1a). It was also found in M8 and K562 cells lines transfected with the HLA-G1 cDNA that MEM-G/9 specifically reacts against the full-length HLA-G1 products (Fig. 1b).

Fig. 1
Fig. 1
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The expression of HLA-G on the surface of peripheral monocytes (CD14+) and T lymphocytes (CD3+), obtained from HIV-1-infected individuals, is shown in Fig. 2a. It was found that 92.9 ± 1.7% of the monocytes obtained from HIV-1-infected individuals expressed HLA-G, whereas only a very low proportion (14.2 ± 4.3%) of monocytes from normal individuals expressed this molecule (Fig. 1a). When T lymphocytes from HIV-1-infected individuals were studied, it was found that 33.6 ± 3.5% of them expressed HLA-G, whereas only 0.7 ± 0.5% were HLA-G positive in healthy individuals. A representative example of HLA-G expression on T lymphocytes and monocytes measured by flow cytometry in healthy and HIV-infected individuals is shown in Fig. 2b.

Fig. 2
Fig. 2
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The increase of HLA-G molecules in the PBMC of HIV-1-seropositive individuals was confirmed by Western blot using the specific anti-HLA-G MEM-G/1 mAb. Several bands, including one of 37–39 000 Mr, which corresponds to HLA-G1, appear in HIV-1-seropositive individuals, whereas no bands recognized by the anti HLA-G mAb are present in healthy individuals. Fig. 2c shows a Western blot gel as a representative example of the results obtained, including JEG-3 and M8 cells transfected with HLA-G1 used as controls.

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Discussion

One of several means used by HIV-1 to escape destruction by the immune system is to vary the levels of histocompatibility molecules (HLA) on the surface of cells in which viruses are replicating [1]. One HLA molecule of particular interest for its possible implication in inducing tolerance to the fetus in the mother is the non-classic HLA-G [6,7]. We have investigated the possibility that this molecule could be induced after HIV-1 virus infection. We found that the surface expression of HLA-G is strongly induced after HIV-1 infection in nearly all monocytes and in some T lymphocytes. Interestingly, when HLA-G levels were measured using a second antibody anti-HLA-G (mAb 87G), the results obtained (data not shown) were similar to those obtained with MEM-G/9 mAb.

The importance of these findings lies in this being the first report to demonstrate an increased number of monocytes and T lymphocytes expressing HLA-G cell-surface molecules in HIV-1-positive individuals. This membrane-bound molecule has been confirmed by Western blot. Effectively, the increased bands of 37–39 000 Mr observed in HIV-1-infected compared with healthy individuals correspond to membrane-bound HLA-G1. Additional bands observed in HIV-positive individuals could be in relation to the presence of other HLA-G isoforms, although the possibility is not excluded that some of them are products of the degradation of HLA-G1. Further analysis is required to define the identity of these bands that are present in HIV-seropositive individuals and absent in control individuals.

In a second preliminary study, the levels of HLA-G expressed on CD4 and CD8 T cell subpopulations in HIV-positive individuals were analysed. The results (data not shown) indicate that CD3+ cells expressing HLA-G were restricted to the CD8 cell subpopulation.

Our data suggest that HIV-1 induces the expression of membrane-bound HLA-G isoforms on PBMC by an indirect effect of viral products, as HLA-G expression occurs in a very high proportion on monocytes, which are not all likely to be infected, and HLA-G-positive expression in lymphocytes is associated with the CD8 compartment. Other possible indirect mechanisms by which HIV-1 could affect the expression of HLA-G is through cytokines, which are known to be upregulated in these patients. The increased level of IL-10 observed in HIV-1 infection [20] could upregulate HLA-G because it has been demonstrated that IL-10 induces HLA-G expression in normal monocytes, where this molecule is not normally present [21]. However, other factors, such as a decreased level of IL-2 [22] or the increased levels of IL-4, IL-5, IL-6, IL-15 and transforming growth factor in HIV-infected patients [23] cannot be excluded. The expression of HLA-G appears to be unrelated to the direct effects of the antiretroviral therapy being received by these patients, as we observed similarly elevated levels of HLA-G molecules in three untreated HIV-positive individuals.

The increased proportion of monocytes and lymphocytes expressing HLA-G in HIV-1 patients appears to be subsidiary to HIV infection, and could be related to the pathogenesis of the infection. The possibility that the expression of HLA-G on monocytes forms part of the strategy used by HIV-1 for evading destruction by the immune system is not excluded. Accordingly, the upregulation of HLA-G expression on monocytes may disturb their antigen-presenting capacity. Also, the cytotoxicity capacity of HLA-G-positive CD8 T cells may be affected. HLA-G interacts with several inhibitory receptors such as ILT2 (LIR1) expressed in B, T, NK and dendritic cells, ILT4 (LIR2) expressed on monocytes and dendritic cells [11], KIR2DL4 expressed on NK and certain T cells [24], and p-49 expressed on decidual NK cells [25]. These data not only offer new information about the cellular basis of AIDS, but could also suggest possible future therapeutic approaches. For example, although it is known that part of the beneficial effect of HAART in HIV-infected patients is due to their capacity to reverse certain immune functions including NK, cytotoxic T lymphocyte and monocyte/macrophage activities [26–29], it could also be important to increase the vulnerability of HIV-infected cells. In this sense the downregulation or blockage of HLA-G expression on monocytes and T lymphocytes of HIV-infected individuals would be useful, and requires further attention.

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Keywords:

Cytotoxic T lymphocytes; HAART; HIV-1; HLA-G; IL-10; monocytes

© 2002 Lippincott Williams & Wilkins, Inc.

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