Nitric oxide produces HLA-G nitration and induces metalloprotease-dependent shedding creating a tolerogenic milieu

被引:26
作者
Diaz-Lagares, Angel [1 ]
Alegre, Estibaliz [1 ]
LeMaoult, Joel [2 ]
Carosella, Edgardo D. [2 ]
Gonzalez, Alvaro [1 ]
机构
[1] Univ Navarra Clin, Dept Biochem, Pamplona 31008, Spain
[2] Hop St Louis, Inst Univ Hematol, Serv Rech Hematoimmunol, CEA DSV DRM, Paris, France
关键词
human leucocyte antigen-G; immunosuppression; monocytes; nitration; nitric oxide; NF-KAPPA-B; G MESSENGER-RNA; G EXPRESSION; TUMOR-CELLS; ANTIGEN; MONOCYTES; MOLECULE; PROTEIN; PEROXYNITRITE; SYNTHASE;
D O I
10.1111/j.1365-2567.2008.02911.x
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
Human leucocyte antigen G (HLA-G) is a tolerogenic molecule that protects the fetus from maternal immune attack, may favour tumoral immunoescape and is up-regulated in viral and inflammatory diseases. The aim of this work was to discover if nitric oxide (NO) could affect HLA-G expression or function because NO is an important modulator of innate and adaptive immunity. For this purpose HLA-G expression and function were analysed following treatment with a NO donor or a peroxynitrite donor in various cell lines expressing HLA-G either spontaneously or upon transfection. Results showed NO-dependent nitration of both cellular and soluble HLA-G protein, but not all HLA-G moieties underwent nitration. Endogenous biosynthesis of NO by both U-937-HLA-G1 and M8-HLA-G5 stable transfectants also caused HLA-G nitration. The NO decreased total HLA-G cellular protein content and expression on the cell surface, while increasing HLA-G shedding into the culture medium. This effect was post-transcriptional and the result of metalloprotease activity. By contrast, NO pretreatment did not affect HLA-G capability to suppress NK cytotoxicity and lymphocyte proliferation. Our studies show that NO regulates the availability of HLA-G molecules without modifying their biological activities.
引用
收藏
页码:436 / 445
页数:10
相关论文
共 49 条
[1]   Maternal antigen presenting cells are a source of plasmatic HLA-G during pregnancy:: Longitudinal study during pregnancy [J].
Alegre, Estibaliz ;
Diaz-Lagares, Angel ;
LeMaoult, Joel ;
Lopez-Moratalla, Natalia ;
Carosella, Edgardo D. ;
Gonzalez, Alvaro .
HUMAN IMMUNOLOGY, 2007, 68 (08) :661-667
[2]   Soluble HLA-G inhibits cell cycle progression in human alloreactive T lymphocytes [J].
Bahri, R ;
Hirsch, F ;
Josse, A ;
Rouas-Freiss, N ;
Bidere, N ;
Vasquez, A ;
Carosella, ED ;
Charpentier, B ;
Durrbach, A .
JOURNAL OF IMMUNOLOGY, 2006, 176 (03) :1331-1339
[3]   Nitric oxide modulates oxygen sensing by hypoxia-inducible factor 1-dependent induction of prolyl hydroxylase 2 [J].
Berchner-Pfannschmidt, Utta ;
Yamac, Hatice ;
Trinidad, Buena ;
Fandrey, Joachim .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2007, 282 (03) :1788-1796
[4]   Nitric oxide increased interleukin-4 expression in T lymphocytes [J].
Chang, RH ;
Feng, MHL ;
Liu, WH ;
Lai, MZ .
IMMUNOLOGY, 1997, 90 (03) :364-369
[5]   Crystal structure of HLA-G: A nonclassical MHC class I molecule expressed at the fetal-maternal interface [J].
Clements, CS ;
Kjer-Nielsen, L ;
Kostenko, L ;
Hoare, HL ;
Dunstone, MA ;
Moses, E ;
Freed, K ;
Brooks, AG ;
Rossjohn, J ;
McCluskey, J .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (09) :3360-3365
[6]  
Colonna M, 1998, J IMMUNOL, V160, P3096
[7]   Biphasic regulation of NF-κB activity underlies the pro- and anti-inflammatory actions of nitric oxide [J].
Connelly, L ;
Palacios-Callender, M ;
Ameixa, C ;
Moncada, S ;
Hobbs, AJ .
JOURNAL OF IMMUNOLOGY, 2001, 166 (06) :3873-3881
[8]   The role of NF-κB, IRF-1, and STAT-1α transcription factors in the iNOS gene induction by gliadin and IFN-γ in RAW 264.7 macrophages [J].
De Stefano, D ;
Maiuri, MC ;
Iovine, B ;
Ialenti, A ;
Bevilacqua, M ;
Carnuccio, R .
JOURNAL OF MOLECULAR MEDICINE-JMM, 2006, 84 (01) :65-74
[9]   Nitroglycerin upregulates matrix metalloproteinase expression by human macrophages [J].
Death, AK ;
Nakhla, S ;
McGrath, KCY ;
Martell, S ;
Yue, DK ;
Jessup, W ;
Celermajer, DS .
JOURNAL OF THE AMERICAN COLLEGE OF CARDIOLOGY, 2002, 39 (12) :1943-1950
[10]   Elevated levels of soluble non-classical major histocompatibility class I molecule human leucocyte antigen (HLA)-G in the blood of HIV-infected patients with or without visceral leishmaniasis [J].
Donaghy, L. ;
Gros, F. ;
Amiot, L. ;
Mary, C. ;
Maillard, A. ;
Guiguen, C. ;
Gangneux, J. -P. .
CLINICAL AND EXPERIMENTAL IMMUNOLOGY, 2007, 147 (02) :236-240