Interactions between HLA-G and HLA-E in physiological and pathological conditions

Frontiers in Immunology

Volumn 5, Issue AUG, 2014, Pages

  Morandi, Fabio ^a   Pistoia, Vito ^a  

^a G GASLINI INSTITUTE   (Italy)

Author keywords

Autoimmune disease; HLA E; HLA G; Tumor; Viral infections

Indexed keywords

CD94 ANTIGEN; HLA E ANTIGEN; HLA G ANTIGEN; HLA G1 ANTIGEN; HLA G2 ANTIGEN; HLA G3 ANTIGEN; HLA G4 ANTIGEN; NATURAL KILLER CELL RECEPTOR NKG2A; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; AUTOIMMUNE DISEASE; BREAST CANCER; CELLULAR IMMUNITY; COOPERATION; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INFLAMMATORY DISEASE; MOLECULAR INTERACTION; NATURAL KILLER CELL; NEOPLASM; NONHUMAN; PATHOLOGY; PHYSIOLOGY; PREGNANCY; SHORT SURVEY; TUMOR ASSOCIATED LEUKOCYTE; VIRUS INFECTION;

EID: 84918780617     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00394     Document Type: Short Survey

References (60)

1. Braciale TJ. Antigen processing for presentation by MHC class I molecules. Curr Opin Immunol (1992) 4:59-62. doi: 10.1016/0952-7915(92)90126-Y
2. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, et al. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol (2001) 19:197-223. doi:10.1146/annurev.immunol.19.1.197
3. Le Bouteiller P, Lenfant F. Antigen-presenting function(s) of the non-classical HLA-E, -F and -G class I molecules: the beginning of a story. Res Immunol (1996) 147:301-13. doi:10.1016/0923-2494(96)89643-X
4. Pistoia V, Morandi F, Wang X, Ferrone S. Soluble HLA-G: are they clinically relevant? Semin Cancer Biol (2007) 17:469-79. doi:10.1016/j.semcancer.2007.07.004
5. Rizzo R, Trentini A, Bortolotti D, Manfrinato MC, Rotola A, Castellazzi M, et al. Matrix metalloproteinase-2 (MMP-2) generates soluble HLA-G1 by cell surface proteolytic shedding. Mol Cell Biochem (2013) 381:243-55. doi:10.1007/s11010-013-1708-5
6. Kovats S, Main EK, Librach C, Stubblebine M, Fisher SJ, Demars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science (1990) 248:220-3. doi:10.1126/science.2326636
7. Crisa L, Mcmaster MT, Ishii JK, Fisher SJ, Salomon DR. Identification of a thymic epithelial cell subset sharing expression of the class Ib HLA-G molecule with fetal trophoblasts. J Exp Med (1997) 186:289-98. doi:10.1084/jem.186.2.289
8. Le Discorde M, Moreau P, Sabatier P, Legeais JM, Carosella ED. Expression of HLA-G in human cornea, an immune-privileged tissue. Hum Immunol (2003) 64:1039-44. doi:10.1016/j.humimm.2003.08.346
9. Ito T, Ito N, Saathoff M, Stampachiacchiere B, Bettermann A, Bulfone-Paus S, et al. Immunology of the human nail apparatus: the nail matrix is a site of relative immune privilege. J Invest Dermatol (2005) 125:1139-48. doi:10.1111/j.0022-202X.2005.23927.x
10. Cirulli V, Zalatan J, Mcmaster M, Prinsen R, Salomon DR, Ricordi C, et al. The class I HLA repertoire of pancreatic islets comprises the nonclassical class Ib antigen HLA-G. Diabetes (2006) 55:1214-22. doi:10.2337/db05-0731
11. Yang Y, Chu W, Geraghty DE, Hunt JS. Expression of HLA-G in human mononuclear phagocytes and selective induction by IFN-gamma. J Immunol (1996) 156:4224-31.
12. Menier C, Rabreau M, Challier JC, Le Discorde M, Carosella ED, Rouas-Freiss N. Erythroblasts secrete the nonclassical HLA-G molecule from primitive to definitive hematopoiesis. Blood (2004) 104:3153-60. doi:10.1182/blood-2004-03-0809
13. Blaschitz A, Lenfant F, Mallet V, Hartmann M, Bensussan A, Geraghty DE, et al. Endothelial cells in chorionic fetal vessels of first trimester placenta express HLA-G. Eur J Immunol (1997) 27:3380-8. doi:10.1002/eji.1830271237
14. Huang YH, Zozulya AL, Weidenfeller C, Schwab N, Wiendl H. T cell suppression by naturally occurring HLA-G-expressing regulatory CD4+ T cells is IL-10-dependent and reversible. J Leukoc Biol (2009) 86:273-81. doi:10.1189/jlb.1008649
15. Amodio G, Mugione A, Sanchez AM, Vigano P, Candiani M, Somigliana E, et al. HLA-G expressing DC-10 and CD4(+) T cells accumulate in human decidua during pregnancy. Hum Immunol (2013) 74:406-11. doi:10.1016/j.humimm.2012.11.031
16. LeMaoult J, Krawice-Radanne I, Dausset J, Carosella ED. HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4+ T cells. Proc Natl Acad Sci U S A (2004) 101:7064-9. doi:10.1073/pnas.0401922101
17. Gregori S, Tomasoni D, Pacciani V, Scirpoli M, Battaglia M, Magnani CF, et al. Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway. Blood (2010) 116:935-44. doi:10.1182/blood-2009-07-234872
18. Morandi F, Raffaghello L, Bianchi G, Meloni F, Salis A, Millo E, et al. Immunogenicity of human mesenchymal stem cells in HLA-class I-restricted T-cell responses against viral or tumor-associated antigens. Stem Cells (2008) 26:1275-87. doi:10.1634/stemcells.2007-0878
19. Selmani Z, Naji A, Gaiffe E, Obert L, Tiberghien P, Rouas-Freiss N, et al. HLA-G is a crucial immunosuppressive molecule secreted by adult human mesenchymal stem cells. Transplantation (2009) 87:S62-6. doi:10.1097/TP.0b013e3181a2a4b3
20. Cabestre FA, Lefebvre S, Moreau P, Rouas-Friess N, Dausset J, Carosella ED, et al. HLA-G expression: immune privilege for tumour cells? Semin Cancer Biol (1999) 9:27-36. doi:10.1006/scbi.1998.0104
21. Fainardi E, Castellazzi M, Stignani M, Morandi F, Sana G, Gonzalez R, et al. Emerging topics and new perspectives on HLA-G. Cell Mol Life Sci (2011) 68:433-51. doi:10.1007/s00018-010-0584-3
22. Rouas-Freiss N, Goncalves RM, Menier C, Dausset J, Carosella ED. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci U S A (1997) 94:11520-5. doi:10.1073/pnas.94.21.11520
23. Riteau B, Menier C, Khalil-Daher I, Martinozzi S, Pla M, Dausset J, et al. HLA-G1 co-expression boosts the HLA class I-mediated NK lysis inhibition. Int Immunol (2001) 13:193-201. doi:10.1093/intimm/13.2.193
24. Riteau B, Rouas-Freiss N, Menier C, Paul P, Dausset J, Carosella ED. HLA-G2, -G3, and -G4 isoforms expressed as nonmature cell surface glycoproteins inhibit NK and antigen-specific CTL cytolysis. J Immunol (2001) 166:5018-26. doi:10.4049/jimmunol.166.8.5018
25. Gros F, Cabillic F, Toutirais O, Maux AL, Sebti Y, Amiot L. Soluble HLA-G molecules impair natural killer/dendritic cell crosstalk via inhibition of dendritic cells. Eur J Immunol (2008) 38:742-9. doi:10.1002/eji.200736918
26. Castellaneta A, Mazariegos GV, Nayyar N, Zeevi A, Thomson AW. HLA-G level on monocytoid dendritic cells correlates with regulatory T-cell Foxp3 expression in liver transplant tolerance. Transplantation (2011) 91:1132-40. doi:10.1097/TP.0b013e31821414c9
27. Deschaseaux F, Delgado D, Pistoia V, Giuliani M, Morandi F, Durrbach A. HLA-G in organ transplantation: towards clinical applications. Cell Mol Life Sci (2011) 68:397-404. doi:10.1007/s00018-010-0581-6
28. Rouas-Freiss N, Moreau P, Menier C, Lemaoult J, Carosella ED. Expression of tolerogenic HLA-G molecules in cancer prevents antitumor responses. Semin Cancer Biol (2007) 17:413-21. doi:10.1016/j.semcancer.2007.07.003
29. Braud VM, Allan DS, Wilson D, McMichael AJ. TAP- and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Curr Biol (1998) 8:1-10. doi:10.1016/S0960-9822(98)70014-4
30. Braud VM, Allan DS, O'Callaghan CA, Soderstrom K, D'Andrea A, Ogg GS, et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature (1998) 391:795-9. doi:10.1038/35869
31. Llano M, Lee N, Navarro F, Garcia P, Albar JP, Geraghty DE, et al. HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur J Immunol (1998) 28:2854-63. doi:10.1002/(SICI)1521-4141(199809)28:09<2854::AID-IMMU2854>3.0.CO;2-W
32. Kaiser BK, Pizarro JC, Kerns J, Strong RK. Structural basis for NKG2A/CD94 recognition of HLA-E. Proc Natl Acad Sci U S A (2008) 105:6696-701. doi:10.1073/pnas.0802736105
33. Romagnani C, Pietra G, Falco M, Millo E, Mazzarino P, Biassoni R, et al. Identification of HLA-E-specific alloreactive T lymphocytes: a cell subset that undergoes preferential expansion in mixed lymphocyte culture and displays a broad cytolytic activity against allogeneic cells. Proc Natl Acad Sci U S A (2002) 99:11328-33. doi:10.1073/pnas.172369799
34. Mazzarino P, Pietra G, Vacca P, Falco M, Colau D, Coulie P, et al. Identification of effector-memory CMV-specific T lymphocytes that kill CMV-infected target cells in an HLA-E-restricted fashion. Eur J Immunol (2005) 35:3240-7. doi:10.1002/eji.200535343
35. Jiang H, Canfield SM, Gallagher MP, Jiang HH, Jiang Y, Zheng Z, et al. HLA-E-restricted regulatory CD8(+) T cells are involved in development and control of human autoimmune type 1 diabetes. J Clin Invest (2010) 120:3641-50. doi:10.1172/JCI43522
36. Teklemariam T, Zhao L, Hantash BM. Full-length HLA-G1 and truncated HLA-G3 differentially increase HLA-E surface localization. Hum Immunol (2012) 73:898-905. doi:10.1016/j.humimm.2012.06.007
37. Ulbrecht M, Maier S, Hofmeister V, Falk CS, Brooks AG, Mcmaster MT, et al. Truncated HLA-G isoforms are retained in the endoplasmic reticulum and insufficiently provide HLA-E ligands. Hum Immunol (2004) 65:200-8. doi:10.1016/j.humimm.2003.12.004
38. Sala FG, Del Moral PM, Pizzato N, Legrand-Abravanel F, Le Bouteiller P, Lenfant F. The HLA-G*0105N null allele induces cell surface expression of HLA-E molecule and promotes CD94/NKG2A-mediated recognition in JAR choriocarcinoma cell line. Immunogenetics (2004) 56:617-24. doi:10.1007/s00251-004-0733-7
39. Ishitani A, Sageshima N, Lee N, Dorofeeva N, Hatake K, Marquardt H, et al. Protein expression and peptide binding suggest unique and interacting functional roles for HLA-E, F, and G in maternal-placental immune recognition. J Immunol (2003) 171:1376-84. doi:10.4049/jimmunol.171.3.1376
40. Shaikly V, Shakhawat A, Withey A, Morrison I, Taranissi M, Dealtry GB, et al. Cell bio-imaging reveals co-expression of HLA-G and HLA-E in human preimplantation embryos. Reprod Biomed Online (2010) 20:223-33. doi:10.1016/j.rbmo.2009.11.008
41. Stubbendorff M, Deuse T, Hua X, Phan TT, Bieback K, Atkinson K, et al. Immunological properties of extraembryonic human mesenchymal stromal cells derived from gestational tissue. Stem Cells Dev (2013) 22:2619-29. doi:10.1089/scd.2013.0043
42. Kim EM, Manzar G, Zavazava N. Human iPS cell-derived hematopoietic progenitor cells induce T-cell anergy in in vitro-generated alloreactive CD8(+) T cells. Blood (2013) 121:5167-75. doi:10.1182/blood-2012-11-467753
43. De Kruijf EM, Sajet A, Van Nes JG, Natanov R, Putter H, Smit VT, et al. HLA-E and HLA-G expression in classical HLA class I-negative tumors is of prognostic value for clinical outcome of early breast cancer patients. J Immunol (2010) 185:7452-9. doi:10.4049/jimmunol.1002629
44. Zeestraten EC, Reimers MS, Saadatmand S, Dekker JW, Liefers GJ, Van Den Elsen PJ, et al. Combined analysis of HLA class I, HLA-E and HLA-G predicts prognosis in colon cancer patients. Br J Cancer (2014) 110:459-68. doi:10.1038/bjc.2013.696
45. Malmberg KJ, Levitsky V, Norell H, De Matos CT, Carlsten M, Schedvins K, et al. IFN-gamma protects short-term ovarian carcinoma cell lines from CTL lysis via a CD94/NKG2A-dependent mechanism. J Clin Invest (2002) 110:1515-23. doi:10.1172/JCI200215564
46. da Silva GB, Silva TG, Duarte RA, Neto NL, Carrara HH, Donadi EA, et al. Expression of the classical and nonclassical HLA molecules in breast cancer. Int J Breast Cancer (2013) 2013:250435. doi:10.1155/2013/250435
47. Kren L, Valkovsky I, Dolezel J, Capak I, Pacik D, Poprach A, et al. HLA-G and HLA-E specific mRNAs connote opposite prognostic significance in renal cell carcinoma. Diagn Pathol (2012) 7:58. doi:10.1186/1746-1596-7-58
48. Silva TG, Crispim JC, Miranda FA, Hassumi MK, De Mello JM, Simoes RT, et al. Expression of the nonclassical HLA-G and HLA-E molecules in laryngeal lesions as biomarkers of tumor invasiveness. Histol Histopathol (2011) 26:1487-97.
49. Goncalves MA, Le Discorde M, Simoes RT, Rabreau M, Soares EG, Donadi EA, et al. Classical and non-classical HLA molecules and p16(INK4a) expression in precursors lesions and invasive cervical cancer. Eur J Obstet Gynecol Reprod Biol (2008) 141:70-4. doi:10.1016/j.ejogrb.2008.06.010
50. Kren L, Slaby O, Muckova K, Lzicarova E, Sova M, Vybihal V, et al. Expression of immune-modulatory molecules HLA-G and HLA-E by tumor cells in glioblastomas: an unexpected prognostic significance? Neuropathology (2011) 31:129-34. doi:10.1111/j.1440-1789.2010.01149.x
51. Marchesi M, Andersson E, Villabona L, Seliger B, Lundqvist A, Kiessling R, et al. HLA-dependent tumour development: a role for tumour associate macrophages? J Transl Med (2013) 11:247. doi:10.1186/1479-5876-11-247
52. Pangault C, Le Friec G, Caulet-Maugendre S, Lena H, Amiot L, Guilloux V, et al. Lung macrophages and dendritic cells express HLA-G molecules in pulmonary diseases. Hum Immunol (2002) 63:83-90. doi:10.1016/S0198-8859(01)00373-1
53. Rajagopalan S, Bryceson YT, Kuppusamy SP, Geraghty DE, Van Der Meer A, Joosten I, et al. Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol (2006) 4:e9. doi:10.1371/journal.pbio.0040009
54. Kren L, Muckova K, Lzicarova E, Sova M, Vybihal V, Svoboda T, et al. Production of immune-modulatory nonclassical molecules HLA-G and HLA-E by tumor infiltrating ameboid microglia/macrophages in glioblastomas: a role in innate immunity? J Neuroimmunol (2010) 220:131-5. doi:10.1016/j.jneuroim.2010.01.014
55. Jinushi M, Takehara T, Tatsumi T, Kanto T, Miyagi T, Suzuki T, et al. Negative regulation of NK cell activities by inhibitory receptor CD94/NKG2A leads to altered NK cell-induced modulation of dendritic cell functions in chronic hepatitis C virus infection. J Immunol (2004) 173:6072-81. doi:10.4049/jimmunol.173.10.6072
56. Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J Exp Med (1998) 187:813-8. doi:10.1084/jem.187.5.813
57. Megret F, Prehaud C, Lafage M, Moreau P, Rouas-Freiss N, Carosella ED, et al. Modulation of HLA-G and HLA-E expression in human neuronal cells after rabies virus or herpes virus simplex type 1 infections. Hum Immunol (2007) 68:294-302. doi:10.1016/j.humimm.2006.12.003
58. Vasireddi M, Hilliard J. Herpes B virus, macacine herpesvirus 1, breaks simplex virus tradition via major histocompatibility complex class I expression in cells from human and macaque hosts. J Virol (2012) 86:12503-11. doi:10.1128/JVI.01350-12
59. Prigione I, Penco F, Martini A, Gattorno M, Pistoia V, Morandi F. HLA-G and HLA-E in patients with juvenile idiopathic arthritis. Rheumatology (Oxford) (2011) 50:966-72. doi:10.1093/rheumatology/keq418
60. Morandi F, Venturi C, Rizzo R, Castellazzi M, Baldi E, Caniatti ML, et al. Intrathecal soluble HLA-E correlates with disease activity in patients with multiple sclerosis and may cooperate with soluble HLA-G in the resolution of neuroinflammation. J Neuroimmune Pharmacol (2013) 8:944-55. doi:10.1007/s11481-013-9459-3