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Journal of Immunology Research
Volume 2014 (2014), Article ID 359748, 10 pages
http://dx.doi.org/10.1155/2014/359748
Review Article

The Dual Role of HLA-G in Cancer

1CEA, Institut des Maladies Emergentes et des Therapies Innovantes (IMETI), Service de Recherche en Hemato-Immunologie (SRHI), Hopital Saint-Louis, 75010 Paris, France
2Université Paris Diderot, Sorbonne Paris Cité, IUH, Hopital Saint-Louis, UMR_E5, 75010 Paris, France

Received 7 January 2014; Accepted 25 February 2014; Published 31 March 2014

Academic Editor: Fabio Morandi

Copyright © 2014 Nathalie Rouas-Freiss et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. Bronte, D. B. Chappell, E. Apolloni et al., “Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation,” Journal of Immunology, vol. 162, no. 10, pp. 5728–5737, 1999. View at Google Scholar · View at Scopus
  2. N. Rouas-Freiss, P. Moreau, C. Menier, J. LeMaoult, and E. D. Carosella, “Expression of tolerogenic HLA-G molecules in cancer prevents antitumor responses,” Seminars in Cancer Biology, vol. 17, no. 6, pp. 413–421, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. E. D. Carosella, P. Moreau, J. LeMaoult, and N. Rouas-Freiss, “HLA-G: from biology to clinical benefits,” Trends in Immunology, vol. 29, no. 3, pp. 125–132, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. E. C. Ibrahim, S. Aractingi, Y. Allory et al., “Analysis of HLA antigen expression in benign and malignant melanocytic lesions reveals that upregulation of HLA-G expression correlates with malignant transformation, high inflammatory infiltration and HLA-A1 genotype,” International Journal of Cancer, vol. 108, no. 2, pp. 243–250, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Paul, F. A. Cabestré, F.-A. Le Gal et al., “Heterogeneity of HLA-G gene transcription and protein expression in malignant melanoma biopsies,” Cancer Research, vol. 59, no. 8, pp. 1954–1960, 1999. View at Google Scholar · View at Scopus
  6. G. Singer, V. Rebmann, Y.-C. Chen et al., “HLA-G is a potential tumor marker in malignant ascites,” Clinical Cancer Research, vol. 9, no. 12, pp. 4460–4464, 2003. View at Google Scholar · View at Scopus
  7. S.-M. Yie, H. Yang, S.-R. Ye, K. Li, D.-D. Dong, and X.-M. Lin, “Expression of human leukocyte antigen G (HLA-G) correlates with poor prognosis in gastric carcinoma,” Annals of Surgical Oncology, vol. 14, no. 10, pp. 2721–2729, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Urosevic, M. O. Kurrer, J. Kamarashev et al., “Human leukocyte antigen G up-regulation in lung cancer associates with high-grade histology, human leukocyte antigen class I loss and interleukin-10 production,” American Journal of Pathology, vol. 159, no. 3, pp. 817–824, 2001. View at Google Scholar · View at Scopus
  9. S.-R. Ye, H. Yang, K. Li, D.-D. Dong, X.-M. Lin, and S.-M. Yie, “Human leukocyte antigen G expression: as a significant prognostic indicator for patients with colorectal cancer,” Modern Pathology, vol. 20, no. 3, pp. 375–383, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. A. A. Erikci, B. Karagoz, M. Ozyurt, A. Ozturk, S. Kilic, and O. Bilgi, “HLA-G expression in B chronic lymphocytic leukemia: a new prognostic marker?” Hematology, vol. 14, no. 2, pp. 101–105, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. W.-H. Yan, A. Lin, B.-G. Chen et al., “Unfavourable clinical implications for HLA-G expression in acute myeloid leukaemia,” Journal of Cellular and Molecular Medicine, vol. 12, no. 3, pp. 889–898, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. G. P. Dunn, L. J. Old, and R. D. Schreiber, “The three Es of cancer immunoediting,” Annual Review of Immunology, vol. 22, pp. 329–360, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Rouas-Freiss, R. E. Marchal, M. Kirszenbaum, J. Dausset, and E. D. Carosella, “The alpha1 domain of HLA-G1 and HLA-G2 inhibits cytotoxicity induced by natural killer cells: is HLA-G the public ligand for natural killer cell inhibitory receptors?” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, pp. 5249–5254, 1997. View at Publisher · View at Google Scholar
  14. B. Favier, J. Lemaoult, E. Lesport, and E. D. Carosella, “ILT2/HLA-G interaction impairs NK-cell functions through the inhibition of the late but not the early events of the NK-cell activating synapse,” The FASEB Journal, vol. 24, no. 3, pp. 689–699, 2010. View at Publisher · View at Google Scholar
  15. C. Menier, B. Riteau, E. D. Carosella, and N. Rouas-Freiss, “MICA triggering signal for NK cell tumor lysis is counteracted by HLA-G1-mediated inhibitory signal,” International Journal of Cancer, vol. 100, no. 1, pp. 63–70, 2002. View at Publisher · View at Google Scholar
  16. F. Morandi, E. Ferretti, P. Bocca, I. Prigione, L. Raffaghello, and V. Pistoia, “A novel mechanism of soluble HLA-G mediated immune modulation: downregulation of T cell chemokine receptor expression and impairment of chemotaxis,” PLoS ONE, vol. 5, Article ID e11763, 2010. View at Publisher · View at Google Scholar
  17. F. Morandi, E. Ferretti, R. Castriconi et al., “Soluble HLA-G dampens CD94/NKG2A expression and function and differentially modulates chemotaxis and cytokine and chemokine secretion in CD56bright and CD56dim NK cells,” Blood, vol. 118, no. 22, pp. 5840–5850, 2011. View at Publisher · View at Google Scholar
  18. F. Gros, F. Cabillic, O. Toutirais, A. L. Maux, Y. Sebti, and L. Amiot, “Soluble HLA-G molecules impair natural killer/dendritic cell crosstalk via inhibition of dendritic cells,” European Journal of Immunology, vol. 38, no. 3, pp. 742–749, 2008. View at Publisher · View at Google Scholar
  19. F. A. Le Gal, B. Riteau, C. Sedlik et al., “HLA-G-mediated inhibition of antigen-specific cytotoxic T lymphocytes,” International Immunology, vol. 11, no. 8, pp. 1351–1356, 1999. View at Publisher · View at Google Scholar
  20. E. Lesport, J. Baudhuin, S. Sousa et al., “Inhibition of human gamma delta [corrected] T-cell antitumoral activity through HLA-G: implications for immunotherapy of cancer,” Cellular and Molecular Life Sciences, vol. 68, no. 20, pp. 3385–3399, 2011. View at Publisher · View at Google Scholar
  21. J. Baudhuin, J. Migraine, V. Faivre et al., “Exocytosis acts as a modulator of the ILT4-mediated inhibition of neutrophil functions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, pp. 17957–17962, 2013. View at Publisher · View at Google Scholar
  22. S. Lefebvre, S. Berrih-Aknin, F. Adrian et al., “A specific interferon (IFN)-stimulated response element of the distal HLA-G promoter binds IFN-regulatory factor 1 and mediates enhancement of this nonclassical class I gene by IFN-β,” The Journal of Biological Chemistry, vol. 276, no. 9, pp. 6133–6139, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. V. Ristich, S. Liang, W. Zhang, J. Wu, and A. Horuzsko, “Tolerization of dendritic cells by HLA-G,” European Journal of Immunology, vol. 35, no. 4, pp. 1133–1142, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Moreau, F. Adrian-Cabestre, C. Menier et al., “IL-10 selectively induces HLA-G expression in human trophoblasts and monocytes,” International Immunology, vol. 11, no. 5, pp. 803–811, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Urosevic and R. Dummer, “HLA-G and IL-10 expression in human cancer—different stories with the same message,” Seminars in Cancer Biology, vol. 13, no. 5, pp. 337–342, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. J. LeMaoult, I. Krawice-Radanne, J. Dausset, and E. D. Carosella, “HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4+ T cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 18, pp. 7064–7069, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Le Rond, C. Azéma, I. Krawice-Radanne et al., “Evidence to support the role of HLA-G5 in allograft acceptance through induction of immunosuppressive/regulatory T cells,” Journal of Immunology, vol. 176, no. 5, pp. 3266–3276, 2006. View at Google Scholar · View at Scopus
  28. A. Naji, S. Le Rond, A. Durrbach et al., “CD3+CD4low and CD3+CD8low are induced by HLA-G: novel human peripheral blood suppressor T-cell subsets involved in transplant acceptance,” Blood, vol. 110, no. 12, pp. 3936–3948, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. Z. Selmani, A. Naji, I. Zidi et al., “Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+ CD25highFOXP3+ regulatory T cells,” Stem Cells, vol. 26, no. 1, pp. 212–222, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Agaugué, E. D. Carosella, and N. Rouas-Freiss, “Role of HLA-G in tumor escape through expansion of myeloid-derived suppressor cells and cytokinic balance in favor of Th2 versus Th1/Th17,” Blood, vol. 117, no. 26, pp. 7021–7031, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. L. Loumagne, J. Baudhuin, B. Favier, F. Montespan, E. D. Carosella, and N. Rouas-Freiss, “In vivo evidence that secretion of HLA-G by immunogenic tumor cells allows their evasion from immunosurveillance,” International Journal of Cancer. In press.
  32. S. Liang, B. Baibakov, and A. Horuzsko, “HLA-G inhibits the functions of murine dendritic cells via the PIR-B immune inhibitory receptor,” European Journal of Immunology, vol. 32, pp. 2418–2426, 2002. View at Google Scholar
  33. N. Rouas-Freiss, P. Moreau, S. Ferrone, and E. D. Carosella, “HLA-G proteins in cancer: do they provide tumor cells with an escape mechanism?” Cancer Research, vol. 65, no. 22, pp. 10139–10144, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. S.-M. Yie, H. Yang, S.-R. Ye, K. Li, D.-D. Dong, and X.-M. Lin, “Expression of human leucocyte antigen G (HLA-G) is associated with prognosis in non-small cell lung cancer,” Lung Cancer, vol. 58, no. 2, pp. 267–274, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. X. Leleu, G. Le Friec, T. Facon et al., “Total soluble HLA class I and soluble HLA-G in multiple myeloma and monoclonal gammopathy of undetermined significance,” Clinical Cancer Research, vol. 11, no. 20, pp. 7297–7303, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Sebti, A. Le Maux, F. Gros et al., “Expression of functional soluble human leucocyte antigen-G molecules in lymphoproliferative disorders,” British Journal of Haematology, vol. 138, no. 2, pp. 202–212, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Naji, C. Menier, G. Maki, E. D. Carosella, and N. Rouas-Freiss, “Neoplastic B-cell growth is impaired by HLA-G/ILT2 interaction,” Leukemia, vol. 26, pp. 1889–1892, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Pracht, S. Minguet, M. Leitges, M. Reth, and M. Huber, “Association of protein kinase C-δ with the B cell antigen receptor complex,” Cellular Signalling, vol. 19, no. 4, pp. 715–722, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. F. Deschaseaux, J. Gaillard, A. Langonne et al., “Regulation and function of immunosuppressive molecule human leukocyte antigen G5 in human bone tissue,” Federation of American Societies for Experimental Biology, vol. 27, pp. 2977–2987, 2013. View at Google Scholar
  40. A. Naji, N. Rouas-Freiss, A. Durrbach, E. D. Carosella, L. Sensebe, and F. Deschaseaux, “Concise review: combining human leukocyte antigen G and mesenchymal stem cells for immunosuppressant biotherapy,” Stem Cells, vol. 31, no. 11, pp. 2296–2303, 2013. View at Google Scholar
  41. C. Menier, M. Rabreau, J.-C. Challier, M. Le Discorde, E. D. Carosella, and N. Rouas-Freiss, “Erythroblasts secrete the nonclassical HLA-G molecule from primitive to definitive hematopoiesis,” Blood, vol. 104, no. 10, pp. 3153–3160, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Menier, C. Guillard, B. Cassinat, E. D. Carosella, and N. Rouas-Freiss, “HLA-G turns off erythropoietin receptor signaling through JAK2 and JAK2 V617F dephosphorylation: clinical relevance in polycythemia vera,” Leukemia, vol. 22, no. 3, pp. 578–584, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Mascarenhas, T. I. Mughal, and S. Verstovsek, “Biology and clinical management of myeloproliferative neoplasms and development of the JAK inhibitor ruxolitinib,” Current Medicinal Chemistry, vol. 19, no. 26, pp. 4399–4413, 2012. View at Google Scholar
  44. J. E. Boyson, R. Erskine, M. C. Whitman et al., “Disulfide bond-mediated dimerization of HLA-G on the cell surface,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 25, pp. 16180–16185, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Gonen-Gross, H. Achdout, T. I. Arnon et al., “The CD85J/leukocyte inhibitory receptor-1 distinguishes between conformed and β2-microglobulin-free HLA-G molecules,” Journal of Immunology, vol. 175, no. 8, pp. 4866–4874, 2005. View at Google Scholar · View at Scopus
  46. T. Gonen-Gross, R. Gazit, H. Achdout et al., “Special organization of the HLA-G protein on the cell surface,” Human Immunology, vol. 64, no. 11, pp. 1011–1016, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Juch, A. Blaschitz, C. Daxböck, C. Rueckert, K. Kofler, and G. Dohr, “A novel sandwich ELISA for α1 domain based detection of soluble HLA-G heavy chains,” Journal of Immunological Methods, vol. 307, no. 1-2, pp. 96–106, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. P. J. Morales, J. L. Pace, J. S. Platt, D. K. Langat, and J. S. Hunt, “Synthesis of β2-microglobulin-free, disulphide-linked HLA-G5 homodimers in human placental villous cytotrophoblast cells,” Immunology, vol. 122, no. 2, pp. 179–188, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Shiroishi, D. Kohda, and K. Maenaka, “Preparation and crystallization of the disulfide-linked HLA-G dimer,” Biochimica et Biophysica Acta: Proteins and Proteomics, vol. 1764, no. 5, pp. 985–988, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. K. Y. Howangyin, M. Loustau, J. Wu et al., “Multimeric structures of HLA-G isoforms function through differential binding to LILRB receptors,” Cellular and Molecular Life Sciences. In press.
  51. M. McMaster, Y. Zhou, S. Shorter et al., “HLA-G isoforms produced by placental cytotrophoblasts and found in amniotic fluid are due to unusual glycosylation,” Journal of Immunology, vol. 160, no. 12, pp. 5922–5928, 1998. View at Google Scholar · View at Scopus
  52. A. Díaz-Lagares, E. Alegre, J. LeMaoult, E. D. Carosella, and Á. González, “Nitric oxide produces HLA-G nitration and induces metalloprotease-dependent shedding creating a tolerogenic milieu,” Immunology, vol. 126, no. 3, pp. 436–445, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Alegre, V. Rebmann, J. Lemaoult et al., “In vivo identification of an HLA-G complex as ubiquitinated protein circulating in exosomes,” European Journal of Immunology, vol. 43, no. 7, pp. 1933–1939, 2013. View at Publisher · View at Google Scholar
  54. S. Gregori, D. Tomasoni, V. Pacciani et al., “Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway,” Blood, vol. 118, no. 18, p. 5060, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. A. González-Hernandez, J. LeMaoult, A. Lopez et al., “Linking two immuno-suppressive molecules: indoleamine 2,3 dioxygenase can modify HLA-G cell-surface expression,” Biology of Reproduction, vol. 73, no. 3, pp. 571–578, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. A. S. López, E. Alegre, J. LeMaoult, E. Carosella, and Á. González, “Regulatory role of tryptophan degradation pathway in HLA-G expression by human monocyte-derived dendritic cells,” Molecular Immunology, vol. 43, no. 14, pp. 2151–2160, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. B. Riteau, F. Faure, C. Menier et al., “Exosomes bearing HLA-G are released by melanoma cells,” Human Immunology, vol. 64, no. 11, pp. 1064–1072, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Loustau, H. Wiendl, S. Ferrone, and E. D. Carosella, “HLA-G 2012 conference: the 15-year milestone update,” Tissue Antigens, vol. 81, no. 3, pp. 127–136, 2013. View at Publisher · View at Google Scholar
  59. E. D. Carosella, B. Favier, N. Rouas-Freiss, P. Moreau, and J. Lemaoult, “Beyond the increasing complexity of the immunomodulatory HLA-G molecule,” Blood, vol. 111, no. 10, pp. 4862–4870, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. J. LeMaoult, J. Caumartin, M. Daouya et al., “Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells,” Blood, vol. 109, no. 5, pp. 2040–2048, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Caumartin, B. Favier, M. Daouya et al., “Trogocytosis-based generation of suppressive NK cells,” EMBO Journal, vol. 26, no. 5, pp. 1423–1433, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. K.-Y. HoWangYin, J. Caumartin, B. Favier et al., “Proper regrafting of Ig-like transcript 2 after trogocytosis allows a functional cell-cell transfer of sensitivity,” Journal of Immunology, vol. 186, no. 4, pp. 2210–2218, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. J. LeMaoult, K. Zafaranloo, C. Le Banff, and E. D. Carosella, “HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cells,” FASEB Journal, vol. 19, no. 6, pp. 662–664, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. J. LeMaoult, M. Daouya, J. Wu, M. Loustau, A. Horuzsko, and E. D. Carosella, “Synthetic HLA-G proteins for therapeutic use in transplantation,” FASEB Journal, vol. 27, no. 9, pp. 3643–3651, 2013. View at Publisher · View at Google Scholar
  65. S. Kovats, E. K. Main, C. Librach, M. Stubblebine, S. J. Fisher, and R. Demars, “A class I antigen, HLA-G, expressed in human trophoblasts,” Science, vol. 248, no. 4952, pp. 220–223, 1990. View at Google Scholar · View at Scopus
  66. J. M. Houlihan, P. A. Biro, H. M. Harper, H. J. Jenkinson, and C. H. Holmes, “The human amnion is a site of MHC class Ib expression: evidence for the expression of HLA-E and HLA-G,” Journal of Immunology, vol. 154, no. 11, pp. 5665–5674, 1995. View at Google Scholar · View at Scopus
  67. L. Crisa, M. T. McMaster, J. K. Ishii, S. J. Fisher, and D. R. Salomon, “Identification of a thymic epithelial cell subset sharing expression of the class Ib HLA-G molecule with fetal trophoblasts,” Journal of Experimental Medicine, vol. 186, no. 2, pp. 289–298, 1997. View at Publisher · View at Google Scholar · View at Scopus
  68. V. Cirulli, J. Zalatan, M. McMaster et al., “The class I HLA repertoire of pancreatic islets comprises the nonclassical class Ib antigen HLA-G,” Diabetes, vol. 55, no. 5, pp. 1214–1222, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Le Discorde, P. Moreau, P. Sabatier, J.-M. Legeais, and E. D. Carosella, “Expression of HLA-G in human cornea, an immune-privileged tissue,” Human Immunology, vol. 64, no. 11, pp. 1039–1044, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. T. Ito, N. Ito, M. Saathoff et al., “Immunology of the human nail apparatus: the nail matrix is a site of relative immune privilege,” Journal of Investigative Dermatology, vol. 125, no. 6, pp. 1139–1148, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. P. Moreau, G. Mouillot, P. Rousseau, C. Marcou, J. Dausset, and E. D. Carosella, “HLA-G gene repression is reversed by demethylation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 3, pp. 1191–1196, 2003. View at Publisher · View at Google Scholar · View at Scopus
  72. G. Mouillot, C. Marcou, P. Rousseau, N. Rouas-Freiss, E. D. Carosella, and P. Moreau, “HLA-G gene activation in tumor cells involves cis-acting epigenetic changes,” International Journal of Cancer, vol. 113, no. 6, pp. 928–936, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. P. Moreau, S. Flajollet, and E. D. Carosella, “Non-classical transcriptional regulation of HLA-G: an update,” Journal of Cellular and Molecular Medicine, vol. 13, no. 9, pp. 2973–2989, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. C. M. Schmidt, R. G. Ehlenfeldt, M. C. Athanasiou et al., “Extraembryonic expression of the human MHC class I gene HLA-G in transgenic mice: evidence for a positive regulatory region located 1 kilobase 5' to the start site of transcription,” Journal of Immunology, vol. 151, no. 5, pp. 2633–2645, 1993. View at Google Scholar · View at Scopus
  75. C. M. Schmidt, H. L. C. Hua Lin Chen, I. Chiu, R. G. Ehlenfeldt, J. S. Hunt, and H. T. Orr, “Temporal and spatial expression of HLA-G messenger RNA in extraembryonic tissues of transgenic mice,” Journal of Immunology, vol. 155, no. 2, pp. 619–629, 1995. View at Google Scholar · View at Scopus
  76. S. J. P. Gobin, P. Biesta, J. E. M. De Steenwinkel, G. Datema, and P. J. Van Den Elsen, “HLA-G transactivation by cAMP-response element-binding protein (CREB). An alternative transactivation pathway to the conserved major histocompatibility complex (MHC) class I regulatory routes,” The Journal of Biological Chemistry, vol. 277, no. 42, pp. 39525–39531, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. E. C. Ibrahim, M. Morange, J. Dausset, E. D. Carosella, and P. Paul, “Heat shock and arsenite induce expression of the nonclassical class I histocompatibility HLA-G gene in tumor cell lines,” Cell Stress and Chaperones, vol. 5, no. 3, pp. 207–218, 2000. View at Google Scholar · View at Scopus
  78. S.-M. Yie, L.-H. Li, R. Xiao, and C. L. Librach, “A single base-pair mutation in the 3'-untranslated region of HLA-G mRNA is associated with pre-eclampsia,” Molecular Human Reproduction, vol. 14, no. 11, pp. 649–653, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Flajollet, I. Poras, E. D. Carosella, and P. Moreau, “RREB-1 is a transcriptional repressor of HLA-G,” Journal of Immunology, vol. 183, no. 11, pp. 6948–6959, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Ikeno, N. Suzuki, M. Kamiya, Y. Takahashi, J. Kudoh, and T. Okazaki, “LINE1 family member is negative regulator of HLA-G expression,” Nucleic Acids Research, vol. 40, no. 21, pp. 10742–10752, 2012. View at Publisher · View at Google Scholar
  81. P. Rousseau, M. Le Discorde, G. Mouillot, C. Marcou, E. D. Carosella, and P. Moreau, “The 14 bp deletion-insertion polymorphism in the 3' UT region of the HLA-G gene influences HLA-G mRNA stability,” Human Immunology, vol. 64, no. 11, pp. 1005–1010, 2003. View at Publisher · View at Google Scholar · View at Scopus
  82. X. Wang, B. Li, J. Wang et al., “Evidence that miR-133a causes recurrent spontaneous abortion by reducing HLA-G expression,” Reproductive BioMedicine Online, vol. 25, no. 4, pp. 415–424, 2012. View at Publisher · View at Google Scholar
  83. Z. Tan, G. Randall, J. Fan et al., “Allele-specific targeting of microRNAs to HLA-G and risk of asthma,” American Journal of Human Genetics, vol. 81, no. 4, pp. 829–834, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. W. H. Yan, A. F. Lin, C. C. Chang, and S. Ferrone, “Induction of HLA-G expression in a melanoma cell line OCM-1A following the treatment with 5-aza-2'-deoxycytidine,” Cell research, vol. 15, no. 7, pp. 523–531, 2005. View at Google Scholar · View at Scopus
  85. I. J. Wastowski, R. T. Simoes, L. Yaghi et al., “Human leukocyte antigen-G is frequently expressed in glioblastoma and may be induced in vitro by combined 5-aza-2'-deoxycytidine and interferon-γ treatments: results from a multicentric study,” The American Journal of Pathology, vol. 182, pp. 540–552, 2013. View at Publisher · View at Google Scholar
  86. B. Park, S. Lee, E. Kim, S. Chang, M. Jin, and K. Ahn, “The truncated cytoplasmic tail of HLA-G serves a quality-control function in post-ER compartments,” Immunity, vol. 15, no. 2, pp. 213–224, 2001. View at Publisher · View at Google Scholar · View at Scopus
  87. N. Rouas-Freiss, S. Bruel, C. Menier, C. Marcou, P. Moreau, and E. D. Carosella, “Switch of HLA-G alternative splicing in a melanoma cell line causes loss of HLA-G1 expression and sensitivity to NK lysis,” International Journal of Cancer, vol. 117, no. 1, pp. 114–122, 2005. View at Publisher · View at Google Scholar · View at Scopus
  88. Y. Yang, W. Chu, D. E. Geraghty, and J. S. Hunt, “Expression of HLA-G in human mononuclear phagocytes and selective induction by IFN-γ,” Journal of Immunology, vol. 156, no. 11, pp. 4224–4231, 1996. View at Google Scholar · View at Scopus
  89. Y. Sebti, G. Le Friec, C. Pangault et al., “Soluble HLA-G molecules are increased in lymphoproliferative Disorders,” Human Immunology, vol. 64, no. 11, pp. 1093–1101, 2003. View at Publisher · View at Google Scholar · View at Scopus
  90. F. Gros, Y. Sebti, S. De Guibert et al., “Soluble HLA-G molecules are increased during acute leukemia, especially in subtypes affecting monocytic and lymphoid lineages,” Neoplasia, vol. 8, no. 3, pp. 223–230, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. A.-M. Bamberger, S. Henatschke, H. M. Schulte, T. Löning, and C. M. Bamberge, “Leukemia inhibitory factor (LIF) stimulates the human HLA-G promoter in JEG3 choriocarcinoma cells,” Journal of Clinical Endocrinology and Metabolism, vol. 85, no. 10, pp. 3932–3936, 2000. View at Google Scholar · View at Scopus
  92. P. Moreau, O. Faure, S. Lefebvre et al., “Glucocorticoid hormones upregulate levels of HLA-G transcripts in trophoblasts,” Transplantation Proceedings, vol. 33, no. 3, pp. 2277–2280, 2001. View at Google Scholar · View at Scopus
  93. I. Tirado-Gonzalez, N. Freitag, G. Barrientos et al., “Galectin-1 influences trophoblast immune evasion and emerges as a predictive factor for the outcome of pregnancy,” Molecular Human Reproduction, vol. 19, pp. 43–53, 2013. View at Google Scholar
  94. C.-C. Chang and S. Ferrone, “HLA-G in melanoma: can the current controversies be solved?” Seminars in Cancer Biology, vol. 13, no. 5, pp. 361–369, 2003. View at Publisher · View at Google Scholar · View at Scopus
  95. G. Mouillot, C. Marcou, I. Zidi et al., “Hypoxia modulates HLA-G gene expression in tumor cells,” Human Immunology, vol. 68, no. 4, pp. 277–285, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. Z. Tan, A. M. Shon, and C. Ober, “Evidence of balancing selection at the HLA-G promoter region,” Human Molecular Genetics, vol. 14, no. 23, pp. 3619–3628, 2005. View at Publisher · View at Google Scholar · View at Scopus
  97. E. C. Castelli, C. T. Mendes-Junior, L. C. Veiga-Castelli, M. Roger, P. Moreau, and E. A. Donadi, “A comprehensive study of polymorphic sites along the HLA-G gene: implication for gene regulation and evolution,” Molecular Biology and Evolution, vol. 28, no. 11, pp. 3069–3086, 2011. View at Publisher · View at Google Scholar · View at Scopus
  98. T. V. F. Hviid, R. Rizzo, L. Melchiorri, M. Stignani, and O. R. Baricordi, “Polymorphism in the 5' upstream regulatory and 3' untranslated regions of the HLA-G gene in relation to soluble HLA-G and IL-10 expression,” Human Immunology, vol. 67, no. 1-2, pp. 53–62, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. D. S. Berger, W. A. Hogge, M. M. Barmada, and R. E. Ferrell, “Comprehensive analysis of HLA-G: implications for recurrent spontaneous abortion,” Reproductive Sciences, vol. 17, no. 4, pp. 331–338, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. E. A. Donadi, E. C. Castelli, A. Arnaiz-Villena, M. Roger, D. Rey, and P. Moreau, “Implications of the polymorphism of HLA-G on its function, regulation, evolution and disease association,” Cellular and Molecular Life Sciences, vol. 68, no. 3, pp. 369–395, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. C. Ober, C. Billstrand, S. Kuldanek, and Z. Tan, “The miscarriage-associated HLA-G-725G allele influences transcription rates in JEG-3 cells,” Human Reproduction, vol. 21, no. 7, pp. 1743–1748, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. G. K. da Silva, P. Vianna, T. D. Veit et al., “Influence of HLA-G polymorphisms in human immunodeficiency virus infection and hepatitis C virus co-infection in Brazilian and Italian individuals,” Infection, Genetics and Evolution, vol. 21, pp. 418–423, 2014. View at Google Scholar
  103. G. A. Harrison, K. E. Humphrey, I. B. Jakobsen, and D. W. Cooper, “A 14 bp deletion polymorphism in the HLA-G gene,” Human Molecular Genetics, vol. 2, no. 12, p. 2200, 1993. View at Google Scholar · View at Scopus
  104. E. C. Castelli, C. T. Mendes-Junior, N. H. S. Deghaide et al., “The genetic structure of 3'untranslated region of the HLA-G gene: polymorphisms and haplotypes,” Genes and Immunity, vol. 11, no. 2, pp. 134–141, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. M. O'Brien, T. McCarthy, D. Jenkins et al., “Altered HLA-G transcription in pre-eclampsia is associated with allele specific inheritance: possible role of the HLA-G gene in susceptibility to the disease,” Cellular and Molecular Life Sciences, vol. 58, no. 12-13, pp. 1943–1949, 2001. View at Google Scholar · View at Scopus
  106. T. V. F. Hviid, S. Hylenius, C. Rørbye, and L. G. Nielsen, “HLA-G allelic variants are associated with differences in the HLA-G mRNA isoform profile and HLA-G mRNA levels,” Immunogenetics, vol. 55, no. 2, pp. 63–79, 2003. View at Google Scholar · View at Scopus
  107. T. V. F. Hviid, R. Rizzo, O. B. Christiansen, L. Melchiorri, A. Lindhard, and O. R. Baricordi, “HLA-G and IL-10 in serum in relation to HLA-G genotype and polymorphisms,” Immunogenetics, vol. 56, no. 3, pp. 135–141, 2004. View at Google Scholar · View at Scopus
  108. G. Martelli-Palomino, J. A. Pancotto, Y. C. Muniz et al., “Polymorphic sites at the 3' untranslated region of the HLA-G gene are associated with differential hla-g soluble levels in the Brazilian and French population,” PLoS ONE, vol. 8, Article ID e71742, 2013. View at Publisher · View at Google Scholar
  109. I. Manaster, D. Goldman-Wohl, C. Greenfield et al., “MiRNA-mediated control of HLA-G expression and function,” PLoS ONE, vol. 7, no. 3, Article ID e33395, 2012. View at Publisher · View at Google Scholar · View at Scopus
  110. E. C. Castelli, P. Moreau, A. O. E. Chiromatzo et al., “In silico analysis of microRNAS targeting the HLA-G 3' untranslated region alleles and haplotypes,” Human Immunology, vol. 70, no. 12, pp. 1020–1025, 2009. View at Publisher · View at Google Scholar · View at Scopus