Table of Contents Author Guidelines Submit a Manuscript
Journal of Immunology Research
Volume 2014, Article ID 636292, 10 pages
http://dx.doi.org/10.1155/2014/636292
Research Article

HLA-G Expression on Blasts and Tolerogenic Cells in Patients Affected by Acute Myeloid Leukemia

1San Raffaele Telethon Institute for Gene Therapy (HSR-TIGET), Division of Regenerative Medicine, Stem Cells and Gene Therapy, San Raffaele Scientific Institute (HSR-DREaM-GENE), Via Olgettina 58, 20132 Milan, Italy
2Ph.D Program in Translational and Molecular Medicine (DIMET), University of Milan-Bicocca, Piazza della Scienza 3, 20126 Milan, Italy
3Immunohematology Blood Transfusion Service (S.I.M.T.), San Raffaele Hospital, Via Olgettina 60, 20132 Milan, Italy
4Hematology and Bone Marrow Transplantation Unit, Division of Regenerative Medicine, Stem Cells and Gene Therapy, San Raffaele Scientific Institute (HSR-DREaM-GENE), Via Olgettina 58, 20132 Milan, Italy

Received 13 December 2013; Accepted 30 January 2014; Published 13 March 2014

Academic Editor: Enrico Fainardi

Copyright © 2014 Grazia Locafaro 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. N. Rouas-Freiss, R. M.-B. Gonçalves, C. Menier, J. Dausset, and E. D. Carosella, “Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 21, pp. 11520–11525, 1997. View at Publisher · View at Google Scholar · View at Scopus
  2. J. S. Hunt, M. G. Petroff, R. H. McIntire, and C. Ober, “HLA-G and immune tolerance in pregnancy,” The FASEB Journal, vol. 19, no. 7, pp. 681–693, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Gonzalez, V. Rebmann, J. LeMaoult, P. A. Horn, E. D. Carosella, and E. Alegre, “The immunosuppressive molecule HLA-G and its clinical implications,” Critical Reviews in Clinical Laboratory Sciences, vol. 49, no. 3, pp. 63–84, 2012. View at Google Scholar
  4. T. Fujii, A. Ishitani, and D. E. Geraghty, “A soluble form of the HLA-G antigen is encoded by a messenger ribonucleic acid containing intron 4,” Journal of Immunology, vol. 153, no. 12, pp. 5516–5524, 1994. View at Google Scholar · View at Scopus
  5. A. Ishitani and D. E. Geraghty, “Alternative splicing of HLA-G transcripts yields proteins with primary structures resembling both class I and class II antigens,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 9, pp. 3947–3951, 1992. View at Google Scholar · View at Scopus
  6. B. Riteau, N. Rouas-Freiss, C. Menier, P. Paul, J. Dausset, and E. D. Carosella, “HLA-G2, -G3, and -G4 isoforms expressed as nonmature cell surface glycoproteins inhibit NK and antigen-specific CTL cytolysis,” Journal of Immunology, vol. 166, no. 8, pp. 5018–5026, 2001. View at Google Scholar · View at Scopus
  7. N. Lila, N. Rouas-Freiss, J. Dausset, A. Carpentier, and E. D. Carosella, “Soluble HLA-G protein secreted by allo-specific CD4+ T cells suppresses the allo-proliferative response: a CD4+ T cell regulatory mechanism,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 21, pp. 12150–12155, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Le Rond, J. Le Maoult, C. Créput et al., “Alloreactive CD4+ and CD8+ T cells express the immunotolerant HLA-G molecule in mixed lymphocyte reactions: in vivo implications in transplanted patients,” European Journal of Immunology, vol. 34, no. 3, pp. 649–660, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. E. D. Carosella, S. Gregori, N. Rouas-Freiss, J. Lemaoult, C. Menier, and B. Favier, “The role of HLA-G in immunity and hematopoiesis,” Cellular and Molecular Life Sciences, vol. 68, no. 3, pp. 353–368, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. 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
  11. A. Naji, A. Durrbach, E. D. Carosella, and N. Rouas-Freiss, “Soluble HLA-G and HLA-G1 expressing antigen-presenting cells inhibit T-cell alloproliferation through ILT-2/ILT-4/FasL-mediated pathways,” Human Immunology, vol. 68, no. 4, pp. 233–239, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Gregori, “Dendritic cells in networks of immunological tolerance,” Tissue Antigens, vol. 77, no. 2, pp. 89–99, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. 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. 116, no. 6, pp. 935–944, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Amodio and S. Gregori, “Human tolerogenic DC-10: perspectives for clinical applications,” Transplantation Research, vol. 1, no. 1, article 14, 2012. View at Google Scholar
  15. G. Amodio, A. Mugione, A. M. Sanchez et al., “HLA-G expressing DC-10 and CD4(+) T cells accumulate in human decidua during pregnancy,” Human Immunology, vol. 74, no. 4, pp. 406–411, 2013. View at Google Scholar
  16. G. Curigliano, C. Criscitiello, L. Gelao, and A. Goldhirsch, “Molecular pathways: human leukocyte antigen G, (HLA-G),” Clinical Cancer Research, vol. 19, no. 20, pp. 5564–5571, 2013. View at Google Scholar
  17. L. Amiot, S. Ferrone, H. Grosse-Wilde, and B. Seliger, “Biology of HLA-G in cancer: a candidate molecule for therapeutic intervention?” Cellular and Molecular Life Sciences, vol. 68, no. 3, pp. 417–431, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Rouas-Freiss, P. Moreau, C. Menier, and E. D. Carosella, “HLA-G in cancer: a way to turn off the immune system,” Seminars in Cancer Biology, vol. 13, no. 5, pp. 325–336, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. 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
  20. K. Poláková, M. Kŕčová, D. Kuba, and G. Russ, “Analysis of HLA-G expression in malignant hematopoetic cells from leukemia patients,” Leukemia Research, vol. 27, no. 7, pp. 643–648, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Mizuno, N. Emi, M. Kasai, A. Ishitani, and H. Saito, “Aberrant expression of HLA-G antigen in interferon γ-stimulated acute myelogenous leukaemia,” British Journal of Haematology, vol. 111, no. 1, pp. 280–282, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Nückel, V. Rebmann, J. Dürig, U. Dührsen, and H. Grosse-Wilde, “HLA-G expression is associated with an unfavorable outcome and immunodeficiency in chronic lymphocytic leukemia,” Blood, vol. 105, no. 4, pp. 1694–1698, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. V. Rebmann, H. Nückel, U. Dührsen, and H. Grosse-Wilde, “HLA-G in B-chronic lymphocytic leukaemia: clinical relevance and functional implications,” Seminars in Cancer Biology, vol. 17, no. 6, pp. 430–435, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. 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
  25. 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
  26. K. Polakova, T. Zeleznikova, and G. Russ, “HLA-G5 in the blood of leukemia patients and healthy individuals,” Leukemia Research, vol. 37, no. 2, pp. 139–145, 2013. View at Google Scholar
  27. 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
  28. S. E. Hiby, A. King, A. Sharkey, and Y. W. Loke, “Molecular studies of trophoblast HLA-G: polymorphism, isoforms, imprinting and expression in preimplantation embryo,” Tissue Antigens, vol. 53, no. 1, pp. 1–13, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. 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
  30. 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
  31. Z. Tan, G. Randall, J. Fan et al., “Allele-specific targeting of microRNAs to HLA-G and risk of asthma,” The American Journal of Human Genetics, vol. 81, no. 4, pp. 829–834, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. T. D. Veit and J. A. B. Chies, “Tolerance versus immune response: MicroRNAs as important elements in the regulation of the HLA-G gene expression,” Transplant Immunology, vol. 20, no. 4, pp. 229–231, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. 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
  34. M. Alvarez, J. Piedade, S. Balseiro, G. Ribas, and F. Regateiro, “HLA-G 3′-UTR SNP and 14-bp deletion polymorphisms in Portuguese and Guinea-Bissau populations,” International Journal of Immunogenetics, vol. 36, no. 6, pp. 361–366, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. 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
  36. R. Rizzo, T. V. F. Hviid, M. Govoni et al., “HLA-G genotype and HLA-G expression in systemic lupus erythematosus: HLA-G as a putative susceptibility gene in systemic lupus erythematosus,” Tissue Antigens, vol. 71, no. 6, pp. 520–529, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. O. R. Baricordi, M. Govoni, R. Rizzo, and F. Trotta, “In rheumatoid arthritis, a polymorphism in the HLA-G gene concurs in the clinical response to methotrexate treatment,” Annals of the Rheumatic Diseases, vol. 66, no. 8, pp. 1125–1126, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Fainardi, R. Rizzo, L. Melchiorri et al., “Presence of detectable levels of soluble HLA-G molecules in CSF of relapsing-remitting multiple sclerosis: relationship with CSF soluble HLA-I and IL-10 concentrations and MRI findings,” Journal of Neuroimmunology, vol. 142, no. 1-2, pp. 149–158, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. T. V. Hviid, S. Hylenius, A. M. Hoegh, C. Kruse, and O. B. Christiansen, “HLA-G polymorphisms in couples with recurrent spontaneous abortions,” Tissue Antigens, vol. 60, no. 2, pp. 122–132, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Tripathi, A. Abbas, S. Naik, and S. Agrawal, “Role of 14-bp deletion in the HLA-G gene in the maintenance of pregnancy,” Tissue Antigens, vol. 64, no. 6, pp. 706–710, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Lin, W. H. Yan, M. Z. Dai et al., “Maternal human leukocyte antigen-G polymorphism is not associated with pre-eclampsia in a Chinese Han population,” Tissue Antigens, vol. 68, no. 4, pp. 311–316, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. W. H. Yan, A. Lin, X. J. Chen et al., “Association of the maternal 14-bp insertion polymorphism in the HLA-G gene in women with recurrent spontaneous abortions,” Tissue Antigens, vol. 68, no. 6, pp. 521–523, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. A.-C. Iversen, O. T. D. Nguyen, L. F. Tømmerdal et al., “The HLA-G 14bp gene polymorphism and decidual HLA-G 14bp gene expression in pre-eclamptic and normal pregnancies,” Journal of Reproductive Immunology, vol. 78, no. 2, pp. 158–165, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Hylenius, A.-M. N. Andersen, M. Melbye, and T. V. F. Hviid, “Association between HLA-G genotype and risk of pre-eclampsia: a case-control study using family triads,” Molecular Human Reproduction, vol. 10, no. 4, pp. 237–246, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Bermingham, D. Jenkins, T. McCarthy, and M. O'Brien, “Genetic analysis of insulin-like growth factor II and HLA-G in pre-eclampsia,” Biochemical Society Transactions, vol. 28, no. 2, pp. 215–219, 2000. View at Google Scholar · View at Scopus
  46. G. La Nasa, R. Littera, F. Locatelli et al., “The human leucocyte antigen-G 14-basepair polymorphism correlates with graft-versus-host disease in unrelated bone marrow transplantation for thalassaemia,” British Journal of Haematology, vol. 139, no. 2, pp. 284–288, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Sizzano, M. Testi, L. Zito et al., “Genotypes and haplotypes in the 3′ untranslated region of the HLA-G gene and their association with clinical outcome of hematopoietic stem cell transplantation for beta-thalassemia,” Tissue Antigens, vol. 79, no. 5, pp. 326–332, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. D.-D. Dong, H. Y. Hong Yang, K. L. Ke Li et al., “Human leukocyte antigen-G (HLA-G) expression in cervical lesions: association with cancer progression, HPV 16/18 infection, and host immune response,” Reproductive Sciences, vol. 17, no. 8, pp. 718–723, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. R. Ferguson, A. V. Ramanakumar, A. Koushik, F. Coutlée, E. Franco, and M. Roger, “Human leukocyte antigen G polymorphism is associated with an increased risk of invasive cancer of the uterine cervix,” International Journal of Cancer, vol. 131, no. 3, pp. E312–E319, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Ferguson, A. V. Ramanakumar, H. Richardson et al., “Human leukocyte antigen (HLA)-E and HLA-G polymorphisms in human papillomavirus infection susceptibility and persistence,” Human Immunology, vol. 72, no. 4, pp. 337–341, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. X. He, D.-D. Dong, S.-M. Yie et al., “HLA-G expression in human breast cancer: implications for diagnosis and prognosis, and effect on allocytotoxic lymphocyte response after hormone treatment in vitro,” Annals of Surgical Oncology, vol. 17, no. 5, pp. 1459–1469, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. I. D. Silva, Y. C. Muniz, M. C. Sousa et al., “HLA-G 3'UTR polymorphisms in high grade and invasive cervico-vaginal cancer,” Human Immunology, vol. 74, no. 4, pp. 452–458, 2013. View at Google Scholar
  53. F. Mitelman, Ed., ISCN: Guidelines for Cancer Cytogenetics. Supplement to an International System for Human Cytogenetic Nomenclature, S. Karger AG, Basel, Switzerland, 1991.
  54. F. Lacombe, F. Durrieu, A. Briais et al., “Flow cytometry CD45 gating for immunophenotyping of acute myeloid leukemia,” Leukemia, vol. 11, no. 11, pp. 1878–1886, 1997. View at Google Scholar · View at Scopus
  55. R. Rizzo, T. V. F. Hviid, M. Stignani et al., “The HLA-G genotype is associated with IL-10 levels in activated PBMCs,” Immunogenetics, vol. 57, no. 3-4, pp. 172–181, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Rizzo, C. E. Mapp, L. Melchiorri et al., “Defective production of soluble HLA-G molecules by peripheral blood monocytes in patients with asthma,” Journal of Allergy and Clinical Immunology, vol. 115, no. 3, pp. 508–513, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. Shimizu, D. E. Geraghty, B. H. Koller, H. T. Orr, and R. DeMars, “Transfer and expression of three cloned human non-HLA-A,B,C class I major histocompatibility complex genes in mutant lymphoblastoid cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 1, pp. 227–231, 1988. View at Google Scholar · View at Scopus
  58. Q. Y. Guo, B. G. Chen, Y. Y. Ruan, A. Lin, and W. H. Yan, “HLA-G expression is irrelevant to prognosis in patients with acute myeloid leukemia,” Leukemia Research, vol. 35, no. 10, pp. 1350–1354, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. W. H. Yan, L. A. Fan, J. Q. Yang, L. D. Xu, Y. Ge, and F. J. Yao, “HLA-G polymorphism in a Chinese Han population with recurrent spontaneous abortion,” International Journal of Immunogenetics, vol. 33, no. 1, pp. 55–58, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. U. Feger, E. Tolosa, Y.-H. Huang et al., “HLA-G expression defines a novel regulatory T-cell subset present in human peripheral blood and sites of inflammation,” Blood, vol. 110, no. 2, pp. 568–577, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. Y.-H. Huang, A. L. Zozulya, C. Weidenfeller et al., “Specific central nervous system recruitment of HLA-G+ regulatory T cells in multiple sclerosis,” Annals of Neurology, vol. 66, no. 2, pp. 171–183, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Poláková, E. Bandžuchová, and G. Russ, “Impact of blood processing on estimation of soluble HLA-G,” Neoplasma, vol. 58, no. 4, pp. 337–342, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. G. B. Rolfsen, E. C. Castelli, E. A. Donadi, R. A. Duarte, and C. P. Soares, “HLA-G polymorphism and breast cancer,” International Journal of Immunogenetics, 2013. View at Publisher · View at Google Scholar
  64. E. Eskandari-Nasab, M. Hashemi, S. S. Hasani, M. Omrani, M. Taheri, and M. A. Mashhadi, “Association between HLA-G 3′UTR 14-bp ins/del polymorphism and susceptibility to breast cancer,” Cancer Biomarkers, vol. 13, no. 4, pp. 253–259, 2013. View at Google Scholar