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

American Journal of Pathology

Volumn 182, Issue 2, 2013, Pages 540-552

  Wastowski, Isabela J ^a,b   Simões, Renata T ^a,b   Yaghi, Layale ^a,b   Donadi, Eduardo A ^c   Pancoto, João T ^a,b   Poras, Isabelle ^a,b   Lechapt Zalcman, Emmanuèle ^c,d,e   Bernaudin, Myriam ^c,d,e   Valable, Samuel ^c,d,e   Carlotti, Carlos G ^f   Flajollet, Sébastien ^a,b   Jensen, Stine S ^g   Ferrone, Soldano ^h   Carosella, Edgardo D ^a,b   Kristensen, Bjarne W ^g   Moreau, Philippe ^a,b  

^a SAINT LOUIS HOSPITAL   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d GIP CYCERON   (France)

^e UNIVERSITÉ DE CAEN   (France)

^f CAEN UNIVERSITY HOSPITAL   (France)

^g ODENSE UNIVERSITY HOSPITAL   (Denmark)

^h UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; GAMMA INTERFERON; HLA G ANTIGEN; MESSENGER RNA;

ADULT; AGED; ANTIGEN PRESENTATION; ARTICLE; BRAZIL; CHROMATIN; CPG ISLAND; DENMARK; DNA METHYLATION; FEMALE; FRANCE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOLOGICAL TOLERANCE; MAJOR CLINICAL STUDY; MALE; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SURVIVAL; SURVIVAL TIME; UPREGULATION;

EID: 84872745338     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.10.021     Document Type: Article

References (67)

1. P. Moreau, S. Flajollet, and E.D. Carosella Non-classical transcriptional regulation of HLA-G: an update J Cell Mol Med 13 2009 2973 2989
2. 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 Cell Mol Life Sci 68 2011 369 395
3. 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 Proc Natl Acad Sci U S A 89 1992 3947 3951
4. M. Kirszenbaum, P. Moreau, E. Gluckman, J. Dausset, and E. Carosella An alternatively spliced form of HLA-G mRNA in human trophoblasts and evidence for the presence of HLA-G transcript in adult lymphocytes Proc Natl Acad Sci USA 91 1994 4209 4213
5. N. Rouas-Freiss, R.M. Goncalves, 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 Proc Natl Acad Sci U S A 94 1997 11520 11525
6. F.A. Le Gal, B. Riteau, C. Sedlik, I. Khalil-Daher, C. Menier, J. Dausset, J.G. Guillet, E.D. Carosella, and N. Rouas-Freiss HLA-G-mediated inhibition of antigen-specific cytotoxic T lymphocytes Int Immunol 11 1999 1351 1356
7. B. Riteau, C. Menier, I. Khalil-Daher, C. Sedlik, J. Dausset, N. Rouas-Freiss, and E.D. Carosella HLA-G inhibits the allogeneic proliferative response J Reprod Immunol 43 1999 203 211
8. M. Colonna, F. Navarro, T. Bellon, M. Llano, P. Garcia, J. Samaridis, L. Angman, M. Cella, and M. Lopez-Botet A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells J Exp Med 186 1997 1809 1818
9. M. Colonna, J. Samaridis, M. Cella, L. Angman, R.L. Allen, C.A. O'Callaghan, R. Dunbar, G.S. Ogg, V. Cerundolo, and A. Rolink Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules J Immunol 160 1998 3096 3100
10. S. Rajagopalan, and E.O. Long A human histocompatibility leucocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells J Exp Med 189 1999 1093 1099
11. N. Gomez-Lozano, R. de Pablo, S. Puente, and C. Vilches Recognition of HLA-G by the NK cell receptor KIR2DL4 is not essential for human reproduction Eur J Immunol 33 2003 639 644
12. S. Rajagopalan Endosomal signaling and a novel pathway defined by the natural killer receptor KIR2DL4 (CD158d) Traffic 11 2010 1381 1390
13. M.T. McMaster, C.L. Librach, Y. Zhou, K.H. Lim, M.J. Janatpour, R. DeMars, S. Kovats, C. Damsky, and S.J. Fisher Human placental HLA-G expression is restricted to differentiated cytotrophoblasts J Immunol 154 1995 3771 3778
14. E.D. Carosella, P. Moreau, J. Lemaoult, and N. Rouas-Freiss HLA-G: from biology to clinical benefits Trends Immunol 29 2008 125 132
15. N. Rouas-Freiss, P. Moreau, C. Menier, J. LeMaoult, and E.D. Carosella Expression of tolerogenic HLA-G molecules in cancer prevents antitumor responses Semin Cancer Biol 17 2007 413 421
16. S.N. Wagner, V. Rebmann, C.P. Willers, H. Grosse-Wilde, and M. Goos Expression analysis of classic and non-classic HLA molecules before interferon alfa-2b treatment of melanoma Lancet 356 2000 220 221
17. H. Nuckel, V. Rebmann, J. Durig, U. Duhrsen, and H. Grosse-Wilde HLA-G expression is associated with an unfavorable outcome and immunodeficiency in chronic lymphocytic leukemia Blood 105 2005 1694 1698
18. Ghandri N, Gabbouj S, Farhat K, Bouaouina N, Abdelaziz H, Nouri A, Chouchane L, Hassen E: Association of HLA-G polymorphisms with nasopharyngeal carcinoma risk and clinical outcome. Hum Immunol 72:150-158
19. E.M. de Kruijf, A. Sajet, J.G. van Nes, R. Natanov, H. Putter, V.T. Smit, G.J. Liefers, P.J. van den Elsen, C.J. van de Velde, and P.J. Kuppen 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 185 2010 7452 7459
20. A. Lin, X. Zhang, W.J. Zhou, Y.Y. Ruan, D.P. Xu, Q. Wang, and W.H. Yan HLA-G expression is associated with a poor prognosis in patients with esophageal squamous cell carcinoma Int J Cancer 129 2011 1382 1390
21. 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 58 2007 267 274
22. C.B. Zhu, C.X. Wang, X. Zhang, J. Zhang, and W. Li Serum sHLA-G levels: A useful indicator in distinguishing colorectal cancer from benign colorectal diseases Int J Cancer 128 2010 617 622
23. F. Morandi, I. Levreri, P. Bocca, B. Galleni, L. Raffaghello, S. Ferrone, I. Prigione, and V. Pistoia Human neuroblastoma cells trigger an immunosuppressive program in monocytes by stimulating soluble HLA-G release Cancer Res 67 2007 6433 6441
24. S. Agaugue, E.D. Carosella, and N. Rouas-Freiss Role of HLA-G in tumor escape through expansion of myeloid-derived suppressor cells and cytokinic balance favoring Th2 vs Th1/Th17 Blood 117 2011 7021 7031
25. R. Stupp, M.E. Hegi, W.P. Mason, M.J. van den Bent, M.J. Taphoorn, R.C. Janzer, S.K. Ludwin, A. Allgeier, B. Fisher, K. Belanger, P. Hau, A.A. Brandes, J. Gijtenbeek, C. Marosi, C.J. Vecht, K. Mokhtari, P. Wesseling, S. Villa, E. Eisenhauer, T. Gorlia, M. Weller, D. Lacombe, J.G. Cairncross, and R.O. Mirimanoff Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial Lancet Oncol 10 2009 459 466
26. H. Wiendl, M. Mitsdoerffer, V. Hofmeister, J. Wischhusen, A. Bornemann, R. Meyermann, E.H. Weiss, A. Melms, and M. Weller A functional role of HLA-G expression in human gliomas: an alternative strategy of immune escape J Immunol 168 2002 4772 4780
27. L. Kren, O. Slaby, K. Muckova, E. Lzicarova, M. Sova, V. Vybihal, T. Svoboda, P. Fadrus, R. Lakomy, P. Vanhara, Z. Krenova, J. Sterba, M. Smrcka, and J. Michalek Expression of immune-modulatory molecules HLA-G and HLA-E by tumor cells in glioblastomas: an unexpected prognostic significance? Neuropathology 31 2011 129 134
28. L. Kren, K. Muckova, E. Lzicarova, M. Sova, V. Vybihal, T. Svoboda, P. Fadrus, M. Smrcka, O. Slaby, R. Lakomy, P. Vanhara, Z. Krenova, and J. Michalek 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 220 2010 131 135
29. G. Frumento, S. Franchello, E. Geraghty, and G.B. Ferrara Analysis of HLA-G expression in tumor cell lines Transplant Proc 31 1999 1847 1848
30. 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 Res 65 2005 10139 10144
31. J. Bukur, B. Malenica, C. Huber, and B. Seliger Altered expression of nonclassical HLA class Ib antigens in human renal cell carcinoma and its association with impaired immune response Hum Immunol 64 2003 1081 1092
32. K.J. Malmberg, V. Levitsky, H. Norell, C.T. de Matos, M. Carlsten, K. Schedvins, H. Rabbani, A. Moretta, K. Soderstrom, J. Levitskaya, and R. Kiessling IFN-gamma protects short- term ovarian carcinoma cell lines from CTL lysis via a CD94/NKG2A-dependent mechanism J Clin Invest 110 2002 1515 1523
33. P. Moreau, G. Mouillot, P. Rousseau, C. Marcou, J. Dausset, and E.D. Carosella HLA-G gene repression is reversed by demethylation Proc Natl Acad Sci U S A 100 2003 1191 1196
34. 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 Int J Cancer 113 2005 928 936
35. B. Park, and K. Ahn An essential function of tapasin in quality control of HLA-G molecules J Biol Chem 278 2003 14337 14345
36. 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 Res 15 2005 523 531
37. A. Facoetti, R. Nano, P. Zelini, P. Morbini, E. Benericetti, M. Ceroni, M. Campoli, and S. Ferrone Human leukocyte antigen and antigen processing machinery component defects in astrocytic tumors Clin Cancer Res 11 2005 8304 8311
38. 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 Mol Biol Evol 28 2011 3069 3086
39. L.A. Lampson, C.A. Fisher, and J.P. Whelan Striking paucity of HLA-A, B, C and beta 2-microglobulin on human neuroblastoma cell lines J Immunol 130 1983 2471 2478
40. N. Bandoh, T. Ogino, H.S. Cho, S.Y. Hur, J. Shen, X. Wang, S. Kato, N. Miyokawa, Y. Harabuchi, and S. Ferrone Development and characterization of human constitutive proteasome and immunoproteasome subunit-specific monoclonal antibodies Tissue Antigens 66 2005 185 194
41. T. Ogino, X. Wang, S. Kato, N. Miyokawa, Y. Harabuchi, and S. Ferrone Endoplasmic reticulum chaperone-specific monoclonal antibodies for flow cytometry and immunohistochemical staining Tissue Antigens 62 2003 385 393
42. X. Wang, M. Campoli, H.S. Cho, T. Ogino, N. Bandoh, J. Shen, S.Y. Hur, T. Kageshita, and S. Ferrone A method to generate antigen-specific mAb capable of staining formalin-fixed, paraffin-embedded tissue sections J Immunol Methods 299 2005 139 151
43. M. Temponi, T. Kageshita, F. Perosa, R. Ono, H. Okada, and S. Ferrone Purification of murine IgG monoclonal antibodies by precipitation with caprylic acid: comparison with other methods of purification Hybridoma 8 1989 85 95
44. C. Larochelle, J.I. Alvarez, and A. Prat How do immune cells overcome the blood-brain barrier in multiple sclerosis? FEBS Lett 585 2011 3770 3780
45. I. Yang, T. Tihan, S.J. Han, M.R. Wrensch, J. Wiencke, M.E. Sughrue, and A.T. Parsa CD8+ T-cell infiltrate in newly diagnosed glioblastoma is associated with long-term survival J Clin Neurosci 17 2010 1381 1385
46. I. Yang, S.J. Han, G. Kaur, C. Crane, and A.T. Parsa The role of microglia in central nervous system immunity and glioma immunology J Clin Neurosci 17 2010 6 10
47. G.G. Gomez, and C.A. Kruse Mechanisms of malignant glioma immune resistance and sources of immunosuppression Gene Ther Mol Biol 10 2006 133 146
48. S. Wintterle, B. Schreiner, M. Mitsdoerffer, D. Schneider, L. Chen, R. Meyermann, M. Weller, and H. Wiendl Expression of the B7-related molecule B7-H1 by glioma cells: a potential mechanism of immune paralysis Cancer Res 63 2003 7462 7467
49. E.C. Brantley, L.B. Nabors, G.Y. Gillespie, Y.H. Choi, C.A. Palmer, K. Harrison, K. Roarty, and E.N. Benveniste Loss of protein inhibitors of activated STAT-3 expression in glioblastoma multiforme tumors: implications for STAT-3 activation and gene expression Clin Cancer Res 14 2008 4694 4704
50. M. Mehling, P. Simon, M. Mittelbronn, R. Meyermann, S. Ferrone, M. Weller, and H. Wiendl WHO grade associated downregulation of MHC class I antigen-processing machinery components in human astrocytomas: does it reflect a potential immune escape mechanism? Acta Neuropathol 114 2007 111 119
51. M. de Tayrac, A. Etcheverry, M. Aubry, S. Saikali, A. Hamlat, V. Quillien, A. Le Treut, M.D. Galibert, and J. Mosser Integrative genome-wide analysis reveals a robust genomic glioblastoma signature associated with copy number driving changes in gene expression Genes Chromosomes Cancer 48 2009 55 68
52. T. Gonen-Gross, H. Achdout, T.I. Arnon, R. Gazit, N. Stern, V. Horejsi, D. Goldman-Wohl, S. Yagel, and O. Mandelboim The CD85J/leukocyte inhibitory receptor-1 distinguishes between conformed and beta2-microglobulin-free HLA-G molecules J Immunol 175 2005 4866 4874
53. M. Shiroishi, K. Kuroki, L. Rasubala, K. Tsumoto, I. Kumagai, E. Kurimoto, K. Kato, D. Kohda, and K. Maenaka Structural basis for recognition of the nonclassical MHC molecule HLA-G by the leukocyte Ig-like receptor B2 (LILRB2/LIR2/ILT4/CD85d) Proc Natl Acad Sci U S A 103 2006 16412 16417
54. L. Amiot, S. Ferrone, H. Grosse-Wilde, and B. Seliger Biology of HLA-G in cancer: a candidate molecule for therapeutic intervention? Cell Mol Life Sci 68 2011 417 431
55. H. Wiendl, M. Mitsdoerffer, and M. Weller Hide-and-seek in the brain: a role for HLA-G mediating immune privilege for glioma cells Semin Cancer Biol 13 2003 343 351
56. 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 Cell Mol Life Sci 68 2011 369 395
57. Z. Tan, A.M. Shon, and C. Ober Evidence of balancing selection at the HLA-G promoter region Hum Mol Genet 14 2005 3619 3628
58. Z. Tan, G. Randall, J. Fan, B. Camoretti-Mercado, R. Brockman-Schneider, L. Pan, J. Solway, J.E. Gern, R.F. Lemanske, D. Nicolae, and C. Ober Allele-specific targeting of microRNAs to HLA-G and risk of asthma Am J Hum Genet 81 2007 829 834
59. A. Waha, S. Guntner, T.H. Huang, P.S. Yan, B. Arslan, T. Pietsch, and O.D. Wiestler Epigenetic silencing of the protocadherin family member PCDH-gamma-A11 in astrocytomas Neoplasia 7 2005 193 199
60. G. Liu, H. Ying, G. Zeng, C.J. Wheeler, K.L. Black, and J.S. Yu HER-2, gp100, and MAGE-1 are expressed in human glioblastoma and recognized by cytotoxic T cells Cancer Res 64 2004 4980 4986
61. R. Patel, L. Shervington, R. Lea, and A. Shervington Epigenetic silencing of telomerase and a non-alkylating agent as a novel therapeutic approach for glioma Brain Res 1188 2008 173 181
62. M. Teyssier, A. Bensussan, M. Kirszenbaum, P. Moreau, E. Gluckman, J. Dausset, and E. Carosella Natural killer cells are the unique lymphocyte cell subset which do not express HLA-G Nat Immun 14 1995 262 270
63. W. Cao, X. Yang, J. Zhou, Z. Teng, L. Cao, X. Zhang, and Z. Fei Targeting 14-3-3 protein, difopein induces apoptosis of human glioma cells and suppresses tumor growth in mice Apoptosis 15 2010 230 241
64. E.C. Castelli, P. Moreau, A. Oya e Chiromatzo, C.T. Mendes-Junior, L.C. Veiga-Castelli, L. Yaghi, S. Giuliatti, E.D. Carosella, and E.A. Donadi In silico analysis of microRNAS targeting the HLA-G 3′ untranslated region alleles and haplotypes Hum Immunol 70 2009 1020 1025
65. E. Satoh, T. Mabuchi, H. Satoh, T. Asahara, H. Nukui, and H. Naganuma Reduced expression of the transporter associated with antigen processing 1 molecule in malignant glioma cells, and its restoration by interferon-gamma and -beta J Neurosurg 104 2006 264 271
66. C. Ober, C. Billstrand, S. Kuldanek, and Z. Tan The miscarriage- associated HLA-G -725G allele influences transcription rates in JEG-3 cells Hum Reprod 21 2006 1743 1748
67. E.C. Castelli, C.T. Mendes-Junior, N.H. Deghaide, R.S. de Albuquerque, Y.C. Muniz, R.T. Simoes, E.D. Carosella, P. Moreau, and E.A. Donadi The genetic structure of 3′untranslated region of the HLA-G gene: polymorphisms and haplotypes Genes Immun 11 2010 134 141