The role of classical and non-classical HLA class I antigens in human tumors

Seminars in Cancer Biology

Volumn 22, Issue 4, 2012, Pages 350-358

  Bukur, Juergen ^a   Jasinski, Simon ^a   Seliger, Barbara ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Antigen processing; HLA class I; HLA G; Immune response; Tumor

Indexed keywords

HLA ANTIGEN CLASS 1; HLA G ANTIGEN;

ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ANTIGEN STRUCTURE; CANCER GRADING; CANCER GROWTH; EPIGENETICS; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; IMMUNOSURVEILLANCE; MALIGNANT NEOPLASTIC DISEASE; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR ESCAPE;

ANIMALS; ANTIGEN PRESENTATION; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INTERFERON-GAMMA; NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR ESCAPE;

EID: 84862122547     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2012.03.003     Document Type: Review

References (129)

1. Besser M.J., Shapira-Frommer R., Treves A.J., Zippel D., Itzhaki O., Hershkovitz L., et al. Clinical responses in a phase II study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin Cancer Res 2010, 16:2646-2655.
2. Garrido C., Algarra I., Maleno I., Stefanski J., Collado A., Garrido F., et al. Alterations of HLA class I expression in human melanoma xenografts in immunodeficient mice occur frequently and are associated with higher tumorigenicity. Cancer Immunol Immunother 2010, 59:13-26.
3. Klages K., Mayer C.T., Lahl K., Loddenkemper C., Teng M.W., Ngiow S.F., et al. Selective depletion of Foxp3+ regulatory T cells improves effective therapeutic vaccination against established melanoma. Cancer Res 2010, 70:7788-7799.
4. Mitsui J., Nishikawa H., Muraoka D., Wang L., Noguchi T., Sato E., et al. Two distinct mechanisms of augmented antitumor activity by modulation of immunostimulatory/inhibitory signals. Clin Cancer Res 2010, 16:2781-2791.
5. Yan X., Zhang X., Wang Y., Li X., Wang S., Zhao B., et al. Regulatory T-cell depletion synergizes with gp96-mediated cellular responses and antitumor activity. Cancer Immunol Immunother 2011, 60:1763-1774.
6. Cany J., Tran L., Gauttier V., Judor J.P., Vassaux G., Ferry N., et al. Immunotherapy of hepatocellular carcinoma: is there a place for regulatory T-lymphocyte depletion. Immunotherapy 2011, 3:32-34.
7. Elkord E., Dangoor A., Burt D.J., Southgate T.D., Daayana S., Harrop R., et al. Immune evasion mechanisms in colorectal cancer liver metastasis patients vaccinated with TroVax (MVA-5T4). Cancer Immunol Immunother 2009, 58:1657-1667.
8. Frey A.B., Monu N. Signaling defects in anti-tumor T cells. Immunol Rev 2008, 222:192-205.
9. Jorritsma A., Schotte R., Coccoris M., de Witte M.A., Schumacher T.N. Prospects and limitations of T cell receptor gene therapy. Curr Gene Ther 2011, 11:276-287.
10. Tjin E.P., Konijnenberg D., Krebbers G., Mallo H., Drijfhout J.W., Franken K.L., et al. T-cell immune function in tumor, skin, and peripheral blood of advanced stage melanoma patients: implications for immunotherapy. Clin Cancer Res 2011, 17:5736-5747.
11. Aptsiauri N., Carretero R., Garcia-Lora A., Real L.M., Cabrera T., Garrido F. Regressing and progressing metastatic lesions: resistance to immunotherapy is predetermined by irreversible HLA class I antigen alterations. Cancer Immunol Immunother 2008, 57:1727-1733.
12. Carretero R., Romero J.M., Ruiz-Cabello F., Maleno I., Rodriguez F., Camacho F.M., et al. Analysis of HLA class I expression in progressing and regressing metastatic melanoma lesions after immunotherapy. Immunogenetics 2008, 60:439-447.
13. Garrido F., Algarra I., Garcia-Lora A.M. The escape of cancer from T lymphocytes: immunoselection of MHC class I loss variants harboring structural-irreversible hard lesions. Cancer Immunol Immunother 2010, 59:1601-1606.
14. Garrido F., Cabrera T., Aptsiauri N. Hard and soft lesions underlying the HLA class I alterations in cancer cells: implications for immunotherapy. Int J Cancer 2010, 127:249-256.
15. Rosenberg S.A., Sherry R.M., Morton K.E., Scharfman W.J., Yang J.C., Topalian S.L., et al. Tumor progression can occur despite the induction of very high levels of self/tumor antigen-specific CD8+ T cells in patients with melanoma. J Immunol 2005, 175:6169-6176.
16. Laugel B., Cole D.K., Clement M., Wooldridge L., Price D.A., Sewell A.K. The multiple roles of the CD8 coreceptor in T cell biology: opportunities for the selective modulation of self-reactive cytotoxic T cells. J Leukoc Biol 2011, 90:1089-1099.
17. Poschke I., Mougiakakos D., Kiessling R. Camouflage and sabotage: tumor escape from the immune system. Cancer Immunol Immunother 2011, 60:1161-1171.
18. Vyas J.M., Van der Veen A.G., Ploegh H.L. The known unknowns of antigen processing and presentation. Nat Rev Immunol 2008, 8:607-618.
19. Zhang N., Bevan M.J. CD8(+) T cells: foot soldiers of the immune system. Immunity 2011, 35:161-168.
20. Seidel U.J., Oliveira C.C., Lampen M.H., Hall T. A novel category of antigens enabling CTL immunity to tumor escape variants: cinderella antigens. Cancer Immunol Immunother 2012, 61:119-125.
21. Seliger B., Maeurer M.J., Ferrone S. TAP off - tumors on. Immunol Today 1997, 18:292-299.
22. Groothuis T.A., Griekspoor A.C., Neijssen J.J., Herberts C.A., Neefjes J.J. MHC class I alleles and their exploration of the antigen-processing machinery. Immunol Rev 2005, 207:60-76.
23. Neefjes J., Jongsma M.L., Paul P., Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol 2011, 11:823-836.
24. Nitta T., Murata S., Sasaki K., Fujii H., Ripen A.M., Ishimaru N., et al. Thymoproteasome shapes immunocompetent repertoire of CD8+ T cells. Immunity 2010, 32:29-40.
25. Saunders P.M., van Endert P. Running the gauntlet: from peptide generation to antigen presentation by MHC class I. Tissue Antigens 2011, 78:161-170.
26. Scholz C., Tampe R. The peptide-loading complex - antigen translocation and MHC class I loading. Biol Chem 2009, 390:783-794.
27. Wearsch P.A., Cresswell P. Selective loading of high-affinity peptides onto major histocompatibility complex class I molecules by the tapasin-ERp57 heterodimer. Nat Immunol 2007, 8:873-881.
28. Yewdell J.W. DRiPs solidify: progress in understanding endogenous MHC class I antigen processing. Trends Immunol 2011, 32:548-558.
29. de Graaf N., van Helden M.J., Textoris-Taube K., Chiba T., Topham D.J., Kloetzel P.M., et al. PA28 and the proteasome immunosubunits play a central and independent role in the production of MHC class I-binding peptides in vivo. Eur J Immunol 2011, 41:926-935.
30. Sijts E.J., Kloetzel P.M. The role of the proteasome in the generation of MHC class I ligands and immune responses. Cell Mol Life Sci 2011, 68:1491-1502.
31. van Endert P. Post-proteasomal and proteasome-independent generation of MHC class I ligands. Cell Mol Life Sci 2011, 68:1553-1567.
32. Vigneron N., Van den Eynde B.J. Insights into the processing of MHC class I ligands gained from the study of human tumor epitopes. Cell Mol Life Sci 2011, 68:1503-1520.
33. Evans C., Dalgleish A.G., Kumar D. Review article: immune suppression and colorectal cancer. Aliment Pharmacol Ther 2006, 24:1163-1177.
34. Cathro H.P., Smolkin M.E., Theodorescu D., Jo V.Y., Ferrone S., Frierson H.F. Relationship between HLA class I antigen processing machinery component expression and the clinicopathologic characteristics of bladder carcinomas. Cancer Immunol Immunother 2010, 59:465-472.
35. Geertsen R., Boni R., Blasczyk R., Romero P., Betts D., Rimoldi D., et al. Loss of single HLA class I allospecificities in melanoma cells due to selective genomic abbreviations. Int J Cancer 2002, 99:82-87.
36. Maleno I., Aptsiauri N., Cabrera T., Gallego A., Paschen A., Lopez-Nevot M.A., et al. Frequent loss of heterozygosity in the beta2-microglobulin region of chromosome 15 in primary human tumors. Immunogenetics 2011, 63:65-71.
37. Garrido C., Romero I., Berruguilla E., Cancela B., Algarra I., Collado A., et al. Immunotherapy eradicates metastases with reversible defects in MHC class I expression. Cancer Immunol Immunother 2011, 60:1257-1268.
38. Kasajima A., Sers C., Sasano H., Johrens K., Stenzinger A., Noske A., et al. Down-regulation of the antigen processing machinery is linked to a loss of inflammatory response in colorectal cancer. Hum Pathol 2010, 41:1758-1769.
39. Lampen M.H., van Hall T. Strategies to counteract MHC-I defects in tumors. Curr Opin Immunol 2011, 23:293-298.
40. Reinis M. Immunotherapy of MHC class I-deficient tumors. Future Oncol 2010, 6:1577-1589.
41. Hansen T.H., Bouvier M. MHC class I antigen presentation: learning from viral evasion strategies. Nat Rev Immunol 2009, 9:503-513.
42. Fruci D., Benevolo M., Cifaldi L., Lorenzi S., Lo Monaco E., Tremante E., et al. Major histocompatibility complex class i and tumour immuno-evasion: how to fool T cells and natural killer cells at one time. Curr Oncol 2012, 19:39-41.
43. Peters H.L., Tuli A., Sharma M., Naslavsky N., Caplan S., MacDonald R.G., et al. Regulation of major histocompatibility complex class I molecule expression on cancer cells by amyloid precursor-like protein 2. Immunol Res 2011, 51:39-44.
44. Seliger B. Molecular mechanisms of MHC class I abnormalities and APM components in human tumors. Cancer Immunol Immunother 2008, 57:1719-1726.
45. Hirata T., Yamamoto H., Taniguchi H., Horiuchi S., Oki M., Adachi Y., et al. Characterization of the immune escape phenotype of human gastric cancers with and without high-frequency microsatellite instability. J Pathol 2007, 211:516-523.
46. Kloor M., Michel S., Buckowitz B., Ruschoff J., Buttner R., Holinski-Feder E., et al. Beta2-microglobulin mutations in microsatellite unstable colorectal tumors. Int J Cancer 2007, 121:454-458.
47. Kloor M., Michel S., von Knebel Doeberitz M. Immune evasion of microsatellite unstable colorectal cancers. Int J Cancer 2010, 127:1001-1010.
48. Hodson I., Bock M., Ritz U., Brenner W., Huber C., Seliger B. Analysis of the structural integrity of the TAP2 gene in renal cell carcinoma. Int J Oncol 2003, 23:991-999.
49. Campo M.S., Graham S.V., Cortese M.S., Ashrafi G.H., Araibi E.H., Dornan E.S., et al. HPV-16 E5 down-regulates expression of surface HLA class I and reduces recognition by CD8 T cells. Virology 2010, 407:137-142.
50. Chuang L.C., Hu C.Y., Chen H.C., Lin P.J., Lee B., Lin C.Y., et al. Associations of human leukocyte antigen class II genotypes with human papillomavirus 18 infection and cervical intraepithelial neoplasia risk. Cancer 2012, 118:223-231.
51. Deshpande A., Wheeler C.M., Hunt W.C., Peyton C.L., White P.S., Valdez Y.E., et al. Variation in HLA class I antigen-processing genes and susceptibility to human papillomavirus type 16-associated cervical cancer. J Infect Dis 2008, 197:371-381.
52. Rodriguez J.A., Galeano L., Palacios D.M., Gomez C., Serrano M.L., Bravo M.M., et al. Altered HLA class I and HLA-G expression is associated with IL-10 expression in patients with cervical cancer. Pathobiology 2012, 79:72-83.
53. Sers C., Kuner R., Falk C.S., Lund P., Sueltmann H., Braun M., et al. Down-regulation of HLA class I and NKG2D ligands through a concerted action of MAPK and DNA methyltransferases in colorectal cancer cells. Int J Cancer 2009, 125:1626-1639.
54. Setiadi A.F., Omilusik K., David M.D., Seipp R.P., Hartikainen J., Gopaul R., et al. Epigenetic enhancement of antigen processing and presentation promotes immune recognition of tumors. Cancer Res 2008, 68:9601-9607.
55. Ye Q., Shen Y., Wang X., Yang J., Miao F., Shen C., et al. Hypermethylation of HLA class I gene is associated with HLA class I down-regulation in human gastric cancer. Tissue Antigens 2010, 75:30-39.
56. Bao L., Dunham K., Lucas K. MAGE-A1, MAGE-A3, and NY-ESO-1 can be upregulated on neuroblastoma cells to facilitate cytotoxic T lymphocyte-mediated tumor cell killing. Cancer Immunol Immunother 2011, 60:1299-1307.
57. Del Campo A.B., Carretero J., Aptsiauri N., Garrido F. Targeting HLA class I expression to increase tumor immunogenicity. Tissue Antigens 2012, 79:147-154.
58. Yan M., Himoudi N., Basu B.P., Wallace R., Poon E., Adams S., et al. Increased PRAME antigen-specific killing of malignant cell lines by low avidity CTL following treatment with 5-Aza-2'-deoxycytidine. Cancer Immunol Immunother 2011, 60:1243-1255.
59. Fonsatti E., Nicolay H.J., Sigalotti L., Calabro L., Pezzani L., Colizzi F., et al. Functional up-regulation of human leukocyte antigen class I antigens expression by 5-aza-2'-deoxycytidine in cutaneous melanoma: immunotherapeutic implications. Clin Cancer Res 2007, 13:3333-3338.
60. Khan A.N., Gregorie C.J., Tomasi T.B. Histone deacetylase inhibitors induce TAP, LMP, Tapasin genes and MHC class I antigen presentation by melanoma cells. Cancer Immunol Immunother 2008, 57:647-654.
61. Kitamura H., Torigoe T., Asanuma H., Honma I., Sato N., Tsukamoto T. Down-regulation of HLA class I antigens in prostate cancer tissues and up-regulation by histone deacetylase inhibition. J Urol 2007, 178:692-696.
62. Bukur J., Herrmann F., Handke D., Recktenwald C., Seliger B. Identification of E2F1 as an important transcription factor for the regulation of tapasin expression. J Biol Chem 2010, 285:30419-30426.
63. Herrmann F., Lehr H.A., Drexler I., Sutter G., Hengstler J., Wollscheid U., et al. HER-2/neu-mediated regulation of components of the MHC class I antigen-processing pathway. Cancer Res 2004, 64:215-220.
64. Doody G.M., Stephenson S., McManamy C., Tooze R.M. PRDM1/BLIMP-1 modulates IFN-gamma-dependent control of the MHC class I antigen-processing and peptide-loading pathway. J Immunol 2007, 179:7614-7623.
65. Seliger B. Novel insights into the molecular mechanisms of HLA class I abnormalities. Cancer Immunol Immunother 2012, 61:249-254.
66. Carretero R., Wang E., Rodriguez A.I., Reinboth J., Ascierto M.L., Engle A.M., et al. Regression of melanoma metastases after immunotherapy is associated with activation of antigen presentation and interferon-mediated rejection genes. Int J Cancer 2011.
67. Liu X., Ye L., Bai Y., Mojidi H., Simister N.E., Zhu X. Activation of the JAK/STAT-1 signaling pathway by IFN-gamma can down-regulate functional expression of the MHC class I-related neonatal Fc receptor for IgG. J Immunol 2008, 181:449-463.
68. Respa A., Bukur J., Ferrone S., Pawelec G., Zhao Y., Wang E., et al. Association of IFN-gamma signal transduction defects with impaired HLA class I antigen processing in melanoma cell lines. Clin Cancer Res 2011, 17:2668-2678.
69. Zhou F. Molecular mechanisms of IFN-gamma to up-regulate MHC class I antigen processing and presentation. Int Rev Immunol 2009, 28:239-260.
70. Geldmacher A., Freier A., Losch F.O., Walden P. Therapeutic vaccination for cancer immunotherapy: antigen selection and clinical responses. Hum Vaccine 2011, 7(Suppl.):115-119.
71. Rosenberg S.A., Dudley M.E. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol 2009, 21:233-240.
72. del Campo A.B., Aptsiauri N., Mendez R., Zinchenko S., Vales A., Paschen A., et al. Efficient recovery of HLA class I expression in human tumor cells after beta2-microglobulin gene transfer using adenoviral vector: implications for cancer immunotherapy. Scand J Immunol 2009, 70:125-135.
73. Qin Z., Harders C., Cao X., Huber C., Blankenstein T., Seliger B. Increased tumorigenicity, but unchanged immunogenicity, of transporter for antigen presentation 1-deficient tumors. Cancer Res 2002, 62:2856-2860.
74. Tanaka K., Isselbacher K.J., Khoury G., Jay G. Reversal of oncogenesis by the expression of a major histocompatibility complex class I gene. Science 1985, 228:26-30.
75. Wallich R., Bulbuc N., Hammerling G.J., Katzav S., Segal S., Feldman M. Abrogation of metastatic properties of tumour cells by de novo expression of H-2K antigens following H-2 gene transfection. Nature 1985, 315:301-305.
76. Carosella E.D. The tolerogenic molecule HLA-G. Immunol Lett 2011, 138:22-24.
77. Yan W.H. Human leukocyte antigen-G in cancer: are they clinically relevant?. Cancer Lett 2011, 311:123-130.
78. Zidi I., Ben Amor N. HLA-G regulators in cancer medicine: an outline of key requirements. Tumour Biol 2011, 32:1071-1086.
79. Castelli E.C., Moreau P., Oya e Chiromatzo A., Mendes-Junior C.T., Veiga-Castelli L.C., Yaghi L., et al. In silico analysis of microRNAS targeting the HLA-G 3'-untranslated region alleles and haplotypes. Hum Immunol 2009, 70:1020-1025.
80. Menier C., Rouas-Freiss N., Favier B., LeMaoult J., Moreau P., Carosella E.D. Recent advances on the non-classical major histocompatibility complex class I HLA-G molecule. Tissue Antigens 2010, 75:201-206.
81. Carosella E.D., Favier B., Rouas-Freiss N., Moreau P., Lemaoult J. Beyond the increasing complexity of the immunomodulatory HLA-G molecule. Blood 2008, 111:4862-4870.
82. Kaiser B.K., Pizarro J.C., Kerns J., Strong R.K. Structural basis for NKG2A/CD94 recognition of HLA-E. Proc Natl Acad Sci USA 2008, 105:6696-6701.
83. Ishitani A., Sageshima N., Hatake K. The involvement of HLA-E and -F in pregnancy. J Reprod Immunol 2006, 69:101-113.
84. Lepin E.J., Bastin J.M., Allan D.S., Roncador G., Braud V.M., Mason D.Y., et al. Functional characterization of HLA-F and binding of HLA-F tetramers to ILT2 and ILT4 receptors. Eur J Immunol 2000, 30:3552-3561.
85. Lin A., Zhang X., Zhou W.J., Ruan Y.Y., Xu D.P., Wang Q., et al. Human leukocyte antigen-G expression is associated with a poor prognosis in patients with esophageal squamous cell carcinoma. Int J Cancer 2011, 129:1382-1390.
86. Silva T.G., Crispim J.C., Miranda F.A., Hassumi M.K., de Mello J.M., Simoes R.T., et al. Expression of the nonclassical HLA-G and HLA-E molecules in laryngeal lesions as biomarkers of tumor invasiveness. Histol Histopathol 2011, 26:1487-1497.
87. Yie S.M., Hu Z. Human leukocyte antigen-G (HLA-G) as a marker for diagnosis, prognosis and tumor immune escape in human malignancies. Histol Histopathol 2011, 26:409-420.
88. de Kruijf E.M., Sajet A., van Nes J.G., Natanov R., Putter H., Smit V.T., 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, 185:7452-7459.
89. Donadi E.A., Castelli E.C., Arnaiz-Villena A., Roger M., Rey D., Moreau P. Implications of the polymorphism of HLA-G on its function, regulation, evolution and disease association. Cell Mol Life Sci 2011, 68:369-395.
90. Ferguson R., Ramanakumar A.V., Koushik A., Coutlee F., Franco E., Roger M. Human leukocyte antigen G polymorphism is associated with an increased risk of invasive cancer of the uterine cervix. Int J Cancer 2011.
91. Cao M., Yie S.M., Liu J., Ye S.R., Xia D., Gao E. Plasma soluble HLA-G is a potential biomarker for diagnosis of colorectal, gastric, esophageal and lung cancer. Tissue Antigens 2011, 78:120-128.
92. Guo Q.Y., Chen B.G., Ruan Y.Y., Lin A., Yan W.H. HLA-G expression is irrelevant to prognosis in patients with acute myeloid leukemia. Leuk Res 2011, 35:1350-1354.
93. Coupel S., Moreau A., Hamidou M., Horejsi V., Soulillou J.P., Charreau B. Expression and release of soluble HLA-E is an immunoregulatory feature of endothelial cell activation. Blood 2007, 109:2806-2814.
94. Lin A., Zhang X., Ruan Y.Y., Wang Q., Zhou W.J., Yan W.H. HLA-F expression is a prognostic factor in patients with non-small-cell lung cancer. Lung Cancer 2011, 74:504-509.
95. Diaz-Lagares A., Alegre E., LeMaoult J., Carosella E.D., Gonzalez A. Nitric oxide produces HLA-G nitration and induces metalloprotease-dependent shedding creating a tolerogenic milieu. Immunology 2009, 126:436-445.
96. Flajollet S., Poras I., Carosella E.D., Moreau P. RREB-1 is a transcriptional repressor of HLA-G. J Immunol 2009, 183:6948-6959.
97. Agaugue S., Carosella E.D., Rouas-Freiss N. 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 2011, 117:7021-7031.
98. Amiot L., Ferrone S., Grosse-Wilde H., Seliger B. Biology of HLA-G in cancer: a candidate molecule for therapeutic intervention. Cell Mol Life Sci 2011, 68:417-431.
99. Morandi F., Ferretti E., Bocca P., Prigione I., Raffaghello L., Pistoia V. A novel mechanism of soluble HLA-G mediated immune modulation: downregulation of T cell chemokine receptor expression and impairment of chemotaxis. PLoS One 2010, 5:e11763.
100. Gooden M., Lampen M., Jordanova E.S., Leffers N., Trimbos J.B., van der Burg S.H., et al. HLA-E expression by gynecological cancers restrains tumor-infiltrating CD8 T lymphocytes. Proc Natl Acad Sci USA 2011, 108:10656-10661.
101. Morandi F., Ferretti E., Castriconi R., Dondero A., Petretto A., Bottino C., 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 2011, 118:5840-5850.
102. Vitale M., Rezzani R., Rodella L., Zauli G., Grigolato P., Cadei M., et al. HLA class I antigen and transporter associated with antigen processing (TAP1 and TAP2) down-regulation in high-grade primary breast carcinoma lesions. Cancer Res 1998, 58:737-742.
103. Mehta A.M., Jordanova E.S., Kenter G.G., Ferrone S., Fleuren G.J. Association of antigen processing machinery and HLA class I defects with clinicopathological outcome in cervical carcinoma. Cancer Immunol Immunother 2008, 57:197-206.
104. Atkins D., Breuckmann A., Schmahl G.E., Binner P., Ferrone S., Krummenauer F., et al. MHC class I antigen processing pathway defects, ras mutations and disease stage in colorectal carcinoma. Int J Cancer 2004, 109:265-273.
105. Ayshamgul H., Ma H., Ilyar S., Zhang L.W., Abulizi A. Association of defective HLA-I expression with antigen processing machinery and their association with clinicopathological characteristics in Kazak patients with esophageal cancer. Chin Med J (Engl) 2011, 124:341-346.
106. Tan L.F., Wang F., Chao H., Zhou Y.F., Weng C. Ruthenium(II) mixed-ligand complex containing 2-(4'-benzyloxy-phenyl)imidazo[4,5-f][1,10]phenanthroline: synthesis, DNA-binding and photocleavage studies. J Inorg Biochem 2007, 101:700-708.
107. Ogino T., Shigyo H., Ishii H., Katayama A., Miyokawa N., Harabuchi Y., et al. HLA class I antigen down-regulation in primary laryngeal squamous cell carcinoma lesions as a poor prognostic marker. Cancer Res 2006, 66:9281-9289.
108. Kageshita T., Hirai S., Ono T., Hicklin D.J., Ferrone S. Down-regulation of HLA class I antigen-processing molecules in malignant melanoma: association with disease progression. Am J Pathol 1999, 154:745-754.
109. Racanelli V., Leone P., Frassanito M.A., Brunetti C., Perosa F., Ferrone S., et al. Alterations in the antigen processing-presenting machinery of transformed plasma cells are associated with reduced recognition by CD8+ T cells and characterize the progression of MGUS to multiple myeloma. Blood 2010, 115:1185-1193.
110. Ramnath N., Tan D., Li Q., Hylander B.L., Bogner P., Ryes L., et al. Is downregulation of MHC class I antigen expression in human non-small cell lung cancer associated with prolonged survival. Cancer Immunol Immunother 2006, 55:891-899.
111. Han L.Y., Fletcher M.S., Urbauer D.L., Mueller P., Landen C.N., Kamat A.A., et al. HLA class I antigen processing machinery component expression and intratumoral T-cell infiltrate as independent prognostic markers in ovarian carcinoma. Clin Cancer Res 2008, 14:3372-3379.
112. Seliger B., Atkins D., Bock M., Ritz U., Ferrone S., Huber C., et al. Characterization of human lymphocyte antigen class I antigen-processing machinery defects in renal cell carcinoma lesions with special emphasis on transporter-associated with antigen-processing down-regulation. Clin Cancer Res 2003, 9:1721-1727.
113. Esteban F., Concha A., Delgado M., Perez-Ayala M., Ruiz-Cabello F., Garrido F. Lack of MHC class I antigens and tumour aggressiveness of the squamous cell carcinoma of the larynx. Br J Cancer 1990, 62:1047-1051.
114. Meissner M., Reichert T.E., Kunkel M., Gooding W., Whiteside T.L., Ferrone S., et al. Defects in the human leukocyte antigen class I antigen processing machinery in head and neck squamous cell carcinoma: association with clinical outcome. Clin Cancer Res 2005, 11:2552-2560.
115. Tang Q., Zhang J., Qi B., Shen C., Xie W. Downregulation of HLA class I molecules in primary oral squamous cell carcinomas and cell lines. Arch Med Res 2009, 40:256-263.
116. Weinman E.C., Roche P.C., Kasperbauer J.L., Cha S.S., Sargent D.J., Cheville J., et al. Characterization of antigen processing machinery and Survivin expression in tonsillar squamous cell carcinoma. Cancer 2003, 97:2203-2211.
117. Nuckel H., Rebmann V., Durig J., Duhrsen U., Grosse-Wilde H. HLA-G expression is associated with an unfavorable outcome and immunodeficiency in chronic lymphocytic leukemia. Blood 2005, 105:1694-1698.
118. Gan L.H., Huang L.F., Zhang X., Lin A., Xu D.P., Wang Q., et al. Tumor-specific upregulation of human leukocyte antigen-G expression in bladder transitional cell carcinoma. Hum Immunol 2010, 71:899-904.
119. He X., Dong D.D., Yie S.M., Yang H., Cao M., Ye S.R., 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. Ann Surg Oncol 2010, 17:1459-1469.
120. Sayed D., Badr G., Maximous D., Mikhail N.N., Abu-Tarboush F., Alhazza I.M. HLA-G and its relation to proliferation index in detection and monitoring breast cancer patients. Tissue Antigens 2010, 75:40-47.
121. Singer G., Rebmann V., Chen Y.C., Liu H.T., Ali S.Z., Reinsberg J., et al. HLA-G is a potential tumor marker in malignant ascites. Clin Cancer Res 2003, 9:4460-4464.
122. Zheng N., Wang C.X., Zhang X., Du L.T., Zhang J., Kan S.F., et al. Up-regulation of HLA-G expression in cervical premalignant and malignant lesions. Tissue Antigens 2011, 77:218-224.
123. Zhu C.B., Wang C.X., Zhang X., Zhang J., Li W. Serum sHLA-G levels: a useful indicator in distinguishing colorectal cancer from benign colorectal diseases. Int J Cancer 2011, 128:617-622.
124. 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, 31:129-134.
125. Diepstra A., Poppema S., Boot M., Visser L., Nolte I.M., Niens M., et al. HLA-G protein expression as a potential immune escape mechanism in classical Hodgkin's lymphoma. Tissue Antigens 2008, 71:219-226.
126. Schutt P., Schutt B., Switala M., Bauer S., Stamatis G., Opalka B., et al. Prognostic relevance of soluble human leukocyte antigen-G and total human leukocyte antigen class I molecules in lung cancer patients. Hum Immunol 2010, 71:489-495.
127. Bukur J., Rebmann V., Grosse-Wilde H., Luboldt H., Ruebben H., Drexler I., et al. Functional role of human leukocyte antigen-G up-regulation in renal cell carcinoma. Cancer Res 2003, 63:4107-4111.
128. Li B.L., Lin A., Zhang X.J., Zhang X., Zhang J.G., Wang Q., et al. Characterization of HLA-G expression in renal cell carcinoma. Tissue Antigens 2009, 74:213-221.
129. Kalhor N., Ramirez P.T., Deavers M.T., Malpica A., Silva E.G. Immunohistochemical studies of trophoblastic tumors. Am J Surg Pathol 2009, 33:633-638.