HLA-E expression and its clinical relevance in human renal cell carcinoma

Oncotarget

Volumn 7, Issue 41, 2016, Pages 67360-67372

  Seliger, Barbara ^a   Jasinski Bergner, Simon ^a   Quandt, Dagmar ^a   Stoehr, Christine ^b   Bukur, Juergen ^a   Wach, Sven ^b   Legal, Wolfgang ^b   Taubert, Helge ^b   Wullich, Bernd ^b   Hartmann, Arndt ^b  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

HLA E; Immune escape; Non classical HLA class I; Renal cell carcinoma; Tumor progression

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; HLA E ANTIGEN; HLA G ANTIGEN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY TFL 033; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 1; HLA-E ANTIGEN;

ANTIGEN ANTIBODY REACTION; ANTIGEN EXPRESSION; ARTICLE; CANCER SURVIVAL; CELL INFILTRATION; CONTROLLED STUDY; CYTOTOXICITY TEST; DISEASE ASSOCIATION; EMBRYO; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KIDNEY CARCINOMA; KIDNEY EPITHELIUM; TISSUE MICROARRAY; BIOSYNTHESIS; IMMUNOLOGY; KIDNEY TUMOR; RENAL CELL CARCINOMA; TUMOR CELL LINE; TUMOR ESCAPE;

CARCINOMA, RENAL CELL; CELL LINE, TUMOR; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; KIDNEY NEOPLASMS; TUMOR ESCAPE;

EID: 84993969547     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.11744     Document Type: Article

References (55)

1. Cavallo F, De Giovanni C, Nanni P, Forni G, Lollini PL. 2011: the immune hallmarks of cancer. Cancer Immunol Immunother. 2011; 60:319-326.
2. Gong F, Song S, Lv G, Pan Y, Zhang D, Jiang H. Human leukocyte antigen E in human cytomegalovirus infection: friend or foe? Acta Biochim Biophys Sin (Shanghai). 2012; 44:551-554.
3. Bukur J, Jasinski S, Seliger B. The role of classical and non-classical HLA class I antigens in human tumors. Semin Cancer Biol. 2012; 22:350-358.
4. Braud VM, Allan DS, O'Callaghan CA, Soderstrom K, D'Andrea A, Ogg GS, Lazetic S, Young NT, Bell JI, Phillips JH, Lanier LL, McMichael AJ. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature. 1998; 391:795-799.
5. Speiser DE, Valmori D, Rimoldi D, Pittet MJ, Lienard D, Cerundolo V, MacDonald HR, Cerottini JC, Romero P. CD28-negative cytolytic effector T cells frequently express NK receptors and are present at variable proportions in circulating lymphocytes from healthy donors and melanoma patients. European journal of immunology. 1999; 29:1990-1999.
6. Braud VM, Aldemir H, Breart B, Ferlin WG. Expression of CD94-NKG2A inhibitory receptor is restricted to a subset of CD8+ T cells. Trends Immunol. 2003; 24:162-164.
7. Derre L, Corvaisier M, Charreau B, Moreau A, Godefroy E, Moreau-Aubry A, Jotereau F, Gervois N. Expression and release of HLA-E by melanoma cells and melanocytes: potential impact on the response of cytotoxic effector cells. J Immunol. 2006; 177:3100-3107.
8. Rizzo R, Trentini A, Bortolotti D, Manfrinato MC, Rotola A, Castellazzi M, Melchiorri L, Di Luca D, Dallocchio F, Fainardi E, Bellini T. Matrix metalloproteinase-2 (MMP-2) generates soluble HLA-G1 by cell surface proteolytic shedding. Mol Cell Biochem. 2013; 381:243-255.
9. Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequencederived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. Journal of Experimental Medicine. 1998; 187:813-818.
10. Lee N, Goodlett DR, Ishitani A, Marquardt H, Geraghty DE. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J Immunol. 1998; 160:4951-4960.
11. Andersson E, Poschke I, Villabona L, Carlson JW, Lundqvist A, Kiessling R, Seliger B, Masucci GV. Nonclassical HLA-class I expression in serous ovarian carcinoma: Correlation with the HLA-genotype, tumor infiltrating immune cells and prognosis. Oncoimmunology. 2016; 5:e1052213.
12. Palmisano GL, Contardi E, Morabito A, Gargaglione V, Ferrara GB, Pistillo MP. HLA-E surface expression is independent of the availability of HLA class I signal sequence-derived peptides in human tumor cell lines. Hum Immunol. 2005; 66:1-12.
13. Teklemariam T, Zhao L, Hantash BM. Full-length HLAG1 and truncated HLA-G3 differentially increase HLA-E surface localization. Hum Immunol. 2012; 73:898-905.
14. Silva TG, Crispim JC, Miranda FA, Hassumi MK, de Mello JM, Simoes RT, Souto F, Soares EG, Donadi EA, Soares CP. Expression of the nonclassical HLA-G, HLA-E molecules in laryngeal lesions as biomarkers of tumor invasiveness. Histol Histopathol. 2011; 26:1487-1497.
15. de Kruijf EM, Sajet A, van Nes JG, Natanov R, Putter H, Smit VT, Liefers GJ, van den Elsen PJ, van de Velde CJ, Kuppen PJ. 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.
16. Talebian Yazdi M, van Riet S, van Schadewijk A, Fiocco M, van Hall T, Taube C, Hiemstra PS, van der Burg SH. The positive prognostic effect of stromal CD8+ tumorinfiltrating T cells is restrained by the expression of HLA-E in non-small cell lung carcinoma. Oncotarget. 2016; 7:3477-3488. doi: 10.18632/oncotarget.6506.
17. Hiraoka N, Onozato K, Kosuge T, Hirohashi S. Prevalence of FOXP3+ regulatory T cells increases during the progression of pancreatic ductal adenocarcinoma and its premalignant lesions. Clin Cancer Res. 2006; 12:5423-5434.
18. Guo ZY, Lv YG, Wang L, Shi SJ, Yang F, Zheng GX, Wen WH, Yang AG. Predictive value of HLA-G and HLA-E in the prognosis of colorectal cancer patients. Cell Immunol. 2015; 293:10-16.
19. Zhen ZJ, Ling JY, Cai Y, Luo WB, He YJ. Impact of HLA-E gene polymorphism on HLA-E expression in tumor cells and prognosis in patients with stage III colorectal cancer. Med Oncol. 2013; 30:482.
20. Lo Monaco E, Tremante E, Cerboni C, Melucci E, Sibilio L, Zingoni A, Nicotra MR, Natali PG, Giacomini P. Human leukocyte antigen E contributes to protect tumor cells from lysis by natural killer cells. Neoplasia. 2011; 13:822-830.
21. Nguyen S, Beziat V, Dhedin N, Kuentz M, Vernant JP, Debre P, Vieillard V. HLA-E upregulation on IFN-gammaactivated AML blasts impairs CD94/NKG2A-dependent NK cytolysis after haplo-mismatched hematopoietic SCT. Bone Marrow Transplant. 2009; 43:693-699.
22. Tremante E, Lo Monaco E, Ingegnere T, Sampaoli C, Fraioli R, Giacomini P. Monoclonal antibodies to HLA-E bind epitopes carried by unfolded beta2 m-free heavy chains. European journal of immunology. 2015; 45:2356-2364.
23. Jucaud V, Ravindranath MH, Terasaki PI. Immunobiology of HLA Class-Ib Molecules in Transplantation. SOJ Immunol 2015; 3: 1-15.
24. Sasaki T, Ravindranath MH, Terasaki PI, Freitas MC, Kawakita S, Jucaud V. Gastric cancer progression may involve a shift in HLA-E profile from an intact heterodimer to beta2-microglobulin-free monomer. Int J Cancer. 2014; 734:558-570.
25. Ravindranath MH, Terasaki PI, Pham T, Jucaud V. The Monospecificity of Novel Anti-HLA-E Monoclonal Antibodies Enables Reliable Immunodiagnosis, Immunomodulation of HLA-E, and Upregulation of CD8+ T Lymphocytes. Monoclon Antib Immunodiagn Immunother. 2015; 34:135-153.
26. Dunker K, Schlaf G, Bukur J, Altermann WW, Handke D, Seliger B. Expression and regulation of non-classical HLA-G in renal cell carcinoma. Tissue antigens. 2008; 72:137-148.
27. Jasinski-Bergner S, Stoehr C, Bukur J, Massa C, Braun J, Huttelmaier S, Spath V, Wartenberg R, Legal W, Taubert H, Wach S, Wullich B, Hartmann A, Seliger B. Clinical relevance of miR-mediated HLA-G regulation and the associated immune cell infiltration in renal cell carcinoma. Oncoimmunology. 2015; 4:e1008805.
28. Kren L, Valkovsky I, Dolezel J, Capak I, Pacik D, Poprach A, Lakomy R, Redova M, Fabian P, Krenova Z, Slaby O. HLA-G and HLA-E specific mRNAs connote opposite prognostic significance in renal cell carcinoma. Diagn Pathol. 2012; 7:58-60.
29. Reimers MS, Engels CC, Putter H, Morreau H, Liefers GJ, van de Velde CJ, Kuppen PJ. Prognostic value of HLA class I, HLA-E, HLA-G and Tregs in rectal cancer: a retrospective cohort study. BMC Cancer. 2014; 14:486-498.
30. Zeestraten EC, Reimers MS, Saadatmand S, Goossens-Beumer IJ, Dekker JW, Liefers GJ, van den Elsen PJ, van de Velde CJ, Kuppen PJ. Combined analysis of HLA class I, HLA-E and HLA-G predicts prognosis in colon cancer patients. Br J Cancer. 2014; 111:2459-2468.
31. Kong XF, Vogt G, Chapgier A, Lamaze C, Bustamante J, Prando C, Fortin A, Puel A, Feinberg J, Zhang XX, Gonnord P, Pihkala-Saarinen UM, Arola M, Moilanen P, Abel L, Korppi M, et al. A novel form of cell type-specific partial IFN-gammaR1 deficiency caused by a germ line mutation of the IFNGR1 initiation codon. Hum Mol Genet. 2010; 19:434-444.
32. Seliger B, Dunn T, Schwenzer A, Casper J, Huber C, Schmoll HJ. Analysis of the MHC class I antigen presentation machinery in human embryonal carcinomas: evidence for deficiencies in TAP, LMP and MHC class I expression and their upregulation by IFN-gamma. Scandinavian journal of immunology. 1997; 46:625-632.
33. Li BL, Lin A, Zhang XJ, Zhang X, Zhang JG, Wang Q, Zhou WJ, Chen HX, Wang TJ, Yan WH. Characterization of HLA-G expression in renal cell carcinoma. Tissue antigens. 2009; 74:213-221.
34. Atkins D, Ferrone S, Schmahl GE, Storkel S, Seliger B. Down-regulation of HLA class I antigen processing molecules: an immune escape mechanism of renal cell carcinoma? J Urol. 2004; 171:885-889.
35. Dovhey SE, Ghosh NS, Wright KL. Loss of interferongamma inducibility of TAP1 and LMP2 in a renal cell carcinoma cell line. Cancer Res. 2000; 60:5789-5796.
36. Zhang Q, Zhang L, Li L, Wang Z, Ying J, Fan Y, Xu B, Wang L, Liu Q, Chen G, Tao Q, Jin J. Interferon regulatory factor 8 functions as a tumor suppressor in renal cell carcinoma and its promoter methylation is associated with patient poor prognosis. Cancer Lett. 2014; 354:227-234.
37. Geissler K, Fornara P, Lautenschlager C, Holzhausen HJ, Seliger B, Riemann D. Immune signature of tumor infiltrating immune cells in renal cancer. Oncoimmunology. 2015; 4:e985082.
38. Hase S, Weinitschke K, Fischer K, Fornara P, Hoda R, Unverzagt S, Seliger B, Riemann D. Monitoring perioperative immune suppression in renal cancer patients. Oncol Rep. 2011; 25:1455-1464.
39. Lindau D, Gielen P, Kroesen M, Wesseling P, Adema GJ. The immunosuppressive tumour network: myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology. 2013; 138:105-115.
40. Whiteside TL. Clinical Impact of Regulatory T cells (Treg) in Cancer and HIV. Cancer Microenviron. 2015; 8:201-207.
41. Celik AA, Kraemer T, Huyton T, Blasczyk R, Bade-Doding C. The diversity of the HLA-E-restricted peptide repertoire explains the immunological impact of the Arg107Gly mismatch. Immunogenetics. 2016; 68:29-41.
42. Lauterbach N, Wieten L, Popeijus HE, Vanderlocht J, van Zon PM, Voorter CE, Tilanus MG. Peptide-induced HLA-E expression in human PBMCs is dependent on peptide sequence and the HLA-E genotype. Tissue antigens. 2015; 85:242-251.
43. Carosella ED, Gregori S, LeMaoult J. The tolerogenic interplay(s) among HLA-G, myeloid APCs, and regulatory cells. Blood. 2011; 118:6499-6505.
44. Andersen R, Donia M, Westergaard MC, Pedersen M, Hansen M, Svane IM. Tumor infiltrating lymphocyte therapy for ovarian cancer and renal cell carcinoma. Hum Vaccin Immunother. 2015; 11:2790-2795.
45. Cohen J, Sznol M. Therapeutic combinations of immunemodulating antibodies in melanoma and beyond. Semin Oncol. 2015; 42:488-494.
46. Combe P, de Guillebon E, Thibault C, Granier C, Tartour E, Oudard S. Trial Watch: Therapeutic vaccines in metastatic renal cell carcinoma. Oncoimmunology. 2015; 4:e1001236.
47. Menon AG, Morreau H, Tollenaar RA, Alphenaar E, Van Puijenbroek M, Putter H, Janssen-Van Rhijn CM, Van De Velde CJ, Fleuren GJ, Kuppen PJ. Down-regulation of HLA-A expression correlates with a better prognosis in colorectal cancer patients. Lab Invest. 2002; 82:1725-1733.
48. Watson NF, Ramage JM, Madjd Z, Spendlove I, Ellis IO, Scholefield JH, Durrant LG. Immunosurveillance is active in colorectal cancer as downregulation but not complete loss of MHC class I expression correlates with a poor prognosis. Int J Cancer. 2006; 118:6-10.
49. Bukur J, Rebmann V, Grosse-Wilde H, Luboldt H, Ruebben H, Drexler I, Sutter G, Huber C, Seliger B. Functional role of human leukocyte antigen-G up-regulation in renal cell carcinoma. Cancer Res. 2003; 63:4107-4111.
50. Quandt D, Jasinski-Bergner S, Muller U, Schulze B, Seliger B. Synergistic effects of IL-4 and TNFalpha on the induction of B7-H1 in renal cell carcinoma cells inhibiting allogeneic T cell proliferation. J Transl Med. 2014; 12:151.
51. Real LM, Cabrera T, Collado A, Jimenez P, Garcia A, Ruiz-Cabello F, Garrido F. Expression of HLA G in human tumors is not a frequent event. Int J Cancer. 1999; 81:512-518.
52. Kallfelz M, Jung D, Hilmes C, Knuth A, Jaeger E, Huber C, Seliger B. Induction of immunogenicity of a human renalcell carcinoma cell line by TAP1-gene transfer. Int J Cancer. 1999; 81:125-133.
53. Respa A, Bukur J, Ferrone S, Pawelec G, Zhao Y, Wang E, Marincola FM, Seliger B. 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.
54. Jasinski-Bergner S, Stehle F, Gonschorek E, Kalich J, Schulz K, Huettelmaier S, Braun J, Seliger B. Identification of 14-3-3beta gene as a novel miR-152 target using a proteome-based approach. J Biol Chem. 2014 (b); 289:31121-31135.
55. Kononen J, Bubendorf L, Kallioniemi A, Barlund M, Schraml P, Leighton S, Torhorst J, Mihatsch MJ, Sauter G, Kallioniemi OP. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med. 1998; 4:844-847.