Reduced human leukocyte antigen expression in advanced-stage Ewing sarcoma: Implications for immune recognition

Journal of Pathology

Volumn 218, Issue 2, 2009, Pages 222-231

  Berghuis, Dagmar ^a   De Hooge, Alfons S K ^a   Santos, Susy J ^a   Horst, Danielle ^a,b   Wiertz, Emmanuel J ^a,b   Van Eggermond, Marja C ^a   Van Den Elsen, Peter J ^a   Taminiau, Antonie H M ^a   Ottaviano, Laura ^c   Schaefer, Karl Ludwig ^c   Dirksen, Uta ^d   Hooijberg, Erik ^e   Mulder, Arend ^a   Melief, Cornelis J M ^a   Egeler, R Maarten ^a   Schilham, Marco W ^a   Jordanova, Ekaterina S ^a   Hogendoorn, Pancras C W ^a   Lankester, Arjan C ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^e VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Antigen processing pathway; Bone tumour; Ewing sarcoma; Flow cytometry; Human leukocyte antigen; Immune recognition; Immunohistochemistry; Immunotherapy; Soft tissue tumour

Indexed keywords

BETA 2 MICROGLOBULIN; GAMMA INTERFERON; HLA A ANTIGEN; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; HLA B ANTIGEN; HLA C ANTIGEN; LMP 2 PROTEIN; PROTEASOME; TAPASIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; UNCLASSIFIED DRUG;

ADULT; ADVANCED CANCER; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; BONE METASTASIS; CANCER CELL; CANCER GROWTH; CLINICAL ARTICLE; CONTROLLED STUDY; EWING SARCOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREGULATION; LUNG METASTASIS; PRIORITY JOURNAL;

ADOLESCENT; ANTIGEN PRESENTATION; BETA 2-MICROGLOBULIN; BIOLOGICAL MARKERS; BLOTTING, WESTERN; BONE NEOPLASMS; CELL LINE, TUMOR; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-DR ANTIGENS; HUMANS; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; INTERFERON-GAMMA; KAPLAN-MEIERS ESTIMATE; NUCLEAR PROTEINS; SARCOMA, EWING'S; STATISTICS, NONPARAMETRIC; TRANS-ACTIVATORS; TUMOR CELLS, CULTURED; TUMOR ESCAPE;

EID: 66849124862     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2537     Document Type: Article

References (51)

1. van den Berg H, Kroon HM, Slaar A, Hogendoorn PCW. Incidence of biopsy-proven bone tumors in children: a report based on the Dutch pathology registration 'PALGA'. J Pediatr Orthop 2008;28:29-35.
2. Ushigome S, Machinami R, Sorensen PH. Ewing sarcoma/ primitive neuroectodermal tumour. In World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of Soft tissue and Bone, Fletcher CDM, Unni KK, Mertens F (eds). IARC Press: Lyon, 2002; 298-300.
3. Bernstein M, Kovar H, Paulussen M, Randall RL, Schuck A, Teot LA, et al. Ewing's sarcoma family of tumors: current management. Oncologist 2006;11:503-519. (Pubitemid 43788277)
4. Gattinoni L, Powell DJ Jr, Rosenberg SA, Restifo NP. Adoptive immunotherapy for cancer: building on success. Nature Rev Immunol 2006;6:383-393.
5. Melief CJ, Toes RE, Medema JP, van der Burg SH, Ossendorp F, Offringa R. Strategies for immunotherapy of cancer. Adv Immunol 2000;75:235-282. (Pubitemid 30436846)
6. Malmberg KJ, Bryceson YT, Carlsten M, Andersson S, Bjorklund A, Bjorkstrom NK, et al. NK cell-mediated targeting of human cancer and possibilities for new means of immunotherapy. Cancer Immunol Immunother 2008;57:1541-1552.
7. Tait BD. HLA class I expression on human cancer cells. Implications for effective immunotherapy. Hum Immunol 2000;61:158-165. (Pubitemid 30075238)
8. Bjorkman PJ, Parham P. Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem 1990;59:253-288. (Pubitemid 20207008)
9. Pamer E, Cresswell P. Mechanisms of MHC class I - restricted antigen processing. Annu Rev Immunol 1998;16:323-358. (Pubitemid 28183368)
10. Jensen PE. Recent advances in antigen processing and presentation. Nature Immunol 2007;8:1041-1048. (Pubitemid 47423752)
11. van den Elsen PJ, Holling TM, Kuipers HF, van der Stoep N. Transcriptional regulation of antigen presentation. Curr Opin Immunol 2004;16:67-75. (Pubitemid 38198119)
12. Chang CC, Ferrone S. Immune selective pressure and HLA class I antigen defects in malignant lesions. Cancer Immunol Immunother 2007;56:227-236. (Pubitemid 44833096)
13. Tsukahara T, Kawaguchi S, Torigoe T, Asanuma H, Nakazawa E, Shimozawa K, et al. Prognostic significance of HLA class I expression in osteosarcoma defined by anti-pan HLA class I monoclonal antibody, EMR8-5. Cancer Sci 2006;97:1374-1380. (Pubitemid 44614990)
14. Vitale M, Pelusi G, Taroni B, Gobbi G, Micheloni C, Rezzani R, et al. HLA class I antigen down-regulation in primary ovary carcinoma lesions: association with disease stage. Clin Cancer Res 2005;11:67-72. (Pubitemid 40075779)
15. Watson NF, Ramage JM, Madjd Z, Spendlove I, Ellis IO, Scholefield JH, et al. 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. (Pubitemid 41681574)
16. Rodriguez T, Mendez R, Del Campo A, Aptsiauri N, Martin J, Orozco G, et al. Patterns of constitutive and IFN-gamma inducible expression of HLA class II molecules in human melanoma cell lines. Immunogenetics 2007;59:123-133. (Pubitemid 46130791)
17. Holling TM, Schooten E, Langerak AW, van den Elsen PJ. Regulation of MHC class II expression in human T-cell malignancies. Blood 2004;103:1438-1444. (Pubitemid 38168660)
18. Urano F, Umezawa A, Yabe H, Hong W, Yoshida K, Fujinaga K, et al. Molecular analysis of Ewing's sarcoma: another fusion gene, EWS-E1AF, available for diagnosis. Jpn J Cancer Res 1998;89:703-711. (Pubitemid 28401155)
19. Szuhai K, Ijszenga M, Tanke HJ, Rosenberg C, Hogendoorn PCW. Molecular cytogenetic characterization of four previously established and two newly established Ewing sarcoma cell lines. Cancer Genet Cytogenet 2006;166:173-179.
20. Heemskerk MH, Hooijberg E, Ruizendaal JJ, van der Weide MM, Kueter E, Bakker AQ, et al. Enrichment of an antigen-specific T cell response by retrovirally transduced human dendritic cells. Cell Immunol 1999;195:10-17. (Pubitemid 29384258)
21. de Hooge ASK, Berghuis D, Santos SJ, Mooiman E, Romeo S, Kummer JA, et al. Expression of cellular FLICE inhibitory protein, caspase-8, and protease inhibitor-9 in Ewing sarcoma and implications for susceptibility to cytotoxic pathways. Clin Cancer Res 2007;13:206-214. (Pubitemid 46121870)
22. Juergens C, Weston C, Lewis I, Whelan J, Paulussen M, Oberlin O, et al. Safety assessment of intensive induction with vincristine, ifosfamide, doxorubicin, and etoposide (VIDE) in the treatment of Ewing tumors in the EURO-E.W.I.N.G. 99 clinical trial. Pediatr Blood Cancer 2006;47:22-29. (Pubitemid 43787904)
23. Bovee JVMG, van den Broek LJ, de Boer WI, Hogendoorn PCW. Expression of growth factors and their receptors in adamantinoma of long bones and the implication for its histogenesis. J Pathol 1998;184:24-30. (Pubitemid 28086149)
24. Ruiter DJ, Ferrier CM, van Muijen GN, Henzen-Logmans SC, Kennedy S, Kramer MD, et al. Quality control of immunohistochemical evaluation of tumour-associated plasminogen activators and related components. European BIOMED-1 Concerted Action on Clinical Relevance of Proteases in Tumour Invasion and Metastasis. Eur J Cancer 1998;34:1334-1340.
25. Borowski A, van Valen F, Ulbrecht M, Weiss EH, Blasczyk R, Jurgens H, et al. Monomorphic HLA class I-(non-A, non-B) expression on Ewing's tumor cell lines, modulation by TNF-alpha and IFN-gamma. Immunobiology 1999;200:1-20. (Pubitemid 29089954)
26. Mechtersheimer G, Barth T, Ludwig R, Staudter M, Moller P. Differential expression of leukocyte differentiation antigens in small round blue cell sarcomas. Cancer 1993;71:237-248. (Pubitemid 23019308)
27. Mechtersheimer G, Staudter M, Majdic O, Dorken B, Moldenhauer G, Moller P. Expression of HLA-A,B,C, beta 2-microglobulin (beta 2m), HLA-DR, -DP, -DQ and of HLA-Dassociated invariant chain (Ii) in soft-tissue tumors. Int J Cancer 1990;46:813-823.
28. Lipinski M, Braham K, Philip I, Wiels J, Philip T, Goridis C, et al. Neuroectoderm-associated antigens on Ewing's sarcoma cell lines. Cancer Res 1987;47:183-187. (Pubitemid 17002120)
29. Garcia-Lora A, Algarra I, Garrido F. MHC class I antigens, immune surveillance, and tumor immune escape. J Cell Physiol 2003;195:346-355. (Pubitemid 36529863)
30. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 2004;21:137-148. (Pubitemid 39094044)
31. Storkus WJ, Alexander J, Payne JA, Dawson JR, Cresswell P. Reversal of natural killing susceptibility in target cells expressing transfected class I HLA genes. Proc Natl Acad Sci U S A 1989;86:2361-2364. (Pubitemid 19102508)
32. Wagtmann N, Rajagopalan S, Winter CC, Peruzzi M, Long EO. Killer cell inhibitory receptors specific for HLA-C and HLA-B identified by direct binding and by functional transfer. Immunity 1995;3:801-809. (Pubitemid 26092193)
33. Hurks HM, Metzelaar-Blok JA, Mulder A, Claas FH, Jager MJ. High frequency of allele-specific down-regulation of HLA class I expression in uveal melanoma cell lines. Int J Cancer 2000;85:697-702. (Pubitemid 30080484)
34. Ikeda H, Lethe B, Lehmann F, van Baren N, Baurain JF, de Smet C, et al. Characterization of an antigen that is recognized on a melanoma showing partial HLA loss by CTL expressing an NK inhibitory receptor. Immunity 1997;6:199-208. (Pubitemid 27145564)
35. Lankat-Buttgereit B, Tampe R. The transporter associated with antigen processing: function and implications in human diseases. Physiol Rev 2002;82:187-204. (Pubitemid 34654218)
36. Wright KL, White LC, Kelly A, Beck S, Trowsdale J, Ting JP. Coordinate regulation of the human TAP1 and LMP2 genes from a shared bidirectional promoter. J Exp Med 1995;181:1459-1471.
37. Gobin SJ, van Zutphen M, Woltman AM, van den Elsen PJ. Transactivation of classical and nonclassical HLA class I genes through the IFN-stimulated response element. J Immunol 1999;163:1428-1434. (Pubitemid 29352763)
38. Romero JM, Jimenez P, Cabrera T, Cozar JM, Pedrinaci S, Tallada M, et al. Coordinated downregulation of the antigen presentation machinery and HLA class I/beta2-microglobulin complex is responsible for HLA-ABC loss in bladder cancer. Int J Cancer 2005;113:605-610. (Pubitemid 40038737)
39. Johnsen A, France J, Sy MS, Harding CV. Down-regulation of the transporter for antigen presentation, proteasome subunits, and class I major histocompatibility complex in tumor cell lines. Cancer Res 1998;58:3660-3667. (Pubitemid 28376566)
40. Lou Y, Vitalis TZ, Basha G, Cai B, Chen SS, Choi KB, et al. Restoration of the expression of transporters associated with antigen processing in lung carcinoma increases tumor-specific immune responses and survival. Cancer Res 2005;65:7926-7933. (Pubitemid 41297271)
41. Brisset S, Schleiermacher G, Peter M, Mairal A, Oberlin O, Delattre O, et al. CGH analysis of secondary genetic changes in Ewing tumors: correlation with metastatic disease in a series of 43 cases. Cancer Genet Cytogenet 2001;130:57-61. (Pubitemid 32979167)
42. Ferreira BI, Alonso J, Carrillo J, Acquadro F, Largo C, Suela J, et al. Array CGH and gene-expression profiling reveals distinct genomic instability patterns associated with DNA repair and cell-cycle checkpoint pathways in Ewing's sarcoma. Oncogene 2007;27:2084-2090.
43. van den Elsen PJ, Holling TM, van der Stoep N, Boss JM. DNA methylation and expression of major histocompatibility complex class I and class II transactivator genes in human developmental tumor cells and in T cell malignancies. Clin Immunol 2003;109:46-52. (Pubitemid 37324741)
44. Morimoto Y, Toyota M, Satoh A, Murai M, Mita H, Suzuki H, et al. Inactivation of class II transactivator by DNA methylation and histone deacetylation associated with absence of HLA-DR induction by interferon-gamma in haematopoietic tumour cells. Br J Cancer 2004;90:844-852. (Pubitemid 38406596)
45. Satoh A, Toyota M, Ikeda H, Morimoto Y, Akino K, Mita H, et al. Epigenetic inactivation of class II transactivator (CIITA) is associated with the absence of interferon-gamma-induced HLA-DR expression in colorectal and gastric cancer cells. Oncogene 2004;23:8876-8886. (Pubitemid 39657778)
46. Peijnenburg A, van den Berg R, Van Eggermond MJ, Sanal O, Vossen JM, Lennon AM, et al. Defective MHC class II expression in an MHC class II deficiency patient is caused by a novel deletion of a splice donor site in the MHC class II transactivator gene. Immunogenetics 2000;51:42-49. (Pubitemid 30150958)
47. Tirode F, Laud-Duval K, Prieur A, Delorme B, Charbord P, Delattre O. Mesenchymal stem cell features of Ewing tumors. Cancer Cell 2007;11:421-429. (Pubitemid 46680428)
48. Llombart-Bosch A, Carda C, Peydro-Olaya A, Noguera R, Perez-Bacete M, Pellin A, et al. Soft tissue Ewing's sarcoma. Characterization in established cultures and xenografts with evidence of a neuroectodermic phenotype. Cancer 1990;66:2589-2601.
49. Staege MS, Hansen G, Baersch G, Burdach S. Functional and molecular characterization of interleukin-2 transgenic Ewing tumor cells for in vivo immunotherapy. Pediatr Blood Cancer 2004;43:23-34. (Pubitemid 38738268)
50. Mulder A, Kardol M, Regan J, Buelow R, Claas F. Reactivity of twenty-two cytotoxic human monoclonal HLA antibodies towards soluble HLA class I in an enzyme-linked immunosorbent assay (PRA-STAT). Hum Immunol 1997;56:106-113. (Pubitemid 28018605)
51. Mehta AM, Jordanova ES, Kenter GG, Ferrone S, Fleuren G. Association of antigen processing machinery and HLA class I defects with clinicopathological outcome in cervical carcinoma. Cancer Immunol Immunother 2008;57:197-206. (Pubitemid 350159921)