Detection of aberrant transcription of major histocompatibility complex class II antigen presentation genes in chronic lymphocytic leukaemia identifies HLA-DOA mRNA as a prognostic factor for survival

British Journal of Haematology

Volumn 145, Issue 3, 2009, Pages 334-343

  Souwer, Yuri ^a,b,c,d   Chamuleau, Martine E D ^d   Van De Loosdrecht, Arjan A ^d   Tolosa, Eva ^e   Jorritsma, Tineke ^b   Muris, Jettie J F ^d   Dinnissen Van Poppel, Marion J ^d   Snel, Sander N ^d   Van De Corput, Lisette ^c   Ossenkoppele, Gert J ^d   Meijer, Chris J L M ^d   Neefjes, Jacques J ^c   Marieke Van Ham, S ^b,d  

^a Department of Immunopathology ^*  (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Antigen processing; Chronic lymphocytic leukaemia; Class II transactivator; HLA DM; HLA DO

Indexed keywords

GAMMA INTERFERON; HLA ANTIGEN CLASS 2; MESSENGER RNA; TRANSACTIVATOR PROTEIN;

ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; BLOOD SAMPLING; CANCER DIAGNOSIS; CANCER SURVIVAL; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; GENETIC TRANSCRIPTION; HUMAN; MALE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REAL TIME POLYMERASE CHAIN REACTION; RNA TRANSLATION; UPREGULATION;

AGED; ANTIGEN PRESENTATION; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; CASE-CONTROL STUDIES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-D ANTIGENS; HLA-DR ANTIGENS; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MIDDLE AGED; NUCLEAR PROTEINS; PROGNOSIS; PROMOTER REGIONS, GENETIC; PROPORTIONAL HAZARDS MODELS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 64149115125     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2009.07625.x     Document Type: Article

References (48)

1. Adams, T.E., Bodmer, J.G. Bodmer, W.F. (1983) Production and characterization of monoclonal antibodies recognizing the alpha-chain subunits of human ia alloantigens. Immunology, 50, 613 624.
2. Bartik, M.M., Welker, D. Kay, N.E. (1998) Impairments in immune cell function in B cell chronic lymphocytic leukemia. Seminars in Oncology, 25, 27 33.
3. Chang, C.H., Guerder, S., Hong, S.C., van Ewijk, W. Flavell, R.A. (1996) Mice lacking the MHC class II transactivator (CIITA) show tissue-specific impairment of MHC class II expression. Immunity, 4, 167 178.
4. Cheson, B.D., Bennett, J.M., Grever, M., Kay, N., Keating, M.J., O'Brien, S. Rai, K.R. (1996) National Cancer Institute-sponsored Working Group guidelines for chronic lymphocytic leukemia: revised guidelines for diagnosis and treatment. Blood, 87, 4990 4997.
5. Cromme, F.V., Airey, J., Heemels, M.T., Ploegh, H.L., Keating, P.J., Stern, P.L., Meijer, C.J. Walboomers, J.M. (1994a) Loss of transporter protein, encoded by the TAP-1 gene, is highly correlated with loss of HLA expression in cervical carcinomas. Journal of Experimental Medicine, 179, 335 340.
6. Cromme, F.V., van Bommel, P.F., Walboomers, J.M., Gallee, M.P., Stern, P.L., Kenemans, P., Helmerhorst, T.J., Stukart, M.J. Meijer, C.J. (1994b) Differences in MHC and TAP-1 expression in cervical cancer lymph node metastases as compared with the primary tumours. British Journal of Cancer, 69, 1176 1181.
7. Denzin, L.K. Cresswell, P. (1995) HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell, 82, 155 165.
8. Ferrajoli, A., Keating, M.J., Manshouri, T., Giles, F.J., Dey, A., Estrov, Z., Koller, C.A., Kurzrock, R., Thomas, D.A., Faderl, S., Lerner, S., O'Brien, S. Albitar, M. (2002) The clinical significance of tumor necrosis factor-alpha plasma level in patients having chronic lymphocytic leukemia. Blood, 100, 1215 1219.
9. Hake, S.B., Tobin, H.M., Steimle, V. Denzin, L.K. (2003) Comparison of the transcriptional regulation of classical and non-classical MHC class II genes. European Journal of Immunology, 33, 2361 2371.
10. van Ham, S.M., Gruneberg, U., Malcherek, G., Broker, I., Melms, A. Trowsdale, J. (1996) Human histocompatibility leukocyte antigen (HLA)-DM edits peptides presented by HLA-DR according to their ligand binding motifs. Journal of Experimental Medicine, 184, 2019 2024.
11. van Ham, S.M., Tjin, E.P., Lillemeier, B.F., Gruneberg, U., van Meijgaarden, K.E., Pastoors, L., Verwoerd, D., Tulp, A., Canas, B., Rahman, D., Ottenhoff, T.H., Pappin, D.J., Trowsdale, J. Neefjes, J. (1997) HLA-DO is a negative modulator of HLA-DM-mediated MHC class II peptide loading. Current Biology, 7, 950 957.
12. van Ham, M., van Lith, M., Lillemeier, B., Tjin, E., Gruneberg, U., Rahman, D., Pastoors, L., van Meijgaarden, K., Roucard, C., Trowsdale, J., Ottenhoff, T., Pappin, D. Neefjes, J. (2000) Modulation of the major histocompatibility complex class II-associated peptide repertoire by human histocompatibility leukocyte antigen (HLA)-DO. Journal of Experimental Medicine, 191, 1127 1136.
13. Holling, T.M., Schooten, E., Langerak, A.W. Van den Elsen, P.J. (2004) Regulation of MHC class II expression in human T-cell malignancies. Blood, 103, 1438 1444.
14. Hornell, T.M., Beresford, G.W., Bushey, A., Boss, J.M. Mellins, E.D. (2003) Regulation of the class II MHC pathway in primary human monocytes by granulocyte-macrophage colony-stimulating factor. Journal of Immunology, 171, 2374 2383.
15. Johnsen, A.K., Templeton, D.J., Sy, M. Harding, C.V. (1999) Deficiency of transporter for antigen presentation (TAP) in tumor cells allows evasion of immune surveillance and increases tumorigenesis. Journal of Immunology, 163, 4224 4231.
16. Jordanova, E.S., Philippo, K., Giphart, M.J., Schuuring, E. Kluin, P.M. (2003) Mutations in the HLA class II genes leading to loss of expression of HLA-DR and HLA-DQ in diffuse large B-cell lymphoma. Immunogenetics, 55, 203 209.
17. Josefsson, P., Geisler, C.H., Leffers, H., Petersen, J.H., Andersen, M.K., Jurlander, J. Buhl, A.M. (2007) CLLU1 expression analysis adds prognostic information to risk prediction in chronic lymphocytic leukemia. Blood, 109, 4973 4979.
18. Juffs, H., Fowler, N., Saal, R., Grimmett, K., Beasley, S., O'Sullivan, B., Frazer, I., Gill, D. Thomas, R. (2004) B cell chronic lymphocytic leukaemia cells have reduced capacity to upregulate expression of MHC class I in response to interferon-gamma. Pathology, 36, 69 76.
19. Kamper, E.F., Papaphilis, A.D., Angelopoulou, M.K., Kopeikina, L.T., Siakantaris, M.P., Pangalis, G.A. Stavridis, J.C. (1999) Serum levels of tetranectin, intercellular adhesion molecule-1 and interleukin-10 in B-chronic lymphocytic leukemia. Clinical Biochemistry, 32, 639 645.
20. Kiaii, S., Choudhury, A., Mozaffari, F., Kimby, E., Osterborg, A. Mellstedt, H. (2005) Signaling molecules and cytokine production in T cells of patients with B-cell chronic lymphocytic leukemia (B-CLL): comparison of indolent and progressive disease. Medical Oncology, 22, 291 302.
21. Kiaii, S., Choudhury, A., Mozaffari, F., Rezvany, R., Lundin, J., Mellstedt, H. Osterborg, A. (2006) Signaling molecules and cytokine production in T cells of patients with B-cell chronic lymphocytic leukemia: long-term effects of fludarabine and alemtuzumab treatment. Leukemia and Lymphoma, 47, 1229 1238.
22. Klebanoff, C.A., Gattinoni, L. Restifo, N.P. (2006) CD8+ T-cell memory in tumor immunology and immunotherapy. Immunological Reviews, 211, 214 224.
23. Kropshofer, H., Vogt, A.B., Thery, C., Armandola, E.A., Li, B.C., Moldenhauer, G., Amigorena, S. Hammerling, G.J. (1998) A role for HLA-DO as a co-chaperone of HLA-DM in peptide loading of MHC class II molecules. EMBO Journal, 17, 2971 2981.
24. Lai, R., O'Brien, S., Maushouri, T., Rogers, A., Kantarjian, H., Keating, M. Albitar, M. (2002) Prognostic value of plasma interleukin-6 levels in patients with chronic lymphocytic leukemia. Cancer, 95, 1071 1075.
25. Liljedahl, M., Kuwana, T., Fung-Leung, W.P., Jackson, M.R., Peterson, P.A. Karlsson, L. (1996) HLA-DO is a lysosomal resident which requires association with HLA-DM for efficient intracellular transport. EMBO Journal, 15, 4817 4824.
26. Morimoto, Y., Toyota, M., Satoh, A., Murai, M., Mita, H., Suzuki, H., Takamura, Y., Ikeda, H., Ishida, T., Sato, N., Tokino, T. Imai, K. (2004) 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. British Journal of Cancer, 90, 844 852.
27. Muhlethaler-Mottet, A., Otten, L.A., Steimle, V. Mach, B. (1997) Expression of MHC class II molecules in different cellular and functional compartments is controlled by differential usage of multiple promoters of the transactivator CIITA. EMBO Journal, 16, 2851 2860.
28. Muhlethaler-Mottet, A., Di Berardino, W., Otten, L.A. Mach, B. (1998) Activation of the MHC class II transactivator CIITA by interferon-gamma requires cooperative interaction between Stat1 and USF-1. Immunity, 8, 157 166.
29. Nagarajan, U.M., Lochamy, J., Chen, X., Beresford, G.W., Nilsen, R., Jensen, P.E. Boss, J.M. (2002) Class II transactivator is required for maximal expression of HLA-DOB in B cells. Journal of Immunology, 168, 1780 1786.
30. Neefjes, J.J., Stollorz, V., Peters, P.J., Geuze, H.J. Ploegh, H.L. (1990) The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell, 61, 171 183.
31. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, 2002 2007.
32. Piskurich, J.F., Wang, Y., Linhoff, M.W., White, L.C. Ting, J.P. (1998) Identification of distinct regions of 5′ flanking DNA that mediate constitutive, IFN-gamma, STAT1, and TGF-beta-regulated expression of the class II transactivator gene. Journal of Immunology, 160, 233 240.
33. Piskurich, J.F., Gilbert, C.A., Ashley, B.D., Zhao, M., Chen, H., Wu, J., Bolick, S.C. Wright, K.L. (2006) Expression of the MHC class II transactivator (CIITA) type IV promoter in B lymphocytes and regulation by IFN-gamma. Molecular Immunology, 43, 519 528.
34. Reith, W. Mach, B. (2001) The bare lymphocyte syndrome and the regulation of MHC expression. Annual Reviews of Immunology, 19, 331 373.
35. Rimsza, L.M., Roberts, R.A., Miller, T.P., Unger, J.M., LeBlanc, M., Braziel, R.M., Weisenberger, D.D., Chan, W.C., Muller-Hermelink, H.K., Jaffe, E.S., Gascoyne, R.D., Campo, E., Fuchs, D.A., Spier, C.M., Fisher, R.I., Delabie, J., Rosenwald, A., Staudt, L.M. Grogan, T.M. (2004) Loss of MHC class II gene and protein expression in diffuse large B-cell lymphoma is related to decreased tumor immunosurveillance and poor patient survival regardless of other prognostic factors: a follow-up study from the leukemia and lymphoma molecular profiling project. Blood, 103, 4251 4258.
36. Roche, P.A. Cresswell, P. (1990) Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature, 345, 615 618.
37. Roucard, C., Thomas, C., Pasquier, M.A., Trowsdale, J., Sotto, J.J., Neefjes, J. van Ham, M. (2001) In vivo and in vitro modulation of HLA-DM and HLA-DO is induced by B lymphocyte activation. Journal of Immunology, 167, 6849 6858.
38. Rozman, C. Montserrat, E. (1995) Chronic lymphocytic leukemia. New England Journal of Medicine, 333, 1052 1057.
39. Sanderson, F., Kleijmeer, M.J., Kelly, A., Verwoerd, D., Tulp, A., Neefjes, J.J., Geuze, H.J. Trowsdale, J. (1994) Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments. Science, 266, 1566 1569.
40. Seliger, B., Hohne, A., Knuth, A., Bernhard, H., Meyer, T., Tampe, R., Momburg, F. Huber, C. (1996) Analysis of the major histocompatibility complex class I antigen presentation machinery in normal and malignant renal cells: evidence for deficiencies associated with transformation and progression. Cancer Research, 56, 1756 1760.
41. Sherman, M.A., Weber, D.A. Jensen, P.E. (1995) DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide. Immunity, 3, 197 205.
42. Shi, B., Vinyals, A., Alia, P., Broceno, C., Chen, F., Adrover, M., Gelpi, C., Price, J.E. Fabra, A. (2006) Differential expression of MHC class II molecules in highly metastatic breast cancer cells is mediated by the regulation of the CIITA transcription Implication of CIITA in tumor and metastasis development. International Journal of Biochemisrty & Cell Biology, 38, 544 562.
43. Sloan, V.S., Cameron, P., Porter, G., Gammon, M., Amaya, M., Mellins, E. Zaller, D.M. (1995) Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature, 375, 802 806.
44. Smit, L.A., van Maldegem, F., Langerak, A.W., van der Schoot, C.E., de Wit, M.J., Bea, S., Campo, E., Bende, R.J. van Noesel, C.J. (2006) Antigen receptors and somatic hypermutation in B-cell chronic lymphocytic leukemia with Richter's transformation. Haematologica, 91, 903 911.
45. Taxman, D.J., Cressman, D.E. Ting, J.P. (2000) Identification of class II transcriptional activator-induced genes by representational difference analysis: discoordinate regulation of the DN alpha/DO beta heterodimer. Journal of Immunology, 165, 1410 1416.
46. Ullrich, H.J., Doring, K., Gruneberg, U., Jahnig, F., Trowsdale, J. van Ham, S.M. (1997) Interaction between HLA-DM and HLA-DR involves regions that undergo conformational changes at lysosomal pH. Proceedings of The National Academy of Sciences of the United States of America, 94, 13163 13168.
47. Van den Elsen, P.J., Holling, T.M., Kuipers, H.F. Van der, Stoep.N. (2004) Transcriptional regulation of antigen presentation. Current Opinion in Immunology, 16, 67 75.
48. Wierda, W.G., Johnson, M.M., Do, K.A., Manshouri, T., Dey, A., O'Brien, S., Giles, F.J., Kantarjian, H., Thomas, D., Faderl, S., Lerner, S., Keating, M. Albitar, M. (2003) Plasma interleukin 8 level predicts for survival in chronic lymphocytic leukaemia. British Journal of Haematology, 120, 452 456.