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 Biochemistry and Cell Biology

Volumn 38, Issue 4, 2006, Pages 544-562

  Shi, Bo ^a,d   Vinyals, Antònia ^a   Alia, Pedro ^a   Broceño, Cristina ^a   Chen, Feisong ^a   Adrover, Marc ^a   Gelpi, Carme ^b   Price, Janet E ^c   Fabra, Àngels ^a  

^a HOSPITAL DURAN I REYNALS   (Spain)

^b HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^c UNIVERSITY OF TEXAS   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

5 Aza CR; CIITA; Differential expression metastasis; Epigenetic; INF ; MHC class II; RAP PCR

Indexed keywords

GAMMA INTERFERON; INTERFERON REGULATORY FACTOR; INTERFERON REGULATORY FACTOR 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NUCLEAR PROTEIN; UPSTREAM STIMULATORY FACTOR 1;

ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BREAST CANCER; CANCER CELL; CARCINOGENICITY; CONTROLLED STUDY; E BOX ELEMENT; GENE EXPRESSION; HUMAN; HUMAN CELL; METASTASIS; METHYLATION; MOUSE; NONHUMAN; NUDE MOUSE; PROMOTER REGION; SOUTHERN BLOTTING; TRANSACTIVATION;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; DNA METHYLATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; KILLER CELLS, NATURAL; MICE; MICE, NUDE; NEOPLASM METASTASIS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEOPLASMS, EXPERIMENTAL; NUCLEAR PROTEINS; RESPONSE ELEMENTS; TRANS-ACTIVATORS;

ANIMALIA; MUS MUSCULUS;

EID: 30944439492     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2005.07.012     Document Type: Article

References (61)

1. S. Baskar, V. Azarenko, E. Garcia Marshall, E. Hughes, and S. Ostrand-Rosenberg MHC class II-transfected tumor cells induce long-term tumor-specific immunity in autologous mice Cell Immunol. 155 1994 123 133
2. F. Bertucci, R. Houlgatte, S. Granjeaud, V. Nasser, B. Loriod, and E. Beaudoing Prognosis of breast cancer and gene expression profiling using DNA arrays Ann. N.Y. Acad. Sci. 975 2002 217 231
3. A.S. Beutler, M.S. Banck, D. Wedekind, and H.J. Hedrich Tumor gene therapy made easy: allogeneic major histocompatibility complex in the C6 rat glioma model Hum. Gene Ther. 10 1999 95 101
4. J.M. Boss Regulation of transcription of MHC class II genes Curr. Opin. Immunol. 9 1997 107 113
5. J.J. Bright, S. Kausalya, and A. Khar Natural killer cell activation-associated induction of target cell DNA fragmentation in a spontaneously regressing rat histiocytoma Immunology 85 1995 638 644
6. M.Y. Cao, Y. Lee, N. Feng, H. Li, C. Du, and D. Miao NK cell activation and tumor infiltration are involved in the antitumor mechanism of Virulizin Cancer Immunol. Immunother. 54 2005 229 242
7. A.I. Chapoval, J.A. Fuller, S.G. Kremlev, S.J. Kamdar, and R. Evans Combination chemotherapy and IL-15 administration induce permanent tumor regression in a mouse lung tumor model: NK and T cell-mediated effects antagonized by B cells J. Immunol. 161 1998 6977 6984
8. M. Croce, A. De Ambrosis, M.V. Corrias, V. Pistoia, M. Occhino, and R. Meazza Different levels of control prevent interferon-gamma-inducible HLA-class II expression in human neuroblastoma cells Oncogene 22 2003 7848 7857
9. R. Dadmarz, M.K. Sgagias, S.A. Rosenberg, and D.J. Schwartzentruber CD4+ T lymphocytes infiltrating human breast cancer recognise autologous tumor in an MHC-class-II restricted fashion Cancer Immunol. Immunother. 40 1995 1 9
10. Fidler I. J., Fabra, A., Nakajima M., & Radinsky R. (1992). Genetic and epigenetic regulation of human colon carcinoma metastasis. In H. Rabes, P. E. Peters, K. Munk (Eds.), Metastasis: Basic research and its clinical applications (Vol. 44, pp. 13-26). Basel: Karger.
11. F. Garrido, and F. Ruiz-Cabello MHC expression on human tumors - its relevance for local tumor growth and metastasis Semin. Cancer Biol. 2 1991 3 10
12. S.J. Gobin, A. Peijnenburg, M. van Eggermond, M. van Zutphen, R. van den Berg, and P.J. van den Elsen The RFX complex is crucial for the constitutive and CIITA-mediated transactivation of MHC class I and beta2-microglobulin genes Immunity 9 1998 531 541
13. B.L. Goodwin, H. Xi, R. Tejiram, D.D. Eason, N. Ghosh, and K.L. Wright Varying functions of specific major histocompatibility class II transactivator promoter III and IV elements in melanoma cell lines Cell Growth Differ. 12 2001 327 335
14. E. Gorelik, M. Kim, L. Duty, T. Henion, and U. Galili Control of metastatic properties of BL6 melanoma cells by H-2Kb gene: immunological and nonimmunological mechanisms Clin. Exp. Metast. 11 1993 439 452
15. N. Hanna The role of natural killer cells in the control of tumor growth and metastasis Biochim. Biophys. Acta 780 1985 213 226
16. J.A. Harton, and J.P. Ting Class II transactivator: mastering the art of major histocompatibility complex expression Mol. Cell Biol. 20 2000 6185 6194
17. T.M. Holling, N. van der Stoep, E. Quinten, and P.J. van den Elsen Activated human T cells accomplish MHC class II expression through T cell-specific occupation of class II transactivator promoter III J. Immunol. 168 2002 763 770
18. T.M. Holling, N. Van der Stoep, and P.J. Van den Elsen Epigenetic control of CIITA expression in leukemic T cells Biochem. Pharmacol. 68 2004 1209 1213
19. H.M. Kluger, Y. Kluger, M. Gilmore-Hebert, K. DiVito, J.T. Chang, and S. Rodov cDNA microarray analysis of invasive and tumorigenic phenotypes in a breast cancer model Lab. Invest. 84 2004 320 331
20. S. Landmann, A. Muhlethaler-Mottet, L. Bernasconi, T. Suter, J.M. Waldburger, and K. Masternak Maturation of dendritic cells is accompanied by rapid transcriptional silencing of class II transactivator (CIITA) expression J. Exp. Med. 194 2001 379 391
21. H. Lee, E.C. Lin, L. Liu, and J.W. Smith Gene expression profiling of tumor xenografts: in vivo analysis of organ-specific metastasis Int. J. Cancer 107 2003 528 534
22. S. LeibundGut-Landmann, J.M. Waldburger, M. Krawczyk, L.A. Otten, T. Suter, and A. Fontana Mini-review: specificity and expression of CIITA, the master regulator of MHC class II genes Eur. J. Immunol. 34 2004 1513 1525
23. A.M. Lennon, C. Ottone, G. Rigaud, L.L. Deaven, J. Longmire, and M. Fellous Isolation of a B-cell-specific promoter for the human class II transactivator Immunogenetics 45 1997 266 273
24. A. Maiorana, A.M. Cesinaro, R.A. Fano, and G. Collina Expression of MHC class I and class II antigens in primary breast carcinomas and synchronous nodal metastases Clin. Exp. Metast. 13 1995 43 48
25. B.K. Martin, K.C. Chin, J.C. Olsen, C.A. Skinner, A. Dey, and K. Ozato Induction of MHC class I expression by the MHC class II transactivator CIITA Immunity 6 1997 591 600
26. B.K. Martin, J.G. Frelinger, and J.P. Ting Combination gene therapy with CD86 and the MHC class II transactivator in the control of lung tumor growth J. Immunol. 162 1999 6663 6670
27. K. Masternak, A. Muhlethaler-Mottet, J. Villard, M. Peretti, and W. Reith Molecular genetics of the Bare lymphocyte syndrome Rev. Immunogenet. 2 2000 267 282
28. R. Mattsson The non-expression of MHC class II in trophoblast cells Am. J. Reprod. Immunol. 40 1998 383 384
29. J. Mehrotra, M. Vali, M. McVeigh, S.L. Kominsky, M.J. Fackler, and J. Lahti-Domenici Very high frequency of hypermethylated genes in breast cancer metastasis to the bone, brain, and lung Clin. Cancer Res. 10 2004 3104 3109
30. A.C. Morris, J.L. Riley, W.H. Fleming, and J.M. Boss MHC class II gene silencing in trophoblast cells is caused by inhibition of CIITA expression Am. J. Reprod. Immunol. 40 1998 385 394
31. A.C. Morris, W.E. Spangler, and J.M. Boss Methylation of class II trans-activator promoter IV: a novel mechanism of MHC class II gene control J. Immunol. 164 2000 4143 4149
32. A. Muhlethaler-Mottet, L.A. Otten, V. Steimle, and B. Mach 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 J. 16 1997 2851 2860
33. S. Nozell, Z. Ma, C. Wilson, R. Shah, and E.N. Benveniste Class II major histocompatibility complex transactivator (CIITA) inhibits matrix metalloproteinase-9 gene expression J. Biol. Chem. 279 2004 38577 38589
34. S. Ostrand-Rosenberg, A. Thakur, and V. Clements Rejection of mouse sarcoma cells after transfection of MHC class II genes J. Immunol. 144 1990 4068 4071
35. L.A. Otten, V. Steimle, S. Bontron, and B. Mach Quantitative control of MHC class II expression by the transactivator CIITA Eur. J. Immunol. 28 1998 473 478
36. R.K. Pai, D. Askew, W.H. Boom, and C.V. Harding Regulation of class II MHC expression in APCs: roles of types I, III, and IV class II transactivator J. Immunol. 169 2002 1326 1333
37. M. Perucho, J. Welsh, M.A. Peinado, Y. Ionov, and M. McClelland Fingerprinting of DNA and RNA by arbitrarily primed polymerase chain reaction: applications in cancer research Meth. Enzymol. 254 1995 275 290
38. J.F. Piskurich, M.W. Linhoff, Y. Wang, and J.P. Ting Two distinct gamma interferon-inducible promoters of the major histocompatibility complex class II transactivator gene are differentially regulated by STAT1, interferon regulatory factor 1, and transforming growth factor beta Mol. Cell Biol. 19 1999 431 440
39. J.E. Price, F.A. Zhang, R.D. Radinsky, and R. Pathak S Characterization of variants of a human breast cancer cell line isolated from metastases in different organs of nude mice Int. J. Oncol. 5 1994 459 467
40. J.E. Price The biology of metastatic breast cancer Cancer 66 1990 1313 1320
41. M. Radosevich, Z. Song, J.C. Gorga, B. Ksander, and S.J. Ono Epigenetic silencing of the CIITA gene and posttranscriptional regulation of class II MHC genes in ocular melanoma cells Invest. Ophthalmol. Vis. Sci. 45 2004 3185 3195
42. A. Sierra, J.E. Price, M. Garcia-Ramirez, O. Mendez, L. Lopez, and A. Fabra Astrocyte-derived cytokines contribute to the metastatic brain specificity of breast cancer cells Lab. Invest. 77 1997 357 368
43. D.D. Sloan, B. Nicholson, V. Urquidi, and S. Goodison Detection of differentially expressed genes in an isogenic breast metastasis model using RNA arbitrarily primed-polymerase chain reaction coupled with array hybridization (RAP-array) Am. J. Pathol. 164 2004 315 323
44. J.M. Soos, J.I. Krieger, O. Stuve, C.L. King, J.C. Patarroyo, and K. Aldape Malignant glioma cells use MHC class II transactivator (CIITA) promoters III and IV to direct IFN-gamma-inducible CIITA expression and can function as non-professional antigen presenting cells in endocytic processing and CD4(+) T-cell activation Glia 36 2001 391 405
45. R. Sotiriadou, S.A. Perez, A.D. Gritzapis, P.A. Sotiropoulou, H. Echner, and S. Heinzel Peptide HER2(776-788) represents a naturally processed broad MHC class II-restricted T cell epitope Br. J. Cancer 85 2001 1527 1534
46. V. Steimle, W. Reith, and B. Mach Major histocompatibility complex class II deficiency: a disease of gene regulation Adv. Immunol. 61 1996 327 340
47. M. Szyf, P. Pakneshan, and S.A. Rabbani DNA methylation and breast cancer Biochem. Pharmacol. 68 2004 1187 1197
48. Y. Takamura, H. Ikeda, T. Kanaseki, M. Toyota, T. Tokino, and K. Imai Regulation of MHC class II expression in glioma cells by class II transactivator (CIITA) Glia 45 2004 392 405
49. J.P. Ting, and J. Trowsdale Genetic control of MHC class II expression Cell 109 Suppl 2002 S21 S33
50. N. van der Stoep, P. Biesta, E. Quinten, and P.J. van den Elsen Lack of IFN-gamma-mediated induction of the class II transactivator (CIITA) through promoter methylation is predominantly found in developmental tumor cell lines Int. J. Cancer 97 2002 501 507
51. W. Walter, K. Lingnau, E. Schmitt, M. Loos, and M.J. Maeurer MHC class II antigen presentation pathway in murine tumours: tumour evasion from immunosurveillance? Br. J. Cancer 83 2000 1192 1201
52. M. Warabi, M. Kitagawa, and K. Hirokawa Loss of MHC class II expression is associated with a decrease of tumor-infiltrating T cells and an increase of metastatic potential of colorectal cancer: immunohistological and histopathological analyses as compared with normal colonic mucosa and adenomas Pathol. Res. Pract. 196 2000 807 815
53. P.M. Warnecke, C. Stirzaker, J. Song, C. Grunau, J.R. Melki, and S.J. Clark Identification and resolution of artifacts in bisulfite sequencing Methods 27 2002 101 107
54. H.S. Warren, and M.J. Smyth NK cells and apoptosis Immunol. Cell Biol. 77 1999 64 75
55. D.R. Welch Microarrays bring new insights into understanding of breast cancer metastasis to bone Breast Cancer Res. 6 2004 61 64
56. J. Welsh, N. Rampino, M. McClelland, and M. Perucho Nucleic acid fingerprinting by PCR-based methods: applications to problems in aging and mutagenesis Mutat. Res. 338 1995 215 229
57. S. Yano, Y. Nishioka, H. Nokihara, and S. Sone Macrophage colony-stimulating factor gene transduction into human lung cancer cells differentially regulates metastasis formations in various organ microenvironments of natural killer cell-depleted SCID mice Cancer Res. 57 1997 784 790
58. T. Yazawa, T. Ito, H. Kamma, T. Suzuki, K. Okudela, and H. Hayashi Complicated mechanisms of class II transactivator transcription deficiency in small cell lung cancer and neuroblastoma Am. J. Pathol. 161 2002 291 300
59. T. Yazawa, H. Kamma, M. Fujiwara, M. Matsui, H. Horiguchi, and H. Satoh Lack of class II transactivator causes severe deficiency of HLA-DR expression in small cell lung cancer J. Pathol. 187 1999 191 199
60. D.A. Zajchowski, M.F. Bartholdi, Y. Gong, L. Webster, H.L. Liu, and A. Munishkin Identification of gene expression profiles that predict the aggressive behavior of breast cancer cells Cancer Res. 61 2001 5168 5178
61. R.D. Zhang, I.J. Fidler, and J.E. Price Relative malignant potential of human breast carcinoma cell lines established from pleural effusions and a brain metastasis Invas. Metast. 11 1991 204 215