CML cells actively evade host immune surveillance through cytokine-mediated downregulation of MHC-II expression

Blood

Volumn 129, Issue 2, 2017, Pages 199-208

  Tarafdar, Anuradha ^a   Hopcroft, Lisa E M ^a   Gallipoli, Paolo ^a,b   Pellicano, Francesca ^a   Cassels, Jennifer ^a   Hair, Alan ^a   Korfi, Koorosh ^a   Jørgensen, Heather G ^a   Vetrie, David ^a   Holyoake, Tessa L ^a   Michie, Alison M ^a,c  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c GARTNAVEL GENERAL HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CD34 ANTIGEN; CD4 ANTIGEN; CD69 ANTIGEN; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RUXOLITINIB; CYTOKINE; HLA ANTIGEN CLASS 2;

ANTIGEN EXPRESSION; ARTICLE; CANCER PATIENT; CANCER STEM CELL; CD4+ T LYMPHOCYTE; CHRONIC MYELOID LEUKEMIA; CHRONIC MYELOID LEUKEMIA CELL LINE; DOWN REGULATION; HUMAN; HUMAN CELL; IMMUNOSURVEILLANCE; LYMPHOCYTE PROLIFERATION; MIXED LYMPHOCYTE REACTION; PRIORITY JOURNAL; TUMOR IMMUNOGENICITY; TUMOR MICROENVIRONMENT; UPREGULATION; BIOSYNTHESIS; CELL CULTURE; DNA MICROARRAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; IMMUNOLOGY; MALE; METABOLISM; MIXED LYMPHOCYTE CULTURE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR ESCAPE;

CELLS, CULTURED; CYTOKINES; DOWN-REGULATION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; LYMPHOCYTE CULTURE TEST, MIXED; MALE; NEOPLASTIC STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR ESCAPE;

EID: 85016314182     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-09-742049     Document Type: Article

References (49)

1. Druker BJ, Guilhot F, O’Brien SG, et al; IRIS Investigators. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med. 2006;355(23):2408-2417.
2. Bower H, Björkholm M, Dickman PW, Höglund M, Lambert PC, Andersson TM. Life expectancy of patients with chronic myeloid leukemia approaches the life expectancy of the general population. J Clin Oncol. 2016;34(24): 2851-2857.
3. Mahon FX, Réa D, Guilhot J, et al; Intergroupe Français des Leucémies Myéloïdes Chroniques. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre Stop Imatinib (STIM) trial. Lancet Oncol. 2010;11(11):1029-1035.
4. Ross DM, Branford S, Seymour JF, et al. Safety and efficacy of imatinib cessation for CML patients with stable undetectable minimal residual disease: results from the TWISTER study. Blood. 2013; 122(4):515-522.
5. Rousselot P, Charbonnier A, Cony-Makhoul P, et al. Loss of major molecular response as a trigger for restarting tyrosine kinase inhibitor therapy in patients with chronic-phase chronic myelogenous leukemia who have stopped imatinib after durable undetectable disease. J Clin Oncol. 2014;32(5):424-430.
6. Chalandon Y, Passweg JR, Schmid C, et al; Chronic Leukemia Working Party of European Group for Blood and Marrow Transplantation. Outcome of patients developing GVHD after DLI given to treat CML relapse: a study by the Chronic Leukemia Working Party of the EBMT. Bone Marrow Transplant. 2010;45(3): 558-564.
7. Bocchia M, Defina M, Aprile L, et al. Complete molecular response in CML after p210 BCR-ABL1-derived peptide vaccination. Nat Rev Clin Oncol. 2010;7(10):600-603.
8. Biernacki MA, Marina O, Zhang W, et al. Efficacious immune therapy in chronic myelogenous leukemia (CML) recognizes antigens that are expressed on CML progenitor cells. Cancer Res. 2010;70(3):906-915.
9. Hung K, Hayashi R, Lafond-Walker A, Lowenstein C, Pardoll D, Levitsky H. The central role of CD4(1) T cells in the antitumor immune response. J Exp Med. 1998;188(12):2357-2368.
10. Ossendorp F, Mengedé E, Camps M, Filius R, Melief CJ. Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. J Exp Med. 1998;187(5): 693-702.
11. Løvig T, Andersen SN, Thorstensen L, et al. Strong HLA-DR expression in microsatellite stable carcinomas of the large bowel is associated with good prognosis. Br J Cancer. 2002;87(7): 756-762.
12. Rimsza LM, Roberts RA, Miller TP, et al. 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. 2004;103(11):4251-4258.
13. Graham SM, Vass JK, Holyoake TL, Graham GJ. Transcriptional analysis of quiescent and proliferating CD341 human hemopoietic cells from normal and chronic myeloid leukemia sources. Stem Cells. 2007;25(12):3111-3120.
14. Affer M, Dao S, Liu C, et al. Gene expression differences between enriched normal and chronic myelogenous leukemia quiescent stem/progenitor cells and correlations with biological abnormalities. J Oncol. 2011;2011:798592.
15. Cramer-Morales K, Nieborowska-Skorska M, Scheibner K, et al. Personalized synthetic lethality induced by targeting RAD52 in leukemias identified by gene mutation and expression profile. Blood. 2013;122(7):1293-1304.
16. Abraham SA, Hopcroft LE, Carrick E, et al. Dual targeting of p53 and c-MYC selectively eliminates leukaemic stem cells. Nature. 2016;534(7607): 341-346.
17. Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102(43):15545-15550.
18. Reith W, LeibundGut-Landmann S, Waldburger JM. Regulation of MHC class II gene expression by the class II transactivator. Nat Rev Immunol. 2005;5(10):793-806.
19. Silacci P, Mottet A, Steimle V, Reith W, Mach B. Developmental extinction of major histocompatibility complex class II gene expression in plasmocytes is mediated by silencing of the transactivator gene CIITA. J Exp Med. 1994;180(4):1329-1336.
20. Holling TM, Schooten E, Langerak AW, van den Elsen PJ. Regulation of MHC class II expression in human T-cell malignancies. Blood. 2004; 103(4):1438-1444.
21. Satoh A, Toyota M, Ikeda 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(55): 8876-8886.
22. O’Keefe GM, Nguyen VT, Benveniste EN. Class II transactivator and class II MHC gene expression in microglia: modulation by the cytokines TGF-beta, IL-4, IL-13 and IL-10. Eur J Immunol. 1999;29(4): 1275-1285.
23. Lee YJ, Han Y, Lu HT, et al. TGF-beta suppresses IFN-gamma induction of class II MHC gene expression by inhibiting class II transactivator messenger RNA expression. J Immunol. 1997;158(5):2065-2075.
24. Naka K, Hoshii T, Muraguchi T, et al. TGF-beta-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature. 2010; 463(7281):676-680.
25. Zhang B, Ho YW, Huang Q, et al. Altered microenvironmental regulation of leukemic and normal stem cells in chronic myelogenous leukemia. Cancer Cell. 2012;21(4):577-592.
26. DaCosta Byfield S, Major C, Laping NJ, Roberts AB. SB-505124 is a selective inhibitor of transforming growth factor-beta type I receptors ALK4, ALK5, and ALK7. Mol Pharmacol. 2004; 65(3):744-752.
27. Gregory MA, Phang TL, Neviani P, et al. Wnt/ Ca21/NFAT signaling maintains survival of Ph1 leukemia cells upon inhibition of Bcr-Abl. Cancer Cell. 2010;18(1):74-87.
28. Quintás-Cardama A, Vaddi K, Liu P, et al. Preclinical characterization of the selective JAK1/2 inhibitor INCB018424: therapeutic implications for the treatment of myeloproliferative neoplasms. Blood. 2010;115(15):3109-3117.
29. Steidl C, Shah SP, Woolcock BW, et al. MHC class II transactivator CIITA is a recurrent gene fusion partner in lymphoid cancers. Nature. 2011; 471(7338):377-381.
30. Wright KL, Ting JP. Epigenetic regulation of MHC-II and CIITA genes. Trends Immunol. 2006;27(9): 405-412.
31. Morimoto Y, Toyota M, Satoh A, 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(4):844-852.
32. Zhu XS, Linhoff MW, Li G, Chin KC, Maity SN, Ting JP. Transcriptional scaffold: CIITA interacts with NF-Y, RFX, and CREB to cause stereospecific regulation of the class II major histocompatibility complex promoter. Mol Cell Biol. 2000;20(16):6051-6061.
33. Beresford GW, Boss JM. CIITA coordinates multiple histone acetylation modifications at the HLA-DRA promoter. Nat Immunol. 2001;2(7): 652-657.
34. Gallipoli P, Pellicano F, Morrison H, et al. Autocrine TNF-a production supports CML stem and progenitor cell survival and enhances their proliferation. Blood. 2013;122(19):3335-3339.
35. Zhang B, Chu S, Agarwal P, et al. Inhibition of interleukin-1 signaling enhances elimination of tyrosine kinase inhibitor–treated CML stem cells [published online ahead of print 12 September 2016]. Blood. doi:10.1182/blood-2015-11-679928.
36. Xie S, Wang Y, Liu J, et al. Involvement of Jak2 tyrosine phosphorylation in Bcr-Abl transformation. Oncogene. 2001;20(43): 6188-6195.
37. Ilaria RLJ Jr, Van Etten RA. P210 and P190(BCR/ ABL) induce the tyrosine phosphorylation and DNA binding activity of multiple specific STAT family members. J Biol Chem. 1996;271(49): 31704-31710.
38. Xie S, Lin H, Sun T, Arlinghaus RB. Jak2 is involved in c-Myc induction by Bcr-Abl. Oncogene. 2002;21(47):7137-7146.
39. Neviani P, Harb JG, Oaks JJ, et al. PP2A-activating drugs selectively eradicate TKI-resistant chronic myeloid leukemic stem cells. J Clin Invest. 2013;123(10):4144-4157.
40. Dawson MA, Bannister AJ, Göttgens B, et al. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature. 2009;461(7265):819-822.
41. Ghoreschi K, Laurence A, O’Shea JJ. Janus kinases in immune cell signaling. Immunol Rev. 2009;228(1):273-287.
42. Fujiwara H, Melenhorst JJ, El Ouriaghli F, et al. In vitro induction of myeloid leukemia-specific CD4 and CD8 T cells by CD40 ligand-activated B cells gene modified to express primary granule proteins. Clin Cancer Res. 2005;11(12): 4495-4503.
43. Jiang YZ, Mavroudis D, Dermime S, et al. Alloreactive CD41 T lymphocytes can exert cytotoxicity to chronic myeloid leukaemia cells processing and presenting exogenous antigen. Br J Haematol. 1996;93(3):606-612.
44. Das R, Guan P, Sprague L, et al. Janus kinase inhibition lessens inflammation and ameliorates disease in murine models of hemophagocytic lymphohistiocytosis. Blood. 2016;127(13): 1666-1675.
45. Spoerl S, Mathew NR, Bscheider M, et al. Activity of therapeutic JAK 1/2 blockade in graft-versus-host disease. Blood. 2014;123(24):3832-3842.
46. Carniti C, Gimondi S, Vendramin A, et al. Pharmacologic Inhibition of JAK1/JAK2 Signaling Reduces Experimental Murine Acute GVHD While Preserving GVT Effects. Clin Cancer Res. 2015; 21(16):3740-3749.
47. Choi J, Cooper ML, Alahmari B, et al. Pharmacologic blockade of JAK1/JAK2 reduces GvHD and preserves the graft-versus-leukemia effect. PLoS One. 2014;9(10):e109799.
48. Chen M, Gallipoli P, DeGeer D, et al. Targeting primitive chronic myeloid leukemia cells by effective inhibition of a new AHI-1-BCR-ABL-JAK2 complex. J Natl Cancer Inst. 2013;105(6): 405-423.
49. Gallipoli P, Cook A, Rhodes S, et al. JAK2/STAT5 inhibition by nilotinib with ruxolitinib contributes to the elimination of CML CD341 cells in vitro and in vivo. Blood. 2014;124(9):1492-1501.