Epigenetic Silencing of TAP1 in Aldefluor + Breast Cancer Stem Cells Contributes to Their Enhanced Immune Evasion

Stem Cells

Volumn 36, Issue 5, 2018, Pages 641-654

  Sultan, Mohammad ^a   Vidovic, Dejan ^a   Paine, Arianne S ^a   Huynh, Thomas T ^a   Coyle, Krysta M ^a   Thomas, Margaret L ^a   Cruickshank, Brianne M ^a   Dean, Cheryl A ^a   Clements, Derek R ^a   Kim, Youra ^a   Lee, Kristen ^b   Gujar, Shashi A ^a,b   Weaver, Ian C G ^b   Marcato, Paola ^a,b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Aldefluor activity; Antigen processing; Breast cancer stem cells; T cell activation

Indexed keywords

ALDEHYDE DEHYDROGENASE; B7 ANTIGEN; BISULFITE; CD24 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; DECITABINE; HERMES ANTIGEN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1;

4T1 CELL LINE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER STEM CELL; CARCINOGENICITY; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE KNOCKDOWN; GENE SILENCING; IMMUNOCOMPETENCE; IMMUNOCOMPROMISED PATIENT; MOUSE; NONHUMAN; PYROSEQUENCING; T LYMPHOCYTE; TUMOR ESCAPE; TUMOR GROWTH; ANIMAL; BREAST TUMOR; CELL TRANSFORMATION; CYTOLOGY; DISEASE MODEL; GENETIC EPIGENESIS; GENETICS; HUMAN; IMMUNE EVASION; IMMUNOLOGY; TUMOR CELL LINE;

ANIMALS; ATP BINDING CASSETTE TRANSPORTER, SUBFAMILY B, MEMBER 2; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; EPIGENESIS, GENETIC; GENE SILENCING; HUMANS; IMMUNE EVASION; MICE; NEOPLASTIC STEM CELLS;

EID: 85041207092     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2780     Document Type: Article

References (83)

1. Lapidot T, Sirard C, Vormoor J et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994;367:645–648.
2. Singh SK, Hawkins C, Clarke ID et al. Identification of human brain tumour initiating cells. Nature 2004;432:396–401.
3. O'Brien CA, Pollett A, Gallinger S et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007;445:106–110.
4. Ma S, Chan K-W, Hu L et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 2007;132:2542–2556.
5. Al-Hajj M, Wicha MS, Benito-Hernandez A et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003;100:3983–3988.
6. da Silveira WA, Palma PVB, Sicchieri RD et al. Transcription factor networks derived from breast cancer stem cells control the immune response in the Basal subtype. Sci Rep 2017;7:2851.
7. Ginestier C, Hur MH, Charafe-Jauffret E et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1:555–567.
8. Huang EH, Hynes MJ, Zhang T et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009;69:3382–3389.
9. Ma S, Chan KW, Lee TK et al. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res 2008;6:1146–1153.
10. Jiang F, Qiu Q, Khanna A et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 2009;7:330–338.
11. van den Hoogen C, van der Horst G, Cheung H et al. High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res 2010;70:5163–5173.
12. Rasper M, Schafer A, Piontek G et al. Aldehyde dehydrogenase 1 positive glioblastoma cells show brain tumor stem cell capacity. Neuro Oncol 2010;12:1024–1033.
13. Luo Y, Dallaglio K, Chen Y et al. ALDH1A isozymes are markers of human melanoma stem cells and potential therapeutic targets. Stem Cells 2012;30:2100–2113.
14. Clay MR, Tabor M, Owen JH et al. Single-marker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase. Head Neck 2010;32:1195–1201.
15. Liu G, Yuan X, Zeng Z et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006;5:67.
16. Ma S, Lee TK, Zheng B-J et al. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008;27:1749–1758.
17. Silva IA, Bai S, McLean K et al. Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Res 2011;71:3991–4001.
18. Kantoff PW, Schuetz TJ, Blumenstein BA et al. Overall survival analysis of a phase II randomized controlled trial of a Poxviral-based PSA-targeted immunotherapy in metastatic castration-resistant prostate cancer. J Clin Oncol 2010;28:1099–1105.
19. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: Moving beyond current vaccines. Nat Med 2004;10:909–915.
20. Sultan M, Coyle KM, Vidovic D et al. Hide-and-seek: The interplay between cancer stem cells and the immune system. Carcinogenesis 2017;38:107–118.
21. Roemer MGM, Advani RH, Redd RA et al. Classical hodgkin lymphoma with reduced 2M/MHC class I expression is associated with inferior outcome independent of 9p24.1 status. Cancer Immunol Res 2016;4:910–916.
22. Woo EY, Yeh H, Chu CS et al. Cutting edge: Regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation. J Immunol 2002;168:4272.
23. Kusmartsev S, Nefedova Y, Yoder D et al. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J Immunol 2004;172:989.
24. Curiel TJ. Regulatory T cells and treatment of cancer. Curr Opin Immunol 2008;20:241–246.
25. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: Linking inflammation and cancer. J Immunol 2009;182:4499.
26. Sica A, Schioppa T, Mantovani A et al. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: Potential targets of anti-cancer therapy. Eur J Cancer 2006;42:717–727.
27. Chikamatsu K, Takahashi G, Sakakura K et al. Immunoregulatory properties of CD44+ cancer stem-like cells in squamous cell carcinoma of the head and neck. Head Neck 2011;33:208–215.
28. Volonte A, Di Tomaso T, Spinelli M et al. Cancer-initiating cells from colorectal cancer patients escape from T cell-mediated immunosurveillance in vitro through membrane-bound IL-4. J Immunol 2014;192:523–532.
29. Inoda S, Hirohashi Y, Torigoe T et al. Cytotoxic T lymphocytes efficiently recognize human colon cancer stem-like cells. Am J Pathol 2011;178:1805–1813.
30. Lee Y, Sunwoo J. PD-L1 is preferentially expressed on CD44+ tumor-initiating cells in head and neck squamous cell carcinoma. J Immunother Cancer 2014;2:P270.
31. Wu A, Wei J, Kong L-Y et al. Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro Oncol 2010;12:1113–1125.
32. Jinushi M. Role of cancer stem cell-associated inflammation in creating pro-inflammatory tumorigenic microenvironments. Oncoimmunology 2014;3:e28862.
33. Ames E, Canter RJ, Grossenbacher SK et al. NK cells preferentially target tumor cells with a cancer stem cell phenotype. J Immunol 2015;195:4010–4019.
34. Wang B, Wang Q, Wang Z et al. Metastatic consequences of immune escape from NK cell cytotoxicity by human breast cancer stem cells. Cancer Res 2014;74:5746–5757.
35. Lu H, Clauser KR, Tam WL et al. A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages. Nat Cell Biol 2014;16:1105–1117.
36. Okuda H, Kobayashi A, Xia B et al. Hyaluronan synthase HAS2 promotes tumor progression in bone by stimulating the interaction of breast cancer stem-like cells with macrophages and stromal cells. Cancer Res 2012;72:537–547.
37. Cheng L, Ramesh AV, Flesken-Nikitin A et al. Mouse models for cancer stem cell research. Toxicol Pathol 2010;38:62–71.
38. Grange C, Lanzardo S, Cavallo F et al. Sca-1 identifies the tumor-initiating cells in mammary tumors of BALB-neuT transgenic mice. Neoplasia 2008;10:1433–1443.
39. Park SJ, Kim RJ, Nam JS. Inhibitor of DNA-binding 4 contributes to the maintenance and expansion of cancer stem cells in 4T1 mouse mammary cancer cell line. Lab Anim Res 2011;27:333.
40. Choi AR, Park JR, Kim RJ et al. Inhibition of Wnt1 expression reduces the enrichment of cancer stem cells in a mouse model of breast cancer. Biochem Biophys Res Commun 2012;425:436–442.
41. Zhuang X, Zhang W, Chen Y et al. Doxorubicin-enriched, ALDHbr mouse breast cancer stem cells are treatable to oncolytic herpes simplex virus type 1. BMC Cancer 2012;12:549.
42. Nguyen ST, Nguyen HL, Pham VQ et al. Targeting specificity of dendritic cells on breast cancer stem cells: In vitro and in vivo evaluations. Onco Targets Ther 2015;8:323–334.
43. Kim RJ, Park JR, Roh KJ et al. High aldehyde dehydrogenase activity enhances stem cell features in breast cancer cells by activating hypoxia-inducible factor-2α. Cancer Lett 2013;333:18–31.
44. Bonci D, Coppola V, Musumeci M et al. The miR-15a–miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 2008;14:1271–1277.
45. Gjerdrum C, Tiron C, Høiby T et al. Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proc Natl Acad Sci USA 2010;107:1124–1129.
46. Creighton CJ, Li X, Landis M et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA 2009;106:13820–13825.
47. Liu S, Cong Y, Wang D et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports 2014;2:78–91.
48. Ciriello G, Gatza ML, Beck AH et al. Comprehensive molecular portraits of invasive lobular breast cancer. Cell 2015;163:506–519.
49. Weaver ICG, Hellstrom IC, Brown SE et al. The methylated-DNA binding protein MBD2 enhances NGFI-A (egr-1)-mediated transcriptional activation of the glucocorticoid receptor. Philos Trans R Soc Lond B Biol Sci 2014;369:20130513.
50. Delaney C, Garg SK Yung R. Analysis of DNA methylation by pyrosequencing. Methods Mol Biol 2015;1343:249–264.
51. Tost J, Gut IG. DNA methylation analysis by pyrosequencing. Nat Protoc 2007;2:2265–2275.
52. Caudrillier A, Mallavia B, Rouse L et al. Transfusion of human platelets treated with mirasol pathogen reduction technology does not induce acute lung injury in mice. PLoS One 2015;10:e0133022.
53. Markees TG, Serreze DV, Phillips NE et al. NOD mice have a generalized defect in their response to transplantation tolerance induction. Diabetes 1999;48:967–974.
54. Bosma GC, Custer RP, Bosma MJ. A severe combined immunodeficiency mutation in the mouse. Nature 1983;301:527–530.
55. Hira VVV, Ploegmakers KJ, Grevers F et al. CD133+ and nestin+ glioma stem-like cells reside around CD31+ arterioles in niches that express SDF-1α, CXCR4, osteopontin and cathepsin K. J Histochem Cytochem 2015;63:481–493.
56. Lee CG, Das B, Lin TL et al. A rare fraction of drug-resistant follicular lymphoma cancer stem cells interacts with follicular dendritic cells to maintain tumourigenic potential. Br J Haematol 2012;158:79–90.
57. Zhu Q, Zhang X, Zhang L et al. The IL-6-STAT3 axis mediates a reciprocal crosstalk between cancer-derived mesenchymal stem cells and neutrophils to synergistically prompt gastric cancer progression. Cell Death Dis 2014;5:e1295.
58. Wan S, Zhao E, Kryczek I et al. Tumor-associated macrophages produce interleukin 6 and signal via STAT3 to promote expansion of human hepatocellular carcinoma stem cells. Gastroenterology 2014;147:1393–1404.
59. Panni RZ, Sanford DE, Belt BA et al. Tumor-induced STAT3 activation in monocytic myeloid-derived suppressor cells enhances stemness and mesenchymal properties in human pancreatic cancer. Cancer Immunol Immunother 2014;63:513–528.
60. Jaenisch R, Bird A. Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nat Genet 2003;33:245–254.
61. Baylin SB. DNA methylation and gene silencing in cancer. Nat Clin Pract Oncol 2005;2:S4–S11.
62. Hasim A, Abudula M, Aimiduo R et al. Post-transcriptional and epigenetic regulation of antigen processing machinery (APM) components and HLA-I in cervical cancers from Uighur women. PLoS One 2012;7:e44952.
63. Poage GM, Butler RA, Houseman EA et al. Identification of an epigenetic profile classifier that is associated with survival in head and neck cancer. Cancer Res 2012;72:2728–2737.
64. Qifeng S, Bo C, Xingtao J et al. Methylation of the promoter of human leukocyte antigen class I in human esophageal squamous cell carcinoma and its histopathological characteristics. J Thorac Cardiovasc Surg 2011;141:808–814.
65. Wang C, Cicek MS, Charbonneau B et al. Tumor hypomethylation at 6p21.3 associates with longer time to recurrence of high-grade serous epithelial ovarian cancer. Cancer Res 2014;74:3084–3091.
66. Wright KL, White LC, Kelly A et al. Coordinate regulation of the human TAP1 and LMP2 genes from a shared bidirectional promoter. J Exp Med 1995;181:1459–1471.
67. Brucet M, Marqués L, Sebastián C et al. Regulation of murine Tap1 and Lmp2 genes in macrophages by interferon gamma is mediated by STAT1 and IRF-1. Genes Immun 2004;5:26–35.
68. Thomas L. Discussion of paper by P.B. Hoeber. In: Lawrence HS, ed. Cellular and Humoral Aspects of the Hypersensitive States. New York: Hoeber- Harper, 1959:1–529.
69. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 2004;21:137–148.
70. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420:860–867.
71. Dong H, Strome SE, Salomao DR et al. Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion. Nat Med 2002;8:793–800.
72. Drake CG, Jaffee E, Pardoll DM. Mechanisms of immune evasion by tumors. Adv Immunol 2006;90:51–81.
73. Brahmer JR, Tykodi SS, Chow LQM et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012;366:2455–2465.
74. Leon L, Areses MC, Anido U et al. Poxviral-based prostate-specific antigen vaccine in prostate cancer. J Clin Oncol 2010;28:e416.
75. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012;12:252–264.
76. Colombo MP, Trinchieri G. Interleukin-12 in anti-tumor immunity and immunotherapy. Cytokine Growth Factor Rev 2002;13:155–168.
77. Kane A, Yang I. Interferon-gamma in brain tumor immunotherapy. Neurosurg Clin N Am 2010;21:77–86.
78. Ritchie DS, Neeson PJ, Khot A et al. Persistence and efficacy of second generation CAR T cell against the LeY antigen in acute myeloid leukemia. Mol Ther 2013;21:2122–2129.
79. Cheng M, Chen Y, Xiao W et al. NK cell-based immunotherapy for malignant diseases. Cell Mol Immunol 2013;10:230–252.
80. Coulie PG, Karanikas V, Colau D et al. A monoclonal cytolytic T-lymphocyte response observed in a melanoma patient vaccinated with a tumor-specific antigenic peptide encoded by gene MAGE-3. Proc Natl Acad Sci USA 2001;98:10290–10295.
81. Okada H, Kalinski P, Ueda R et al. Induction of CD8+ T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with {alpha}-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. J Clin Oncol 2011;29:330–336.
82. Gujar SA, Marcato P, Pan D et al. Reovirus virotherapy overrides tumor antigen presentation evasion and promotes protective antitumor immunity. Mol Cancer Ther 2010;9:2924.
83. Liu Y, Nenutil R, Appleyard MV et al. Lack of correlation of stem cell markers in breast cancer stem cells. Br J Cancer 2014;110:2063–2071