Identification of a cancer stem cell-specific function for the histone deacetylases, HDAC1 and HDAC7, in breast and ovarian cancer

Oncogene

Volumn 36, Issue 12, 2017, Pages 1707-1720

  Witt, A E ^a   Lee, C W ^b   Lee, T I ^c   Azzam, D J ^d   Wang, B ^a   Caslini, C ^a   Petrocca, F ^e   Grosso, J ^a   Jones, M ^a   Cohick, E B ^b,c   Gropper, A B ^c   Wahlestedt, C ^d   Richardson, A L ^b   Shiekhattar, R ^d   Young, R A ^c   Ince, T A ^a  

^a UNIVERSITY OF MIAMI   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 (1,3 DIOXO 1H,3H BENZO[DE]ISOQUINOLIN 2 YL) N HYDROXYHEXANAMIDE; ACTIN; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; ANTINEOPLASTIC AGENT; APICIDIN; CD44V ANTIGEN; ENTINOSTAT; EPITHELIAL CELL ADHESION MOLECULE; FLUOROURACIL; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 7; HISTONE DEACETYLASE INHIBITOR; LOPERAMIDE; MESSENGER RNA; MOCETINOSTAT; PACLITAXEL; RICOLINOSTAT; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRIAMTERENE; TRICHOSTATIN A; VORINOSTAT; BIOLOGICAL MARKER; HDAC7 PROTEIN, HUMAN; HISTONE DEACETYLASE;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER SIZE; CANCER STEM CELL; FEMALE; HUMAN; HUMAN CELL; OVARY CANCER; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR XENOGRAFT; ANIMAL; BREAST TUMOR; DISEASE MODEL; DRUG DEVELOPMENT; DRUG EFFECTS; GENE SILENCING; GENETICS; LETHAL GENE; METABOLISM; MOUSE; OVARY TUMOR; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; BIOMARKERS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DRUG DISCOVERY; FEMALE; GENE KNOCKDOWN TECHNIQUES; GENES, LETHAL; HETEROGRAFTS; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; MICE; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; PHENOTYPE; RNA, SMALL INTERFERING;

EID: 84989827185     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2016.337     Document Type: Article

References (59)

1. Ablett MP, Singh JK, Clarke RB. Stem cells in breast tumours: are they ready for the clinic? Eur J Cancer [Research Support, Non-US Gov't Review] 2012; 48: 2104-2116.
2. Vincent A, Van Seuningen I. On the epigenetic origin of cancer stem cells. Biochimica et biophysica acta 2012; 1826: 83-88.
3. Seto E, Yoshida M. Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol [Review] 2014; 6: a018713.
4. Kidder BL, Palmer S. HDAC1 regulates pluripotency and lineage specific transcriptional networks in embryonic and trophoblast stem cells. Nucleic Acids Res 2012; 40: 2925-2939.
5. Liang J, Wan M, Zhang Y, Gu P, Xin H, Jung SY et al. Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat Cell Biol 2008; 10: 731-739.
6. Dovey OM, Foster CT, Cowley SM. Histone deacetylase 1 (HDAC1), but not HDAC2, controls embryonic stem cell differentiation. Proc Natl Acad Sci USA 2010; 107: 8242-8247.
7. McCool KW, Xu X, Singer DB, Murdoch FE, Fritsch MK. The role of histone acetylation in regulating early gene expression patterns during early embryonic stem cell differentiation. J Biol Chem 2007; 282: 6696-6706.
8. Karantzali E, Schulz H, Hummel O, Hubner N, Hatzopoulos A, Kretsovali A. Histone deacetylase inhibition accelerates the early events of stem cell differentiation: transcriptomic and epigenetic analysis. Genome Biol 2008; 9: R65.
9. Zhu C, Chen Q, Xie Z, Ai J, Tong L, Ding J et al. The role of histone deacetylase 7 (HDAC7) in cancer cell proliferation: regulation on c-Myc. J Mol Med (Berl) 2011; 89: 279-289.
10. You JS, Kang JK, Seo DW, Park JH, Park JW, Lee JC et al. Depletion of embryonic stem cell signature by histone deacetylase inhibitor in NCCIT cells: involvement of Nanog suppression. Cancer Res 2009; 69: 5716-5725.
11. Jiao J, Hindoyan A, Wang S, Tran LM, Goldstein AS, Lawson D et al. Identification of CD166 as a surface marker for enriching prostate stem/progenitor and cancer initiating cells. PloS One [Research Support, N.I.H., Extramural Research Support, Non-US Gov't Research Support, US Gov't, Non-P.H.S.] 2012; 7: e42564.
12. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 2007; 104: 10158-10163.
13. Rowehl RA, Burke S, Bialkowska AB, Pettet DW 3rd, Rowehl L, Li E et al. Establishment of highly tumorigenic human colorectal cancer cell line (CR4) with properties of putative cancer stem cells. PloS One [Research Support, Non-US Gov't] 2014; 9: e99091.
14. Fillmore CM, Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res: BCR. [Research Support, N.I.H., Extramural Research Support, Non-US Gov't] 2008; 10: R25.
15. Stuelten CH, Mertins SD, Busch JI, Gowens M, Scudiero DA, Burkett MW et al. Complex display of putative tumor stem cell markers in the NCI60 tumor cell line panel. Stem Cells [Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural] 2010; 28: 649-660.
16. Kok M, Koornstra RH, Margarido TC, Fles R, Armstrong NJ, Linn SC et al. Mammosphere-derived gene set predicts outcome in patients with ER-positive breast cancer. J Pathol [Research Support, Non-US Gov't] 2009; 218: 316-326.
17. Azzam DJ, Zhao D, Sun J, Minn AJ, Ranganathan P, Drews-Elger K et al. Triple negative breast cancer initiating cell subsets differ in functional and molecular characteristics and in gamma-secretase inhibitor drug responses. EMBO Mol Med [Research Support, N.I.H., Extramural Research Support, Non-US Gov't Research Support, US Gov't, Non-P.H.S.] 2013; 5: 1502-1522.
18. Civenni G, Walter A, Kobert N, Mihic-Probst D, Zipser M, Belloni B et al. Human CD271-positive melanoma stem cells associated with metastasis establish tumor heterogeneity and long-term growth. Cancer Res [Research Support, Non-US Gov't] 2011; 71: 3098-3109.
19. Munz M, Baeuerle PA, Gires O. The emerging role of EpCAM in cancer and stem cell signaling. Cancer Res [Research Support, Non-US Gov't Review] 2009; 69: 5627-5629.
20. Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang HY et al. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology [Research Support, N.I.H., Extramural Research Support, Non-US Gov't Research Support, US Gov't, Non-P.H.S.] 2009; 136: 1012-1024.
21. Williams K, Motiani K, Giridhar PV, Kasper S. CD44 integrates signaling in normal stem cell, cancer stem cell and (pre)metastatic niches. Exp Biol Med (Maywood) [Research Support, N.I.H., Extramural Research Support, Non-US Gov't Review] 2013; 238: 324-338.
22. Belsky DW, Moffitt TE, Baker TB, Biddle AK, Evans JP, Harrington H et al. Polygenic risk and the developmental progression to heavy, persistent smoking and nicotine dependence: evidence from a 4-decade longitudinal study. JAMA Psychiatry [Research Support, N.I.H., Extramural Research Support, Non-US Gov't Research Support, US Gov't, P.H.S.] 2013; 70: 534-542.
23. Ince TA, Richardson AL, Bell GW, Saitoh M, Godar S, Karnoub AE et al. Transformation of different human breast epithelial cell types leads to distinct tumor phenotypes. Cancer Cell 2007; 12: 160-170.
24. Sauder CA, Koziel JE, Choi M, Fox MJ, Grimes BR, Badve S et al. Phenotypic plasticity in normal breast derived epithelial cells. BMC Cell Biol 2014; 15: 20.
25. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T et al. Identification of human brain tumour initiating cells. Nature [Research Support, Non-US Gov't] 2004; 432: 396-401.
26. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/ progenitor cell properties. Cancer Res [Research Support, Non-US Gov't] 2005; 65: 5506-5511.
27. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C et al. Identification and expansion of human colon-cancer-initiating cells. Nature [Research Support, Non-US Gov't] 2007; 445: 111-115.
28. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ [Research Support, Non-US Gov't] 2008; 15: 504-514.
29. Han ME, Jeon TY, Hwang SH, Lee YS, Kim HJ, Shim HE et al. Cancer spheres from gastric cancer patients provide an ideal model system for cancer stem cell research. Cell Mol Life Sci: CMLS. [Research Support, Non-US Gov't] 2011; 68: 3589-3605.
30. Merritt MA, Bentink S, Schwede M, Iwanicki MP, Quackenbush J, Woo T et al. Gene expression signature of normal cell-of-origin predicts ovarian tumor outcomes. PLoS One 2013; 8: e80314.
31. Petrocca F, Altschuler G, Tan SM, Mendillo ML, Yan H, Jerry DJ et al. A genomewide siRNA screen identifies proteasome addiction as a vulnerability of basal-like triple-negative breast cancer cells. Cancer Cell 2013; 24: 182-196.
32. Leth-Larsen R, Terp MG, Christensen AG, Elias D, Kuhlwein T, Jensen ON et al. Functional heterogeneity within the CD44 high human breast cancer stem celllike compartment reveals a gene signature predictive of distant metastasis. Mol Med [Research Support, Non-US Gov't] 2012; 18: 1109-1121.
33. Pasto A, Bellio C, Pilotto G, Ciminale V, Silic-Benussi M, Guzzo G et al. Cancer stem cells from epithelial ovarian cancer patients privilege oxidative phosphorylation, and resist glucose deprivation. Oncotarget [Research Support, Non-US Gov't] 2014; 5: 4305-4319.
34. Kasler HG, Young BD, Mottet D, Lim HW, Collins AM, Olson EN et al. Histone deacetylase 7 regulates cell survival and TCR signaling in CD4/CD8 doublepositive thymocytes. J Immunol [Research Support, N.I.H., Extramural] 2011; 186: 4782-4793.
35. Schuettengruber B, Simboeck E, Khier H, Seiser C. Autoregulation of mouse histone deacetylase 1 expression. Mol Cell Biol [Research Support, Non-US Gov't] 2003; 23: 6993-7004.
36. Chikamatsu K, Ishii H, Murata T, Sakakura K, Shino M, Toyoda M et al. Alteration of cancer stem cell-like phenotype by histone deacetylase inhibitors in squamous cell carcinoma of the head and neck. Cancer Sci [Research Support, Non-US Gov't] 2013; 104: 1468-1475.
37. Salvador MA, Wicinski J, Cabaud O, Toiron Y, Finetti P, Josselin E et al. The histone deacetylase inhibitor abexinostat induces cancer stem cells differentiation in breast cancer with low Xist expression. Clin Cancer Res: An Official Journal of the American Association for Cancer Research [Research Support, Non-US Gov't] 2013; 19: 6520-6531.
38. Debeb BG, Lacerda L, Xu W, Larson R, Solley T, Atkinson R et al. Histone deacetylase inhibitors stimulate dedifferentiation of human breast cancer cells through WNT/beta-catenin signaling. Stem Cells [Research Support, N.I.H., Extramural Research Support, Non-US Gov't] 2012; 30: 2366-2377.
39. Munster PN, Troso-Sandoval T, Rosen N, Rifkind R, Marks PA, Richon VM. The histone deacetylase inhibitor suberoylanilide hydroxamic acid induces differentiation of human breast cancer cells. Cancer Res [Research Support, US Gov't, P.H. S.] 2001; 61: 8492-8497.
40. Galanis E, Jaeckle KA, Maurer MJ, Reid JM, Ames MM, Hardwick JS et al. Phase II trial of vorinostat in recurrent glioblastoma multiforme: a north central cancer treatment group study. J Clin Oncol: Official Journal of the American Society of Clinical Oncology [Clinical Trial, Phase II Research Support, N.I.H., Extramural Research Support, Non-US Gov't] 2009; 27: 2052-2058.
41. Beckers T, Burkhardt C, Wieland H, Gimmnich P, Ciossek T, Maier T et al. Distinct pharmacological properties of second generation HDAC inhibitors with the benzamide or hydroxamate head group. Int J Cancer [Journal international du cancer] 2007; 121: 1138-1148.
42. Boissinot M, Inman M, Hempshall A, James SR, Gill JH, Selby P et al. Induction of differentiation and apoptosis in leukaemic cell lines by the novel benzamide family histone deacetylase 2 and 3 inhibitor MI-192. Leukemia Res [Research Support, Non-US Gov't] 2012; 36: 1304-1310.
43. Khan N, Jeffers M, Kumar S, Hackett C, Boldog F, Khramtsov N et al. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J 2008; 409: 581-589.
44. Wood TE, Dalili S, Simpson CD, Sukhai MA, Hurren R, Anyiwe K et al. Selective inhibition of histone deacetylases sensitizes malignant cells to death receptor ligands. Mol Cancer Ther [Research Support, Non-US Gov't] 2010; 9: 246-256.
45. Ince TA, Sousa AD, Jones MA, Harrell JC, Agoston ES, Krohn M et al. Characterization of twenty-five ovarian tumour cell lines that phenocopy primary tumours. Nat Commun 2015; 6: 7419.
46. Zhang L, Jin M, Margariti A, Wang G, Luo Z, Zampetaki A et al. Sp1-dependent activation of HDAC7 is required for platelet-derived growth factor-BB-induced smooth muscle cell differentiation from stem cells. J Biol Chem 2010; 285: 38463-38472.
47. Clocchiatti A, Di Giorgio E, Ingrao S, Meyer-Almes FJ, Tripodo C, Brancolini C. Class IIa HDACs repressive activities on MEF2-depedent transcription are associated with poor prognosis of ER(+) breast tumors. FASEB Journal: Official publication of the Federation of American Societies for Experimental Biology [Research Support, Non-US Gov't] 2013; 27: 942-954.
48. Milde T, Oehme I, Korshunov A, Kopp-Schneider A, Remke M, Northcott P et al. HDAC5 and HDAC9 in medulloblastoma: novel markers for risk stratification and role in tumor cell growth. Clini Cancer Res: An Official Journal of the American Association for Cancer Research [Research Support, Non-US Gov't] 2010; 16: 3240-3252.
49. Van Damme M, Crompot E, Meuleman N, Mineur P, Bron D, Lagneaux L et al. HDAC isoenzyme expression is deregulated in chronic lymphocytic leukemia B-cells and has a complex prognostic significance. Epigenetics: Official Journal of the DNA Methylation Society [Research Support, Non-US Gov't] 2012; 7: 1403-1412.
50. Wu MY, Fu J, Xiao X, Wu J, Wu RC. MiR-34a regulates therapy resistance by targeting HDAC1 and HDAC7 in breast cancer. Cancer Lett 2014; 354: 311-319.
51. Wang Y, Jia LS, Yuan W, Wu Z, Wang HB, Xu T et al. Low miR-34a and miR-192 are associated with unfavorable prognosis in patients suffering from osteosarcoma. Am J Transl Res 2015; 7: 111-119.
52. Gao H, Zhao H, Xiang W. Expression level of human miR-34a correlates with glioma grade and prognosis. J Neurooncol 2013; 113: 221-228.
53. Dokmanovic M, Perez G, Xu W, Ngo L, Clarke C, Parmigiani RB et al. Histone deacetylase inhibitors selectively suppress expression of HDAC7. Mol Cancer Ther 2007; 6: 2525-2534.
54. Higashijima J, Kurita N, Miyatani T, Yoshikawa K, Morimoto S, Nishioka M et al. Expression of histone deacetylase 1 and metastasis-associated protein 1 as prognostic factors in colon cancer. Oncol Rep [Research Support, Non-US Gov't] 2011; 26: 343-348.
55. Miyake K, Yoshizumi T, Imura S, Sugimoto K, Batmunkh E, Kanemura H et al. Expression of hypoxia-inducible factor-1alpha, histone deacetylase 1, and metastasis-associated protein 1 in pancreatic carcinoma: correlation with poor prognosis with possible regulation. Pancreas 2008; 36: e1-e9.
56. Minamiya Y, Ono T, Saito H, Takahashi N, Ito M, Mitsui M et al. Expression of histone deacetylase 1 correlates with a poor prognosis in patients with adenocarcinoma of the lung. Lung Cancer 2011; 74: 300-304.
57. Garcia-Manero G, Assouline S, Cortes J, Estrov Z, Kantarjian H, Yang H et al. Phase 1 study of the oral isotype specific histone deacetylase inhibitor MGCD0103 in leukemia. Blood [Clinical Trial, Phase I Research Support, Non-US Gov't] 2008; 112: 981-989.
58. Carrasco E, Alvarez PJ, Prados J, Melguizo C, Rama AR, Aranega A et al. Cancer stem cells and their implication in breast cancer. Eur J Clin Invest [Research Support, Non-US Gov't Review] 2014; 44: 678-687.
59. Hu Y, Smyth GK. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods [Comparative Study] 2009; 347: 70-78.