Identification of thiostrepton as a novel therapeutic agent that targets human colon cancer stem cells

Cell Death and Disease

Volumn 6, Issue , 2015, Pages

  Ju, S Y ^a   Huang, C Y F ^a   Huang, W C ^a   Su, Y ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

OXALIPLATIN; THIOSTREPTON; ANTINEOPLASTIC AGENT; CD133 ANTIGEN; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE; PLATINUM COMPLEX;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER STEM CELL; CELL SUBPOPULATION; COLON CANCER; COLONY FORMATION; COLONY FORMING UNIT; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; HL 60 CELL LINE; HT 29 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; PHENOTYPE; PRIORITY JOURNAL; COLONIC NEOPLASMS; DRUG EFFECTS; HCT 116 CELL LINE; HT-29 CELL LINE; METABOLISM; MULTICELLULAR SPHEROID; NEOPLASM METASTASIS; PATHOLOGY; PREVENTION AND CONTROL; TUMOR CELL CULTURE; TUMOR RECURRENCE;

AC133 ANTIGEN; ANTIGENS, CD; ANTINEOPLASTIC AGENTS; APOPTOSIS; COLONIC NEOPLASMS; GLYCOPROTEINS; HCT116 CELLS; HT29 CELLS; HUMANS; NEOPLASM METASTASIS; NEOPLASM RECURRENCE, LOCAL; NEOPLASTIC STEM CELLS; ORGANOPLATINUM COMPOUNDS; PEPTIDES; SPHEROIDS, CELLULAR; THIOSTREPTON; TUMOR CELLS, CULTURED;

EID: 84942906792     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2015.155     Document Type: Article

References (62)

1. Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet 2014; 383: 1490-1502.
2. Siegel R, Desantis C, Jemal A. Colorectal cancer statistics2014 CA Cancer J Clin 2014; 64: 104-117.
3. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N Engl J Med 2006; 355: 1253-1261.
4. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 2009; 69: 1302-1313.
5. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007; 445: 106-110.
6. 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 2007; 445: 111-115.
7. Chu P, Clanton DJ, Snipas TS, Lee J, Mitchell E, Nguyen ML et al. Characterization of a subpopulation of colon cancer cells with stem cell-like properties. Int J Cancer 2009; 124: 1312-1321.
8. 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.
9. Pang R, Law WL, Chu AC, Poon JT, Lam CS, Chow AK et al. A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 2010; 6: 603-615.
10. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H 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.
11. Haraguchi N, Utsunomiya T, Inoue H, Tanaka F, Mimori K, Barnard GF et al. Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 2006; 24: 506-513.
12. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-5828.
13. Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L et al. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One 2008; 3: e2428.
14. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715.
15. van Es JH, Clevers H. Notch and Wnt inhibitors as potential new drugs for intestinal neoplastic disease. Trends Mol Med 2005; 11: 496-502.
16. You L, He B, Xu Z, Uematsu K, Mazieres J, Fujii N et al. An anti-Wnt-2 monoclonal antibody induces apoptosis in malignant melanoma cells and inhibits tumor growth. Cancer Res 2004; 64: 5385-5389.
17. Liu J, Pan S, Hsieh MH, Ng N, Sun F, Wang T et al. Targeting Wnt-driven cancer through the inhibition of Porcupine by LGK974. Proc Natl Acad Sci USA 2013; 110: 20224-20229.
18. Sandhiya S, Melvin G, Kumar SS, Dkhar SA. The dawn of hedgehog inhibitors: Vismodegib. J Pharmacol Pharmacother 2013; 4: 4-7.
19. Sahebjam S, Bedard PL, Castonguay V, Chen Z, Reedijk M, Liu G et al. A phase I study of the combination of ro4929097 and cediranib in patients with advanced solid tumours (PJC-004/NCI 8503). Br J Cancer 2013; 109: 943-949.
20. Marangoni E, Lecomte N, Durand L, de Pinieux G, Decaudin D, Chomienne C et al. CD44 targeting reduces tumour growth and prevents post-chemotherapy relapse of human breast cancers xenografts. Br J Cancer 2009; 100: 918-922.
21. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 2006; 12: 1167-1174.
22. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009; 138: 645-659.
23. Dallas NA, Xia L, Fan F, Gray MJ, Gaur P, van Buren G 2nd et al. Chemoresistant colorectal cancer cells, the cancer stem cell phenotype, and increased sensitivity to insulin-like growth factor-I receptor inhibition. Cancer Res 2009; 69: 1951-1957.
24. Ramirez A, Boulaiz H, Morata-Tarifa C, Peran M, Jimenez G, Picon-Ruiz M et al. HER2-signaling pathway, JNK and ERKs kinases, and cancer stem-like cells are targets of Bozepinib small compound. Oncotarget 2014; 5: 3590-3606.
25. Todaro M, Alea MP, Di Stefano AB, Cammareri P, Vermeulen L, Iovino F et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007; 1: 389-402.
26. Lombardo Y, Scopelliti A, Cammareri P, Todaro M, Iovino F, Ricci-Vitiani L et al. Bone morphogenetic protein 4 induces differentiation of colorectal cancer stem cells and increases their response to chemotherapy in mice. Gastroenterology 2011; 140: 297-309.
27. Cai Z, Ke J, He X, Yuan R, Chen Y, Wu X et al. Significance of mTOR signaling and its inhibitor against cancer stem-like cells in colorectal cancer. Ann Surg Oncol 2013; 21: 179-188.
28. Qu XA, Rajpal DK. Applications of Connectivity Map in drug discovery and development. Drug Discov Today 2012; 17: 1289-1298.
29. Gartel AL. FoxM1 inhibitors as potential anticancer drugs. Expert Opin Ther Targets 2008; 12: 663-665.
30. Radhakrishnan SK, Bhat UG, Hughes DE, Wang IC, Costa RH, Gartel AL. Identification of a chemical inhibitor of the oncogenic transcription factor forkhead box M1. Cancer Res 2006; 66: 9731-9735.
31. Lamb J, Crawford ED, Peck D, Modell JW, Blat IC, Wrobel MJ et al. The Connectivity Map: using gene-expression signatures to connect small molecules, genes, and disease. Science 2006; 313: 1929-1935.
32. Suva ML, Riggi N, Janiszewska M, Radovanovic I, Provero P, Stehle JC et al. EZH2 is essential for glioblastoma cancer stem cell maintenance. Cancer Res 2009; 69: 9211-9218.
33. Yang AD, Fan F, Camp ER, van Buren G, Liu W, Somcio R et al. Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res 2006; 12: 4147-4153.
34. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-284.
35. Haraguchi N, Ohkuma M, Sakashita H, Matsuzaki S, Tanaka F, Mimori K et al. CD133+ CD44+ population efficiently enriches colon cancer initiating cells. Ann Surg Oncol 2008; 15: 2927-2933.
36. Bhat UG, Zipfel PA, Tyler DS, Gartel AL. Novel anticancer compounds induce apoptosis in melanoma cells. Cell Cycle 2008; 7: 1851-1855.
37. Uddin S, Ahmed M, Hussain A, Abubaker J, Al-Sanea N, AbdulJabbar A et al. Genome-wide expression analysis of Middle Eastern colorectal cancer reveals FOXM1 as a novel target for cancer therapy. Am J Pathol 2011; 178: 537-547.
38. Bhat UG, Halasi M, Gartel AL. FoxM1 is a general target for proteasome inhibitors. PLoS One 2009; 4: e6593.
39. Wierstra I. FOXM1 (Forkhead box M1) in tumorigenesis: overexpression in human cancer, implication in tumorigenesis, oncogenic functions, tumor-suppressive properties, and target of anticancer therapy. Adv Cancer Res 2013; 119: 191-419.
40. Chiu WT, Huang YF, Tsai HY, Chen CC, Chang CH, Huang SC et al. FOXM1 confers to epithelial-mesenchymal transition, stemness and chemoresistance in epithelial ovarian carcinoma cells. Oncotarget 2015; 6: 2349-2365.
41. Bergamaschi A, Madak-Erdogan Z, Kim YJ, Choi YL, Lu H, Katzenellenbogen BS. The forkhead transcription factor FOXM1 promotes endocrine resistance and invasiveness in estrogen receptor-positive breast cancer by expansion of stem-like cancer cells. Breast Cancer Res 2014; 16: 436.
42. Myatt SS, Lam EW. The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer 2007; 7: 847-859.
43. Xie Z, Tan G, Ding M, Dong D, Chen T, Meng X et al. Foxm1 transcription factor is required for maintenance of pluripotency of P19 embryonal carcinoma cells. Nucleic Acids Res 2010; 38: 8027-8038.
44. Joshi K, Banasavadi-Siddegowda Y, Mo X, Kim SH, Mao P, Kig C et al. MELK-dependent FOXM1 phosphorylation is essential for proliferation of glioma stem cells. Stem Cells 2013; 31: 1051-1063.
45. Visnyei K, Onodera H, Damoiseaux R, Saigusa K, Petrosyan S, De Vries D et al. A molecular screening approach to identify and characterize inhibitors of glioblastoma stem cells. Mol Cancer Ther 2011; 10: 1818-1828.
46. Wang IC, Chen YJ, Hughes D, Petrovic V, Major ML, Park HJ et al. Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol Cell Biol 2005; 25: 10875-10894.
47. Bao B, Wang Z, Ali S, Kong D, Banerjee S, Ahmad A et al. Over-expression of FoxM1 leads to epithelial-mesenchymal transition and cancer stem cell phenotype in pancreatic cancer cells. J Cell Biochem 2011; 112: 2296-2306.
48. Halasi M, Schraufnagel DP, Gartel AL.Wild-type p53 protects normal cells against apoptosis induced by thiostrepton. Cell Cycle 2009; 8: 2850-2851.
49. Bhat UG, Halasi M, Gartel AL. Thiazole antibiotics target FoxM1 and induce apoptosis in human cancer cells. PLoS One 2009; 4: e5592.
50. Pilarsky C, Wenzig M, Specht T, Saeger HD, Grutzmann R. Identification and validation of commonly overexpressed genes in solid tumors by comparison of microarray data. Neoplasia 2004; 6: 744-750.
51. Liu M, Dai B, Kang SH, Ban K, Huang FJ, Lang FF et al. FoxM1B is overexpressed in human glioblastomas and critically regulates the tumorigenicity of glioma cells. Cancer Res 2006; 66: 3593-3602.
52. Dai B, Kang SH, Gong W, Liu M, Aldape KD, Sawaya R et al. Aberrant FoxM1B expression increases matrix metalloproteinase-2 transcription and enhances the invasion of glioma cells. Oncogene 2007; 26: 6212-6219.
53. Huang C, Qiu Z, Wang L, Peng Z, Jia Z, Logsdon CD et al. A novel FoxM1-caveolin signaling pathway promotes pancreatic cancer invasion and metastasis. Cancer Res 2012; 72: 655-665.
54. Li Q, Zhang N, Jia Z, Le X, Dai B, Wei D et al. Critical role and regulation of transcription factor FoxM1 in human gastric cancer angiogenesis and progression. Cancer Res 2009; 69: 3501-3509.
55. Zhang N, Wei P, Gong A, Chiu WT, Lee HT, Colman H et al. FoxM1 promotes beta-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell 2011; 20: 427-442.
56. Carr JR, Park HJ, Wang Z, Kiefer MM, Raychaudhuri P. FoxM1 mediates resistance to herceptin and paclitaxel. Cancer Res 2010; 70: 5054-5063.
57. Kwok JM, Peck B, Monteiro LJ, Schwenen HD, Millour J, Coombes RC et al. FOXM1 confers acquired cisplatin resistance in breast cancer cells. Mol Cancer Res 2010; 8: 24-34.
58. Mraz M, Zent CS, Church AK, Jelinek DF, Wu X, Pospisilova S et al. Bone marrow stromal cells protect lymphoma B-cells from rituximab-induced apoptosis and targeting integrin alpha-4-beta-1 (VLA-4) with natalizumab can overcome this resistance. Br J Haematol 2011; 155: 53-64.
59. Akhdar H, Loyer P, Rauch C, Corlu A, Guillouzo A, Morel F. Involvement of Nrf2 activation in resistance to 5-fluorouracil in human colon cancer HT-29 cells. Eur J Cancer 2009; 45: 2219-2227.
60. Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M et al. NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res 2013; 41: D991-D995.
61. Ju SY, Chiou SH, Su Y. Maintenance of the stemness in CD44(+) HCT-15 and HCT-116 human colon cancer cells requires miR-203 suppression. Stem Cell Res 2014; 12: 86-100.
62. Ghosh S, Spagnoli GC, Martin I, Ploegert S, Demougin P, Heberer M et al. Three-dimensional culture of melanoma cells profoundly affects gene expression profile: a high density oligonucleotide array study. J Cell Physiol 2005; 204: 522-531.