Targeting breast cancer stem cells in triple-negative breast cancer using a combination of LBH589 and salinomycin

Breast Cancer Research and Treatment

Volumn 151, Issue 2, 2015, Pages 281-294

  Kai, Masaya ^a   Kanaya, Noriko ^a   Wu, Shang V ^a   Mendez, Carlos ^a   Nguyen, Duc ^a   Luu, Thehang ^a   Chen, Shiuan ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Breast cancer stem cells (BCSCs); Histone deacetylase (HDAC) inhibitor; LBH589 (panobinostat); Salinomycin; Triple negative breast cancer (TNBC)

Indexed keywords

ANTINEOPLASTIC AGENT; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; INDOLE DERIVATIVE; PANOBINOSTAT; PYRAN DERIVATIVE; SALINOMYCIN;

ANIMAL; APOPTOSIS; CANCER STEM CELL; CELL CYCLE CHECKPOINT; CELL PROLIFERATION; CELL SELF-RENEWAL; CELL TRANSFORMATION; DISEASE MODEL; DRUG EFFECTS; DRUG POTENTIATION; DRUG SCREENING; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; METABOLISM; MOUSE; PATHOLOGY; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL CULTURE; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SELF RENEWAL; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; INDOLES; MICE; NEOPLASTIC STEM CELLS; PYRANS; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR BURDEN; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84937762843     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-015-3376-5     Document Type: Article

References (65)

1. Siegel R, Ma J, Zou Z, Jemal A (2014) Cancer statistics, 2014. CA Cancer J Clin 64(1):9–29. doi:10.3322/caac.21208
2. Anders CK, Carey LA (2009) Biology, metastatic patterns, and treatment of patients with triple-negative breast cancer. Clin Breast Cancer 9(Suppl 2):S73–S81. doi:10.3816/CBC.2009.s.008
3. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, Lickley LA, Rawlinson E, Sun P, Narod SA (2007) Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 13(15 Pt 1):4429–4434. doi:10.1158/1078-0432.CCR-06-3045
4. Carey L, Winer E, Viale G, Cameron D, Gianni L (2010) Triple-negative breast cancer: disease entity or title of convenience? Nat Rev Clin Oncol 7(12):683–692. doi:10.1038/nrclinonc.2010.154
5. Schneider BP, Winer EP, Foulkes WD, Garber J, Perou CM, Richardson A, Sledge GW, Carey LA (2008) Triple-negative breast cancer: risk factors to potential targets. Clin Cancer Res 14(24):8010–8018. doi:10.1158/1078-0432.CCR-08-1208
6. Oakman C, Viale G, Di Leo A (2010) Management of triple negative breast cancer. Breast 19(5):312–321. doi:10.1016/j.breast.2010.03.026
7. Rakha EA, El-Sayed ME, Green AR, Lee AH, Robertson JF, Ellis IO (2007) Prognostic markers in triple-negative breast cancer. Cancer 109(1):25–32. doi:10.1002/cncr.22381
8. Dalerba P, Cho RW, Clarke MF (2007) Cancer stem cells: models and concepts. Annu Rev Med 58:267–284. doi:10.1146/annurev.med.58.062105.204854
9. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH, Goulet R Jr, Badve S, Nakshatri H (2006) CD44+/CD24− breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast cancer Res 8(5):R59. doi:10.1186/bcr1610
10. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J, Brown M, Viens P, Xerri L, Bertucci F, Stassi G, Dontu G, Birnbaum D, Wicha MS (2009) Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 69(4):1302–1313. doi:10.1158/0008-5472.CAN-08-2741
11. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, Wong H, Rosen J, Chang JC (2008) Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100(9):672–679. doi:10.1093/jnci/djn123
12. Dean M, Fojo T, Bates S (2005) Tumour stem cells and drug resistance. Nat Rev Cancer 5(4):275–284. doi:10.1038/nrc1590
13. Gangemi R, Paleari L, Orengo AM, Cesario A, Chessa L, Ferrini S, Russo P (2009) Cancer stem cells: a new paradigm for understanding tumor growth and progression and drug resistance. Curr Med Chem 16(14):1688–1703
14. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100(7):3983–3988. doi:10.1073/pnas.0530291100
15. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, Schott A, Hayes D, Birnbaum D, Wicha MS, Dontu G (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1(5):555–567. doi:10.1016/j.stem.2007.08.014
16. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA (2008) The epithelial–mesenchymal transition generates cells with properties of stem cells. Cell 133(4):704–715. doi:10.1016/j.cell.2008.03.027
17. Hollier BG, Tinnirello AA, Werden SJ, Evans KW, Taube JH, Sarkar TR, Sphyris N, Shariati M, Kumar SV, Battula VL, Herschkowitz JI, Guerra R, Chang JT, Miura N, Rosen JM, Mani SA (2013) FOXC2 expression links epithelial–mesenchymal transition and stem cell properties in breast cancer. Cancer Res 73(6):1981–1992. doi:10.1158/0008-5472.CAN-12-2962
18. Fang X, Cai Y, Liu J, Wang Z, Wu Q, Zhang Z, Yang CJ, Yuan L, Ouyang G (2011) Twist2 contributes to breast cancer progression by promoting an epithelial–mesenchymal transition and cancer stem-like cell self-renewal. Oncogene 30(47):4707–4720. doi:10.1038/onc.2011.181
19. Gunasinghe NP, Wells A, Thompson EW, Hugo HJ (2012) Mesenchymal–epithelial transition (MET) as a mechanism for metastatic colonisation in breast cancer. Cancer Metastasis Rev 31(3–4):469–478. doi:10.1007/s10555-012-9377-5
20. Polyak K, Weinberg RA (2009) Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9(4):265–273. doi:10.1038/nrc2620
21. Drummond DC, Noble CO, Kirpotin DB, Guo Z, Scott GK, Benz CC (2005) Clinical development of histone deacetylase inhibitors as anticancer agents. Annu Rev Pharmacol Toxicol 45:495–528. doi:10.1146/annurev.pharmtox.45.120403.095825
22. Slingerland M, Guchelaar HJ, Gelderblom H (2014) Histone deacetylase inhibitors: an overview of the clinical studies in solid tumors. Anticancer Drugs 25(2):140–149. doi:10.1097/CAD.0000000000000040
23. Bose P, Dai Y, Grant S (2014) Histone deacetylase inhibitor (HDACI) mechanisms of action: emerging insights. Pharmacol Ther 143(3):323–336. doi:10.1016/j.pharmthera.2014.04.004
24. Chen S, Ye J, Kijima I, Evans D (2010) The HDAC inhibitor LBH589 (panobinostat) is an inhibitory modulator of aromatase gene expression. Proc Natl Acad Sci USA 107(24):11032–11037. doi:10.1073/pnas.1000917107
25. Kubo M, Kanaya N, Petrossian K, Ye J, Warden C, Liu Z, Nishimura R, Osako T, Okido M, Shimada K, Takahashi M, Chu P, Yuan YC, Chen S (2013) Inhibition of the proliferation of acquired aromatase inhibitor-resistant breast cancer cells by histone deacetylase inhibitor LBH589 (panobinostat). Breast Cancer Res Treat 137(1):93–107. doi:10.1007/s10549-012-2332-x
26. Tate CR, Rhodes LV, Segar HC, Driver JL, Pounder FN, Burow ME, Collins-Burow BM (2012) Targeting triple-negative breast cancer cells with the histone deacetylase inhibitor panobinostat. Breast Cancer Res 14(3):R79. doi:10.1186/bcr3192
27. Miyazaki Y, Shibuya M, Sugawara H, Kawaguchi O, Hirsoe C (1974) Salinomycin, a new polyether antibiotic. J Antibiot 27(11):814–821
28. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138(4):645–659. doi:10.1016/j.cell.2009.06.034
29. King TD, Suto MJ, Li Y (2012) The Wnt/beta-catenin signaling pathway: a potential therapeutic target in the treatment of triple negative breast cancer. J Cell Biochem 113(1):13–18. doi:10.1002/jcb.23350
30. Booth L, Roberts JL, Conley A, Cruickshanks N, Ridder T, Grant S, Poklepovic A, Dent P (2014) HDAC inhibitors enhance the lethality of low dose salinomycin in parental and stem-like GBM cells. Cancer Biol Ther 15(3):305–316. doi:10.4161/cbt.27309
31. Chou TC (2010) Drug combination studies and their synergy quantification using the Chou–Talalay method. Cancer Res 70(2):440–446. doi:10.1158/0008-5472.CAN-09-1947
32. Gangopadhyay S, Nandy A, Hor P, Mukhopadhyay A (2013) Breast cancer stem cells: a novel therapeutic target. Clin Breast Cancer 13(1):7–15. doi:10.1016/j.clbc.2012.09.017
33. West AC, Johnstone RW (2014) New and emerging HDAC inhibitors for cancer treatment. J Clin Invest 124(1):30–39. doi:10.1172/JCI69738
34. Zhou J, Zhang H, Gu P, Bai J, Margolick JB, Zhang Y (2008) NF-kappaB pathway inhibitors preferentially inhibit breast cancer stem-like cells. Breast Cancer Res Treat 111(3):419–427. doi:10.1007/s10549-007-9798-y
35. Huczynski A (2012) Salinomycin: a new cancer drug candidate. Chem Biol Drug Des 79(3):235–238. doi:10.1111/j.1747-0285.2011.01287.x
36. Dini L, Coppola S, Ruzittu MT, Ghibelli L (1996) Multiple pathways for apoptotic nuclear fragmentation. Exp Cell Res 223(2):340–347. doi:10.1006/excr.1996.0089
37. Gui CY, Ngo L, Xu WS, Richon VM, Marks PA (2004) Histone deacetylase (HDAC) inhibitor activation of p21WAF1 involves changes in promoter-associated proteins, including HDAC1. Proc Natl Acad Sci USA 101(5):1241–1246. doi:10.1073/pnas.0307708100
38. Richon VM, Sandhoff TW, Rifkind RA, Marks PA (2000) Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc Natl Acad Sci USA 97(18):10014–10019. doi:10.1073/pnas.180316197
39. Dawson MA, Kouzarides T (2012) Cancer epigenetics: from mechanism to therapy. Cell 150(1):12–27. doi:10.1016/j.cell.2012.06.013
40. Wagner JM, Hackanson B, Lubbert M, Jung M (2010) Histone deacetylase (HDAC) inhibitors in recent clinical trials for cancer therapy. Clin Epigenetics 1(3–4):117–136. doi:10.1007/s13148-010-0012-4
41. Mann BS, Johnson JR, Cohen MH, Justice R, Pazdur R (2007) FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 12(10):1247–1252. doi:10.1634/theoncologist.12-10-1247
42. Atadja P (2009) Development of the pan-DAC inhibitor panobinostat (LBH589): successes and challenges. Cancer Lett 280(2):233–241. doi:10.1016/j.canlet.2009.02.019
43. Rhodes LV, Tate CR, Segar HC, Burks HE, Phamduy TB, Hoang V, Elliott S, Gilliam D, Pounder FN, Anbalagan M, Chrisey DB, Rowan BG, Burow ME, Collins-Burow BM (2014) Suppression of triple-negative breast cancer metastasis by pan-DAC inhibitor panobinostat via inhibition of ZEB family of EMT master regulators. Breast Cancer Res Treat 145(3):593–604. doi:10.1007/s10549-014-2979-6
44. Rao R, Balusu R, Fiskus W, Mudunuru U, Venkannagari S, Chauhan L, Smith JE, Hembruff SL, Ha K, Atadja P, Bhalla KN (2012) Combination of pan-histone deacetylase inhibitor and autophagy inhibitor exerts superior efficacy against triple-negative human breast cancer cells. Mol Cancer Ther 11(4):973–983. doi:10.1158/1535-7163.MCT-11-0979
45. Conte P, Campone M, Pronzato P, Amadori D, Frank R, Schuetz F, Rea D, Wardley A, Britten C, Elias A (2009) Phase I trial of panobinostat (LBH589) in combination with trastuzumab in pretreated HER2-positive metastatic breast cancer (mBC): Preliminary safety and tolerability results. J Clin Oncol 27(15S):1081
46. Winston TJB, Alvaro MA, Donald WN, James NI, Edith AP (2012) Phase I study of panobinostat (LBH589) and letrozole in post-menopausal women with metastatic breast cancer. J Clin Oncol 30:e13501
47. Salvador MA, Wicinski J, Cabaud O, Toiron Y, Finetti P, Josselin E, Lelievre H, Kraus-Berthier L, Depil S, Bertucci F, Collette Y, Birnbaum D, Charafe-Jauffret E, Ginestier C (2013) The histone deacetylase inhibitor abexinostat induces cancer stem cells differentiation in breast cancer with low Xist expression. Clin Cancer Res 19(23):6520–6531. doi:10.1158/1078-0432.CCR-13-0877
48. Liu S, Ginestier C, Charafe-Jauffret E, Foco H, Kleer CG, Merajver SD, Dontu G, Wicha MS (2008) BRCA1 regulates human mammary stem/progenitor cell fate. Proc Natl Acad Sci USA 105(5):1680–1685. doi:10.1073/pnas.0711613105
49. Resetkova E, Reis-Filho JS, Jain RK, Mehta R, Thorat MA, Nakshatri H, Badve S (2010) Prognostic impact of ALDH1 in breast cancer: a story of stem cells and tumor microenvironment. Breast Cancer Res Treat 123(1):97–108. doi:10.1007/s10549-009-0619-3
50. Charafe-Jauffret E, Ginestier C, Bertucci F, Cabaud O, Wicinski J, Finetti P, Josselin E, Adelaide J, Nguyen TT, Monville F, Jacquemier J, Thomassin-Piana J, Pinna G, Jalaguier A, Lambaudie E, Houvenaeghel G, Xerri L, Harel-Bellan A, Chaffanet M, Viens P, Birnbaum D (2013) ALDH1-positive cancer stem cells predict engraftment of primary breast tumors and are governed by a common stem cell program. Cancer Res 73(24):7290–7300. doi:10.1158/0008-5472.CAN-12-4704
51. Bane A, Viloria-Petit A, Pinnaduwage D, Mulligan AM, O’Malley FP, Andrulis IL (2013) Clinical-pathologic significance of cancer stem cell marker expression in familial breast cancers. Breast Cancer Res Treat 140(1):195–205. doi:10.1007/s10549-013-2591-1
52. Alamgeer M, Ganju V, Kumar B, Fox J, Hart S, White M, Harris M, Stuckey J, Prodanovic Z, Schneider-Kolsky ME, Watkins DN (2014) Changes in aldehyde dehydrogenase-1 expression during neoadjuvant chemotherapy predict outcome in locally advanced breast cancer. Breast Cancer Res 16(2):R44. doi:10.1186/bcr3648
53. Marcato P, Dean CA, Liu RZ, Coyle KM, Bydoun M, Wallace M, Clements D, Turner C, Mathenge EG, Gujar SA, Giacomantonio CA, Mackey JR, Godbout R, Lee PW (2015) Aldehyde dehydrogenase 1A3 influences breast cancer progression via differential retinoic acid signaling. Mol Oncol 9(1):17–31. doi:10.1016/j.molonc.2014.07.010
54. Tsang JY, Huang YH, Luo MH, Ni YB, Chan SK, Lui PC, Yu AM, Tan PH, Tse GM (2012) Cancer stem cell markers are associated with adverse biomarker profiles and molecular subtypes of breast cancer. Breast Cancer Res Treat 136(2):407–417. doi:10.1007/s10549-012-2271-6
55. Debeb BG, Lacerda L, Xu W, Larson R, Solley T, Atkinson R, Sulman EP, Ueno NT, Krishnamurthy S, Reuben JM, Buchholz TA, Woodward WA (2012) Histone deacetylase inhibitors stimulate dedifferentiation of human breast cancer cells through WNT/beta-catenin signaling. Stem Cells 30(11):2366–2377. doi:10.1002/stem.1219
56. Lee CH, Hong HM, Chang YY, Chang WW (2012) Inhibition of heat shock protein (Hsp) 27 potentiates the suppressive effect of Hsp90 inhibitors in targeting breast cancer stem-like cells. Biochimie 94(6):1382–1389. doi:10.1016/j.biochi.2012.02.034
57. Danforth HD, Ruff MD, Reid WM, Johnson J (1977) Anticoccidial activity of salinomycin in floor-pen experiments with broilers. Poult Sci 56(3):933–938
58. Plumlee KH, Johnson B, Galey FD (1995) Acute salinomycin toxicosis of pigs. J Vet Diagn Invest 7(3):419–420
59. Kosal ME, Anderson DE (2004) An unaddressed issue of agricultural terrorism: a case study on feed security. J Anim Sci 82(11):3394–3400
60. Naujokat C, Steinhart R (2012) Salinomycin as a drug for targeting human cancer stem cells. J Biomed Biotechnol 2012:950658. doi:10.1155/2012/950658
61. Oliver FJ, de la Rubia G, Rolli V, Ruiz-Ruiz MC, de Murcia G, Murcia JM (1998) Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J Biol Chem 273(50):33533–33539
62. Fang JY, Lu YY (2002) Effects of histone acetylation and DNA methylation on p21(WAF1) regulation. World J Gastroenterol 8(3):400–405
63. Wilson AJ, Byun DS, Popova N, Murray LB, L’Italien K, Sowa Y, Arango D, Velcich A, Augenlicht LH, Mariadason JM (2006) Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem 281(19):13548–13558. doi:10.1074/jbc.M510023200
64. Abbas T, Dutta A (2009) p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 9(6):400–414. doi:10.1038/nrc2657
65. Al Dhaheri Y, Attoub S, Arafat K, Abuqamar S, Eid A, Al Faresi N, Iratni R (2013) Salinomycin induces apoptosis and senescence in breast cancer: upregulation of p21, downregulation of survivin and histone H3 and H4 hyperacetylation. Biochim Biophys Acta 1830(4):3121–3135. doi:10.1016/j.bbagen.2013.01.010