Selective inhibition of SIN3 corepressor with avermectins as a novel therapeutic strategy in triple-negative breast cancer

Molecular Cancer Therapeutics

Volumn 14, Issue 8, 2015, Pages 1824-1836

  Kwon, Yeon Jin ^a   Petrie, Kevin ^b   Leibovitch, Boris A ^a   Zeng, Lei ^a   Mezei, Mihaly ^a   Howell, Louise ^b   Gil, Veronica ^b   Christova, Rossitza ^b   Bansal, Nidhi ^a   Yang, Shuai ^a   Sharma, Rajal ^a   Ariztia, Edgardo V ^a   Frankum, Jessica ^b   Brough, Rachel ^b   Sbirkov, Yordan ^b   Ashworth, Alan ^b   Lord, Christopher J ^b   Zelent, Arthur ^b,c   Farias, Eduardo ^a   Zhou, Ming Ming ^a   Waxman, Samuel ^a   more..

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c UNIVERSITY OF MIAMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 TERT BUTYL 3 [6 (3,5 DIMETHOXYPHENYL) 2 (4 DIETHYLAMINOBUTYLAMINO)PYRIDO[2,3 D]PYRIMIDIN 7 YL]UREA; 2 AMINO 8 [4 (2 HYDROXYETHOXY)CYCLOHEXYL] 6 (6 METHOXY 3 PYRIDINYL) 4 METHYLPYRIDO[2,3 D]PYRIMIDIN 7(8H) ONE; 8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; AFIMOXIFENE; AZD 4547; ESTROGEN RECEPTOR ALPHA; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; FIBROBLAST GROWTH FACTOR RECEPTOR 4; GELATINASE B; INHIBITOR OF DIFFERENTIATION 2; INTEGRIN LINKED KINASE; IVERMECTIN; N [3 (5 CHLORO 1H PYRROLO[2,3 B]PYRIDINE 3 CARBONYL) 2,4 DIFLUOROPHENYL]PROPANESULFONAMIDE; PEPTIDE; PEVONEDISTAT; PROTEIN TYROSINE KINASE; RUCAPARIB; SELAMECTIN; SIN3 INTERACTION DOMAIN PEPTIDE; SMAD2 PROTEIN; SOTRASTAURIN; SUNITINIB; TAMOXIFEN; TRANSCRIPTION FACTOR SIN3A; UNCLASSIFIED DRUG; UNINDEXED DRUG; UVOMORULIN; WNT5A PROTEIN; ANTIPARASITIC AGENT; AVERMECTIN; CADHERIN; CDH1 PROTEIN, HUMAN; ESTROGEN RECEPTOR ALPHA, HUMAN; REPRESSOR PROTEIN;

ALPHA HELIX; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; CANCER INHIBITION; CANCER STEM CELL; CELL RENEWAL; CLINICAL ASSESSMENT; CLINICAL EFFECTIVENESS; COMPUTER MODEL; DISTANT METASTASIS; DRUG SENSITIZATION; ENZYME INHIBITION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE TARGETING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MOLECULARLY TARGETED THERAPY; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; SENSITIVITY ANALYSIS; SYSTEMATIC REVIEW; TRIPLE NEGATIVE BREAST CANCER; TUMOR GROWTH; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; CHEMISTRY; CONFORMATION; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR MODEL; PATHOLOGY; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTIPARASITIC AGENTS; CADHERINS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IVERMECTIN; MICE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; REPRESSOR PROTEINS; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942124287     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-14-0980-T     Document Type: Article

References (67)

1. Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med 2010;363:1938-48.
2. Rakha EA, El-Sayed ME, Green AR, Lee AH, Robertson JF, Ellis IO. Prognostic markers in triple-negative breast cancer. Cancer 2007;109:25-32.
3. Tomao F, Papa A, Zaccarelli E, Rossi L, Caruso D, Minozzi M, et al. Triple-negative breast cancer: new perspectives for targeted therapies. Onco Targets Ther 2015;8:177-93.
4. Perou CM. Molecular stratification of triple-negative breast cancers. Oncologist 2011;16 Suppl 1:61-70.
5. Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours.Nature 2012;490:61-70.
6. Weigelt B, Baehner FL, Reis-Filho JS. The contribution of gene expression profiling to breast cancer classification, prognostication and prediction: a retrospective of the last decade. J Pathol 2010;220:263-80.
7. Roll JD, Rivenbark AG, Sandhu R, Parker JS, Jones WD, Carey LA, et al. Dysregulation of the epigenome in triple-negative breast cancers: basal-like and claudin-low breast cancers express aberrant DNA hypermethylation. Exp Mol Pathol 2013;95:276-87.
8. Kagara N, Huynh KT, Kuo C, Okano H, Sim MS, Elashoff D, et al. Epigenetic regulation of cancer stem cell genes in triple-negative breast cancer. Am J Pathol 2012;181:257-67.
9. Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med 2013;19:1438-49.
10. Farias EF, Petrie K, Leibovitch B, Murtagh J, Chornet MB, Schenk T, et al. Interference with Sin3 function induces epigenetic reprogramming and differentiation in breast cancer cells. Proc Natl Acad Sci U S A 2010;107:11811-6.
11. Ellison-Zelski SJ, Solodin NM, Alarid ET. Repression of ESR1 through actions of estrogen receptor alpha and Sin3A at the proximal promoter. Mol Cell Biol 2009;29:4949-58.
12. Ellison-Zelski SJ, Alarid ET. Maximum growth and survival of estrogen receptor-alpha positive breast cancer cells requires the Sin3A transcriptional repressor. Mol Cancer 2010;9:263.
13. Silverstein RA, Ekwall K. Sin3: a flexible regulator of global gene expression and genome stability. Curr Genet 2005;47:1-17.
14. Grzenda A, Lomberk G, Zhang JS, Urrutia R. Sin3: master scaffold and transcriptional corepressor. Biochim Biophys Acta 2009;1789:443-50.
15. Kadamb R, Mittal S, Bansal N, Batra H, Saluja D. Sin3: insight into its transcription regulatory functions. Eur J Cell Biol 2013;92:237-46.
16. Jenkins DE, Hornig YS, Oei Y, Dusich J, Purchio T. Bioluminescent human breast cancer cell lines that permit rapid and sensitive in vivo detection of mammary tumors and multiple metastases in immune deficient mice. Breast Cancer Res 2005;7:R444-54.
17. Bosch A, Bertran SP, Lu Y, Garcia A, Jones AM, Dawson MI, et al. Reversal by RARalpha agonist Am580 of c-Myc-induced imbalance in RARalpha/RARgamma expression during MMTV-Myc tumorigenesis. Breast Cancer Res 2012;14:R121.
18. Stewart TA, Pattengale PK, Leder P. Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell 1984;38:627-37.
19. Brubaker K, Cowley SM, Huang K, Loo L, Yochum GS, Ayer DE, et al. Solution structure of the interacting domains of the Mad-Sin3 complex: implications for recruitment of a chromatin-modifying complex. Cell 2000;103:655-65.
20. Clore GM, Gronenborn AM. Multidimensional heteronuclear nuclear magnetic resonance of proteins. Methods Enzymol 1994;239:349-63.
21. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, et al. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J Comput Chem 2009;30:2785-91.
22. Zsoldos Z, Reid D, Simon A, Sadjad SB, Johnson AP. eHiTS: a new fast, exhaustive flexible ligand docking system. J Mol Graph Model 2007;26:198-212.
23. Mezei M, Zhou MM. Dockres: a computer program that analyzes the output of virtual screening of small molecules. Source Code Biol Med 2010;5:2.
24. Ishii Y, Pirkmaier A, Alvarez JV, Frank DA, Keselman I, Logothetis D, et al. Cyclin D1 overexpression and response to bortezomib treatment in a breast cancer model. J Natl Cancer Inst 2006;98:1238-47.
25. Shaw FL, Harrison H, Spence K, Ablett MP, Simoes BM, Farnie G, et al. A detailed mammosphere assay protocol for the quantification of breast stem cell activity. J Mammary Gland Biol Neoplasia 2012;17:111-7.
26. Bajrami I, Kigozi A, Van Weverwijk A, Brough R, Frankum J, Lord CJ, et al. Synthetic lethality of PARP and NAMPT inhibition in triple-negative breast cancer cells. EMBO Mol Med 2012;4:1087-96.
27. Ayer DE, Laherty CD, Lawrence QA, Armstrong AP, Eisenman RN. Mad proteins contain a dominant transcription repression domain. Mol Cell Biol 1996;16:5772-81.
28. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J, et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 2006;3:995-1000.
29. Griffin J, Fletcher N, Clemence R, Blanchflower S, Brayden DJ. Selamectin is a potent substrate and inhibitor of human and canine P-glycoprotein. J Vet Pharmacol Ther 2005;28:257-65.
30. Nolan TJ, Lok JB. Macrocyclic lactones in the treatment and control of parasitism in small companion animals. Curr Pharm Biotechnol 2012;13:1078-94.
31. Lespine A, Dupuy J, Alvinerie M, Comera C, Nagy T, Krajcsi P, et al. Interaction of macrocyclic lactones with the multidrug transporters: the bases of the pharmacokinetics of lipid-like drugs. Curr Drug Metab 2009;10:272-88.
32. Monteiro P, Rosse C, Castro-Castro A, Irondelle M, Lagoutte E, Paul-Gilloteaux P, et al. Endosomal WASH and exocyst complexes control exocytosis of MT1-MMP at invadopodia. J Cell Biol 2013;203:1063-79.
33. Jacob A, Jing J, Lee J, Schedin P, Gilbert SM, Peden AA, et al. Rab40b regulates trafficking of MMP2 and MMP9 during invadopodia formation and invasion of breast cancer cells. J Cell Sci 2013;126:4647-58.
34. Baltus GA, Kowalski MP, Tutter AV, Kadam S. A positive regulatory role for the mSin3A-HDAC complex in pluripotency through Nanog and Sox2. J Biol Chem 2009;284:6998-7006.
35. 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;10:731-9.
36. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, 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;1:555-67.
37. Li K, Yao L, Chen L, Cao ZG, Yu SJ, Kuang XY, et al. ID2 predicts poor prognosis in breast cancer, especially in triple-negative breast cancer, and inhibits E-cadherin expression. Onco Targets Ther 2014;7:1083-94.
38. Larue L, Bellacosa A. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 30 kinase/AKT pathways. Oncogene 2005;24:7443-54.
39. Anastas JN, Moon RT. WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer 2013;13:11-26.
40. Katoh M, Nakagama H. FGF receptors: cancer biology and therapeutics. Med Res Rev 2014;34:280-300.
41. Hannigan G, Troussard AA, Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat Rev Cancer 2005;5:51-63.
42. Davison Z, de Blacquiere GE, Westley BR, May FE. Insulin-like growth factor-dependent proliferation and survival of triple-negative breast cancer cells: implications for therapy. Neoplasia 2011;13:504-15.
43. Gordon V, Banerji S. Molecular pathways: PI3K pathway targets in triple-negative breast cancers. Clin Cancer Res 2013;19:3738-44.
44. Galliher AJ, Schiemann WP. Beta3 integrin and Src facilitate transforming growth factor-beta mediated induction of epithelial-mesenchymal transition in mammary epithelial cells. Breast Cancer Res 2006;8:R42.
45. Seguin L, Kato S, Franovic A, Camargo MF, Lesperance J, Elliott KC, et al. An integrin beta(3)-KRAS-RalB complex drives tumour stemness and resistance to EGFR inhibition. Nat Cell Biol 2014;16:457-68.
46. Mitra D, Das PM, Huynh FC, Jones FE. Jumonji/ARID1 B (JARID1B) protein promotes breast tumor cell cycle progression through epigenetic repression of microRNA let-7e. J Biol Chem 2011;286:40531-5.
47. Vire E, Curtis C, Davalos V, Git A, Robson S, Villanueva A, et al. The breast cancer oncogene EMSY represses transcription of antimetastatic microRNA miR-31. Mol Cell 2014;53:806-18.
48. Yamamoto S, Wu Z, Russnes HG, Takagi S, Peluffo G, Vaske C, et al. JARID1B is a luminal lineage-driving oncogene in breast cancer. Cancer Cell 2014;25:762-77.
49. Jelinic P, Pellegrino J, David G. A novel mammalian complex containing Sin3B mitigates histone acetylation and RNA polymerase II progression within transcribed loci. Mol Cell Biol 2011;31:54-62.
50. Johnsen SA, Subramaniam M, Janknecht R, Spelsberg TC. TGFbeta inducible early gene enhances TGFbeta/Smad-dependent transcriptional responses. Oncogene 2002;21:5783-90.
51. Johnsen SA, Subramaniam M, Katagiri T, Janknecht R, Spelsberg TC. Transcriptional regulation of Smad2 is required for enhancement of TGFbeta/Smad signaling by TGFbeta inducible early gene. J Cell Biochem 2002;87:233-41.
52. Sanchez-Tillo E, Lazaro A, Torrent R, Cuatrecasas M, Vaquero EC, Castells A, et al. ZEB1 represses E-cadherin and induces an EMT by recruiting the SWI/SNF chromatin-remodeling protein BRG1. Oncogene 2010;29:3490-500.
53. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998;393:386-9.
54. Boeke J, Ammerpohl O, Kegel S, Moehren U, Renkawitz R. The minimal repression domain of MBD2b overlaps with the methyl-CpG-binding domain and binds directly to Sin3A. J Biol Chem 2000;275:34963-7.
55. Geiman TM, Sankpal UT, Robertson AK, Chen Y, Mazumdar M, Heale JT, et al. Isolation and characterization of a novel DNA methyltransferase complex linking DNMT3B with components of the mitotic chromosome condensation machinery. Nucleic Acids Res 2004;32:2716-29.
56. Cortazar P, Zhang L, Untch M, Mehta K, Costantino JP, Wolmark N, et al. Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet 2014;384:164-72.
57. Liedtke C, Mazouni C, Hess KR, Andre F, Tordai A, Mejia JA, et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J Clin Oncol 2008;26:1275-81.
58. Sharma D, Saxena NK, Davidson NE, Vertino PM. Restoration of tamoxifen sensitivity in estrogen receptor-negative breast cancer cells: tamoxifen-bound reactivated ER recruits distinctive corepressor complexes. Cancer Res 2006;66:6370-8.
59. Kassam F, Enright K, Dent R, Dranitsaris G, Myers J, Flynn C, et al. Survival outcomes for patients with metastatic triple-negative breast cancer: implications for clinical practice and trial design. Clin Breast Cancer 2009;9:29-33.
60. Al-Lazikani B, Banerji U, Workman P. Combinatorial drug therapy for cancer in the post-genomic era. Nat Biotechnol 2012;30:679-92.
61. Balch C, Nephew KP. Epigenetic targeting therapies to overcome chemotherapy resistance. Adv Exp Med Biol 2013;754:285-311.
62. Melotti A, Mas C, Kuciak M, Lorente-Trigos A, Borges I, Ruiz IAA. The river blindness drug Ivermectin and related macrocyclic lactones inhibit WNT-TCF pathway responses in human cancer. EMBO Mol Med 2014;6:1263-78.
63. Thylefors B. The Mectizan Donation Program (MDP). Ann Trop Med Parasitol 2008;102 Suppl 1:39-44.
64. Yang CC. Acute human toxicity of macrocyclic lactones. Curr Pharm Biotechnol 2012;13:999-1003.
65. Pacque M, Munoz B, Poetschke G, Foose J, Greene BM, Taylor HR. Pregnancy outcome after inadvertent ivermectin treatment during community-based distribution. Lancet 1990;336:1486-9.
66. Kokoz YM, Tsyganova VG, Korystova AF, Grichenko AS, Zenchenko KI, Drinyaev VA, et al. Selective cytostatic and neurotoxic effects of avermectins and activation of the GABAalpha receptors. Biosci Rep 1999;19:535-46.
67. Mealey KL, Bentjen SA, Gay JM, Cantor GH. Ivermectin sensitivity in collies is associated with a deletion mutation of the mdr1 gene. Pharmacogenetics 2001;11:727-33.