Targeting the SIN3A-PF1 interaction inhibits epithelial to mesenchymal transition and maintenance of a stem cell phenotype in triple negative breast cancer

Oncotarget

Volumn 6, Issue 33, 2015, Pages 34087-34105

  Bansal, Nidhi ^a   Petrie, Kevin ^b   Christova, Rossitza ^b   Chung, Chi Yeh ^a   Leibovitch, Boris A ^a   Howell, Louise ^b   Gil, Veronica ^b   Sbirkov, Yordan ^b   Lee, EunJee ^a   Wexler, Joanna ^a   Ariztia, Edgardo V ^a   Sharma, Rajal ^a   Zhu, Jun ^a   Bernstein, Emily ^a   Zhou, Ming Ming ^a   Zelent, Arthur ^c   Farias, Eduardo ^a   Waxman, Samuel ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

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

Author keywords

Cancer stem cells; Epigenetics; PF1; SIN3; Triple negative breast cancer

Indexed keywords

ADAPTOR PROTEIN; ESTROGEN RECEPTOR ALPHA; HISTONE H3; PEPTIDE DERIVATIVE; PROTEIN PF1; TRANSCRIPTION FACTOR SIN3A; TYROSYLGLYCYLARGINYLLYSYLLYSYLARGINYLARGINYLGLUTAMINYLGLYCYLGLYCYLGLYCYLVALYLARGINYLMETHIONYLASPARAGINYLISOLEUCYLGLUTAMINYLMETHIONYLLEUCYLLEUCYLGLUTAMYLALANYLALANYLASPARTYLTYROSYLLEUCYLGLUTAMYLARGINYLARGINYLGLUTAMYLARGININE; UNCLASSIFIED DRUG; UVOMORULIN; HOMEODOMAIN PROTEIN; PHF12 PROTEIN, HUMAN; REPRESSOR PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SIN3A TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER CELL LINE; CANCER INHIBITION; CANCER STEM CELL; CDH1 GENE; CONTROLLED STUDY; DOWN REGULATION; DRUG SYNTHESIS; DRUG TARGETING; EPITHELIAL MESENCHYMAL TRANSITION; ESR1 GENE; EX VIVO STUDY; GENE EXPRESSION; GENE SILENCING; HISTONE METHYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; METASTASIS; MOUSE; NONHUMAN; PF1 GENE; PHENOTYPE; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; TRIPLE NEGATIVE BREAST CANCER; TUMOR GROWTH; TUMOR INVASION; ANIMAL; FEMALE; GENETICS; METABOLISM; MULTICELLULAR SPHEROID; PATHOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; TUMOR CELL CULTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; MICE; NEOPLASTIC STEM CELLS; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; SPHEROIDS, CELLULAR; TRANSCRIPTION FACTORS; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELLS, CULTURED;

EID: 84946569351     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6048     Document Type: Article

References (71)

1. Abramson VG and Mayer IA. Molecular Heterogeneity of Triple Negative Breast Cancer. Curr Breast Cancer Rep. 2014; 6:154-158.
2. Hudis CA and Gianni L. Triple-negative breast cancer: an unmet medical need. Oncologist. 2011; 16 Suppl 1:1-11.
3. Arnedos M, Bihan C, Delaloge S and Andre F. Triplenegative breast cancer: are we making headway at least? Ther Adv Med Oncol. 2012; 4:195-210.
4. Roll JD, Rivenbark AG, Sandhu R, Parker JS, Jones WD, Carey LA, Livasy CA and Coleman WB. Dysregulation of the epigenome in triple-negative breast cancers: basallike and claudin-low breast cancers express aberrant DNA hypermethylation. Exp Mol Pathol. 2013; 95:276-287.
5. Tam WL and Weinberg RA. The epigenetics of epithelialmesenchymal plasticity in cancer. Nat Med. 2013; 19:1438-1449.
6. Federico M and Bagella L. Histone deacetylase inhibitors in the treatment of hematological malignancies and solid tumors. J Biomed Biotechnol. 2011; 2011:475641.
7. Valdespino-Gomez VM and Valdespino-Castillo VE. [Targeted epigenetic therapy of cancer. Achievements and perspectives]. Cir Cir. 2012; 80:470-480.
8. Ho AS, Turcan S and Chan TA. Epigenetic therapy: use of agents targeting deacetylation and methylation in cancer management. Onco Targets Ther. 2013; 6:223-232.
9. Connolly R and Stearns V. Epigenetics as a therapeutic target in breast cancer. Journal of mammary gland biology and neoplasia. 2012; 17:191-204.
10. Kadamb R, Mittal S, Bansal N, Batra H and Saluja D. Sin3: insight into its transcription regulatory functions. Eur J Cell Biol. 2013; 92:237-246.
11. Bansal N, Kadamb R, Mittal S, Vig L, Sharma R, Dwarakanath BS and Saluja D. Tumor suppressor protein p53 recruits human Sin3B/HDAC1 complex for downregulation of its target promoters in response to genotoxic stress. PLoS One. 2011; 6:e26156.
12. Silverstein RA and Ekwall K. Sin3: a flexible regulator of global gene expression and genome stability. Curr Genet. 2005; 47:1-17.
13. Ellison-Zelski SJ and Alarid ET. Maximum growth and survival of estrogen receptor-alpha positive breast cancer cells requires the Sin3A transcriptional repressor. Mol Cancer. 2010; 9:263.
14. Ellison-Zelski SJ, Solodin NM and Alarid ET. Repression of ESR1 through actions of estrogen receptor alpha and Sin3A at the proximal promoter. Mol Cell Biol. 2009; 29:4949-4958.
15. Farias EF, Petrie K, Leibovitch B, Murtagh J, Chornet MB, Schenk T, Zelent A and Waxman S. Interference with Sin3 function induces epigenetic reprogramming and differentiation in breast cancer cells. Proc Natl Acad Sci U S A. 2010; 107:11811-11816.
16. Kwon YJ, Petrie K, Leibovitch BA, Zeng L, Mezei M, Howell L, Gil V, Christova R, Bansal N, Yang S, Sharma R, Ariztia EV, Frankum J, Brough R, Sbirkov Y, Ashworth A, et al. Selective inhibition of SIN3 corepressor with avermectins as a novel therapeutic strategy in triple negative breast cancer. Mol Cancer Ther. 2015 ;14:1824-36.
17. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, Mc Henry KT, Pinchback RM, Ligon AH, Cho YJ, Haery L, Greulich H, et al. The landscape of somatic copynumber alteration across human cancers. Nature. 2010; 463:899-905.
18. Jonsson G, Staaf J, Vallon-Christersson J, Ringner M, Holm K, Hegardt C, Gunnarsson H, Fagerholm R, Strand C, Agnarsson BA, Kilpivaara O, Luts L, Heikkila P, Aittomaki K, Blomqvist C, Loman N, et al. Genomic subtypes of breast cancer identified by array-comparative genomic hybridization display distinct molecular and clinical characteristics. Breast Cancer Res. 2010; 12:R42.
19. Ayer DE, Lawrence QA and Eisenman RN. Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell. 1995; 80:767-776.
20. Yochum GS and Ayer DE. Pf1, a novel PHD zinc finger protein that links the TLE corepressor to the mSin3Ahistone deacetylase complex. Mol Cell Biol. 2001; 21:4110-4118.
21. Swanson KA, Knoepfler PS, Huang K, Kang RS, Cowley SM, Laherty CD, Eisenman RN and Radhakrishnan I. HBP1 and Mad1 repressors bind the Sin3 corepressor PAH2 domain with opposite helical orientations. Nat Struct Mol Biol. 2004; 11:738-746.
22. Le Guezennec X, Vermeulen M and Stunnenberg HG. Molecular characterization of Sin3 PAH-domain interactor specificity and identification of PAH partners. Nucleic Acids Res. 2006; 34:3929-3937.
23. Yochum GS and Ayer DE. Role for the mortality factors MORF4, MRGX, and MRG15 in transcriptional repression via associations with Pf1, mSin3A, and Transducin-Like Enhancer of Split. Mol Cell Biol. 2002; 22:7868-7876.
24. Malovannaya A, Lanz RB, Jung SY, Bulynko Y, Le NT, Chan DW, Ding C, Shi Y, Yucer N, Krenciute G, Kim BJ, Li C, Chen R, Li W, Wang Y, O'Malley BW, et al. Analysis of the human endogenous coregulator complexome. Cell. 2011; 145:787-799.
25. Moshkin YM, Kan TW, Goodfellow H, Bezstarosti K, Maeda RK, Pilyugin M, Karch F, Bray SJ, Demmers JA and Verrijzer CP. Histone chaperones ASF1 and NAP1 differentially modulate removal of active histone marks by LID-RPD3 complexes during NOTCH silencing. Mol Cell. 2009; 35:782-793.
26. Barrett A, Santangelo S, Tan K, Catchpole S, Roberts K, Spencer-Dene B, Hall D, Scibetta A, Burchell J, Verdin E, Freemont P and Taylor-Papadimitriou J. Breast cancer associated transcriptional repressor PLU-1/JARID1B interacts directly with histone deacetylases. Int J Cancer. 2007; 121:265-275.
27. Catchpole S, Spencer-Dene B, Hall D, Santangelo S, Rosewell I, Guenatri M, Beatson R, Scibetta AG, Burchell JM and Taylor-Papadimitriou J. PLU-1/JARID1B/KDM5B is required for embryonic survival and contributes to cell proliferation in the mammary gland and in ER+ breast cancer cells. Int J Oncol. 2011; 38:1267-1277.
28. Mitra D, Das PM, Huynh FC and Jones FE. Jumonji/ARID1 B (JARID1B) protein promotes breast tumor cell cycle progression through epigenetic repression of microRNA let-7e. J Biol Chem. 2011; 286:40531-40535.
29. Vire E, Curtis C, Davalos V, Git A, Robson S, Villanueva A, Vidal A, Barbieri I, Aparicio S, Esteller M, Caldas C and Kouzarides T. The breast cancer oncogene EMSY represses transcription of antimetastatic microRNA miR-31. Mol Cell. 2014; 53:806-818.
30. Yamamoto S, Wu Z, Russnes HG, Takagi S, Peluffo G, Vaske C, Zhao X, Moen Vollan HK, Maruyama R, Ekram MB, Sun H, Kim JH, Carver K, Zucca M, Feng J, Almendro V, et al. JARID1B is a luminal lineage-driving oncogene in breast cancer. Cancer Cell. 2014; 25:762-777.
31. Kumar GS, Xie T, Zhang Y and Radhakrishnan I. Solution structure of the mSin3A PAH2-Pf1 SID1 complex: a Mad1/Mxd1-like interaction disrupted by MRG15 in the Rpd3S/Sin3S complex. J Mol Biol. 2011; 408:987-1000.
32. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, Itzkovitz S, Noske A, Zurrer-Hardi U, Bell G, Tam WL, Mani SA, van Oudenaarden A and Weinberg RA. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell. 2012; 148:1015-1028.
33. Ricardo S, Vieira AF, Gerhard R, Leitao D, Pinto R, Cameselle-Teijeiro JF, Milanezi F, Schmitt F and Paredes J. Breast cancer stem cell markers CD44, CD24 and ALDH1: expression distribution within intrinsic molecular subtype. J Clin Pathol. 2011; 64:937-946.
34. 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, 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.
35. Azzam DJ, Zhao D, Sun J, Minn AJ, Ranganathan P, Drews-Elger K, Han X, Picon-Ruiz M, Gilbert CA, Wander SA, Capobianco AJ, El-Ashry D and Slingerland JM. Triple negative breast cancer initiating cell subsets differ in functional and molecular characteristics and in gammasecretase inhibitor drug responses. EMBO Mol Med. 2013; 5:1502-1522.
36. 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 and Dontu G. 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.
37. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, BhatNakshatri P, Turner CH, Goulet R, Jr., Badve S and Nakshatri H. CD44+/CD24-breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res. 2006; 8:R59.
38. Honeth G, Bendahl PO, Ringner M, Saal LH, GruvbergerSaal SK, Lovgren K, Grabau D, Ferno M, Borg A and Hegardt C. The CD44+/CD24-phenotype is enriched in basal-like breast tumors. Breast Cancer Res. 2008; 10:R53.
39. Meyer MJ, Fleming JM, Lin AF, Hussnain SA, Ginsburg E and Vonderhaar BK. CD44posCD49fhiCD133/2hi defines xenograft-initiating cells in estrogen receptor-negative breast cancer. Cancer Res. 2010; 70:4624-4633.
40. To K, Fotovati A, Reipas KM, Law JH, Hu K, Wang J, Astanehe A, Davies AH, Lee L, Stratford AL, Raouf A, Johnson P, Berquin IM, Royer HD, Eaves CJ and Dunn SE. Y-box binding protein-1 induces the expression of CD44 and CD49f leading to enhanced self-renewal, mammosphere growth, and drug resistance. Cancer Res. 2010; 70:2840-2851.
41. Strobl-Mazzulla PH and Bronner ME. A PHD12-Snail2 repressive complex epigenetically mediates neural crest epithelial-to-mesenchymal transition. J Cell Biol. 2012; 198:999-1010.
42. Shiozawa Y, Eber MR, Berry JE and Taichman RS. Bone marrow as a metastatic niche for disseminated tumor cells from solid tumors. Bonekey Rep. 2015; 4:689.
43. Hartkopf AD, Stefanescu D, Wallwiener M, Hahn M, Becker S, Solomayer EF, Fehm TN, Brucker SY and Taran FA. Tumor cell dissemination to the bone marrow and blood is associated with poor outcome in patients with metastatic breast cancer. Breast Cancer Res Treat. 2014; 147:345-351.
44. Jelinic P, Pellegrino J and 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.
45. Roesch A, Fukunaga-Kalabis M, Schmidt EC, Zabierowski SE, Brafford PA, Vultur A, Basu D, Gimotty P, Vogt T and Herlyn M. A temporarily distinct subpopulation of slowcycling melanoma cells is required for continuous tumor growth. Cell. 2010; 141:583-594.
46. Enkhbaatar Z, Terashima M, Oktyabri D, Tange S, Ishimura A, Yano S and Suzuki T. KDM5B histone demethylase controls epithelial-mesenchymal transition of cancer cells by regulating the expression of the microRNA-200 family. Cell Cycle. 2013; 12:2100-2112.
47. Kidder BL, Hu G and Zhao K. KDM5B focuses H3K4 methylation near promoters and enhancers during embryonic stem cell self-renewal and differentiation. Genome Biol. 2014; 15:R32.
48. Krishnakumar R and Kraus WL. PARP-1 regulates chromatin structure and transcription through a KDM5Bdependent pathway. Mol Cell. 2010; 39:736-749.
49. Zou MR, Cao J, Liu Z, Huh SJ, Polyak K and Yan Q. Histone demethylase jumonji AT-rich interactive domain 1B (JARID1B) controls mammary gland development by regulating key developmental and lineage specification genes. J Biol Chem. 2014; 289:17620-17633.
50. Baymaz HI, Karemaker ID and Vermeulen M. Perspective on unraveling the versatility of 'co-repressor' complexes. Biochim Biophys Acta. 2015; 1849:1051-1056.
51. Lee N, Erdjument-Bromage H, Tempst P, Jones RS and Zhang Y. The H3K4 demethylase lid associates with and inhibits histone deacetylase Rpd3. Mol Cell Biol. 2009; 29:1401-1410.
52. Johnsen SA, Subramaniam M, Janknecht R and Spelsberg TC. TGFbeta inducible early gene enhances TGFbeta/Smad-dependent transcriptional responses. Oncogene. 2002; 21:5783-5790.
53. Johnsen SA, Subramaniam M, Katagiri T, Janknecht R and Spelsberg TC. Transcriptional regulation of Smad2 is required for enhancement of TGFbeta/Smad signaling by TGFbeta inducible early gene. Journal of cellular biochemistry. 2002; 87:233-241.
54. Dave B, Mittal V, Tan NM and Chang JC. Epithelialmesenchymal transition, cancer stem cells and treatment resistance. Breast Cancer Res. 2012; 14:202.
55. Blick T, Hugo H, Widodo E, Waltham M, Pinto C, Mani SA, Weinberg RA, Neve RM, Lenburg ME and Thompson EW. Epithelial mesenchymal transition traits in human breast cancer cell lines parallel the CD44(hi/)CD24 (lo/-) stem cell phenotype in human breast cancer. J Mammary Gland Biol Neoplasia. 2010; 15:235-252.
56. Croker AK, Goodale D, Chu J, Postenka C, Hedley BD, Hess DA and Allan AL. High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J Cell Mol Med. 2009; 13:2236-2252.
57. Vesuna F, Lisok A, Kimble B and Raman V. Twist modulates breast cancer stem cells by transcriptional regulation of CD24 expression. Neoplasia. 2009; 11:1318-1328.
58. Muenst S, Daster S, Obermann EC, Droeser RA, Weber WP, von Holzen U, Gao F, Viehl C, Oertli D and Soysal SD. Nuclear expression of snail is an independent negative prognostic factor in human breast cancer. Dis Markers. 2013; 35:337-344.
59. Peinado H, Ballestar E, Esteller M and Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol Cell Biol. 2004; 24:306-319.
60. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J and Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol. 2000; 2:84-89.
61. Dhasarathy A, Kajita M and Wade PA. The transcription factor snail mediates epithelial to mesenchymal transitions by repression of estrogen receptor-alpha. Mol Endocrinol. 2007; 21:2907-2918.
62. Bosch A, Bertran SP, Lu Y, Garcia A, Jones AM, Dawson MI and Farias EF. Reversal by RARalpha agonist Am580 of c-Myc-induced imbalance in RARalpha/RARgamma expression during MMTV-Myc tumorigenesis. Breast Cancer Res. 2012; 14:R121.
63. Stewart TA, Pattengale PK and Leder P. Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell. 1984; 38:627-637.
64. Debnath J, Muthuswamy SK and Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods. 2003; 30:256-268.
65. Gaspar-Maia A, Qadeer ZA, Hasson D, Ratnakumar K, Leu NA, Leroy G, Liu S, Costanzi C, Valle-Garcia D, Schaniel C, Lemischka I, Garcia B, Pehrson JR and Bernstein E. MacroH2A histone variants act as a barrier upon reprogramming towards pluripotency. Nat Commun. 2013; 4:1565.
66. Mendoza-Parra MA, Van Gool W, Mohamed Saleem MA, Ceschin DG and Gronemeyer H. A quality control system for profiles obtained by ChIP sequencing. Nucleic Acids Res. 2013; 41:e196.
67. Langmead B, Trapnell C, Pop M and Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10:R25.
68. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W and Liu XS. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008; 9:R137.
69. Zang C, Schones DE, Zeng C, Cui K, Zhao K and Peng W. A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics. 2009; 25:1952-1958.
70. Liu T, Ortiz JA, Taing L, Meyer CA, Lee B, Zhang Y, Shin H, Wong SS, Ma J, Lei Y, Pape UJ, Poidinger M, Chen Y, Yeung K, Brown M, Turpaz Y, et al. Cistrome: an integrative platform for transcriptional regulation studies. Genome Biol. 2011; 12:R83.
71. Aslakson CJ and Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 1992; 52:1399-1405.