Endocrine resistance and breast cancer plasticity are controlled by CoREST.
Journal
Nature structural & molecular biology
ISSN: 1545-9985
Titre abrégé: Nat Struct Mol Biol
Pays: United States
ID NLM: 101186374
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
received:
16
09
2021
accepted:
29
09
2022
pubmed:
8
11
2022
medline:
18
11
2022
entrez:
7
11
2022
Statut:
ppublish
Résumé
Resistance to cancer treatment remains a major clinical hurdle. Here, we demonstrate that the CoREST complex is a key determinant of endocrine resistance and ER
Identifiants
pubmed: 36344844
doi: 10.1038/s41594-022-00856-x
pii: 10.1038/s41594-022-00856-x
pmc: PMC9707522
mid: NIHMS1844909
doi:
Substances chimiques
Co-Repressor Proteins
0
Histone Demethylases
EC 1.14.11.-
Nerve Tissue Proteins
0
Chromatin
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1122-1135Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM141349
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA240139
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA233945
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM121595
Pays : United States
Organisme : NIH HHS
ID : S10 OD030286
Pays : United States
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature America, Inc.
Références
Siegel, R. L., Miller, K. D. & Jemal, A. Cancer statistics, 2020. CA Cancer J. Clin. 70, 7–30 (2020).
pubmed: 31912902
doi: 10.3322/caac.21590
DeSantis, C. E. et al. Breast cancer statistics, 2019. CA Cancer J. Clin. 69, 438–451 (2019).
pubmed: 31577379
doi: 10.3322/caac.21583
Hanker, A. B., Sudhan, D. R. & Arteaga, C. L. Overcoming endocrine resistance in breast cancer. Cancer Cell 37, 496–513 (2020).
pubmed: 32289273
pmcid: 7169993
doi: 10.1016/j.ccell.2020.03.009
Patten, D. K. et al. Enhancer mapping uncovers phenotypic heterogeneity and evolution in patients with luminal breast cancer. Nat. Med. 24, 1469–1480 (2018).
pubmed: 30038216
pmcid: 6130800
doi: 10.1038/s41591-018-0091-x
Marine, J. C., Dawson, S. J. & Dawson, M. A. Non-genetic mechanisms of therapeutic resistance in cancer. Nat. Rev. Cancer 20, 743–756 (2020).
pubmed: 33033407
doi: 10.1038/s41568-020-00302-4
Zhu, C. et al. A non-canonical role of YAP/TEAD is required for activation of estrogen-regulated enhancers in breast cancer. Mol. Cell 75, 791–806 (2019).
pubmed: 31303470
pmcid: 6707877
doi: 10.1016/j.molcel.2019.06.010
Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43–49 (2011).
pubmed: 21441907
pmcid: 3088773
doi: 10.1038/nature09906
Garcia-Martinez, L., Zhang, Y., Nakata, Y., Chan, H. L. & Morey, L. Epigenetic mechanisms in breast cancer therapy and resistance. Nat. Commun. 12, 1786 (2021).
pubmed: 33741974
pmcid: 7979820
doi: 10.1038/s41467-021-22024-3
Sharma, S. V. et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69–80 (2010).
pubmed: 20371346
pmcid: 2851638
doi: 10.1016/j.cell.2010.02.027
Boumahdi, S. & de Sauvage, F. J. The great escape: tumour cell plasticity in resistance to targeted therapy. Nat. Rev. Drug Discov. 19, 39–56 (2020).
pubmed: 31601994
doi: 10.1038/s41573-019-0044-1
Razavi, P. et al. The genomic landscape of endocrine-resistant advanced breast cancers. Cancer Cell 34, 427–438 (2018).
pubmed: 30205045
pmcid: 6327853
doi: 10.1016/j.ccell.2018.08.008
Ellis, M. J. et al. Whole-genome analysis informs breast cancer response to aromatase inhibition. Nature 486, 353–360 (2012).
pubmed: 22722193
pmcid: 3383766
doi: 10.1038/nature11143
Berns, E. M. et al. Complete sequencing of TP53 predicts poor response to systemic therapy of advanced breast cancer. Cancer Res. 60, 2155–2162 (2000).
pubmed: 10786679
Abubakar, M. et al. Clinicopathological and epidemiological significance of breast cancer subtype reclassification based on p53 immunohistochemical expression. NPJ Breast Cancer 5, 20 (2019).
pubmed: 31372496
pmcid: 6658470
doi: 10.1038/s41523-019-0117-7
Yamashita, H. et al. p53 protein accumulation predicts resistance to endocrine therapy and decreased post-relapse survival in metastatic breast cancer. Breast Cancer Res. 8, R48 (2006).
pubmed: 16869955
pmcid: 1779473
doi: 10.1186/bcr1536
Yamamoto, M. et al. p53 accumulation is a strong predictor of recurrence in estrogen receptor-positive breast cancer patients treated with aromatase inhibitors. Cancer Sci. 105, 81–88 (2014).
pubmed: 24118529
doi: 10.1111/cas.12302
Bertucci, F. et al. Genomic characterization of metastatic breast cancers. Nature 569, 560–564 (2019).
pubmed: 31118521
doi: 10.1038/s41586-019-1056-z
Silwal-Pandit, L., Langerod, A. & Borresen-Dale, A. L. TP53 mutations in breast and ovarian cancer. Cold Spring Harb. Perspect. Med. 7, a026252 (2017).
Yates, L. R. et al. Genomic evolution of breast cancer metastasis and relapse. Cancer Cell 32, 169–184 (2017).
pubmed: 28810143
pmcid: 5559645
doi: 10.1016/j.ccell.2017.07.005
Lee, M. G., Wynder, C., Cooch, N. & Shiekhattar, R. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437, 432–435 (2005).
pubmed: 16079794
doi: 10.1038/nature04021
Shi, Y. et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941–953 (2004).
pubmed: 15620353
doi: 10.1016/j.cell.2004.12.012
Perillo, B., Tramontano, A., Pezone, A. & Migliaccio, A. LSD1: more than demethylation of histone lysine residues. Exp. Mol. Med 52, 1936–1947 (2020).
pubmed: 33318631
pmcid: 8080763
doi: 10.1038/s12276-020-00542-2
Magliulo, D., Bernardi, R. & Messina, S. Lysine-specific demethylase 1A as a promising target in acute myeloid leukemia. Front Oncol. 8, 255 (2018).
pubmed: 30073149
pmcid: 6060236
doi: 10.3389/fonc.2018.00255
Bennani-Baiti, I. M., Machado, I., Llombart-Bosch, A. & Kovar, H. Lysine-specific demethylase 1 (LSD1/KDM1A/AOF2/BHC110) is expressed and is an epigenetic drug target in chondrosarcoma, Ewing’s sarcoma, osteosarcoma, and rhabdomyosarcoma. Hum. Pathol. 43, 1300–1307 (2012).
pubmed: 22245111
doi: 10.1016/j.humpath.2011.10.010
Wang, Y. et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138, 660–672 (2009).
pubmed: 19703393
doi: 10.1016/j.cell.2009.05.050
Wu, Y. et al. The deubiquitinase USP28 stabilizes LSD1 and confers stem-cell-like traits to breast cancer cells. Cell Rep. 5, 224–236 (2013).
pubmed: 24075993
pmcid: 4004762
doi: 10.1016/j.celrep.2013.08.030
Shahbandi, A., Nguyen, H. D. & Jackson, J. G. TP53 mutations and outcomes in breast cancer: reading beyond the headlines. Trends Cancer 6, 98–110 (2020).
pubmed: 32061310
pmcid: 7931175
doi: 10.1016/j.trecan.2020.01.007
Fu, X. et al. FOXA1 overexpression mediates endocrine resistance by altering the ER transcriptome and IL-8 expression in ER-positive breast cancer. Proc. Natl Acad. Sci. USA 113, E6600–E6609 (2016).
pubmed: 27791031
pmcid: 5087040
doi: 10.1073/pnas.1612835113
Jeselsohn, R. et al. Embryonic transcription factor SOX9 drives breast cancer endocrine resistance. Proc. Natl Acad. Sci. USA 114, E4482–E4491 (2017).
pubmed: 28507152
pmcid: 5465894
doi: 10.1073/pnas.1620993114
Morrison, G. et al. Therapeutic potential of the dual EGFR/HER2 inhibitor AZD8931 in circumventing endocrine resistance. Breast Cancer Res. Treat. 144, 263–272 (2014).
pubmed: 24554387
pmcid: 4030601
doi: 10.1007/s10549-014-2878-x
Murphy, C. S., Pink, J. J. & Jordan, V. C. Characterization of a receptor-negative, hormone-nonresponsive clone derived from a T47D human breast cancer cell line kept under estrogen-free conditions. Cancer Res. 50, 7285–7292 (1990).
pubmed: 2224859
Murphy, C. S., Meisner, L. F., Wu, S. Q. & Jordan, V. C. Short- and long-term estrogen deprivation of T47D human breast cancer cells in culture. Eur. J. Cancer Clin. Oncol. 25, 1777–1788 (1989).
pubmed: 2632259
doi: 10.1016/0277-5379(89)90348-9
Inman, J. L., Robertson, C., Mott, J. D. & Bissell, M. J. Mammary gland development: cell fate specification, stem cells and the microenvironment. Development 142, 1028–1042 (2015).
pubmed: 25758218
doi: 10.1242/dev.087643
Idowu, M. O. et al. CD44
pubmed: 21835433
doi: 10.1016/j.humpath.2011.05.005
Honeth, G. et al. The CD44
pubmed: 18559090
pmcid: 2481503
doi: 10.1186/bcr2108
Fang, Y., Liao, G. & Yu, B. LSD1/KDM1A inhibitors in clinical trials: advances and prospects. J. Hematol. Oncol. 12, 129 (2019).
pubmed: 31801559
pmcid: 6894138
doi: 10.1186/s13045-019-0811-9
Ravasio, R. et al. Targeting the scaffolding role of LSD1 (KDM1A) poises acute myeloid leukemia cells for retinoic acid-induced differentiation. Sci. Adv. 6, eaax2746 (2020).
pubmed: 32284990
pmcid: 7141832
doi: 10.1126/sciadv.aax2746
Anastas, J. N. et al. Re-programing chromatin with a bifunctional LSD1/HDAC inhibitor induces therapeutic differentiation in DIPG. Cancer Cell 36, 528–544 (2019).
pubmed: 31631026
doi: 10.1016/j.ccell.2019.09.005
Kalin, J. H. et al. Targeting the CoREST complex with dual histone deacetylase and demethylase inhibitors. Nat. Commun. 9, 53 (2018).
pubmed: 29302039
pmcid: 5754352
doi: 10.1038/s41467-017-02242-4
Foster, C. T. et al. Lysine-specific demethylase 1 regulates the embryonic transcriptome and CoREST stability. Mol. Cell. Biol. 30, 4851–4863 (2010).
pubmed: 20713442
pmcid: 2950538
doi: 10.1128/MCB.00521-10
Luo, H. et al. MOF acetylates the histone demethylase LSD1 to suppress epithelial-to-mesenchymal transition. Cell Rep. 15, 2665–2678 (2016).
pubmed: 27292636
doi: 10.1016/j.celrep.2016.05.050
Zhang, J. et al. SFMBT1 functions with LSD1 to regulate expression of canonical histone genes and chromatin-related factors. Genes Dev. 27, 749–766 (2013).
pubmed: 23592795
pmcid: 3639416
doi: 10.1101/gad.210963.112
Liu, J. et al. Arginine methylation-dependent LSD1 stability promotes invasion and metastasis of breast cancer. EMBO Rep. 21, e48597 (2020).
pubmed: 31833203
doi: 10.15252/embr.201948597
Bahreini, A. et al. Mutation site and context dependent effects of ESR1 mutation in genome-edited breast cancer cell models. Breast Cancer Res. 19, 60 (2017).
pubmed: 28535794
pmcid: 5442865
doi: 10.1186/s13058-017-0851-4
Fang, R. et al. Human LSD2/KDM1b/AOF1 regulates gene transcription by modulating intragenic H3K4me2 methylation. Mol. Cell 39, 222–233 (2010).
pubmed: 20670891
pmcid: 3518444
doi: 10.1016/j.molcel.2010.07.008
Karytinos, A. et al. A novel mammalian flavin-dependent histone demethylase. J. Biol. Chem. 284, 17775–17782 (2009).
pubmed: 19407342
pmcid: 2719416
doi: 10.1074/jbc.M109.003087
Hatzi, K. et al. Histone demethylase LSD1 is required for germinal center formation and BCL6-driven lymphomagenesis. Nat. Immunol. 20, 86–96 (2019).
pubmed: 30538335
doi: 10.1038/s41590-018-0273-1
Grose, R. Epithelial migration: open your eyes to c-Jun. Curr. Biol. 13, R678–R680 (2003).
pubmed: 12956972
doi: 10.1016/S0960-9822(03)00607-9
Sioletic, S. et al. c-Jun promotes cell migration and drives expression of the motility factor ENPP2 in soft tissue sarcomas. J. Pathol. 234, 190–202 (2014).
pubmed: 24852265
pmcid: 4472460
Zhang, Y. et al. Critical role of c-Jun overexpression in liver metastasis of human breast cancer xenograft model. BMC Cancer 7, 145 (2007).
pubmed: 17672916
pmcid: 1959235
doi: 10.1186/1471-2407-7-145
Kappelmann-Fenzl, M. et al. c-Jun drives melanoma progression in PTEN wild type melanoma cells. Cell Death Dis. 10, 584 (2019).
pubmed: 31378787
pmcid: 6680049
doi: 10.1038/s41419-019-1821-9
Malorni, L. et al. Blockade of AP-1 potentiates endocrine therapy and overcomes resistance. Mol. Cancer Res. 14, 470–481 (2016).
pubmed: 26965145
pmcid: 4867274
doi: 10.1158/1541-7786.MCR-15-0423
Bi, M. et al. Enhancer reprogramming driven by high-order assemblies of transcription factors promotes phenotypic plasticity and breast cancer endocrine resistance. Nat. Cell Biol. 22, 701–715 (2020).
pubmed: 32424275
pmcid: 7737911
doi: 10.1038/s41556-020-0514-z
Munne, P. M. et al. Compressive stress-mediated p38 activation required for ERα + phenotype in breast cancer. Nat. Commun. 12, 6967 (2021).
pubmed: 34845227
pmcid: 8630031
doi: 10.1038/s41467-021-27220-9
Gross, K., Wronski, A., Skibinski, A., Phillips, S. & Kuperwasser, C. Cell fate decisions during breast cancer development. J. Dev. Biol. 4, 4 (2016).
pubmed: 27110512
pmcid: 4840277
doi: 10.3390/jdb4010004
Ku, S. Y. et al. Rb1 and Trp53 cooperate to suppress prostate cancer lineage plasticity, metastasis, and antiandrogen resistance. Science 355, 78–83 (2017).
pubmed: 28059767
pmcid: 5367887
doi: 10.1126/science.aah4199
Gao, S. et al. Chromatin binding of FOXA1 is promoted by LSD1-mediated demethylation in prostate cancer. Nat. Genet. 52, 1011–1017 (2020).
pubmed: 32868907
pmcid: 7541538
doi: 10.1038/s41588-020-0681-7
Smith, L. M. et al. cJun overexpression in MCF-7 breast cancer cells produces a tumorigenic, invasive and hormone resistant phenotype. Oncogene 18, 6063–6070 (1999).
pubmed: 10557095
doi: 10.1038/sj.onc.1202989
Beroukhim, R. et al. The landscape of somatic copy-number alteration across human cancers. Nature 463, 899–905 (2010).
pubmed: 20164920
pmcid: 2826709
doi: 10.1038/nature08822
Mariani, O. et al. JUN oncogene amplification and overexpression block adipocytic differentiation in highly aggressive sarcomas. Cancer Cell 11, 361–374 (2007).
pubmed: 17418412
doi: 10.1016/j.ccr.2007.02.007
Shao, J. et al. COP1 and GSK3β cooperate to promote c-Jun degradation and inhibit breast cancer cell tumorigenesis. Neoplasia 15, 1075–1085 (2013).
pubmed: 24027432
pmcid: 3769886
doi: 10.1593/neo.13966
Musgrove, E. A. & Sutherland, R. L. Biological determinants of endocrine resistance in breast cancer. Nat. Rev. Cancer 9, 631–643 (2009).
pubmed: 19701242
doi: 10.1038/nrc2713
Zhang, X., Jin, B. & Huang, C. The PI3K/Akt pathway and its downstream transcriptional factors as targets for chemoprevention. Curr. Cancer Drug Targets 7, 305–316 (2007).
pubmed: 17979625
doi: 10.2174/156800907780809741
Wang, L. et al. CARM1 methylates chromatin remodeling factor BAF155 to enhance tumor progression and metastasis. Cancer Cell 25, 21–36 (2014).
pubmed: 24434208
pmcid: 4004525
doi: 10.1016/j.ccr.2013.12.007
Mohammad, H. P., Barbash, O. & Creasy, C. L. Targeting epigenetic modifications in cancer therapy: erasing the roadmap to cancer. Nat. Med. 25, 403–418 (2019).
pubmed: 30842676
doi: 10.1038/s41591-019-0376-8
Sehrawat, A. et al. LSD1 activates a lethal prostate cancer gene network independently of its demethylase function. Proc. Natl Acad. Sci. USA 115, E4179–E4188 (2018).
pubmed: 29581250
pmcid: 5939079
doi: 10.1073/pnas.1719168115
Zhang, Y. et al. The Polycomb protein RING1B enables estrogen-mediated gene expression by promoting enhancer-promoter interaction and R-loop formation. Nucleic Acids Res. 49, 9768–9782 (2021).
pubmed: 34428304
pmcid: 8464076
doi: 10.1093/nar/gkab723
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).
pubmed: 24097267
pmcid: 3959825
doi: 10.1038/nmeth.2688
Aguilan, J. T., Kulej, K. & Sidoli, S. Guide for protein fold change and P value calculation for non-experts in proteomics. Mol. Omics 16, 573–582 (2020).
pubmed: 32968743
doi: 10.1039/D0MO00087F
Yuan, Z. F. et al. EpiProfile 2.0: a computational platform for processing epi-proteomics mass spectrometry data. J. Proteome Res. 17, 2533–2541 (2018).
pubmed: 29790754
pmcid: 6387837
doi: 10.1021/acs.jproteome.8b00133