ARID1A determines luminal identity and therapeutic response in estrogen-receptor-positive breast cancer.


Journal

Nature genetics
ISSN: 1546-1718
Titre abrégé: Nat Genet
Pays: United States
ID NLM: 9216904

Informations de publication

Date de publication:
02 2020
Historique:
received: 01 02 2019
accepted: 21 11 2019
pubmed: 15 1 2020
medline: 14 4 2020
entrez: 15 1 2020
Statut: ppublish

Résumé

Mutations in ARID1A, a subunit of the SWI/SNF chromatin remodeling complex, are the most common alterations of the SWI/SNF complex in estrogen-receptor-positive (ER

Identifiants

pubmed: 31932695
doi: 10.1038/s41588-019-0554-0
pii: 10.1038/s41588-019-0554-0
pmc: PMC7341683
mid: NIHMS1598098
doi:

Substances chimiques

ARID1A protein, human 0
Chromatin 0
DNA-Binding Proteins 0
FOXA1 protein, human 0
GATA3 Transcription Factor 0
GATA3 protein, human 0
Hepatocyte Nuclear Factor 3-alpha 0
Receptors, Estrogen 0
Transcription Factors 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

198-207

Subventions

Organisme : NCI NIH HHS
ID : K00 CA212478
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA190642
Pays : United States
Organisme : NCI NIH HHS
ID : T32 CA160001
Pays : United States

Références

Perou, C. M. et al. Molecular portraits of human breast tumours. Nature 406, 747–752 (2000).
pubmed: 10963602
Sørlie, T. et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl Acad. Sci. USA 98, 10869–10874 (2001).
pubmed: 11553815
Koboldt, D. C. et al. Comprehensive molecular portraits of human breast tumours. Nature 490, 61–70 (2012).
Stephens, P. J. et al. The landscape of cancer genes and mutational processes in breast cancer. Nature 486, 400–404 (2012).
pubmed: 22722201 pmcid: 3428862
Ciriello, G. et al. Comprehensive molecular portraits of invasive lobular breast cancer. Cell 163, 506–519 (2015).
pubmed: 26451490 pmcid: 4603750
Banerji, S. et al. Sequence analysis of mutations and translocations across breast cancer subtypes. Nature 486, 405–409 (2012).
pubmed: 22722202 pmcid: 4148686
Shah, S. P. et al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 486, 395–399 (2012).
pubmed: 22495314
Ellis, M. J. et al. Whole-genome analysis informs breast cancer response to aromatase inhibition. Nature 486, 353–360 (2012).
pubmed: 22722193 pmcid: 3383766
Nik-Zainal, S. et al. Landscape of somatic mutations in 560 breast cancer whole-genome sequences. Nature 534, 47–54 (2016).
pubmed: 27135926 pmcid: 4910866
Pereira, B. et al. The somatic mutation profiles of 2,433 breast cancers refines their genomic and transcriptomic landscapes. Nat. Commun. 7, 11479 (2016).
pubmed: 27161491
Green, K. A. & Carroll, J. S. Oestrogen-receptor-mediated transcription and the influence of co-factors and chromatin state. Nat. Rev. Cancer 7, 713–722 (2007).
pubmed: 17721435
Schiavon, G. et al. Analysis of ESR1 mutation in circulating tumor DNA demonstrates evolution during therapy for metastatic breast cancer. Sci. Transl. Med. 7, 313ra182 (2015).
pubmed: 26560360 pmcid: 4998737
Toy, W. et al. ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. Nat. Genet. 45, 1439–1445 (2013).
pubmed: 24185512
Kadoch, C. et al. Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet. 45, 592–601 (2013).
pubmed: 23644491
Garraway, L. A. & Lander, E. S. Lessons from the cancer genome. Cell 153, 17–37 (2013).
pubmed: 23540688
Mathur, R. et al. ARID1A loss impairs enhancer-mediated gene regulation and drives colon cancer in mice. Nat. Genet. 49, 296–302 (2017).
pubmed: 27941798
Nakayama, R. T. et al. SMARCB1 is required for widespread BAF complex-mediated activation of enhancers and bivalent promoters. Nat. Genet. 49, 1613–1623 (2017).
pubmed: 28945250 pmcid: 5803080
Wang, X. et al. SMARCB1-mediated SWI/SNF complex function is essential for enhancer regulation. Nat. Genet. 49, 289–295 (2017).
pubmed: 27941797
Kelso, T. W. R. et al. Chromatin accessibility underlies synthetic lethality of SWI/SNF subunits in ARID1A-mutant cancers. eLife 6, e30506 (2017).
pubmed: 28967863 pmcid: 5643100
Bossen, C. et al. The chromatin remodeler Brg1 activates enhancer repertoires to establish B cell identity and modulate cell growth. Nat. Immunol. 16, 775–784 (2015).
pubmed: 25985234 pmcid: 4474778
Mashtalir, N. et al. Modular organization and assembly of SWI/SNF family chromatin remodeling complexes. Cell 175, 1272–1288.e20 (2018).
pubmed: 30343899
Razavi, P. et al. The genomic landscape of endocrine-resistant advanced breast cancers. Cancer Cell 34, 427–438.e6 (2018).
pubmed: 30205045
Cheng, D. T. et al. Memorial Sloan Kettering-integrated mutation profiling of actionable cancer targets (MSK-IMPACT): a hybridization capture-based next-generation sequencing clinical assay for solid tumor molecular oncology. J. Mol. Diagn. 17, 251–264 (2015).
pubmed: 25801821 pmcid: 5808190
Pan, J. et al. Interrogation of mammalian protein complex structure, function, and membership using genome-scale fitness screens. Cell Syst. 6, 555–568.e7 (2018).
pubmed: 29778836 pmcid: 6152908
Sandoval, G. J. et al. Binding of TMPRSS2-ERG to BAF chromatin remodeling complexes mediates prostate oncogenesis. Mol. Cell 71, 554–566.e7 (2018).
pubmed: 30078722 pmcid: 6140332
Grant, C. E., Bailey, T. L. & Noble, W. S. FIMO: scanning for occurrences of a given motif. Bioinformatics 27, 1017–1018 (2011).
pubmed: 21330290 pmcid: 3065696
Hurtado, A., Holmes, K. A., Ross-Innes, C. S., Schmidt, D. & Carroll, J. S. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat. Genet. 43, 27–33 (2011).
pubmed: 21151129
Bernardo, G. M. et al. FOXA1 is an essential determinant of ERα expression and mammary ductal morphogenesis. Development 137, 2045–2054 (2010).
pubmed: 20501593
Theodorou, V., Stark, R., Menon, S. & Carroll, J. S. GATA3 acts upstream of FOXA1 in mediating ESR1 binding by shaping enhancer accessibility. Genome Res. 23, 12–22 (2013).
pubmed: 23172872
Asselin-Labat, M. L. et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat. Cell Biol. 9, 201–209 (2007).
pubmed: 17187062
Dravis, C. et al. Epigenetic and transcriptomic profiling of mammary gland development and tumor models disclose regulators of cell state plasticity. Cancer Cell 34, 466–482.e6 (2018).
pubmed: 30174241 pmcid: 6152943
Mu, P. et al. SOX2 promotes lineage plasticity and antiandrogen resistance in TP53- and RB1-deficient prostate cancer. Science 355, 84–88 (2017).
pubmed: 28059768 pmcid: 5247742
Britschgi, A. et al. The Hippo kinases LATS1 and 2 control human breast cell fate via crosstalk with ERα. Nature 541, 541–545 (2017).
pubmed: 28068668 pmcid: 6726477
Malta, T. M. et al. Machine learning identifies stemness features associated with oncogenic dedifferentiation. Cell 173, 338–354.e15 (2018).
pubmed: 29625051 pmcid: 29625051
Wuidart, A. et al. Early lineage segregation of multipotent embryonic mammary gland progenitors. Nat. Cell Biol. 20, 666–676 (2018).
pubmed: 29784918 pmcid: 5985933
Kadoch, C. et al. Dynamics of BAF–Polycomb complex opposition on heterochromatin in normal and oncogenic states. Nat. Genet. 49, 213–222 (2017).
pubmed: 27941796
Miller, E. L. et al. TOP2 synergizes with BAF chromatin remodeling for both resolution and formation of facultative heterochromatin. Nat. Struct. Mol. Biol. 24, 344–352 (2017).
pubmed: 28250416 pmcid: 5395302
Sun, X. et al. Arid1a has context-dependent oncogenic and tumor suppressor functions in liver cancer. Cancer Cell 32, 574–589.e6 (2017).
pubmed: 29136504 pmcid: 5728182
Vierbuchen, T. et al. AP-1 transcription factors and the BAF complex mediate signal-dependent enhancer selection. Mol. Cell 68, 1067–1082.e12 (2017).
pubmed: 29272704 pmcid: 5744881
Zaret, K. S. & Carroll, J. S. Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25, 2227–2241 (2011).
pubmed: 22056668 pmcid: 3219227
Lupien, M. et al. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132, 958–970 (2008).
pubmed: 18358809 pmcid: 2323438
Toska, E. et al. PI3K pathway regulates ER-dependent transcription in breast cancer through the epigenetic regulator KMT2D. Science 355, 1324–1330 (2017).
pubmed: 28336670 pmcid: 5485411
Kuukasjärvi, T., Kononen, J., Helin, H., Holli, K. & Isola, J. Loss of estrogen receptor in recurrent breast cancer is associated with poor response to endocrine therapy. J. Clin. Oncol. 14, 2584–2589 (1996).
pubmed: 8823339
Musgrove, E. A. & Sutherland, R. L. Biological determinants of endocrine resistance in breast cancer. Nat. Rev. Cancer 9, 631–643 (2009).
pubmed: 19701242
Lindström, L. S. et al. Clinically used breast cancer markers such as estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 are unstable throughout tumor progression. J. Clin. Oncol. 30, 2601–2608 (2012).
pubmed: 22711854
Dieci, M. V. et al. Discordance in receptor status between primary and recurrent breast cancer has a prognostic impact: a single-institution analysis. Ann. Oncol. 24, 101–108 (2013).
pubmed: 23002281
Caumanns, J. J., Wisman, G. B. A., Berns, K., van der Zee, A. G. J. & de Jong, S. ARID1A mutant ovarian clear cell carcinoma: a clear target for synthetic lethal strategies. Biochim. Biophys. Acta Rev. Cancer 1870, 176–184 (2018).
pubmed: 30025943
Bitler, B. G. et al. Synthetic lethality by targeting EZH2 methyltransferase activity in ARID1A-mutated cancers. Nat. Med. 21, 231–238 (2015).
pubmed: 25686104
Doench, J. G. et al. Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9. Nat. Biotechnol. 34, 184–191 (2016).
pubmed: 26780180 pmcid: 4744125
Toska, E. et al. PI3K inhibition activates SGK1 via a feedback loop to promote chromatin-based regulation of ER-dependent gene expression. Cell Rep. 27, 294–306.e5 (2019).
pubmed: 30943409
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: 24097267
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 4103590 pmcid: 4103590
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286 pmcid: 22388286
Feng, J., Liu, T., Qin, B., Zhang, Y. & Liu, X. S. Identifying ChIP-seq enrichment using MACS. Nat. Protoc. 7, 1728–1740 (2012).
pubmed: 22936215
Lawrence, M. et al. Software for computing and annotating genomic ranges. PLoS Comput. Biol. 9, e1003118 (2013).
pubmed: 23950696 pmcid: 3738458
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281 pmcid: 4302049
Philip, M. et al. Chromatin states define tumour-specific T cell dysfunction and reprogramming. Nature 545, 452–456 (2017).
pubmed: 28514453
Friedman, J., Hastie, T. & Tibshirani, R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1–22 (2010).
pubmed: 20808728
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
Anders, S., Pyl, P. T. & Huber, W. HTSeq: a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).
pubmed: 25260700
Chen, C. W. et al. DOT1L inhibits SIRT1-mediated epigenetic silencing to maintain leukemic gene expression in MLL-rearranged leukemia. Nat. Med. 21, 335–343 (2015).
pubmed: 25822366 pmcid: 4390532
Bailey, T. L. & Machanick, P. Inferring direct DNA binding from ChIP-seq. Nucleic Acids Res. 40, e128 (2012).
pubmed: 22610855
Ramírez, F., Dündar, F., Diehl, S., Grüning, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187–W191 (2014).
pubmed: 24799436
Shen, R. & Seshan, V. E. FACETS: allele-specific copy number and clonal heterogeneity analysis tool for high-throughput DNA sequencing. Nucleic Acids Res. 44, e131 (2016).
pubmed: 27270079 pmcid: 5027494
Weinreb, I. et al. Hotspot activating PRKD1 somatic mutations in polymorphous low-grade adenocarcinomas of the salivary glands. Nat. Genet. 46, 1166–1169 (2014).
pubmed: 25240283

Auteurs

Guotai Xu (G)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Sagar Chhangawala (S)

Computational and Systems Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Physiology, Biophysics, and Systems Biology Program, Weill Cornell Graduate School, New York, NY, USA.

Emiliano Cocco (E)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Pedram Razavi (P)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Yanyan Cai (Y)

Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Jordan E Otto (JE)

Depatment of Pediatric Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA, USA.

Lorenzo Ferrando (L)

Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Internal Medicine, Università degli Studi di Genova, Genova, Italy.

Pier Selenica (P)

Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Erik Ladewig (E)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Computational and Systems Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Carmen Chan (C)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Arnaud Da Cruz Paula (A)

Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Matthew Witkin (M)

Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Yuanming Cheng (Y)

Molecular Pharmacology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Jane Park (J)

Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Cristian Serna-Tamayo (C)

Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Brookdale Department of Geriatrics and Palliative Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

HuiYong Zhao (H)

Tumor Assessment Core, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Fan Wu (F)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Mirna Sallaku (M)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Xuan Qu (X)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Alison Zhao (A)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Clayton K Collings (CK)

Depatment of Pediatric Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA, USA.
Broad Institute of Harvard and MIT, Cambridge, MA, USA.

Andrew R D'Avino (AR)

Depatment of Pediatric Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA, USA.
Broad Institute of Harvard and MIT, Cambridge, MA, USA.

Komal Jhaveri (K)

Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Richard Koche (R)

Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Ross L Levine (RL)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Jorge S Reis-Filho (JS)

Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Cigall Kadoch (C)

Depatment of Pediatric Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA, USA.
Broad Institute of Harvard and MIT, Cambridge, MA, USA.

Maurizio Scaltriti (M)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Christina S Leslie (CS)

Computational and Systems Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA. cleslie@cbio.mskcc.org.

José Baselga (J)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA. Jose.Baselga@astrazeneca.com.
Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA. Jose.Baselga@astrazeneca.com.
Research & Development Oncology, AstraZeneca Pharmaceuticals, Gaithersburg, MD, USA. Jose.Baselga@astrazeneca.com.

Eneda Toska (E)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA. toskae@mskcc.org.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH