Altered BAF occupancy and transcription factor dynamics in PBAF-deficient melanoma
ARID2 is the most recurrently mutated SWI/SNF complex member in melanoma; however, its tumor-suppressive mechanisms in the context of the chromatin landscape remain to be elucidated. Here, we model ARID2 deficiency in melanoma cells, which results in defective PBAF complex assembly with a concomitan...
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| Published in | Cell reports (Cambridge) Vol. 39; no. 1; p. 110637 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
05.04.2022
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2211-1247 2211-1247 |
| DOI | 10.1016/j.celrep.2022.110637 |
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| Abstract | ARID2 is the most recurrently mutated SWI/SNF complex member in melanoma; however, its tumor-suppressive mechanisms in the context of the chromatin landscape remain to be elucidated. Here, we model ARID2 deficiency in melanoma cells, which results in defective PBAF complex assembly with a concomitant genomic redistribution of the BAF complex. Upon ARID2 depletion, a subset of PBAF and shared BAF-PBAF-occupied regions displays diminished chromatin accessibility and associated gene expression, while BAF-occupied enhancers gain chromatin accessibility and expression of genes linked to the process of invasion. As a function of altered accessibility, the genomic occupancy of melanoma-relevant transcription factors is affected and significantly correlates with the observed transcriptional changes. We further demonstrate that ARID2-deficient cells acquire the ability to colonize distal organs in multiple animal models. Taken together, our results reveal a role for ARID2 in mediating BAF and PBAF subcomplex chromatin dynamics with consequences for melanoma metastasis.
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•ARID2 loss results in impaired PBAF complex assembly and BAF genomic redistribution•Altered SWI/SNF dynamics results in chromatin accessibility and TF binding changes•PBAF loss drives an invasive gene expression signature and phenotype in melanoma
The tumor-suppressive functions of the SWI/SNF subunit ARID2 remain ill-defined in the context of melanoma. Carcamo et al. demonstrate that, upon ARID2 depletion, the PBAF complex fails to assemble, altering BAF genomic occupancy with consequences on chromatin accessibility, transcription factor binding, and transcriptional changes that promote metastasis. |
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| AbstractList | ARID2 is the most recurrently mutated SWI/SNF complex member in melanoma; however, its tumor-suppressive mechanisms in the context of the chromatin landscape remain to be elucidated. Here, we model ARID2 deficiency in melanoma cells, which results in defective PBAF complex assembly with a concomitant genomic redistribution of the BAF complex. Upon ARID2 depletion, a subset of PBAF and shared BAF-PBAF-occupied regions displays diminished chromatin accessibility and associated gene expression, while BAF-occupied enhancers gain chromatin accessibility and expression of genes linked to the process of invasion. As a function of altered accessibility, the genomic occupancy of melanoma-relevant transcription factors is affected and significantly correlates with the observed transcriptional changes. We further demonstrate that ARID2-deficient cells acquire the ability to colonize distal organs in multiple animal models. Taken together, our results reveal a role for ARID2 in mediating BAF and PBAF subcomplex chromatin dynamics with consequences for melanoma metastasis.
[Display omitted]
•ARID2 loss results in impaired PBAF complex assembly and BAF genomic redistribution•Altered SWI/SNF dynamics results in chromatin accessibility and TF binding changes•PBAF loss drives an invasive gene expression signature and phenotype in melanoma
The tumor-suppressive functions of the SWI/SNF subunit ARID2 remain ill-defined in the context of melanoma. Carcamo et al. demonstrate that, upon ARID2 depletion, the PBAF complex fails to assemble, altering BAF genomic occupancy with consequences on chromatin accessibility, transcription factor binding, and transcriptional changes that promote metastasis. ARID2 is the most recurrently mutated SWI/SNF complex member in melanoma; however, its tumor-suppressive mechanisms in the context of the chromatin landscape remain to be elucidated. Here, we model ARID2 deficiency in melanoma cells, which results in defective PBAF complex assembly with a concomitant genomic redistribution of the BAF complex. Upon ARID2 depletion, a subset of PBAF and shared BAF-PBAF-occupied regions displays diminished chromatin accessibility and associated gene expression, while BAF-occupied enhancers gain chromatin accessibility and expression of genes linked to the process of invasion. As a function of altered accessibility, the genomic occupancy of melanoma-relevant transcription factors is affected and significantly correlates with the observed transcriptional changes. We further demonstrate that ARID2-deficient cells acquire the ability to colonize distal organs in multiple animal models. Taken together, our results reveal a role for ARID2 in mediating BAF and PBAF subcomplex chromatin dynamics with consequences for melanoma metastasis. The tumor-suppressive functions of the SWI/SNF subunit ARID2 remain ill-defined in the context of melanoma. Carcamo et al. demonstrate that, upon ARID2 depletion, the PBAF complex fails to assemble, altering BAF genomic occupancy with consequences on chromatin accessibility, transcription factor binding, and transcriptional changes that promote metastasis. ARID2 is the most recurrently mutated SWI/SNF complex member in melanoma; however, its tumor-suppressive mechanisms in the context of the chromatin landscape remain to be elucidated. Here, we model ARID2 deficiency in melanoma cells, which results in defective PBAF complex assembly with a concomitant genomic redistribution of the BAF complex. Upon ARID2 depletion, a subset of PBAF and shared BAF-PBAF-occupied regions displays diminished chromatin accessibility and associated gene expression, while BAF-occupied enhancers gain chromatin accessibility and expression of genes linked to the process of invasion. As a function of altered accessibility, the genomic occupancy of melanoma-relevant transcription factors is affected and significantly correlates with the observed transcriptional changes. We further demonstrate that ARID2-deficient cells acquire the ability to colonize distal organs in multiple animal models. Taken together, our results reveal a role for ARID2 in mediating BAF and PBAF subcomplex chromatin dynamics with consequences for melanoma metastasis. ARID2 is the most recurrently mutated SWI/SNF complex member in melanoma; however, its tumor-suppressive mechanisms in the context of the chromatin landscape remain to be elucidated. Here, we model ARID2 deficiency in melanoma cells, which results in defective PBAF complex assembly with a concomitant genomic redistribution of the BAF complex. Upon ARID2 depletion, a subset of PBAF and shared BAF-PBAF-occupied regions displays diminished chromatin accessibility and associated gene expression, while BAF-occupied enhancers gain chromatin accessibility and expression of genes linked to the process of invasion. As a function of altered accessibility, the genomic occupancy of melanoma-relevant transcription factors is affected and significantly correlates with the observed transcriptional changes. We further demonstrate that ARID2-deficient cells acquire the ability to colonize distal organs in multiple animal models. Taken together, our results reveal a role for ARID2 in mediating BAF and PBAF subcomplex chromatin dynamics with consequences for melanoma metastasis.ARID2 is the most recurrently mutated SWI/SNF complex member in melanoma; however, its tumor-suppressive mechanisms in the context of the chromatin landscape remain to be elucidated. Here, we model ARID2 deficiency in melanoma cells, which results in defective PBAF complex assembly with a concomitant genomic redistribution of the BAF complex. Upon ARID2 depletion, a subset of PBAF and shared BAF-PBAF-occupied regions displays diminished chromatin accessibility and associated gene expression, while BAF-occupied enhancers gain chromatin accessibility and expression of genes linked to the process of invasion. As a function of altered accessibility, the genomic occupancy of melanoma-relevant transcription factors is affected and significantly correlates with the observed transcriptional changes. We further demonstrate that ARID2-deficient cells acquire the ability to colonize distal organs in multiple animal models. Taken together, our results reveal a role for ARID2 in mediating BAF and PBAF subcomplex chromatin dynamics with consequences for melanoma metastasis. |
| ArticleNumber | 110637 |
| Author | Aguirre-Ghiso, Julio A. Grossi, Elena Hasson, Dan Dhiman, Alisha Dykhuizen, Emily C. Martin, Tiphaine C. Carcamo, Saul Bernstein, Emily Imig, Jochen Tsirigos, Aristotelis Parsons, Ramon Nguyen, Christie B. Filipescu, Dan Sun, Dan Alpsoy, Aktan Narang, Sonali Aifantis, Iannis |
| AuthorAffiliation | 12 These authors contributed equally 13 Lead contact 2 Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 1 Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 3 Division of Hematology and Oncology, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 5 Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 10 Applied Bioinformatics Laboratories, NYU School of Medicine, New York, NY 10016, USA 8 Department of Medicinal Chemistry and Molecular Pharmacology, Purdue University, West Lafayette, IN 47907, USA 9 Department of Pathology and Laura & Isaac Perlmutter Cancer Center, New York, NY 10016, USA 11 Present address: Department of Cell Biology, Department of Medicine-Oncology, Cancer Dormancy and Tumor Microenvironment Institute, Gruss-Lipper Biophotonics Center, Albert Einstein Cancer Center, Ruth L. and David S. Gottesman Institute for |
| AuthorAffiliation_xml | – name: 9 Department of Pathology and Laura & Isaac Perlmutter Cancer Center, New York, NY 10016, USA – name: 12 These authors contributed equally – name: 11 Present address: Department of Cell Biology, Department of Medicine-Oncology, Cancer Dormancy and Tumor Microenvironment Institute, Gruss-Lipper Biophotonics Center, Albert Einstein Cancer Center, Ruth L. and David S. Gottesman Institute for Stem Cell Research and Regenerative Medicine, Albert Einstein College of Medicine, Bronx, NY 10461, USA – name: 2 Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 10 Applied Bioinformatics Laboratories, NYU School of Medicine, New York, NY 10016, USA – name: 5 Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 8 Department of Medicinal Chemistry and Molecular Pharmacology, Purdue University, West Lafayette, IN 47907, USA – name: 3 Division of Hematology and Oncology, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 13 Lead contact – name: 4 Department of Otolaryngology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 1 Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 7 Tisch Cancer Institute Bioinformatics for Next Generation Sequencing (BiNGS) Shared Resource Facility, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 6 Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA |
| Author_xml | – sequence: 1 givenname: Saul surname: Carcamo fullname: Carcamo, Saul organization: Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 2 givenname: Christie B. surname: Nguyen fullname: Nguyen, Christie B. organization: Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 3 givenname: Elena orcidid: 0000-0003-3938-5000 surname: Grossi fullname: Grossi, Elena organization: Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 4 givenname: Dan orcidid: 0000-0001-6381-2557 surname: Filipescu fullname: Filipescu, Dan organization: Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 5 givenname: Aktan orcidid: 0000-0002-8940-8277 surname: Alpsoy fullname: Alpsoy, Aktan organization: Department of Medicinal Chemistry and Molecular Pharmacology, Purdue University, West Lafayette, IN 47907, USA – sequence: 6 givenname: Alisha surname: Dhiman fullname: Dhiman, Alisha organization: Department of Medicinal Chemistry and Molecular Pharmacology, Purdue University, West Lafayette, IN 47907, USA – sequence: 7 givenname: Dan surname: Sun fullname: Sun, Dan organization: Division of Hematology and Oncology, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 8 givenname: Sonali orcidid: 0000-0002-1138-0067 surname: Narang fullname: Narang, Sonali organization: Department of Pathology and Laura & Isaac Perlmutter Cancer Center, New York, NY 10016, USA – sequence: 9 givenname: Jochen orcidid: 0000-0003-0385-1081 surname: Imig fullname: Imig, Jochen organization: Department of Pathology and Laura & Isaac Perlmutter Cancer Center, New York, NY 10016, USA – sequence: 10 givenname: Tiphaine C. surname: Martin fullname: Martin, Tiphaine C. organization: Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 11 givenname: Ramon surname: Parsons fullname: Parsons, Ramon organization: Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 12 givenname: Iannis surname: Aifantis fullname: Aifantis, Iannis organization: Department of Pathology and Laura & Isaac Perlmutter Cancer Center, New York, NY 10016, USA – sequence: 13 givenname: Aristotelis surname: Tsirigos fullname: Tsirigos, Aristotelis organization: Department of Pathology and Laura & Isaac Perlmutter Cancer Center, New York, NY 10016, USA – sequence: 14 givenname: Julio A. surname: Aguirre-Ghiso fullname: Aguirre-Ghiso, Julio A. organization: Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 15 givenname: Emily C. surname: Dykhuizen fullname: Dykhuizen, Emily C. organization: Department of Medicinal Chemistry and Molecular Pharmacology, Purdue University, West Lafayette, IN 47907, USA – sequence: 16 givenname: Dan surname: Hasson fullname: Hasson, Dan organization: Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 17 givenname: Emily orcidid: 0000-0001-6533-8326 surname: Bernstein fullname: Bernstein, Emily email: emily.bernstein@mssm.edu organization: Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35385731$$D View this record in MEDLINE/PubMed |
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| Keywords | PBAF invasion transcription factors CP: Cancer SWI/SNF BAF melanoma ARID2 chromatin |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceptualization, S.C., D.H., and E.B.; investigation, S.C., D.H., C.B.N., E.G., D.F., A.A., A.D., J.I., and D.S.; formal analysis, S.C., D.H., C.B.N., and T.C.M.; writing – original draft, S.C. and E.B; writing – review & editing, S.C., D.H., C.B.N., E.G., D.F., J.A.A.-G., T.C.M., E.C.D., and E.B.; visualization, S.C. and D.H.; resources, expertise, and methods, I.A., J.A.A.-G., R.P., A.T., and E.C.D.; data curation, S.C., C.B.N., S.N., and D.H.; supervision, E.C.D., D.H., and E.B.; funding acquisition, R.P., J.A.A.-G., E.C.D., and E.B. AUTHOR CONTRIBUTIONS |
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| SubjectTerms | Animals ARID2 BAF Chromatin Chromatin Assembly and Disassembly Chromosomal Proteins, Non-Histone Gene Expression Regulation Humans invasion melanoma Melanoma - genetics PBAF SWI/SNF transcription factors Transcription Factors - genetics Transcription Factors - metabolism |
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| Title | Altered BAF occupancy and transcription factor dynamics in PBAF-deficient melanoma |
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