Canonical BAF complex regulates the oncogenic program in human T-cell acute lymphoblastic leukemia

•cBAF inhibition reduces chromatin accessibility mainly at RUNX1 binding sites and disrupts the RUNX1-driven oncogenic program in T-ALL.•cBAF regulates migration activity toward CXCL12 and cell-autonomous growth in T-ALL cells, thus representing a promising therapeutic target. [Display omitted] Acut...

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Published inBlood Vol. 143; no. 7; pp. 604 - 618
Main Authors Aoki, Kazunari, Hyuga, Mizuki, Tarumoto, Yusuke, Nishibuchi, Gohei, Ueda, Atsushi, Ochi, Yotaro, Sugino, Seiichi, Mikami, Takashi, Kobushi, Hirokazu, Kato, Itaru, Akahane, Koshi, Inukai, Takeshi, Takaori-Kondo, Akifumi, Takita, Junko, Ogawa, Seishi, Yusa, Kosuke
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 15.02.2024
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Abstract •cBAF inhibition reduces chromatin accessibility mainly at RUNX1 binding sites and disrupts the RUNX1-driven oncogenic program in T-ALL.•cBAF regulates migration activity toward CXCL12 and cell-autonomous growth in T-ALL cells, thus representing a promising therapeutic target. [Display omitted] Acute leukemia cells require bone marrow microenvironments, known as niches, which provide leukemic cells with niche factors that are essential for leukemic cell survival and/or proliferation. However, it remains unclear how the dynamics of the leukemic cell–niche interaction are regulated. Using a genome-wide CRISPR screen, we discovered that canonical BRG1/BRM-associated factor (cBAF), a variant of the switch/sucrose nonfermenting chromatin remodeling complex, regulates the migratory response of human T-cell acute lymphoblastic leukemia (T-ALL) cells to a niche factor CXCL12. Mechanistically, cBAF maintains chromatin accessibility and allows RUNX1 to bind to CXCR4 enhancer regions. cBAF inhibition evicts RUNX1 from the genome, resulting in CXCR4 downregulation and impaired migration activity. In addition, cBAF maintains chromatin accessibility preferentially at RUNX1 binding sites, ensuring RUNX1 binding at these sites, and is required for expression of RUNX1-regulated genes, such as CDK6; therefore, cBAF inhibition negatively impacts cell proliferation and profoundly induces apoptosis. This anticancer effect was also confirmed using T-ALL xenograft models, suggesting cBAF as a promising therapeutic target. Thus, we provide novel evidence that cBAF regulates the RUNX1-driven leukemic program and governs migration activity toward CXCL12 and cell-autonomous growth in human T-ALL. Aoki et al investigated the signaling pathway that allows T-cell acute lymphoblastic leukemia (T-ALL) cells to migrate toward the niche factor CXCL12. The authors report that canonical BRG1/BRM-associated factor (cBAF) is a required regulator of T-ALL cell migration. cBAF depletion inhibits RUNX1 from binding to target genes, thus impairing proliferation and inducing apoptosis in vitro and in T-ALL xenografts. This suggests that cBAF may provide a new clinical target for the treatment of T-ALL.
AbstractList Acute leukemia cells require bone marrow microenvironments, known as niches, which provide leukemic cells with niche factors that are essential for leukemic cell survival and/or proliferation. However, it remains unclear how the dynamics of the leukemic cell-niche interaction are regulated. Using a genome-wide CRISPR screen, we discovered that canonical BRG1/BRM-associated factor (cBAF), a variant of the switch/sucrose nonfermenting chromatin remodeling complex, regulates the migratory response of human T-cell acute lymphoblastic leukemia (T-ALL) cells to a niche factor CXCL12. Mechanistically, cBAF maintains chromatin accessibility and allows RUNX1 to bind to CXCR4 enhancer regions. cBAF inhibition evicts RUNX1 from the genome, resulting in CXCR4 downregulation and impaired migration activity. In addition, cBAF maintains chromatin accessibility preferentially at RUNX1 binding sites, ensuring RUNX1 binding at these sites, and is required for expression of RUNX1-regulated genes, such as CDK6; therefore, cBAF inhibition negatively impacts cell proliferation and profoundly induces apoptosis. This anticancer effect was also confirmed using T-ALL xenograft models, suggesting cBAF as a promising therapeutic target. Thus, we provide novel evidence that cBAF regulates the RUNX1-driven leukemic program and governs migration activity toward CXCL12 and cell-autonomous growth in human T-ALL.
Abstract Acute leukemia cells require bone marrow microenvironments, known as niches, which provide leukemic cells with niche factors that are essential for leukemic cell survival and/or proliferation. However, it remains unclear how the dynamics of the leukemic cell–niche interaction are regulated. Using a genome-wide CRISPR screen, we discovered that canonical BRG1/BRM-associated factor (cBAF), a variant of the switch/sucrose nonfermenting chromatin remodeling complex, regulates the migratory response of human T-cell acute lymphoblastic leukemia (T-ALL) cells to a niche factor CXCL12. Mechanistically, cBAF maintains chromatin accessibility and allows RUNX1 to bind to CXCR4 enhancer regions. cBAF inhibition evicts RUNX1 from the genome, resulting in CXCR4 downregulation and impaired migration activity. In addition, cBAF maintains chromatin accessibility preferentially at RUNX1 binding sites, ensuring RUNX1 binding at these sites, and is required for expression of RUNX1-regulated genes, such as CDK6; therefore, cBAF inhibition negatively impacts cell proliferation and profoundly induces apoptosis. This anticancer effect was also confirmed using T-ALL xenograft models, suggesting cBAF as a promising therapeutic target. Thus, we provide novel evidence that cBAF regulates the RUNX1-driven leukemic program and governs migration activity toward CXCL12 and cell-autonomous growth in human T-ALL.
ABSTRACTAcute leukemia cells require bone marrow microenvironments, known as niches, which provide leukemic cells with niche factors that are essential for leukemic cell survival and/or proliferation. However, it remains unclear how the dynamics of the leukemic cell-niche interaction are regulated. Using a genome-wide CRISPR screen, we discovered that canonical BRG1/BRM-associated factor (cBAF), a variant of the switch/sucrose nonfermenting chromatin remodeling complex, regulates the migratory response of human T-cell acute lymphoblastic leukemia (T-ALL) cells to a niche factor CXCL12. Mechanistically, cBAF maintains chromatin accessibility and allows RUNX1 to bind to CXCR4 enhancer regions. cBAF inhibition evicts RUNX1 from the genome, resulting in CXCR4 downregulation and impaired migration activity. In addition, cBAF maintains chromatin accessibility preferentially at RUNX1 binding sites, ensuring RUNX1 binding at these sites, and is required for expression of RUNX1-regulated genes, such as CDK6; therefore, cBAF inhibition negatively impacts cell proliferation and profoundly induces apoptosis. This anticancer effect was also confirmed using T-ALL xenograft models, suggesting cBAF as a promising therapeutic target. Thus, we provide novel evidence that cBAF regulates the RUNX1-driven leukemic program and governs migration activity toward CXCL12 and cell-autonomous growth in human T-ALL.
•cBAF inhibition reduces chromatin accessibility mainly at RUNX1 binding sites and disrupts the RUNX1-driven oncogenic program in T-ALL.•cBAF regulates migration activity toward CXCL12 and cell-autonomous growth in T-ALL cells, thus representing a promising therapeutic target. [Display omitted] Acute leukemia cells require bone marrow microenvironments, known as niches, which provide leukemic cells with niche factors that are essential for leukemic cell survival and/or proliferation. However, it remains unclear how the dynamics of the leukemic cell–niche interaction are regulated. Using a genome-wide CRISPR screen, we discovered that canonical BRG1/BRM-associated factor (cBAF), a variant of the switch/sucrose nonfermenting chromatin remodeling complex, regulates the migratory response of human T-cell acute lymphoblastic leukemia (T-ALL) cells to a niche factor CXCL12. Mechanistically, cBAF maintains chromatin accessibility and allows RUNX1 to bind to CXCR4 enhancer regions. cBAF inhibition evicts RUNX1 from the genome, resulting in CXCR4 downregulation and impaired migration activity. In addition, cBAF maintains chromatin accessibility preferentially at RUNX1 binding sites, ensuring RUNX1 binding at these sites, and is required for expression of RUNX1-regulated genes, such as CDK6; therefore, cBAF inhibition negatively impacts cell proliferation and profoundly induces apoptosis. This anticancer effect was also confirmed using T-ALL xenograft models, suggesting cBAF as a promising therapeutic target. Thus, we provide novel evidence that cBAF regulates the RUNX1-driven leukemic program and governs migration activity toward CXCL12 and cell-autonomous growth in human T-ALL. Aoki et al investigated the signaling pathway that allows T-cell acute lymphoblastic leukemia (T-ALL) cells to migrate toward the niche factor CXCL12. The authors report that canonical BRG1/BRM-associated factor (cBAF) is a required regulator of T-ALL cell migration. cBAF depletion inhibits RUNX1 from binding to target genes, thus impairing proliferation and inducing apoptosis in vitro and in T-ALL xenografts. This suggests that cBAF may provide a new clinical target for the treatment of T-ALL.
Author Ueda, Atsushi
Inukai, Takeshi
Yusa, Kosuke
Ogawa, Seishi
Takaori-Kondo, Akifumi
Nishibuchi, Gohei
Sugino, Seiichi
Takita, Junko
Hyuga, Mizuki
Kato, Itaru
Akahane, Koshi
Aoki, Kazunari
Mikami, Takashi
Kobushi, Hirokazu
Tarumoto, Yusuke
Ochi, Yotaro
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Snippet •cBAF inhibition reduces chromatin accessibility mainly at RUNX1 binding sites and disrupts the RUNX1-driven oncogenic program in T-ALL.•cBAF regulates...
Acute leukemia cells require bone marrow microenvironments, known as niches, which provide leukemic cells with niche factors that are essential for leukemic...
Abstract Acute leukemia cells require bone marrow microenvironments, known as niches, which provide leukemic cells with niche factors that are essential for...
ABSTRACTAcute leukemia cells require bone marrow microenvironments, known as niches, which provide leukemic cells with niche factors that are essential for...
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Title Canonical BAF complex regulates the oncogenic program in human T-cell acute lymphoblastic leukemia
URI https://dx.doi.org/10.1182/blood.2023020857
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