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Article ; Online: Targeting SWI/SNF ATPases in H3.3K27M diffuse intrinsic pontine gliomas.

Mota, Mateus / Sweha, Stefan R / Pun, Matt / Natarajan, Siva Kumar / Ding, Yujie / Chung, Chan / Hawes, Debra / Yang, Fusheng / Judkins, Alexander R / Samajdar, Susanta / Cao, Xuhong / Xiao, Lanbo / Parolia, Abhijit / Chinnaiyan, Arul M / Venneti, Sriram

Proceedings of the National Academy of Sciences of the United States of America

2023 Volume 120, Issue 18, Page(s) e2221175120

Abstract: Diffuse midline gliomas (DMGs) including diffuse intrinsic pontine gliomas (DIPGs) bearing lysine-to-methionine mutations in histone H3 at lysine 27 (H3K27M) are lethal childhood brain cancers. These tumors harbor a global reduction in the ... ...

Abstract	Diffuse midline gliomas (DMGs) including diffuse intrinsic pontine gliomas (DIPGs) bearing lysine-to-methionine mutations in histone H3 at lysine 27 (H3K27M) are lethal childhood brain cancers. These tumors harbor a global reduction in the transcriptional repressive mark H3K27me3 accompanied by an increase in the transcriptional activation mark H3K27ac. We postulated that H3K27M mutations, in addition to altering H3K27 modifications, reprogram the master chromatin remodeling switch/sucrose nonfermentable (SWI/SNF) complex. The SWI/SNF complex can exist in two main forms termed BAF and PBAF that play central roles in neurodevelopment and cancer. Moreover, BAF antagonizes PRC2, the main enzyme catalyzing H3K27me3. We demonstrate that H3K27M gliomas show increased protein levels of the SWI/SNF complex ATPase subunits SMARCA4 and SMARCA2, and the PBAF component PBRM1. Additionally, knockdown of mutant H3K27M lowered SMARCA4 protein levels. The proteolysis targeting chimera (PROTAC) AU-15330 that simultaneously targets SMARCA4, SMARCA2, and PBRM1 for degradation exhibits cytotoxicity in H3.3K27M but not H3 wild-type cells. AU-15330 lowered chromatin accessibility measured by ATAC-Seq at nonpromoter regions and reduced global H3K27ac levels. Integrated analysis of gene expression, proteomics, and chromatin accessibility in AU-15330-treated cells demonstrated reduction in the levels of FOXO1, a key member of the forkhead family of transcription factors. Moreover, genetic or pharmacologic targeting of FOXO1 resulted in cell death in H3K27M cells. Overall, our results suggest that H3K27M up-regulates SMARCA4 levels and combined targeting of SWI/SNF ATPases in H3.3K27M can serve as a potent therapeutic strategy for these deadly childhood brain tumors.
MeSH term(s)	Humans ; Child ; Histones/genetics ; Adenosine Triphosphatases/metabolism ; Diffuse Intrinsic Pontine Glioma ; Lysine/genetics ; Chromatin ; Glioma/genetics ; Brain Neoplasms/genetics ; Mutation ; DNA Helicases/metabolism ; Nuclear Proteins/metabolism ; Transcription Factors/metabolism
Chemical Substances	Histones ; Adenosine Triphosphatases (EC 3.6.1.-) ; Lysine (K3Z4F929H6) ; Chromatin ; SMARCA4 protein, human (EC 3.6.1.-) ; DNA Helicases (EC 3.6.4.-) ; Nuclear Proteins ; Transcription Factors
Language	English
Publishing date	2023-04-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2221175120
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Article ; Online: Molecular biomarkers predictive of sertraline treatment response in young children with fragile X syndrome.

AlOlaby, Reem Rafik / Sweha, Stefan R / Silva, Marisol / Durbin-Johnson, Blythe / Yrigollen, Carolyn M / Pretto, Dalyir / Hagerman, Randi J / Tassone, Flora

Brain & development

2017 Volume 39, Issue 6, Page(s) 483–492

Abstract: Objectives: Several neurotransmitters involved in brain development are altered in fragile X syndrome (FXS), the most common monogenic cause of autism spectrum disorder (ASD). Serotonin plays a vital role in synaptogenesis and postnatal brain ... ...

Abstract	Objectives: Several neurotransmitters involved in brain development are altered in fragile X syndrome (FXS), the most common monogenic cause of autism spectrum disorder (ASD). Serotonin plays a vital role in synaptogenesis and postnatal brain development. Deficits in serotonin synthesis and abnormal neurogenesis were shown in young children with autism, suggesting that treating within the first years of life with a selective serotonin reuptake inhibitor might be the most effective time. In this study we aimed to identify molecular biomarkers involved in the serotonergic pathway that could predict the response to sertraline treatment in young children with FXS. Methods: Genotypes were determined for several genes involved in serotonergic pathway in 51 children with FXS, ages 24-72months. Correlations between genotypes and deviations from baseline in primary and secondary outcome measures were modeled using linear regression models. Results: A significant association was observed between a BDNF polymorphism and improvements for several clinical measures, including the Clinical Global Impression scale (P=0.008) and the cognitive T score (P=0.017) in those treated with sertraline compared to those in the placebo group. Additionally, polymorphisms in the MAOA, Cytochrome P450 2C19 and 2D6, and in the 5-HTTLPR gene showed a significant correlation with some of the secondary measures included in this study. Conclusion: This study shows that polymorphisms of genes involved in the serotonergic pathway could play a potential role in predicting response to sertraline treatment in young children with FXS. Larger studies are warranted to confirm these initial findings.
MeSH term(s)	Autism Spectrum Disorder/drug therapy ; Autism Spectrum Disorder/genetics ; Biomarkers/metabolism ; Brain-Derived Neurotrophic Factor/blood ; Child ; Child, Preschool ; Cohort Studies ; Cytochrome P-450 Enzyme System/genetics ; Cytochrome P-450 Enzyme System/metabolism ; Double-Blind Method ; Female ; Fragile X Syndrome/blood ; Fragile X Syndrome/drug therapy ; Fragile X Syndrome/genetics ; Genotype ; Humans ; Male ; Matrix Metalloproteinase 9/metabolism ; Monoamine Oxidase/genetics ; Monoamine Oxidase/metabolism ; Serotonin Plasma Membrane Transport Proteins/genetics ; Serotonin Plasma Membrane Transport Proteins/metabolism ; Serotonin Uptake Inhibitors/therapeutic use ; Sertraline/therapeutic use ; Severity of Illness Index
Chemical Substances	Biomarkers ; Brain-Derived Neurotrophic Factor ; SLC6A4 protein, human ; Serotonin Plasma Membrane Transport Proteins ; Serotonin Uptake Inhibitors ; Cytochrome P-450 Enzyme System (9035-51-2) ; Monoamine Oxidase (EC 1.4.3.4) ; monoamine oxidase A, human (EC 1.4.3.4.) ; Matrix Metalloproteinase 9 (EC 3.4.24.35) ; Sertraline (QUC7NX6WMB)
Language	English
Publishing date	2017-02-24
Publishing country	Netherlands
Document type	Journal Article ; Randomized Controlled Trial
ZDB-ID	604822-5
ISSN	1872-7131 ; 0387-7604
ISSN (online)	1872-7131
ISSN	0387-7604
DOI	10.1016/j.braindev.2017.01.012
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Zs.A 1788: Show issues

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Article ; Online: Integrated Metabolic and Epigenomic Reprograming by H3K27M Mutations in Diffuse Intrinsic Pontine Gliomas.

Cancer cell

2020 Volume 38, Issue 3, Page(s) 334–349.e9

Abstract: H3K27M diffuse intrinsic pontine gliomas (DIPGs) are fatal and lack treatments. They mainly harbor H3.3K27M mutations resulting in H3K27me3 reduction. Integrated analysis in H3.3K27M cells, tumors, and in vivo imaging in patients showed enhanced ... ...

Abstract	H3K27M diffuse intrinsic pontine gliomas (DIPGs) are fatal and lack treatments. They mainly harbor H3.3K27M mutations resulting in H3K27me3 reduction. Integrated analysis in H3.3K27M cells, tumors, and in vivo imaging in patients showed enhanced glycolysis, glutaminolysis, and tricarboxylic acid cycle metabolism with high alpha-ketoglutarate (α-KG) production. Glucose and/or glutamine-derived α-KG maintained low H3K27me3 in H3.3K27M cells, and inhibition of key enzymes in glycolysis or glutaminolysis increased H3K27me3, altered chromatin accessibility, and prolonged survival in animal models. Previous studies have shown that mutant isocitrate-dehydrogenase (mIDH)1/2 glioma cells convert α-KG to D-2-hydroxyglutarate (D-2HG) to increase H3K27me3. Here, we show that H3K27M and IDH1 mutations are mutually exclusive and experimentally synthetic lethal. Overall, we demonstrate that H3.3K27M and mIDH1 hijack a conserved and critical metabolic pathway in opposing ways to maintain their preferred epigenetic state. Consequently, interruption of this metabolic/epigenetic pathway showed potent efficacy in preclinical models, suggesting key therapeutic targets for much needed treatments.
MeSH term(s)	Animals ; Brain Stem Neoplasms/genetics ; Brain Stem Neoplasms/metabolism ; Cell Line, Tumor ; Diffuse Intrinsic Pontine Glioma/genetics ; Diffuse Intrinsic Pontine Glioma/metabolism ; Epigenomics/methods ; Gene Expression Regulation, Neoplastic ; Glycolysis ; Histones/genetics ; Histones/metabolism ; Humans ; Lysine/genetics ; Lysine/metabolism ; Methylation ; Mice, Inbred NOD ; Mice, Knockout ; Mice, Nude ; Mice, SCID ; Mutation ; Transplantation, Heterologous
Chemical Substances	Histones ; Lysine (K3Z4F929H6)
Language	English
Publishing date	2020-08-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2078448-X
ISSN	1878-3686 ; 1535-6108
ISSN (online)	1878-3686
ISSN	1535-6108
DOI	10.1016/j.ccell.2020.07.008
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Zs.A 5650: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
Zs.MG 104: Show issues

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Article ; Online: Epigenetically defined therapeutic targeting in H3.3G34R/V high-grade gliomas.

Sweha, Stefan R / Chung, Chan / Natarajan, Siva Kumar / Panwalkar, Pooja / Pun, Matthew / Ghali, Amer / Bayliss, Jill / Pratt, Drew / Shankar, Anand / Ravikumar, Visweswaran / Rao, Arvind / Cieslik, Marcin / Wilder-Romans, Kari / Scott, Andrew J / Wahl, Daniel R / Jessa, Selin / Kleinman, Claudia L / Jabado, Nada / Mackay, Alan /

Jones, Chris / Martinez, Daniel / Santi, Mariarita / Judkins, Alexander R / Yadav, Viveka Nand / Qin, Tingting / Phoenix, Timothy N / Koschmann, Carl J / Baker, Suzanne J / Chinnaiyan, Arul M / Venneti, Sriram

Science translational medicine

2021 Volume 13, Issue 615, Page(s) eabf7860

Abstract: High-grade gliomas with arginine or valine substitutions of the histone H3.3 glycine-34 residue (H3.3G34R/V) carry a dismal prognosis, and current treatments, including radiotherapy and chemotherapy, are not curative. Because H3.3G34R/V mutations ... ...

Abstract	High-grade gliomas with arginine or valine substitutions of the histone H3.3 glycine-34 residue (H3.3G34R/V) carry a dismal prognosis, and current treatments, including radiotherapy and chemotherapy, are not curative. Because H3.3G34R/V mutations reprogram epigenetic modifications, we undertook a comprehensive epigenetic approach using ChIP sequencing and ChromHMM computational analysis to define therapeutic dependencies in H3.3G34R/V gliomas. Our analyses revealed a convergence of epigenetic alterations, including (i) activating epigenetic modifications on histone H3 lysine (K) residues such as H3K36 trimethylation (H3K36me3), H3K27 acetylation (H3K27ac), and H3K4 trimethylation (H3K4me3); (ii) DNA promoter hypomethylation; and (iii) redistribution of repressive histone H3K27 trimethylation (H3K27me3) to intergenic regions at the
MeSH term(s)	Animals ; Brain Neoplasms/genetics ; Brain Neoplasms/therapy ; Epigenesis, Genetic ; Glioma/genetics ; Glycine ; Histones/metabolism ; Humans ; Mice
Chemical Substances	Histones ; Glycine (TE7660XO1C)
Language	English
Publishing date	2021-10-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2518854-9
ISSN	1946-6242 ; 1946-6234
ISSN (online)	1946-6242
ISSN	1946-6234
DOI	10.1126/scitranslmed.abf7860
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Zs.A 6941: Show issues

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Article: Clinical and molecular correlates in fragile X premutation females.

Jiraanont, Poonnada / Sweha, Stefan R / AlOlaby, Reem R / Silva, Marisol / Tang, Hiu-Tung / Durbin-Johnson, Blythe / Schneider, Andrea / Espinal, Glenda M / Hagerman, Paul J / Rivera, Susan M / Hessl, David / Hagerman, Randi J / Chutabhakdikul, Nuanchan / Tassone, Flora

eNeurologicalSci

2017 Volume 7, Page(s) 49–56

Abstract: The prevalence of the fragile X premutation (55-200 CGG repeats) among the general population is relatively high, but there remains a lack of clear understanding of the links between molecular biomarkers and clinical outcomes. In this study we ... ...

Abstract	The prevalence of the fragile X premutation (55-200 CGG repeats) among the general population is relatively high, but there remains a lack of clear understanding of the links between molecular biomarkers and clinical outcomes. In this study we investigated the correlations between molecular measures (CGG repeat size,
Language	English
Publishing date	2017-04-11
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	2838045-9
ISSN	2405-6502
ISSN	2405-6502
DOI	10.1016/j.ensci.2017.04.003
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Article ; Online: Therapeutic targeting of prenatal pontine ID1 signaling in diffuse midline glioma.

Messinger, Dana / Harris, Micah K / Cummings, Jessica R / Thomas, Chase / Yang, Tao / Sweha, Stefan R / Woo, Rinette / Siddaway, Robert / Burkert, Martin / Stallard, Stefanie / Qin, Tingting / Mullan, Brendan / Siada, Ruby / Ravindran, Ramya / Niculcea, Michael / Dowling, Abigail R / Bradin, Joshua / Ginn, Kevin F / Gener, Melissa A H /

Dorris, Kathleen / Vitanza, Nicholas A / Schmidt, Susanne V / Spitzer, Jasper / Li, Jiang / Filbin, Mariella G / Cao, Xuhong / Castro, Maria G / Lowenstein, Pedro R / Mody, Rajen / Chinnaiyan, Arul / Desprez, Pierre-Yves / McAllister, Sean / Dun, Matthew D / Hawkins, Cynthia / Waszak, Sebastian M / Venneti, Sriram / Koschmann, Carl / Yadav, Viveka Nand

Neuro-oncology

2022 Volume 25, Issue 1, Page(s) 54–67

Abstract: Background: Diffuse midline gliomas (DMG) are highly invasive brain tumors with rare survival beyond two years past diagnosis and limited understanding of the mechanism behind tumor invasion. Previous reports demonstrate upregulation of the protein ID1 ... ...

Abstract	Background: Diffuse midline gliomas (DMG) are highly invasive brain tumors with rare survival beyond two years past diagnosis and limited understanding of the mechanism behind tumor invasion. Previous reports demonstrate upregulation of the protein ID1 with H3K27M and ACVR1 mutations in DMG, but this has not been confirmed in human tumors or therapeutically targeted. Methods: Whole exome, RNA, and ChIP-sequencing was performed on the ID1 locus in DMG tissue. Scratch-assay migration and transwell invasion assays of cultured cells were performed following shRNA-mediated ID1-knockdown. In vitro and in vivo genetic and pharmacologic [cannabidiol (CBD)] inhibition of ID1 on DMG tumor growth was assessed. Patient-reported CBD dosing information was collected. Results: Increased ID1 expression in human DMG and in utero electroporation (IUE) murine tumors is associated with H3K27M mutation and brainstem location. ChIP-sequencing indicates ID1 regulatory regions are epigenetically active in human H3K27M-DMG tumors and prenatal pontine cells. Higher ID1-expressing astrocyte-like DMG cells share a transcriptional program with oligo/astrocyte-precursor cells (OAPCs) from the developing human brain and demonstrate upregulation of the migration regulatory protein SPARCL1. Genetic and pharmacologic (CBD) suppression of ID1 decreases tumor cell invasion/migration and tumor growth in H3.3/H3.1K27M PPK-IUE and human DIPGXIIIP* in vivo models of pHGG. The effect of CBD on cell proliferation appears to be non-ID1 mediated. Finally, we collected patient-reported CBD treatment data, finding that a clinical trial to standardize dosing may be beneficial. Conclusions: H3K27M-mediated re-activation of ID1 in DMG results in a SPARCL1+ migratory transcriptional program that is therapeutically targetable with CBD.
MeSH term(s)	Animals ; Humans ; Mice ; Brain/pathology ; Brain Neoplasms/genetics ; Calcium-Binding Proteins ; Extracellular Matrix Proteins/genetics ; Glioma/genetics ; Histones/genetics ; Inhibitor of Differentiation Protein 1/genetics ; Mutation ; Signal Transduction
Chemical Substances	Calcium-Binding Proteins ; Extracellular Matrix Proteins ; Histones ; ID1 protein, human ; Inhibitor of Differentiation Protein 1 ; Sparcl1 protein, mouse ; Idb1 protein, mouse
Language	English
Publishing date	2022-06-02
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2028601-6
ISSN	1523-5866 ; 1522-8517
ISSN (online)	1523-5866
ISSN	1522-8517
DOI	10.1093/neuonc/noac141
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Zs.A 5307: Show issues

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Article ; Online: Clinical Efficacy of ONC201 in H3K27M-Mutant Diffuse Midline Gliomas Is Driven by Disruption of Integrated Metabolic and Epigenetic Pathways.

Venneti, Sriram / Kawakibi, Abed Rahman / Ji, Sunjong / Waszak, Sebastian M / Sweha, Stefan R / Mota, Mateus / Pun, Matthew / Deogharkar, Akash / Chung, Chan / Tarapore, Rohinton S / Ramage, Samuel / Chi, Andrew / Wen, Patrick Y / Arrillaga-Romany, Isabel / Batchelor, Tracy T / Butowski, Nicholas A / Sumrall, Ashley / Shonka, Nicole / Harrison, Rebecca A /

de Groot, John / Mehta, Minesh / Hall, Matthew D / Daghistani, Doured / Cloughesy, Timothy F / Ellingson, Benjamin M / Beccaria, Kevin / Varlet, Pascale / Kim, Michelle M / Umemura, Yoshie / Garton, Hugh / Franson, Andrea / Schwartz, Jonathan / Jain, Rajan / Kachman, Maureen / Baum, Heidi / Burant, Charles F / Mottl, Sophie L / Cartaxo, Rodrigo T / John, Vishal / Messinger, Dana / Qin, Tingting / Peterson, Erik / Sajjakulnukit, Peter / Ravi, Karthik / Waugh, Alyssa / Walling, Dustin / Ding, Yujie / Xia, Ziyun / Schwendeman, Anna / Hawes, Debra / Yang, Fusheng / Judkins, Alexander R / Wahl, Daniel / Lyssiotis, Costas A / de la Nava, Daniel / Alonso, Marta M / Eze, Augustine / Spitzer, Jasper / Schmidt, Susanne V / Duchatel, Ryan J / Dun, Matthew D / Cain, Jason E / Jiang, Li / Stopka, Sylwia A / Baquer, Gerard / Regan, Michael S / Filbin, Mariella G / Agar, Nathalie Y R / Zhao, Lili / Kumar-Sinha, Chandan / Mody, Rajen / Chinnaiyan, Arul / Kurokawa, Ryo / Pratt, Drew / Yadav, Viveka N / Grill, Jacques / Kline, Cassie / Mueller, Sabine / Resnick, Adam / Nazarian, Javad / Allen, Joshua E / Odia, Yazmin / Gardner, Sharon L / Koschmann, Carl

Cancer discovery

2023 Volume 13, Issue 11, Page(s) 2370–2393

Abstract: Patients with H3K27M-mutant diffuse midline glioma (DMG) have no proven effective therapies. ONC201 has recently demonstrated efficacy in these patients, but the mechanism behind this finding remains unknown. We assessed clinical outcomes, tumor ... ...

Abstract	Patients with H3K27M-mutant diffuse midline glioma (DMG) have no proven effective therapies. ONC201 has recently demonstrated efficacy in these patients, but the mechanism behind this finding remains unknown. We assessed clinical outcomes, tumor sequencing, and tissue/cerebrospinal fluid (CSF) correlate samples from patients treated in two completed multisite clinical studies. Patients treated with ONC201 following initial radiation but prior to recurrence demonstrated a median overall survival of 21.7 months, whereas those treated after recurrence had a median overall survival of 9.3 months. Radiographic response was associated with increased expression of key tricarboxylic acid cycle-related genes in baseline tumor sequencing. ONC201 treatment increased 2-hydroxyglutarate levels in cultured H3K27M-DMG cells and patient CSF samples. This corresponded with increases in repressive H3K27me3 in vitro and in human tumors accompanied by epigenetic downregulation of cell cycle regulation and neuroglial differentiation genes. Overall, ONC201 demonstrates efficacy in H3K27M-DMG by disrupting integrated metabolic and epigenetic pathways and reversing pathognomonic H3K27me3 reduction. Significance: The clinical, radiographic, and molecular analyses included in this study demonstrate the efficacy of ONC201 in H3K27M-mutant DMG and support ONC201 as the first monotherapy to improve outcomes in H3K27M-mutant DMG beyond radiation. Mechanistically, ONC201 disrupts integrated metabolic and epigenetic pathways and reverses pathognomonic H3K27me3 reduction. This article is featured in Selected Articles from This Issue, p. 2293.
MeSH term(s)	Humans ; Glioma/genetics ; Glioma/pathology ; Brain Neoplasms/genetics ; Brain Neoplasms/pathology ; Histones/genetics ; Treatment Outcome ; Epigenesis, Genetic ; Mutation
Chemical Substances	Histones ; TIC10 compound (9U35A31JAI)
Language	English
Publishing date	2023-08-16
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	2625242-9
ISSN	2159-8290 ; 2159-8274
ISSN (online)	2159-8290
ISSN	2159-8274
DOI	10.1158/2159-8290.CD-23-0131
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Article ; Online: Targeting SWI/SNF ATPases in H3.3K27M diffuse intrinsic pontine gliomas.

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Article ; Online: Molecular biomarkers predictive of sertraline treatment response in young children with fragile X syndrome.

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Article ; Online: Integrated Metabolic and Epigenomic Reprograming by H3K27M Mutations in Diffuse Intrinsic Pontine Gliomas.

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Article ; Online: Epigenetically defined therapeutic targeting in H3.3G34R/V high-grade gliomas.

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Article: Clinical and molecular correlates in fragile X premutation females.

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Article ; Online: Therapeutic targeting of prenatal pontine ID1 signaling in diffuse midline glioma.

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Article ; Online: Clinical Efficacy of ONC201 in H3K27M-Mutant Diffuse Midline Gliomas Is Driven by Disruption of Integrated Metabolic and Epigenetic Pathways.

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