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Article: Regulation of Versican Expression in Macrophages is Mediated by Canonical Type I Interferon Signaling via ISGF3.

Chang, Mary Y / Chan, Christina K / Brune, Jourdan E / Manicone, Anne M / Bomsztyk, Karol / Frevert, Charles W / Altemeier, William A

bioRxiv : the preprint server for biology

2024

Abstract: Growing evidence supports a role for versican as an important component of the inflammatory response, with both pro- and anti-inflammatory roles depending on the specific context of the system or disease under investigation. Our goal is to understand the ...

Abstract	Growing evidence supports a role for versican as an important component of the inflammatory response, with both pro- and anti-inflammatory roles depending on the specific context of the system or disease under investigation. Our goal is to understand the regulation of macrophage-derived versican and the role it plays in innate immunity. In previous work, we showed that LPS triggers a signaling cascade involving TLR4, the Trif adaptor, type I interferons, and the type I interferon receptor, leading to increased versican expression by macrophages. In the present study, we used a combination of chromatin immunoprecipitation, siRNA, chemical inhibitors, and mouse model approaches to investigate the regulatory events downstream of the type I interferon receptor to better define the mechanism controlling versican expression. Results indicate that transcriptional regulation by canonical type I interferon signaling via the heterotrimeric transcription factor, ISGF3, controls versican expression in macrophages exposed to LPS. This pathway is not dependent on MAPK signaling, which has been shown to regulate versican expression in other cell types. The stability of versican mRNA may also contribute to prolonged versican expression in macrophages. These findings strongly support a role for macrophage-derived versican as a type I interferon-stimulated gene and further our understanding of versican's role in regulating inflammation.
Language	English
Publishing date	2024-03-14
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.14.585097
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Article ; Online: Genome-bound enzymes as epigenetic drug targets in cancer.

Bomsztyk, Karol / Wang, Yuliang

Epigenomics

2019 Volume 11, Issue 13, Page(s) 1463–1467

MeSH term(s)	Antineoplastic Agents/pharmacology ; Antineoplastic Agents/therapeutic use ; Enzyme Inhibitors/pharmacology ; Enzyme Inhibitors/therapeutic use ; Enzymes/metabolism ; Epigenesis, Genetic/drug effects ; Gene Expression Regulation, Neoplastic/drug effects ; Humans ; Molecular Targeted Therapy ; Neoplasms/drug therapy ; Neoplasms/enzymology ; Neoplasms/genetics ; Precision Medicine
Chemical Substances	Antineoplastic Agents ; Enzyme Inhibitors ; Enzymes
Language	English
Publishing date	2019-09-19
Publishing country	England
Document type	Editorial ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1750-192X
ISSN (online)	1750-192X
DOI	10.2217/epi-2019-0197
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Article: MultiomicsTracks96: A high throughput PIXUL-Matrix-based toolbox to profile frozen and FFPE tissues multiomes.

Mar, Daniel / Babenko, Ilona M / Zhang, Ran / Noble, William Stafford / Denisenko, Oleg / Vaisar, Tomas / Bomsztyk, Karol

bioRxiv : the preprint server for biology

2023

Abstract: Background: The multiome is an integrated assembly of distinct classes of molecules and molecular properties, or "omes," measured in the same biospecimen. Freezing and formalin-fixed paraffin-embedding (FFPE) are two common ways to store tissues, and ... ...

Abstract	Background: The multiome is an integrated assembly of distinct classes of molecules and molecular properties, or "omes," measured in the same biospecimen. Freezing and formalin-fixed paraffin-embedding (FFPE) are two common ways to store tissues, and these practices have generated vast biospecimen repositories. However, these biospecimens have been underutilized for multi-omic analysis due to the low throughput of current analytical technologies that impede large-scale studies. Methods: Tissue sampling, preparation, and downstream analysis were integrated into a 96-well format multi-omics workflow, MultiomicsTracks96. Frozen mouse organs were sampled using the CryoGrid system, and matched FFPE samples were processed using a microtome. The 96-well format sonicator, PIXUL, was adapted to extract DNA, RNA, chromatin, and protein from tissues. The 96-well format analytical platform, Matrix, was used for chromatin immunoprecipitation (ChIP), methylated DNA immunoprecipitation (MeDIP), methylated RNA immunoprecipitation (MeRIP), and RNA reverse transcription (RT) assays followed by qPCR and sequencing. LC-MS/MS was used for protein analysis. The Segway genome segmentation algorithm was used to identify functional genomic regions, and linear regressors based on the multi-omics data were trained to predict protein expression. Results: MultiomicsTracks96 was used to generate 8-dimensional datasets including RNA-seq measurements of mRNA expression; MeRIP-seq measurements of m6A and m5C; ChIP-seq measurements of H3K27Ac, H3K4m3, and Pol II; MeDIP-seq measurements of 5mC; and LC-MS/MS measurements of proteins. We observed high correlation between data from matched frozen and FFPE organs. The Segway genome segmentation algorithm applied to epigenomic profiles (ChIP-seq: H3K27Ac, H3K4m3, Pol II; MeDIP-seq: 5mC) was able to recapitulate and predict organ-specific super-enhancers in both FFPE and frozen samples. Linear regression analysis showed that proteomic expression profiles can be more accurately predicted by the full suite of multi-omics data, compared to using epigenomic, transcriptomic, or epitranscriptomic measurements individually. Conclusions: The MultiomicsTracks96 workflow is well suited for high dimensional multi-omics studies - for instance, multiorgan animal models of disease, drug toxicities, environmental exposure, and aging as well as large-scale clinical investigations involving the use of biospecimens from existing tissue repositories.
Language	English
Publishing date	2023-03-20
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.03.16.533031
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Article ; Online: A High-Throughput PIXUL-Matrix-Based Toolbox to Profile Frozen and Formalin-Fixed Paraffin-Embedded Tissues Multiomes.

Mar, Daniel / Babenko, Ilona M / Zhang, Ran / Noble, William Stafford / Denisenko, Oleg / Vaisar, Tomas / Bomsztyk, Karol

Laboratory investigation; a journal of technical methods and pathology

2023 Volume 104, Issue 1, Page(s) 100282

Abstract: Large-scale high-dimensional multiomics studies are essential to unravel molecular complexity in health and disease. We developed an integrated system for tissue sampling (CryoGrid), analytes preparation (PIXUL), and downstream multiomic analysis in a 96- ...

Abstract	Large-scale high-dimensional multiomics studies are essential to unravel molecular complexity in health and disease. We developed an integrated system for tissue sampling (CryoGrid), analytes preparation (PIXUL), and downstream multiomic analysis in a 96-well plate format (Matrix), MultiomicsTracks96, which we used to interrogate matched frozen and formalin-fixed paraffin-embedded (FFPE) mouse organs. Using this system, we generated 8-dimensional omics data sets encompassing 4 molecular layers of intracellular organization: epigenome (H3K27Ac, H3K4m3, RNA polymerase II, and 5mC levels), transcriptome (messenger RNA levels), epitranscriptome (m6A levels), and proteome (protein levels) in brain, heart, kidney, and liver. There was a high correlation between data from matched frozen and FFPE organs. The Segway genome segmentation algorithm applied to epigenomic profiles confirmed known organ-specific superenhancers in both FFPE and frozen samples. Linear regression analysis showed that proteomic profiles, known to be poorly correlated with transcriptomic data, can be more accurately predicted by the full suite of multiomics data, compared with using epigenomic, transcriptomic, or epitranscriptomic measurements individually.
MeSH term(s)	Mice ; Animals ; Fixatives ; Formaldehyde ; Tissue Fixation/methods ; Proteomics/methods ; Paraffin Embedding/methods
Chemical Substances	Fixatives ; Formaldehyde (1HG84L3525)
Language	English
Publishing date	2023-11-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	80178-1
ISSN	1530-0307 ; 0023-6837
ISSN (online)	1530-0307
ISSN	0023-6837
DOI	10.1016/j.labinv.2023.100282
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Article: Analysis of gliomas DNA methylation: Assessment of pre-analytical variables.

Bomsztyk, Karol / Mar, Daniel / Denisenko, Oleg / Powell, Suzanne / Vishnoi, Monika / Delegard, Jennifer / Patel, Anoop / Ellenbogen, Richard G / Ramakrishna, Rohan / Rostomily, Robert

bioRxiv : the preprint server for biology

2024

Abstract: Precision oncology is driven by molecular biomarkers. For glioblastoma multiforme (GBM), the most common malignant adult primary brain tumor, O6-methylguanine-DNA methyltransferase ( ...

Abstract	Precision oncology is driven by molecular biomarkers. For glioblastoma multiforme (GBM), the most common malignant adult primary brain tumor, O6-methylguanine-DNA methyltransferase (
Language	English
Publishing date	2024-03-27
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.26.586350
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Article ; Online: Chromatin changes trigger laminin genes dysregulation in aging kidneys.

Denisenko, Oleg / Mar, Daniel / Trawczynski, Matthew / Bomsztyk, Karol

Aging

2018 Volume 10, Issue 5, Page(s) 1133–1145

Abstract: Dysregulation of gene expression is a hallmark of aging. We examined epigenetic mechanisms that mediate aberrant expression of laminin genes in aging rat kidneys. In old animals, no alterations were found in the levels of abundant laminin mRNAs, whereas ... ...

Abstract	Dysregulation of gene expression is a hallmark of aging. We examined epigenetic mechanisms that mediate aberrant expression of laminin genes in aging rat kidneys. In old animals, no alterations were found in the levels of abundant laminin mRNAs, whereas Lama3, b3, and c2 transcripts were increased compared to young animals. Lamc2 showed the strongest changes at the mRNA and protein levels. Lamc2 upregulation was transcriptional, as indicated by the elevated RNA polymerase II density at the gene. Furthermore, aging is associated with the loss of H3K27m3 and 5mC silencing modifications at the Lamc2 gene. Western blot analysis revealed no changes in cellular levels of H3K27m3 and cognate enzyme Ezh2 in old kidneys. Thus, the decrease in H3K27m3 at Lamc2 resulted from the re-distribution of this mark among genomic sites. Studies in kidney cells
MeSH term(s)	Aging/physiology ; Animals ; Chromatin/genetics ; Chromatin/metabolism ; DNA Methylation/genetics ; Gene Expression Regulation/physiology ; HEK293 Cells ; Humans ; Kidney ; Laminin/genetics ; Laminin/metabolism ; Male ; Rats
Chemical Substances	Chromatin ; Laminin
Language	English
Publishing date	2018-05-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1945-4589
ISSN (online)	1945-4589
DOI	10.18632/aging.101453
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Article ; Online: Sporadic DUX4 expression in FSHD myocytes is associated with incomplete repression by the PRC2 complex and gain of H3K9 acetylation on the contracted D4Z4 allele.

Haynes, Premi / Bomsztyk, Karol / Miller, Daniel G

Epigenetics & chromatin

2018 Volume 11, Issue 1, Page(s) 47

Abstract: Background: Facioscapulohumeral muscular dystrophy 1 (FSHD1) has an autosomal dominant pattern of inheritance and primarily affects skeletal muscle. The genetic cause of FSHD1 is contraction of the D4Z4 macrosatellite array on chromosome 4 alleles ... ...

Abstract	Background: Facioscapulohumeral muscular dystrophy 1 (FSHD1) has an autosomal dominant pattern of inheritance and primarily affects skeletal muscle. The genetic cause of FSHD1 is contraction of the D4Z4 macrosatellite array on chromosome 4 alleles associated with a permissive haplotype causing infrequent sporadic expression of the DUX4 gene. Epigenetically, the contracted D4Z4 array has decreased cytosine methylation and an open chromatin structure. Despite these genetic and epigenetic changes, the majority of FSHD myoblasts are able to repress DUX4 transcription. In this study we hypothesized that histone modifications distinguish DUX4 expressing and non-expressing cells from the same individuals. Results: FSHD myocytes containing the permissive 4qA haplotype with a long terminal D4Z4 unit were sorted into DUX4 expressing and non-expressing groups. We found similar CpG hypomethylation between the groups of FSHD-affected cells suggesting that CpG hypomethylation is not sufficient to trigger DUX4 expression. A survey of histone modifications present at the D4Z4 region during cell lineage commitment revealed that this region is bivalent in FSHD iPS cells with both H3K4me3 activating and H3K27me3 repressive marks present, making D4Z4 poised for DUX4 activation in pluripotent cells. After lineage commitment, the D4Z4 region becomes univalent with H3K27me3 in FSHD and non-FSHD control myoblasts and a concomitant increase in H3K4me3 in a small fraction of cells. Chromatin immunoprecipitation (ChIP) for histone modifications, chromatin modifier proteins and chromatin structural proteins on sorted FSHD myocytes revealed that activating H3K9Ac modifications were ~ fourfold higher in DUX4 expressing FSHD myocytes, while the repressive H3K27me3 modification was ~ fourfold higher at the permissive allele in DUX4 non-expressing FSHD myocytes from the same cultures. Similarly, we identified EZH2, a member of the polycomb repressive complex involved in H3K27 methylation, to be present more frequently on the permissive allele in DUX4 non-expressing FSHD myocytes. Conclusions: These results implicate PRC2 as the complex primarily responsible for DUX4 repression in the setting of FSHD and H3K9 acetylation along with reciprocal loss of H3K27me3 as key epigenetic events that result in DUX4 expression. Future studies focused on events that trigger H3K9Ac or augment PRC2 complex activity in a small fraction of nuclei may expose additional drug targets worthy of study.
MeSH term(s)	Acetylation ; Cells, Cultured ; Chromatin Assembly and Disassembly ; Histones/metabolism ; Homeodomain Proteins/genetics ; Homeodomain Proteins/metabolism ; Humans ; Muscle Cells/metabolism ; Muscular Dystrophy, Facioscapulohumeral/genetics ; Muscular Dystrophy, Facioscapulohumeral/metabolism ; Polycomb Repressive Complex 2/metabolism ; Protein Processing, Post-Translational
Chemical Substances	DUX4L1 protein, human ; Histones ; Homeodomain Proteins ; Polycomb Repressive Complex 2 (EC 2.1.1.43)
Language	English
Publishing date	2018-08-20
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2462129-8
ISSN	1756-8935 ; 1756-8935
ISSN (online)	1756-8935
ISSN	1756-8935
DOI	10.1186/s13072-018-0215-z
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Article ; Online: DNA methylation yields epigenetic clues into the diabetic nephropathy of Pima Indians.

Bomsztyk, Karol / Denisenko, Oleg / Wang, Yuliang

Kidney international

2018 Volume 93, Issue 6, Page(s) 1272–1275

Abstract: Environmental factors drive epigenetic programming. DNA methylation is the best studied modification transmitting epigenetic information. A study by Qiu et al. examined potential epigenetic roots for the decline of renal function in Pima Indians. A ... ...

Abstract	Environmental factors drive epigenetic programming. DNA methylation is the best studied modification transmitting epigenetic information. A study by Qiu et al. examined potential epigenetic roots for the decline of renal function in Pima Indians. A genomewide survey of blood leukocytes uncovered differentially methylated DNA sites in regulatory regions of genes associated with chronic kidney disease. This longitudinal study provides the first clues on epigenetic links between environmental factors and a high prevalence of diabetic kidney disease in Pima Indians.
MeSH term(s)	DNA Methylation ; Diabetes Mellitus, Type 2/genetics ; Diabetic Nephropathies ; Humans ; Indians, North American ; Longitudinal Studies ; Potassium Iodide
Chemical Substances	Potassium Iodide (1C4QK22F9J)
Language	English
Publishing date	2018-05-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Comment
ZDB-ID	120573-0
ISSN	1523-1755 ; 0085-2538
ISSN (online)	1523-1755
ISSN	0085-2538
DOI	10.1016/j.kint.2018.02.015
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Article ; Online: CryoGrid-PIXUL-RNA: high throughput RNA isolation platform for tissue transcript analysis.

Schactler, Scott A / Scheuerman, Stephen J / Lius, Andrea / Altemeier, William A / An, Dowon / Matula, Thomas J / Mikula, Michal / Kulecka, Maria / Denisenko, Oleg / Mar, Daniel / Bomsztyk, Karol

BMC genomics

2023 Volume 24, Issue 1, Page(s) 446

Abstract: Background: Disease molecular complexity requires high throughput workflows to map disease pathways through analysis of vast tissue repositories. Great progress has been made in tissue multiomics analytical technologies. To match the high throughput of ... ...

Abstract	Background: Disease molecular complexity requires high throughput workflows to map disease pathways through analysis of vast tissue repositories. Great progress has been made in tissue multiomics analytical technologies. To match the high throughput of these advanced analytical platforms, we have previously developed a multipurpose 96-well microplate sonicator, PIXUL, that can be used in multiple workflows to extract analytes from cultured cells and tissue fragments for various downstream molecular assays. And yet, the sample preparation devices, such as PIXUL, along with the downstream multiomics analytical capabilities have not been fully exploited to interrogate tissues because storing and sampling of such biospecimens remain, in comparison, inefficient. Results: To mitigate this tissue interrogation bottleneck, we have developed a low-cost user-friendly system, CryoGrid, to catalog, cryostore and sample tissue fragments. TRIzol is widely used to isolate RNA but it is labor-intensive, hazardous, requires fume-hoods, and is an expensive reagent. Columns are also commonly used to extract RNA but they involve many steps, are prone to human errors, and are also expensive. Both TRIzol and column protocols use test tubes. We developed a microplate PIXUL-based TRIzol-free and column-free RNA isolation protocol that uses a buffer containing proteinase K (PK buffer). We have integrated the CryoGrid system with PIXUL-based PK buffer, TRIzol, and PureLink column methods to isolate RNA for gene-specific qPCR and genome-wide transcript analyses. CryoGrid-PIXUL, when integrated with either PK buffer, TRIzol or PureLink column RNA isolation protocols, yielded similar transcript profiles in frozen organs (brain, heart, kidney and liver) from a mouse model of sepsis. Conclusions: RNA isolation using the CryoGrid-PIXUL system combined with the 96-well microplate PK buffer method offers an inexpensive user-friendly high throughput workflow to study transcriptional responses in tissues in health and disease as well as in therapeutic interventions.
MeSH term(s)	Animals ; Mice ; Humans ; RNA ; Phenols ; Cells, Cultured ; Specimen Handling
Chemical Substances	RNA (63231-63-0) ; trizol ; Phenols
Language	English
Publishing date	2023-08-08
Publishing country	England
Document type	Journal Article
ZDB-ID	2041499-7
ISSN	1471-2164 ; 1471-2164
ISSN (online)	1471-2164
ISSN	1471-2164
DOI	10.1186/s12864-023-09527-7
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Article ; Online: Single cell epigenetic visualization assay.

Kint, Sam / Van Criekinge, Wim / Vandekerckhove, Linos / De Vos, Winnok H / Bomsztyk, Karol / Krause, Diane S / Denisenko, Oleg

Nucleic acids research

2021 Volume 49, Issue 8, Page(s) e43

Abstract: Characterization of the epigenetic status of individual cells remains a challenge. Current sequencing approaches have limited coverage, and it is difficult to assign an epigenetic status to the transcription state of individual gene alleles in the same ... ...

Abstract	Characterization of the epigenetic status of individual cells remains a challenge. Current sequencing approaches have limited coverage, and it is difficult to assign an epigenetic status to the transcription state of individual gene alleles in the same cell. To address these limitations, a targeted microscopy-based epigenetic visualization assay (EVA) was developed for detection and quantification of epigenetic marks at genes of interest in single cells. The assay is based on an in situ biochemical reaction between an antibody-conjugated alkaline phosphatase bound to the epigenetic mark of interest, and a 5'-phosphorylated fluorophore-labeled DNA oligo tethered to a target gene by gene-specific oligonucleotides. When the epigenetic mark is present at the gene, phosphate group removal by the phosphatase protects the oligo from λ-exonuclease activity providing a quantitative fluorescent readout. We applied EVA to measure 5-methylcytosine (5mC) and H3K9Ac levels at different genes and the HIV-1 provirus in human cell lines. To link epigenetic marks to gene transcription, EVA was combined with RNA-FISH. Higher 5mC levels at the silenced compared to transcribed XIST gene alleles in female somatic cells validated this approach and demonstrated that EVA can be used to relate epigenetic marks to the transcription status of individual gene alleles.
MeSH term(s)	5-Methylcytosine/metabolism ; Acetylation ; Cell Line ; DNA Methylation ; Early Growth Response Protein 1/genetics ; Early Growth Response Protein 1/metabolism ; Epigenesis, Genetic ; Epigenomics ; Female ; Gene Expression Regulation/genetics ; Gene Silencing ; HIV-1/metabolism ; Histones/metabolism ; Humans ; Image Processing, Computer-Assisted ; In Situ Hybridization, Fluorescence/methods ; Proviruses/metabolism ; RNA, Long Noncoding/genetics ; RNA, Long Noncoding/metabolism ; Real-Time Polymerase Chain Reaction ; Single-Cell Analysis/methods
Chemical Substances	EGR1 protein, human ; Early Growth Response Protein 1 ; Histones ; RNA, Long Noncoding ; XIST non-coding RNA ; 5-Methylcytosine (6R795CQT4H)
Language	English
Publishing date	2021-01-29
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gkab009
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