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Article: HiExM: high-throughput expansion microscopy enables scalable super-resolution imaging.

Day, John H / Della Santina, Catherine Marin / Maretich, Pema / Auld, Alexander L / Schnieder, Kirsten K / Shin, Tay / Boyden, Edward S / Boyer, Laurie A

bioRxiv : the preprint server for biology

2024

Abstract: Expansion microscopy (ExM) enables nanoscale imaging using a standard confocal microscope through the physical, isotropic expansion of fixed immunolabeled specimens. ExM is widely employed to image proteins, nucleic acids, and lipid membranes in single ... ...

Abstract	Expansion microscopy (ExM) enables nanoscale imaging using a standard confocal microscope through the physical, isotropic expansion of fixed immunolabeled specimens. ExM is widely employed to image proteins, nucleic acids, and lipid membranes in single cells at nanoscale resolution; however, current methods cannot be performed in multi-well cell culture plates which limits the number of samples that can be processed simultaneously. We developed High-throughput Expansion Microscopy (HiExM), a robust platform that enables expansion microscopy of cells cultured in a standard 96-well plate. Our method enables consistent ~4.2x expansion within individual wells, across multiple wells, and between plates processed in parallel. We also demonstrate that HiExM can be combined with high-throughput confocal imaging platforms greatly improve the ease and scalability of image acquisition. As an example, we analyzed the effects of doxorubicin, a known cardiotoxic agent, in human cardiomyocytes (CMs) based on Hoechst signal intensity. We show a dose dependent effect on nuclear chromatin that is not observed in unexpanded CMs, suggesting that HiExM improves the detection of cellular phenotypes in response to drug treatment. Our method broadens the application of ExM as a tool for scalable super-resolution imaging in biological research applications.
Language	English
Publishing date	2024-01-11
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.02.07.527509
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Article ; Online: Rapid and Live-Cell Detection of Senescence in Mesenchymal Stem Cells by Micro Magnetic Resonance Relaxometry.

Thamarath, Smitha Surendran / Tee, Ching Ann / Neo, Shu Hui / Yang, Dahou / Othman, Rashidah / Boyer, Laurie A / Han, Jongyoon

Stem cells translational medicine

2023 Volume 12, Issue 5, Page(s) 266–280

Abstract: Detection of cellular senescence is important quality analytics of cell therapy products, including mesenchymal stromal cells (MSCs). However, its detection is critically limited by the lack of specific markers and the destructive assays used to read out ...

Abstract	Detection of cellular senescence is important quality analytics of cell therapy products, including mesenchymal stromal cells (MSCs). However, its detection is critically limited by the lack of specific markers and the destructive assays used to read out these markers. Here, we establish a rapid, live-cell assay for detecting senescent cells in heterogeneous mesenchymal stromal cell (MSC) cultures. We report that the T2 relaxation time measured by microscale Magnetic Resonance Relaxometry, which is related to intracellular iron accumulation, correlates strongly with senescence markers in MSC cultures under diverse conditions, including different passages and donors, size-sorted MSCs by inertial spiral microfluidic device, and drug-induced senescence. In addition, the live-cell and non-destructive method presented here has general applicability to other cells and tissues and can critically advance our understanding of cellular senescence.
MeSH term(s)	Cell Proliferation ; Cellular Senescence ; Mesenchymal Stem Cells ; Cell- and Tissue-Based Therapy ; Magnetic Resonance Spectroscopy ; Cells, Cultured
Language	English
Publishing date	2023-03-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2642270-0
ISSN	2157-6580 ; 2157-6580
ISSN (online)	2157-6580
ISSN	2157-6580
DOI	10.1093/stcltm/szad014
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Article ; Online: Size-Based Microfluidic-Enriched Mesenchymal Stem Cell Subpopulations Enhance Articular Cartilage Repair.

Yang, Zheng / Wu, Yingnan / Neo, Shu Hui / Yang, Dahou / Jeon, Hyungkook / Tee, Ching Ann / Denslin, Vinitha / Lin, Daryl Jimian / Lee, Eng Hin / Boyer, Laurie A / Han, Jongyoon

The American journal of sports medicine

2024 Volume 52, Issue 2, Page(s) 503–515

Abstract: Background: The functional heterogeneity of culture-expanded mesenchymal stem cells (MSCs) has hindered the clinical application of MSCs. Previous studies have shown that MSC subpopulations with superior chondrogenic capacity can be isolated using a ... ...

Abstract	Background: The functional heterogeneity of culture-expanded mesenchymal stem cells (MSCs) has hindered the clinical application of MSCs. Previous studies have shown that MSC subpopulations with superior chondrogenic capacity can be isolated using a spiral microfluidic device based on the principle of inertial cell focusing. Hypothesis: The delivery of microfluidic-enriched chondrogenic MSCs that are consistent in size and function will overcome the challenge of the functional heterogeneity of expanded MSCs and will significantly improve MSC-based cartilage repair. Study design: Controlled laboratory study. Methods: A next-generation, fully automated multidimensional double spiral microfluidic device was designed to provide more refined and efficient isolation of MSC subpopulations based on size. Analysis of in vitro chondrogenic potential and RNA sequencing was performed on size-sorted MSC subpopulations. In vivo cartilage repair efficacy was demonstrated in an osteochondral injury model in 12-week-old rats. Defects were implanted with MSC subpopulations (n = 6 per group) and compared with those implanted with unsegregated MSCs (n = 6). Osteochondral repair was assessed at 6 and 12 weeks after surgery by histological, micro-computed tomography, and mechanical analysis. Results: A chondrogenic MSC subpopulation was efficiently isolated using the multidimensional double spiral device. RNA sequencing revealed distinct transcriptomic profiles and identified differential gene expression between subpopulations. The delivery of a chondrogenic MSC subpopulation resulted in improved cartilage repair, as indicated by histological scoring, the compression modulus, and micro-computed tomography of the subchondral bone. Conclusion: We have established a rapid, label-free, and reliable microfluidic protocol for more efficient size-based enrichment of a chondrogenic MSC subpopulation. Our proof-of-concept in vivo study demonstrates the enhanced cartilage repair efficacy of these enriched chondrogenic MSCs. Clinical relevance: The delivery of microfluidic-enriched chondrogenic MSCs that are consistent in size and function can overcome the challenge of the functional heterogeneity of expanded MSCs, resulting in significant improvement in MSC-based cartilage repair. The availability of such rapid, label-free enriched chondrogenic MSCs can enable better cell therapy products for cartilage repair with improved treatment outcomes.
MeSH term(s)	Animals ; Rats ; Cartilage, Articular/surgery ; Microfluidics ; X-Ray Microtomography ; Cell Differentiation ; Mesenchymal Stem Cells ; Mesenchymal Stem Cell Transplantation/methods ; Chondrogenesis
Language	English
Publishing date	2024-01-08
Publishing country	United States
Document type	Journal Article
ZDB-ID	197482-8
ISSN	1552-3365 ; 0363-5465
ISSN (online)	1552-3365
ISSN	0363-5465
DOI	10.1177/03635465231214431
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Article ; Online: A dual role for H2A.Z.1 in modulating the dynamics of RNA polymerase II initiation and elongation.

Mylonas, Constantine / Lee, Choongman / Auld, Alexander L / Cisse, Ibrahim I / Boyer, Laurie A

Nature structural & molecular biology

2021 Volume 28, Issue 5, Page(s) 435–442

Abstract: RNA polymerase II (RNAPII) pausing immediately downstream of the transcription start site is a critical rate-limiting step for the expression of most metazoan genes. During pause release, RNAPII encounters a highly conserved +1 H2A.Z nucleosome, yet how ... ...

Abstract	RNA polymerase II (RNAPII) pausing immediately downstream of the transcription start site is a critical rate-limiting step for the expression of most metazoan genes. During pause release, RNAPII encounters a highly conserved +1 H2A.Z nucleosome, yet how this histone variant contributes to transcription is poorly understood. Here, using an inducible protein degron system combined with genomic approaches and live cell super-resolution microscopy, we show that H2A.Z.1 modulates RNAPII dynamics across most genes in murine embryonic stem cells. Our quantitative analysis shows that H2A.Z.1 slows the rate of RNAPII pause release and consequently impacts negative elongation factor dynamics as well as nascent transcription. Consequently, H2A.Z.1 also impacts re-loading of the pre-initiation complex components TFIIB and TBP. Altogether, this work provides a critical mechanistic link between H2A.Z.1 and the proper induction of mammalian gene expression programs through the regulation of RNAPII dynamics and pause release.
MeSH term(s)	Animals ; Histones/metabolism ; Mice ; Mice, Inbred C57BL ; Mouse Embryonic Stem Cells/cytology ; Mouse Embryonic Stem Cells/metabolism ; Nucleosomes/metabolism ; RNA Polymerase II/metabolism ; Transcription, Genetic
Chemical Substances	H2az1 protein, mouse ; Histones ; Nucleosomes ; RNA Polymerase II (EC 2.7.7.-)
Language	English
Publishing date	2021-05-10
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2126708-X
ISSN	1545-9985 ; 1545-9993
ISSN (online)	1545-9985
ISSN	1545-9993
DOI	10.1038/s41594-021-00589-3
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Article ; Online: Lncing epigenetic control of transcription to cardiovascular development and disease.

Rizki, Gizem / Boyer, Laurie A

Circulation research

2015 Volume 117, Issue 2, Page(s) 192–206

Abstract: Transcriptional and epigenetic regulation is critical for proper heart development, cardiac homeostasis, and pathogenesis. Long noncoding RNAs have emerged as key components of the transcriptional regulatory pathways that govern cardiac development as ... ...

Abstract	Transcriptional and epigenetic regulation is critical for proper heart development, cardiac homeostasis, and pathogenesis. Long noncoding RNAs have emerged as key components of the transcriptional regulatory pathways that govern cardiac development as well as stress response, signaling, and remodeling in cardiac pathologies. Within the past few years, studies have identified many long noncoding RNAs in the context of cardiovascular biology and have begun to reveal the key functions of these transcripts. In this review, we discuss the growing roles of long noncoding RNAs in different aspects of cardiovascular development as well as pathological responses during injury or disease. In addition, we discuss diverse mechanisms by which long noncoding RNAs orchestrate cardiac transcriptional programs. Finally, we explore the exciting potential of this novel class of transcripts as biomarkers and novel therapeutic targets for cardiovascular diseases.
MeSH term(s)	Animals ; Cardiovascular Diseases/genetics ; Cardiovascular Diseases/physiopathology ; Cardiovascular Physiological Phenomena/genetics ; Cardiovascular System/growth & development ; Chromatin Assembly and Disassembly/physiology ; Epigenesis, Genetic ; Fetal Heart/metabolism ; Forecasting ; Gene Expression Regulation, Developmental ; Heart/embryology ; Heart Septal Defects, Ventricular/genetics ; Histones/metabolism ; Humans ; Mice ; MicroRNAs/genetics ; Myocytes, Cardiac/metabolism ; RNA, Long Noncoding/classification ; RNA, Long Noncoding/genetics ; Transcription, Genetic
Chemical Substances	Histones ; MicroRNAs ; RNA, Long Noncoding
Language	English
Publishing date	2015-07-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	80100-8
ISSN	1524-4571 ; 0009-7330 ; 0931-6876
ISSN (online)	1524-4571
ISSN	0009-7330 ; 0931-6876
DOI	10.1161/CIRCRESAHA.117.304156
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Article ; Online: Expansion of human bone marrow-derived mesenchymal stromal cells with enhanced immunomodulatory properties.

Neo, Shu Hui / Her, Zhisheng / Othman, Rashidah / Tee, Ching Ann / Ong, Li Ching / Wang, Yuehua / Tan, Irwin / Tan, Jaylen / Yang, Yanmeng / Yang, Zheng / Chen, Qingfeng / Boyer, Laurie A

Stem cell research & therapy

2023 Volume 14, Issue 1, Page(s) 259

Abstract: Background: Mesenchymal stromal cells (MSCs) have broad potential as a cell therapy including for the treatment of drug-resistant inflammatory conditions with abnormal T cell proliferation such as graft-versus-host disease (GVHD). Clinical success, ... ...

Abstract	Background: Mesenchymal stromal cells (MSCs) have broad potential as a cell therapy including for the treatment of drug-resistant inflammatory conditions with abnormal T cell proliferation such as graft-versus-host disease (GVHD). Clinical success, however, has been complicated by the heterogeneity of culture-expanded MSCs as well as donor variability. Here, we devise culture conditions that promote expansion of MSCs with enhanced immunomodulatory functions both in vitro and in animal models of GVHD. Methods: Human bone marrow-derived MSCs were expanded at high-confluency (MSC Results: As compared to MSC Conclusion: Our study provides evidence that ex vivo expansion of MSCs at high confluency alters the metabolic and transcriptomic states of these cells. Importantly, this approach maximizes the production of MSCs with enhanced immunomodulatory functions without priming, thus providing a non-invasive and generalizable strategy for improving the use of MSCs for the treatment of inflammatory diseases.
MeSH term(s)	Animals ; Mice ; Humans ; Leukocytes, Mononuclear ; Bone Marrow ; Phosphatidylinositol 3-Kinases ; Mesenchymal Stem Cells ; Cytokines ; Disease Models, Animal ; DNA-Binding Proteins ; Transcription Factors ; Intercellular Signaling Peptides and Proteins
Chemical Substances	Phosphatidylinositol 3-Kinases (EC 2.7.1.-) ; Cytokines ; TRIM29 protein, human ; DNA-Binding Proteins ; Transcription Factors ; BPIFB4 protein, human ; Intercellular Signaling Peptides and Proteins
Language	English
Publishing date	2023-09-19
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2548671-8
ISSN	1757-6512 ; 1757-6512
ISSN (online)	1757-6512
ISSN	1757-6512
DOI	10.1186/s13287-023-03481-7
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Article ; Online: Getting to the heart of the matter: long non-coding RNAs in cardiac development and disease.

Scheuermann, Johanna C / Boyer, Laurie A

The EMBO journal

2013 Volume 32, Issue 13, Page(s) 1805–1816

Abstract: Cardiogenesis in mammals requires exquisite control of gene expression and faulty regulation of transcriptional programs underpins congenital heart disease (CHD), the most common defect among live births. Similarly, many adult cardiac diseases involve ... ...

Abstract	Cardiogenesis in mammals requires exquisite control of gene expression and faulty regulation of transcriptional programs underpins congenital heart disease (CHD), the most common defect among live births. Similarly, many adult cardiac diseases involve transcriptional changes and sometimes have a developmental basis. Long non-coding RNAs (lncRNAs) are a novel class of transcripts that regulate cellular processes by controlling gene expression; however, detailed insights into their biological and mechanistic functions are only beginning to emerge. Here, we discuss recent findings suggesting that lncRNAs are important factors in regulation of mammalian cardiogenesis and in the pathogenesis of CHD as well as adult cardiac disease. We also outline potential methodological and conceptual considerations for future studies of lncRNAs in the heart and other contexts.
MeSH term(s)	Adult ; Gene Expression Regulation, Developmental ; Heart Diseases/genetics ; Heart Diseases/pathology ; Humans ; RNA, Long Noncoding ; Transcription, Genetic
Chemical Substances	RNA, Long Noncoding
Language	English
Publishing date	2013-06-11
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	586044-1
ISSN	1460-2075 ; 0261-4189
ISSN (online)	1460-2075
ISSN	0261-4189
DOI	10.1038/emboj.2013.134
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Article: H2A.Z: a molecular rheostat for transcriptional control.

Subramanian, Vidya / Fields, Paul A / Boyer, Laurie A

F1000prime reports

2015 Volume 7, Page(s) 1

Abstract: The replacement of nucleosomal H2A with the histone variant H2A.Z is critical for regulating DNA-mediated processes across eukaryotes and for early development of multicellular organisms. How this variant performs these seemingly diverse roles has ... ...

Abstract	The replacement of nucleosomal H2A with the histone variant H2A.Z is critical for regulating DNA-mediated processes across eukaryotes and for early development of multicellular organisms. How this variant performs these seemingly diverse roles has remained largely enigmatic. Here, we discuss recent mechanistic insights that have begun to reveal how H2A.Z functions as a molecular rheostat for gene control. We focus on specific examples in metazoans as a model for understanding how H2A.Z integrates information from histone post-translational modifications, other histone variants, and transcription factors (TFs) to regulate proper induction of gene expression programs in response to cellular cues. Finally, we propose a general model of how H2A.Z incorporation regulates chromatin states in diverse processes.
Language	English
Publishing date	2015-01-05
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2709303-7
ISSN	2051-7599
ISSN	2051-7599
DOI	10.12703/P7-01
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Article ; Online: Polycomb Repressive Complex 2 regulates lineage fidelity during embryonic stem cell differentiation.

Thornton, Seraphim R / Butty, Vincent L / Levine, Stuart S / Boyer, Laurie A

PloS one

2014 Volume 9, Issue 10, Page(s) e110498

Abstract: Polycomb Repressive Complex 2 (PRC2) catalyzes histone H3 lysine 27 tri-methylation (H3K27me3), an epigenetic modification associated with gene repression. H3K27me3 is enriched at the promoters of a large cohort of developmental genes in embryonic stem ... ...

Abstract	Polycomb Repressive Complex 2 (PRC2) catalyzes histone H3 lysine 27 tri-methylation (H3K27me3), an epigenetic modification associated with gene repression. H3K27me3 is enriched at the promoters of a large cohort of developmental genes in embryonic stem cells (ESCs). Loss of H3K27me3 leads to a failure of ESCs to properly differentiate, making it difficult to determine the precise roles of PRC2 during lineage commitment. Moreover, while studies suggest that PRC2 prevents DNA methylation, how these two epigenetic regulators coordinate to regulate lineage programs is poorly understood. Using several PRC2 mutant ESC lines that maintain varying levels of H3K27me3, we found that partial maintenance of H3K27me3 allowed for proper temporal activation of lineage genes during directed differentiation of ESCs to spinal motor neurons (SMNs). In contrast, genes that function to specify other lineages failed to be repressed in these cells, suggesting that PRC2 is also necessary for lineage fidelity. We also found that loss of H3K27me3 leads to a modest gain in DNA methylation at PRC2 target regions in both ESCs and in SMNs. Our study demonstrates a critical role for PRC2 in safeguarding lineage decisions and in protecting genes against inappropriate DNA methylation.
MeSH term(s)	Animals ; Cell Differentiation ; Cell Line ; Cell Lineage ; CpG Islands ; DNA Methylation ; Embryonic Stem Cells/cytology ; Embryonic Stem Cells/metabolism ; Gene Expression ; Histones/genetics ; Histones/metabolism ; Mice ; Mice, Inbred C57BL ; Motor Neurons/cytology ; Motor Neurons/metabolism ; Polycomb Repressive Complex 2/genetics ; Polycomb Repressive Complex 2/metabolism ; Promoter Regions, Genetic
Chemical Substances	Histones ; Suz12 protein, mouse ; Polycomb Repressive Complex 2 (EC 2.1.1.43)
Language	English
Publishing date	2014-10-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0110498
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Article ; Online: Distal enhancers: new insights into heart development and disease.

Wamstad, Joseph A / Wang, Xinchen / Demuren, Olukunle O / Boyer, Laurie A

Trends in cell biology

2014 Volume 24, Issue 5, Page(s) 294–302

Abstract: Advances in genome research have provided an unprecedented opportunity to investigate the function of non-coding DNA regulatory regions that control transcription. Large-scale studies have recently identified hundreds of thousands of distal enhancer ... ...

Abstract	Advances in genome research have provided an unprecedented opportunity to investigate the function of non-coding DNA regulatory regions that control transcription. Large-scale studies have recently identified hundreds of thousands of distal enhancer elements; their discovery has revealed new insights into the mechanistic details of how tissue-specific gene expression patterns are established and maintained during development. Emerging evidence indicates that lineage-specific transcription factors and chromatin regulators coordinate the activation of distal enhancers to ensure robust control of gene expression programs in a cell type-specific manner. We discuss recent progress in the field and emphasize examples related to the cardiac lineage, where possible, as a model for understanding the contribution of enhancer biology to development and how disruption of enhancer function leads to disease.
MeSH term(s)	Animals ; Cell Differentiation ; Cell Lineage ; Chromatin Assembly and Disassembly ; Enhancer Elements, Genetic ; Epigenesis, Genetic ; Genetic Predisposition to Disease ; Heart/growth & development ; Heart Diseases/genetics ; Heart Diseases/metabolism ; Heart Diseases/pathology ; Humans ; Polymorphism, Single Nucleotide ; Transcription Factors/physiology
Chemical Substances	Transcription Factors
Language	English
Publishing date	2014-05
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	30122-x
ISSN	1879-3088 ; 0962-8924
ISSN (online)	1879-3088
ISSN	0962-8924
DOI	10.1016/j.tcb.2013.10.008
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