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Article ; Online: SUV39H2 controls trophoblast stem cell fate.

Wang, Lei / Chakraborty, Damayanti / Iqbal, Khursheed / Soares, Michael J

Biochimica et biophysica acta. General subjects

2021 Volume 1865, Issue 6, Page(s) 129867

Abstract: Background: The placenta is formed by the coordinated expansion and differentiation of trophoblast stem (TS) cells along a multi-lineage pathway. Dynamic regulation of histone 3 lysine 9 (H3K9) methylation is pivotal to cell differentiation for many ... ...

Abstract	Background: The placenta is formed by the coordinated expansion and differentiation of trophoblast stem (TS) cells along a multi-lineage pathway. Dynamic regulation of histone 3 lysine 9 (H3K9) methylation is pivotal to cell differentiation for many cell lineages, but little is known about its involvement in trophoblast cell development. Methods: Expression of H3K9 methyltransferases was surveyed in rat TS cells maintained in the stem state and following differentiation. The role of suppressor of variegation 3-9 homolog 2 (SUV39H2) in the regulation of trophoblast cell lineage development was investigated using a loss-of-function approach in rat TS cells and ex vivo cultured rat blastocysts. Results: Among the twelve-known H3K9 methyltransferases, only SUV39H2 exhibited robust differential expression in stem versus differentiated TS cells. SUV39H2 transcript and protein expression were high in the stem state and declined as TS cells differentiated. Disruption of SUV39H2 expression in TS cells led to an arrest in TS cell proliferation and activation of trophoblast cell differentiation. SUV39H2 regulated H3K9 methylation status at loci exhibiting differentiation-dependent gene expression. Analyses of SUV39H2 on ex vivo rat blastocyst development supported its role in regulating TS cell expansion and differentiation. We further identified SUV39H2 as a downstream target of caudal type homeobox 2, a master regulator of trophoblast lineage development. Conclusions: Our findings indicate that SUV39H2 contributes to the maintenance of TS cells and restrains trophoblast cell differentiation. General significance: SUV39H2 serves as a contributor to the epigenetic regulation of hemochorial placental development.
MeSH term(s)	Animals ; Cell Differentiation ; Cell Lineage ; Cell Proliferation ; Epigenesis, Genetic ; Female ; Histone-Lysine N-Methyltransferase/genetics ; Histone-Lysine N-Methyltransferase/metabolism ; Histones/genetics ; Histones/metabolism ; Pregnancy ; Rats ; Rats, Sprague-Dawley ; Stem Cells/cytology ; Stem Cells/metabolism ; Trophoblasts/cytology ; Trophoblasts/metabolism
Chemical Substances	Histones ; Histone-Lysine N-Methyltransferase (EC 2.1.1.43)
Language	English
Publishing date	2021-02-05
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	60-7
ISSN	1872-8006 ; 1879-2596 ; 1879-260X ; 1879-2642 ; 1879-2618 ; 1879-2650 ; 0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
ISSN (online)	1872-8006 ; 1879-2596 ; 1879-260X ; 1879-2642 ; 1879-2618 ; 1879-2650
ISSN	0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
DOI	10.1016/j.bbagen.2021.129867
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Article ; Online: Simultaneous Inhibition of LSD1 and TGFβ Enables Eradication of Poorly Immunogenic Tumors with Anti-PD-1 Treatment.

Sheng, Wanqiang / Liu, Yi / Chakraborty, Damayanti / Debo, Brian / Shi, Yang

Cancer discovery

2021 Volume 11, Issue 8, Page(s) 1970–1981

Abstract: Epigenetic regulators are a class of promising targets in combination with immune checkpoint inhibitors for cancer treatment, but the impact of the broad effects of perturbing epigenetic regulators on tumor immunotherapy remains to be fully explored. ... ...

Abstract	Epigenetic regulators are a class of promising targets in combination with immune checkpoint inhibitors for cancer treatment, but the impact of the broad effects of perturbing epigenetic regulators on tumor immunotherapy remains to be fully explored. Here we show that ablation of the histone demethylase LSD1 in multiple tumor cells induces TGFβ expression, which exerts an inhibitory effect on T-cell immunity through suppressing the cytotoxicity of intratumoral CD8
MeSH term(s)	Animals ; Cell Line, Tumor/drug effects ; Female ; Histone Demethylases/metabolism ; Humans ; Immune Checkpoint Inhibitors/pharmacology ; Immunotherapy ; Mice ; Mice, Inbred C57BL ; Programmed Cell Death 1 Receptor/antagonists & inhibitors ; Programmed Cell Death 1 Receptor/metabolism ; Transforming Growth Factor beta/metabolism
Chemical Substances	Immune Checkpoint Inhibitors ; PDCD1 protein, human ; Programmed Cell Death 1 Receptor ; Transforming Growth Factor beta ; Histone Demethylases (EC 1.14.11.-) ; KDM1A protein, human (EC 1.5.-)
Language	English
Publishing date	2021-03-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; 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-20-0017
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Article: SUV39H2 controls trophoblast stem cell fate

Wang, Lei / Chakraborty, Damayanti / Iqbal, Khursheed / Soares, Michael J

Biochimica et biophysica acta. 2021 June, v. 1865, no. 6

2021

Abstract: The placenta is formed by the coordinated expansion and differentiation of trophoblast stem (TS) cells along a multi-lineage pathway. Dynamic regulation of histone 3 lysine 9 (H3K9) methylation is pivotal to cell differentiation for many cell lineages, ... ...

Abstract	The placenta is formed by the coordinated expansion and differentiation of trophoblast stem (TS) cells along a multi-lineage pathway. Dynamic regulation of histone 3 lysine 9 (H3K9) methylation is pivotal to cell differentiation for many cell lineages, but little is known about its involvement in trophoblast cell development.Expression of H3K9 methyltransferases was surveyed in rat TS cells maintained in the stem state and following differentiation. The role of suppressor of variegation 3–9 homolog 2 (SUV39H2) in the regulation of trophoblast cell lineage development was investigated using a loss-of-function approach in rat TS cells and ex vivo cultured rat blastocysts.Among the twelve-known H3K9 methyltransferases, only SUV39H2 exhibited robust differential expression in stem versus differentiated TS cells. SUV39H2 transcript and protein expression were high in the stem state and declined as TS cells differentiated. Disruption of SUV39H2 expression in TS cells led to an arrest in TS cell proliferation and activation of trophoblast cell differentiation. SUV39H2 regulated H3K9 methylation status at loci exhibiting differentiation-dependent gene expression. Analyses of SUV39H2 on ex vivo rat blastocyst development supported its role in regulating TS cell expansion and differentiation. We further identified SUV39H2 as a downstream target of caudal type homeobox 2, a master regulator of trophoblast lineage development.Our findings indicate that SUV39H2 contributes to the maintenance of TS cells and restrains trophoblast cell differentiation.SUV39H2 serves as a contributor to the epigenetic regulation of hemochorial placental development.
Keywords	cell differentiation ; cell proliferation ; epigenetics ; gene expression ; gene expression regulation ; histones ; loss-of-function mutation ; lysine ; methylation ; methyltransferases ; protein synthesis ; rats ; stem cells ; trophoblast
Language	English
Dates of publication	2021-06
Publishing place	Elsevier B.V.
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	840755-1
ISSN	0304-4165
ISSN	0304-4165
DOI	10.1016/j.bbagen.2021.129867
Database	NAL-Catalogue (AGRICOLA)

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Article: Ex vivo

Chakraborty, Damayanti / Muto, Masanaga / Soares, Michael J

Bio-protocol

2018 Volume 7, Issue 24

Abstract: In this protocol report, we describe a lentiviral gene delivery technique for genetic modification of the rat trophoblast cell lineage. Lentiviral packaged gene constructs can be efficiently and specifically delivered to the trophoblast cell lineage of ... ...

Abstract	In this protocol report, we describe a lentiviral gene delivery technique for genetic modification of the rat trophoblast cell lineage. Lentiviral packaged gene constructs can be efficiently and specifically delivered to the trophoblast cell lineage of the blastocyst. The consequences of 'gain-of-function' and 'loss-of-function' blastocyst manipulations can be evaluated with
Language	English
Publishing date	2018-01-18
Publishing country	United States
Document type	Journal Article
ZDB-ID	2833269-6
ISSN	2331-8325
ISSN	2331-8325
DOI	10.21769/BioProtoc.2652
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Article ; Online: Hypoxia Signaling and Placental Adaptations.

Chakraborty, Damayanti / Scott, Regan L / Soares, Michael J

Methods in molecular biology (Clifton, N.J.)

2017 Volume 1742, Page(s) 167–183

Abstract: Oxygen is an essential nutrient for cells. Oxygen is delivered to tissues via red blood cells through the vasculature. Molecular mechanisms mediating cellular responses to low oxygen tension have been identified. Hypoxia-inducible factors (HIFs) are ... ...

Abstract	Oxygen is an essential nutrient for cells. Oxygen is delivered to tissues via red blood cells through the vasculature. Molecular mechanisms mediating cellular responses to low oxygen tension have been identified. Hypoxia-inducible factors (HIFs) are activated by low oxygen and promote transcriptional regulation of downstream effector genes, which lead to cellular adaptations. Controlled hypoxia exposure is utilized as an experimental tool to investigate biological processes, regulating cellular adaptations. Here we describe detailed protocols for hypoxia exposure of pregnant rodent models and low oxygen exposure of trophoblast stem cells, utilizing gas-regulated chamber systems. The presentation also includes phenotypic analyses of the manipulated animal models and cells.
MeSH term(s)	Adaptation, Physiological ; Animals ; Cell Hypoxia ; Female ; Gene Expression Profiling/methods ; Gene Regulatory Networks ; Oxygen/metabolism ; Phenotype ; Placenta/cytology ; Placenta/metabolism ; Pregnancy ; Rats ; Signal Transduction ; Trophoblasts/cytology ; Trophoblasts/metabolism
Chemical Substances	Oxygen (S88TT14065)
Language	English
Publishing date	2017-12-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-7665-2_15
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Collective regulation of chromatin modifications predicts replication timing during cell cycle.

Van Rechem, Capucine / Ji, Fei / Chakraborty, Damayanti / Black, Joshua C / Sadreyev, Ruslan I / Whetstine, Johnathan R

Cell reports

2021 Volume 37, Issue 1, Page(s) 109799

Abstract: Replication timing (RT) associates with genome architecture, while having a mixed relationship to histone marks. By profiling replication at high resolution and assessing broad histone marks across the cell cycle at the resolution of RT with and without ... ...

Abstract	Replication timing (RT) associates with genome architecture, while having a mixed relationship to histone marks. By profiling replication at high resolution and assessing broad histone marks across the cell cycle at the resolution of RT with and without genetic perturbation, we address the causal relationship between histone marks and RT. Four primary chromatin states, including an uncharacterized H3K36me2 state, emerge and define 97% of the mappable genome. RT and local replication patterns (e.g., initiation zones) quantitatively associate with chromatin states, histone mark dynamics, and spatial chromatin structure. Manipulation of broad histone marks and enhancer elements by overexpressing the histone H3 lysine 9/36 tri-demethylase KDM4A impacts RT across 11% of the genome. Broad histone modification changes were strong predictors of the observed RT alterations. Lastly, replication within H3K36me2-enriched neighborhoods is sensitive to KDM4A overexpression and is controlled at a megabase scale. These studies establish a role for collective chromatin mark regulation in modulating RT.
MeSH term(s)	Cell Line ; Chromatin/chemistry ; Chromatin/metabolism ; DNA Replication Timing/physiology ; Enhancer Elements, Genetic/genetics ; Genome ; Histone Code/genetics ; Humans ; Jumonji Domain-Containing Histone Demethylases/genetics ; Jumonji Domain-Containing Histone Demethylases/metabolism ; Methylation ; S Phase
Chemical Substances	Chromatin ; Jumonji Domain-Containing Histone Demethylases (EC 1.14.11.-) ; KDM4A protein, human (EC 1.5.-)
Language	English
Publishing date	2021-10-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2021.109799
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Article ; Online: The lysine demethylase KDM4A controls the cell-cycle expression of replicative canonical histone genes.

Van Rechem, Capucine / Ji, Fei / Mishra, Sweta / Chakraborty, Damayanti / Murphy, Sedona E / Dillingham, Megan E / Sadreyev, Ruslan I / Whetstine, Johnathan R

Biochimica et biophysica acta. Gene regulatory mechanisms

2020 Volume 1863, Issue 10, Page(s) 194624

Abstract: Chromatin modulation provides a key checkpoint for controlling cell cycle regulated gene networks. The replicative canonical histone genes are one such gene family under tight regulation during cell division. These genes are most highly expressed during ... ...

Abstract	Chromatin modulation provides a key checkpoint for controlling cell cycle regulated gene networks. The replicative canonical histone genes are one such gene family under tight regulation during cell division. These genes are most highly expressed during S phase when histones are needed to chromatinize the new DNA template. While this fact has been known for a while, limited knowledge exists about the specific chromatin regulators controlling their temporal expression during cell cycle. Since histones and their associated mutations are emerging as major players in diseases such as cancer, identifying the chromatin factors modulating their expression is critical. The histone lysine tri-demethylase KDM4A is regulated over cell cycle and plays a direct role in DNA replication timing, site-specific rereplication, and DNA amplifications during S phase. Here, we establish an unappreciated role for the catalytically active KDM4A in directly regulating canonical replicative histone gene networks during cell cycle. Of interest, we further demonstrate that KDM4A interacts with proteins controlling histone expression and RNA processing (i.e., hnRNPUL1 and FUS/TLS). Together, this study provides a new function for KDM4A in modulating canonical histone gene expression.
MeSH term(s)	Catalysis ; DNA Replication ; Epigenesis, Genetic ; Gene Expression Profiling ; Gene Expression Regulation ; Histones/genetics ; Histones/metabolism ; Humans ; Jumonji Domain-Containing Histone Demethylases/genetics ; Transcription, Genetic
Chemical Substances	Histones ; Jumonji Domain-Containing Histone Demethylases (EC 1.14.11.-) ; KDM4A protein, human (EC 1.5.-)
Language	English
Publishing date	2020-08-13
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2918786-2
ISSN	1876-4320 ; 1874-9399
ISSN (online)	1876-4320
ISSN	1874-9399
DOI	10.1016/j.bbagrm.2020.194624
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Zs.A 7156: Show issues

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Article ; Online: Natural killer-cell deficiency alters placental development in rats.

Renaud, Stephen J / Scott, Regan L / Chakraborty, Damayanti / Rumi, Mohammad A K / Soares, Michael J

Biology of reproduction

2017 Volume 96, Issue 1, Page(s) 145–158

Abstract: Natural killer (NK) cells are the most prevalent leukocyte population in the uterus during early pregnancy. Natural killer cells contribute to uterine vascular (spiral artery) remodeling in preparation for the increased demand on these vessels later in ... ...

Abstract	Natural killer (NK) cells are the most prevalent leukocyte population in the uterus during early pregnancy. Natural killer cells contribute to uterine vascular (spiral artery) remodeling in preparation for the increased demand on these vessels later in pregnancy. A second wave of spiral artery modification is directed by invasive trophoblast cells. The significance of the initial wave of NK-cell-mediated vascular remodeling in species exhibiting deep trophoblast invasion such as humans and rats is not known. The purpose of this study was to generate a genetic model of NK-cell deficiency in rats, and determine the consequences of NK-cell deficiency on spiral artery remodeling and reproductive outcomes. To accomplish this task, we utilized zinc finger nuclease-mediated genome editing of the rat interleukin-15 (Il15) gene. Il15 encodes a cytokine required for NK-cell lineage development. Using this strategy, a founder rat was generated containing a frameshift deletion in Il15. Uteri of females harboring a homozygous mutation at the Il15 locus contained no detectable NK cells. NK-cell deficiency did not impact fetal growth or viability. However, NK-cell deficiency caused major structural changes to the placenta, including expansion of the junctional zone and robust, early-onset activation of invasive trophoblast-guided spiral artery remodeling. In summary, we successfully generated an NK-cell-deficient rat and showed, using this model, that NK cells dampen the extent of trophoblast invasion and delay trophoblast-directed spiral artery remodeling. This study furthers our understanding of the role of NK cells on uterine vascular remodeling, trophoblast invasion, and placental development.
MeSH term(s)	Animals ; Body Weight ; Female ; Interleukin-15/deficiency ; Interleukin-15/genetics ; Killer Cells, Natural/physiology ; Male ; Mutagenesis, Site-Directed ; Organ Size ; Placentation ; Pregnancy ; Pregnancy Outcome ; Rats, Sprague-Dawley ; Spleen/pathology
Chemical Substances	Interleukin-15
Language	English
Publishing date	2017-04-28
Publishing country	United States
Document type	Journal Article
ZDB-ID	1118-6
ISSN	1529-7268 ; 0006-3363
ISSN (online)	1529-7268
ISSN	0006-3363
DOI	10.1095/biolreprod.116.142752
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Zs.A 551: Show issues

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Article ; Online: NK cells, hypoxia and trophoblast cell differentiation.

Chakraborty, Damayanti / Rumi, M A Karim / Soares, Michael J

Cell cycle (Georgetown, Tex.)

2012 Volume 11, Issue 13, Page(s) 2427–2430

Abstract: Hemochorial placentation is characterized by extensive remodeling of the maternal vasculature, converting them to flaccid low resistance vessels. This process greatly facilitates exchange of nutrients and gases between the mother and the fetus. Two key ... ...

Abstract	Hemochorial placentation is characterized by extensive remodeling of the maternal vasculature, converting them to flaccid low resistance vessels. This process greatly facilitates exchange of nutrients and gases between the mother and the fetus. Two key modulators that orchestrate these vascular changes have been identified at the maternal fetal interface, natural killer (NK) cells and invasive trophoblast cells. Hypoxia-inducible factor (HIF) transcription factors direct cellular responses to low oxygen, influencing trophoblast lineage commitment and promoting development of the invasive trophoblast lineage. This short review focuses on role of NK cells on uterine spiral artery development and subsequent modulation of oxygen tensions at the maternal fetal interface.
MeSH term(s)	Basic Helix-Loop-Helix Transcription Factors/metabolism ; Cell Differentiation ; Female ; Humans ; Hypoxia ; Killer Cells, Natural/immunology ; Killer Cells, Natural/metabolism ; Maternal-Fetal Exchange ; Placenta/blood supply ; Pregnancy ; Trophoblasts/cytology ; Trophoblasts/metabolism
Chemical Substances	Basic Helix-Loop-Helix Transcription Factors
Language	English
Publishing date	2012-07-01
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2146183-1
ISSN	1551-4005 ; 1538-4101 ; 1554-8627
ISSN (online)	1551-4005
ISSN	1538-4101 ; 1554-8627
DOI	10.4161/cc.20542
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Zs.A 5881: Show issues

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Article: Relative expression of proprotein convertases in rat ovaries during pregnancy.

Kwok, Simon Cm / Chakraborty, Damayanti / Soares, Michael J / Dai, Guoli

Journal of ovarian research

2013 Volume 6, Issue 1, Page(s) 91

Abstract: Background: Proprotein convertases are a family of serine proteinases that are related to bacterial subtilisin and yeast kexin. They are involved in posttranslational processing of the precursors of a vast number of cellular proteins. With the exception ...

Abstract	Background: Proprotein convertases are a family of serine proteinases that are related to bacterial subtilisin and yeast kexin. They are involved in posttranslational processing of the precursors of a vast number of cellular proteins. With the exception of PC1/3, the relative expression levels of the proprotein convertases in the ovary during pregnancy have not been reported. The purpose of this study is to determine by real-time PCR the relative expression levels of all nine proprotein convertases in rat ovaries during pregnancy and at 3 days postpartum. Methods: RNA was extracted from ovaries at Day 0, 4, 9, 11, 13, 15, 18, and 20 of pregnancy as well as 3 days postpartum. Relative expression levels of Pcsk1, Pcsk2, Furin, Pcsk4, Pcsk5, Pcsk6, Pcsk7, Mbtps1 and Pcsk9 were determined with real-time PCR. Results were reported as fold-change over the level at Day 0 of pregnancy. Results: Results showed that Pcsk1 and Pcsk6 were upregulated as gestation advanced, in parallel with an observed increase in relaxin transcript. Pcsk2 showed downregulation as gestation advanced, while Pcsk5 showed relatively higher levels in early pregnancy and postpartum, but lower level in mid-pregnancy. On the other hand, Furin, Pcsk4, Pcsk7, Mbtps1 and Pcsk9 showed little change of expression throughout gestation. Conclusion: PC1/3 (PCSK1) and PACE4 (PCSK6) may play an important role in proprotein processing in the ovary during late pregnancy.
Language	English
Publishing date	2013-12-11
Publishing country	England
Document type	Journal Article
ZDB-ID	2455679-8
ISSN	1757-2215
ISSN	1757-2215
DOI	10.1186/1757-2215-6-91
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