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Article ; Online: Histone H3K4me3 breadth in hypoxia reveals endometrial core functions and stress adaptation linked to endometriosis.

Rytkönen, Kalle T / Faux, Thomas / Mahmoudian, Mehrad / Heinosalo, Taija / Nnamani, Mauris C / Perheentupa, Antti / Poutanen, Matti / Elo, Laura L / Wagner, Günter P

iScience

2022 Volume 25, Issue 5, Page(s) 104235

Abstract: Trimethylation of histone H3 at lysine 4 (H3K4me3) is a marker of active promoters. Broad H3K4me3 promoter domains have been associated with cell type identity, but H3K4me3 dynamics upon cellular stress have not been well characterized. We assessed this ... ...

Abstract	Trimethylation of histone H3 at lysine 4 (H3K4me3) is a marker of active promoters. Broad H3K4me3 promoter domains have been associated with cell type identity, but H3K4me3 dynamics upon cellular stress have not been well characterized. We assessed this by exposing endometrial stromal cells to hypoxia, which is a major cellular stress condition. We observed that hypoxia modifies the existing H3K4me3 marks and that promoter H3K4me3 breadth rather than height correlates with transcription. Broad H3K4me3 domains mark genes for endometrial core functions and are maintained or selectively extended upon hypoxia. Hypoxic extension of H3K4me3 breadth associates with stress adaptation genes relevant for the survival of endometrial cells including transcription factor KLF4, for which we found increased protein expression in the stroma of endometriosis lesions. These results substantiate the view on broad H3K4me3 as a marker of cell identity genes and reveal participation of H3K4me3 extension in cellular stress adaptation.
Language	English
Publishing date	2022-04-12
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2022.104235
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Article ; Online: Cis-Regulatory Evolution of Forkhead Box O1 (FOXO1), a Terminal Selector Gene for Decidual Stromal Cell Identity.

Park, Yeonwoo / Nnamani, Mauris C / Maziarz, Jamie / Wagner, Günter P

Molecular biology and evolution

2016 Volume 33, Issue 12, Page(s) 3161–3169

Abstract: Studies in human and mouse have shown that decidual stromal cells (DSC), which develop in the innermost lining of uterus, mediate placentation by regulating maternal immune response against the fetus and the extent of fetal invasion. Investigating when ... ...

Abstract	Studies in human and mouse have shown that decidual stromal cells (DSC), which develop in the innermost lining of uterus, mediate placentation by regulating maternal immune response against the fetus and the extent of fetal invasion. Investigating when and how DSC evolved is thus a key step to reconstructing the evolutionary history of mammalian pregnancy. We present molecular evidence placing the origin of DSC in the stem lineage of eutherians (extant placental mammals). The transcription factor forkhead box O1 (FOXO1) is a part of the core regulatory transcription factor complex (CoRC) that establishes the cell type identity of DSC. Decidualization, the process through which DSC differentiate from endometrial stromal fibroblasts, requires transcriptional upregulation of FOXO1 Contrary to other examples in mammals where gene recruitment is caused by the origin of an alternative promoter, FOXO1 is transcribed from the same promoter in DSC as in endometrial stromal fibroblasts. Comparing the activities of FOXO1 promoters from human, mouse, manatee (Afrotheria), and opossum (marsupial) revealed that FOXO1 promoter evolved responsiveness to decidualization signals in the stem lineage of eutherians. This eutherian vs. marsupial pattern of promoter activity was not observed in some other cell types expressing FOXO1, suggesting that this cis-regulatory evolution occurred specifically in the context of the origin of DSC. Sequence comparison revealed eutherian-specifically conserved nucleotides that contribute to the eutherian promoter activity. We conclude that the cis-regulatory activity of a terminal selector gene for decidual stromal cell identity evolved in the stem lineage of eutherians supporting a model where decidual cells are a eutherian innovation.
MeSH term(s)	Animals ; Biological Evolution ; Decidua/cytology ; Decidua/metabolism ; Decidua/physiology ; Evolution, Molecular ; Female ; Forkhead Box Protein O1/genetics ; Forkhead Box Protein O1/metabolism ; Humans ; Mice ; Opossums ; Placenta/metabolism ; Pregnancy ; Promoter Regions, Genetic ; Rabbits ; Selection, Genetic ; Sequence Analysis, DNA ; Stromal Cells/cytology ; Stromal Cells/metabolism ; Stromal Cells/physiology ; Trichechus
Chemical Substances	Forkhead Box Protein O1
Language	English
Publishing date	2016-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	998579-7
ISSN	1537-1719 ; 0737-4038
ISSN (online)	1537-1719
ISSN	0737-4038
DOI	10.1093/molbev/msw193
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Article ; Online: The mammalian decidual cell evolved from a cellular stress response.

Erkenbrack, Eric M / Maziarz, Jamie D / Griffith, Oliver W / Liang, Cong / Chavan, Arun R / Nnamani, Mauris C / Wagner, Günter P

PLoS biology

2018 Volume 16, Issue 8, Page(s) e2005594

Abstract: Among animal species, cell types vary greatly in terms of number and kind. The number of cell types found within an organism differs considerably between species, and cell type diversity is a significant contributor to differences in organismal structure ...

Abstract	Among animal species, cell types vary greatly in terms of number and kind. The number of cell types found within an organism differs considerably between species, and cell type diversity is a significant contributor to differences in organismal structure and function. These observations suggest that cell type origination is a significant source of evolutionary novelty. The molecular mechanisms that result in the evolution of novel cell types, however, are poorly understood. Here, we show that a novel cell type of eutherians mammals, the decidual stromal cell (DSC), evolved by rewiring an ancestral cellular stress response. We isolated the precursor cell type of DSCs, endometrial stromal fibroblasts (ESFs), from the opossum Monodelphis domestica. We show that, in opossum ESFs, the majority of decidual core regulatory genes respond to decidualizing signals but do not regulate decidual effector genes. Rather, in opossum ESFs, decidual transcription factors function in apoptotic and oxidative stress response. We propose that rewiring of cellular stress responses was an important mechanism for the evolution of the eutherian decidual cell type.
MeSH term(s)	Animals ; Biological Evolution ; Decidua/physiology ; Endometrium/physiology ; Evolution, Molecular ; Female ; Fibroblasts ; Mammals ; Monodelphis/physiology ; Stress, Physiological/genetics ; Stress, Physiological/physiology ; Stromal Cells/metabolism ; Stromal Cells/physiology ; Transcription Factors/metabolism
Chemical Substances	Transcription Factors
Language	English
Publishing date	2018-08-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2126776-5
ISSN	1545-7885 ; 1544-9173
ISSN (online)	1545-7885
ISSN	1544-9173
DOI	10.1371/journal.pbio.2005594
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Book ; Online: Ancient Transposable Elements Transformed the Uterine Regulatory Landscape and Transcriptome during the Evolution of Mammalian Pregnancy

Lynch, Vincent J. / Nnamani, Mauris C. / Feschotte, Cédric / Wagner, Günter P.

2016

Keywords	TRANSPOSONS + INSERTIONSSEQUENZEN + INTRONE + SPRINGENDE GENE + EXONE (GENETIK) ; GEBÄRMUTTER (ANATOMIE UND PHYSIOLOGIE) ; GENREGULATION ; REGULATION DER GENEXPRESSION (MOLEKULARBIOLOGIE) ; SCHWANGERSCHAFT + GEBURT + ZEUGUNG (ANATOMIE UND PHYSIOLOGIE)
Language	English
Publisher	Zürich, ETH-Zürich
Publishing country	ch
Document type	Book ; Online
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Article: Evidence for independent evolution of functional progesterone withdrawal in primates and guinea pigs.

Nnamani, Mauris C / Plaza, Silvia / Romero, Roberto / Wagner, Günter P

Evolution, medicine, and public health

2013 Volume 2013, Issue 1, Page(s) 273–288

Abstract: Background and objectives: Cervix remodeling (CRM) is a critical process in preparation for parturition. Early cervix shortening is a powerful clinical predictor of preterm birth, and thus understanding how CRM is regulated is important for the ... ...

Abstract	Background and objectives: Cervix remodeling (CRM) is a critical process in preparation for parturition. Early cervix shortening is a powerful clinical predictor of preterm birth, and thus understanding how CRM is regulated is important for the prevention of prematurity. Humans and other primates differ from most other mammals by the maintenance of high levels of systemic progesterone concentrations. Humans have been hypothesized to perform functional progesterone withdrawal (FPW). Guinea pigs are similar to humans in maintaining high-progesterone concentrations through parturition, thus making them a prime model for studying CRM. Here, we analyze the phylogenetic history of FPW and document gene expression in the guinea pig uterine cervix. Methodology: Data on progesterone withdrawal were collected from the literature, and character evolution was analyzed. Uterine cervix samples were collected from non-pregnant, mid-pregnant and late pregnant guinea pigs. RNA was extracted and sequenced. Relative transcript levels were estimated and compared among sample groups. Results: The phylogenetic analysis shows that FPW evolved independently in primates and guinea pigs. The transcriptome data confirms that guinea pigs down-regulate progesterone receptor toward parturition, in contrast to humans. Some of the similarities between human and guinea pig are: down-regulation of estrogen receptor, up-regulation of VCAN and IGFBP4 as well as likely involvement of prostaglandins. Conclusions and implications: (i) FPW in guinea pigs evolved independently from that in primates. (ii) A small set of conserved gene regulatory changes has been detected.
Language	English
Publishing date	2013-12-03
Publishing country	England
Document type	Journal Article
ZDB-ID	2684837-5
ISSN	2050-6201
ISSN	2050-6201
DOI	10.1093/emph/eot022
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Article ; Online: Cell-type phylogenetics and the origin of endometrial stromal cells.

Kin, Koryu / Nnamani, Mauris C / Lynch, Vincent J / Michaelides, Elias / Wagner, Günter P

Cell reports

2015 Volume 10, Issue 8, Page(s) 1398–1409

Abstract: A challenge of genome annotation is the identification of genes performing specific biological functions. Here, we propose a phylogenetic approach that utilizes RNA-seq data to infer the historical relationships among cell types and to trace the pattern ... ...

Abstract	A challenge of genome annotation is the identification of genes performing specific biological functions. Here, we propose a phylogenetic approach that utilizes RNA-seq data to infer the historical relationships among cell types and to trace the pattern of gene-expression changes on the tree. The hypothesis is that gene-expression changes coincidental with the origin of a cell type will be important for the function of the derived cell type. We apply this approach to the endometrial stromal cells (ESCs), which are critical for the initiation and maintenance of pregnancy. Our approach identified well-known regulators of ESCs, PGR and FOXO1, as well as genes not yet implicated in female fertility, including GATA2 and TFAP2C. Knockdown analysis confirmed that they are essential for ESC differentiation. We conclude that phylogenetic analysis of cell transcriptomes is a powerful tool for discovery of genes performing cell-type-specific functions.
MeSH term(s)	Cell Differentiation ; Cell Line ; Cluster Analysis ; Endometrium/cytology ; Female ; Forkhead Box Protein O1 ; Forkhead Transcription Factors/antagonists & inhibitors ; Forkhead Transcription Factors/genetics ; Forkhead Transcription Factors/metabolism ; GATA2 Transcription Factor/antagonists & inhibitors ; GATA2 Transcription Factor/genetics ; GATA2 Transcription Factor/metabolism ; Humans ; Myofibroblasts/cytology ; Myofibroblasts/metabolism ; Pregnancy ; Principal Component Analysis ; RNA Interference ; RNA, Small Interfering/metabolism ; Sequence Analysis, RNA ; Stromal Cells/cytology ; Stromal Cells/metabolism ; Transcription Factor AP-2/antagonists & inhibitors ; Transcription Factor AP-2/genetics ; Transcription Factor AP-2/metabolism
Chemical Substances	FOXO1 protein, human ; Forkhead Box Protein O1 ; Forkhead Transcription Factors ; GATA2 Transcription Factor ; GATA2 protein, human ; RNA, Small Interfering ; TFAP2C protein, human ; Transcription Factor AP-2
Language	English
Publishing date	2015-03-03
Publishing country	United States
Document type	Journal Article ; 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.2015.01.062
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Article ; Online: Evolution of Gene Expression in the Uterine Cervix related to Steroid Signaling: Conserved features in the regulation of cervical ripening.

Wagner, Günter P / Nnamani, Mauris C / Chavan, Arun Rajendra / Maziarz, Jamie / Protopapas, Stella / Condon, Jennifer / Romero, Roberto

Scientific reports

2017 Volume 7, Issue 1, Page(s) 4439

Abstract: The uterine cervix is the boundary structure between the uterus and the vagina and is key for the maintenance of pregnancy and timing of parturition. Here we report on a comparative transcriptomic study of the cervix of four placental mammals, mouse, ... ...

Abstract	The uterine cervix is the boundary structure between the uterus and the vagina and is key for the maintenance of pregnancy and timing of parturition. Here we report on a comparative transcriptomic study of the cervix of four placental mammals, mouse, guinea pig, rabbit and armadillo, and one marsupial, opossum. Our aim is to investigate the evolution of cervical gene expression as related to putative mechanisms for functional progesterone withdrawal. Our findings are: 1) The patterns of gene expression in eutherian (placental) mammals are consistent with the notion that an increase in the E/P4 signaling ratio is critical for cervical ripening. How the increased E/P4 ratio is achieved, however, is variable between species. 2) None of the genes related to steroid signaling, that are modulated in eutherian species, change expression during opossum gestation. 3) A tendency for decreased expression of progesterone receptor co-activators (NCOA1, -2 and -3, and CREBBP) towards term is a shared derived feature of eutherians. This suggests that parturition is associated with broad scale histone de-acetylation. Western-blotting on mouse cervix confirmed large scale histone de-acetylation in labor. This finding may have important implications for the control of premature cervical ripening and prevention of preterm birth in humans.
MeSH term(s)	Acetylation ; Animals ; Cervical Ripening ; Cervix Uteri/metabolism ; Estrogens/metabolism ; Female ; Gene Expression Profiling ; Gene Expression Regulation ; Guinea Pigs ; Histones/metabolism ; Mice ; Pregnancy ; Pregnancy, Animal ; Progesterone/metabolism ; Prostaglandins/metabolism ; Rabbits ; Relaxin/metabolism ; Signal Transduction ; Steroids/metabolism
Chemical Substances	Estrogens ; Histones ; Prostaglandins ; Steroids ; Progesterone (4G7DS2Q64Y) ; Relaxin (9002-69-1)
Language	English
Publishing date	2017-06-30
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-017-04759-6
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Article ; Online: A Derived Allosteric Switch Underlies the Evolution of Conditional Cooperativity between HOXA11 and FOXO1.

Nnamani, Mauris C / Ganguly, Soumya / Erkenbrack, Eric M / Lynch, Vincent J / Mizoue, Laura S / Tong, Yingchun / Darling, Heather L / Fuxreiter, Monika / Meiler, Jens / Wagner, Günter P

Cell reports

2016 Volume 15, Issue 10, Page(s) 2097–2108

Abstract: Transcription factors (TFs) play multiple roles in development. Given this multifunctionality, it has been assumed that TFs are evolutionarily highly constrained. Here, we investigate the molecular mechanisms for the origin of a derived functional ... ...

Abstract	Transcription factors (TFs) play multiple roles in development. Given this multifunctionality, it has been assumed that TFs are evolutionarily highly constrained. Here, we investigate the molecular mechanisms for the origin of a derived functional interaction between two TFs, HOXA11 and FOXO1. We have previously shown that the regulatory role of HOXA11 in mammalian endometrial stromal cells requires interaction with FOXO1, and that the physical interaction between these proteins evolved before their functional cooperativity. Here, we demonstrate that the derived functional cooperativity between HOXA11 and FOXO1 is due to derived allosteric regulation of HOXA11 by FOXO1. This study shows that TF function can evolve through changes affecting the functional output of a pre-existing protein complex.
Language	English
Publishing date	2016-06-7
Publishing country	United States
Document type	Journal Article
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2016.04.088
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Article ; Online: Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy.

Lynch, Vincent J / Nnamani, Mauris C / Kapusta, Aurélie / Brayer, Kathryn / Plaza, Silvia L / Mazur, Erik C / Emera, Deena / Sheikh, Shehzad Z / Grützner, Frank / Bauersachs, Stefan / Graf, Alexander / Young, Steven L / Lieb, Jason D / DeMayo, Francesco J / Feschotte, Cédric / Wagner, Günter P

Cell reports

2015 Volume 10, Issue 4, Page(s) 551–561

Abstract: A major challenge in biology is determining how evolutionarily novel characters originate; however, mechanistic explanations for the origin of new characters are almost completely unknown. The evolution of pregnancy is an excellent system in which to ... ...

Abstract	A major challenge in biology is determining how evolutionarily novel characters originate; however, mechanistic explanations for the origin of new characters are almost completely unknown. The evolution of pregnancy is an excellent system in which to study the origin of novelties because mammals preserve stages in the transition from egg laying to live birth. To determine the molecular bases of this transition, we characterized the pregnant/gravid uterine transcriptome from tetrapods to trace the evolutionary history of uterine gene expression. We show that thousands of genes evolved endometrial expression during the origins of mammalian pregnancy, including genes that mediate maternal-fetal communication and immunotolerance. Furthermore, thousands of cis-regulatory elements that mediate decidualization and cell-type identity in decidualized stromal cells are derived from ancient mammalian transposable elements (TEs). Our results indicate that one of the defining mammalian novelties evolved from DNA sequences derived from ancient mammalian TEs co-opted into hormone-responsive regulatory elements distributed throughout the genome.
MeSH term(s)	Animals ; Biological Evolution ; DNA Transposable Elements/genetics ; Female ; Mammals ; Molecular Sequence Data ; Pregnancy ; Transcriptome/genetics ; Uterus/metabolism
Chemical Substances	DNA Transposable Elements
Language	English
Publishing date	2015-02-03
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.2014.12.052
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Article ; Online: Ancient Transposable Elements Transformed the Uterine Regulatory Landscape and Transcriptome during the Evolution of Mammalian Pregnancy

Lynch, Vincent J. / Nnamani, Mauris C. / Kapusta, Aurélie / Brayer, Kathryn / Plaza, Silvia L. / Mazur, Eric C. / Emera, Deena / Sheikh, Shehzad Z. / Grützner, Frank / Bauersachs, Stefan / Graf, Alexander / Young, Steven L. / Lieb, Jason D. / DeMayo, Francesco J. / Feschotte, Cédric / Wagner, Günter P.

Cell Reports, 10 (4)

2015

Abstract: ISSN:2666-3864 ... ISSN:2211- ... ...

Abstract	ISSN:2666-3864 ISSN:2211-1247
Keywords	info:eu-repo/classification/ddc/610 ; Medical sciences ; medicine
Language	English
Publishing date	2015-02-03
Publisher	Elsevier
Publishing country	ch
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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