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Article ; Online: Autophagy is required for stem-cell-mediated endometrial programming and the establishment of pregnancy.

Popli, Pooja / Kommagani, Ramakrishna

2023 Volume 20, Issue 4, Page(s) 970–972

Abstract: Autophagy plays an important role in the normal growth and morphogenesis of a variety of tissues. Its role in uterine maturation, however, is not fully characterized. Recently, we reported that BECN1 (Beclin1)-dependent autophagy, but not apoptosis, is ... ...

Abstract	Autophagy plays an important role in the normal growth and morphogenesis of a variety of tissues. Its role in uterine maturation, however, is not fully characterized. Recently, we reported that BECN1 (Beclin1)-dependent autophagy, but not apoptosis, is crucial for stem cell-mediated endometrial programming and the establishment of pregnancy in mice. Upon genetic and pharmacological inhibition of BECN1-mediated autophagy, female mice displayed severe endometrial structural and functional defects leading to infertility. Specifically, conditional loss of
MeSH term(s)	Female ; Autophagy/physiology ; Animals ; Endometrium/metabolism ; Pregnancy ; Stem Cells/metabolism ; Stem Cells/cytology ; Mice ; Apoptosis ; Beclin-1/metabolism ; Uterus
Chemical Substances	Beclin-1
Language	English
Publishing date	2023-07-05
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2454135-7
ISSN	1554-8635 ; 1554-8627
ISSN (online)	1554-8635
ISSN	1554-8627
DOI	10.1080/15548627.2023.2231270
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Article ; Online: The Multifaceted Role of Autophagy in Endometrium Homeostasis and Disease.

Popli, Pooja / Sun, Ally J / Kommagani, Ramakrishna

Reproductive sciences (Thousand Oaks, Calif.)

2021 Volume 29, Issue 4, Page(s) 1054–1067

Abstract: Autophagy is a conserved fundamental cellular process with a primary function of catabolizing harmful or surplus cellular contents such as protein aggregates, dysfunctional/long-lived organelles, intracellular pathogens, and storage nutrients. An ... ...

Abstract	Autophagy is a conserved fundamental cellular process with a primary function of catabolizing harmful or surplus cellular contents such as protein aggregates, dysfunctional/long-lived organelles, intracellular pathogens, and storage nutrients. An increasing body of evidence reveals that basal autophagy is essential for maintaining endometrial homeostasis and mediating endometrial-specific functions, including menstrual cycle, embryo implantation, and decidualization. However, perturbed levels of autophagy can lead to severe endometrial pathologies, including endometriosis, endometrial hyperplasia, endometrial cancer, adenomyosis, and leiomyoma. This review highlights the most recent findings on the activity, regulation, and function of autophagy in endometrium physiology and pathology. Understanding the mechanistic roles of autophagy in endometrium homeostasis and disease is key to developing novel therapeutic strategies for endometrium-related infertility and malignancies.
MeSH term(s)	Adenomyosis/metabolism ; Autophagy ; Endometriosis/metabolism ; Endometrium/metabolism ; Female ; Homeostasis ; Humans ; Leiomyoma/metabolism
Language	English
Publishing date	2021-04-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2276411-2
ISSN	1933-7205 ; 1933-7191
ISSN (online)	1933-7205
ISSN	1933-7191
DOI	10.1007/s43032-021-00587-2
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Zs.A 4113: Show issues

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Article: SF3B1-dependent alternative splicing is critical for maintaining endometrial homeostasis and the establishment of pregnancy.

Popli, Pooja / Chadchan, Sangappa B / Dias, Michelle / Deng, Xinchao / Gunderson, Stephanie J / Jimenez, Patricia / Yalamanchili, Hari / Kommagani, Ramakrishna

bioRxiv : the preprint server for biology

2023

Abstract: The remarkable potential of human endometrium to undergo spontaneous remodeling is shaped by controlled spatiotemporal gene expression patterns. Although hormone-driven transcription shown to govern these patterns, the post-transcriptional processing of ... ...

Abstract	The remarkable potential of human endometrium to undergo spontaneous remodeling is shaped by controlled spatiotemporal gene expression patterns. Although hormone-driven transcription shown to govern these patterns, the post-transcriptional processing of these mRNA transcripts, including the mRNA splicing in the endometrium is not studied yet. Here, we report that the splicing factor, SF3B1 is central in driving alternative splicing (AS) events that are vital for physiological responses of the endometrium. We show that loss of SF3B1 splicing activity impairs stromal cell decidualization as well as embryo implantation. Transcriptomic analysis revealed that SF3B1 depletion decidualizing stromal cells led to differential mRNA splicing. Specifically, a significant upregulation in mutually exclusive AS events (MXEs) with SF3B1 loss resulted in the generation of aberrant transcripts. Further, we found that some of these candidate genes phenocopy SF3B1 function in decidualization. Importantly, we identify progesterone as a potential upstream regulator of SF3B1-mediated functions in endometrium possibly via maintaining its persistently high levels, in coordination with deubiquitinating enzymes. Collectively, our data suggest that SF3B1-driven alternative splicing plays a critical role in mediating the endometrial-specific transcriptional paradigms. Thus, the identification of novel mRNA variants associated with successful pregnancy establishment may help to develop new strategies to diagnose or prevent early pregnancy loss.
Language	English
Publishing date	2023-05-20
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.05.20.541590
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Article: The autophagy protein, ATG14 safeguards against unscheduled pyroptosis activation to enable embryo transport during early pregnancy.

Popli, Pooja / Oestreich, Arin K / Maurya, Vineet K / Rowen, Marina N / Masand, Ramya / Holtzman, Michael J / Zhang, Yong / Lydon, John / Akira, Shizuo / Moley, Kelle H / Kommagani, Ramakrishna

bioRxiv : the preprint server for biology

2024

Abstract: Recurrent pregnancy loss (RPL), characterized by two or more failed clinical pregnancies, poses a significant challenge to reproductive health. In addition to embryo quality and endometrial function, proper oviduct function is also essential for ... ...

Abstract	Recurrent pregnancy loss (RPL), characterized by two or more failed clinical pregnancies, poses a significant challenge to reproductive health. In addition to embryo quality and endometrial function, proper oviduct function is also essential for successful pregnancy establishment. Therefore, structural abnormalities or inflammation resulting from infection in the oviduct may impede the transport of embryos to the endometrium, thereby increasing the risk of miscarriage. However, the precise cellular mechanisms that maintain the structural and functional integrity of the oviduct are not studied yet. Here, we report that autophagy is critical for maintaining the oviduct homeostasis and keeping the inflammation under check to enable embryo transport. Specifically, the loss of the autophagy-related gene,
Language	English
Publishing date	2024-03-20
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.19.585812
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Article: The SARS-CoV-2 receptor, Angiotensin converting enzyme 2 (ACE2) is required for human endometrial stromal cell decidualization.

Chadchan, Sangappa B / Maurya, Vineet K / Popli, Pooja / Kommagani, Ramakrishna

bioRxiv : the preprint server for biology

2020

Abstract: Study question: Is SARS-CoV-2 receptor, angiotensin-converting enzyme 2 (ACE 2) expressed in the human endometrium during the menstrual cycle, and does it participate in endometrial decidualization?: Summary answer: ACE2 protein is highly expressed ... ...

Abstract	Study question: Is SARS-CoV-2 receptor, angiotensin-converting enzyme 2 (ACE 2) expressed in the human endometrium during the menstrual cycle, and does it participate in endometrial decidualization? Summary answer: ACE2 protein is highly expressed in human endometrial stromal cells during the secretory phase and is essential for human endometrial stromal cell decidualization. What is known already: ACE2 is expressed in numerous human tissues including the lungs, heart, intestine, kidneys and placenta. ACE2 is also the receptor by which SARS-CoV-2 enters human cells. Study design size duration: Proliferative (n = 9) and secretory (n = 6) phase endometrium biopsies from healthy reproductive-age women and primary human endometrial stromal cells from proliferative phase endometrium were used in the study. Participants/materials setting methods: ACE2 expression and localization were examined by qRT-PCR, Western blot, and immunofluorescence in both human endometrial samples and mouse uterine tissue. The effect of Main results and the role of chance: In human tissue, ACE2 protein is expressed in both endometrial epithelial and stromal cells in the proliferative phase of the menstrual cycle, and expression increases in stromal cells in the secretory phase. The Large scale data: N/A. Limitations reasons for caution: Experiments assessing the function of ACE2 in human endometrial stromal cell decidualization were Wider implications of the findings: Expression of ACE2 in the endometrium allow SARS-CoV-2 to enter endometrial epithelial and stromal cells, which could impair Study fundings/competing interests: This study was supported by National Institutes of Health / National Institute of Child Health and Human Development grants R01HD065435 and R00HD080742 to RK and Washington University School of Medicine start-up funds to RK. The authors declare that they have no conflicts of interest.
Keywords	covid19
Language	English
Publishing date	2020-06-24
Publishing country	United States
Document type	Preprint
DOI	10.1101/2020.06.23.168252
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Article ; Online: The SARS-CoV-2 receptor, angiotensin-converting enzyme 2, is required for human endometrial stromal cell decidualization†.

Chadchan, Sangappa B / Popli, Pooja / Maurya, Vineet K / Kommagani, Ramakrishna

Biology of reproduction

2020 Volume 104, Issue 2, Page(s) 336–343

Abstract: The coronavirus disease 2019 (COVID-19) first appeared in December 2019 and rapidly spread throughout the world. The SARS-CoV-2 virus enters the host cells by binding to the angiotensin-converting enzyme 2 (ACE2). Although much of the focus is on ... ...

Abstract	The coronavirus disease 2019 (COVID-19) first appeared in December 2019 and rapidly spread throughout the world. The SARS-CoV-2 virus enters the host cells by binding to the angiotensin-converting enzyme 2 (ACE2). Although much of the focus is on respiratory symptoms, recent reports suggest that SARS-CoV-2 can cause pregnancy complications such as pre-term birth and miscarriages; and women with COVID-19 have had maternal vascular malperfusion and decidual arteriopathy in their placentas. Here, we report that the ACE2 protein is expressed in both endometrial epithelial and stromal cells in the proliferative phase of the menstrual cycle, and the expression increases in stromal cells in the secretory phase. It was observed that the ACE2 mRNA and protein abundance increased during primary human endometrial stromal cell (HESC) decidualization. Furthermore, HESCs transfected with ACE2-targeting siRNA impaired the full decidualization response, as evidenced by a lack of morphology change and lower expression of the decidualization markers PRL and IGFBP1. Additionally, in mice during pregnancy, the ACE2 protein was expressed in the uterine epithelial cells, and stromal cells increased through day 6 of pregnancy. Finally, progesterone induced Ace2 mRNA expression in mouse uteri more than vehicle or estrogen. These data establish a role for ACE2 in endometrial physiology, suggesting that SARS-CoV-2 may be able to enter endometrial stromal cells and elicit pathological manifestations in women with COVID-19, including an increased risk of early pregnancy loss.
MeSH term(s)	Angiotensin-Converting Enzyme 2/genetics ; Angiotensin-Converting Enzyme 2/metabolism ; Animals ; COVID-19/complications ; COVID-19/virology ; Cells, Cultured ; Endometrium/cytology ; Endometrium/physiology ; Female ; Gene Expression Regulation, Enzymologic/physiology ; Gene Knockdown Techniques ; Humans ; Insulin-Like Growth Factor Binding Protein 1/genetics ; Insulin-Like Growth Factor Binding Protein 1/metabolism ; Mice ; Pregnancy ; Prolactin/genetics ; Prolactin/metabolism ; RNA Interference ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; SARS-CoV-2/physiology ; Serine Endopeptidases/genetics ; Serine Endopeptidases/metabolism ; Stromal Cells/physiology
Chemical Substances	IGFBP1 protein, human ; Insulin-Like Growth Factor Binding Protein 1 ; RNA, Messenger ; Prolactin (9002-62-4) ; Ace2 protein, mouse (EC 3.4.17.23) ; Angiotensin-Converting Enzyme 2 (EC 3.4.17.23) ; Serine Endopeptidases (EC 3.4.21.-) ; TMPRSS2 protein, human (EC 3.4.21.-)
Keywords	covid19
Language	English
Publishing date	2020-06-23
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	10.1093/biolre/ioaa211
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Zs.A 551: Show issues

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Article ; Online: Peroxiredoxin 6 Plays Essential Role in Mediating Fertilization and Early Embryonic Development in Rabbit Oviduct.

Popli, Pooja / Shukla, Vinay / Kaushal, Jyoti B / Kumar, Rohit / Gupta, Kanchan / Dwivedi, Anila

Reproductive sciences (Thousand Oaks, Calif.)

2021 Volume 29, Issue 5, Page(s) 1560–1576

Abstract: The oviduct is a site for early reproductive events including gamete maturation, fertilization, and early embryo development. Secretory cells lining the oviduct lumen synthesize and secrete proteins that interact with gametes and developing embryos. ... ...

Abstract	The oviduct is a site for early reproductive events including gamete maturation, fertilization, and early embryo development. Secretory cells lining the oviduct lumen synthesize and secrete proteins that interact with gametes and developing embryos. Although previous studies have identified some of the secretory proteins in the oviduct, however, knowledge and their precise specific functions in the oviduct are poorly understood. In this study, by using proteomic approach, we identified a secretory protein, Peroxiredoxin 6 (PRDX6), and evaluated its role in mediating early pregnancy events, fertilization, and embryo development in rabbit oviduct. The expression of PRDX6 was significantly higher in ampulla and isthmus sections of the oviduct in mated animal groups compared to non-mated controls. Furthermore, significant reduction in number of embryos recovered from PRDX6 siRNA-transfected oviductal horn was observed compared to the control contralateral horn. Moreover, in animals receiving PRDX6 siRNA in their oviductal horn, the number of implanted blastocysts was significantly less in the uterus as observed on day 9 post-coital (p.c.). Further, during embryo-rabbit oviduct epithelial cell (ROEC) co-culture, siRNA-mediated PRDX6 silencing attenuated the early embryonic development. Mechanistically, increased levels of ROS and expression of oxidative stress- and inflammation-related proteins were found in PRDX6 siRNA-treated ROEC cells as compared to control cells, implicating that ablation of PRDX6 in the oviduct creates a stress-induced micro-environment detrimental to early embryonic development in oviduct. Taken together, our data suggest that PRDX6 maintains an optimal micro-environment conducive to successful embryo development and can be considered as a candidate to evaluate its therapeutic potential in IVF strategies.
MeSH term(s)	Animals ; Embryonic Development ; Fallopian Tubes ; Female ; Fertilization ; Oviducts/metabolism ; Peroxiredoxin VI/metabolism ; Pregnancy ; Proteins/metabolism ; Proteomics ; RNA, Small Interfering/metabolism ; Rabbits
Chemical Substances	Proteins ; RNA, Small Interfering ; Peroxiredoxin VI (EC 1.11.1.15)
Language	English
Publishing date	2021-08-23
Publishing country	United States
Document type	Journal Article
ZDB-ID	2276411-2
ISSN	1933-7205 ; 1933-7191
ISSN (online)	1933-7205
ISSN	1933-7191
DOI	10.1007/s43032-021-00689-x
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Zs.A 4113: Show issues

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Article: Gut microbiota and microbiota-derived metabolites promotes endometriosis.

Chadchan, Sangappa B / Naik, Sumanta K / Popli, Pooja / Talwar, Chandni / Putluri, Satwikreddy / Ambati, Chandrasekhar R / Lint, Michael A / Kau, Andrew L / Stallings, Christina L / Kommagani, Ramakrishna

Cell death discovery

2023 Volume 9, Issue 1, Page(s) 28

Abstract: Endometriosis is a pathological condition of the female reproductive tract characterized by the existence of endometrium-like tissue at ectopic sites, affecting 10% of women between the age 15 and 49 in the USA. However, currently there is no reliable ... ...

Abstract	Endometriosis is a pathological condition of the female reproductive tract characterized by the existence of endometrium-like tissue at ectopic sites, affecting 10% of women between the age 15 and 49 in the USA. However, currently there is no reliable non-invasive method to detect the presence of endometriosis without surgery and many women find hormonal therapy and surgery as ineffective in avoiding the recurrences. There is a lack of knowledge on the etiology and the factors that contribute to the development of endometriosis. A growing body of recent evidence suggests an association between gut microbiota and endometriosis pathophysiology. However, the direct impact of microbiota and microbiota-derived metabolites on the endometriosis disease progression is largely unknown. To understand the causal role of gut microbiota and endometriosis, we have implemented a novel model using antibiotic-induced microbiota-depleted (MD) mice to investigate the endometriosis disease progression. Interestingly, we found that MD mice showed reduced endometriotic lesion growth and, the transplantation of gut microbiota by oral gavage of feces from mice with endometriosis rescued the endometriotic lesion growth. Additionally, using germ-free donor mice, we indicated that the uterine microbiota is dispensable for endometriotic lesion growth in mice. Furthermore, we showed that gut microbiota modulates immune cell populations in the peritoneum of lesions-bearing mice. Finally, we found a novel signature of microbiota-derived metabolites that were significantly altered in feces of mice with endometriosis. Finally, we found one the altered metabolite, quinic acid promoted the survival of endometriotic epithelial cells in vitro and lesion growth in vivo, suggesting the disease-promoting potential of microbiota-derived metabolites. In summary, these data suggest that gut microbiota and microbiota-derived metabolome contribute to lesion growth in mice, possibly through immune cell adaptations. Of translational significance, these findings will aid in designing non-invasive diagnostics using stool metabolites for endometriosis.
Language	English
Publishing date	2023-01-25
Publishing country	United States
Document type	Journal Article
ISSN	2058-7716
ISSN	2058-7716
DOI	10.1038/s41420-023-01309-0
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Article ; Online: Beclin-1-dependent autophagy, but not apoptosis, is critical for stem-cell-mediated endometrial programming and the establishment of pregnancy.

Popli, Pooja / Tang, Suni / Chadchan, Sangappa B / Talwar, Chandni / Rucker, Edmund B / Guan, Xiaoming / Monsivais, Diana / Lydon, John P / Stallings, Christina L / Moley, Kelle H / Kommagani, Ramakrishna

Developmental cell

2023 Volume 58, Issue 10, Page(s) 885–897.e4

Abstract: The human endometrium shows a remarkable regenerative capacity that enables cyclical regeneration and remodeling throughout a woman's reproductive life. Although early postnatal uterine developmental cues direct this regeneration, the vital factors that ... ...

Abstract	The human endometrium shows a remarkable regenerative capacity that enables cyclical regeneration and remodeling throughout a woman's reproductive life. Although early postnatal uterine developmental cues direct this regeneration, the vital factors that govern early endometrial programming are largely unknown. We report that Beclin-1, an essential autophagy-associated protein, plays an integral role in uterine morphogenesis during the early postnatal period. We show that conditional depletion of Beclin-1 in the uterus triggers apoptosis and causes progressive loss of Lgr5
MeSH term(s)	Animals ; Female ; Humans ; Mice ; Pregnancy ; Autophagy ; Beclin-1 ; Endometrium ; Stem Cells ; Uterus
Chemical Substances	Beclin-1 ; BECN1 protein, human ; Becn1 protein, mouse
Language	English
Publishing date	2023-04-10
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2023.03.013
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Zs.A 5742: 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)
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Article ; Online: The SARS-CoV-2 receptor, Angiotensin converting enzyme 2 (ACE2) is required for human endometrial stromal cell decidualization

Chadchan, Sangappa B / Maurya, Vineet K / Popli, Pooja / Kommagani, Ramakrishna

bioRxiv

Abstract: STUDY QUESTION: Is SARS-CoV-2 receptor, angiotensin-converting enzyme 2 (ACE 2) expressed in the human endometrium during the menstrual cycle, and does it participate in endometrial decidualization? SUMMARY ANSWER: ACE2 protein is highly expressed in ... ...

Abstract	STUDY QUESTION: Is SARS-CoV-2 receptor, angiotensin-converting enzyme 2 (ACE 2) expressed in the human endometrium during the menstrual cycle, and does it participate in endometrial decidualization? SUMMARY ANSWER: ACE2 protein is highly expressed in human endometrial stromal cells during the secretory phase and is essential for human endometrial stromal cell decidualization. WHAT IS KNOWN ALREADY: ACE2 is expressed in numerous human tissues including the lungs, heart, intestine, kidneys and placenta. ACE2 is also the receptor by which SARS-CoV-2 enters human cells. STUDY DESIGN, SIZE, DURATION: Proliferative (n = 9) and secretory (n = 6) phase endometrium biopsies from healthy reproductive-age women and primary human endometrial stromal cells from proliferative phase endometrium were used in the study. PARTICIPANTS/MATERIALS, SETTING, METHODS: ACE2 expression and localization were examined by qRT-PCR, Western blot, and immunofluorescence in both human endometrial samples and mouse uterine tissue. The effect of ACE2 knockdown on morphological and molecular changes of human endometrial stromal cell decidualization were assessed. Ovariectomized mice were treated with estrogen or progesterone to determine the effects of these hormones on ACE2 expression. MAIN RESULTS AND THE ROLE OF CHANCE: In human tissue, ACE2 protein is expressed in both endometrial epithelial and stromal cells in the proliferative phase of the menstrual cycle, and expression increases in stromal cells in the secretory phase. The ACE2 mRNA (P ˂ 0.0001) and protein abundance increased during primary human endometrial stromal cell (HESC) decidualization. HESCs transfected with ACE2-targeting siRNA were less able to decidualize than controls, as evidenced by a lack of morphology change and lower expression of the decidualization markers PRL and IGFBP1 (P ˂ 0.05). In mice during pregnancy, ACE2 protein was expressed in uterine epithelial and stromal cells increased through day six of pregnancy. Finally, progesterone induced expression of Ace2 mRNA in mouse uteri more than vehicle or estrogen (P ˂ 0.05). LARGE SCALE DATA: N/A. LIMITATIONS, REASONS FOR CAUTION: Experiments assessing the function of ACE2 in human endometrial stromal cell decidualization were in vitro. Whether SARS-CoV-2 can enter human endometrial stromal cells and affect decidualization have not been assessed. WIDER IMPLICATIONS OF THE FINDINGS: Expression of ACE2 in the endometrium allow SARS-CoV-2 to enter endometrial epithelial and stromal cells, which could impair in vivo decidualization, embryo implantation, and placentation. If so, women with COVID-19 may be at increased risk of early pregnancy loss. STUDY FUNDINGS/COMPETING INTEREST(S): This study was supported by National Institutes of Health / National Institute of Child Health and Human Development grants R01HD065435 and R00HD080742 to RK and Washington University School of Medicine start-up funds to RK. The authors declare that they have no conflicts of interest.
Keywords	covid19
Language	English
Publishing date	2020-06-24
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2020.06.23.168252
Database	COVID19

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