- Characteristic Changes in Decidual Gene Expression Signature in Spontaneous Term Parturition
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Haidy El-Azzamy, Andrea Balogh, Roberto Romero, Yi Xu, Christopher LaJeunesse, Olesya Plazyo, Zhonghui Xu, Theodore G. Price, Zhong Dong, Adi L. Tarca, Zoltan Papp, Sonia S. Hassan, Tinnakorn Chaiworapongsa, Chong Jai Kim, Nardhy Gomez-Lopez, Nandor Gabor Than
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J Pathol Transl Med. 2017;51(3):264-283. Published online February 22, 2017
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DOI: https://doi.org/10.4132/jptm.2016.12.20
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 Abstract
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- Background
The decidua has been implicated in the “terminal pathway” of human term parturition, which is characterized by the activation of pro-inflammatory pathways in gestational tissues. However, the transcriptomic changes in the decidua leading to terminal pathway activation have not been systematically explored. This study aimed to compare the decidual expression of developmental signaling and inflammation-related genes before and after spontaneous term labor in order to reveal their involvement in this process.
Methods
Chorioamniotic membranes were obtained from normal pregnant women who delivered at term with spontaneous labor (TIL, n = 14) or without labor (TNL, n = 15). Decidual cells were isolated from snap-frozen chorioamniotic membranes with laser microdissection. The expression of 46 genes involved in decidual development, sex steroid and prostaglandin signaling, as well as pro- and anti-inflammatory pathways, was analyzed using high-throughput quantitative real-time polymerase chain reaction (qRT-PCR). Chorioamniotic membrane sections were immunostained and then semi-quantified for five proteins, and immunoassays for three chemokines were performed on maternal plasma samples.
Results
The genes with the highest expression in the decidua at term gestation included insulin-like growth factor-binding protein 1 (IGFBP1), galectin-1 (LGALS1), and progestogen-associated endometrial protein (PAEP); the expression of estrogen receptor 1 (ESR1), homeobox A11 (HOXA11), interleukin 1β (IL1B), IL8, progesterone receptor membrane component 2 (PGRMC2), and prostaglandin E synthase (PTGES) was higher in TIL than in TNL cases; the expression of chemokine C-C motif ligand 2 (CCL2), CCL5, LGALS1, LGALS3, and PAEP was lower in TIL than in TNL cases; immunostaining confirmed qRT-PCR data for IL-8, CCL2, galectin-1, galectin-3, and PAEP; and no correlations between the decidual gene expression and the maternal plasma protein concentrations of CCL2, CCL5, and IL-8 were found.
Conclusions
Our data suggests that with the initiation of parturition, the decidual expression of anti-inflammatory mediators decreases, while the expression of pro-inflammatory mediators and steroid receptors increases. This shift may affect downstream signaling pathways that can lead to parturition.
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Citations
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American Journal of Reproductive Immunology.2024;[Epub] CrossRef - Is human labor at term an inflammatory condition?
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Fetal Diagnosis and Therapy.2023; 50(4): 236. CrossRef - Galectins-1, -3 and -9 Are Present in Breast Milk and Have a Role in Early Life Development
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Nutrients.2022; 14(20): 4338. CrossRef - The Expression of IL-1β Correlates with the Expression of Galectin-3 in the Tissue at the Maternal–Fetal Interface during the Term and Preterm Labor
Nikola Jovic, Marija Milovanovic, Jovana Joksimovic Jovic, Marija Bicanin Ilic, Dejana Rakic, Vladimir Milenkovic, Bojana Stojanovic, Jelena Milovanovic, Aleksandar Arsenijevic, Nebojsa Arsenijevic, Mirjana Varjacic
Journal of Clinical Medicine.2022; 11(21): 6521. CrossRef - Galectin-1 and Galectin-9 Concentration in Maternal Serum: Implications in Pregnancies Complicated with Preterm Prelabor Rupture of Membranes
Dorota Grażyna Boroń, Aleksy Świetlicki, Michał Potograbski, Grażyna Kurzawińska, Przemysław Wirstlein, Daniel Boroń, Krzysztof Drews, Agnieszka Seremak-Mrozikiewicz
Journal of Clinical Medicine.2022; 11(21): 6330. CrossRef - Placental galectins regulate innate and adaptive immune responses in pregnancy
Orsolya Oravecz, Roberto Romero, Eszter Tóth, Judit Kapitány, Máté Posta, Dahiana M. Gallo, Simona W. Rossi, Adi L. Tarca, Offer Erez, Zoltán Papp, János Matkó, Nándor Gábor Than, Andrea Balogh
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Frontiers in Immunology.2021;[Epub] CrossRef - Inflammatory Amplification: A Central Tenet of Uterine Transition for Labor
Kelycia B. Leimert, Wendy Xu, Magdalena M. Princ, Sylvain Chemtob, David M. Olson
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Seminars in Immunopathology.2020; 42(4): 397. CrossRef - Role of galectin-glycan circuits in reproduction: from healthy pregnancy to preterm birth (PTB)
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Seminars in Immunopathology.2020; 42(4): 469. CrossRef - Functional changes in decidual mesenchymal stem/stromal cells are associated with spontaneous onset of labour
Joan C Wijaya, Ramin Khanabdali, Harry M Georgiou, Maria I Kokkinos, Patrick F James, Shaun P Brennecke, Bill Kalionis
Molecular Human Reproduction.2020; 26(8): 636. CrossRef - Ageing in human parturition: impetus of the gestation clock in the decidua†
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Biology of Reproduction.2020; 103(4): 695. CrossRef - Cytotrophoblast extracellular vesicles enhance decidual cell secretion of immune modulators via TNF-alpha
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Immunobiology.2019; 224(1): 177. CrossRef - Transcriptomic analysis of fetal membranes reveals pathways involved in preterm birth
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BMC Medical Genomics.2019;[Epub] CrossRef - Placental Galectins Are Key Players in Regulating the Maternal Adaptive Immune Response
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