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Novel pathways of inflammation in human fetal membranes associated with preterm birth and preterm pre-labor rupture of the membranes

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Abstract

Spontaneous preterm birth (PTB) and preterm pre-labor rupture of the membranes (pPROM) are major pregnancy complications. Although PTB and pPROM have common etiologies, they arise from distinct pathophysiologic pathways. Inflammation is a common underlying mechanism in both conditions. Balanced inflammation is required for fetoplacental growth; however, overwhelming inflammation (physiologic at term and pathologic at preterm) can lead to term and preterm parturition. A lack of effective strategies to control inflammation and reduce the risk of PTB and pPROM suggests that there are several modes of the generation of inflammation which may be dependent on the type of uterine tissue. The avascular fetal membrane (amniochorion), which provides structure, support, and protection to the intrauterine cavity, is one of the key contributors of inflammation. Localized membrane inflammation helps tissue remodeling during pregnancy. Two unique mechanisms that generate balanced inflammation are the progressive development of senescence (aging) and cyclic cellular transitions: epithelial to mesenchymal (EMT) and mesenchymal to epithelial (MET). The intrauterine build-up of oxidative stress at term or in response to risk factors (preterm) can accelerate senescence and promote a terminal state of EMT, resulting in the accumulation of inflammation. Inflammation degrades the matrix and destabilizes membrane function. Inflammatory mediators from damaged membranes are propagated via extracellular vesicles (EV) to maternal uterine tissues and transition quiescent maternal uterine tissues into an active state of labor. Membrane inflammation and its propagation are fetal signals that may promote parturition. This review summarizes the mechanisms of fetal membrane cellular senescence, transitions, and the generation of inflammation that contributes to term and preterm parturitions.

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Funding

This study is funded by NIH/NIAD (1R21AI140249-01A1) and NIH/NICHD (5 R03 HD098469 02 and 1R01HD084532-01A1) to R Menon

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Authors and Affiliations

  1. Division of Maternal-Fetal Medicine and Perinatal Research Department of Obstetrics & Gynecology, Division of Maternal-Fetal Medicine & Perinatal Research, The University of Texas Medical Branch at Galveston, MRB 11.138, 301 301 University Blvd, Galveston, TX, 77555-1062, USA

    Ramkumar Menon & Lauren S. Richardson

  2. Department of Obstetrics, Gynecology, and Reproductive Sciences, McGovern Medical School at the University of Texas Health Science Center at Houston, UT Health, Houston, Texas, USA

    Faranak Behnia

  3. Universidade Federal da Fronteira Sul, Campus Passo Fundo, Rua Capitão Araujo, 20, Centro, Passo Fundo, Rio Grande do Sul, Brazil

    Jossimara Polettini

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  1. Ramkumar Menon
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  3. Jossimara Polettini
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  4. Lauren S. Richardson
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This article is a contribution to the special issue on Preterm birth: Pathogenesis and clinical consequences revisited – Guest Editors: Anke Diemert and Petra Arck

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Menon, R., Behnia, F., Polettini, J. et al. Novel pathways of inflammation in human fetal membranes associated with preterm birth and preterm pre-labor rupture of the membranes. Semin Immunopathol 42, 431–450 (2020). https://doi.org/10.1007/s00281-020-00808-x

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