IL-1 signaling mediates intrauterine inflammation and chorio-decidua neutrophil recruitment and activation

Presicce, Pietro; Park, Chan Wook; Senthamaraikannan, Paranthaman; Bhattacharyya, Somnath; Jackson, Courtney M.; Kong, Fanrong; Rueda, Cesar M.; DeFranco, Emily; Miller, Lisa; Hildeman, David; Salomonis, Nathan; Chougnet, Claire; Jobe, Alan H.; Kallapur, Suhas G.

doi:10.1172/jci.insight.98306

Cited by 80 publications

(144 citation statements)

References 93 publications

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“…Data in the non-human primate demonstrate that infectious agents confined to the choriodecidua induce preterm labor at a much lower frequency compared to infection in the amniotic fluid (81)(82)(83). Our data demonstrate that macromolecules such as cytokines (IL1ra) do not efficiently cross the amniotic epithelial barrier but readily cross the placenta from the mother to the fetus (84). Thus, the evaluation of compartment-specific mechanisms of inflammation is important.…”

Section: Vaginal Microbiomementioning

confidence: 81%

“…Neutrophils infiltrating the choriodecidua are largely of maternal origin (147,148), while neutrophils in the amniotic fluid are largely of fetal origin (149), although a recent study reported mixed fetal/maternal origin of neutrophils in the amniotic fluid (150). During normal pregnancy, there are small numbers of neutrophils, but the numbers increase dramatically during IUI presumably due to secretion of neutrophilic chemotactic factors such as IL-8 by the amnion (84,108). CD15 + neutrophils represent the most abundant leukocyte population in AF from women with intraamniotic infection/inflammation (151).…”

Section: Neutrophilsmentioning

confidence: 99%

“…During IUI, the choriodecidual neutrophils predominantly produce TNFα, IL-8, and MIP-1β/CCL4 (114,116). Although blood neutrophils have a short life-span, neutrophils in the decidua have greatly increased survival, mediated in part by up-regulating anti-apoptotic mediators including Bcl-2 family members (e.g., Bcl2A1, called Bfl-1 in humans) (84,152). Neutrophils can amplify the inflammatory response and neutralize microorganisms by releasing neutrophil extracellular traps (NETs), producing antimicrobial enzymes such as defensins, neutrophil elastase, and myeloperoxidase (MPO), and releasing reactive oxygen species (ROS) (153)(154)(155).…”

Section: Neutrophilsmentioning

confidence: 99%

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Immunobiology of Acute Chorioamnionitis

2020

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Acute chorioamnionitis is characterized by neutrophilic infiltration and inflammation at the maternal fetal interface. It is a relatively common complication of pregnancy and can have devastating consequences including preterm labor, maternal infections, fetal infection/inflammation, fetal lung, brain, and gastrointestinal tract injury. In this review, we will discuss current understanding of the pathogenesis, immunobiology, and mechanisms of this condition. Most commonly, acute chorioamnionitis is a result of ascending infection with relatively low-virulence organisms such as the Ureaplasma species. Furthermore, recent vaginal microbiome studies suggest that there is a link between vaginal dysbiosis, vaginal inflammation, and ascending infection. Although less common, microorganisms invading the maternal-fetal interface via hematogenous route (e.g., Zika virus, Cytomegalovirus, and Listeria) can cause placental villitis and severe fetal inflammation and injury. We will provide an overview of the knowledge gleaned from different animal models of acute chorioamnionitis and the role of different immune cells in different maternal-fetal compartments. Lastly, we will discuss how infectious agents can break the maternal tolerance of fetal allograft during pregnancy and highlight the novel future therapeutic approaches.

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Section: Vaginal Microbiomementioning

confidence: 81%

Section: Neutrophilsmentioning

confidence: 99%

Section: Neutrophilsmentioning

confidence: 99%

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Immunobiology of Acute Chorioamnionitis

2020

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“…All these genes may be in one way or another related to PTB: CCRL2 and CXCL2 belong to inflammatory pathways [55,56], GPR84 is a receptor of fatty acids also related to inflammation [57]. BCL2A1 and CHI3L1 were recently associated with chorioamnionitis in monkey and human [58], SLC16A10 is up-regulated in the mid-gestational placenta [59] and SAMSN1 is a poorly characterized gene that may be involved in differentiation of lymphocytes B [60]. The fact that these subsets of genes overlap in both studies using different experimental techniques stresses that they should be a target of further research of PTB.…”

Section: Discussionmentioning

confidence: 99%

Transcriptomic analysis of fetal membranes reveals pathways involved in preterm birth

Pereyra

Bertoni

Sosa

et al. 2018

Preprint

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15 16 Short title: Transcriptomic analysis of severe preterm birth 17 Key words: RNA-seq, preterm birth, gestational age, biomarkers 18 2 19Abstract 20 Preterm birth (PTB), defined as infant delivery before 37 weeks of completed gestation, results of 21 the interaction of both genetic and environmental components and constitutes a complex 22 multifactorial syndrome. Transcriptome analysis of PTB has proved challenging because of the 23 multiple causes of PTB and the numerous maternal and fetal gestational tissues that must interact 24 to facilitate parturition. A common pathway of labor and PTB may be the activation of fetal 25 membranes. In this work, chorioamnion membranes from severe preterm and term fetus were 26 analyzed using RNA sequencing. A total of 270 genes were differentially expressed (DE): 252 27 were up-regulated and 18 were down-regulated in the severe preterm compared to the term births. 28 We found great gene expression homogeneity in the control samples, and not in severe preterm 29 samples. In this work, we identified up-regulated pathways that were previously suggested as 30 leading to PTB like immunological and inflammatory paths. New pathways that were not 31 identified in preterm like the hemopoietic path appeared up-regulated in preterm membranes. A 32 group of 18 down-regulated genes discriminates between term and severe preterm cases. These 33 genes potentially characterize a severe preterm transcriptome pattern and therefore are candidate 34 genes for understanding the syndrome. Some of the down-regulated genes are involved in the 35 nervous system, morphogenesis (WNT-1, DLX5, PAPPA2) and ion channel complexes (KCNJ16, 36 KCNB1), making them good candidates as biomarkers of PTB.37 The identification of this DE gene pattern may help to develop a multi-gene disease classifier.38 These markers were generated in an admixtured South American population where PTB has a high 39 incidence. Since genetic background may impact differentially in different populations it is 40 mandatory to include populations like South American and African ones that are usually excluded 3 41 from high throughput approaches. These classifiers should be compared to those in other 42 populations to get a global landscape of PTB. 43 44 Introduction 45 Preterm birth (PTB), defined as the delivery of an infant before 37 weeks of completed gestation, 46 is a worldwide health problem and remains the leading cause of global perinatal morbidity and 47 mortality [1][2][3]. PTB is a complex, multifactorial syndrome comprised of multiple clinical 48 subtypes that can be defined as either 'spontaneous' or 'medically indicated' [4,5]. 70 % of PTB 49 cases are idiopathic; 5 % are due to the spontaneous onset of labor (sPTB) and the remaining 25 50 % are consequence of the preterm premature rupture of membranes (PPROM) [5,6]. PTB has also 51 been stratified according to gestational age (GA); neonates born between 24 and 33 weeks (severe 52 PTB) are at higher risk of death, and diseases later in life, than moderate PTB (GA betwee...

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“…Resident immune cells were followed by live imaging. Notably, neutrophils are normally scarce in the maternal-fetal membranes in the absence of infection (47). Phagocytic cells were present at the surface as soon as 15 min pi.…”

Section: Discussionmentioning

confidence: 99%

Streptococcus pyogenes infects human endometrium by limiting its immune response

Weckel¹,

Guilbert²,

Lambert³

et al. 2019

Preprint

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Group A Streptococcus (GAS), a Gram-positive human-specific pathogen yields 517,000 deaths annually worldwide, including 163,000 due to invasive infections and among them puerperal fever. GAS is their most feared etiologic agent. Puerperal fever still accounts for more than 75,000 maternal deaths annually and before the introduction of efficient prophylactic measures 10% childbirths were followed by the mother's death. Yet little is known regarding GAS invasive infection establishment or GAS efficiency in causing postpartum infection. To characterize its early steps, we set up coordinated analyses of ex vivo infection of the human decidua, the puerperal fever portal of entry. We analyzed GAS behavior and the immune response triggered. We demonstrate that GAS (i) benefits from tissue secreted products to multiply; (ii) invades the tissue and leads to the death of half the cells within two hours via SpeB protease and Streptolysin O activities, respectively; (iii) impairs the tissue immune response. Immune impairment occurs both at the RNA level, with the induction of only a restricted immediate innate immune response, and at the protein level, in a SLO-and SpeB-dependent manner. Our study indicates that GAS efficient decidua invasion and immune response restraint favor its propensity to develop rapid invasive infections in a gynecological-obstetrical context.

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IL-1 signaling mediates intrauterine inflammation and chorio-decidua neutrophil recruitment and activation

Cited by 80 publications

References 93 publications

Immunobiology of Acute Chorioamnionitis

Immunobiology of Acute Chorioamnionitis

Transcriptomic analysis of fetal membranes reveals pathways involved in preterm birth

Streptococcus pyogenes infects human endometrium by limiting its immune response

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