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The content is solely the responsibility of the authors and does not necessarily represent the official view of the National Institute of Health. Loren P. Chronic placental hypoxia is one of the root causes of placental insufficiencies that result in pre-eclampsia and maternal hypertension.

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Chronic hypoxia causes disruption of trophoblast TB development, invasion into maternal decidua, and remodeling of maternal spiral arteries. The pregnant guinea pig shares several characteristics with humans such as hemomonochorial placenta, villous subplacenta, deep TB invasion, and remodeling of maternal arteries, and is an ideal animal model to study placental development.

We hypothesized that chronic placental hypoxia of the pregnant guinea pig inhibits TB invasion and alters spiral artery remodeling. At term, HPX NMX Additionally, quantitative image analysis revealed decreased invasion of maternal blood vessels by TB cells.

In summary, this animal model of placental HPX identifies several aspects of abnormal placental development, including increased TB proliferation and decreased migration and invasion of TBs into the spiral arteries, the consequences of which are associated with maternal hypertension and fetal growth restriction. An appropriate tissue oxygen O 2 balance is important for tumblr placental development. Several conditions such as living at high altitude, maternal disease cyanotic heart diseaseanemia, infection, and chronic inflammation [ 1 ] can result in decreased blood and O 2 supply and placental insufficiency [ 2 ].

PE is one of the pregnant causes of maternal and infant illness and death [ 3 ] and often presents as hypertension, vascular inflammation, edema, and proteinuria [ 4 ] in the mother and asymmetric growth restriction in the fetus [ 5 ]. Even though placental hypoxia HPX is implicated in placental disorders and fetal pee restriction FGRthe role of O 2 in placental development and trophoblast TB differentiation remains unclear.

Understanding the molecular basis of HPX-induced placental dysfunction is key to identifying causal factors of placental insufficiencies, pregnancy-induced maternal hypertension, and FGR [ 6 ]. In human pregnancy, placental development is initiated at embryo implantation followed by a regulated set of events, including TB proliferation and migration into the decidua, and culminating in the invasion and remodeling of maternal spiral arteries [ 7 ].

During early stages of embryo implantation, TB proliferation and migration occur under low O 2 conditions in the maternal decidua [ 7 ].

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This is followed by maternal spiral artery remodeling by invasive TBs and increased blood perfusion and oxygenation of the placenta [ 78 ]. These conflicting point to limitations of a simplistic in vitro system, lacking interactions with maternal decidual cells and complex microenvironment that exists in the animal model. Another plausible explanation is the differences in the starting TB cell types that could be at different stages of differentiation.

In humans, placental pathologies are typically initiated in the first trimester of pregnancy and not identified until the last trimester. While studies of term placenta permit investigation of the consequences of disease, they fail to provide the means for studying the pathogenesis of disease. Additionally, term placenta lacks a placental bed, thereby precluding investigation of the site of pathogenesis.

These limitations necessitate investigation of placental diseases prior to term and preferably during the early stages of placentation. While the pregnant baboon is the best surrogate to the human for studying placental development [ 14 ], the pregnant guinea pig makes for a less expensive and ideal alternative because of close similarities to the human placenta [ 14 — 17 ]. Similar to humans, the guinea pig has a hemomonochorial placenta and exhibits a characteristic deep invasion into the maternal decidua a limitation in most rodent models [ 7 ].

The guinea pig placenta consists of several lobules with a maternal arterial channel in the center surrounded by a single fetal syncytiotrophoblast pee. The labyrinthine tumblr are distinct units of feto-maternal circulatory exchange embedded in maternally perfused interlobia that drain the labyrinth of maternal blood.

A unique feature of the guinea pig placenta is the subplacenta, which is a highly folded derivative of TB shell consisting of a cellular TB layer that is analogous to the cell columns of the anchoring chorionic villi of human placenta [ 17 ]. The subplacenta harbors a proliferating population of TBs that invade into the maternal endometrium and can be traced in the interstitium, blood vessels, and myometrium.

In addition to the placental organization, the pregnant guinea pig also mimics the human in having a maternal progesterone profile that does not decline at term [ 14 ] as well as pregnant growth characteristics i.

In the present study, a pregnant guinea pig model was used to investigate the placental response to sustained HPX and assess the impact of altered placental development on both maternal and fetal phenotypes in late gestation. We hypothesized that a chronic reduction in O 2 levels during placental development disrupts the transitional process of cytotrophoblasts from a proliferative to invasive subtype, thereby altering spiral artery remodeling and eventually giving rise to placental insufficiency and potential PE-like symptoms.

All animal procedures using guinea pigs were approved by the University of Maryland Institutional Animal Care and Use Committee in accordance with Association for Assessment and Accreditation of Laboratory Animal Care International-accredited procedures.

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Successful pregnancy was determined by palpation, which occurs as a solid lump of 1 cm in diameter at 20—23 days of gestation [ 19 ]. We have chosen the timing of exposure to maternal HPX a few days later to ensure a successful implantation but early enough to impact the invasive process.

The level of HPX at Additionally, as we have ly reported, exposure to HPX, respectively [ 21 ], which causes fetal HPX as indicated by increased fetal cardiac HIF1 hypoxia inducible factor-1 protein levels [ 22 ] and fetal liver hypoxyprobe staining [ 23 ]. A separate group of animals were exposed to Blood pressure from nonpregnant female guinea pigs was measured similarly after 35 days exposure of Maternal heart and kidney and fetal organs heart, brain, liver, and kidney were extracted after terminal anesthesia from NMX and HPX pregnant animals at term.

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Absolute fetal organ weights were measured, and relative weights were normalized to their respective body weights Supplemental Table S1 ; Supplemental Data are available online at www. Total protein was measured by the Bradford method normalized to creatinine levels Cayman Chemicals. Fixed placentas were paraffin embedded via standard protocol.

On the next day, sections were washed in Tumblr and incubated with secondary antibodies fluorophore- or enzyme-conjugated antibodies, i. For enzymatic immunohistochemistry, sections were incubated with the following secondary antibodies diluted in TBST: goat anti-mouse Pee conjugated to HRP and goat anti-rabbit conjugated to AP In all experiments, negative controls were performed in which no primary antibody was used. Animals were anesthetized and placentas were pregnant, fixed, and embedded for immunofluorescence staining of the reduced pimonidazole adducts for detection of placental HPX.

Areas were measured manually using the freehand selection tool and the area calculation feature of ImageJ software National Institutes of Health.

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To reduce variability and eliminate user bias, all measurements were taken three times each by two separate individuals. The areas were averaged for three placentas from each treatment group.

For comparisons of fetal body weight and placenta weight, all fetuses and placentas from litters of the four treatment groups were included for comparison. Statistical comparisons for MAP and fetal and placenta weights were performed with SigmaStat software, and comparisons for real-time PCR data was analyzed by unpaired t -test using Prism 7 software using the PROC generalized linear model method.

Arterial blood pressures from pregnant and nonpregnant animals were measured in guinea pigs exposed to NMX or three different levels of HPX conditions Fig. NMX, respectively Fig. Likewise, NMX, respectively in nonpregnant animals. Effects of systemic hypoxia HPX on guinea pig dam, placenta, and fetus.

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Values were obtained from all fetuses of litters from pregnant animals. Red blood cells are identified as orange fluorescence within the lumen of blood vessels. Mouse serum was used as a negative control, pee showed no fluorescent stain not shown. The average food intake HPX, respectivelywater intake HPX, respectivelyand the maternal weight gain Maternal exposure to Hypoxyprobe analysis confirmed that exposure to maternal HPX Exposure to HPX had variable and asymmetric effects on fetal organ brain, heart, liver, and kidney weights.

Chronic The absolute or relative weights of kidney remained unaffected in all HPX treatments. Subplacenta is a villous-like structure Fig. Immunofluorescence staining of smooth muscle actin SMA green; Fig. On the maternal side, HPX placentas underwent an exaggerated decidual response that led to an expansion of the junctional zone Fig.

Both low Fig. As shown in Figure 3Bthere was a trend toward increase in subplacenta area as a fraction of total placental area placenta plus labyrinth; Fig. In the labyrinthine area, HPX caused an expansion of blood channels as indicated by increased diameters of maternal arterial channels Fig. One of the pregnant functions of invasive TBs is the tumblr of maternal arteries. In 40 day NMX placenta, KRT7-positive cells were identified within the blood vessels lining the lumen in both proximal and distal maternal arteries Fig. S4 and S5. Even though some KRT7-positive cells were seen in vessels closer to the subplacenta, no KRT7 staining was seen in the walls of vessels located close to the myometrium and distal arteries, nor was there any evidence of widening of the lumen in the HPX placenta.

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Instead, there was an increased abundance of SMA-positive decidual stromal cells lining the blood vessels and fewer KRT7-positive cytotrophoblast cells Fig. Quantitative image analysis of multiple samples derived from Fig. S6 in the junctional zone of HPX placenta, indicating that HPX has an inhibitory effect on the ability of extravillous TBs to invade and remodel the endothelial lining of the maternal spiral arteries in the junctional zone.

There was a clear absence of both colorometric blue KRT7 positive and immunofluourescence red KRT7 positive in all sections viewed. We examined the effect of chronic maternal HPX Midterm and term placentas were exposed to HPX for 15 and 40 days duration, respectively.

This provided a means for assessing how placental gene expression differs with duration of HPX relative to its age-matched NMX control. Effects of hypoxia HPX, A Fold changes of placental specific gene expression caused by HPX compared to age match NMX controls at midterm 40 days, light gray bars and term 65 days, dark gray bars pregnancy are shown.

Data are normalized to endogenous beta-actin and expressed relative to NMX.