Hypoxia inhibits invasion of extravillous trophoblast cells through reduction of matrix metalloproteinase (MMP)-2 activation in the early first trimester of human pregnancy

Onogi, Akira; Naruse, Katsuhiko; Sado, Toshiyuki; Tsunemi, Taihei; Shinmoto, Hiroshi; Noguchi, Taketoshi; Yumura, Yasushi; Akasaki, Masayoshi; Oi, Hidekazu; Kobayashi, Hiroshi

doi:10.1016/j.placenta.2011.06.023

Cited by 78 publications

(63 citation statements)

References 26 publications

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“…16,17 When employing these cells to study trophoblast migration it is crucial to assess purity of cell isolates, as cytotrophoblast isolation procedures are prone to contamination with low levels of fibroblasts that are highly motile and multiply rapidly in culture. 18 A number of researchers have reported that first trimester cytotrophoblasts exhibit invasive activity (indicative of EVT differentiation) following culture on Matrigel, [19][20][21] but the resulting cell population is frequently not well characterized, and the proportion of differentiated EVT progeny obtained is unclear. In contrast, cytotrophoblasts isolated from term placentae appear to demonstrate a greater propensity to syncytialize in culture and do not differentiate into an invasive EVT phenotype.…”

Section: Isolated Primary Trophoblastsmentioning

confidence: 99%

Quantifying trophoblast migration: In vitro approaches to address in vivo situations

James

Tun

Clark

2016

Cell Adhesion & Migration

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When trophoblasts migrate and invade in vivo, they do so by interacting with a range of other cell types, extracellular matrix proteins, chemotactic factors and physical forces such as fluid shear stress. These factors combine to influence overall trophoblast migration and invasion into the decidua, which in turn determines the success of spiral artery remodeling, and pregnancy itself. Our understanding of these important but complex processes is limited by the simplified conditions in which we often study cell migration in vitro, and many discrepancies are observed between different in vitro models in the literature. On top of these experimental considerations, the migration of individual trophoblasts can vary widely. While time-lapse microscopy provides a wealth of information on trophoblast migration, manual tracking of individual cell migration is a time consuming task that ultimately restricts the numbers of cells quantified, and thus the ability to extract meaningful information from the data. However, the development of automated imaging algorithms is likely to aid our ability to accurately interpret trophoblast migration in vitro, and better allow us to relate these observations to in vivo scenarios. This commentary discusses the advantages and disadvantages of techniques commonly used to quantify trophoblast migration and invasion, both from a cell biology and a mathematical perspective, and examines how such techniques could be improved to help us relate trophoblast migration more accurately to in vivo function in the future.

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Section: Isolated Primary Trophoblastsmentioning

confidence: 99%

Quantifying trophoblast migration: In vitro approaches to address in vivo situations

James

Tun

Clark

2016

Cell Adhesion & Migration

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“…Hypoxic conditions are the typical factor that regulates the invasion of trophoblast cells which migrate and invade the surrounding blood vessels of the endometrium in the maternal uterus in persisting hypoxic conditions. Hypoxia induces alteration of various genes including integrin, MMP and TIMP (Luo et al, 2011;Onogi et al, 2011;Na et al, 2012). It was found that the invasion ability of trophoblast is regulated by the expression of HIF-1α (Dubinsky et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Hypoxia-Inducible Factor 1Î± Expression in Chorionic Tissue and Decidua of Women with Spontaneous Abortion at the First Trimester of Pregnancy

Машкина¹,

Коваленко²,

Butenko³

2014

American Journal of Biochemistry and Biotechnology

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Oxygen-regulated genes expression has important role in preimplantation embryonic metabolism regulation. Hypoxia Inducible Factor (HIF) regulated by hypoxia oxygen tension is crucial for placenta development. But the data about its role in spontaneous abortion is very poor. Thus, we aimed to determine an expression level of HIF-1α in chorionic tissue and decidua at pregnancy. Samples of chorionic tissue and decidua were taken after surgical termination of normally progressing pregnancies in 5-9 week of gestation (n = 8) and spontaneous abortion in 5-9 week of gestation (n = 9). HIF-1α expression was analyzed using semiquantitative reverse transcription-polymerase chain reaction. Compared with decidual tissue, the expression of HIF-1α was increased in chorionic tissue in condition of normally progressing pregnancy. HIF-1α expression in samples of both tissues is equal in spontaneous abortion. In same time the expression of HIF-1α was decreased (1,5 fold) in chorionic tissue for spontaneous abortion compared with control group. The results demonstrated that low HIF-1α expression level in chorionic tissue can be associated with spontaneous abortion in first trimester of pregnancy.

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“…Trophoblast cells were isolated from placental tissue using our previously published method [18][19][20] with some modifications. In brief, placental chorionic villi were washed in Hank's balanced salt solution (HBSS; SigmaAldrich Co., St. Louis, MO), and villous material was dissected, minced, and digested for 35 min at 37°C in 0.25% trypsin (Invitrogen Co., Carlsbad, CA) and 0.5 mg DNase I (Sigma-Aldrich Co.) twice without stirring and a third time with agitation.…”

Section: Trophoblast Isolationmentioning

confidence: 99%

“…27) In hypoxic conditions, MMP-2 activity has been found to decrease in invasive trophoblast cells from early human pregnancy, 20) even though MMP-2 and other proteases are regarded as target molecules of hypoxia-induced factor (HIF) in placental development. 28) Although gelatinase activity was not measured in the current study, reduced activity of the MMP-2/TIMP-2 pathway under hypoxic stress may Values are expressed relative to the concentrati ons of normal culture (mean ± SEM).…”

Section: )mentioning

confidence: 99%

“…38) The appropriate oxygen tension to mimic healthy or preeclamptic placenta remains controversial. We regard 5% oxygen as the "normal" condition for trophoblasts in the first trimester, 20) but used 20% oxygen in this study because the oxygen concentration might be higher in term placenta, and it may change dramatically with complications in pregnancy and during the course of labor. We cannot exclude the possibility that our culture conditions subjected trophoblasts to hyperoxidative stress, since cell injury shown by the LDH assay decreased with hypoxic stimulation.…”

Section: )mentioning

confidence: 99%

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Cytokines, proteases, and ligands of receptor for advanced glycation endproducts (RAGE) released by primary trophoblasts from human term placenta under hypoxic stimulation

Naruse

Tsunemi

Onogi

et al. 2013

Hypertens Res Pregnancy

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Aim:In the placenta, hypoxia followed by reoxygenation (ischemia and reperfusion) is regarded as a trigger for the pathological onset of preeclampsia. In this study, we isolated primary trophoblasts from human term placenta, exposed them to hypoxic stress, and measured subsequent levels of cytokines, proteases, protease inhibitors, and ligands of receptor for advanced glycation endproducts (RAGE) to identify the trigger molecule released from hypoxic placenta into maternal circulation. Methods: Ten placental samples were taken from healthy elective caesarean section patients. Trophoblasts were isolated using a Percoll-based method and cultured under 20% oxygen with or without 3 rounds of 0.1% hypoxic stimulation for 1 h. Results: Cell viability did not differ between normal and hypoxic cultures (MTT assay), but cell injury was attenuated in hypoxic culture (LDH assay). In cell culture supernatants, concentrations of MMP-2, TIMP-2, IL-6, and IL-10 decreased in hypoxia compared to normal culture, while the RAGE ligand HMGB1 increased significantly in hypoxic culture. There were no significant differences in concentrations of MMP-9, TIMP-1, IL-8, or S100A12. Conclusions: These results suggest that human term placenta under hypoxia and reperfusion releases the RAGE ligand HMGB1, a "danger signal", that can trigger systemic inflammation and lead to preeclampsia or placenta-based complications in pregnancy.

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Hypoxia inhibits invasion of extravillous trophoblast cells through reduction of matrix metalloproteinase (MMP)-2 activation in the early first trimester of human pregnancy

Cited by 78 publications

References 26 publications

Quantifying trophoblast migration: In vitro approaches to address in vivo situations

Quantifying trophoblast migration: In vitro approaches to address in vivo situations

Hypoxia-Inducible Factor 1Î± Expression in Chorionic Tissue and Decidua of Women with Spontaneous Abortion at the First Trimester of Pregnancy

Cytokines, proteases, and ligands of receptor for advanced glycation endproducts (RAGE) released by primary trophoblasts from human term placenta under hypoxic stimulation

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