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Magnetic Resonance Imaging Reveals Distinct Roles for Tissue Transglutaminase and Factor XIII in Maternal Angiogenesis During Early Mouse Pregnancy.

ABSTRACT: OBJECTIVE:The early embryo implantation is characterized by enhanced uterine vascular permeability at the site of blastocyst attachment, followed by extracellular-matrix remodeling and angiogenesis. Two TG (transglutaminase) isoenzymes, TG2 (tissue TG) and FXIII (factor XIII), catalyze covalent cross-linking of the extracellular-matrix. However, their specific role during embryo implantation is not fully understood. Approach and Results: For mapping the distribution as well as the enzymatic activities of TG2 and FXIII towards blood-borne and resident extracellular-matrix substrates, we synthetized selective and specific low molecular weight substrate analogs for each of the isoenzymes. The implantation sites were challenged by genetically modifying the trophoblast cells in the outer layer of blastocysts, to either overexpress or deplete TG2 or FXIII, and the angiogenic response was studied by dynamic contrast-enhanced-magnetic resonance imaging. Dynamic contrast-enhanced-magnetic resonance imaging revealed a decrease in the permeability of decidual vasculature surrounding embryos in which FXIII were overexpressed in trophoblast cell. Reduction in decidual blood volume fraction was demonstrated when either FXIII or TG2 were overexpressed in embryonic trophoblast cell and was elevated when trophoblast cell was depleted of FXIII. These results were corroborated by histological analysis. CONCLUSIONS:In this study, we report on the isoenzyme-specific roles of TG2 and FXIII during the early days of mouse pregnancy and further reveal their involvement in decidual angiogenesis. Our results reveal an important magnetic resonance imaging-detectable function of embryo-derived TG2 and FXIII on regulating maternal angiogenesis during embryo implantation in mice.Visual Overview: An online visual overview is available for this article.

SUBMITTER: Cohen G

PROVIDER: S-EPMC6656598 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Magnetic Resonance Imaging Reveals Distinct Roles for Tissue Transglutaminase and Factor XIII in Maternal Angiogenesis During Early Mouse Pregnancy.

Cohen Gadi G Hadas Ron R Stefania Rachele R Pagoto Amerigo A Ben-Dor Shifra S Kohen Fortune F Longo Dario D Elbaz Michal M Dekel Nave N Gershon Eran E Aime Silvio S Neeman Michal M

Arteriosclerosis, thrombosis, and vascular biology 20190613 8

<h4>Objective</h4>The early embryo implantation is characterized by enhanced uterine vascular permeability at the site of blastocyst attachment, followed by extracellular-matrix remodeling and angiogenesis. Two TG (transglutaminase) isoenzymes, TG2 (tissue TG) and FXIII (factor XIII), catalyze covalent cross-linking of the extracellular-matrix. However, their specific role during embryo implantation is not fully understood. Approach and Results: For mapping the distribution as well as the enzyma ...[more]

PMID: 31189431

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Project description:For acute adnexal torsion of pregnant women, appropriate treatment based on an accurate diagnosis is especially important for fertility preservation and timely treatment. The 2017 American College of Obstetricians and Gynecologists (ACOG) Committee Opinion No. 723 announced its practice-changing guidelines to ensure that diagnostic magnetic resonance imaging (MRI) conducted during the first trimester and gadolinium exposure at any time during pregnancy are safe for fetal stability. Unfortunately, few studies have been performed to evaluate the usefulness of the diagnostic accuracy of MRI for acute adnexal torsion during pregnancy. We sought to determine the efficacy of diagnostic MRI modality using multiparameter for maternal adnexal torsion during pregnancy. From 1 January 2007 to 31 January 2019, 131 pregnant with MRI tests were reviewed. In this retrospective cohort study, 94 women were excluded due to conditions other than an adnexal mass, and 37 were identified through MRI analyses conducted before surgery for suspected adnexal torsion. The primary outcome was the diagnostic accuracy of sonography and MRI, and the secondary outcome was the usefulness of Apparent diffusion coefficient (ADC) values for predicting the severity of hemorrhagic infarction between the medulla and cortex of the torsed ovarian parenchyma. Our study demonstrates that in the diagnosis of adnexal torsion during pregnancy, the sensitivity, specificity, positive predictive value, and negative predictive value are 62.5%, 83.3%, 90.9%, and 45.5% for sonography and 100%, 77.8%, 90.5%, and 100% for MRI. MRI results in surgical-proven adnexal torsion patients revealed unilocular ovarian cysts (36.8% (7/19)), multilocular ovarian cysts (31.6% (6/19)), and near normal-appearing ovaries (31.6% (6/19)). Pathology in adnexal torsion revealed a corpus luteal ovarian cyst (63.2% (12/19)) and underlying adnexal pathology (46.8% (7/19)). Maternal adnexal torsion during pregnancy was more likely to occur in corpus luteal ovarian cysts than in underlying adnexal masses (odds ratio, 2.14; 95% confidence interval (CI), 0.428-10.738). MRI features for adnexal torsion were as follows: tubal wall thickness, 100% (19/19); ovarian stromal (medullary) edema, 100% (19/19); symmetrical or asymmetrical ovarian cystic wall, 100%(19/19); prominent follicles in the ovarian parenchyma periphery, 57.9% (11/19); periadenxal fat stranding, 84.2% (16/19); uterine deviation to the twisted side, 21.1% (4/19); and peritoneal fluid, 42.1% (8/19). The signal intensity of the ADC values of the ovarian medulla and cortex were compared between the cystectomy and detorsion (CD) and salpingo-oophorectomy (SO) groups. The ADC values of the CD and SO groups were 1.81 ± 0.09 × 10-3 mm2/s and 1.91 ± 0.18 × 10-3 mm2/s, respectively (P = 0.209), in the ovarian medulla and 1.37 ± 0.32 × 10-3 mm2/s and 0.96 ± 0.36 × 10-3 mm2/s, respectively (P = 0.022), in the ovarian cortex. The optimal cut-off value of ADC values for predictable total necrosis in the torsed ovarian cortex was ≤ 1.31 × 10-3 mm2/s (area under the curve (AUC) = 0.81; 95% CI 0.611-1.0; P = 0.028). Our data showed that maternal adnexal torsion during pregnancy occurred in most corpus luteal cystic ovary cases and some normal-appearing ovary during the 1st and 2nd trimesters of gestation. Therefore, this study is the first study to elaborate on the existence or usefulness of the diagnostic MRI for acute maternal adnexal torsion during pregnancy and to provide a predictive diagnosis of the severity of hemorrhagic infarction for deciding surgical radicality.

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Dataset Information

Magnetic Resonance Imaging Reveals Distinct Roles for Tissue Transglutaminase and Factor XIII in Maternal Angiogenesis During Early Mouse Pregnancy.

Publications

Magnetic Resonance Imaging Reveals Distinct Roles for Tissue Transglutaminase and Factor XIII in Maternal Angiogenesis During Early Mouse Pregnancy.

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