Molecular regulation of vascular smooth muscle cell phenotype switching by trophoblast cells at the maternal-fetal interface

Nandy, Debdyuti; Das, Shreya; Islam, Safirul; Ain, Rupasri

doi:10.1016/j.placenta.2020.02.017

Cited by 11 publications

(24 citation statements)

References 56 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…It was quite intriguing that PRNP formed a ter-molecular complex with PDGFRβ-FAK. VSMC de-differentiation is primarily directed by the invading interstitial trophoblast cells (Ain et al, 2003;Nandy et al, 2020) and trophendothelial cells (Paul et al, 2022). Trophoblast cellinduced de-differentiation leads to phenotypic switching in VSMCs that involve suppression of contractile markers expression and elevation of synthetic state markers (Nandy et al, 2020) Previous studies demonstrated that trophoblast cells isolated from first trimester human placenta expressed membrane-associated TRAIL and induced apoptosis of human aortic VSMC (Keogh et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

Cellular Prion protein moonlights vascular smooth muscle cell fate: Surveilled by trophoblast cells

Bose,

Jana,

Ain

2023

Journal Cellular Physiology

Self Cite

View full text Add to dashboard Cite

Uterine spiral artery remodeling (uSAR) is a hallmark of hemochorial placentation. Compromised uSAR leads to adverse pregnancy outcomes. Salient developmental events involved in uSAR are active areas of research and include (a) trophendothelial cell invasion into the spiral arteries, selected demise of endothelial cells; (b) de‐differentiation of vascular smooth muscle cells (VSMC); and (c) migration and/or death of VSMCs surrounding spiral arteries. Here we demonstrated that cellular prion (PRNP) is expressed in the rat metrial gland, the entry point of spiral arteries with the highest expression on E16.5, the day at which trophoblast invasion peaks. PRNP is expressed in VSMCs that drift away from the arterial wall. RNA interference of Prnp functionally restricted migration and invasion of rat VSMCs. Furthermore, PRNP interacted with two migration‐promoting factors, focal adhesion kinase (FAK) and platelet‐derived growth factor receptor‐β (PDGFR‐β), forming a ter‐molecular complex in both the metrial gland and A7r5 cells. The presence of multiple putative binding site of odd skipped related‐1 (OSR1) transcription factor on the Prnp promoter was observed using in silico promoter analysis. Ectopic overexpression of OSR1 increased, and knockdown of OSR1 decreased expression of PRNP in VSMCs. Coculture of VSMCs with rat primary trophoblast cells decreased the levels of OSR1 and PRNP. Interestingly, PRNP knockdown led to apoptotic death in ~9% of VSMCs and activated extrinsic apoptotic pathways. PRNP interacts with TRAIL‐receptor DR4 and protects VSMCs from TRAIL‐mediated apoptosis. These results highlight the biological functions of PRNP in VSMC cell‐fate determination during uteroplacental development, an important determinant of healthy pregnancy outcome.

show abstract

Section: Discussionmentioning

confidence: 99%

Cellular Prion protein moonlights vascular smooth muscle cell fate: Surveilled by trophoblast cells

Bose,

Jana,

Ain

2023

Journal Cellular Physiology

Self Cite

View full text Add to dashboard Cite

show abstract

“…Acquisition of endothelial character by the trophoblast cells during placental development is considered as a remarkable process of spiral artery remodeling, which is associated with erosion/de-differentiation of the smooth muscle cells lining the maternal arteries to regulate their vascular tone ( Whitley & Cartwright, 2010 ; Rai & Cross, 2014 ; Nandy et al, 2020 ). These trophoblast cells are specialized subtypes of TGCs and are classified based on their developmental origin and function, and they have the potential to undergo morphogenesis to form vascular tubes ( Simmons & Cross, 2005 ; Simmons et al, 2007 ; Knöfler et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

“…It has been proposed that the “trophoblastic vascular colonization” is an effective mechanism for removing maternal vasomotor control and thus dramatically augmenting the delivery of maternal resources to the placenta ( Pijnenborg et al, 1981 ). This hallmark developmental event in effect creates flaccid, low-resistance blood vessels, known as spiral artery remodeling ( Nandy et al, 2020 ), and is fundamental for optimal delivery of nutrients to the fetus.…”

Section: Introductionmentioning

confidence: 99%

Trans-differentiation of trophoblast stem cells: implications in placental biology

et al. 2022

Self Cite

View full text Add to dashboard Cite

Trophoblast invasion is a hallmark of hemochorial placentation. Invasive trophoblast cells replace the endothelial cells of uterine spiral arteries. The mechanism by which the invasive trophoblast cells acquire this phenotype is unknown. Here, we demonstrate that, during differentiation, a small population of trophoblast stem (TS) cells trans-differentiate into a hybrid cell type expressing markers of both trophoblast (TC) and endothelial (EC) cells. In addition, a compendium of EC-specific genes was found to be associated with TS cell differentiation. Using functional annotation, these genes were categorized into angiogenesis, cell adhesion molecules, and apoptosis-related genes. HES1 repressed transcription of EC genes in TS cells. Interestingly, differentiated TCs secrete TRAIL, but its receptor DR4 is expressed only in ECs and not in TCs. TRAIL induced apoptosis in EC but not in TC. Co-culture of ECs with TC induced apoptosis in ECs via extrinsic apoptotic pathway. These results highlight that (a) TS cells possess the potential to trans-differentiate into “trophendothelial” phenotype, regulated by HES1 and (b) trophoblast differentiation-induced TRAIL secretion directs preferential demise of ECs located in their vicinity.

show abstract

“…They shift to a synthetic phenotype, migrate from the vessel wall, and undergo apoptosis. Trophoblasts secrete platelet derived growth factor BB (PDGF-BB) to bind the PDGF receptor β (PDGFR-β) of VSMCs to activate the PDGF signaling pathway and induce de-differentiation of VSMCs ( 21 ). EVT secretes tumor necrosis factor α (TNF-α), tumor necrosis factor-related apoptosis-inducing ligand (TRAIL), and Fas ligand to induce apoptosis of VSMCs ( 22 ) ( Figure 1A ).…”

Section: Trophoblasts and Uterine Sa Remodelingmentioning

confidence: 99%

Hyperglycemia disturbs trophoblast functions and subsequently leads to failure of uterine spiral artery remodeling

Zhu

Liu

et al. 2023

Front. Endocrinol.

View full text Add to dashboard Cite

Uterine spiral artery remodeling is necessary for fetal growth and development as well as pregnancy outcomes. During remodeling, trophoblasts invade the arteries, replace the endothelium and disrupt the vascular smooth muscle, and are strictly regulated by the local microenvironment. Elevated glucose levels at the fetal-maternal interface are associated with disorganized placental villi and poor placental blood flow. Hyperglycemia disturbs trophoblast proliferation and invasion via inhibiting the epithelial-mesenchymal transition, altering the protein expression of related proteases (MMP9, MMP2, and uPA) and angiogenic factors (VEGF, PIGF). Besides, hyperglycemia influences the cellular crosstalk between immune cells, trophoblast, and vascular cells, leading to the failure of spiral artery remodeling. This review provides insight into molecular mechanisms and signaling pathways of hyperglycemia that influence trophoblast functions and uterine spiral artery remodeling.

show abstract

Molecular regulation of vascular smooth muscle cell phenotype switching by trophoblast cells at the maternal-fetal interface

Cited by 11 publications

References 56 publications

Cellular Prion protein moonlights vascular smooth muscle cell fate: Surveilled by trophoblast cells

Cellular Prion protein moonlights vascular smooth muscle cell fate: Surveilled by trophoblast cells

Trans-differentiation of trophoblast stem cells: implications in placental biology

Hyperglycemia disturbs trophoblast functions and subsequently leads to failure of uterine spiral artery remodeling

Contact Info

Product

Resources

About