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Fusion of Cytothrophoblast with Syncytiotrophoblast in the Human Placenta: Factors Involved in Syncytialization Gauster M, Huppertz B J

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Fusion of Cytothrophoblast with Syncytiotrophoblast in the Human Placenta: Factors Involved in Syncytialization Gauster M, Huppertz B J Journal für Reproduktionsmedizin und Endokrinologie – Journal of Reproductive Medicine and Endocrinology – Andrologie • Embryologie & Biologie • Endokrinologie • Ethik & Recht • Genetik Gynäkologie • Kontrazeption • Psychosomatik • Reproduktionsmedizin • Urologie Fusion of Cytothrophoblast with Syncytiotrophoblast in the Human Placenta: Factors Involved in Syncytialization Gauster M, Huppertz B J. Reproduktionsmed. Endokrinol 2008; 5 (2), 76-82 www.kup.at/repromedizin Online-Datenbank mit Autoren- und Stichwortsuche Offizielles Organ: AGRBM, BRZ, DVR, DGA, DGGEF, DGRM, D·I·R, EFA, OEGRM, SRBM/DGE Indexed in EMBASE/Excerpta Medica/Scopus Krause & Pachernegg GmbH, Verlag für Medizin und Wirtschaft, A-3003 Gablitz FERRING-Symposium digitaler DVR 2021 Mission possible – personalisierte Medizin in der Reproduktionsmedizin Was kann die personalisierte Kinderwunschbehandlung in der Praxis leisten? Freuen Sie sich auf eine spannende Diskussion auf Basis aktueller Studiendaten. SAVE THE DATE 02.10.2021 Programm 12.30 – 13.20Uhr Chair: Prof. Dr. med. univ. Georg Griesinger, M.Sc. 12:30 Begrüßung Prof. Dr. med. univ. Georg Griesinger, M.Sc. & Dr. Thomas Leiers 12:35 Sind Sie bereit für die nächste Generation rFSH? Im Gespräch Prof. Dr. med. univ. Georg Griesinger, Dr. med. David S. Sauer, Dr. med. Annette Bachmann 13:05 Die smarte Erfolgsformel: Value Based Healthcare Bianca Koens 13:15 Verleihung Frederik Paulsen Preis 2021 Wir freuen uns auf Sie! Fusion of Cytotrophoblast with Syncytiotrophoblast in the Human Placenta: Factors Involved in Syncytialization M. Gauster, B. Huppertz Human placental villi are covered by a characteristic epithelial-like layer. It consists of mononucleated cytotrophoblasts and an overlying syncytiotrophoblast layer both in contact to the trophoblastic basement membrane. The syncytiotrophoblast mostly lacks DNA replication and seems to transcribe only barely mRNA. Therefore, the syncytiotrophoblast depends on cell compounds delivered by fusing cytotrophoblasts. Delivery of fresh cytoplasmic contents into the syncytiotrophoblast is achieved by continuous fusion with cytotrophoblasts throughout gesta- tion. Fusion between cytotrophoblasts and the syncytiotrophoblast is driven by multiple factors, including environmental growth factors and cytokines, which turn on a specific cascade of fusogenic proteins in cytotrophoblasts destined for fusion. The cascade includes protein kinases and transcription factors, as well as induced expression of fusion-promoting proteins associated with the cell membrane. Additionally, specific proteases are activated, which cleave and remodel structural proteins to prepare the cell for fusion. However, not only fusogenic proteins, but also plasma membrane architecture and physicochemical factors such as calcium and oxygen affect intertrophoblastic fusion. Coordinated action of all factors involved is crucial for proper cytotrophoblast – syncytiotrophoblast fusion. Deregulation of a single factor might cause an inadequate fusion rate and could lead to pregnancy complications such as preeclampsia or even spontaneous abortion. J Reproduktionsmed Endokrinol 2008; 5 (2): 76–82. Key words: cytotrophoblast, syncytiotrophoblast, syncytialization, intertrophoblastic fusion Intercellular Fusion Human Trophoblast trophoblast derived nuclei and other in the Human organelles, proteins and RNA as well Arising from the trophoblast of the as cytoplasm and membranes are In human, the phenomenon of cell- blastocyst, two trophoblast popula- transferred into the syncytiotropho- cell fusion occurs in several different tions differentiate early during gesta- blast. cell types. During fertilization, after tion. Extravillous trophoblasts leave penetration of the zona pellucida the basal membrane of anchoring Experiments using 3H-thymidine in- and entry of the sperm into the egg’s villi and invade the tissues of the ma- corporation revealed that DNA syn- perivitelline space, fusion of the egg ternal decidua basalis to attach the thesis does not occur in syncytio- and sperm cell membranes takes placenta to the uterus and to re- trophoblast, implying that syncytial place [1]. Macrophages can differen- model maternal spiral arteries. nuclei are unable to replicate [3]. In tiate and fuse to form multinucleated addition, 3H-uridine incorporation chondroclasts and osteoclasts [2], The second population is the villous experiments showed that the syncy- which are important for cartilage and cytotrophoblast, which upon specific tiotrophoblast is mostly lacking RNA bone development and remodelling. stimulation differentiate and fuse synthesis [4]. Taking in consideration Macrophages are also able to fuse with the covering syncytiotropho- that the syncytiotrophoblast does not into giant cells important in immune blast. The multinucleated syncytio- replicate and shows only little tran- defense. During embryonic develop- trophoblast in concert with the un- scriptional activity, the mechanism ment of skeletal muscle, mononu- derlying mononucleated cytotropho- of fusion with cytotrophoblasts be- cleated myoblasts fuse to form multi- blasts are located on a basement comes highly important. The integ- nucleated myotubes. Even in the membrane and constitute the villous rity of the syncytiotrophoblast de- adult skeletal muscle satellite cells trophoblast, the epithelial-like layer pends on continuous fusion and de- fuse with skeletal muscle fibers. In of the placental villous tree. Some of livery of cytotrophoblast derived cy- the human placenta, villous tropho- the cytotrophoblasts are trophoblast toplasmic contents throughout preg- blasts fuse to generate the character- progenitor cells and divide in an nancy. istic multinucleated syncytial layer, asymmetric way. While one daughter the syncytiotrophoblast. Extravillous cell retains its progenitor character, At the same time acquisition of fresh trophoblasts differentiate and fuse to the other is destined for differentia- cellular material requires deposition generate the trophoblastic giant cells tion. The final differentiation stage of of aged cytosolic content to keep characteristic for the decidua basalis a cytotrophoblast is fusion with the the biological balance of the syncy- during pregnancy. syncytiotrophoblast. This way, cyto- tium. Apoptotic material is packed in Received: February 6, 2008; accepted after revision: May 14, 2008. From the Institute of Cell Biology, Histology and Embryology, Center of Molecular Medicine, Medical University of Graz Correspondence: Martin Gauster, PhD, Institute of Cell Biology, Histology and Embryology, Center of Molecular Medicine, Medical University of Graz, A-8010 Graz, Harrachgasse 21/VII, Austria; e-mail: [email protected] 76 J. REPRODUKTIONSMED. ENDOKRINOL. 2/2008 For personal use only. Not to be reproduced without permission of Krause & Pachernegg GmbH. tor (GM-CSF) have also been demon- strated to trigger syncytialization and hCG synthesis [7]. Moreover, trans- forming growth factor (TGF)-α and leukemia-inhibitory factor (LIF) have been suggested to promote syn- cytialization and production of hCG [8]. Interestingly, hCG itself, pro- duced by the syncytiotrophoblast can act as inducer of cytotrophoblast differentiation [8, 9]. In contrast, transforming growth factor (TGF)-β inhibits syncytial formation as well as secretion of hCG and hPL [10]. Also tumor necrosis factor (TNF)-α impairs syncytium formation of pri- Figure 1. Schematic representation of trophoblast differentiation within the villous trophoblast. mary term trophoblasts in vitro and Derived from trophoblast progenitor cells daughter cells start to differentiate and finally fuse represses hCG synthesis by down- with the overlying syncytiotrophoblast. Nuclei that have become an integrative part of the syn- regulation of β-hCG subunit expres- cytiotrophoblast change their morphology and display chromatin condensation. Finally late apoptotic syncytial nuclei are packed into syncytial knots and are released into the maternal sion [11]. blood stream. The arrows follow the route of cell types and nuclear changes during trophoblast differentiation. When environmental factors bind to their receptors on target tropho- membrane sealed vesicles – the so staining these cells with membrane blasts, mitogen-activated protein called syncytial knots – and is re- associated proteins such as desmo- kinases (MAPKs) may be activated leased from the apical cytoplasmic plakin or E-cadherin (Fig. 2). which in turn regulate complex pro- membrane of the syncytiotropho- grams of cell differentiation. Two blast into the maternal circulation. classical MAPKs, the extracellular Hence, the turnover of villous tro- Regulation of Trophoblast signal-regulated kinase1/2 (ERK1/2) phoblast in a placental villus is simi- Differentiation and p38, are implicated to play sig- lar to the turnover in stratified epithe- nificant roles in initiation of tropho- lia and includes proliferation, differ- Since cytotrophoblasts can either ac- blast differentiation and fusion. Stud- entiation, fusion and controlled re- quire the extravillous (invasive path- ies employing specific ERK1/2 and/ lease of apoptotic material (Fig. 1). way) or the villous (syncytial path- or p38 inhibitors to primary tropho- way) phenotype, it is apparent that blast cultures revealed impaired To study the fusion process between differentiation has to be strictly regu- differentiation and syncytialization trophoblasts in greater detail in vitro lated. Factors that are involved in [12]. the BeWo cell model has attracted a governing
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