Trophoblast

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Introduction

(Greek, trophe = "nutrition" and -blast, a primordial cell) During early development the trophoblast cells have an important contribution to extraembryonic tissues (fetal placenta and membranes) and processes of early development (adplantation, implantation and endocrine support of pregnancy).

Human embryo day 5.jpg Mouse blastocyst trophoblast 01.jpg
Human Blastocyst (day 5), trophoblast cells form the peripheral flattened epithelial layer of cells directly under the zona pellucida.[1] Mouse blastocyst labelled with trophoblast marker.[2]

In humans, week 1 blastocyst formation the outer layer of cells (adjacent to the zona pellucida) form a flat squamous epithelial layer of cells, the trophoblast layer. Week 2 following blastocyst hatching the trophoblast layer is involved with initial adhesion to the uterine wall and subsequent implantation within the wall. During this period the trophoblast layer proliferates and differentiates into two distinct layers (syncitiotrophoblast and cytotrophoblast).


Following implantation, trophoblast cells continue to contribute to the placenta. Prenatal diagnosis by invasive chorionic villus sampling and [[ non-invasive cervical cell sampling[3] uses mainly DNA from these cells.


Historical - Who named the trophoblast cell?  
From an 1905 paper on tubal implantation - "Hubrecht in 1889 published a monograph on the placentation of the hedgehog, showing that the developing ovum in this animal, after sequestration in a crypt, becomes imbedded in the sub-epithelial portion of the mucoa of the uterus by the action of the non-foetal ectodermal cells of the blastocyst. These cells Hubrecht named trophoblast because of their nutritive function, for by their agency the blastocyst “burrows” into the maternal tissues, both destroying and absorbing them."


Links: Blastocyst | Implantation | Week 2 | Week 3 | Placenta Development | Prenatal Diagnosis | Trophoblast - Protein Expression | Ectopic Implantation Research
Placenta Links: Introduction | Lecture - Placenta | Lecture Movie | Practical - Placenta | Implantation | Villi Development | Trophoblast | Maternal Decidua | Endocrine | Cord | Membranes | Abnormalities | Stage 13 | Stage 22 | Histology | Vascular Beds | Blood Vessel Development | Stem Cells | 2013 Meeting Presentation | Placenta Terms | Category:Placenta
Historic Embryology - Placenta 
1883 Embryonic Membranes | 1907 Development Atlas | 1909 | 1910 Textbook | 1917 Textbook | 1921 Textbook | 1921 Foetal Membranes |1921 human | 1921 Pig implantation | 1923 Placenta Review | 1939 umbilical cord | 1943 human and monkey | 1944 chorionic villus and decidua parietalis | 1946 placenta ageing | 1960 monkey | 1972 Placental circulation | Historic Disclaimer
Extravillous trophoblasts week 5.5
Extravillous trophoblasts (week 5.5)[4]

Some Recent Findings

  • A comparative study of five physiological key parameters between four different human trophoblast-derived cell lines[5] "Here, we present a comparative study on the functional aspects of the choriocarcinoma cell lines BeWo, JAR and Jeg-3, as well as the first trimester trophoblast cell line ACH-3P as placental in vitro barrier models for endocrine and transport studies. Functional assays including tight junction immunostaining, sodium fluorescein retardation, trans epithelial resistance, glucose transport, hormone secretion as well as size-dependent polystyrene nanoparticle transport were performed using the four cell types to evaluate key functional parameters of each cell line to act a relevant in vitro placental barrier model."
  • Human extravillous trophoblasts penetrate decidual veins and lymphatics before remodeling spiral arteries during early pregnancy[4] "To study the invasion of maternal endometrium between (W) 5.5 - 12 weeks of gestation by EVTs, we combined fluorescence in situ hybridization, immunofluorescence and immunohistochemistry to determine the presence of (male) EVTs in the vasculature of the maternal decidua. We observed that interstitial mononuclear EVTs directly entered decidual veins and lymphatics from W5.5. This invasion of decidual veins and lymphatics occurred long before endovascular EVTs remodelled decidual spiral arteries."
  • The trophoblast plug during early pregnancy: a deeper insight[6] "During the first trimester of pregnancy, foetal endovascular trophoblasts invade into maternal spiral arteries, accumulate and form plugs in the lumen of the vessels. These plugs only allow blood plasma to seep through. Hence, during the first trimester of pregnancy, a first flow of fluids through the placental intervillous space is established, resulting in a physiological oxygen gradient between mother and foetus. The trophoblast plugs block spiral arteries until the beginning of the second trimester (11-14 weeks)."
  • MSX2 Induces Trophoblast Invasion in Human Placenta[7] "Normal implantation depends on appropriate trophoblast growth and invasion. Meanwhile, overexpression of MSX2 and treatment with the MSX2-specific siRNA resulted in decreased and increased E-cadherin expression, respectively, in JEG-3 cells. Lastly, the protein expression levels of MSX2 were significantly lower in human pre-eclamptic placental villi than in the matched control placentas. Collectively, our results suggest that MSX2 may induce human trophoblast cell invasion, and dysregulation of MSX2 expression may be associated with pre-eclampsia."
  • OVO-like 1 regulates progenitor cell fate in human trophoblast development[8] "Epithelial barrier integrity is dependent on progenitor cells that either divide to replenish themselves or differentiate into a specialized epithelium. This paradigm exists in human placenta, where cytotrophoblast cells either propagate or undergo a unique differentiation program: fusion into an overlying syncytiotrophoblast. Syncytiotrophoblast is the primary barrier regulating the exchange of nutrients and gases between maternal and fetal blood and is the principal site for synthesizing hormones vital for human pregnancy. How trophoblast cells regulate their differentiation into a syncytium is not well understood. In this study, we show that the transcription factor OVO-like 1 (OVOL1), a homolog of Drosophila ovo, regulates the transition from progenitor to differentiated trophoblast cells. OVOL1 is expressed in human placenta and was robustly induced following stimulation of trophoblast differentiation. Disruption of OVOL1 abrogated cytotrophoblast fusion and inhibited the expression of a broad set of genes required for trophoblast cell fusion and hormonogenesis. OVOL1 was required to suppress genes that maintain cytotrophoblast cells in a progenitor state, including MYC, ID1, TP63, and ASCL2, and bound specifically to regions upstream of each of these genes." OMIM - OVOL1
  • Establishment of Trophoblast Stem Cells under Defined Culture Conditions in Mice[9] "Here, we report that addition of FGF2, activin A, XAV939, and Y27632 are necessary and sufficient for derivation of TS cells from both of E3.5 blastocysts and E6.5 early postimplantation extraembryonic ectoderm. Moreover, the undifferentiated TS cell state can be stably maintained in chemically defined culture conditions. Cells derived in this manner expressed TS cell marker genes, including Eomes, Elf5, Cdx2, Klf5, Cdh1, Esrrb, Sox2, and Tcfap2c; differentiated into all trophoblast subtypes (trophoblast giant cells, spongiotrophoblast, and labyrinthine trophoblast) in vitro; and exclusively contributed to trophoblast lineages in chimeric animals. This delineation of minimal requirements for derivation and self-renewal provides a defined platform for precise description and dissection of the molecular state of TS cells."
More recent papers  
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Search term: Trophoblast

Tianying Pan, Guolin He, Meng Chen, Chenyi Bao, Yan Chen, Guangyu Liu, Mi Zhou, Shuying Li, Wenming Xu, Xinghui Liu Abnormal CYP11A1 gene expression induces excessive autophagy, contributing to the pathogenesis of preeclampsia. Oncotarget: 2017, 8(52);89824-89836 PubMed 29163791

Shang Li, Junyu Zhai, Jiansheng Liu, Yan Hong, Weixiu Zhao, Aimin Zhao, Kang Sun, Yanzhi Du, Zi-Jiang Chen BMAL1 facilitates trophoblast migration and invasion via SP1-DNMT1/DAB2IP pathway in recurrent spontaneous abortion. Oncotarget: 2017, 8(52);89451-89464 PubMed 29163762

V Mahajan, H S Banga, G Filia, M P Gupta, K Gupta Comparison of diagnostic tests for the detection of bovine brucellosis in the natural cases of abortion. Iran J Vet Res: 2017, 18(3);183-189 PubMed 29163647

Thy Ph Nguyen, Hannah Ej Yong, Tejasvy Chollangi, Shaun P Brennecke, Susan J Fisher, Euan M Wallace, Peter R Ebeling, Padma Murthi Altered downstream target gene expression of the placental Vitamin D receptor in human idiopathic fetal growth restriction. Cell Cycle: 2017;1-29 PubMed 29161966

Shuang Hou, Jie-Fu Chen, Min Song, Yazhen Zhu, Yu Jen Jan, Szu Hao Chen, Tzu-Hua Weng, Dean-An Ling, Shang-Fu Chen, Tracy Ro, An-Jou Liang, Tom Lee, Helen Jin, Man Li, Lian Liu, Yu-Sheng Hsiao, Peilin Chen, Hsiao-Hua Yu, Ming-Song Tsai, Margareta D Pisarska, Angela Chen, Li-Ching Chen, Hsian-Rong Tseng Correction to Imprinted NanoVelcro Microchips for Isolation and Characterization of Circulating Fetal Trophoblasts: Toward Noninvasive Prenatal Diagnostics. ACS Nano: 2017; PubMed 29160690

Older papers  
  • Cell fusion induced by ERVWE1 or measles virus causes cellular senescence.[10] "Cellular senescence limits proliferation of potentially detrimental cells, preventing tumorigenesis and restricting tissue damage. However, the function of senescence in nonpathological conditions is unknown. We found that the human placental syncytiotrophoblast exhibited the phenotype and expressed molecular markers of cellular senescence. During embryonic development, ERVWE1-mediated cell fusion results in formation of the syncytiotrophoblast, which serves as the maternal/fetal interface at the placenta."
  • Early Expression of Pregnancy-Specific Glycoprotein 22 (PSG22) by Trophoblast Cells Modulates Angiogenesis in Mice[11] "Mouse and human pregnancy-specific glycoproteins (PSG) are known to exert immunomodulatory functions during pregnancy by inducing maternal leukocytes to secrete anti-inflammatory cytokines that promote a tolerogenic decidual microenvironment. Many such anti-inflammatory mediators also function as pro-angiogenic factors, which, along with the reported association of -murine PSG - with the uterine vasculature, suggest that PSG may contribute to the vascular adaptations necessary for successful implantation and placental development. ...Therefore, our findings indicate that despite the independent evolution and expansion of human and rodent PSG, members in both families have conserved functions, which include their ability to induce anti-inflammatory cytokines and pro-angiogenic factors as well as to induce the formation of capillary structures by endothelial cells. In summary, our results indicate that PSG22, the most abundant PSG expressed during mouse early pregnancy, is likely a major contributor to the establishment of a successful pregnancy."
  • Involvement of transcription factor NR2F2 in human trophoblast differentiation[12] "During the in vitro differentiation of human villous cytotrophoblast (CTB) cells to a syncytiotrophoblast (STB) phenotype, mRNA levels for the nuclear hormone receptor NR2F2 (ARP-1, COUP-TFII) increase rapidly, reaching a peak at day 1 of differentiation that is 8.8-fold greater than that in undifferentiated CTB cells."
  • Angiogenic growth factors[13] "Fourteen angiogenic growth factors were measured by multiplex growth factor analysis or ELISA in tissue culture supernatants from EVT and CTB from pregnancies at 8-10 and 12-14 weeks' gestation. Gestational age and cell type differences were observed. Extravillous trophoblast (EVT) and villous cytotrophoblast (CTB) are major producers of angiogenic growth factors that likely contribute to placental vascular development and spiral artery remodelling."

Trophoblast and Placental Villi

Early placental structure.jpg

Early placental development cartoon showing trophoblast contribution to placental villi.[14]

Legend

  • SYN - syncytiotrophoblasts
  • sCTB - subsyncytial cytotrophoblasts (this layer grows increasingly discontinuous in later trimesters)
  • EVT - extravillous cytotrophoblasts (anchor the villous tree in the decidua)

Cytotrophoblasts

Hyperglycosylated human Chorionic Gonadotropin (hCG) promotes the growth of cytotrophoblast cells and the endometrial invasion by these cells during implantation.[15]

Extravillous Cytotrophoblasts

Maintain open maternal spiral arteries emptying into the maternal lacunae[16]

At term, depending on maternal decidual localization, there are several identifiable subtypes:[4]

  • interstitial mononuclear (and multinuclear) - dispersed in decidual mesenchyme
  • endovascular - in spiral arteries lumen (or replacing endothelial cells)
  • intramural - in spiral arteries tunica media
  • "epithelial" lines - maternal decidua basalis basal plate with maternal endothelial cells in a mosaic fashion

Syncytiotrophoblasts

File:Cytotrophoblast to syncytiotrophoblast cartoon
  • form by fusion of rapidly dividing cytotrophoblast cells
  • secrete proteolytic enzymes, enzymes break down extracellular matrix around cells
  • Allow passage of blastocyst into endometrial wall, totally surround the blastocyst
  • generate spaces, lacunae, that fill with maternal blood
  • secrete Human Chorionic Gonadotropin (hCG), hormone, maintains decidua and Corpus Luteum, basis of pregnancy diagnostic test, present in urine is diagnostic of pregnancy
    • Later in development placenta will secrete hCG

Cell–cell Fusion Activity

Two pairs of envelope genes of retroviral origin, syncytins, have fusogenic properties. Human endogenous retroviruses (HERVs) make up about 8% of the human genome. Recent study has shown that placentae from intrauterine growth restriction have impaired cell fusion and differentiation that correlates with reduced levels of HERV envelope genes.[17]

Human - syncytin 1 and syncytin 2

  • Syncytin 2 is an envelope gene from the human endogenous retrovirus FRD (HERV-FRD)[18]
  • Syncytin 2 receptor is Major Facilitator Superfamily Domain Containing 2 (MFSD2) (at chromosomal position 1p34.2)
  • belongs to family of presumptive carbohydrate transporters with 10-12 membrane-spanning domains
  • Syncytin 1 (-FRD) receptor is ASCT-1/-2

Mouse - syncytin A and syncytin B

  • syncytin A is essential for trophoblast cell differentiation and syncytiotrophoblast morphogenesis[19]
Links: OMIM Syncytin-2

Human Chorionic Gonadotropin

hCG sources - produced by villous syncytiotrophoblast cells, hyperglycosylated hCG produced by cytotrophoblast cells, free beta-subunit made by multiple primary non-trophoblastic malignancies, and pituitary hCG made by the gonadotrope cells of the anterior pituitary.

  • levels peak at 8 to 10 weeks of pregnancy, then decline and are lower for rest of pregnancy
0-1 week: 0-50 mIU/ml 

1-2 weeks: 40-300 mIU/ml
3-4 weeks: 500-6,000 mIU/ml
1-2 months: 5,000-200,000 mIU/ml
2-3 months: 10,000-100,000 mIU/ml
2nd trimester: 3,000-50,000 mIU/ml
3rd trimester: 1,000-50,000 mIU/ml

Non-pregnant females: <5.0 mIU/ml Postmenopausal females: <9.5 mIU/ml

HLA-G

An acronym for histocompatibility antigen, class I, G (also called: Human Leukocyte Antigen G, (HLA-6.0; HLA60, T-CELL A LOCUS, TCA) and is expressed on placental cytotrophoblast cells and other adult tissues. This distinct tissue distribution differs from the other HLA antigens (HLA-A, HLA-B, HLA-C) leading to the description as a non-classical class I antigen. May have a role in protecting the fetus from the maternal immune response. For example, expression of the HLA-G class, instead of HLA-A and HLA-B, may be a mechanism for avoiding clearance by maternal natural killer cells.


Human gene is located at 6p22.1 and there exist several protein isoforms from alternative splicing of messenger RNAs, membrane-bound isoforms (HLA-G 1-4) and soluble soluble (HLA-G 5-6)[20]. The molecule is a heterodimer consisting of both a heavy chain and a light chain (beta-2 microglobulin). The membrane-bound isoform heavy chain is anchored in the membrane and increased expression of the soluble form is related to higher implantation rates. Changes in HLA-G expression have been associated with increased miscarriage rates.[21] Killer cell immunoglobulin-like receptor (KIR) 2DL4 (KIR2DL4) has been shown to act as a receptor for the soluble HLA-G, leading to a stimulation of resting natural killer (NK) cells.[22]


Links: HLA-G | OMIM142871

Trophoblast Infiltration

Human trophoblast invasion 01.jpg Human trophoblast invasion[23]

(A) The placenta connects the fetus to the uterine wall and establishes a vascular connection between mother and child. The placenta is structured as villous tree and is in direct contact with maternal blood and, thus referred to as hemochorial. The site where the placenta comes in direct contact with the maternal decidua is called the fetal-maternal interface.

(B) During early pregnancy, vCTBs fuse to form multinucleated STs, which surround the placental villus. STs transport nutrients and gases from the maternal to the fetal circulation and represent the major endocrine unit of the placenta by secreting hormones such as chorionic gonadotropin, placental growth hormone or placental lactogen. AV form cell columns that attach to the maternal decidua and give rise to the EVT lineage. Invasive EVTs can be divided into iCTBs, which invade the decidual stroma and become terminally differentiated multinucleated GCs, or eCTBs.

(i) The latter colonise the lumen of uterine spiral arteries and together with iCTBs, macrophages and uNK cells convert these vessels into larger conduits to guarantee adequate blood flow to the growing fetus.
(ii) Various decidual cell types such as macrophages, uNK cells and decidual stromal cells interact with the interstitial cytotrophoblasts in order to control iCTB invasion in an in a spatio-temporal manner.
(iii) In addition, iCTBs invade and replace the epithelium of endometrial glands.


AV, anchoring villus; CC, cell column; EVT, extravillous cytotrophoblast; eCTB, endovascular cytotrophoblast; iCTB, interstitial cytotrophoblast; SA, spiral artery; ST, syncytiotrophoblast; uNK, uterine natural killer cell.

Spiral artery trophoblast plug cartoon1.jpg Trophoblast plugs within Spiral Arteries Week 9, GA week 11.[6]


Trophoblast plugs (A) are composed of endovascular trophoblast cells. Depending on the stage of invasion and on the localization of sectioning the lumen of the spiral artery can be either completely filled with trophoblasts (1, 2) or (B) partly infiltrated (3, 4). In a plugged artery, the approaching erythrocytes are stowed by the trophoblast plug (1). Uterine glands are invaded and opened towards the intervillous space (C) by endoglandular trophoblasts. Glandular epithelial cells are replaced by endoglandular trophoblasts (5)


Trophoblast Cell Lines

A useful component of current placentation and trophoblast research are a number of trophoblast cell lines that have been derived from a number of different sources including term placenta, choriocarcinomas and transformation of primary isolated cells. BeWo cell line is the earliest human choriocarcinoma, established in 1968[24]. Most appear to be examples of extravillous trophoblast cells, some examples of various human "trophoblast" cell lines are listed below.

  • BeWo - human choriocarcinoma[24], hypotetraploid (modal number = 86; range = 71 to 178) (ATCC CCL-98)
  • JEG-3 - choriocarcinoma HTR8/SVneo a transformed extravillous trophoblast line
  • SGHPL-4 - [25][26] SV40 (pSV3neo) transformed primary cell line express cytokeratin-7, HLA class I antigen, HLA-G, BC-1, CD9, human chorionic gonadotrophin, and human placental lactogen.
  • TEV-1 - (HPV16) E6/E7 infection first-trimester extravillous trophoblast cell line[27]
  • ACH-3P - fusion of primary human first trimester trophoblasts (GA week 12) with a human choriocarcinoma cell line (AC1-1).[28]
  • HChEpC1b - retroviral infection by E6/E7/hTERT[29]


Search PubMed: BeWo | JEG-3 | SGHPL-4

History

image of Ambrosius Arnold Willem Hubrecht
Ambrosius Arnold Willem Hubrecht (1853 – 1915)

The name "Trophoblast" was used for the first time by Ambrosius Arnold Willem Hubrecht (1853 – 1915) at the meeting of the Anatomical Congress at Wiirzburg in 1888, and its earliest definition is found in the report of that meeting in Nos. 17 and 18 of the Anatomischer Anzeiger, Bd. III. "We there read, concerning a very early stage of the hedgehog (p. 510) : Die aussere Wand der Keimblase ist verdickt (drei bis vierschichtig) und besitzt wabige Lacunen. Fur diese aussere (epiblastische) Schicht sei der. Name Trophoblast gewahlt."



Links: The Trophoblast - A Rejoinder (1904) | Ambrosius Arnold Willem Hubrecht | Hubrecht Collection | Embryologists | Embryology History

Abnormalities

Hydatidiform Mole

Hydatidiform Mole

A type of placental abnormality when only the conceptus trophoblast layers proliferates and not the embryoblast, no embryo develops, this is called a "hydatidiform mole", which is due to the continuing presence of the trophoblastic layer, this abnormal conceptus can also implant in the uterus. The trophoblast cells will secrete human chorionic gonadotropin (hCG), as in a normal pregnancy, and may appear maternally and by pregnancy test to be "normal". Prenatal diagnosis by ultrasound analysis demonstrates the absence of a embryo.

There are several forms of hydatidiform mole: partial mole, complete mole and persistent gestational trophoblastic tumor. Many of these tumours arise from a haploid sperm fertilizing an egg without a female pronucleus (the alternative form, an embryo without sperm contribution, is called parthenogenesis). The tumour has a "grape-like" placental appearance without enclosed embryo formation. Following a first molar pregnancy, there is approximately a 1% risk of a second molar pregnancy.

This topic is also covered in Placenta - Abnormalities

Trophoblast Infections

References

  1. Pu Zhang, Marco Zucchelli, Sara Bruce, Fredwell Hambiliki, Anneli Stavreus-Evers, Lev Levkov, Heli Skottman, Erja Kerkelä, Juha Kere, Outi Hovatta Transcriptome profiling of human pre-implantation development. PLoS ONE: 2009, 4(11);e7844 PubMed 19924284 | PMC2773928 | PLoS One
  2. Noriko Tanaka, Takumi Takeuchi, Queenie V Neri, Eric Scott Sills, Gianpiero D Palermo Laser-assisted blastocyst dissection and subsequent cultivation of embryonic stem cells in a serum/cell free culture system: applications and preliminary results in a murine model. J Transl Med: 2006, 4;20 PubMed 16681851 | PMC1479373 | J Transl Med.
  3. Chandni V Jain, Leena Kadam, Marie van Dijk, Hamid-Reza Kohan-Ghadr, Brian A Kilburn, Craig Hartman, Vicki Mazzorana, Allerdien Visser, Michael Hertz, Alan D Bolnick, Rani Fritz, D Randall Armant, Sascha Drewlo Fetal genome profiling at 5 weeks of gestation after noninvasive isolation of trophoblast cells from the endocervical canal. Sci Transl Med: 2016, 8(363);363re4 PubMed 27807286
  4. 4.0 4.1 4.2 Nannan He, Liesbeth van Iperen, Danielle de Jong, Karoly Szuhai, Frans M Helmerhorst, Lucette A J van der Westerlaken, Susana M Chuva de Sousa Lopes Human Extravillous Trophoblasts Penetrate Decidual Veins and Lymphatics before Remodeling Spiral Arteries during Early Pregnancy. PLoS ONE: 2017, 12(1);e0169849 PubMed 28081266
  5. Mario Rothbauer, Nilaykumar Patel, Hajnalka Gondola, Monika Siwetz, Berthold Huppertz, Peter Ertl A comparative study of five physiological key parameters between four different human trophoblast-derived cell lines. Sci Rep: 2017, 7(1);5892 PubMed 28724925
  6. 6.0 6.1 Gregor Weiss, Monika Sundl, Andreas Glasner, Berthold Huppertz, Gerit Moser The trophoblast plug during early pregnancy: a deeper insight. Histochem. Cell Biol.: 2016; PubMed 27510415
  7. Hao Liang, Qian Zhang, Junjie Lu, Genling Yang, Na Tian, Xiaojie Wang, Yi Tan, Dongmei Tan MSX2 Induces Trophoblast Invasion in Human Placenta. PLoS ONE: 2016, 11(4);e0153656 PubMed 27088357
  8. Renaud, SJ. entail., OVO-like 1 regulates progenitor cell fate in human trophoblast development PNAS
  9. Yasuhide Ohinata, Tomoyuki Tsukiyama Establishment of trophoblast stem cells under defined culture conditions in mice. PLoS ONE: 2014, 9(9);e107308 PubMed 25203285
  10. Anna Chuprin, Hilah Gal, Tal Biron-Shental, Anat Biran, Aliza Amiel, Shmuel Rozenblatt, Valery Krizhanovsky Cell fusion induced by ERVWE1 or measles virus causes cellular senescence. Genes Dev.: 2013, 27(21);2356-66 PubMed 24186980 | Genes Dev.
  11. Sandra M Blois, Irene Tirado-González, Julie Wu, Gabriela Barrientos, Briana Johnson, James Warren, Nancy Freitag, Burghard F Klapp, Ster Irmak, Suleyman Ergun, Gabriela S Dveskler Early expression of pregnancy-specific glycoprotein 22 (PSG22) by trophoblast cells modulates angiogenesis in mice. Biol. Reprod.: 2012, 86(6);191 PubMed 22423048
  12. Michael A Hubert, Susan L Sherritt, Cindy J Bachurski, Stuart Handwerger Involvement of transcription factor NR2F2 in human trophoblast differentiation. PLoS ONE: 2010, 5(2);e9417 PubMed 20195529 | PLoS One
  13. G E Lash, K Naruse, B A Innes, S C Robson, R F Searle, J N Bulmer Secretion of angiogenic growth factors by villous cytotrophoblast and extravillous trophoblast in early human pregnancy. Placenta: 2010, 31(6);545-8 PubMed 20338637
  14. Jennifer R Robbins, Kasia M Skrzypczynska, Varvara B Zeldovich, Mirhan Kapidzic, Anna I Bakardjiev Placental syncytiotrophoblast constitutes a major barrier to vertical transmission of Listeria monocytogenes. PLoS Pathog.: 2010, 6(1);e1000732 PubMed 20107601 | PLoS
  15. Laurence A Cole Biological functions of hCG and hCG-related molecules. Reprod. Biol. Endocrinol.: 2010, 8;102 PubMed 20735820
  16. G St J Whitley, J E Cartwright Cellular and molecular regulation of spiral artery remodelling: lessons from the cardiovascular field. Placenta: 2010, 31(6);465-74 PubMed 20359743
  17. Matthias Ruebner, Pamela L Strissel, Manuela Langbein, Fabian Fahlbusch, David L Wachter, Florian Faschingbauer, Matthias W Beckmann, Reiner Strick Impaired cell fusion and differentiation in placentae from patients with intrauterine growth restriction correlate with reduced levels of HERV envelope genes. J. Mol. Med.: 2010, 88(11);1143-56 PubMed 20664994
  18. Cécile Esnault, Stéphane Priet, David Ribet, Cécile Vernochet, Thomas Bruls, Christian Lavialle, Jean Weissenbach, Thierry Heidmann A placenta-specific receptor for the fusogenic, endogenous retrovirus-derived, human syncytin-2. Proc. Natl. Acad. Sci. U.S.A.: 2008, 105(45);17532-7 PubMed 18988732 | PNAS
  19. Anne Dupressoir, Cécile Vernochet, Olivia Bawa, Francis Harper, Gérard Pierron, Paule Opolon, Thierry Heidmann Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc. Natl. Acad. Sci. U.S.A.: 2009, 106(29);12127-32 PubMed 19564597
  20. Yuan Q Yao, David H Barlow, Ian L Sargent Differential expression of alternatively spliced transcripts of HLA-G in human preimplantation embryos and inner cell masses. J. Immunol.: 2005, 175(12);8379-85 PubMed 16339579
  21. Theodora Papamitsou, Alexandros Toskas, Kyriaki Papadopoulou, Antonia Sioga, Sotirios Lakis, Maria Chatzistamatiou, Zinon Economou, Luisa Adriopoulou Immunohistochemical study of immunological markers: HLAG, CD16, CD25, CD56 and CD68 in placenta tissues in recurrent pregnancy loss. Histol. Histopathol.: 2014, 29(8);1047-55 PubMed 24557735
  22. Sumati Rajagopalan, Yenan T Bryceson, Shanmuga P Kuppusamy, Daniel E Geraghty, Arnold van der Meer, Irma Joosten, Eric O Long Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol.: 2006, 4(1);e9 PubMed 16366734
  23. Philipp Velicky, Martin Knöfler, Jürgen Pollheimer Function and control of human invasive trophoblast subtypes: intrinsic vs. maternal control. Cell Adh Migr: 2015; PubMed 26418186
  24. 24.0 24.1 R A Pattillo, G O Gey, E Delfs, R F Mattingly Human hormone production in vitro. Science: 1968, 159(3822);1467-9 PubMed 5753554
  25. M Y Choy, I T Manyonda The phagocytic activity of human first trimester extravillous trophoblast. Hum. Reprod.: 1998, 13(1O);2941-9 PubMed 9804259
  26. H L LaMarca, C M Ott, K Höner Zu Bentrup, C L Leblanc, D L Pierson, A B Nelson, A B Scandurro, G St J Whitley, C A Nickerson, C A Morris Three-dimensional growth of extravillous cytotrophoblasts promotes differentiation and invasion. Placenta: 2005, 26(10);709-20 PubMed 16226120
  27. Hui Chen Feng, Mei Yee Choy, Wen Deng, Hing Lok Wong, Wui Man Lau, Annie N Y Cheung, Hextan Y S Ngan, Sai Wah Tsao Establishment and characterization of a human first-trimester extravillous trophoblast cell line (TEV-1). J. Soc. Gynecol. Investig.: 2005, 12(4);e21-32 PubMed 15866109
  28. Ursula Hiden, Christian Wadsack, Nicole Prutsch, Martin Gauster, Ursula Weiss, Hans-Georg Frank, Ulrike Schmitz, Christa Fast-Hirsch, Markus Hengstschläger, Andy Pötgens, Angela Rüben, Martin Knöfler, Peter Haslinger, Berthold Huppertz, Martin Bilban, Peter Kaufmann, Gernot Desoye The first trimester human trophoblast cell line ACH-3P: a novel tool to study autocrine/paracrine regulatory loops of human trophoblast subpopulations--TNF-alpha stimulates MMP15 expression. BMC Dev. Biol.: 2007, 7;137 PubMed 18093301
  29. Hiroko Omi, Aikou Okamoto, Takashi Nikaido, Mitsuyoshi Urashima, Rie Kawaguchi, Nagayoshi Umehara, Kentaro Sugiura, Misato Saito, Tohru Kiyono, Tadao Tanaka Establishment of an immortalized human extravillous trophoblast cell line by retroviral infection of E6/E7/hTERT and its transcriptional profile during hypoxia and reoxygenation. Int. J. Mol. Med.: 2009, 23(2);229-36 PubMed 19148547
  30. Eugenia de la Torre, Melissa J Mulla, Andrew G Yu, Seung-Joon Lee, Paula B Kavathas, Vikki M Abrahams Chlamydia trachomatis infection modulates trophoblast cytokine/chemokine production. J. Immunol.: 2009, 182(6);3735-45 PubMed 19265152
  31. Mariantonietta Di Stefano, Maria Luisa Calabrò, Iole Maria Di Gangi, Santina Cantatore, Massimo Barbierato, Elisa Bergamo, Anfumbom Jude Kfutwah, Margherita Neri, Luigi Chieco-Bianchi, Pantaleo Greco, Loreto Gesualdo, Ahidjo Ayouba, Elisabeth Menu, Josè Ramòn Fiore In vitro and in vivo human herpesvirus 8 infection of placenta. PLoS ONE: 2008, 3(12);e4073 PubMed 19115001
  32. Amber Kaplan, Kathy Chung, Hande Kocak, Cristina Bertolotto, Andy Uh, Calvin J Hobel, Charles F Simmons, Kelly Doran, George Y Liu, Ozlem Equils Group B streptococcus induces trophoblast death. Microb. Pathog.: 2008, 45(3);231-5 PubMed 18599257


Reviews

John D Aplin Developmental cell biology of human villous trophoblast: current research problems. Int. J. Dev. Biol.: 2010, 54(2-3);323-9 PubMed 19876840


Articles

Amy Ralston, Brian J Cox, Noriyuki Nishioka, Hiroshi Sasaki, Evelyn Chea, Peter Rugg-Gunn, Guoji Guo, Paul Robson, Jonathan S Draper, Janet Rossant Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development: 2010, 137(3);395-403 PubMed 20081188

Yohei Hayashi, Miho Kusuda Furue, Satoshi Tanaka, Michiko Hirose, Noriko Wakisaka, Hiroki Danno, Kiyoshi Ohnuma, Shiho Oeda, Yuko Aihara, Kunio Shiota, Atsuo Ogura, Shoichi Ishiura, Makoto Asashima BMP4 induction of trophoblast from mouse embryonic stem cells in defined culture conditions on laminin. In Vitro Cell. Dev. Biol. Anim.: 2010, 46(5);416-30 PubMed 20033790

Jonathan P Stoye Proviral protein provides placental function. Proc. Natl. Acad. Sci. U.S.A.: 2009, 106(29);11827-8 PubMed 19617545

Anne Dupressoir, Cécile Vernochet, Olivia Bawa, Francis Harper, Gérard Pierron, Paule Opolon, Thierry Heidmann Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc. Natl. Acad. Sci. U.S.A.: 2009, 106(29);12127-32 PubMed 19564597

Srinivas R Viswanathan, Craig H Mermel, Jun Lu, Chi-Wei Lu, Todd R Golub, George Q Daley microRNA expression during trophectoderm specification. PLoS ONE: 2009, 4(7);e6143 PubMed 19582159


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Cite this page: Hill, M.A. 2017 Embryology Trophoblast. Retrieved November 23, 2017, from https://embryology.med.unsw.edu.au/embryology/index.php/Trophoblast

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© Dr Mark Hill 2017, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G