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Endocrinology, doi:10.1210/endo-118-4-1567
Endocrinology Vol. 118, No. 4 1567-1582
Copyright © 1986 by the Endocrine Society.
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*CHORIONIC GONADOTROPIN
*PROGESTERONE

Purification, Characterization, and in vitro Differentiation of Cytotrophoblasts from Human Term Placentae*

HARVEY J. KLIMAN, JOHN E. NESTLER{dagger}, EDUARDO SERMASI, JEAN M. SANGER and JEROME F. STRAUSS, III

Departments of Pathology and Laboratory Medicine, Medicine (J.E.N.), Obstetrics and Gynecology, and Anatomy, University of Pennsylvania School of Medicine Philadelphia, Pennsylvania 19104

Address all correspondence and requests for reprints to: Harvey Kliman, M.D., Ph.D., Department of Pathology and Laboratory Medicine, 2 Gibson, 3400 Spruce Street, Philadelphia, Pennsylvania 19104.

Abstract

Highly purified functional cytotrophoblasts have been prepared from human term placentae by adding a Percoll gradient centrifugation step to a standard trypsin-DNase dispersion method. The isolated mononuclear trophoblasts averaged 10 µm in diameter, with occasional cells measuring up to 20–30 µm. Viability was greater than 90%. Transmission electron microscopy revealed that the cells had fine structural features typical of trophoblasts. In contrast to syncytial trophoblasts of intact term placentae, these cells did not stain for hCG, human placental lactogen, pregnancy-specific {alpha}1-glycoprotein or low mol wt cytokeratins by immunoperoxidase methods. Endothelial cells, fibroblasts, or macrophages did not contaminate the purified cytotrophoblasts, as evidenced by the lack of immunoperoxidase staining with antibodies against vimentin or {alpha}1-antichymotrypsin. The cells produced progesterone (1 ng/106 cells-4 h), and progesterone synthesis was stimulated up to 8- fold in the presence of 25-hydroxycholesterol (20 µg/ml). They also produced estrogens (1360 pg/106 cells-4 h) when supplied with androstenedione (1 ng/ml) as a precursor. When placed in culture, the cytotrophoblasts consistently formed aggregates, which subsequently transformed into syncytia within 24–48 h after plating. Time lapse cinematography revealed that this process occurred by cell fusion. The presumptive syncytial groups were proven to be true syncytia by microinjection of fluorescently labeled y9-actinin, which diffused completely throughout the syncytial cytoplasm within 30 min. Immunoperoxidase staining of cultured trophoblasts between 3.5 and 72 h after plating revealed a progressive increase in cytoplasmic pregnancy-specific β1-glycoprotein, hCG, and human placental lactogen concomitant with increasing numbers of aggregates and syncytia. At all time points examined, occasional single cells positive for these markers were identified. RIA of the spent culture media for hCG revealed a significant increase in secreted hCG, paralleling the increase in hCG-positive cells and syncytia identified by immunoperoxidase methods. We conclude that human cytotrophoblasts differentiate in culture and fuse to form functional syncytiotrophoblasts. {Endocrinology 118:1567–1582,1986)

Footnotes

* This work was supported by NICHHD Research Grant HD-06274 (to J.F.S.), USPHS Grant AM-07481 (to J.E.N.), and a grant from the Diabetes Research amd Education Foundation (to H.J.K.).

{dagger} Present address: Division of Endocrinology and Metabolism, Medical College of Virginia, Richmond, Virginia 23298.

Received June 6, 1985.




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E. D. Johnstone, G. Chan, C. P. Sibley, S. T. Davidge, B. Lowen, and L. J. Guilbert
Sphingosine-1-phosphate inhibition of placental trophoblast differentiation through a Gi-coupled receptor response
J. Lipid Res., September 1, 2005; 46(9): 1833 - 1839.
[Abstract] [Full Text] [PDF]

Home page
 EndocrinologyHome page
Z. Strakova, P. Mavrogianis, X. Meng, J. M. Hastings, K. S. Jackson, P. Cameo, A. Brudney, O. Knight, and A. T. Fazleabas
In Vivo Infusion of Interleukin-1{beta} and Chorionic Gonadotropin Induces Endometrial Changes that Mimic Early Pregnancy Events in the Baboon
Endocrinology, September 1, 2005; 146(9): 4097 - 4104.
[Abstract] [Full Text] [PDF]

Home page
 J. Physiol.Home page
G. Daoud, M. Amyot, E. Rassart, A. Masse, L. Simoneau, and J. Lafond
ERK1/2 and p38 regulate trophoblasts differentiation in human term placenta
J. Physiol., July 15, 2005; 566(2): 409 - 423.
[Abstract] [Full Text] [PDF]

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 Reproductive SciencesHome page
H. Chisaka, J. F. Johnstone, M. Premyslova, Z. Manduch, and J. R.G. Challis
Effect of Pro-inflammatory Cytokines on Expression and Activity of 11{beta}-Hydroxysteroid Dehydrogenase Type 2 in Cultured Human Term Placental Trophoblast and Human Choriocarcinoma JEG-3 Cells
Reproductive Sciences, July 1, 2005; 12(5): 303 - 309.
[Abstract] [PDF]

Home page
 Drug Metab. Dispos.Home page
H. E. Meyer zu Schwabedissen, G. Jedlitschky, M. Gratz, S. Haenisch, K. Linnemann, C. Fusch, I. Cascorbi, and H. K. Kroemer
VARIABLE EXPRESSION OF MRP2 (ABCC2) IN HUMAN PLACENTA: INFLUENCE OF GESTATIONAL AGE AND CELLULAR DIFFERENTIATION
Drug Metab. Dispos., July 1, 2005; 33(7): 896 - 904.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
W. T. Schaiff, I. Bildirici, M. Cheong, P. L. Chern, D. M. Nelson, and Y. Sadovsky
Peroxisome Proliferator-Activated Receptor-{gamma} and Retinoid X Receptor Signaling Regulate Fatty Acid Uptake by Primary Human Placental Trophoblasts
J. Clin. Endocrinol. Metab., July 1, 2005; 90(7): 4267 - 4275.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
G. Fiore, P. Florio, L. Micheli, C. Nencini, M. Rossi, D. Cerretani, G. Ambrosini, G. Giorgi, and F. Petraglia
Endothelin-1 Triggers Placental Oxidative Stress Pathways: Putative Role in Preeclampsia
J. Clin. Endocrinol. Metab., July 1, 2005; 90(7): 4205 - 4210.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
D. Marzioni, G. Fiore, A. Giordano, M. Nabissi, P. Florio, F. Verdenelli, F. Petraglia, and M. Castellucci
Placental Expression of Substance P and Vasoactive Intestinal Peptide: Evidence for a Local Effect on Hormone Release
J. Clin. Endocrinol. Metab., April 1, 2005; 90(4): 2378 - 2383.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
E. A. Cowley, M. C. Sellers, and N. P. Illsley
Intracellular pH homeostasis in cultured human placental syncytiotrophoblast cells: recovery from acidification
Am J Physiol Cell Physiol, April 1, 2005; 288(4): C891 - C898.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
M. Hayashi, M. Sakata, T. Takeda, M. Tahara, T. Yamamoto, R. Minekawa, A. Isobe, K. Tasaka, and Y. Murata
Hypoxia Up-Regulates Hypoxia-Inducible Factor-1{alpha} Expression through RhoA Activation in Trophoblast Cells
J. Clin. Endocrinol. Metab., March 1, 2005; 90(3): 1712 - 1719.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
K. J. Barber, J. A. Franklyn, C. J. McCabe, F. L. Khanim, J. N. Bulmer, G. S. J. Whitley, and M. D. Kilby
The in Vitro Effects of Triiodothyronine on Epidermal Growth Factor-Induced Trophoblast Function
J. Clin. Endocrinol. Metab., March 1, 2005; 90(3): 1655 - 1661.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
L. Julan, H. Guan, J. P. van Beek, and K. Yang
Peroxisome Proliferator-Activated Receptor {delta} Suppresses 11{beta}-Hydroxysteroid Dehydrogenase Type 2 Gene Expression in Human Placental Trophoblast Cells
Endocrinology, March 1, 2005; 146(3): 1482 - 1490.
[Abstract] [Full Text] [PDF]

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 Ann Rheum DisHome page
N Di Simone, E Raschi, C Testoni, R Castellani, M D'Asta, T Shi, S A Krilis, A Caruso, and P L Meroni
Pathogenic role of anti-{beta}2-glycoprotein I antibodies in antiphospholipid associated fetal loss: characterisation of {beta}2-glycoprotein I binding to trophoblast cells and functional effects of anti-{beta}2-glycoprotein I antibodies in vitro
Ann Rheum Dis, March 1, 2005; 64(3): 462 - 467.
[Abstract] [Full Text] [PDF]

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 Reproductive SciencesHome page
X. Bai, S. L. Greenwood, J. D. Glazier, P. N. Baker, C. P. Sibley, M. J. Taggart, and G. K. Fyfe
Localization of TASK and TREK, Two-Pore Domain K+ Channels, in Human Cytotrophoblast Cells
Reproductive Sciences, February 1, 2005; 12(2): 77 - 83.
[Abstract] [PDF]

Home page
 Drug Metab. Dispos.Home page
M. Grube, H. M. z. Schwabedissen, K. Draber, D. Prager, K.-U. Moritz, K. Linnemann, C. Fusch, G. Jedlitschky, and H. K. Kroemer
EXPRESSION, LOCALIZATION, AND FUNCTION OF THE CARNITINE TRANSPORTER OCTN2 (SLC22A5) IN HUMAN PLACENTA
Drug Metab. Dispos., January 1, 2005; 33(1): 31 - 37.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
B. Chenais, A. Derjuga, W. Massrieh, K. Red-Horse, V. Bellingard, S. J. Fisher, and V. Blank
Functional and Placental Expression Analysis of the Human NRF3 Transcription Factor
Mol. Endocrinol., January 1, 2005; 19(1): 125 - 137.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Pathol.Home page
H. E.U. Meyer zu Schwabedissen, M. Grube, B. Heydrich, K. Linnemann, C. Fusch, H. K. Kroemer, and G. Jedlitschky
Expression, Localization, and Function of MRP5 (ABCC5), a Transporter for Cyclic Nucleotides, in Human Placenta and Cultured Human Trophoblasts: Effects of Gestational Age and Cellular Differentiation
Am. J. Pathol., January 1, 2005; 166(1): 39 - 48.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
C Niger, A Malassine, and L Cronier
Calcium channels activated by endothelin-1 in human trophoblast
J. Physiol., December 1, 2004; 561(2): 449 - 458.
[Abstract] [Full Text] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
J. P. van Beek, H. Guan, L. Julan, and K. Yang
Glucocorticoids Stimulate the Expression of 11{beta}-Hydroxysteroid Dehydrogenase Type 2 in Cultured Human Placental Trophoblast Cells
J. Clin. Endocrinol. Metab., November 1, 2004; 89(11): 5614 - 5621.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
E. D. Albrecht, V. A. Robb, and G. J. Pepe
Regulation of Placental Vascular Endothelial Growth/Permeability Factor Expression and Angiogenesis by Estrogen during Early Baboon Pregnancy
J. Clin. Endocrinol. Metab., November 1, 2004; 89(11): 5803 - 5809.
[Abstract] [Full Text] [PDF]

Home page
 Biol. Reprod.Home page
V. A. Robb, G. J. Pepe, and E. D. Albrecht
Acute Temporal Regulation of Placental Vascular Endothelial Growth/Permeability Factor Expression in Baboons by Estrogen
Biol Reprod, November 1, 2004; 71(5): 1694 - 1698.
[Abstract] [Full Text] [PDF]

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 Reproductive SciencesHome page
A. Jasinska, V. Han, A. T. Fazleabas, and J. J. Kim
Induction of Insulin-Like Growth Factor Binding Protein-1 Expression in Baboon Endometrial Stromal Cells by Cells of Trophoblast Origin
Reproductive Sciences, September 1, 2004; 11(6): 399 - 405.
[Abstract] [PDF]

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 Am. J. Pathol.Home page
R. M. Gill and J. S. Hunt
Soluble Receptor (DcR3) and Cellular Inhibitor of Apoptosis-2 (cIAP-2) Protect Human Cytotrophoblast Cells Against LIGHT-Mediated Apoptosis
Am. J. Pathol., July 1, 2004; 165(1): 309 - 317.
[Abstract] [Full Text] [PDF]

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 Physiol. GenomicsHome page
Y.-H. Cheng, B. J. Aronow, S. Hossain, B. Trapnell, S. Kong, and S. Handwerger
Critical role for transcription factor AP-2{alpha} in human trophoblast differentiation
Physiol Genomics, June 17, 2004; 18(1): 99 - 107.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
W. Li, N. Alfaidy, and J. R. G. Challis
Expression of Extracellular Matrix Metalloproteinase Inducer in Human Placenta and Fetal Membranes at Term Labor
J. Clin. Endocrinol. Metab., June 1, 2004; 89(6): 2897 - 2904.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
X. Ni, Y. Hou, B. R. King, X. Tang, M. A. Read, R. Smith, and R. C. Nicholson
Estrogen Receptor-Mediated Down-Regulation of Corticotropin-Releasing Hormone Gene Expression Is Dependent on a Cyclic Adenosine 3',5'-Monophosphate Regulatory Element in Human Placental Syncytiotrophoblast Cells
J. Clin. Endocrinol. Metab., May 1, 2004; 89(5): 2312 - 2318.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
M.-J. Lee, Y. Ma, L. LaChapelle, S. S. Kadner, and S. Guller
Glucocorticoid Enhances Transforming Growth Factor-{beta} Effects on Extracellular Matrix Protein Expression in Human Placental Mesenchymal Cells
Biol Reprod, May 1, 2004; 70(5): 1246 - 1252.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. Lecuit, D. M. Nelson, S. D. Smith, H. Khun, M. Huerre, M.-C. Vacher-Lavenu, J. I. Gordon, and P. Cossart
Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: Role of internalin interaction with trophoblast E-cadherin
PNAS, April 20, 2004; 101(16): 6152 - 6157.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
M. Knofler, L. Saleh, S. Bauer, B. Galos, H. Rotheneder, P. Husslein, and H. Helmer
Transcriptional Regulation of the Human Chorionic Gonadotropin {beta} Gene during Villous Trophoblast Differentiation
Endocrinology, April 1, 2004; 145(4): 1685 - 1694.
[Abstract] [Full Text] [PDF]

Home page
 Mol Hum ReprodHome page
E.Y. Anteby, C. Greenfield, S. Natanson-Yaron, D. Goldman-Wohl, Y. Hamani, V. Khudyak, I. Ariel, and S. Yagel
Vascular endothelial growth factor, epidermal growth factor and fibroblast growth factor-4 and -10 stimulate trophoblast plasminogen activator system and metalloproteinase-9
Mol. Hum. Reprod., April 1, 2004; 10(4): 229 - 235.
[Abstract] [Full Text] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
C.-S. Chou, A. G. Beristain, C. D. MacCalman, and P. C. K. Leung
Cellular Localization of Gonadotropin-Releasing Hormone (GnRH) I and GnRH II in First-Trimester Human Placenta and Decidua
J. Clin. Endocrinol. Metab., March 1, 2004; 89(3): 1459 - 1466.
[Abstract] [Full Text] [PDF]

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 Toxicol SciHome page
J. Chen, T. L. Thirkill, P. N. Lohstroh, S. R. Bielmeier, M. G. Narotsky, D. S. Best, R. A. Harrison, K. Natarajan, R. A. Pegram, J. W. Overstreet, et al.
Bromodichloromethane Inhibits Human Placental Trophoblast Differentiation
Toxicol. Sci., March 1, 2004; 78(1): 166 - 174.
[Abstract] [Full Text] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
J.-L. Frendo, J. Guibourdenche, G. Pidoux, M. Vidaud, D. Luton, Y. Giovangrandi, D. Porquet, F. Muller, and D. Evain-Brion
Trophoblast Production of a Weakly Bioactive Human Chorionic Gonadotropin in Trisomy 21-Affected Pregnancy
J. Clin. Endocrinol. Metab., February 1, 2004; 89(2): 727 - 732.
[Abstract] [Full Text] [PDF]

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 Reproductive SciencesHome page
N. Mirazi, N. Alfaidy, R. Martin, and J. R. G. Challis
Effects of Dexamethasone and Sulfasalazine on Prostaglandin E2 Output by Human Placental Cells In Vitro
Reproductive Sciences, January 1, 2004; 11(1): 22 - 26.
[Abstract] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
M. Premyslova, W. Li, N. Alfaidy, A. D. Bocking, K. Campbell, W. Gibb, and J. R. G. Challis
Differential Expression and Regulation of Microsomal Prostaglandin E2 Synthase in Human Fetal Membranes and Placenta with Infection and in Cultured Trophoblast Cells
J. Clin. Endocrinol. Metab., December 1, 2003; 88(12): 6040 - 6047.
[Abstract] [Full Text] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
I. Bildirici, C.-R. Roh, W. T. Schaiff, B. M. Lewkowski, D. M. Nelson, and Y. Sadovsky
The Lipid Droplet-Associated Protein Adipophilin Is Expressed in Human Trophoblasts and Is Regulated by Peroxisomal Proliferator-Activated Receptor-{gamma}/Retinoid X Receptor
J. Clin. Endocrinol. Metab., December 1, 2003; 88(12): 6056 - 6062.
[Abstract] [Full Text] [PDF]

Home page
 Mol Hum ReprodHome page
P.M. Driver, S. Rauz, E.A. Walker, M. Hewison, M.D. Kilby, and P.M. Stewart
Characterization of human trophoblast as a mineralocorticoid target tissue
Mol. Hum. Reprod., December 1, 2003; 9(12): 793 - 798.
[Abstract] [Full Text] [PDF]


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