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Biology of Reproduction 62, 1812-1817 (2000)
© 2000 Society for the Study of Reproduction, Inc.

Articles

Cell Type-Specific Regulation of Fetal Fibronectin Expression in Amnion: Conservation of Glucocorticoid Responsiveness in Human and Nonhuman Primates1

Yuehong Maa, Charles J. Lockwooda, Ari L. Bunima, Dino A. Giussanib, Peter W. Nathanielszc, and S. Guller2,a

a Department of Obstetrics and Gynecology, New York University School of Medicine, New York, New York 10016 b Department of Physiology, University of Cambridge, Cambridge, United Kingdom c Laboratory for Pregnancy and Newborn Research, Department of Physiology, Cornell University, Ithaca, New York 14853-6401


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The appearance of oncofetal fibronectin (FFN) in cervical and vaginal secretions is predictive of human labor. Levels of FFN in amnion increase with the onset of labor in rhesus monkeys. Since glucocorticoid (GC) levels in serum and amniotic fluid increase in association with parturition, we compared GC-mediated regulation of FFN expression in cultures of amnion epithelial cells and fibroblasts isolated from human and baboon amnions. Cells were maintained with and without dexamethasone (DEX), and levels of FFN in the conditioned media were determined by ELISA. We observed that DEX treatment suppressed FFN levels in both human and baboon amnion epithelial cells, whereas it increased FFN levels in amnion fibroblasts. DEX treatment reduced FFN levels in cytotrophoblasts from human placenta and increased FFN levels in placental fibroblasts. Northern blots revealed that DEX reduced levels of fibronectin (FN) mRNA in amnion epithelial cells and cytotrophoblasts, whereas it increased FN mRNA in amnion and placental fibroblasts. We conclude that GC differentially regulates FFN expression in epithelial and mesenchymal cells from amnion and placenta. In addition, this pattern of cell type-specific FFN regulation by GC is conserved in human and nonhuman primates and may be responsible for parturition-dependent changes in FFN expression in gestational tissues.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Fibronectins (FNs) constitute a family of ubiquitous glycoproteins that play major roles in regulating diverse biological functions including cellular adhesion and differentiation, embryogenesis, and tumorigenesis [1]. Oncofetal fibronectin (FFN) is a uniquely glycosylated form of FN that is expressed at high levels in fetal tissues and cancer cell lines but not in adult tissues [2, 3]. Its immunohistochemical distribution revealed abundant expression at regions of uterine-placental and fetal membrane-decidual contact [4, 5], suggesting that FFN plays a critical role in regulating cell adhesion at these maternal-fetal junctions. The appearance of FFN in cervico-vaginal secretions of women between 21 and 36 wk of pregnancy identified a group of women who were at risk for preterm labor [4]. Amnion FFN levels increased in association with labor in rhesus monkeys whether occurring prior to or at term [6], and the labor-induced change in FFN expression at this site was dependent on placental estrogen synthesis [7].

In humans, the concentrations of glucocorticoid (GC) and corticotropin-releasing hormone (CRH) in amniotic fluid and maternal and fetal plasma increase in association with parturition [8–10]. Plasma levels of biologically active (free) CRH were high in women who delivered preterm and were low in those women delivering postterm [11]. Since CRH enhances prostaglandin production in fetal membranes, placenta, and decidua [12], and given that the placenta is the major source of plasma CRH during pregnancy [13], these results are consistent with the hypothesis that altered placental CRH production plays a role in the mechanisms that control the length of gestation [11]. GC treatment increases CRH levels in placental and fetal membrane cells [14], suggesting an important role of GC in the events surrounding parturition.

Epithelial and mesenchymal cells in human fetal membranes carry out extracellular matrix (ECM) protein synthesis [15]. The amnion epithelial cells, the innermost cell layer of fetal membranes, in conjunction with underlying fibroblasts, are the major cell types in amnion responsible for the synthesis of FNs and collagens at this site [15]. Similarly, ECM protein synthesis is carried out by epithelial cells (i.e., cytotrophoblasts) and mesenchymal cells in human placenta [16]. However, the patterns of cytotrophoblast FFN expression reflect their state of differentiation and invasive potential, with FFN restricted to extravillous cytotrophoblasts of the anchoring villi and cytotrophoblastic shell [17, 18]. Previous results obtained in our laboratory indicate that GC treatment reduced the expression of FFN, laminin, and collagen III in primary cultures of cytotrophoblasts and amnion epithelial cells [19, 20]. The GC-mediated reduction in cytotrophoblast FN expression is mediated through a short-lived protein [21], and stands in sharp contrast to the stimulatory effect of GC on FN expression that is observed in most cell types [22, 23].

The purpose of the present study was to elucidate the effects of GC treatment on FFN expression in the predominant ECM-synthesizing epithelial and stromal cell types from human amnion and placenta using primary cell culture models. In addition, we tested whether the patterns of ECM protein regulation observed in human amnion cells were conserved in other primate species, using the baboon as an example.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Materials

Tissue culture media and dexamethasone (DEX) were obtained from Sigma (St. Louis, MO). Bovine sera were obtained from Gemini Bio-Products (Calabasas, CA). Laboratory plasticware was obtained from Falcon, Becton-Dickinson Labware (Lincoln Park, NJ). ITS+, a mixture containing insulin, transferrin, and selenium, was purchased from Collaborative Research-Becton Dickinson (Bedford, MA). Ultraspec used for RNA isolation was purchased from Biotecx Laboratories (Houston, TX). [32P]dCTP was from New England Nuclear (Boston, MA). Plasmids containing cDNAs to fibronectin and glyceraldehyde-3-phosphate dehydrogenase (GAPDH) were from the American Type Culture Collection (Rockville, MD). Other reagents used in tissue culture and Northern blotting were from previously described sources [19, 21].

Methods

Cell culture Amnion epithelial cells were isolated from approximately 5 g of human or baboon amnion tissue by digestion with 5% trypsin [20]. This treatment removes amnion epithelial cells from their basal lamina without disrupting underlying collagenous connective tissue. After digestion with trypsin, amnion fibroblasts were released from membrane fragments by subsequent treatment with 0.25% collagenase [24]. The ratio of isolated epithelial cell to fibroblast was approximately 10:1 for both human and baboon preparations, and cell viability was approximately 90% as judged by trypan blue exclusion. Approximately 50 x 106 and 15 x 106 amnion epithelial cells were obtained per 5 g of human and baboon tissue, respectively.

Cytotrophoblasts were isolated from approximately 90 g of human villous tissue at term after trypsin digestion and centrifugation on continuous Percoll gradients as we have described [19]. Placental fibroblasts were isolated from 5–10 g of villous tissue after treatment with 0.25% collagenase on the basis of our modification [21] of procedures originally described by Fant and Nanu [25]. Fibroblasts between passage 2 and 7 were used for experiments.

After isolation, amnion and placental cells were plated at a density of 1–4 x 105 cells per 24-well dish for ELISA studies and 2–10 x 106 cells per 10-cm dish for Northern blot analysis in culture medium containing a 1:1 mixture of phenol red-free Ham's F-12:Dulbecco's modified Eagle's medium containing 10% charcoal-stripped calf serum (i.e., SCS medium) and ITS+ (a supplement utilized to obtain a final concentration of insulin of 6.25 µg/ml, transferrin 6.25 µg/ml, selenious acid 6.25 ng/ml, BSA 1.25 mg/ml, and linoleic acid 5.35 µg/ml) [19, 21] in the presence and absence of 100 nM DEX. After the indicated time in culture, conditioned media were saved for ELISA, and protein and RNA were extracted from adherent cells.

Cells were maintained at 37°C in SCS medium in a humidified atmosphere of 5% CO2 and 95% air.

FFN ELISA Levels of FFN in culture media were measured by an ELISA using FDC-6 monoclonal antibody according to information provided by the manufacturer (Adeza Biomedical, Sunnyvale, CA) as we have previously described [19, 26]. The concentration of FFN in culture media was determined in triplicate wells and was normalized to cell protein using the DC protein assay from Bio-Rad Laboratories (Hercules, CA).

Northern blotting RNA was extracted from placental and amnion cells using UltraSpec RNA (Biotecx) as we have described [21]. Approximately 20 µg total RNA was separated on a 1% agarose gel containing formaldehyde. After transfer, FN and GAPDH mRNAs were detected using 32P-labeled cDNA probes. Autoradiographic signals were quantitated using the Electrophoresis Documentation and Analysis System 120 and Digital Science 1D Image Software (Eastman Kodak, Rochester, NY).

Statistics Representative results for human and baboon amnion epithelial cells and fibroblasts and human cytotrophoblasts shown in Figures 1, 2, 4, and 5 are from 1 tissue representing 3 or 4 tissues from different subjects. Representative results for placental fibroblasts depict data obtained from 1 cell passage in 1 experiment representing 3 identically conducted experiments from 3 different cell passages. For the analysis of cumulative data shown in Figure 3 and the text accompanying Figure 4, the percentage difference in FFN levels between control and DEX-treated cultures was determined in 3 or 4 independent experiments; the average percentage difference was calculated; and a t-test then determined whether this value differed from 0. Results are expressed as a mean ± SEM. Statistical analysis was carried out using Student's t-test (SigmaStat software; Jandel, San Rafael, CA).



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  		FIG. 1. Regulation of FFN levels in human amnion epithelial cells and fibroblasts by DEX. Amnion epithelial cells (A) and fibroblasts (B) isolated from a human amnion at term were maintained in SCS medium with and without 100 nM DEX. Culture media were collected at the indicated times, and levels of FFN were determined by ELISA. Results from a representative experiment are expressed as a mean ± SEM of determinations carried out in triplicate wells. SEMs that fell within the bar are not presented



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  		FIG. 3. Comparison of DEX effects on FFN concentration in amnion epithelial cells and amnion fibroblasts isolated from human and baboon amnion at term. Cumulative results are presented for pooled data obtained from experiments in which amnion epithelial cells (AEC) and amnion fibroblasts (AMF) isolated from human (n = 4) and baboon (n = 4) amnion were maintained for 6–9 days in SCS medium with and without 100 nM DEX. Levels of FFN in culture media were determined by ELISA, and the FFN value for DEX-treated cells were normalized to control. Results are expressed as a mean ± SEM. *P < 0.01 vs. control; **P < 0.05 vs. control



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  		FIG. 4. Effect of DEX treatment on FFN production in cytotrophoblasts and fibroblasts isolated from human term placentas. Cytotrophoblasts (A) and fibroblasts (B) isolated from a human term placenta were maintained for the indicated times in SCS medium with and without 100 nM DEX. Levels of FFN in culture media were determined in triplicate wells by ELISA and are expressed as a mean ± SEM

Human subjects and animal care Human amnion (n = 6) and placental tissue (n = 4) were obtained from pregnancies with normally grown, singleton fetus delivered by cesarean section at term. The study protocol was approved by the institutional review board committee at New York University School of Medicine. Baboon amnion tissue was obtained from animals delivered in the third trimester by cesarean section (n = 6) in the Laboratory for Pregnancy and Newborn Research Laboratory at Cornell University in compliance with institutional protocols for animal care as previously described [7]. Baboon amnions were shipped on ice to New York University School of Medicine for cell isolation. The time from tissue procurement to initiation of cell isolation was approximately 6 h.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
DEX-Mediated Regulation of FN Expression in Human and Baboon Amnion Cells

Primary cultures of amnion epithelial cells and fibroblasts isolated from human and baboon term amnion were maintained for up to 9 days in SCS medium with and without 100 nM DEX, and levels of FFN in culture media were determined by ELISA. Results from representative experiments are shown in Figures 1 and 2. We observed that DEX treatment down-regulated FFN levels in human and baboon amnion epithelial cells to 5–40% of control levels. Conversely, DEX treatment increased FFN levels in amnion fibroblasts to 120–220% of control levels on Days 6 and 8.

Statistical analysis of cumulative data obtained from 4 experiments indicated that DEX treatment significantly decreased FFN levels in human and baboon amnion epithelial cells to 35 ± 9% and 37 ± 4% of control levels, respectively (P < 0.01, Fig. 3). Conversely, DEX treatment increased FFN levels in human and baboon fibroblast cultures to 156 ± 12% and 193 ± 37% of control values, respectively (P < 0.05). These results suggest that GC differentially regulates FFN expression in epithelial and mesenchymal cells isolated from human and nonhuman primate amnion.

Effects of DEX Treatment on FFN Levels in Placental Cells

To test the effects of DEX on placental FFN expression, cytotrophoblasts and fibroblasts were isolated from a human term placenta and were maintained in SCS medium with and without 100 nM DEX for the indicated times (Fig. 4). Levels of FFN in cytotrophoblast culture media were down-regulated to 5–30% of control levels by a 2- or 4-day treatment with DEX. Since cytotrophoblasts differentiate to syncytiotrophoblasts after 72 h in culture [26, 27], this indicated that DEX suppressed FFN levels in both cytotrophoblasts and syncytiotrophoblasts. In sharp contrast, DEX treatment increased FFN expression in placental fibroblasts to 130–220% of control levels between 3 and 10 days of culture (Fig. 4). Statistical analysis of cumulative data from 3 independent experiments revealed that DEX treatment significantly decreased FFN expression in cytotrophoblasts to 20 ± 6% of the level control (P < 0.01) and increased FFN levels in placental fibroblasts to 226 ± 2% of control (P < 0.01).

GC-Mediated Regulation of FN mRNA in Human Amnion and Placental Cells

Consistent with the FFN protein data described above, DEX treatment down-regulated expression of FN mRNA to approximately 30% of control levels in amnion epithelial cells and cytotrophoblasts as normalized to levels of GAPDH mRNA (Fig. 5). Conversely, DEX treatment up-regulated levels of FN mRNA to approximately 250% of control levels in amnion and placental fibroblasts (Fig. 5). Statistical analysis of cumulative data from 3–4 independent experiments revealed that DEX treatment significantly decreased levels of FN mRNA in amnion epithelial cells and cytotrophoblasts to 27 ± 13% of control (P < 0.01) and 16 ± 3% of control (P < 0.01), respectively. Conversely, analysis of cumulative mRNA results also revealed that DEX treatment significantly increased levels of FN mRNA in amnion fibroblasts to 288 ± 55% of control levels (P < 0.01). We noted that DEX treatment mediated a more modest increase in levels of FN mRNA in placental fibroblasts to 161 ± 47% of control levels that was not statistically significant (P = 0.26). In summary, our results indicate that GC treatment promotes differential effects on FN expression in the major epithelial and fibroblast cell types of amnion and placenta, and that these patterns of GC-mediated regulation are conserved in the human and nonhuman primate.



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  		FIG. 5. Effect of DEX treatment on levels of FN mRNA in cells isolated from human placenta and fetal membranes at term. Epithelial cells and fibroblasts isolated from a human amnion at term were maintained for 6 days in SCS medium with and without 100 nM DEX (A). Cytotrophoblasts and fibroblasts isolated from a human term placenta were maintained for 2 and 6 days, respectively, in SCS medium with and without 100 nM DEX (B). RNA was extracted from cells, and approximately 20 µg of total RNA was separated on an agarose gel containing formaldehyde. After transfer, Northern blots were concomitantly hybridized to 32P-labeled FN and GAPDH cDNAs. Results shown for amnion epithelial cells, amnion fibroblasts, and cytotrophoblasts depict a single experiment representing data obtained using 3 or 4 separate tissues. The Northern blot for placental fibroblasts is from 1 experiment using cells from 1 passage representing 3 identically conducted experiments from 3 different cell passages


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the current study we report that DEX treatment suppressed FFN protein levels in epithelial cells derived from human placenta and fetal membranes (i.e., cytotrophoblasts and amnion epithelial cells) whereas the stromal elements of these tissues showed enhanced FFN protein levels in response to GC treatment. It is of note that in this study and in previous studies [18, 19, 26], we observed that levels of FFN protein accurately reflected levels of FN mRNA in cells isolated from placenta and amnion. This is most likely attributable to the finding that virtually all FN protein expressed and released by placental and other fetal cells contains the oncofetal epitope [26].

In light of the similar structure of human and nonhuman primate amnion [28], we used cell culture techniques developed for human amnion cell isolation [24] for the isolation of amnion epithelial cells and fibroblasts from baboon amnion. Treatment of whole amnion with trypsin gently removes amnion epithelial cells from the amnion basal lamina as essentially a homogeneous preparation [29, 30]. Collagenase treatment of epithelial cell-denuded amnion releases underlying mesenchymal cells [24]. We observed similar effects of GC on FN expression in amnion cells isolated from baboon and human tissue, suggesting that patterns of GC responsiveness are conserved in human and nonhuman primates. The observation of lower cellular yields and FN production in baboon amnion cells may be attributed to the modest delay in tissue processing or may represent interspecies differences.

It is likely that amnion epithelial cells and fibroblasts contribute to the synthesis of major ECM protein components of the amnion basal lamina (laminin, FN, collagen IV) [15]. It is likely that the synthesis of interstitial collagens in amnion (types I and III) is a primary function of amnion mesenchymal cells [24]. It is suggested that decreased levels of the collagen cross-linking enzyme lysyl oxidase [31], reflecting a lower density of mesenchymal cells in fetal membranes late in gestation, plays an important role in the reduction in tensile strength of fetal membranes that accompanies their premature rupture. Although in vitro results must be interpreted conservatively, our data do suggest that when GC levels are high in the third trimester [8], amnion mesenchymal cells will most likely play a more important role in FFN synthesis at this site. Furthermore, GC effects on FFN expression in amnion may be responsible in part for elevated cervico-vaginal levels of FFN observed in women at risk for preterm delivery [4], as well as the parturition-associated increase in FFN expression in fetal membranes [6, 7]. Our results may have important clinical implications in the face of the rising use of antenatal GC for the enhancement of fetal lung maturity [32]. GC therapy may alter the patterns of ECM protein expression in the amnion as well as tensile strength and may increase the risk of premature rupture of the fetal membranes.

Our previous results suggest that GC effects on FFN expression in cytotrophoblasts were not mediated by CRH [33], and therefore it is likely that parturition-dependent changes in FFN in placenta and fetal membranes are direct actions of GC and not of CRH. The GC effects on fetal membrane and placental ECM protein synthesis will be influenced by the tissue and cell type-specific expression of GC receptor and activity of 11ß-hydroxysteroid dehydrogenase (the enzyme that interconverts active cortisol and inactive cortisone), known components of placenta and fetal membranes [34–36]. It is not clear whether these determinants of GC action are altered in activity or distribution in association with parturition.

In conclusion, our results show that GC differentially modulates FFN expression in the major epithelial and mesenchymal cell types isolated from human and baboon fetal membranes and placenta, suggesting that GC may play an important role in remodeling of the ECM at these sites in association with parturition.



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  		FIG. 2. The effect of DEX treatment on FFN levels in epithelial cells and fibroblasts isolated from a baboon amnion. Epithelial cells (A) and fibroblasts (B) were isolated from a baboon amnion and were maintained in SCS medium in the presence and absence of 100 nM DEX. Levels of FFN in culture media from triplicate wells of a representative experiment were analyzed by ELISA and are expressed as a mean ± SEM


   ACKNOWLEDGMENTS
 
We would like to thank Dr. En-Yu Wang for technical assistance and Ron Maddock for help in preparation of this manuscript.


   FOOTNOTES
 
First decision: 20 October 1999.

1 These studies were supported in part through NIH grant HD 33909 (S.G.) and HD 21350 (P.W.N.). Back

2 Correspondence: Seth Guller, Dept. OB/GYN, NYU School of Medicine, 550 First Ave., New York, NY 10016. FAX: 212 263 5742; gulles01{at}mcrcr.med.nyu.edu Back

Accepted: January 14, 2000.

Received: September 27, 1999.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Hynes RO. The dynamic dialogue between cells and matrices: implications of fibronectin's elasticity. Proc Natl Acad Sci USA 1999; 96:2588–2590.[Free Full Text]
  2. Matsuura H, Hakomori SI. The oncofetal domain of fibronectin defined by the monoclonal antibody FDC-6: its presence in fibronectins from fetal and tumor tissues and its absence in those normal adult tissues and plasma. Proc Natl Acad Sci USA 1985; 82:6517–6521.[Abstract/Free Full Text]
  3. Matsuura H, Takio K, Titani K, Greene T, Levery SB, Salyan MKE, Hakomori SI. The oncofetal structure of human fibronectin defined by monoclonal antibody FDC-6. J Biol Chem 1988; 263:3314–3322.[Abstract/Free Full Text]
  4. Lockwood CJ, Senyei AE, Dische MR, Casal D, Shah KD, Thung SN, Jones LJ, Deligdisch L, Garite TJ. Fetal fibronectin in cervical and vaginal secretions as a predictor of preterm delivery. N Engl J Med 1991; 325:669–674.[Abstract]
  5. Feinberg RF, Kliman HJ, Lockwood CJ. Is oncofetal fibronectin a trophoblast glue for implantation? Am J Pathol 1991; 138:537–543.[Abstract]
  6. Mecenas CA, Giussani DA, Owiny JR, Jenkins SL, Wu XX, Honnebier BOM, Lockwood CJ, Kong L, Guller S, Nathanielsz PW. Production of premature delivery in pregnant rhesus monkeys by androstenedione infusion. Nat Med 1996; 2:443–448.[CrossRef][Medline]
  7. Nathanielsz PW, Jenkins SL, Tame JD, Winter JA, Guller S, Giussani DA. Local paracrine effects of estradiol are central to parturition in the rhesus monkey. Nat Med 1998; 4:456–459.[CrossRef][Medline]
  8. Dorr HG, Heller A, Versmold HT, Sippel WG, Herrmann M, Bidlingmaier F, Knorr D. Longitudinal study of progestins, mineralocorticoids, and glucocorticoids throughout human pregnancy. J Clin Endocrinol Metab 1989; 68:863–868.[Abstract/Free Full Text]
  9. Brooks AN, Challis JRG. Regulation of the hypothalamic-pituitary-adrenal axis in birth. Can J Physiol Pharmacol 1988; 66:1106–1112.[Medline]
  10. Wolfe CA, Patel SP, Linton EA, Campbell EA, Anderson J, Dornhorst A, Lowry PJ, Jones MT. Plasma CRH in abnormal pregnancy. Br J Obstet Gynaecol 1988; 95:1003–1006.[Medline]
  11. McClean M, Bisits A, Davies J, Woods R, Lowry P, Smith R. A placental clock controlling the length of human pregnancy. Nat Med 1995; 1:460–463.[CrossRef][Medline]
  12. Jones SA, Challis JR. Local stimulation of prostaglandin production by corticotropin-releasing hormone in human fetal membranes and placenta. Biochem Biophys Res Commun 1989; 159:192–198.[CrossRef][Medline]
  13. Frim D, Emanuel R, Robinson B, Majzoub JA. Characterization and gestational regulation of corticotrophin releasing hormone messenger RNA in human placenta. J Clin Invest 1988; 82:287–292.
  14. Jones SA, Brooks AN, Challis JRG. Steroids modulate corticotropin-releasing hormone production in human fetal membranes and placenta. J Clin Endocrinol Metab 1989; 68:825–830.[Abstract/Free Full Text]
  15. Bryant-Greenwood GD. The extracellular matrix of the human fetal membranes: structure and function. Placenta 1998; 19:1–11.[Medline]
  16. Earl E, Estlin C, Bulmer JN. Fibronectin and laminin in the early human placenta. Placenta 1990; 11:223–231.[CrossRef][Medline]
  17. Damsky CH, Fitzgerald ML, Fisher SJ. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest 1992; 89:210–222.
  18. Aplin JD, Haigh T, Jones CJ, Church HJ, Vicovac L. Development of cytotrophoblast columns from explanted first-trimester human placental villi: role of fibronectin and integrin {alpha}5ß1. Biol Reprod 1999; 60:828–838.[Abstract/Free Full Text]
  19. Guller S, Markiewicz L, Wozniak R, Burnham JM, Wang E-Y, Kaplan P, Lockwood CJ. Developmental regulation of glucocorticoid-mediated effects on extracellular matrix protein expression in the human placenta. Endocrinology 1994; 134:2064–2071.[Abstract]
  20. Guller S, Kong L, Wozniak R, Lockwood CJ. Reduction of extracellular matrix protein expression in human amnion epithelial cells by glucocorticoids: a potential role in preterm rupture of the fetal membranes. J Clin Endocrinol Metab 1995; 80:2244–2250.[Abstract]
  21. Yoon DY, Ma Y, Krikun G, Lockwood CJ, LaChapelle L, Guller S. Glucocorticoid effects in the human placenta: evidence that dexamethasone-mediated inhibition of fibronectin expression in cytotrophoblasts involves a protein intermediate. J Clin Endocrinol Metab 1998; 83:632–637.[Abstract/Free Full Text]
  22. Schwarzbauer JE. Fibronectins: from gene to protein. Curr Opin Cell Biol 1991; 3:786–791.[CrossRef][Medline]
  23. Dean DC, Newby RF, Bourgeois S. Regulation of fibronectin biosynthesis by dexamethasone, transforming growth factor-ß, and cAMP in human cell lines. J Cell Biol 1988; 106:2159–2170.[Abstract/Free Full Text]
  24. Casey ML, MacDonald PC. Interstitial collagen synthesis and processing in human amnion: a property of the mesenchymal cells. Biol Reprod 1996; 55:1253–1260.[Abstract]
  25. Fant ME, Nanu L. Human placental endothelin: expression of endothelin-1 mRNA by human placental fibroblasts in culture. Mol Cell Endocrinol 1995; 109:119–123.[CrossRef][Medline]
  26. Guller S, LaCroix N, Krikun G, Wozniak R, Markiewicz L, Wang E-Y, Kaplan P, Lockwood CJ. Steroid regulation of oncofetal fibronectin expression in human cytotrophoblasts. J Steroid Biochem Mol Biol 1993; 46:1–10.[CrossRef][Medline]
  27. Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Strauss III JF. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 1986; 118:1567–1582.[Abstract/Free Full Text]
  28. Houston ML, Kraemer DC, Gasser RF, Bollert JA. Placenta. In: Hendrickx AG (ed.), Embryology of the Baboon. London: The University of Chicago Press; 1971:153–172.
  29. Alitalo K, Kurkinen M, Vaheri A, Krieg T, Timpl R. Extracellular matrix components synthesized by human amniotic epithelial cells in culture. Cell 1980; 19:1053–1062.[CrossRef][Medline]
  30. Okita JR, Sagawa N, Casey ML, Snyder JM. A comparison of human amnion tissue and amnion cells in primary culture by morphological and biochemical criteria. In Vitro 1983; 19:117–126.[Medline]
  31. Casey ML, MacDonald PC. Lysyl oxidase (ras recision gene) expression in human amnion: ontogeny and cellular localization. J Clin Endocrinol Metab 1997; 82:167–172.[Abstract/Free Full Text]
  32. NIH Consensus Development Panel on the Effect of Corticosteroids for Fetal Maturation on Perinatal Outcomes. Effect of corticosteroids for fetal maturation on perinatal outcomes. JAMA 1995; 273:413–418.[Abstract/Free Full Text]
  33. Guller S, Wozniak R, Liebman MI, Lockwood CJ. Negative regulation of placental fibronectin expression by glucocorticoids and cyclic adenosine 3',5'-monophosphate. Ann N Y Acad Sci 1994; 734:132–142.[Medline]
  34. Giannopoulos G, Jackson K, Tulchinsky D. Specific glucocorticoid binding in human uterine tissues, placenta and fetal membranes. J Steroid Biochem 1983; 19:1375–1378.[CrossRef][Medline]
  35. Patel FA, Sun K, Challis JR. Local modulation by 11ß-hydroxysteroid dehydrogenase of glucocorticoid effects on the activity of 15-hydroxyprostaglandin dehydrogenase in human chorion and placental trophoblast cells. J Clin Endocrinol Metab 1999; 84:395–400.[Abstract/Free Full Text]
  36. Pepe GJ, Waddell BJ, Burch MG, Albrecht ED. Interconversion of cortisol and cortisone in the baboon placenta at midgestation: expression of 11ß-hydroxysteroid dehydrogenase type 1 messenger RNA. J Steroid Biochem Mol Biol 1996; 58:403–410.[CrossRef][Medline]



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