Progestin and thrombin regulate tissue factor expression in human term decidual cells - PubMed (original) (raw)
Progestin and thrombin regulate tissue factor expression in human term decidual cells
C J Lockwood et al. J Clin Endocrinol Metab. 2009 Jun.
Erratum in
- J Clin Endocrinol Metab. 2009 Jul;94(7):2674
- J Clin Endocrinol Metab. 2009 Sep;94(9):3620
Abstract
Context: Perivascular cell membrane-bound tissue factor (TF) initiates hemostasis via thrombin generation. The identity and potential regulation of TF-expressing cells at the human maternal-fetal interface that confers hemostatic protection during normal and preterm delivery is unclear.
Objectives: The objective of the study were to identify TF-expressing cells at the maternal-fetal interface in term and preterm decidual sections by immunohistochemistry and evaluate progestin, thrombin, TNF-alpha, and IL-1beta effects on TF expression by cultured human term decidual cells (DCs).
Interventions and main outcome measures: Serial placental sections were immunostained for TF. Leukocyte-free term DC monolayers were incubated with 10(-8) M estradiol (E2) or E2 plus 10(-7) M medroxyprogestrone acetate (MPA) +/- thrombin or TNF-alpha or IL-1beta. ELISA and Western blotting assessed TF in cell lysates. Quantitative real-time RT-PCR measured TF mRNA levels.
Results: Immunolocalized TF in DC membranes in preterm and term placental sections displayed higher Histologic Scores than villous mesenchymal cells (P < 0.05). TF was undetected in interstitial or extravillous trophoblasts. Compared with DCs incubated with E2, MPA and 2.5 U/ml thrombin each doubled TF levels (P < 0.05) and E2 + MPA + thrombin further doubled TF levels (P < 0.05), whereas TNF-alpha and IL-1beta were ineffective. Western blotting confirmed the ELISA results. Quantitative RT-PCR revealed corresponding changes in TF mRNA levels.
Conclusions: In human term placental sections, DC-expressed TF exceeds that of other cell types at the maternal-fetal interface and is localized at the cell membranes in which it can bind to factor VII and meet the hemostatic demands of labor and delivery via thrombin formation. Unlike the general concept that TF is constitutive in cells that highly express it, MPA and thrombin significantly enhanced TF expression in term DC monolayers.
Figures
Figure 1
Immunohistochemical analysis of tissue factor expression at the decidual/placental interface. Serial sections of decidual basalis specimens were immunostained for TF and vimentin, as shown in an idiopathic preterm specimen (A, TF; B, vimentin). DCs (arrows), identified by positive vimentin staining, exhibited strong perimembranous TF staining. TF staining was virtually absent in interstitial trophoblasts (arrowheads). Similar results were seen in term specimens (C). Placental villi exhibited moderate TF staining in the mesoderm (M), in which the staining was primarily localized to perivascular adventitia (small arrows), as shown in a preterm specimen (D). Syncytiotrophoblasts (S) and cytotrophoblasts (C) exhibited no TF staining. Similar results were seen in term specimens (not shown). Negative control immunostaining using a nonspecific isotype-matched antibody revealed no positive signals (E). TF staining intensity (F); bars indicate HSCORE mean ±
sem
) among cell types was highest in DCs (*, vs. interstitial trophoblasts and the villous mesoderm of the same specimen group, P < 0.05), with moderate staining in the villous mesoderm (†, vs. interstitial trophoblasts of the same specimen group, P < 0.05). There were no significant differences in HSCOREs between specimen groups.
Figure 2
Effects of MPA and thrombin on TF expression in DCs. Term DCs were primed in E2 or E2 + MPA and then switched to DM with corresponding steroids ± 2.5 U/ml thrombin (Th) for 24 h. ELISAs were performed for TF in cell lysates with the results normalized to total cell protein: n = 10 (mean ±
sem
). *, vs. E2; **, vs. E2 + MPA and E2 + Th; P < 0.05.
Figure 3
Concentration-response effects of thrombin on TF expression in DCs. Term DCs were primed in E2 + MPA and then switched to DM with steroids ± thrombin (Th) at varying concentrations in units per milliliter for 24 h. ELISAs were performed for TF in cell lysates and measured by ELISA. Results are normalized to total cell protein (n = 3, mean ±
sem)
. *, vs. E2 + MPA; **, vs. + Th 0.25; P < 0.05.
Figure 4
Effects of thrombin, IL-1β, and TNF-α on TF expression in DCs. Term DCs were primed in E2 or E2 + MPA and then switched to DM with corresponding steroids ± 2.5 U/ml thrombin (Th) or 1 ng/ml of TNF-α or IL-1β for 24 h. ELISAs were performed for TF in cell lysates with the results normalized to total cell protein: n = 8 (mean ±
sem
). *, vs. E2 + MPA; P < 0.05.
Figure 5
Western blot of thrombin effects on TF output by DCs. Term DCs were primed in E2 or E2 + MPA and then switched to DM with corresponding steroids ± 2.5 U/ml thrombin (Th) for 24 h. Cell lysates were subjected to Western blotting after SDS-PAGE. See Patients and Methods for details.
Figure 6
Effects of MPA and thrombin on TF mRNA expression in DCs. Term DCs were primed in E2 or E2 + MPA and then switched to DM with corresponding steroids ± 2.5 U/ml thrombin (Th) for 6 h. TF mRNA was measured by quantitative real-time RT-PCR and normalized to β-actin mRNA; n = 9 (mean ±
sem
). *, vs. E2; P < 0.05.
Similar articles
- Progestin-inflammatory cytokine interactions affect matrix metalloproteinase-1 and -3 expression in term decidual cells: implications for treatment of chorioamnionitis-induced preterm delivery.
Oner C, Schatz F, Kizilay G, Murk W, Buchwalder LF, Kayisli UA, Arici A, Lockwood CJ. Oner C, et al. J Clin Endocrinol Metab. 2008 Jan;93(1):252-9. doi: 10.1210/jc.2007-1538. Epub 2007 Oct 16. J Clin Endocrinol Metab. 2008. PMID: 17940116 Free PMC article. - Progestin suppresses thrombin- and interleukin-1beta-induced interleukin-11 production in term decidual cells: implications for preterm delivery.
Cakmak H, Schatz F, Huang ST, Buchwalder L, Rahman M, Arici A, Lockwood CJ. Cakmak H, et al. J Clin Endocrinol Metab. 2005 Sep;90(9):5279-86. doi: 10.1210/jc.2005-0210. Epub 2005 Jul 5. J Clin Endocrinol Metab. 2005. PMID: 15998775 - Progestin inhibits and thrombin stimulates the plasminogen activator/inhibitor system in term decidual stromal cells: implications for parturition.
Norwitz ER, Snegovskikh V, Schatz F, Foyouzi N, Rahman M, Buchwalder L, Lee HJ, Funai EF, Buhimschi CS, Buhimschi IA, Lockwood CJ. Norwitz ER, et al. Am J Obstet Gynecol. 2007 Apr;196(4):382.e1-8. doi: 10.1016/j.ajog.2007.02.035. Am J Obstet Gynecol. 2007. PMID: 17403427 - Involvement of human decidual cell-expressed tissue factor in uterine hemostasis and abruption.
Lockwood CJ, Paidas M, Murk WK, Kayisli UA, Gopinath A, Huang SJ, Krikun G, Schatz F. Lockwood CJ, et al. Thromb Res. 2009 Nov;124(5):516-20. doi: 10.1016/j.thromres.2009.07.017. Epub 2009 Aug 31. Thromb Res. 2009. PMID: 19720393 Free PMC article. Review. - Progestin-regulated expression of tissue factor in decidual cells: implications in endometrial hemostasis, menstruation and angiogenesis.
Schatz F, Krikun G, Caze R, Rahman M, Lockwood CJ. Schatz F, et al. Steroids. 2003 Nov;68(10-13):849-60. doi: 10.1016/s0039-128x(03)00139-9. Steroids. 2003. PMID: 14667977 Review.
Cited by
- miR-93/106b and their host gene, MCM7, are differentially expressed in leiomyomas and functionally target F3 and IL-8.
Chuang TD, Luo X, Panda H, Chegini N. Chuang TD, et al. Mol Endocrinol. 2012 Jun;26(6):1028-42. doi: 10.1210/me.2012-1075. Epub 2012 May 3. Mol Endocrinol. 2012. PMID: 22556343 Free PMC article. - Characterization of the myometrial transcriptome and biological pathways of spontaneous human labor at term.
Mittal P, Romero R, Tarca AL, Gonzalez J, Draghici S, Xu Y, Dong Z, Nhan-Chang CL, Chaiworapongsa T, Lye S, Kusanovic JP, Lipovich L, Mazaki-Tovi S, Hassan SS, Mesiano S, Kim CJ. Mittal P, et al. J Perinat Med. 2010 Nov;38(6):617-43. doi: 10.1515/jpm.2010.097. Epub 2010 Jul 14. J Perinat Med. 2010. PMID: 20629487 Free PMC article. - The implication of aberrant GM-CSF expression in decidual cells in the pathogenesis of preeclampsia.
Huang SJ, Zenclussen AC, Chen CP, Basar M, Yang H, Arcuri F, Li M, Kocamaz E, Buchwalder L, Rahman M, Kayisli U, Schatz F, Toti P, Lockwood CJ. Huang SJ, et al. Am J Pathol. 2010 Nov;177(5):2472-82. doi: 10.2353/ajpath.2010.091247. Epub 2010 Sep 9. Am J Pathol. 2010. PMID: 20829438 Free PMC article. - Molecular Changes on Maternal-Fetal Interface in Placental Abruption-A Systematic Review.
Bączkowska M, Zgliczyńska M, Faryna J, Przytuła E, Nowakowski B, Ciebiera M. Bączkowska M, et al. Int J Mol Sci. 2021 Jun 21;22(12):6612. doi: 10.3390/ijms22126612. Int J Mol Sci. 2021. PMID: 34205566 Free PMC article. - Abruption-induced preterm delivery is associated with thrombin-mediated functional progesterone withdrawal in decidual cells.
Lockwood CJ, Kayisli UA, Stocco C, Murk W, Vatandaslar E, Buchwalder LF, Schatz F. Lockwood CJ, et al. Am J Pathol. 2012 Dec;181(6):2138-48. doi: 10.1016/j.ajpath.2012.08.036. Epub 2012 Oct 9. Am J Pathol. 2012. PMID: 23058370 Free PMC article.
References
- Bell SC 1990 Decidualization and relevance to menstruation. In: D'Arcangues C, Fraser IS, Newton JR, Odlind V, eds. Contraception and mechanisms of endometrial bleeding. Cambridge, UK: Cambridge University Press; 188
- Tabanelli S, Tang B, Gurpide E 1992 In vitro decidualization of human endometrial stromal cells. J Steroid Biochem Mol Biol 42:337–344 - PubMed
- Lockwood CJ, Krikun G, Papp C, Toth-Pal E, Markiewicz L, Wang EY, Kerenyi T, Zhou X, Hausknecht V, Papp Z 1994 The role of progestationally regulated stromal cell tissue factor and type-1 plasminogen activator inhibitor (PAI-1) in endometrial hemostasis and menstruation. Ann NY Acad Sci 734:57–79 - PubMed
- Lockwood CJ, Nemerson Y, Guller S, Krikun G, Alvarez M, Hausknecht V, Gurpide E, Schatz F 1993 Progestational regulation of human endometrial stromal cell tissue factor expression during decidualization. J Clin Endocrinol Metab 76:231–236 - PubMed
- Runic R, Schatz F, Krey L, Demopoulos R, Thung S, Wan L, Lockwood CJ 1997 Alterations in endometrial stromal cell tissue factor protein and messenger ribonucleic acid expression in patients experiencing abnormal uterine bleeding while using Norplant-2 contraception. J Clin Endocrinol Metab 82:1983–1988 - PubMed
Publication types
MeSH terms
Substances
Grants and funding
- R01 HD033937/HD/NICHD NIH HHS/United States
- R01 HL070004/HL/NHLBI NIH HHS/United States
- 1 R01 HL070004-04/HL/NHLBI NIH HHS/United States
- 2 R01HD33937-05/HD/NICHD NIH HHS/United States
LinkOut - more resources
Full Text Sources
Miscellaneous