Molecular Changes on Maternal–Fetal Interface in Placental Abruption—A Systematic Review
Abstract
:1. Introduction
1.1. Placental Abruption—Overview and Epidemiology
1.2. Placental Abruption—Pathophysiology
2. Material and Methods
3. Results
3.1. Molecular Effects of Thrombin in Placental Abruption
3.1.1. Thrombin-Induced Myometrial Contractions
3.1.2. Thrombin-Induced Fetal Membrane Weakening
3.2. Inflammation-Derived Pathways in Placental Abruption
3.3. Decidual Immunoreactivity
3.4. Links between Placental Abruption and Preterm Premature Rupture of Membranes
3.5. The Role of Tissue Factor in Placental Abruption
3.6. The Role of Progesterone in Placental Abruption
4. Limitations and Risk of Bias Assessment
5. Conclusions and Perspectives
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Tikkanen, M. Placental abruption: Epidemiology, risk factors and consequences. Acta Obstet. Gynecol. Scand. 2011, 90, 140–149. [Google Scholar] [CrossRef]
- Schmidt, P.; Skelly, C.L.; Raines, D.A. Placental Abruption; Statpearls: Treasure Island, FL, USA, 2020. [Google Scholar]
- Ananth, C.V.; Keyes, K.M.; Hamilton, A.; Gissler, M.; Wu, C.; Liu, S.; Luque-Fernandez, M.A.; Skjærven, R.; Williams, M.A.; Tikkanen, M.; et al. An International Contrast of Rates of Placental Abruption: An Age-Period-Cohort Analysis. PLoS ONE 2015, 10, e0125246. [Google Scholar] [CrossRef] [PubMed]
- Hossain, N.; Khan, N.; Sultana, S.S.; Khan, N. Abruptio placenta and adverse pregnancy outcome. J. Pak. Med. Assoc. 2010, 60, 443–446. [Google Scholar] [PubMed]
- Ghaheh, H.S.; Feizi, A.; Mousavi, M.; Sohrabi, D.; Mesghari, L.; Hosseini, Z. Risk factors of placental abruption. J. Res. Med. Sci. 2013, 18, 422–426. [Google Scholar] [PubMed]
- Sheiner, E.; Shoham-Vardi, I.; Hallak, M.; Hadar, A.; Gortzak-Uzan, L.; Katz, M.; Mazor, M. Placental abruption in term pregnancies: Clinical significance and obstetric risk factors. J. Matern. Fetal Neonatal Med. 2003, 13, 45–49. [Google Scholar] [CrossRef]
- Downes, K.L.; Grantz, K.L.; Shenassa, E.D. Maternal, Labor, Delivery, and Perinatal Outcomes Associated with Placental Abruption: A Systematic Review. Am. J. Perinatol. 2017, 34, 935–957. [Google Scholar] [CrossRef]
- Lykke, J.A.; Paidas, M.J.; Langhoff-Roos, J. Recurring Complications in Second Pregnancy. Obstet. Gynecol. 2009, 113, 1217–1224. [Google Scholar] [CrossRef]
- Pariente, G.; Shoham-Vardi, I.; Kessous, R.; Sherf, M.; Sheiner, E. Placental Abruption as a Significant Risk Factor for Long-term Cardiovascular Mortality in a Follow-up Period of More Than a Decade. Paediatr. Périnat. Epidemiol. 2014, 28, 32–38. [Google Scholar] [CrossRef]
- Li, Y.; Tian, Y.; Liu, N.; Chen, Y.; Wu, F. Analysis of 62 placental abruption cases: Risk factors and clinical outcomes. Taiwan. J. Obstet. Gynecol. 2019, 58, 223–226. [Google Scholar] [CrossRef]
- Kawanishi, Y.; Yoshioka, E.; Saijo, Y.; Itoh, T.; Miyamoto, T.; Sengoku, K.; Ito, Y.; Ito, S.; Miyashita, C.; Araki, A.; et al. The relationship between prenatal psychological stress and placental abruption in Japan, The Japan Environment and Children’s Study (JECS). PLoS ONE 2019, 14, e0219379. [Google Scholar] [CrossRef] [Green Version]
- Chahal, H.S.; Gelaye, B.; Mostofsky, E.; Sanchez, S.E.; Mittleman, M.A.; Maclure, M.; Pacora, P.; Torres, J.A.; Romero, R.; Ananth, C.V.; et al. Physical Exertion Immediately Prior to Placental Abruption: A Case-Crossover Study. Am. J. Epidemiol. 2018, 187, 2073–2079. [Google Scholar] [CrossRef] [Green Version]
- Workalemahu, T.; Enquobahrie, D.A.; Gelaye, B.; Sanchez, S.E.; Garcia, P.J.; Tekola-Ayele, F.; Hajat, A.; Thornton, T.A.; Ananth, C.V.; Williams, M.A. Genetic variations and risk of placental abruption: A genome-wide association study and meta-analysis of genome-wide association studies. Placenta 2018, 66, 8–16. [Google Scholar] [CrossRef] [PubMed]
- Ananth, C.V. Ischemic placental disease: A unifying concept for preeclampsia, intrauterine growth restriction, and placental abruption. Semin. Perinatol. 2014, 38, 131–132. [Google Scholar] [CrossRef]
- Ananth, C.V.; Smulian, J.C.; Vintzileos, A.M. Ischemic placental disease: Maternal versus fetal clinical presentations by gestational age. J. Matern. Fetal Neonatal Med. 2010, 23, 887–893. [Google Scholar] [CrossRef]
- Geldenhuys, J.; Rossouw, T.M.; Lombaard, H.A.; Ehlers, M.M.; Kock, M.M. Disruption in the Regulation of Immune Responses in the Placental Subtype of Preeclampsia. Front. Immunol. 2018, 9, 1659. [Google Scholar] [CrossRef]
- Wicherek, L. The role of the endometrium in the regulation of immune cell activity. Front. Biosci. 2008, 13, 1018–1035. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Norman, J.E.; Bollapragada, S.; Yuan, M.; Nelson, S.M. Inflammatory pathways in the mechanism of parturition. BMC Pregnancy Childbirth 2007, 7, S7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gomez-Lopez, N.; Stlouis, D.; Lehr, M.A.; Sanchez-Rodriguez, E.N.; Arenas-Hernandez, M. Immune cells in term and preterm labor. Cell. Mol. Immunol. 2014, 11, 571–581. [Google Scholar] [CrossRef] [Green Version]
- Wicherek, L.; Klimek, M.; Dutsch-Wicherek, M.; Kolodziejski, L.; Skotniczny, K. The molecular changes during placental detachment. Eur. J. Obstet. Gynecol. Reprod. Biol. 2006, 125, 171–175. [Google Scholar] [CrossRef] [PubMed]
- Mhatre, M.V.; Potter, J.A.; Lockwood, C.J.; Krikun, G.; Abrahams, V.M. Thrombin Augments LPS-Induced Human Endometrial Endothelial Cell Inflammation via PAR1 Activation. Am. J. Reprod. Immunol. 2016, 76, 29–37. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, F.; Zheng, Q.; Jin, L. Dynamic Function and Composition Changes of Immune Cells during Normal and Pathological Pregnancy at the Maternal-Fetal Interface. Front. Immunol. 2019, 10, 2317. [Google Scholar] [CrossRef] [Green Version]
- Tang, Z.; Abrahams, V.M.; Mor, G.; Guller, S. Placental Hofbauer cells and complications of pregnancy. Ann. N. Y. Acad. Sci. 2011, 1221, 103–108. [Google Scholar] [CrossRef] [Green Version]
- Goldstein, J.A.; Gallagher, K.; Beck, C.; Kumar, R.; Gernand, A.D. Maternal-Fetal Inflammation in the Placenta and the Developmental Origins of Health and Disease. Front. Immunol. 2020, 11, 531543. [Google Scholar] [CrossRef] [PubMed]
- Steinborn, A.; Rebmann, V.; Scharf, A.; Sohn, C.; Grosse-Wilde, H. Soluble HLA-DR levels in the maternal circulation of normal and pathologic pregnancy. Am. J. Obstet. Gynecol. 2003, 188, 473–479. [Google Scholar] [CrossRef]
- Wilczyński, J.R.; Tchórzewski, H.; Banasik, M.; Głowacka, E.; Wieczorek, A.; Lewkowicz, P.; Malinowski, A.; Szpakowski, M.; Wilczyński, J. Lymphocyte subset distribution and cytokine secretion in third trimester decidua in normal pregnancy and preeclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 2003, 109, 8–15. [Google Scholar] [CrossRef]
- Lockwood, C.J.; Toti, P.; Arcuri, F.; Paidas, M.; Buchwalder, L.; Krikun, G.; Schatz, F. Mechanisms of Abruption-Induced Premature Rupture of the Fetal Membranes: Thrombin-Enhanced Interleukin-8 Expression in Term Decidua. Am. J. Pathol. 2005, 167, 1443–1449. [Google Scholar] [CrossRef]
- Ananth, C.V.; Oyelese, Y.; Prasad, V.; Getahun, D.; Smulian, J.C. Evidence of placental abruption as a chronic process: Associations with vaginal bleeding early in pregnancy and placental lesions. Eur. J. Obstet. Gynecol. Reprod. Biol. 2006, 128, 15–21. [Google Scholar] [CrossRef]
- Wicherek, L.; Galazka, K.; Lazar, A. RCAS1 Decidual Immunoreactivity during Placental Abruption: Immune Cell Presence and Activity. Am. J. Reprod. Immunol. 2007, 58, 46–55. [Google Scholar] [CrossRef]
- Buhimschi, C.S.; Schatz, F.; Krikun, G.; Buhimschi, I.A.; Lockwood, C.J. Novel insights into molecular mechanisms of abruption-induced preterm birth. Expert Rev. Mol. Med. 2010, 12, e35. [Google Scholar] [CrossRef] [Green Version]
- PrabhuDas, M.; Bonney, E.; Caron, K.; Dey, S.; Erlebacher, A.; Fazleabas, A.; Fisher, S.; Golos, T.; Matzuk, M.; McCune, J.M.; et al. Immune mechanisms at the maternal-fetal interface: Perspectives and challenges. Nat. Immunol. 2015, 16, 328–334. [Google Scholar] [CrossRef]
- Zheng, D.; Liwinski, T.; Elinav, E. Inflammasome activation and regulation: Toward a better understanding of complex mechanisms. Cell Discov. 2020, 6, 36. [Google Scholar] [CrossRef] [PubMed]
- Slim, R.; Wallace, E.P. NLRP7 and the Genetics of Hydatidiform Moles: Recent Advances and New Challenges. Front. Immunol. 2013, 4, 242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- The Society of Gynecologic Oncology; American College of Obstetricians and Gynecologists and the Society for Maternal–Fetal Medicine; Cahill, A.G.; Beigi, R.; Heine, R.P.; Silver, R.M.; Wax, J.R. Placenta Accreta Spectrum. Am. J. Obstet. Gynecol. 2018, 219, B2–B16. [Google Scholar] [CrossRef] [Green Version]
- Jauniaux, E.; Burton, G.J. Pathophysiology of Placenta Accreta Spectrum Disorders: A Review of Current Findings. Clin. Obstet. Gynecol. 2018, 61, 743–754. [Google Scholar] [CrossRef]
- Rathbun, K.M.; Hildebrand, J.P. Placenta Abnormalities; Statpearls: Treasure Island, FL, USA, 2021. [Google Scholar]
- Perlman, N.C.; Carusi, D.A. Retained placenta after vaginal delivery: Risk factors and management. Int. J. Womens Health 2019, 11, 527–534. [Google Scholar] [CrossRef] [Green Version]
- Altshuler, G.; De Bault, L.E. Preliminary Report: Immunoperoxidase-Linked Human Placental Lactogen as a Histopathologic Index of Perinatal Morbidity and Mortality. Pediatr. Pathol. 1983, 1, 469–474. [Google Scholar] [CrossRef]
- Wang, C.H.; Schnoll, S.H. Prenatal cocaine use associated with down regulation of receptors in human placenta. Neurotoxicology Teratol. 1987, 9, 301–304. [Google Scholar] [CrossRef]
- Nakatsuka, M.; Asagiri, K.; Kimura, Y.; Kamada, Y.; Tada, K.; Kudo, T. Generation of peroxynitrite and apoptosis in placenta of patients with chorioamnionitis: Possible implications in placental abruption. Hum. Reprod. 1999, 14, 1101–1106. [Google Scholar] [CrossRef]
- Kuczyński, J.; Uszyński, W.; Zekanowska, E.; Soszka, T.; Uszyński, M. Tissue factor (TF) and tissue factor pathway inhibitor (TFPI) in the placenta and myometrium. Eur. J. Obstet. Gynecol. Reprod. Biol. 2002, 105, 15–19. [Google Scholar] [CrossRef]
- Rosen, T.; Schatz, F.; Kuczynski, E.; Lam, H.; Koo, A.B.; Lockwood, C.J. Thrombin-enhanced matrix metalloproteinase-1 expression: A mechanism linking placental abruption with premature rupture of the membranes. J. Matern. Fetal Neonatal Med. 2002, 11, 11–17. [Google Scholar] [CrossRef] [PubMed]
- Di Simone, N.; Maggiano, N.; Caliandro, D.; Riccardi, P.; Evangelista, A.; Carducci, B.; Caruso, A. Homocysteine Induces Trophoblast Cell Death with Apoptotic Features. Biol. Reprod. 2003, 69, 1129–1134. [Google Scholar] [CrossRef]
- Uszyński, M.; Perlik, M.; Uszyński, W.; Zekanowska, E. Urokinase plasminogen activator (uPA) and its receptor (uPAR) in gestational tissues; measurements and clinical implications. Eur. J. Obstet. Gynecol. Reprod. Biol. 2004, 114, 54–58. [Google Scholar] [CrossRef] [PubMed]
- Norwitz, E.R.; Snegovskikh, V.; Schatz, F.; Foyouzi, N.; Rahman, M.; Buchwalder, L.; Lee, H.J.; Funai, E.F.; Buhimschi, C.S.; Buhimschi, I.A.; et al. Progestin inhibits and thrombin stimulates the plasminogen activator/inhibitor system in term decidual stromal cells: Implications for parturition. Am. J. Obstet. Gynecol. 2007, 196, 382.e1–382.e8. [Google Scholar] [CrossRef] [PubMed]
- Galazka, K.; Pitynski, K.; Skret-Magierlo, J.; Mach, P.; Knafel, A.; Sikora, J.; Niemiec, T.; Dobrogowski, J.; Basta, A.; Wicherek, L. The Increase in Metallothionein and Ectopic Decidual Immunoreactivity with Respect to the Progression of Labor at Term and the Lack of Analogical Changes in Placental Abruption. Am. J. Reprod. Immunol. 2008, 60, 204–213. [Google Scholar] [CrossRef] [PubMed]
- Snegovskikh, V.V.; Schatz, F.; Arcuri, F.; Toti, P.; Kayisli, U.A.; Murk, W.; Guoyang, L.; Lockwood, C.J.; Norwitz, E.R. Intra-Amniotic Infection Upregulates Decidual Cell Vascular Endothelial Growth Factor (VEGF) and Neuropilin-1 and -2 Expression: Implications for Infection-Related Preterm Birth. Reprod. Sci. 2009, 16, 767–780. [Google Scholar] [CrossRef] [PubMed]
- Avagliano, L.; Falleni, M.; Marconi, A.M.; Bulfoni, C.; Prada, A.; Barbera, A.F.; Doi, P.; Bulfamante, G.P. An imbalance of COX level is not related to placental abruption. J. Clin. Pathol. 2011, 64, 605–609. [Google Scholar] [CrossRef]
- Kumar, D.; Schatz, F.; Moore, R.M.; Mercer, B.M.; Rangaswamy, N.; Mansour, J.M.; Lockwood, C.J.; Moore, J.J. The effects of thrombin and cytokines upon the biomechanics and remodeling of isolated amnion membrane, in vitro. Placenta 2011, 32, 206–213. [Google Scholar] [CrossRef] [Green Version]
- Lockwood, C.J.; Kayisli, U.A.; Stocco, C.; Murk, W.; Vatandaslar, E.; Buchwalder, L.F.; Schatz, F. Abruption-Induced Preterm Delivery Is Associated with Thrombin-Mediated Functional Progesterone Withdrawal in Decidual Cells. Am. J. Pathol. 2012, 181, 2138–2148. [Google Scholar] [CrossRef] [Green Version]
- Puthiyachirakkal, M.; Lemerand, K.; Kumar, D.; Moore, R.; Philipson, E.; Mercer, B.M.; Mansour, J.M.; Hauguel-de Mouzon, S.; Moore, J.J. Thrombin weakens the amnion extracellular matrix (ECM) directly rather than through protease activated receptors. Placenta 2013, 34, 924–931. [Google Scholar] [CrossRef]
- Kumar, D.; Moore, R.M.; Nash, A.; Springel, E.; Mercer, B.M.; Philipson, E.; Mansour, J.M.; Moore, J.J. Decidual GM-CSF is a critical common intermediate necessary for thrombin and TNF induced in-vitro fetal membrane weakening. Placenta 2014, 35, 1049–1056. [Google Scholar] [CrossRef]
- Singh, N.; Herbert, B.; Sooranna, G.; Das, A.; Sooranna, S.R.; Yellon, S.M.; Johnson, M.R. Distinct preterm labor phenotypes have unique inflammatory signatures and contraction associated protein profiles. Biol. Reprod. 2019, 101, 1031–1045. [Google Scholar] [CrossRef] [PubMed]
- Nishimura, F.; Mogami, H.; Moriuchi, K.; Chigusa, Y.; Mandai, M.; Kondoh, E. Mechanisms of thrombin-Induced myometrial contractions: Potential targets of progesterone. PLoS ONE 2020, 15, e0231944. [Google Scholar] [CrossRef]
- Sinkey, R.G.; Guzeloglu-Kayisli, O.; Arlier, S.; Guo, X.; Semerci, N.; Moore, R.; Ozmen, A.; Larsen, K.; Nwabuobi, C.; Kumar, D.; et al. Thrombin-Induced Decidual Colony-Stimulating Factor-2 Promotes Abruption-Related Preterm Birth by Weakening Fetal Membranes. Am. J. Pathol. 2020, 190, 388–399. [Google Scholar] [CrossRef] [PubMed]
- Nagy, S.; Bush, M.; Stone, J.; Lapinski, R.H.; Gardo, S. Clinical significance of subchorionic and retroplacental hematomas detected in the first trimester of pregnancy. Obstet. Gynecol. 2003, 102, 94–100. [Google Scholar] [CrossRef]
- Norman, S.M.; Odibo, A.O.; Macones, G.A.; Dicke, J.M.; Crane, J.P.; Cahill, A.G. Ultrasound-Detected Subchorionic Hemorrhage and the Obstetric Implications. Obstet. Gynecol. 2010, 116, 311–315. [Google Scholar] [CrossRef]
- Tuuli, M.G.; Norman, S.M.; Odibo, A.O.; Macones, G.A.; Cahill, A.G. Perinatal Outcomes in Women With Subchorionic Hematoma: A systematic review and meta-analysis. Obstet. Gynecol. 2011, 117, 1205–1212. [Google Scholar] [CrossRef]
- Williams, M.A.; Mittendorf, R.; Lieberman, E.; Monson, R.R. Adverse infant outcomes associated with first-trimester vaginal bleeding. Obstet. Gynecol. 1991, 78, 14–18. [Google Scholar]
- Harger, J.H.; Hsing, A.W.; Tuomala, R.E.; Gibbs, R.S.; Mead, P.B.; Eschenbach, D.A.; Knox, G.E.; Polk, B.F. Risk factors for preterm premature rupture of fetal membranes: A multicenter case-control study. Am. J. Obstet. Gynecol. 1990, 163, 130–137. [Google Scholar] [CrossRef]
- Salafia, C.M.; López-Zeno, J.A.; Sherer, D.M.; Whittington, S.S.; Minior, V.K.; Vintzileos, A.M. Histologic evidence of old intrauterine bleeding is more frequent in prematurity. Am. J. Obstet. Gynecol. 1995, 173, 1065–1070. [Google Scholar] [CrossRef]
- Coughlin, S.R. Thrombin signalling and protease-activated receptors. Nature 2000, 407, 258–264. [Google Scholar] [CrossRef]
- Grand, R.J.; Turnell, A.S.; Grabham, P.W. Cellular consequences of thrombin-receptor activation. Biochem. J. 1996, 313, 353–368. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lockwood, C.J.; Krikun, G.; Aigner, S.; Schatz, F. Effects of thrombin on steroid-modulated cultured endometrial stromal cell fibrinolytic potential. J. Clin. Endocrinol. Metab. 1996, 81, 107–112. [Google Scholar] [CrossRef] [Green Version]
- Mogami, H.; Keller, P.W.; Shi, H.; Word, R.A. Effect of Thrombin on Human Amnion Mesenchymal Cells, Mouse Fetal Membranes, and Preterm Birth. J. Biol. Chem. 2014, 289, 13295–13307. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- O’Brien, M.; Morrison, J.J.; Smith, T.J. Expression of Prothrombin and Protease Activated Receptors in Human Myometrium during Pregnancy and Labor1. Biol. Reprod. 2008, 78, 20–26. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elovitz, M.A.; Baron, J.; Phillippe, M. The role of thrombin in preterm parturition. Am. J. Obstet. Gynecol. 2001, 185, 1059–1063. [Google Scholar] [CrossRef]
- Rosen, T.; Kuczynski, E.; O’Neill, L.M.; Funai, E.F.; Lockwood, C.J. Plasma levels of thrombin-antithrombin complexes predict preterm premature rupture of the fetal membranes. J. Matern. Fetal Med. 2001, 10, 297–300. [Google Scholar] [CrossRef]
- Chaiworapongsa, T.; Espinoza, J.; Yoshimatsu, J.; Kim, Y.M.; Bujold, E.; Edwin, S.; Yoon, B.H.; Romero, R. Activation of coagulation system in preterm labor and preterm premature rupture of membranes. J. Matern. Fetal Neonatal Med. 2002, 11, 368–373. [Google Scholar] [CrossRef] [PubMed]
- Phillippe, M.; Elovitz, M.; Saunders, T. Thrombin-stimulated uterine contractions in the pregnant and nonpregnant rat. J. Soc. Gynecol. Investig. 2001, 8, 260–265. [Google Scholar] [CrossRef]
- Lockwood, C.J.; Kumar, P.; Krikun, G.; Kadner, S.; Dubon, P.; Critchley, H.; Schatz, F. Effects of Thrombin, Hypoxia, and Steroids on Interleukin-8 Expression in Decidualized Human Endometrial Stromal Cells: Implications for Long-Term Progestin-Only Contraceptive-Induced Bleeding. J. Clin. Endocrinol. Metab. 2004, 89, 1467–1475. [Google Scholar] [CrossRef] [Green Version]
- MacKenzie, A.P.; Schatz, F.; Krikun, G.; Funai, E.F.; Kadner, S.; Lockwood, C.J. Mechanisms of abruption-induced premature rupture of the fetal membranes: Thrombin enhanced decidual matrix metalloproteinase-3 (stromelysin-1) expression. Am. J. Obstet. Gynecol. 2004, 191, 1996–2001. [Google Scholar] [CrossRef]
- Zhang, Y.; McCluskey, K.; Fujii, K.; Wahl, L.M. Differential regulation of monocyte matrix metalloproteinase and TIMP-1 production by TNF-alpha, granulocyte-macrophage CSF, and IL-1 beta through prostaglandin-dependent and -independent mechanisms. J. Immunol. 1998, 161, 3071–3076. [Google Scholar]
- Tomita, T.; Fujii, M.; Tokumaru, Y.; Imanishi, Y.; Kanke, M.; Yamashita, T.; Ishiguro, R.; Kanzaki, J.; Kameyama, K.; Otani, Y. Granulocyte-macrophage colony-stimulating factor upregulates matrix metalloproteinase-2 (MMP-2) and membrane type-1 MMP (MT1-MMP) in human head and neck cancer cells. Cancer Lett. 2000, 156, 83–91. [Google Scholar] [CrossRef]
- Gutschalk, C.M.; Yanamandra, A.K.; Linde, N.; Meides, A.; Depner, S.; Mueller, M.M. GM-CSF enhances tumor invasion by elevated MMP -2, -9, and -26 expression. Cancer Med. 2013, 2, 117–129. [Google Scholar] [CrossRef]
- Kleiner, D.E., Jr.; Stetler-Stevenson, W.G. Structural biochemistry and activation of matrix metalloproteases. Curr. Opin. Cell Biol. 1993, 5, 891–897. [Google Scholar] [CrossRef]
- Lockwood, C.J.; Nemerson, Y.; Guller, S.; Krikun, G.; Alvarez, M.; Hausknecht, V.; Gurpide, E.; Schatz, F. Progestational regulation of human endometrial stromal cell tissue factor expression during decidualization. J. Clin. Endocrinol. Metab. 1993, 76, 231–236. [Google Scholar] [CrossRef]
- Duhamel-Clérin, E.; Orvain, C.; Lanza, F.; Cazenave, J.-P.; Klein-Soyer, C. Thrombin Receptor-Mediated Increase of Two Matrix Metalloproteinases, MMP-1 and MMP-3, in Human Endothelial Cells. Arterioscler. Thromb. Vasc. Biol. 1997, 17, 1931–1938. [Google Scholar] [CrossRef] [PubMed]
- Stephenson, C.D.; Lockwood, C.J.; Ma, Y.; Guller, S. Thrombin-dependent regulation of matrix metalloproteinase (MMP)-9 levels in human fetal membranes. J. Matern. Fetal Neonatal Med. 2005, 18, 17–22. [Google Scholar] [CrossRef]
- Lijnen, H.R. Plasmin and Matrix Metalloproteinases in Vascular Remodeling. Thromb. Haemost. 2001, 86, 324–333. [Google Scholar] [CrossRef] [PubMed]
- Kumar, D.; Springel, E.; Moore, R.M.; Mercer, B.M.; Philipson, E.; Mansour, J.M.; Mesiano, S.; Schatz, F.; Lockwood, C.J.; Moore, J.J. Progesterone inhibits in vitro fetal membrane weakening. Am. J. Obstet. Gynecol. 2015, 213, 520.e1–520.e9. [Google Scholar] [CrossRef]
- Feng, L.; Allen, T.K.; Marinello, W.P.; Murtha, A.P. Infection-induced thrombin production: A potential novel mechanism for preterm premature rupture of membranes (PPROM). Am. J. Obstet. Gynecol. 2018, 219, 101.e1–101.e12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nath, C.A.; Ananth, C.V.; Smulian, J.C.; Shen-Schwarz, S.; Kaminsky, L.; New Jersey–Placental Abruption Study Investigators. Histologic evidence of inflammation and risk of placental abruption. Am. J. Obstet. Gynecol. 2007, 197, 319.e1–319.e6. [Google Scholar] [CrossRef]
- Ghidini, A.; Salafia, C.M. Histologic placental lesions in women with recurrent preterm delivery. Acta Obstet. Gynecol. Scand. 2005, 84, 547–550. [Google Scholar] [CrossRef] [PubMed]
- Alfaidy, N.; Hoffmann, P.; Boufettal, H.; Samouh, N.; Aboussaouira, T.; Benharouga, M.; Feige, J.J.; Brouillet, S. The Multiple Roles of EG-VEGF/PROK1 in Normal and Pathological Placental Angiogenesis. BioMed Res. Int. 2014, 2014, 451906. [Google Scholar] [CrossRef] [PubMed]
- Hoffmann, P.; Saoudi, Y.; Benharouga, M.; Graham, C.H.; Schaal, J.P.; Mazouni, C.; Feige, J.J.; Alfaidy, N. Role of EG-VEGF in human placentation: Physiological and pathological implications. J. Cell. Mol. Med. 2009, 13, 2224–2235. [Google Scholar] [CrossRef] [Green Version]
- Denison, F.C.; Battersby, S.; King, A.E.; Szuber, M.; Jabbour, H.N. Prokineticin-1: A Novel Mediator of the Inflammatory Response in Third-Trimester Human Placenta. Endocrinology 2008, 149, 3470–3477. [Google Scholar] [CrossRef]
- Marions, L.; Danielsson, K.G. Expression of cyclo-oxygenase in human endometrium during the implantation period. Mol. Hum. Reprod. 1999, 5, 961–965. [Google Scholar] [CrossRef] [Green Version]
- Diao, H.L.; Zhu, H.; Ma, H.; Tan, H.N.; Cong, J.; Su, R.W.; Yang, Z.M. Rat ovulation, implantation and decidualization are severely compromised by COX-2 inhibitors. Front. Biosci. 2007, 12, 3333–3342. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Börekçi, B.; Aksoy, H.; Toker, A.; Özkan, A. Placental tissue cyclo-oxygenase 1 and 2 in pre-eclamptic and normal pregnancy. Int. J. Gynecol. Obstet. 2006, 95, 127–131. [Google Scholar] [CrossRef] [PubMed]
- Okawara, M.; Seki, H.; Matsuoka, K.; Hashimoto, F.; Hayashi, H.; Takeda, S. Examination of the Expression of Cyclooxygenase-2 in Placenta Villi from Sufferers of Pregnancy Induced Hypertension. Biol. Pharm. Bull. 2009, 32, 2053–2056. [Google Scholar] [CrossRef] [Green Version]
- Polydorides, A.D.; Kalish, R.B.; Witkin, S.S.; Baergen, R.N. A Fetal Cyclooxygenase-2 Gene Polymorphism Is Associated With Placental Malperfusion. Int. J. Gynecol. Pathol. 2007, 26, 284–290. [Google Scholar] [CrossRef] [PubMed]
- Jaekle, R.K.; Lutz, P.D.; Rosenn, B.; Siddiqi, T.A.; Myatt, L. Nitric oxide metabolites and preterm pregnancy complications. Am. J. Obstet. Gynecol. 1994, 171, 1115–1119. [Google Scholar] [CrossRef]
- Schatz, F.; Guzeloglu-Kayisli, O.; Arlıer, S.; Kayisli, U.A.; Lockwood, C.J. The role of decidual cells in uterine hemostasis, menstruation, inflammation, adverse pregnancy outcomes and abnormal uterine bleeding. Hum. Reprod. Update 2016, 22, 497–515. [Google Scholar] [CrossRef] [Green Version]
- Nakashima, M.; Sonoda, K.; Watanabe, T. Inhibition of cell growth and induction of apoptotic cell death by the human tumor-associated antigen RCAS1. Nat. Med. 1999, 5, 938–942. [Google Scholar] [CrossRef]
- Sonoda, K.; Kaku, T.; Hirakawa, T.; Kobayashi, H.; Amada, S.; Sakai, K.; Nakashima, M.; Watanabe, T.; Nakano, H. The Clinical Significance of Tumor-Associated Antigen RCAS1 Expression in the Normal, Hyperplastic, and Malignant Uterine Endometrium. Gynecol. Oncol. 2000, 79, 424–429. [Google Scholar] [CrossRef]
- Matsushima, T.; Nakashima, M.; Oshima, K.; Abe, Y.; Nishimura, J.; Nawata, H.; Watanabe, T.; Muta, K. Receptor binding cancer antigen expressed on SiSo cells, a novel regulator of apoptosis of erythroid progenitor cells. Blood 2001, 98, 313–321. [Google Scholar] [CrossRef]
- Ohshima, K.; Nakashima, M.; Sonoda, K.; Kikuchi, M.; Watanabe, T. Expression of RCAS1 and FasL in human trophoblasts and uterine glands during pregnancy: The possible role in immune privilege. Clin. Exp. Immunol. 2001, 123, 481–486. [Google Scholar] [CrossRef] [PubMed]
- Tsuchiya, F.; Ikeda, K.; Tsutsumi, O.; Hiroi, H.; Momoeda, M.; Taketani, Y.; Muramatsu, M.; Inoue, S. Molecular Cloning and Characterization of Mouse EBAG9, Homolog of a Human Cancer Associated Surface Antigen: Expression and Regulation by Estrogen. Biochem. Biophys. Res. Commun. 2001, 284, 2–10. [Google Scholar] [CrossRef] [PubMed]
- Ohshima, K.; Muta, K.; Nakashima, M.; Haraoka, S.; Tutiya, T.; Suzumiya, J.; Kawasaki, C.; Watanabe, T.; Kikuchi, M. Expression of human tumor-associated antigen RCAS1 in Reed-Sternberg cells in association with Epstein-Barr virus infection: A potential mechanism of immune evasion. Int. J. Cancer 2001, 93, 91–96. [Google Scholar] [CrossRef] [Green Version]
- Wicherek, L.; Dutsch, M.; Mak, P.; Klimek, M.; Skladzien, J.; Dubin, A. Comparative analysis of RCAS1 level in neoplasms and placenta. Acta Biochim. Pol. 2003, 50, 1187–1194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Balkundi, D.R.; Hanna, N.; Hileb, M.; Dougherty, J.; Sharma, S. Labor-Associated Changes in Fas Ligand Expression and Function in Human Placenta. Pediatr. Res. 2000, 47, 301–308. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gortzak-Uzan, L.; Mezad, D.; Smolin, A.; Friger, M.; Huleihel, M.; Hallak, M. Increasing amniotic fluid magnesium concentrations with stable maternal serum levels: A prospective clinical trial. J. Reprod. Med. 2005, 50, 817–820. [Google Scholar]
- Wicherek, L.; Dutsch-Wicherek, M.; Mak, P.; Klimek, M. The Role of RCAS1 and Oxytocinase in Immune Tolerance during Pregnancy. Fetal Diagn. Ther. 2005, 20, 420–425. [Google Scholar] [CrossRef] [PubMed]
- Klaassen, C.D.; Liu, J.; Choudhuri, S. Metallothionein: An Intracellular Protein to Protect Against Cadmium Toxicity. Annu. Rev. Pharmacol. Toxicol. 1999, 39, 267–294. [Google Scholar] [CrossRef] [Green Version]
- Cherian, M.G.; Jayasurya, A.; Bay, B.H. Metallothioneins in human tumors and potential roles in carcinogenesis. Mutat. Res. 2003, 533, 201–209. [Google Scholar] [CrossRef] [PubMed]
- Theocharis, S.E.; Margeli, A.P.; Klijanienko, J.T.; Kouraklis, G.P. Metallothionein expression in human neoplasia. Histopathology 2004, 45, 103–118. [Google Scholar] [CrossRef] [PubMed]
- Kondo, Y.; Rusnak, J.M.; Hoyt, D.G.; Settineri, C.E.; Pitt, B.R.; Lazo, J.S. Enhanced Apoptosis in Metallothionein Null Cells. Mol. Pharmacol. 1997, 52, 195–201. [Google Scholar] [CrossRef] [Green Version]
- Tekur, S.; Ho, S.M. Ribozyme-mediated downregulation of human metallothionein II(a) induces apoptosis in human prostate and ovarian cancer cell lines. Mol. Carcinog. 2002, 33, 44–55. [Google Scholar] [CrossRef]
- Shimoda, R.; Achanzar, W.E.; Qu, W.; Nagamine, T.; Takagi, H.; Mori, M.; Waalkes, M.P. Metallothionein Is a Potential Negative Regulator of Apoptosis. Toxicol. Sci. 2003, 73, 294–300. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dutsch-Wicherek, M.; Sikora, J.; Tomaszewska, R. The possible biological role of metallothionein in apoptosis. Front. Biosci. 2008, 13, 4029–4038. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, G.W.; Klein, J.B.; Kang, Y.J. Metallothionein inhibits doxorubicin-induced mitochondrial cytochrome c release and caspase-3 activation in cardiomyocytes. J. Pharmacol. Exp. Ther. 2001, 298, 461–468. [Google Scholar] [PubMed]
- Wicherek, L.; Popiela, T.J.; Galazka, K.; Dutsch-Wicherek, M.; Oplawski, M.; Basta, A.; Klimek, M. Metallothionein and RCAS1 expression in comparison to immunological cells activity in endometriosis, endometrial adenocarcinoma and endometrium according to menstrual cycle changes. Gynecol. Oncol. 2005, 99, 622–630. [Google Scholar] [CrossRef] [PubMed]
- Schroeder, J.J.; Cousins, R.J. Interleukin 6 regulates metallothionein gene expression and zinc metabolism in hepatocyte monolayer cultures. Proc. Natl. Acad. Sci. USA 1990, 87, 3137–3141. [Google Scholar] [CrossRef] [Green Version]
- Sato, M.; Sasaki, M.; Hojo, H. Tissue specific induction of metallothionein synthesis by tumor necrosis factor-alpha. Res. Commun. Chem. Pathol. Pharmacol. 1992, 75, 159–172. [Google Scholar]
- Friedman, R.L.; Manly, S.P.; McMahon, M.; Kerr, I.M.; Stark, G.R. Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells. Cell 1984, 38, 745–755. [Google Scholar] [CrossRef]
- Kikuchi, Y.; Irie, M.; Kasahara, T.; Sawada, J.; Terao, T. Induction of metallothionein in a human astrocytoma cell line by interleukin-1 and heavy metals. FEBS Lett. 1993, 317, 22–26. [Google Scholar] [CrossRef] [Green Version]
- Borghesi, L.A.; Youn, J.; Olson, E.A.; Lynes, M.A. Interactions of metallothionein with murine lymphocytes: Plasma membrane binding and proliferation. Toxicology 1996, 108, 129–140. [Google Scholar] [CrossRef]
- Wicherek, L.; Galazka, K.; Lazar, A. Analysis of Metallothionein, RCAS1 Immunoreactivity Regarding Immune Cell Concentration in the Endometrium and Tubal Mucosa in Ectopic Pregnancy during the Course of Tubal Rupture. Gynecol. Obstet. Investig. 2008, 65, 52–61. [Google Scholar] [CrossRef]
- DeRoo, L.; Skjaerven, R.; Wilcox, A.; Klungsøyr, K.; Wikström, A.K.; Morken, N.H.; Cnattingius, S. Placental abruption and long-term maternal cardiovascular disease mortality: A population-based registry study in Norway and Sweden. Eur. J. Epidemiol. 2016, 31, 501–511. [Google Scholar] [CrossRef] [PubMed]
- Goldenberg, R.L.; Hauth, J.C.; Andrews, W.W. Intrauterine Infection and Preterm Delivery. N. Engl. J. Med. 2000, 342, 1500–1507. [Google Scholar] [CrossRef] [PubMed]
- Lamont, R.F. The role of infection in preterm labour and birth. Hosp. Med. 2003, 64, 644–647. [Google Scholar] [CrossRef] [PubMed]
- Romero, R.; Espinoza, J.; Gonçalves, L.F.; Kusanovic, J.P.; Friel, L.; Hassan, S. The Role of Inflammation and Infection in Preterm Birth. Semin. Reprod. Med. 2007, 25, 21–39. [Google Scholar] [CrossRef]
- Lockwood, C.J.; Krikun, G.; Papp, C.; Toth-Pal, E.; Markiewicz, L.; Wang, E.Y.; Kerenyi, T.; Zhou, X.; Hausknecht, V.; Papp, Z.; et al. The Role of Progestationally Regulated Stromal Cell Tissue Factor and Type-1 Plasminogen Activator Inhibitor (PAI-1) in Endometrial Hemostasis and Menstruation. Ann. N. Y. Acad. Sci. 1994, 734, 57–79. [Google Scholar] [CrossRef]
- Lockwood, C.J.; Krikun, G.; Schatz, F. Decidual cell-expressed tissue factor maintains hemostasis in human endometrium. Ann. N. Y. Acad. Sci. 2001, 943, 77–88. [Google Scholar] [CrossRef]
- Pijnenborg, R.; Vercruysse, L.; Hanssens, M. The Uterine Spiral Arteries in Human Pregnancy: Facts and Controversies. Placenta 2006, 27, 939–958. [Google Scholar] [CrossRef]
- Lockwood, C.J.; Murk, W.; Kayisli, U.A.; Buchwalder, L.F.; Huang, S.-T.; Funai, E.F.; Krikun, G.; Schatz, F. Progestin and Thrombin Regulate Tissue Factor Expression in Human Term Decidual Cells. J. Clin. Endocrinol. Metab. 2009, 94, 2164–2170. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lockwood, C.J.; Bach, R.; Guha, A.; Zhou, X.D.; Miller, W.A.; Nemerson, Y. Amniotic fluid contains tissue factor, a potent initiator of coagulation. Am. J. Obstet. Gynecol. 1991, 165, 1335–1341. [Google Scholar] [CrossRef]
- Uszynski, M.; Zekanowska, E.; Uszynski, W.; Kuczynski, J. Tissue factor (TF) and tissue factor pathway inhibitor (TFPI) in amniotic fluid and blood plasma: Implications for the mechanism of amniotic fluid embolism. Eur. J. Obstet. Gynecol. Reprod. Biol. 2001, 95, 163–166. [Google Scholar] [CrossRef]
- Estelles, A.; Gilabert, J.; Grancha, S.; Yamamoto, K.; Thinnes, T.; Espana, F.; Aznar, J.; Loskutoff, D.J. Abnormal Expression of Type 1 Plasminogen Activator Inhibitor and Tissue Factor in Severe Preeclampsia. Thromb. Haemost. 1998, 79, 500–508. [Google Scholar] [CrossRef]
- Astrup, T. Assay and Content of Tissue Thromboplastin in Different Organs. Thromb. Haemost. 1965, 14, 401–416. [Google Scholar] [CrossRef]
- Nilsen, P.A. The Mechanism of Hypofibrinogenæmia in Premature Separation of the Normally Implanted Placenta. Acta Obstet. Gynecol. Scand. 1963, 42, 11–96. [Google Scholar] [CrossRef]
- Schneider, C.L. Erythrocyte hemolysis and fibrination-fibrinolysis during retained abruptio placentae with hypovolemia and transient anuria. Obstet. Gynecol. 1968, 31, 491–504. [Google Scholar] [PubMed]
- Thijssen, J.H. Progesterone receptors in the human uterus and their possible role in parturition. J. Steroid Biochem. Mol. Biol. 2005, 97, 397–400. [Google Scholar] [CrossRef]
- Renthal, N.E.; Williams, K.C.; Mendelson, C.R. MicroRNAs—mediators of myometrial contractility during pregnancy and labour. Nat. Rev. Endocrinol. 2013, 9, 391–401. [Google Scholar] [CrossRef]
- Lockwood, C.J.; Stocco, C.; Murk, W.; Kayisli, U.A.; Funai, E.F.; Schatz, F. Human Labor Is Associated with Reduced Decidual Cell Expression of Progesterone, But Not Glucocorticoid, Receptors. J. Clin. Endocrinol. Metab. 2010, 95, 2271–2275. [Google Scholar] [CrossRef] [Green Version]
- Guzeloglu-Kayisli, O.; Kayisli, U.A.; Semerci, N.; Başar, M.; Buchwalder, L.F.; Buhimschi, C.S.; Buhimschi, I.A.; Arcuri, F.; Larsen, K.; Huang, J.S.; et al. Mechanisms of chorioamnionitis-associated preterm birth: Interleukin-1beta inhibits progesterone receptor expression in decidual cells. J. Pathol. 2015, 237, 423–434. [Google Scholar] [CrossRef]
- Ackerman, W.E.; Summerfield, T.L.; Mesiano, S.; Schatz, F.; Lockwood, C.J.; Kniss, D.A. Agonist-Dependent Downregulation of Progesterone Receptors in Human Cervical Stromal Fibroblasts. Reprod. Sci. 2016, 23, 112–123. [Google Scholar] [CrossRef] [Green Version]
- Nadeem, L.; Shynlova, O.; Matysiak-Zablocki, E.; Mesiano, S.; Dong, X.; Lye, S. Molecular evidence of functional progesterone withdrawal in human myometrium. Nat. Commun. 2016, 7, 11565. [Google Scholar] [CrossRef] [Green Version]
- Patel, B.; Peters, G.A.; Skomorovska-Prokvolit, Y.; Yi, L.; Tan, H.; Yousef, A.; Wang, J.; Mesiano, S. Control of Progesterone Receptor-A Transrepressive Activity in Myometrial Cells: Implications for the Control of Human Parturition. Reprod. Sci. 2018, 25, 214–221. [Google Scholar] [CrossRef]
- Jacobsen, B.M.; Horwitz, K.B. Progesterone receptors, their isoforms and progesterone regulated transcription. Mol. Cell. Endocrinol. 2012, 357, 18–29. [Google Scholar] [CrossRef] [Green Version]
- Mesiano, S.; Chan, E.-C.; Fitter, J.T.; Kwek, K.; Yeo, G.; Smith, R. Progesterone Withdrawal and Estrogen Activation in Human Parturition Are Coordinated by Progesterone Receptor A Expression in the Myometrium. J. Clin. Endocrinol. Metab. 2002, 87, 2924–2930. [Google Scholar] [CrossRef]
- Madsen, G.; Zakar, T.; Ku, C.Y.; Sanborn, B.M.; Smith, R.; Mesiano, S. Prostaglandins Differentially Modulate Progesterone Receptor-A and -B Expression in Human Myometrial Cells: Evidence for Prostaglandin-Induced Functional Progesterone Withdrawal. J. Clin. Endocrinol. Metab. 2004, 89, 1010–1013. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Merlino, A.A.; Welsh, T.N.; Tan, H.; Yi, L.J.; Cannon, V.; Mercer, B.M.; Mesiano, S. Nuclear Progesterone Receptors in the Human Pregnancy Myometrium: Evidence that Parturition Involves Functional Progesterone Withdrawal Mediated by Increased Expression of Progesterone Receptor-A. J. Clin. Endocrinol. Metab. 2007, 92, 1927–1933. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Inclusion Criteria | Exclusion Criteria | |
---|---|---|
Study status | Completed, Published | Unfinished, Unpublished |
Study type |
|
|
Language | English | Other than English |
Type of examination | Molecular examination of placenta | Histopathological, genetic or blood only examination |
Sample origin | Human | Animal |
Type of conception | Natural | IVF |
Decidua | Fetal Membranes | |
MMP-1 1,2 | ↑ 2 | MS↑ 1 |
MMP-2 3 | ↑ 3 | |
MMP-3 2,4,5 | → 5/↑ 2 | MS↑ 1 |
MMP-7 5 | → | |
MMP-9 3,5,6 | ↑ 5 | ↑ 6/→ 3 |
TIMP-3 6 | ↓ 6 |
THR | LPS | THR + LPS | |
---|---|---|---|
IL-1β | ⦿ | ⦿ | ⦿ |
IL-6 | ↑ | ↑ | ↑↑ |
IL-8 | ↑ | ↑ | ↑↑ |
IL-10 | ⦿ | ⦿ | ↑↑ |
IL-17 | ↓ | ⦿ | ↑↑ |
IFNγ | ⦿ | ↑ | ↑↑ |
IP-10 | ↑ | ↑ | ⦿ |
TNFα | ⦿ | ⦿ | ↑↑ |
G-CSF | ↑ | ↑ | ↑↑ |
GM-CSF | ⦿ | ⦿ | ↑↑ |
MCP-1 | ↑ | ↑ | ↑↑ |
GRO-α | ↑ | ↑ | ↑↑ |
VEGF | ⦿ | ⦿ | ↑↑ |
RANTES | ⦿ | ⦿ | ⦿ |
MIP-1β | ⦿ | ⦿ | ⦿ |
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Bączkowska, M.; Zgliczyńska, M.; Faryna, J.; Przytuła, E.; Nowakowski, B.; Ciebiera, M. Molecular Changes on Maternal–Fetal Interface in Placental Abruption—A Systematic Review. Int. J. Mol. Sci. 2021, 22, 6612. https://doi.org/10.3390/ijms22126612
Bączkowska M, Zgliczyńska M, Faryna J, Przytuła E, Nowakowski B, Ciebiera M. Molecular Changes on Maternal–Fetal Interface in Placental Abruption—A Systematic Review. International Journal of Molecular Sciences. 2021; 22(12):6612. https://doi.org/10.3390/ijms22126612
Chicago/Turabian StyleBączkowska, Monika, Magdalena Zgliczyńska, Jan Faryna, Ewa Przytuła, Błażej Nowakowski, and Michał Ciebiera. 2021. "Molecular Changes on Maternal–Fetal Interface in Placental Abruption—A Systematic Review" International Journal of Molecular Sciences 22, no. 12: 6612. https://doi.org/10.3390/ijms22126612