1,550
Views
0
CrossRef citations to date
0
Altmetric
Original Article

The effect and mechanism of low-molecular-weight heparin on the decidualization of stromal cells in early pregnancy

, , , , , & show all
Article: 2294701 | Received 08 Sep 2023, Accepted 10 Dec 2023, Published online: 04 Jan 2024

References

  • Youssef A, Vermeulen N, Lashley EELO, et al. Comparison and appraisal of (inter) national recurrent pregnancy loss guidelines . Reprod Biomed Online. 2019;39(3):497–503. doi: 10.1016/j.rbmo.2019.04.008.
  • El Hachem H, Crepaux V, May-Panloup P, et al. Recurrent pregnancy loss: current perspectives. Int J Womens Health. 2017;9:331–345. doi: 10.2147/IJWH.S100817.
  • Pang L, Wei Z, Li O, et al. An increase in vascular endothelial growth factor (VEGF)and VEGF soluble receptor-1(sFlt-1)are associated with early recurrent spontaneous abortion . PLOS One. 2013;8(9):e75759. doi: 10.1371/journal.pone.0075759.
  • Kolte AM, Olsen LR, Mikkelsen EM, et al. Depression and emotional stress is highly prevalent among women with recurrent pregnancy loss. Hum Reprod. 2015;30(4):777–782. doi: 10.1093/humrep/dev014.
  • Arias-Sosa LA, Acosta ID, Lucena-Quevedo E, et al. Genetic and epigenetic variations associated with idiopathic recurrent pregnancy loss. J Assist Reprod Genet. 2018;35(3):355–366. doi: 10.1007/s10815-017-1108-y.
  • Huang N, Gao Y, Zhang M, et al. METTL3-Mediated mA RNA methylation of ZBTB4 interferes with trophoblast invasion and maybe involved in RSA. Front Cell Dev Biol. 2022;10:894810. doi: 10.3389/fcell.2022.894810.
  • Caruso A, De Carolis S, Di Simone N. Antiphospholipid antibodies in obstetrics: new complexities and sites of action. Hum Reprod Update. 1999;5(3):267–276. doi: 10.1093/humupd/5.3.267.
  • Veglia M, D'Ippolito S, Marana R, et al. Human IgG antinuclear antibodies induce pregnancy loss in mice by increasing immune complex deposition in placental tissue: in vivo study. Am J Reprod Immunol. 2015;74(6):542–552. doi: 10.1111/aji.12429.
  • Di Simone N, Castellani R, Caliandro D, et al. Monoclonal anti-annexin V antibody inhibits trophoblast gonadotropin secretion and induces syncytiotrophoblast apoptosis. Biol Reprod. 2001;65(6):1766–1770. doi: 10.1095/biolreprod65.6.1766.
  • Ochoa-Bernal MA, Fazleabas AT. Physiologic events of embryo implantation and decidualization in human and non-human primates. Int J Mol Sci. 2020;21(6):1973. doi: 10.3390/ijms21061973.
  • Cho HJ, Baek MO, Khaliq SA, et al. Microgravity inhibits decidualization via decreasing akt activity and FOXO3a expression in human endometrial stromal cells. Sci Rep. 2019;9(1):12094. doi: 10.1038/s41598-019-48580-9.
  • 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. doi: 10.3389/fimmu.2019.02317.
  • Lucas ES, Vrljicak P, Muter J, et al. Recurrent pregnancy loss is associated with a pro-senescent decidual response during the peri-implantation window. Commun Biol. 2020;3(1):37. doi: 10.1038/s42003-020-0763-1.
  • Cottrell HN, Wu J, Rimawi BH, et al. Human endometrial stromal cell plasticity: reversible sFlt1 expression negatively coincides with decidualization. Hypertens Pregnancy. 2017;36(2):204–211.
  • Lv X, Cai Z, Li S. Increased apoptosis rate of human decidual cells and cytotrophoblasts in patients with recurrent spontaneous abortion as a result of abnormal expression of CDKN1A and bax. Exp Ther Med. 2016;12(5):2865–2868. doi: 10.3892/etm.2016.3692.
  • Larsen EC, Christiansen OB, Kolte AM, et al. New insights into mechanisms behind miscarriage. BMC Med. 2013;11(1):154. doi: 10.1186/1741-7015-11-154.
  • Kaya Okur HS, Das A, Taylor RN, et al. Roles of estrogen receptor-α and the coactivator MED1 during human endometrial decidualization. Mol Endocrinol. 2016;30(3):302–313. doi: 10.1210/me.2015-1274.
  • Chen P, Zhou L, Chen J, et al. The immune atlas of human deciduas with unexplained recurrent pregnancy loss. Front Immunol. 2021;12:689019. Published 2021 Jun 7 doi: 10.3389/fimmu.2021.689019.
  • Mani SK, Julian J, Lampelo S, et al. Initiation and maintenance of in vitro decidualization are independent of hormonal sensitization in vivo. Biol Reprod. 1992;47(5):785–799. doi: 10.1095/biolreprod47.5.785.
  • Castro-Leyva V, Zaga-Clavellina V, Espejel-Nunez A, et al. Decidualization mediated by steroid hormones modulates the innate immunity in response to group B streptococcal infection in vitro. Gynecol Obstet Invest. 2017;82(6):592–600. doi: 10.1159/000454770.
  • Ahn JI, Yoo JY, Kim TH, et al. cAMP-response element-binding 3-like protein 1 (CREB3L1) is required for decidualization and its expression is decreased in women with endometriosis. Curr Mol Med. 2016;16(3):276–287. doi: 10.2174/1566524016666160225153659.
  • Lazrak HH, René É, Elftouh N, et al. Safety of low-molecular-weight heparin compared to unfractionated heparin in hemodialysis: a systematic review and meta-analysis. BMC Nephrol. 2017;18(1):187. Published 2017. doi: 10.1186/s12882-017-0596-4.
  • Zee AA, van Lieshout K, van der Heide M, et al. Low molecular weight heparin for prevention of venous thromboembolism in patients with lower-limb immobilization. Cochrane Database Syst Rev. 2017;8(8):CD006681. doi: 10.1002/14651858.CD006681.pub4.
  • Bai W, Zhang X, Sun S, et al. Effect of low-molecular-weight heparins on anti-Xa peak levels and adverse reactions in Chinese patients with recurrent spontaneous abortion: a single-center, observational study. BMC Pregnancy Childbirth. 2021;21(1):683. doi: 10.1186/s12884-021-04161-1.
  • Stief T. LMWH - action-monitoring for all patients. Acta Paediatr. 2012;101:e314.
  • Yoneda M, Brosnan JF, Norris LA, et al. The effect of LMWH (tinzaparin) on coagulation and fibrinolytic activation in pregnant women at risk of thrombosis. Thromb Res. 2006;117(3):283–290. doi: 10.1016/j.thromres.2005.03.016.
  • Jiang F, Hu X, Jiang K, et al. The role of low molecular weight heparin on recurrent pregnancy loss: a systematic review and meta-analysis. Taiwan J Obstet Gynecol. 2021;60(1):1–8. doi: 10.1016/j.tjog.2020.11.001.
  • Schleussner E, Kamin G, Seliger G, et al. Low-molecular-weight heparin for women with unexplained recurrent pregnancy loss: a multicenter trial with a minimization randomization scheme. Ann Intern Med. 2015;162(9):601–609. doi: 10.7326/M14-2062.
  • Luo J, Wang Y, Qi Q, et al. Sinomenine improves embryo survival by regulating Th1/Th2 balance in a mouse model of recurrent spontaneous abortion. Med Sci Monit. 2021;27:e927709. doi: 10.12659/MSM.927709.
  • Wang S, Guo S, Hou X. MicroRNA-24 inhibits CDX1 expression in decidual tissues of recurrent spontaneous abortion mice to reduce the abortion risk. Adv Clin Exp Med. 2020;29(8):929–936. doi: 10.17219/acem/122173.
  • de Jong PG, Kaandorp S, Di Nisio M, et al. Aspirin and/or heparin for women with unexplained recurrent miscarriage with or without inherited thrombophilia. Cochrane Database Syst Rev. 2014;2014(7):CD004734. Published 2014 Jul 4
  • PrabhuDas M, Bonney E, Caron K, et al. Immune mechanisms at the maternal-fetal interface: perspectives and challenges. Nat Immunol. 2015;16(4):328–334. doi: 10.1038/ni.3131.
  • Xu L, Li Y, Sang Y, et al. Crosstalk between trophoblasts and decidual immune cells: the cornerstone of Maternal-Fetal immunotolerance. Front Immunol. 2021;12:642392. doi: 10.3389/fimmu.2021.642392.
  • Hu WT, Huang LL, Li MQ, et al. Decidual stromal cell-derived IL-33 contributes to Th2 bias and inhibits decidual NK cell cytotoxicity through NF-kappaB signaling in human early pregnancy. J Reprod Immunol. 2015;109:52–65. doi: 10.1016/j.jri.2015.01.004.
  • Bolnick AD, Bolnick JM, Kohan-Ghadr HR, et al. Enhancement of trophoblast differentiation and survival by low molecular weight heparin requires heparin-binding EGF-like growth factor. Hum Reprod. 2017;32(6):1218–1229. doi: 10.1093/humrep/dex069.
  • Tersigni C, Marana R, Santamarìa A, et al. In vitro evidences of heparin’s effects on embryo implantation and trophoblast development[J]. Reprod Sci. 2012;19(5):454–462. doi: 10.1177/1933719111430994.
  • Mori M, Barnard GF, Mimori K, et al. Overexpression of matrix metalloproteinase-7 mRNA in human Colon carcinomas. Cancer (Phi1a). 1995;75(S6):1516–1519. doi: 10.1002/1097-0142(19950315)75:6+<1516::AID-CNCR2820751522>3.0.CO;2-7.
  • D'Ippolito S, Marana R, Di Nicuolo F, et al. Effect of low molecular weight heparins (LMWHs) on antiphospholipid antibodies (aPL)-mediated inhibition of endometrial angiogenesis. PLOS One. 2012;7(1):e29660. doi: 10.1371/journal.pone.0029660.
  • Valatkaitė E, Baušytė R, Vitkevičienė A, et al. Decidualization potency and epigenetic changes in human endometrial origin stem cells during propagation. Front Cell Dev Biol. 2021;9:765265. doi: 10.3389/fcell.2021.765265.
  • Peng Y, Jin Z, Liu H, et al. Impaired decidualization of human endometrial stromal cells from women with adenomyosis†. Biol Reprod. 2021;104(5):1034–1044. doi: 10.1093/biolre/ioab017.
  • Gibson DA, Simitsidellis I, Kelepouri O, et al. Dehydroepiandrosterone enhances decidualization in women of advanced reproductive age. Fertil Steril. 2018;109(4):728–734.e2. doi: 10.1016/j.fertnstert.2017.12.024.
  • Ma J, Li J, Yang S, et al. P57 and cyclin G1 express differentially in proliferative phase endometrium and early pregnancy decidua. Int J Clin Exp Med. 2015;8:5144–5149.
  • Cosmi E, Saccardi C, Litta P, et al. Transvaginal ultrasound and sonohysterography for assessment of postpartum residual trophoblastic tissue[J]. Int J Gynaecol Obstet. 2010;110(3):262–∼264. doi: 10.1016/j.ijgo.2010.03.036.
  • Xie J, Zhou X, Wang R, et al. Identification of potential diagnostic biomarkers in MMPs for pancreatic carcinoma. Medicine (Baltimore). 2021;100(23):e26135.)doi: 10.1097/MD.0000000000026135.
  • Quenby S, Booth K, Hiller L, et al. Heparin for women with recurrent miscarriage and inherited thrombophilia (ALIFE2): an international open-label, randomised controlled trial. Lancet. 2023; 402(10395):54–61. doi: 10.1016/S0140-6736(23)00693-1.
  • Lv S, Yu J, Xu X. A comparison of effectiveness among frequent treatments of recurrent spontaneous abortion: a bayesian network meta-analysis. Am J Reprod Immunol. 2018; 80(1):e12856.