600
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Low-dose aspirin inhibits trophoblast cell apoptosis by activating the CREB/Bcl-2 pathway in pre-eclampsia

, , , , &
Pages 2223-2238 | Received 24 Dec 2021, Accepted 31 May 2022, Published online: 06 Jul 2022

References

  • Dachew BA, Mamun A, Maravilla JC, et al. Association between hypertensive disorders of pregnancy and the development of offspring mental and behavioural problems: a systematic review and meta-analysis. Psychiatry Res. 2018;260:458–467.
  • Mol BWJ, Roberts CT, Thangaratinam S, et al. Pre-eclampsia. Lancet. 2016;387(10022):999–1011.
  • Rana S, Karumanchi SA, Lindheimer MD. Angiogenic factors in diagnosis, management, and research in preeclampsia. Hypertension. 2014;63(2):198–202.
  • Redman CW, Sargent IL. The pathogenesis of pre-eclampsia. Gynecol Obstet Fertil. 2001;29(7–8):518–522.
  • Leung DN, Smith SC, To KF, et al. Increased placental apoptosis in pregnancies complicated by preeclampsia. Am J Obstet Gynecol. 2001;184(6):1249–1250.
  • Ouyang L, Shi Z, Zhao S, et al. Programmed cell death pathways in cancer: a review of apoptosis, autophagy and programmed necrosis. Cell Prolif. 2012;45(6):487–498.
  • Akgul C, Moulding DA, Edwards SW. Alternative splicing of Bcl-2-related genes: functional consequences and potential therapeutic applications. Cell Mol Life Sci. 2004;61(17):2189–2199.
  • Aban M, Cinel L, Arslan M, et al. Expression of nuclear factor-kappa B and placental apoptosis in pregnancies complicated with intrauterine growth restriction and preeclampsia: an immunohistochemical study. Tohoku J Exp Med. 2004;204(3):195–202.
  • Tong J, Niu Y, Chen ZJ, et al. Comparison of the transcriptional profile in the decidua of early-onset and late-onset pre-eclampsia. J Obstet Gynaecol Res. 2020;46(7):1055–1066.
  • Cai X, Fu H, Wang Y, et al. Depletion of GPSM1 enhances ovarian granulosa cell apoptosis via cAMP-PKA-CREB pathway in vitro. J Ovarian Res. 2020;13(1):136.
  • Schubert SW, Abendroth A, Kilian K, et al. bZIP-type transcription factors CREB and OASIS bind and stimulate the promoter of the mammalian transcription factor GCMa/Gcm1 in trophoblast cells. Nucleic Acids Res. 2008;36(11):3834–3846.
  • Darashchonak N, Koepsell B, Bogdanova N, et al. Adenosine A2B receptors induce proliferation, invasion and activation of cAMP response element binding protein (CREB) in trophoblast cells. BMC Pregnancy Childbirth. 2014;14(1):2.
  • Shi Y, Ye D, Huang R, et al. Down syndrome critical region 1 reduces oxidative stress-induced retinal ganglion cells apoptosis via CREB-Bcl-2 pathway. Invest Ophthalmol Vis Sci. 2020;61(12):23.
  • Gu M, Zheng W, Zhang M, et al. LncRNA NONHSAT141924 promotes paclitaxel chemotherapy resistance through p-CREB/Bcl-2 apoptosis signaling pathway in breast cancer. J Cancer. 2020;11(12):3645–3654.
  • Cho EC, Mitton B, Sakamoto KM. CREB and leukemogenesis. Crit Rev Oncog. 2011;16(1–2):37–46.
  • Sakamoto K, Karelina K, Obrietan K. CREB: a multifaceted regulator of neuronal plasticity and protection. J Neurochem. 2011;116(1):1–9.
  • Perschbacher KJ, Deng G, Sandgren JA, et al. Reduced mRNA expression of RGS2 (regulator of G protein signaling-2) in the placenta is associated with human preeclampsia and sufficient to cause features of the disorder in mice. Hypertension. 2020;75(2):569–579.
  • Roberts JM, Speer P. Antioxidant therapy to prevent preeclampsia. Semin Nephrol. 2004;24(6):557–564.
  • Patrono C. The multifaceted clinical readouts of platelet inhibition by low-dose aspirin. J Am Coll Cardiol. 2015;66(1):74–85.
  • Atallah A, Lecarpentier E, Goffinet F, et al. Aspirin for prevention of preeclampsia. Drugs. 2017;77(17):1819–1831.
  • Cadavid AP. Aspirin: the mechanism of action revisited in the context of pregnancy complications. Front Immunol. 2017;8:261.
  • Goodlin RC, Haesslein HO, Fleming J. Aspirin for the treatment of recurrent toxaemia. Lancet. 1978;2(8079):51.
  • Poon LC, Wright D, Rolnik DL, et al. Aspirin for evidence-based preeclampsia prevention trial: effect of aspirin in prevention of preterm preeclampsia in subgroups of women according to their characteristics and medical and obstetrical history. Am J Obstet Gynecol. 2017;217(5):585 e581–585 e585.
  • Wright D, Poon LC, Rolnik DL, et al. Aspirin for evidence-based preeclampsia prevention trial: influence of compliance on beneficial effect of aspirin in prevention of preterm preeclampsia. Am J Obstet Gynecol. 2017;217(6):685 e681–685 e685.
  • Rolnik DL, Wright D, Poon LC, et al. Aspirin versus placebo in pregnancies at high risk for preterm preeclampsia. N Engl J Med. 2017;377(7):613–622.
  • Buemi M, Allegra A, D’Anna R, et al. Is apoptosis cause of pre-eclampsia? Eur Rev Med Pharmacol Sci. 1998;2(5–6):185–188.
  • Bilanda DC, Dzeufiet PDD, Kouakep L, et al. Bidens pilosa ethylene acetate extract can protect against L-NAME-induced hypertension on rats. BMC Complement Altern Med. 2017;17(1):479.
  • Zou Y, Li S, Wu D, et al. Resveratrol promotes trophoblast invasion in pre-eclampsia by inducing epithelial-mesenchymal transition. J Cell Mol Med. 2019;23(4):2702–2710.
  • Shin YY, An SM, Jeong JS, et al. Comparison of steroid hormones in three different preeclamptic models. Mol Med Rep. 2021;23. doi:10.3892/mmr.2021.11891.
  • ShamsEldeen AM, Mehesen MN, Aboulhoda BE, et al. Prenatal intake of omega-3 promotes Wnt/beta-catenin signaling pathway, and preserves integrity of the blood-brain barrier in preeclamptic rats. Physiol Rep. 2021;9(12):e14925.
  • Ma XP, Liu CD, Cao GM, et al. Transthyretin increases migration and invasion of rat placental trophoblast cells. FEBS Open Bio. 2020;10(8):1568–1576.
  • Chipuk JE, Green DR. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 2008;18(4):157–164.
  • Wang C, Youle RJ. The role of mitochondria in apoptosis*. Annu Rev Genet. 2009;43(1):95–118.
  • Panagodage S, Yong HE, Da Silva Costa F, et al. Low-dose acetylsalicylic acid treatment modulates the production of cytokines and improves trophoblast function in an in vitro model of early-onset preeclampsia. Am J Pathol. 2016;186(12):3217–3224.
  • Zuo Q, Zou Y, Huang S, et al. Aspirin reduces sFlt-1-mediated apoptosis of trophoblast cells in preeclampsia. Mol Hum Reprod. 2021;27. doi:10.1093/molehr/gaaa089.
  • Garcia-Saez AJ. The secrets of the Bcl-2 family. Cell Death Differ. 2012;19(11):1733–1740.
  • Sharp AN, Heazell AE, Baczyk D, et al. Preeclampsia is associated with alterations in the p53-pathway in villous trophoblast. PLoS One. 2014;9(1):e87621.
  • Sharp AN, Heazell AE, Crocker IP, et al. Placental apoptosis in health and disease. Am J Reprod Immunol. 2010;64(3):159–169.
  • Levy R, Smith SD, Yusuf K, et al. Trophoblast apoptosis from pregnancies complicated by fetal growth restriction is associated with enhanced p53 expression. Am J Obstet Gynecol. 2002;186(5):1056–1061.
  • Hu R, Zhou S, Li X. Altered Bcl-2 and Bax expression is associated with cultured first trimester human cytotrophoblasts apoptosis induced by hypoxia. Life Sci. 2006;79(4):351–355.
  • Dash PR, Cartwright JE, Baker PN, et al. Nitric oxide protects human extravillous trophoblast cells from apoptosis by a cyclic GMP-dependent mechanism and independently of caspase 3 nitrosylation. Exp Cell Res. 2003;287(2):314–324.
  • Xu T, Ding W, Ao X, et al. ARC regulates programmed necrosis and myocardial ischemia/reperfusion injury through the inhibition of mPTP opening. Redox Biol. 2019;20:414–426.
  • Di Meo F, Cuciniello R, Margarucci S, et al. Ginkgo biloba prevents oxidative stress-induced apoptosis blocking p53 activation in neuroblastoma cells. Antioxidants (Basel). 2020;9(4):279.
  • Qian Y, Du YH, Tang YB, et al. ClC-3 chloride channel prevents apoptosis induced by hydrogen peroxide in basilar artery smooth muscle cells through mitochondria dependent pathway. Apoptosis. 2011;16(5):468–477.
  • Jiang L, Liu Y, Ma MM, et al. Mitochondria dependent pathway is involved in the protective effect of bestrophin-3 on hydrogen peroxide-induced apoptosis in basilar artery smooth muscle cells. Apoptosis. 2013;18(5):556–565.
  • Johannessen M, Delghandi MP, Moens U. What turns CREB on? Cell Signal. 2004;16(11):1211–1227.
  • Shaywitz AJ, Greenberg ME. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem. 1999;68(1):821–861.
  • Depoix C, Tee MK, Taylor RN. Molecular regulation of human placental growth factor (PlGF) gene expression in placental villi and trophoblast cells is mediated via the protein kinase a pathway. Reprod Sci. 2011;18(3):219–228.
  • Norris W, Nevers T, Sharma S, et al. Review: hCG, preeclampsia and regulatory T cells. Placenta. 2011;32 Suppl 2:S182–185.
  • Zhang P, Wang J, Lang H, et al. Knockdown of CREB1 promotes apoptosis and decreases estradiol synthesis in mouse granulosa cells. Biomed Pharmacother. 2018;105:1141–1146.
  • Toscano CD, Prabhu VV, Langenbach R, et al. Differential gene expression patterns in cyclooxygenase-1 and cyclooxygenase-2 deficient mouse brain. Genome Biol. 2007;8(1):R14.
  • Taubert D, Berkels R, Grosser N, et al. Aspirin induces nitric oxide release from vascular endothelium: a novel mechanism of action. Br J Pharmacol. 2004;143(1):159–165.
  • Chen J, Wang L, Liu WH, et al. Aspirin protects human coronary artery endothelial cells by inducing autophagy. Physiol Int. 2020;107(2):294–305.
  • Kirkby NS, Tesfai A, Ahmetaj-Shala B, et al. Ibuprofen arginate retains eNOS substrate activity and reverses endothelial dysfunction: implications for the COX-2/ADMA axis. FASEB J. 2016;30(12):4172–4179.
  • Martinez CS, Piagette JT, Escobar AG, et al. Aluminum exposure at human dietary levels promotes vascular dysfunction and increases blood pressure in rats: a concerted action of NAD(P)H oxidase and COX-2. Toxicology. 2017;390:10–21.
  • Zhang QH, Zu XY, Cao RX, et al. An involvement of SR-B1 mediated PI3K-Akt-eNOS signaling in HDL-induced cyclooxygenase 2 expression and prostacyclin production in endothelial cells. Biochem Biophys Res Commun. 2012;420(1):17–23.
  • Schulte JS, Seidl MD, Nunes F, et al. CREB critically regulates action potential shape and duration in the adult mouse ventricle. Am J Physiol Heart Circ Physiol. 2012;302(10):H1998–2007.
  • Sampurno S, Bijenhof A, Cheasley D, et al. The Myb-p300-CREB axis modulates intestine homeostasis, radiosensitivity and tumorigenesis. Cell Death Dis. 2013;4(4):e605.
  • Crisafulli C, Shim DS, Andrisano C, et al. Case-control association study of 14 variants of CREB1, CREBBP and CREM on diagnosis and treatment outcome in major depressive disorder and bipolar disorder. Psychiatry Res. 2012;198(1):39–46.
  • Mamdani F, Alda M, Grof P, et al. Lithium response and genetic variation in the CREB family of genes. Am J Med Genet B Neuropsychiatr Genet. 2008;147B(4):500–504.
  • Sharma N, Mali AM, Bapat SA. Spectrum of CREBBP mutations in Indian patients with Rubinstein-Taybi syndrome. J Biosci. 2010;35(2):187–202.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.