Long noncoding RNA MALAT1 contributes to pregnancy-induced hypertension development by enhancing oxidative stress and inflammation through the regulation of the miR-150-5p/ET-1 axis.
Adult
Animals
Apoptosis
Cell Proliferation
Endothelin-1
/ genetics
Female
Gene Expression Regulation
Humans
Hypertension, Pregnancy-Induced
/ etiology
Inflammation
/ complications
Interleukin-1beta
/ genetics
Male
MicroRNAs
/ genetics
NF-kappa B
/ genetics
Oxidative Stress
Pregnancy
RNA, Long Noncoding
/ genetics
Rats
Rats, Wistar
Signal Transduction
Young Adult
NF-κB pathway
endothelial cells
endothelin-1
metastasis-associated lung adenocarcinoma transcript 1
microRNA-150-5p
pregnancy-induced hypertension
smooth muscle cells
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
05
09
2019
revised:
06
01
2020
accepted:
02
02
2020
pubmed:
5
4
2020
medline:
26
1
2021
entrez:
5
4
2020
Statut:
ppublish
Résumé
Metastasis-associated lung adenocarcinoma transcript 1 (MALAT1) has been identified previously in the pathogenesis of hypertension and some gestational diseases. However, the biological functions of MALAT1 in pregnancy-induced hypertension (PIH) are still poorly understood. Herein, we aim to explore the functional relevance of MALAT1 in PIH and to explain the potential underlying mechanisms. We found that the levels of ET-1 and MALAT1 were upregulated and that of miR-150-5p were downregulated in the serum of pregnant women with PIH and the aortic endothelial cells (ECs) of reduced uterine perfusion pressure (RUPP)-induced rat models. In aortic ECs, MALAT1 could competitively bind to miR-150-5p to upregulate the expression of ET-1. The MALAT1/miR-150-5p/ET-1 axis regulated the expression of endothelin B receptor (ETBR) in aortic ECs leading to oxidative stress imbalance and increased the release of proinflammatory cytokines (IL-18 and IL-1β), which concurrently activated the NF-κB pathway to regulate the ETBR expression and to stimulate smooth muscle cell (SMC) contraction. Furthermore, silencing MALAT1 could alleviate the hypertensive symptoms of RUPP-induced rat models. Taken conjointly, the upregulation of MALAT1 can reduce the expression of ET-1 by competitively binding to miR-150-5p, which enhances the expression of ETBR via the activation of the NF-κB pathway in SMCs, thus exacerbating the hypertensive symptoms in the RUPP-induced rat models.
Identifiants
pubmed: 32246794
doi: 10.1096/fj.201902280R
doi:
Substances chimiques
Endothelin-1
0
IL1B protein, human
0
Interleukin-1beta
0
MALAT1 long non-coding RNA, human
0
MIRN150 microRNA, human
0
MicroRNAs
0
NF-kappa B
0
RNA, Long Noncoding
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6070-6085Informations de copyright
© 2020 Federation of American Societies for Experimental Biology.
Références
Jia XQ, Xu S, Tian MR, Ma YY. The relationship between inflammatory factor expression and blood pressure and urinary protein in the placenta of gestational hypertension rats. Exp Ther Med. 2018;16:3793-3798.
Khanam F, Hossain B, Mistry SK, et al. The association between daily 500 mg calcium supplementation and lower pregnancy-induced hypertension risk in Bangladesh. BMC Pregnancy Childbirth. 2018;18:406.
Ananth CV, Basso O. Impact of pregnancy-induced hypertension on stillbirth and neonatal mortality. Epidemiology. 2010;21:118-123.
Kurabayashi T, Mizunuma H, Kubota T, Kiyohara Y, Nagai K, Hayashi K. Pregnancy-induced hypertension is associated with maternal history and a risk of cardiovascular disease in later life: Japanese cross-sectional study. Maturitas. 2013;75:227-231.
Patsch C, Challet-Meylan L, Thoma EC, et al. Generation of vascular endothelial and smooth muscle cells from human pluripotent stem cells. Nat Cell Biol. 2015;17:994-1003.
Small EM, Olson EN. Pervasive roles of microRNAs in cardiovascular biology. Nature. 2011;469:336-342.
Rhodes CJ, Wharton J, Boon RA, et al. Reduced microRNA-150 is associated with poor survival in pulmonary arterial hypertension. Am J Respir Crit Care Med. 2013;187:294-302.
Park HS, Kim ES, Ahn EH, et al. The microRNApolymorphisms inmiR-150 and miR-1179 are associated with risk of idiopathic recurrent pregnancy loss. Reprod Biomed Online. 2019;39:187-195.
Zhang Y, Wang F, Chen G, He R, Yang L. LncRNA MALAT1 promotes osteoarthritis by modulating miR-150-5p/AKT3 axis. Cell Biosci. 2019;9:54.
Yu B, Wang S. Angio-LncRs: LncRNAs that regulate angiogenesis and vascular disease. Theranostics. 2018;8:3654-3675.
Zhou X, Liu S, Cai G, et al. Long non coding RNA MALAT1 promotes tumor growth and metastasis by inducing epithelial-mesenchymal transition in oral squamous cell carcinoma. Sci Rep. 2015;5:15972.
Zhuo Y, Zeng Q, Zhang P, Li G, Xie Q, Cheng Y. Functional polymorphism of lncRNA MALAT1 contributes to pulmonary arterial hypertension susceptibility in Chinese people. Clin Chem Lab Med. 2017;55:38-46.
Ou M, Dang Y, Mazzuca MQ, Basile R, Khalil RA. Adaptive regulation of endothelin receptor type-A and type-B in vascular smooth muscle cells during pregnancy in rats. J Cell Physiol. 2014;229:489-501.
Caldeira-Dias M, Luizon MR, Deffune E, et al. Preeclamptic plasma stimulates the expression of miRNAs, leading to a decrease in endothelin-1 production in endothelial cells. Pregnancy Hypertens. 2018;12:75-81.
Yeligar S, Tsukamoto H, Kalra VK. Ethanol-induced expression of ET-1 and ET-BR in liver sinusoidal endothelial cells and human endothelial cells involves hypoxia-inducible factor-1alpha and microrNA-199. J Immunol. 2009;183:5232-5243.
Gerstung M, Roth T, Dienes HP, Licht C, Fries JW. Endothelin-1 induces NF-kappaB via two independent pathways in human renal tubular epithelial cells. Am J Nephrol. 2007;27:294-300.
Wang J, Cui J, Chen R, et al. Prenatal exposure to lipopolysaccharide alters renal DNA methyltransferase expression in rat offspring. PLoS ONE. 2017;12:e0169206.
Report of the national high blood pressure education program working group on high blood pressure in pregnancy. Am J Obstet Gynecol. 2000;183, S1-S22.
Mazzuca MQ, Li W, Reslan OM, Yu P, Mata KM, Khalil RA. Downregulation of microvascular endothelial type B endothelin receptor is a central vascular mechanism in hypertensive pregnancy. Hypertension. 2014;64:632-643.
Kobayashi M, Inoue K, Warabi E, Minami T, Kodama T. A simple method of isolating mouse aortic endothelial cells. J Atheroscler Thromb. 2005;12:138-142.
Li QF, Tang DD. Role of p47(phox) in regulating Cdc42GAP, vimentin, and contraction in smooth muscle cells. Am J Physiol Cell Physiol. 2009;297:C1424-C1433.
Lu CQ, Lin J, Yuan L, et al. Pregnancy induced hypertension and outcomes in early and moderate preterm infants. Pregnancy Hypertens. 2018;14:68-71.
He X, He Y, Xi B, et al. LncRNAs expression in preeclampsia placenta reveals the potential role of LncRNAs contributing to preeclampsia pathogenesis. PLoS ONE. 2013;8:e81437.
George EM, Granger JP. Endothelin: key mediator of hypertension in preeclampsia. Am J Hypertens. 2011;24:964-969.
Chen H, Meng T, Liu X, et al. Long non-coding RNA MALAT-1 is downregulated in preeclampsia and regulates proliferation, apoptosis, migration and invasion of JEG-3 trophoblast cells. Int J Clin Exp Pathol. 2015;8:12718-12727.
Liu JY, Yao J, Li XM, et al. Pathogenic role of lncRNA-MALAT1 in endothelial cell dysfunction in diabetes mellitus. Cell Death Dis. 2014;5:e1506.
Chen M, Shen C, Zhang Y, Shu H. MicroRNA-150 attenuates hypoxia-induced excessive proliferation and migration of pulmonary arterial smooth muscle cells through reducing HIF-1alpha expression. Biomed Pharmacother. 2017;93:861-868.
Luo XY, Zhu XQ, Li Y, et al. MicroRNA-150 restores endothelial cell function and attenuates vascular remodeling by targeting PTX3 through the NF-kappaB signaling pathway in mice with acute coronary syndrome. Cell Biol Int. 2018;42:1170-1181.
George EM, Granger JP. Linking placental ischemia and hypertension in preeclampsia: role of endothelin 1. Hypertension. 2012;60:507-511.
Kappers MH, van Esch JH, Sluiter W, Sleijfer S, Danser AH, van den Meiracker AH. Hypertension induced by the tyrosine kinase inhibitor sunitinib is associated with increased circulating endothelin-1 levels. Hypertension. 2010;56:675-681.
He Q, Liu X, Zhong Y, et al. Arginine bioavailability and endothelin-1 system in the regulation of vascular function of umbilical vein endothelial cells from intrauterine growth restricted newborns. Nutr Metab Cardiovasc Dis. 2018;28:1285-1295.
Wang YN, Shan K, Yao MD, et al. Long noncoding RNA-GAS5: a novel regulator of hypertension-induced vascular remodeling. Hypertension. 2016;68:736-748.
Anguiano L, Riera M, Pascual J, Soler MJ. Endothelin blockade in diabetic kidney disease. J Clin Med. 2015;4:1171-1192.
Lankhorst S, Kappers MH, van Esch JH, Danser AH, van den Meiracker AH. Hypertension during vascular endothelial growth factor inhibition: focus on nitric oxide, endothelin-1, and oxidative stress. Antioxid Redox Signal. 2014;20:135-145.
Rautureau Y, Schiffrin EL. Endothelin in hypertension: an update. Curr Opin Nephrol Hypertens. 2012;21:128-136.
Zhao X, Wang X. Candesartan targeting of angiotensin II type 1 receptor demonstrates benefits for hypertension in pregnancy via the NFkappaB signaling pathway. Mol Med Rep. 2018;18:705-714.
Yang JM, Zhou R, Zhang M, Tan HR, Yu JQ. Betaine attenuates monocrotaline-induced pulmonary arterial hypertension in rats via inhibiting inflammatory response. Molecules. 2018;23: pii: E1274.
Tai LW, Pan Z, Sun L, et al. Suppression of Pax2 attenuates allodynia and hyperalgesia through ET-1-ETAR-NFAT5 signaling in a rat model of neuropathic pain. Neuroscience. 2018;384:139-151.
Kowalczyk A, Kleniewska P, Kolodziejczyk M, Skibska B, Goraca A. The role of endothelin-1 and endothelin receptor antagonists in inflammatory response and sepsis. Arch Immunol Ther Exp (Warsz). 2015;63:41-52.