MicroRNAs in Preeclampsia

Author(s): Georgios Skalis*, Vasiliki Katsi, Antigoni Miliou, Georgios Georgiopoulos, Ourania Papazachou, Georgia Vamvakou, Petros Nihoyannopoulos, Dimitrios Tousoulis, Thomas Makris

Journal Name: MicroRNA

Volume 8 , Issue 1 , 2019

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Graphical Abstract:


Preeclampsia (PE) continues to represent a worldwide problem and challenge for both clinicians and laboratory-based doctors. Despite many efforts, the knowledge acquired regarding its pathogenesis and pathophysiology does not allow us to treat it efficiently. It is not possible to arrest its progressive nature, and the available therapies are limited to symptomatic treatment. Furthermore, both the diagnosis and prognosis are frequently uncertain, whilst the ability to predict its occurrence is very limited. MicroRNAs are small non-coding RNAs discovered two decades ago, and present great interest given their ability to regulate almost every aspect of the cell function. A lot of evidence regarding the role of miRNAs in pre-eclampsia has been accumulated in the last 10 years. Differentially expressed miRNAs are characteristic of both mild and severe PE. In many cases they target signaling pathway-related genes that result in altered processes which are directly involved in PE. Immune system, angiogenesis and trophoblast proliferation and invasion, all fundamental aspects of placentation, are controlled in various degrees by miRNAs which are up- or downregulated. Finally, miRNAs represent a potential therapeutic target and a diagnostic tool.

Keywords: Angiogenesis, miRNA, placentation, preeclampsia, trophoblasts, immune system.

Duley L. The global impact of pre-eclampsia and eclampsia. Semin Perinatol 2009; 33(3): 130-7.
Say L, Chou D, Gemmill A, et al. Global causes of maternal death: a WHO systematic analysis. Lancet Glob Health 2014; 2(6): e323-33.
Roberts JM, August PA, Bakris G, et al. Hypertension in pregnancy. Report of the American college of obstetricians and gynecologists’ task force on hypertension in pregnancy. Obstet Gynecol 2013; 122(5): 1122-31.
Tranquilli AL, Brown MA, Zeeman GG, et al. The definition of severe and early-onset preeclampsia. Statements from the International Society for the Study of Hypertension in Pregnancy (ISSHP). Pregnancy Hypertens 2013; 3(1): 44-7.
Hansen AR, Barnes CM, Folkman J, McElrath TF. Maternal preeclampsia predicts the development of bronchopulmonary dysplasia. J Pediatr 2010; 156(4): 532-6.
Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet 2005; 365(9461): 785-99.
Koshiol J, Wang E, Zhao Y, Marincola F, Landi MT. Strengths and limitations of laboratory procedures for microRNA detection. Cancer Epidemiol Biomarkers Prev 2010; 19(4): 907-11.
Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell 2012; 148(6): 1172-87.
Bdolah Y, Lam C, Rajakumar A, et al. Twin pregnancy and the risk of preeclampsia: bigger placenta or relative ischemia? Am J Obstet Gynecol 2008; 198(4): 428.e1-6.
Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science 2005; 308(5728): 1592-4.
Roberts J, Hubel C. The two stage model of preeclampsia: variations on the theme. Placenta 2009; 30(Suppl.): A32-7.
Roberts J. Pre-eclampsia a two stage disorder: what is the linkage? are there directed fetal/ placental signals? In: Lyall F and Belfort M, Ed Preeclampsia: etiology and clinical practice, New YorkUSA: : Cambridge University Press, USA. 2007; pp. 183-92.
Lyall F. Mechanisms regulating cytotrophoblast invasion in normal pregnancy and pre-eclampsia. Aust N Z J Obstet Gynaecol 2006; 46(4): 266-73.
Joanna LJ, Guy SW, Judith EC. Pre-eclampsia: fitting together the placental, immune and cardiovascular pieces. J Pathol 2010; 221(4): 363-78.
Robertson W, Brosens I, Dixon H. The pathological response of the vessels of the placental bed to hypertensive pregnancy. J Pathol Bacteriol 1967; 93(2): 581-92.
Khong TY, DeWolf F, Robertson WB, Brosens I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 1986; 93(10): 1049-59.
Redman C, Sargent I. Microparticles and immunomodulation in pregnancy and pre-eclampsia. J Reprod Immunol 2007; 76(1-2): 61-7.
Heazell A, Moll S, Jones C, Baker P, Crocker I. Formation of syncytial knots is increased by hyperoxia, hypoxia and reactive oxygen speciesPlacenta 2007; 28: Suppl A: S33-40 Epub 2006 Nov 30
Chua S, Wilkins T, Sargent I, Redman C. Trophoblast deportation in pre-eclamptic pregnancy. Br J Obstet Gynaecol 1991; 98: 973-9.
Huppertz BJ. Placental villous trophoblast: the altered balance between proliferation and apoptosis triggers pre-eclampsia reproduktionsmed. Endokrinology 2006; 3(2): 103-8.
Crocker IP, Cooper S, Ong SC, Baker PN. Differences in apoptotic susceptibility of cytotrophoblasts and syncytiotrophoblasts in normal pregnancy to those complicated with preeclampsia and intrauterine growth restriction. Am J Pathol 2003; 162(2): 637-43.
Chen Q, Viall C, Kang Y, Liu B, Stone P, Chamley L. Antiphospholipid antibodies increase non-apoptotic trophoblast shedding: a contribution to the pathogenesis of pre-eclampsia in affected women? Placenta 2009; 30(9): 767-73.
Chen Q, Stone P, Ching L, Chamley L. A role for interleukin-6 in spreading endothelial cell activation after phagocytosis of necrotic trophoblastic material: implications for the pathogenesis of pre-eclampsia. J Pathol 2009; 217(1): 122-30.
Germain S, Sacks G, Soorana S, Sargent I, Redman C. Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of cirulating syncytiotrophoblast microparticles. J Immunol 2007; 178(9): 5949-56.
Sen CK, Gordillo GM, Khanna S, Roy S. Micromanaging vascular biology: tiny microRNAs play big band. J Vasc Res 2009; 46(6): 527-40.
Androulakis ES, Tousoulis D, Papageorgiou N, Tsioufis C, Kallikazaros I, Stefanadis C. Essential hypertension: is there a role for inflammatory mechanisms? Cardiol Rev 2009; 17(5): 216-21.
Libby P. Inflammation in atherosclerosis. Nature 2002; 420(6917): 868-74.
Leik C, Walsh S. Neutrophils infiltrate resistance-sized vessels of subcutaneous fat in women with pre-eclampsia. Hypertension 2004; 44(1): 72-7.
Sacks G, Studena K, Sargent K, Redman C. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 1998; 179(1): 80-6.
Cudihy D, Lee R. The pathophysiology of pre-eclampsia: current clinical concepts. J Obstet Gynaecol 2009; 29(7): 576-82.
Le J, Briggs GG, McKeown A, Bustillo G. Urinary tract infections during pregnancy. Ann Pharmacother 2004; 38(10): 1692-701.
O’Connell RM, Rao DS, Chaudhuri AA, Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 2010; 10(2): 111-22.
Carissimi C, Fulci V, Macino G. MicroRNAs: novel regulators of immunity. Autoimmun Rev 2009; 8(6): 520-4.
Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010; 11(9): 597-610.
Chen K, Rajewsky N. The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet 2007; 8(2): 93-103.
Lund E, Guttinger S, Calado A, Dahlberg JE, Kutay U. Nuclear export of microRNA precursors. Science 2004; 303(5654): 95-8.
Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136(2): 215-33.
Donker RB, Mouillet JF, Nelson DM, Sadovsky Y. The expression of Argonaute2 and related microRNA biogenesis proteins in normal and hypoxic trophoblasts. Mol Hum Reprod 2007; 13(4): 273-9.
Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest 1996; 97(2): 540-50.
Caniggia I, Winter J, Lye SJ, Post M. Oxygen and placental development during the first trimester: implications for the pathophysiology of pre-eclampsia. Placenta 2000; 21(Suppl. A): S25-30.
Adelman DM, Gertsenstein M, Nagy A, Simon MC, Maltepe E. Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 2000; 14(24): 3191-203.
Mouillet JF, Chu T, Nelson DM, Mishima T, Sadovsky Y. MiR-205 silences MED1 in hypoxic primary human trophoblasts. FASEB J 2010; 24(6): 2030-9.
Bavelloni A, Ramazzotti G, Poli A, et al. MiRNA-210: a current overview. Anticancer Res 2017; 37(12): 6511-21.
Zhang Y, Fei M, Xue G, et al. Elevated levels of hypoxia-inducible microRNA-210 in pre-eclampsia: new insights into molecular mechanisms for the disease. J Cell Mol Med 2012; 16(2): 249-59.
Dai Y, Diao Z, Sun H, Li R, Qiu Z, Hu Y. MicroRNA-155 is involved in the remodeling of human-trophoblast-derived HTR-8/SVneo cells induced by lipopolysaccharides. Hum Reprod 2011; 26(7): 1882-91.
Tsai KW, Kao HW, Chen HC, Chen SJ, Lin WC. Epigenetic control of the expression of a primate-specific microRNA cluster in human cancer cells. Epigenetics 2009; 4(8): 587-92.
Morales-Prieto DM, Schleussner E, Markert UR. Reduction in miR-141 is induced by leukemia inhibitory factor and inhibits proliferation in choriocarcinoma cell line JEG-3. Am J Reprod Immunol 2011; 66(Suppl. 1): 57-62.
Maccani MA, Avissar-Whiting M, Banister CE, Mc Gonnigal B, Padbury JF, Marsit CJ. Maternal cigarette smoking during pregnancy is associated with downregulation of miR-16, miR-21, and miR-146a in the placenta. Epigenetics 2010; 5(7): 583-9.
Karumanchi SA, Richard J. Levine How does smoking reduce the risk of preeclampsia? Hypertension 2010; 55(5): 1100-1.
Nothnick WB, Healy C. Estrogen induces distinct patterns of microRNA expression within the mouse uterus. Reprod Sci 2010; 17(11): 987-94.
Kuokkanen S, Chen B, Ojalvo L, Benard L, Santoro N, Pollard JW. Genomic profiling of microRNAs and messenger RNAs reveals hormonal regulation in microRNA expression in human endometrium. Biol Reprod 2010; 82(4): 791-801.
Nothnick WB, Healy C, Hong X. Steroidal regulation of uterine miRNAs is associated with modulation of the miRNA biogenesis components Exportin-5 and Dicer1. Endocrine 2010; 37(2): 265-73.
Gao WL, Liu M, Yang Y, et al. The imprinted H19 gene regulates human placental trophoblast cell proliferation via encoding miR-675 that targets nodal modulator 1 (NOMO1). RNA Biol 2012; 9(7): 1002-10.
Fu G, Ye G, Nadeem L, et al. MicroRNA-376c impairs transforming growth factor-beta and nodal signaling to promote trophoblast cell proliferation and invasion. Hypertension 2013; 61(4): 864-72.
Bai Y, Yang W, Yang H, et al. Downregulated miR-195 detected in preeclamptic placenta affects trophoblast cell invasion via modulating ActRIIA expression. PLoS One 2012; 7: e38875.
Luo L, Ye G, Nadeem L, et al. MicroRNA-378a-5p promotes trophoblast cell survival, migration and invasion by targeting nodal. J Cell Sci 2012; 125(Pt 13): 3124-32.
Baker AH, Delles C. Is microRNA-376c a biomarker or mediator of preeclampsia? Hypertension 2013; 61(4): 767-9.
Munir S, Xu G, Wu Y, Yang B, Lala PK, Peng C. Nodal and ALK7 inhibit proliferation and induce apoptosis in human trophoblast cells. J Biol Chem 2004; 279(30): 31277-86.
Li P, Guo W, Du L, et al. MicroRNA-29b contributes to pre-eclampsia through its effects on apoptosis, invasion and angiogenesis of trophoblast cells. Clin Sci 2013; 124(1): 27-40.
Harap Li Q, Pan Z, Wang X, Gao Z, Ren C, Yang W. miR-125b-1-3p inhibits trophoblastcell invasion by targeting sphingosine-1-phosphate receptor 1 in preeclampsia. Biochem Biophys Res Commun 2014; 453(1): 57-63.
Yang WJ, Yang DD, Na S, Sandusky GE, Zhang Q, Zhao G. Dicer is required for embryonic angiogenesis during mouse development. J Biol Chem 2005; 280(10): 9330-5.
Poliseno L, Tuccoli A, Mariani L, et al. MicroRNAs modulate the angiogenic properties of HUVECs. Blood 2006; 108(9): 3068-71.
Burton GJ, Charnock-Jones DS, Jauniaux E. Regulation of vascular growth and function in the human placenta. Reproduction 2009; 138(6): 895-902.
Suárez Y, Fernández-Hernando C, Pober J, et al. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 2007; 100(8): 1164-73.
Suárez Y, Fernández-Hernando C, Yu J, et al. Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci USA 2008; 105(37): 14082-7.
Wang A, Rana S, Karumanchi SA. Preeclampsia: the role of angiogenic factors in its pathogenesis. Physiology 2009; 24: 147-58.
Harapan H, Meurah Y. The role of microRNAs on angiogenesis and vascular pressure in preeclampsia: the evidence from systematic review. Egypt J Med Hum Genet 2015; 16(4): 313-25.
van Solingen C, Seghers L, Bijkerk R, et al. Antagomir-mediated silencing of endothelial cell specific microRNA-126 impairs ischemia-induced angiogenesis. J Cell Mol Med 2009; 13(8A): 1577-85.
Meister J, Schmidt MH. MiR-126 and miR-126*: new players in cancer. Sci World J 2010; 10: 2090-100.
Okamura K, Liu N, Lai EC. Distinct mechanisms for microRNA strand selection by Drosophila Argonautes. Mol Cell 2009; 36(3): 431-44.
Hong F, Li Y, Xu Y. Decreased placental miR-126 expression and vascular endothelial growth factor levels in patients with pre-eclampsia. J Int Med Res 2014; 42(6): 1243-51.
Yan T, Liu Y, Cui K, Hu B, Wang F, Zou L. MicroRNA-126 regulates EPCs function: implications for a role of miR-126 in preeclampsia. J Cell Biochem 2013; 114(9): 2148-59.
Fish JE, Santoro MM, Morton SU, et al. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 2008; 15(2): 272-84.
Wang W, Feng L, Zhang H, et al. Preeclampsia up-regulates angiogenesis-associated microRNA (i.e., miR-17, -20a, and -20b) that target ephrin-B2 and EPHB4 in human placenta. J Clin Endocrinol Metab 2012; 97(6): E1051-9.
Chennakesava CS, di Santo S, Ziemiecki A, Schneider H, Andres AC. Differential expression of the receptor tyrosine kinase EphB4 and its ligand Ephrin-B2 during human placental development. Placenta 2006; 27(9-10): 959-67.
Red-Horse K, Kapidzic M, Zhou Y, Feng KT, Singh H, Fisher SJ. EPHB4 regulates chemokine-evoked trophoblast responses: a mechanism for incorporating the human placenta into the maternal circulation. Development 2005; 132(18): 4097-106.
Wang Y, Zhang Y, Wang H, et al. Aberrantly upregulated miR-20a in pre-eclampsic placenta compromised the proliferative and invasive behaviors of trophoblast cells by targeting fork head box protein A1. Int J Biol Sci 2014; 10(9): 973-82.
Li P, Guo W, Du L, Zhao J, Wang Y, Liu L. MicroRNA-29b contributes to pre-eclampsia through its effects on apoptosis, invasion and angiogenesis of trophoblast cells. Clin Sci 2013; 124(1): 27-40.
Wang Y, Fan H, Zhao G, et al. MiR-16 inhibits the proliferation and angiogenesis-regulating potential of mesenchymal stem cells in severe pre-eclampsia. FEBS J 2012; 279(24): 4510-24.
Liu Q, Yang J. Expression and significance of miR-155 and vascular endothelial growth factor in placenta of rats with preeclampsia. Int J Clin Exp Med 2015; 8(9): 15731-7.
Shah DM. Role of the renin-angiotensin system in the pathogenesisof preeclampsia. Am J Physiol Renal Physiol 2005; 288(4): F614-25.
AbdAlla S, Lother H, el Massiery A, Quitterer U. Increased AT (1) receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat Med 2001; 7(9): 1003-9.
Walther T, Wallukat G, Jank A, et al. Angiotensin II type 1 receptor agonistic antibodies reflect fundamental alterations in the uteroplacental vasculature. Hypertension 2005; 46(6): 1275-9.
Wallukat G, Homuth V, Fischer T, et al. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest 1999; 103(7): 945-52.
Zhou CC, Zhang Y, Irani RA, et al. Angiotensin receptor agonistic autoantibodies induce preeclampsia in pregnant mice. Nat Med 2008; 14(8): 855-62.
Zhou CC, Irani RA, Dai Y, et al. Autoantibody-mediated IL-6 dependent endothelin-1 elevation underlies pathogenesis in a mouse model of preeclampsia. J Immunol 2011; 186(10): 6024-34.
Cheng W, Liu T, Jiang F, et al. MicroRNA-155 regulates angiotensin II type 1 receptor expression in umbilical vein endothelial cells from severely preeclamptic pregnant women. Int J Mol Med 2011; 27(3): 393-9.
Ceolotto G, Papparella I, Bortoluzzi A, et al. Interplay between miR-155, AT1R A1166C polymorphism, and AT1R expression in young untreated hypertensives. Am J Hypertens 2011; 24(2): 241-6.
Liu L, Wang Y, Fan H, et al. MicroRNA-181a regulates local immune balance by inhibiting proliferation and immunosuppressive properties of mesenchymal stem cells. Stem Cells 2012; 30(8): 1756-70.
Irani RA, Zhang Y, Blackwell SC, et al. The detrimental role of angiotensin receptor agonistic autoantibodies in intrauterine growth restriction seen in preeclampsia. J Exp Med 2009; 206(12): 2809-22.
Luft F. Soluble endoglin (sEng) joins the soluble fms-like tyrosine kinase (sFlt) receptor as a pre-eclampsia molecule. Nephrol Dial Transplant 2006; 21(11): 3052-4.
Fasanaro P, D’Alessandra Y, Di Stefano V, et al. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand ephrin-A3. J Biol Chem 2008; 283(23): 15878-83.
Lee DC, Romero R, Kim JS, et al. MiR-210 targets iron-sulfur cluster scaffold homologue in human trophoblast cell lines: siderosis of interstitial trophoblasts as a novel pathology of pretermpreeclampsia and small-for-gestational-age pregnancies. Am J Pathol 2011; 179(2): 590-602.
Rajakumar A, Brandon HM, Daftary A, Ness R, Conrad KP. Evidence for the functional activity of hypoxia- inducible transcription factors overexpressed in preeclamptic placentae. Placenta 2004; 25(100): 763-9.
Cicchillitti L, Di Stefano V, Isaia E, et al. Hypoxia-inducible factor 1-α induces miR-210 in normoxic differentiating myoblasts. J Biol Chem 2012; 287(53): 44761-71.
Kulshreshtha R, Ferracin M, Wojcik SE, et al. A microRNA signature of hypoxia. Mol Cell Biol 2007; 27(5): 1859-67.
Kelly TJ, Souza AL, Clish CB, Puigserver P. A hypoxia-induced positive feedback loop promotes hypoxia-inducible factor 1alpha stability through miR-210 suppression of glycerol-3-phosphate dehydrogenase 1-like. Mol Cell Biol 2011; 31(13): 2696-706.
Luo R, Shao X, Xu P, et al. MicroRNA-210 contributes to preeclampsia by downregulating potassium channel modulatory factor 1. Hypertension 2014; 64(4): 839-45.
Beilke S, Oswald F, Genze F, Wirth T, Adler G, Wagner M. The zinc-finger protein KCMF1 is overexpressed during pancreatic cancer development and downregulation of KCMF1 inhibits pancreatic cancer development in mice. Oncogene 2010; 29(28): 4058-67.
Anton L, Olarerin-George AO, Schwartz N, et al. miR-210 inhibits trophoblast invasion and is a serum biomarker for preeclampsia. Am J Pathol 2013; 183(5): 1437-45.
Ishibashi O, Ohkuchi A, Ali MM, et al. Hydroxysteroid (17-beta) dehydrogenase 1 is dysregulated by miR-210 and miR-518c that are aberrantly expressed in preeclamptic placentas: a novel marker for predicting preeclampsia. Hypertension 2012; 59(2): 265-73.
Kopriva SE, Chiasson VL, Mitchell BM, Chatterjee P. TLR3-induced placental miR-210 down-regulates the STAT6/interleukin-4 pathway. PLoS One 2013; 8(7): e67760.
Azizieh F, Raghupathy R, Makhseed M. Maternal cytokine production patterns in women with pre-eclampsia. Am J Reprod Immunol 2005; 54(1): 30-7.
Trowsdale J, Betz A. Mothers little helpers: mechanisms of maternal-fetal tolerance. Nat Immunol 2006; 7(3): 241-24.
Blaschitz A, Hutter H, Dohr G. HLA class I protein expression in the human placenta. Early Pregnancy 2001; 5(1): 67-9.
Hofmeister V, Weiss E. HLA-G modulates immune responses by diverse receptor interactions. Semin Cancer Biol 2003; 13(5): 317-23.
Quenby S, Farquharson R. Uterine natural killer cells, implantation failure and recurrent miscarriage. Reprod Biomed Online 2006; 13(1): 24-8.
Tabiasco J, Rabot M, Aguerre-Girr M, et al. Human decidual NK cells: unique phenotype and functional properties: a review. Placenta 2006; 27(Suppl. A): S34-9.
Manaster I, Goldman-Wohl D, Greenfield C, et al. MiRNA-mediated control of HLA-G expression and function. PLoS One 2012; 7: e33395.
Zhu XM, Han T, Wang XH, et al. Overexpression of miR-152 leads to reduced expression of human leukocyte antigen-G and increased natural killer cell mediated cytolysis in JEG-3 cells. Am J Obstet Gynecol 2010; 202(6): 592.e1-7.
Jenny L, Sones I, Heinrich EL, Catherine EI, et al. Role of decidual natural killer cells, interleukin-15, and interferon-in placental development and preeclampsia. Am J Physiol Regul Integr Comp Physiol 2014; 307(5): R490-2.
Murphy SP, Tayade C, Ashkar AA, Hatta K, Zhang J, Croy BA. Interferon gamma in successful pregnancies. Biol Reprod 2009; 80(5): 848-59.
O’Connell RM, Rao DS, Chaudhuri AA, Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 2010; 10(2): 111-22.
Smith S, Dunk C, Aplin J, Harris L, Jones R. Evidence for immune cell involvement in decidual spiral arteriole remodelin in early human pregnancy. Am J Pathol 2009; 174(5): 1959-71.
Greenwood J, Minhas K, Di Santo J, Makita M, Kiso Y, Croy B. Ultrastructural studies of implantation sites from mice deficient in uterine natural killer cells. Placenta 2000; 21(7): 693-702.
Fehniger TA, Wylie T, Germino E, et al. Next-generation sequencing identifies the natural killer cell microRNA transcriptome. Genome Res 2010; 20(11): 1590-604.
Chen Q, Wang H, Liu Y, et al. Inducible microRNA-223 down-regulation promotes TLR-triggered IL-6 and IL-1β production in macrophages by targeting STAT3. PLoS One 2012; 7(8): e42971.
Xu P, Zhao Y, Liu M, et al. Variations of microRNAs in human placentas and plasma from preeclamptic pregnancy. Hypertension 2014; 63(6): 1276-84.
Haneklaus M, Gerlic M, O’Neill LJ, Masters SL. miR-223: infection, inflammation and cancer. J Intern Med 2013; 274(3): 215-26.
Lappas M, Lim R, Riley C, Rice GE, Permezel M. Localisation and expression of FoxO1 proteins in human gestational tissues. Placenta 2009; 30(3): 256-62.
Sheridan R, Belludi C, Khoury J, Stanek J, Handwerger S. FOXO1 expression in villous trophoblast of preeclampsia and fetal growth restriction placentas. Histol Histopathol 2015; 30(2): 213-22.
Lockwood CJ, Yen CF, Basar M, et al. Preeclampsia-related inflammatory cytokines regulate interleukin-6 expression in human decidual cells. Am J Pathol 2008; 172(6): 1571-9.
John ES, Laura H, Zhang B, Sarah AR. The role of microRNA miR223 in immune adaptation for pregnancy and fetal-placental development. Placenta 2015; 36(9): A9.
Redman CWG, Sargent IL. Immunology of pre-eclampsia. Am J Reprod Immunol 2010; 63(6): 534-43.

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Year: 2019
Published on: 27 November, 2018
Page: [28 - 35]
Pages: 8
DOI: 10.2174/2211536607666180813123303
Price: $65

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