Placental expression of miR-517a/b and miR-517c contributes to trophoblast dysfunction and preeclampsia

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Anton, Lauren ^a   Olarerin George, Anthony O ^a   Hogenesch, John B ^a   Elovitz, Michal A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 517A B; MICRORNA 517C; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL GROWTH INHIBITOR; VASCULOTROPIN RECEPTOR 1; COBALT; COBALT CHLORIDE; FLT1 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PGF PROTEIN, HUMAN; PLACENTA PROTEIN; PLACENTAL GROWTH FACTOR; TNFSF15 PROTEIN, HUMAN; VASCULOTROPIN A;

ADULT; ARTICLE; CASE CONTROL STUDY; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; HUMAN; HUMAN CELL; HYPOXIA; MOLECULAR PATHOLOGY; PREECLAMPSIA; PREMATURITY; PROTEIN EXPRESSION; TERM BIRTH; TROPHOBLASTIC DISEASE; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL HYPOXIA; CELL MOTION; CYTOLOGY; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PLACENTA; PREGNANCY; RNA SPLICING; TROPHOBLAST; UPREGULATION;

CASE-CONTROL STUDIES; CELL HYPOXIA; CELL MOVEMENT; CELLS, CULTURED; COBALT; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICRORNAS; PLACENTA; PLACENTA GROWTH FACTOR; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY PROTEINS; RNA SPLICING; TROPHOBLASTS; TUMOR NECROSIS FACTOR LIGAND SUPERFAMILY MEMBER 15; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84925742893     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122707     Document Type: Article

References (66)

1. Chang J, Elam-Evans LD, Berg CJ, Herndon J, Flowers L, Seed KA, et al. Pregnancy-related mortality surveillance-United States, 1991-1999. MMWR Surveill Summ. 2003; 52: 1-8. PMID: 14647014
2. Koonin LM, Atrash HK, RochatRW, Smith JC. Maternal mortality surveillance, United States, 1980-1985. MMWR CDC Surveill Summ. 1988; 37: 19-29. PMID: 3148106
3. Steegers EAP, von Dadelszen P, Duvekot JJ, Pijnenborg R. Pre-eclampsia. The Lancet. 2010; 376: 631-644. doi: 10.1016/S0140-6736(10)60279-6 PMID: 20598363
4. Meekins JW, Pijnenborg R, Hanssens M, McFadyen IR, van Asshe A. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol. 1994; 101: 669-674. PMID: 7947500
5. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest. 2003; 111: 649-658. PMID: 12618519
6. Taylor RN, Grimwood J, Taylor RS, McMaster MT, Fisher SJ, North RA. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol. 2003; 188: 177-182. PMID: 12548214
7. Soleymanlou N, Jurisica I, Nevo O, Ietta F, Zhang X, Zamudio S, et al. Molecular Evidence of Placental Hypoxia in Preeclampsia. Journal of Clinical Endocrinology & Metabolism. 2005; 90: 4299-4308.
8. Laresgoiti-Servitje E, Gomez-Lopez N, Olson DM. An immunological insight into the origins of preeclampsia. Human Reproduction Update. 2010; 16: 510-524. doi: 10.1093/humupd/dmq007 PMID: 20388637
9. Brosens I, Robertson WB, Dixon HG. The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol. 1967; 93: 569-579. PMID: 6054057
10. Karumanchi SA, Bdolah Y. Hypoxia and sFlt-1 in Preeclampsia: The Chicken-and-Egg Question. Endocrinology. 2004; 145: 4835-4837. PMID: 15489315
11. Murphy SR, LaMarca BBD, Parrish M, Cockrell K, Granger JP. Control of soluble fms-like tyrosine-1 (sFlt-1) production response to placental ischemia/hypoxia: role of tumor necrosis factor-a. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 2013; 304: R130-R135.
12. Conrad KP, Miles TM, Benyo DF. Circulating levels of immunoreactive cytokines in women with preeclampsia. Am J Reprod Immunol. 1998; 40: 102-111. PMID: 9764352
13. LaMarca B, Ryan M, Gilbert J, Murphy S, Granger J. Inflammatory cytokines in the pathophysiology of hypertension during preeclampsia. Current Hypertension Reports. 2007; 9: 480-485. PMID: 18367011
14. Qi J-W, Qin T-T, Xu L-X, Zhang K, Yang G-L, Li J, et al. TNFSF15 inhibits vasculogenesis by regulating relative levels of membrane-bound and soluble isoforms of VEGF receptor 1. Proceedings of the National Academy of Sciences. 2013; 110: 13863-13868. doi: 10.1073/pnas.1304529110 PMID: 23918400
15. Enquobahrie DA, Meller M, Rice K, Psaty BM, Siscovick DS, Williams MA. Differential placental gene expression in preeclampsia. American Journal of Obstetrics and Gynecology. 2008; 199: 566.e561-566. e511.
16. Sitras V, Paulssen RH, Gronaas H, Leirvik J, Hanssen TA, Vartun A, et al. Differential Placental Gene Expression in Severe Preeclampsia. Placenta. 2009; 30: 424-433. doi: 10.1016/j.placenta.2009.01. 012 PMID: 19249095
17. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116: 281-297. PMID: 14744438
18. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of micro-RNAs. Genome Res. 2009; 19: 92-105. doi: 10.1101/gr.082701.108 PMID: 18955434
19. Barad O, Meiri E, Avniel A, Aharonov R, Barzilai A, Bentwich I, et al. MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Res. 2004; 14: 2486-2494. PMID: 15574827
20. Wang W, Feng L, Zhang H, Hachy S, Satohisa S, Laurent LC, 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: E1051-1059. doi: 10.1210/jc.2011-3131 PMID: 22438230
21. Noguer-Dance M, Abu-Amero S, Al-Khtib M, Lefevre A, Coullin P, Moore GE, et al. The primate-specific microRNA gene cluster (C19MC) is imprinted in the placenta. Hum Mol Genet. 2010; 19: 3566-3582. doi: 10.1093/hmg/ddq272 PMID: 20610438
22. Zhang R, Wang YQ, Su B. Molecular evolution of a primate-specific microRNA family. Mol Biol Evol. 2008; 25: 1493-1502. doi: 10.1093/molbev/msn094 PMID: 18417486
23. Luo SS, Ishibashi O, Ishikawa G, Ishikawa T, Katayama A, Mishima T, et al. Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol Reprod. 2009; 81: 717-729. doi: 10.1095/biolreprod.108.075481 PMID: 19494253
24. Donker RB, Mouillet JF, Chu T, Hubel CA, Stolz DB, Morelli AE, et al. The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes. Mol Hum Reprod. 2012; 18: 417-424. doi: 10.1093/molehr/gas013 PMID: 22383544
25. Bentwich I, Avniel A, Karov Y, Aharonov R, Gilad S, Barad O, et al. Identification of hundreds of conserved and nonconserved human microRNAs. Nat Genet. 2005; 37: 766-770. PMID: 15965474
26. Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Research. 2014; 42: D68-D73. doi: 10.1093/nar/gkt1181 PMID: 24275495
27. Pineles BL, Romero R, Montenegro D, Tarca AL, Han YM, Kim YM, et al. Distinct subsets of micro-RNAs are expressed differentially in the human placentas of patients with preeclampsia. Am J Obstet Gynecol. 2007; 196: 261 e261-266. PMID: 17346547
28. Zhu XM, Han T, Sargent IL, Yin GW, Yao YQ. Differential expression profile of microRNAs in human placentas from preeclamptic pregnancies vs normal pregnancies. Am J Obstet Gynecol. 2009; 200: 661 e661-667. doi: 10.1016/j.ajog.2008.12.045 PMID: 19285651
29. Enquobahrie DA, Abetew DF, Sorensen TK, Willoughby D, Chidambaram K, Williams MA. Placental microRNA expression in pregnancies complicated by preeclampsia. Am J Obstet Gynecol. 2011; 204: 178 e112-121.
30. Ishibashi O, Ohkuchi A, Ali MM, Kurashina R, Luo S-S, Ishikawa T, et al. Hydroxysteroid (17-B) 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: 265-273. doi:10.1161/HYPERTENSIONAHA.111.180232 PMID: 22203747
31. Srinivas SK, Srinivas SK, Sammel MD, Bastek J, Ofori E, Andrela CM, et al. Evaluating the association between all components of the metabolic syndrome and pre-eclampsia. Journal of Maternal-Fetal and Neonatal Medicine. 2009; 22: 501-509. doi: 10.1080/14767050902794642 PMID: 19479639
32. Srinivas SK,Morrison AC, Andrela CM, Elovitz MA. Allelic variations in angiogenic pathway genes are associated with preeclampsia. American Journal of Obstetrics and Gynecology. 2010; 202: 445.e441-445. e411.
33. Anton L, Olarerin-George AO, Schwartz N, Srinivas S, Bastek J, Hogenesch JB, et al. miR-210 Inhibits Trophoblast Invasion and Is a Serum Biomarker for Preeclampsia. The American Journal of Pathology. 2013; 183: 1437-1445. doi: 10.1016/j.ajpath.2013.07.021 PMID: 24035613
34. Getsios S, Chen GT, Huang DT, MacCalman CD. Regulated expression of cadherin-11 in human extravillous cytotrophoblasts undergoing aggregation and fusion in response to transforming growth factor beta 1. J Reprod Fertil. 1998; 114: 357-363. PMID: 10070366
35. Anton L, Brown AG, Parry S, Elovitz MA. Lipopolysaccharide induces cytokine production and decreases extravillous trophoblast invasion through a mitogen-activated protein kinase-mediated pathway: possible mechanisms of first trimester placental dysfunction. Hum Reprod. 2012; 27: 61-72. doi: 10.1093/humrep/der362 PMID: 22052387
36. Graham CH, Lysiak JJ, McCrae KR, Lala PK. Localization of transforming growth factor-beta at the human fetal-maternal interface: role in trophoblast growth and differentiation. Biol Reprod. 1992; 46: 561-572. PMID: 1374270
37. Koi H, Zhang J,Makrigiannakis A, Getsios S, MacCalman CD, Strauss JF 3rd, et al. Syncytiotrophoblast is a barrier to maternal-fetal transmission of herpes simplex virus. Biol Reprod. 2002; 67: 1572-1579. PMID: 12390890
38. Neudeck H, Oei SL, Stiemer B, Hopp H, Graf R. Binding of antibodies against high and low molecular weight cytokeratin proteins in the human placenta with special reference to infarcts, proliferation and differentiation processes. Histochem J. 1997; 29: 419-430. PMID: 9184857
39. Gomez LM, Anton L, Srinivas SK, Elovitz MA, Parry S. Effects of increased fetuin-A in human trophoblast cells and associated pregnancy outcomes. Am J Obstet Gynecol. 2012; 207: 484 e481-488. doi: 10.1016/j.ajog.2012.10.872 PMID: 23108067
40. Yaung J, Kannan R, Wawrousek EF, Spee C, Sreekumar PG, Hinton DR. Exacerbation of retinal degeneration in the absence of alpha crystallins in an in vivo model of chemically induced hypoxia. Exp Eye Res. 2008; 86: 355-365. doi: 10.1016/j.exer.2007.11.007 PMID: 18191123
41. Piret JP, Mottet D, RaesM, Michiels C. CoCl2, a chemical inducer of hypoxia-inducible factor-1, and hypoxia reduce apoptotic cell death in hepatoma cell line HepG2. Ann N Y Acad Sci. 2002; 973: 443-447. PMID: 12485908
42. 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. The Journal of Clinical Investigation. 1996; 97: 540-550. PMID: 8567979
43. Zhou Y, Genbacev O, Damsky CH, Fisher SJ. Oxygen regulates human cytotrophoblast differentiation and invasion: implications for endovascular invasion in normal pregnancy and in pre-eclampsia. Journal of Reproductive Immunology. 1998; 39: 197-213. PMID: 9786462
44. Boeckel J-N, Guarani V, Koyanagi M, Roexe T, Lengeling A, Schermuly RT, et al. Jumonji domaincontaining protein 6 (Jmjd6) is required for angiogenic sprouting and regulates splicing of VEGFreceptor 1. Proceedings of the National Academy of Sciences. 2011; 108: 3276-3281. doi: 10.1073/ pnas.1008098108 PMID: 21300889
45. Miura K, Morisaki S, Abe S, Higashijima A, Hasegawa Y, Miura S, et al. Circulating levels of maternal plasma cell-free pregnancy-associated placenta-specific microRNAs are associated with placental weight. Placenta. 2014; 35: 848-851. doi: 10.1016/j.placenta.2014.06.002 PMID: 25015175
46. Miura K, Miura S, Yamasaki K, Higashijima A, Kinoshita A, Yoshiura K-i, et al. Identification of Pregnancy-Associated MicroRNAs in Maternal Plasma. Clinical Chemistry. 2010; 56: 1767-1771. doi: 10.1373/ clinchem.2010.147660 PMID: 20729298
47. Kambe S, Yoshitake H, Yuge K, Ishida Y, Ali MM, Takizawa T, et al. Human Exosomal Placenta-Associated miR-517a-3p Modulates the Expression of PRKG1 mRNA in Jurkat Cells. Biology of Reproduction. 2014.
48. Mouillet J-F, Chu T, Nelson DM, Mishima T, Sadovsky Y. MiR-205 silences MED1 in hypoxic primary human trophoblasts. The FASEB Journal. 2010; 24: 2030-2039. doi: 10.1096/fj.09-149724 PMID: 20065103
49. Mouillet JF, Chu T, Hubel CA, Nelson DM, Parks WT, Sadovsky Y. The levels of hypoxia-regulated microRNAs in plasma of pregnant women with fetal growth restriction. Placenta. 2010; 31: 781-784. doi: 10.1016/j.placenta.2010.07.001 PMID: 20667590
50. Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK, et al. Hypoxia-Inducible mir-210 Regulates Normoxic Gene Expression Involved in Tumor Initiation. Molecular Cell. 2009; 35: 856-867. doi: 10.1016/j.molcel.2009.09.006 PMID: 19782034
51. Tsai KW, Kao HW, Chen HC, Chen SJ, Lin WC. Epigenetic control of the expression of a primatespecific microRNA cluster in human cancer cells. Epigenetics. 2009; 4: 587-592. PMID: 19923923
52. Yuen RKC, Chen B, Blair JD, Robinson WP, Nelson DM. Hypoxia alters the epigenetic profile in cultured human placental trophoblasts. Epigenetics. 2013; 8: 192-202. doi: 10.4161/epi.23400 PMID: 23314690
53. Liu R-F, Xu X, Huang J, Fei Q-L, Chen F, Li Y-D, et al. Down-regulation of miR-517a and miR-517c promotes proliferation of hepatocellular carcinoma cells via targeting Pyk2. Cancer Letters. 2013; 329: 164-173. doi: 10.1016/j.canlet.2012.10.027 PMID: 23142219
54. Xie L, Mouillet J-F, Chu T, Parks WT, Sadovsky E, Knöfler M, et al. C19MC MicroRNAs Regulate the Migration of Human Trophoblasts. Endocrinology. 2014; 155: 4975-4985. doi: 10.1210/en.2014-1501 PMID: 25211593
55. Liu X-h, Lu K-h, Wang K-m, Sun M, Zhang E-b, Yang J-s, et al. MicroRNA-196a promotes non-small cell lung cancer cell proliferation and invasion through targeting HOXA5. BMC Cancer. 2012; 12: 348. doi: 10.1186/1471-2407-12-348 PMID: 22876840
56. Nguyen Q-D, Rodrigues S, Rodrigue CM, Rivat C, Grijelmo C, Bruyneel E, et al. Inhibition of vascular endothelial growth factor (VEGF)-165 and semaphorin 3Aâ€"mediated cellular invasion and tumor growth by the VEGF signaling inhibitor ZD4190 in human colon cancer cells and xenografts. Molecular Cancer Therapeutics. 2006; 5: 2070-2077. PMID: 16928828
57. Biadasiewicz K, Sonderegger S, Haslinger P, Haider S, Saleh L, Fiala C, et al. Transcription Factor AP-2α Promotes EGF-Dependent Invasion of Human Trophoblast. Endocrinology. 2011; 152: 1458-1469. doi: 10.1210/en.2010-0936 PMID: 21303946
58. Staun-Ram E, Goldman S, Shalev E. p53 Mediates Epidermal Growth Factor (EGF) Induction of MMP-2 Transcription and Trophoblast Invasion. Placenta. 2009; 30: 1029-1036. doi: 10.1016/j.placenta. 2009.09.010 PMID: 19853299
59. Lipinski CA, Tran NL, Menashi E, Rohl C, Kloss J, Bay RC, et al. The tyrosine kinase pyk2 promotes migration and invasion of glioma cells. Neoplasia. 2005; 7: 435-445. PMID: 15967096
60. Maynard SE, Min J-Y, Merchan J, Lim K-H, Li J, Mondal S, et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. The Journal of Clinical Investigation. 2003; 111: 649-658. PMID: 12618519
61. Ahmad S, Ahmed A. Elevated Placental Soluble Vascular Endothelial Growth Factor Receptor-1 Inhibits Angiogenesis in Preeclampsia. Circulation Research. 2004; 95: 884-891. PMID: 15472115
62. Yu J, Tian S, Metheny-Barlow L, Chew L-J, Hayes AJ, Pan H, et al. Modulation of Endothelial Cell Growth Arrest and Apoptosis by Vascular Endothelial Growth Inhibitor. Circulation Research. 2001; 89: 1161-1167. PMID: 11739281
63. Zhai Y, Ni J, Jiang G-w, Lu J, Xing L, Lincoln C, et al. VEGI, a novel cytokine of the tumor necrosis factor family, is an angiogenesis inhibitor that suppresses the growth of colon carcinomas in vivo. The FASEB Journal. 1999; 13: 181-189. PMID: 9872942
64. Webby CJ,Wolf A, Gromak N, DregerM, Kramer H, Kessler B, et al. Jmjd6 Catalyses Lysyl-Hydroxylation of U2AF65, a Protein Associated with RNA Splicing. Science. 2009; 325: 90-93. doi: 10.1126/science. 1175865 PMID: 19574390
65. Olarerin-George AO, Anton L, Hwang YC, Elovitz MA, Hogenesch JB. A functional genomics screen for microRNA regulators of NF-kappaB signaling. BMC Biol. 2013; 11: 19. doi: 10.1186/1741-7007-11-19 PMID: 23448136
66. Endo K, Kinouchi Y, Kakuta Y, Ueki N, Takahashi S, Shimosegawa T. Involvement of NF-kappa B pathway in TL1A gene expression induced by lipopolysaccharide. Cytokine. 2010; 49: 215-220. doi:10.1016/j.cyto.2009.09.006 PMID: 19815424