Advertisement

Preeclampsia pp 209-224 | Cite as

MicroRNA

  • Toshihiro TakizawaEmail author
  • Akihide Ohkuchi
  • Shigeki Matsubara
  • Toshiyuki Takeshita
  • Shigeru Saito
Chapter
Part of the Comprehensive Gynecology and Obstetrics book series (CGO)

Abstract

Aberrant expression of microRNAs (miRNAs) occurs in the preeclamptic placenta, where it causes dysregulation of functional molecules. The human placenta expresses a unique set of miRNAs (e.g., chromosome 19 miRNA cluster miRNAs). miRNAs, including placenta-specific miRNAs, are released from the placental villous trophoblast into the maternal circulation via exosomes. Because placenta-specific miRNAs are detectable in maternal blood, information about the placenta can be obtained during routine pregnancy screening via minimally invasive tests such as blood sampling, rather than highly invasive tests such as tissue biopsy. Radical treatment for preeclampsia (PE) is termination of the pregnancy, but in cases of early-onset PE, the pregnancy should be prolonged as long as possible to improve the infant’s prognosis. Prediction of PE in the first trimester could make it possible to prevent PE and develop novel therapeutic strategies to treat PE. This chapter explores the predictive utility of plasma placenta-specific miRNAs.

Keywords

Placenta-specific microRNA Exosome Maternal plasma Early-onset preeclampsia 

Notes

Acknowledgments

This work was supported by Grants-in-Aids for Scientific Research and Private University Strategic Research Foundation Support Program (2013–2017) from the Ministry of Education, Culture, Sports, Science and Technology/Japan Society for the Promotion of Science, Japan.

References

  1. 1.
    Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215–33.  https://doi.org/10.1016/j.cell.2009.01.002.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Esteller M. Non-coding RNAs in human disease. Nat Rev Genet. 2011;12(12):861–74.  https://doi.org/10.1038/nrg3074.CrossRefPubMedGoogle Scholar
  3. 3.
    Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC. Mammalian mirtron genes. Mol Cell. 2007;28(2):328–36.  https://doi.org/10.1016/j.molcel.2007.09.028.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Castellano L, Stebbing J. Deep sequencing of small RNAs identifies canonical and non-canonical miRNA and endogenous siRNAs in mammalian somatic tissues. Nucleic Acids Res. 2013;41(5):3339–51.  https://doi.org/10.1093/nar/gks1474.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Miyoshi K, Miyoshi T, Siomi H. Many ways to generate microRNA-like small RNAs: non-canonical pathways for microRNA production. Mol Gen Genomics. 2010;284(2):95–103.  https://doi.org/10.1007/s00438-010-0556-1.CrossRefGoogle Scholar
  6. 6.
    Ladewig E, Okamura K, Flynt AS, Westholm JO, Lai EC. Discovery of hundreds of mirtrons in mouse and human small RNA data. Genome Res. 2012;22(9):1634–45.  https://doi.org/10.1101/gr.133553.111.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Schamberger A, Sarkadi B, Orban TI. Human mirtrons can express functional microRNAs simultaneously from both arms in a flanking exon-independent manner. RNA Biol. 2012;9(9):1177–85.  https://doi.org/10.4161/rna.21359.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Xie M, Li M, Vilborg A, Lee N, Shu MD, Yartseva V, et al. Mammalian 5′-capped microRNA precursors that generate a single microRNA. Cell. 2013;155(7):1568–80.  https://doi.org/10.1016/j.cell.2013.11.027.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Yang JS, Maurin T, Robine N, Rasmussen KD, Jeffrey KL, Chandwani R, et al. Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc Natl Acad Sci U S A. 2010;107(34):15163–8.  https://doi.org/10.1073/pnas.1006432107.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Kim M, Tan YS, Cheng WC, Kingsbury TJ, Heimfeld S, Civin CI. MIR144 and MIR451 regulate human erythropoiesis via RAB14. Br J Haematol. 2015;168(4):583–97.  https://doi.org/10.1111/bjh.13164.CrossRefPubMedGoogle Scholar
  11. 11.
    Morin RD, O'Connor MD, Griffith M, Kuchenbauer F, Delaney A, Prabhu AL, et al. Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res. 2008;18(4):610–21.  https://doi.org/10.1101/gr.7179508.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Vickers KC, Sethupathy P, Baran-Gale J, Remaley AT. Complexity of microRNA function and the role of isomiRs in lipid homeostasis. J Lipid Res. 2013;54(5):1182–91.  https://doi.org/10.1194/jlr.R034801.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Xia J, Zhang W. A meta-analysis revealed insights into the sources, conservation and impact of microRNA 5′-isoforms in four model species. Nucleic Acids Res. 2014;42(3):1427–41.  https://doi.org/10.1093/nar/gkt967.CrossRefPubMedGoogle Scholar
  14. 14.
    Wyman SK, Knouf EC, Parkin RK, Fritz BR, Lin DW, Dennis LM, et al. Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Res. 2011;21(9):1450–61.  https://doi.org/10.1101/gr.118059.110.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    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.  https://doi.org/10.1093/molehr/gam006.CrossRefPubMedGoogle Scholar
  16. 16.
    Forbes K, Farrokhnia F, Aplin JD, Westwood M. Dicer-dependent miRNAs provide an endogenous restraint on cytotrophoblast proliferation. Placenta. 2012;33(7):581–5.  https://doi.org/10.1016/j.placenta.2012.03.006.CrossRefPubMedGoogle Scholar
  17. 17.
    Forbes K. IFPA Gabor Than Award lecture: molecular control of placental growth: the emerging role of microRNAs. Placenta. 2013;34(Suppl):S27–33.  https://doi.org/10.1016/j.placenta.2012.12.011.CrossRefPubMedGoogle Scholar
  18. 18.
    Yang M, Chen Y, Chen L, Wang K, Pan T, Liu X, et al. miR-15b-AGO2 play a critical role in HTR8/SVneo invasion and in a model of angiogenesis defects related to inflammation. Placenta. 2016;41:62–73.  https://doi.org/10.1016/j.placenta.2016.03.007.CrossRefPubMedGoogle Scholar
  19. 19.
    Zhang R, Wang YQ, Su B. Molecular evolution of a primate-specific microRNA family. Mol Biol Evol. 2008;25(7):1493–502.  https://doi.org/10.1093/molbev/msn094.CrossRefPubMedGoogle Scholar
  20. 20.
    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(4):717–29.  https://doi.org/10.1095/biolreprod.108.075481. CrossRefPubMedGoogle Scholar
  21. 21.
    Zhou X, Li Q, Xu J, Zhang X, Zhang H, Xiang Y, et al. The aberrantly expressed miR-193b-3p contributes to preeclampsia through regulating transforming growth factor-beta signaling. Sci Rep. 2016;6:19910.  https://doi.org/10.1038/srep19910.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Morales-Prieto DM, Ospina-Prieto S, Chaiwangyen W, Schoenleben M, Markert UR. Pregnancy-associated miRNA-clusters. J Reprod Immunol. 2013;97(1):51–61.  https://doi.org/10.1016/j.jri.2012.11.001.CrossRefPubMedGoogle Scholar
  23. 23.
    Morales-Prieto DM, Ospina-Prieto S, Schmidt A, Chaiwangyen W, Markert UR. Elsevier Trophoblast Research Award Lecture: origin, evolution and future of placenta miRNAs. Placenta. 2014;35(Suppl):S39–45.  https://doi.org/10.1016/j.placenta.2013.11.017.CrossRefPubMedGoogle Scholar
  24. 24.
    Seitz H, Royo H, Bortolin ML, Lin SP, Ferguson-Smith AC, Cavaille J. A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain. Genome Res. 2004;14(9):1741–8.  https://doi.org/10.1101/gr.2743304.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    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(18):3566–82.  https://doi.org/10.1093/hmg/ddq272.CrossRefPubMedGoogle Scholar
  26. 26.
    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(7):766–70.  https://doi.org/10.1038/ng1590.CrossRefPubMedGoogle Scholar
  27. 27.
    Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9(6):654–9.  https://doi.org/10.1038/ncb1596.CrossRefPubMedGoogle Scholar
  28. 28.
    Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 2010;285(23):17442–52.  https://doi.org/10.1074/jbc.M110.107821.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, et al. The microRNA spectrum in 12 body fluids. Clin Chem. 2010;56(11):1733–41.  https://doi.org/10.1373/clinchem.2010.147405.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    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(8):417–24.  https://doi.org/10.1093/molehr/gas013.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Dragovic RA, Collett GP, Hole P, Ferguson DJ, Redman CW, Sargent IL, et al. Isolation of syncytiotrophoblast microvesicles and exosomes and their characterisation by multicolour flow cytometry and fluorescence Nanoparticle Tracking Analysis. Methods. 2015;87:64–74.  https://doi.org/10.1016/j.ymeth.2015.03.028.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Vargas A, Zhou S, Ethier-Chiasson M, Flipo D, Lafond J, Gilbert C, et al. Syncytin proteins incorporated in placenta exosomes are important for cell uptake and show variation in abundance in serum exosomes from patients with preeclampsia. FASEB J. 2014;28(8):3703–19.  https://doi.org/10.1096/fj.13-239053.CrossRefPubMedGoogle Scholar
  33. 33.
    Mincheva-Nilsson L, Baranov V. The role of placental exosomes in reproduction. Am J Reprod Immunol. 2010;63(6):520–33.  https://doi.org/10.1111/j.1600-0897.2010.00822.x.CrossRefPubMedGoogle Scholar
  34. 34.
    Tannetta D, Masliukaite I, Vatish M, Redman C, Sargent I. Update of syncytiotrophoblast derived extracellular vesicles in normal pregnancy and preeclampsia. J Reprod Immunol. 2016.  https://doi.org/10.1016/j.jri.2016.08.008.
  35. 35.
    Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A. 2011;108(12):5003–8.  https://doi.org/10.1073/pnas.1019055108.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011;39(16):7223–33.  https://doi.org/10.1093/nar/gkr254.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011;13(4):423–33.  https://doi.org/10.1038/ncb2210.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Salomon C, Torres MJ, Kobayashi M, Scholz-Romero K, Sobrevia L, Dobierzewska A, et al. A gestational profile of placental exosomes in maternal plasma and their effects on endothelial cell migration. PLoS One. 2014;9(6):e98667.  https://doi.org/10.1371/journal.pone.0098667.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Sarker S, Scholz-Romero K, Perez A, Illanes SE, Mitchell MD, Rice GE, et al. Placenta-derived exosomes continuously increase in maternal circulation over the first trimester of pregnancy. J Transl Med. 2014;12:204.  https://doi.org/10.1186/1479-5876-12-204.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Dragovic RA, Southcombe JH, Tannetta DS, Redman CW, Sargent IL. Multicolor flow cytometry and nanoparticle tracking analysis of extracellular vesicles in the plasma of normal pregnant and pre-eclamptic women. Biol Reprod. 2013;89(6):151.  https://doi.org/10.1095/biolreprod.113.113266. CrossRefPubMedGoogle Scholar
  41. 41.
    Goswami D, Tannetta DS, Magee LA, Fuchisawa A, Redman CW, Sargent IL, et al. Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta. 2006;27(1):56–61.  https://doi.org/10.1016/j.placenta.2004.11.007.CrossRefPubMedGoogle Scholar
  42. 42.
    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. Biol Reprod. 2014;91(5):129.  https://doi.org/10.1095/biolreprod.114.121616. CrossRefPubMedGoogle Scholar
  43. 43.
    Takahashi H, Ohkuchi A, Kuwata T, Usui R, Baba Y, Suzuki H, et al. Endogenous and exogenous miR-520c-3p modulates CD44-mediated extravillous trophoblast invasion. Placenta. 2017;50:25–31.CrossRefPubMedGoogle Scholar
  44. 44.
    Mitchell MD, Peiris HN, Kobayashi M, Koh YQ, Duncombe G, Illanes SE, et al. Placental exosomes in normal and complicated pregnancy. Am J Obstet Gynecol. 2015;213(4 Suppl):S173–81.  https://doi.org/10.1016/j.ajog.2015.07.001. CrossRefPubMedGoogle Scholar
  45. 45.
    Mouillet JF, Ouyang Y, Coyne CB, Sadovsky Y. MicroRNAs in placental health and disease. Am J Obstet Gynecol. 2015;213(4 Suppl):S163–72.  https://doi.org/10.1016/j.ajog.2015.05.057. CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Pineles BL, Romero R, Montenegro D, Tarca AL, Han YM, Kim YM, et al. Distinct subsets of microRNAs are expressed differentially in the human placentas of patients with preeclampsia. Am J Obstet Gynecol. 2007;196(3):261.e1–6.  https://doi.org/10.1016/j.ajog.2007.01.008.CrossRefGoogle Scholar
  47. 47.
    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(6):661.e1–7.  https://doi.org/10.1016/j.ajog.2008.12.045.CrossRefGoogle Scholar
  48. 48.
    Hu Y, Li P, Hao S, Liu L, Zhao J, Hou Y. Differential expression of microRNAs in the placentae of Chinese patients with severe pre-eclampsia. Clin Chem Lab Med. 2009;47(8):923–9.  https://doi.org/10.1515/cclm.2009.228. CrossRefPubMedGoogle Scholar
  49. 49.
    Zhang Y, Diao Z, Su L, Sun H, Li R, Cui H, et al. MicroRNA-155 contributes to preeclampsia by down-regulating CYR61. Am J Obstet Gynecol. 2010;202(5):466.e1–7.  https://doi.org/10.1016/j.ajog.2010.01.057.CrossRefGoogle Scholar
  50. 50.
    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(2):178.e12–21.  https://doi.org/10.1016/j.ajog.2010.09.004.CrossRefGoogle Scholar
  51. 51.
    Ishibashi O, Ohkuchi A, Ali MM, Kurashina R, Luo SS, Ishikawa T, 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.  https://doi.org/10.1161/hypertensionaha.111.180232.CrossRefPubMedGoogle Scholar
  52. 52.
    Xu P, Zhao Y, Liu M, Wang Y, Wang H, Li YX, et al. Variations of microRNAs in human placentas and plasma from preeclamptic pregnancy. Hypertension. 2014;63(6):1276–84.  https://doi.org/10.1161/hypertensionaha.113.02647.CrossRefPubMedGoogle Scholar
  53. 53.
    Zhang M, Muralimanoharan S, Wortman AC, Mendelson CR. Primate-specific miR-515 family members inhibit key genes in human trophoblast differentiation and are upregulated in preeclampsia. Proc Natl Acad Sci U S A. 2016.  https://doi.org/10.1073/pnas.1607849113.
  54. 54.
    Chan YC, Banerjee J, Choi SY, Sen CK. miR-210: the master hypoxamir. Microcirculation. 2012;19(3):215–23.  https://doi.org/10.1111/j.1549-8719.2011.00154.x.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Miettinen MM, Mustonen MV, Poutanen MH, Isomaa VV, Vihko RK. Human 17 beta-hydroxysteroid dehydrogenase type 1 and type 2 isoenzymes have opposite activities in cultured cells and characteristic cell- and tissue-specific expression. Biochem J. 1996;314(Pt 3):839–45.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Guo L, Yang Q, Lu J, Li H, Ge Q, Gu W, et al. A comprehensive survey of miRNA repertoire and 3′ addition events in the placentas of patients with pre-eclampsia from high-throughput sequencing. PLoS One. 2011;6(6):e21072.  https://doi.org/10.1371/journal.pone.0021072.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Pillay P, Maharaj N, Moodley J, Mackraj I. Placental exosomes and pre-eclampsia: maternal circulating levels in normal pregnancies and, early and late onset pre-eclamptic pregnancies. Placenta. 2016;46:18–25.  https://doi.org/10.1016/j.placenta.2016.08.078.CrossRefPubMedGoogle Scholar
  58. 58.
    Germain SJ, Sacks GP, Sooranna SR, Sargent IL, Redman CW. Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles. J Immunol. 2007;178(9):5949–56.CrossRefPubMedGoogle Scholar
  59. 59.
    Miura K, Miura S, Yamasaki K, Higashijima A, Kinoshita A, Yoshiura K, et al. Identification of pregnancy-associated microRNAs in maternal plasma. Clin Chem. 2010;56(11):1767–71.  https://doi.org/10.1373/clinchem.2010.147660.CrossRefPubMedGoogle Scholar
  60. 60.
    Miura K, Higashijima A, Murakami Y, Tsukamoto O, Hasegawa Y, Abe S, et al. Circulating chromosome 19 miRNA cluster microRNAs in pregnant women with severe pre-eclampsia. J Obstet Gynaecol Res. 2015;41(10):1526–32.  https://doi.org/10.1111/jog.12749.CrossRefPubMedGoogle Scholar
  61. 61.
    Kotlabova K, Doucha J, Hromadnikova I. Placental-specific microRNA in maternal circulation—identification of appropriate pregnancy-associated microRNAs with diagnostic potential. J Reprod Immunol. 2011;89(2):185–91.  https://doi.org/10.1016/j.jri.2011.02.006.CrossRefPubMedGoogle Scholar
  62. 62.
    Hromadnikova I, Kotlabova K, Ondrackova M, Kestlerova A, Novotna V, Hympanova L, et al. Circulating C19MC microRNAs in preeclampsia, gestational hypertension, and fetal growth restriction. Mediat Inflamm. 2013;2013:186041.  https://doi.org/10.1155/2013/186041. Google Scholar
  63. 63.
    Hromadnikova I, Kotlabova K, Doucha J, Dlouha K, Krofta L. Absolute and relative quantification of placenta-specific microRNAs in maternal circulation with placental insufficiency-related complications. J Mol Diagn. 2012;14(2):160–7.  https://doi.org/10.1016/j.jmoldx.2011.11.003.CrossRefPubMedGoogle Scholar
  64. 64.
    Wu L, Zhou H, Lin H, Qi J, Zhu C, Gao Z, et al. Circulating microRNAs are elevated in plasma from severe preeclamptic pregnancies. Reproduction. 2012;143(3):389–97.  https://doi.org/10.1530/rep-11-0304.CrossRefPubMedGoogle Scholar
  65. 65.
    Hromadnikova I, Kotlabova K, Hympanova L, Doucha J, Krofta L. First trimester screening of circulating C19MC microRNAs can predict subsequent onset of gestational hypertension. PLoS One. 2014;9(12):e113735.  https://doi.org/10.1371/journal.pone.0113735.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Williams Z, Ben-Dov IZ, Elias R, Mihailovic A, Brown M, Rosenwaks Z, et al. Comprehensive profiling of circulating microRNA via small RNA sequencing of cDNA libraries reveals biomarker potential and limitations. Proc Natl Acad Sci U S A. 2013;110(11):4255–60.  https://doi.org/10.1073/pnas.1214046110.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Liu Y, Zhao Y, Yu A, Zhao B, Gao Y, Niu H. Diagnostic accuracy of the soluble Fms-like tyrosine kinase-1/placental growth factor ratio for preeclampsia: a meta-analysis based on 20 studies. Arch Gynecol Obstet. 2015;292(3):507–18.  https://doi.org/10.1007/s00404-015-3671-8.CrossRefPubMedGoogle Scholar
  68. 68.
    Sovio U, Gaccioli F, Cook E, Hund M, Charnock-Jones DS, Smith GC. Prediction of preeclampsia using the soluble fms-like tyrosine kinase 1 to placental growth factor ratio: a prospective cohort study of unselected nulliparous women. Hypertension. 2017;69(4):731–8.  https://doi.org/10.1161/hypertensionaha.116.08620.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Takizawa T, Ishibashi O, Matsubara S, Migita M, Takeshita T. Exosomes released from human placenta into maternal circulation: placenta-specific miRNAs (review). Exp Med (Yodosha, Tokyo, Japan [in Japanese]). 2011;29(3):392–8.Google Scholar
  70. 70.
    Farrokhnia F, Aplin JD, Westwood M, Forbes K. MicroRNA regulation of mitogenic signaling networks in the human placenta. J Biol Chem. 2014;289(44):30404–16.  https://doi.org/10.1074/jbc.M114.587295.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Zhu X, Yang Y, Han T, Yin G, Gao P, Ni Y, et al. Suppression of microRNA-18a expression inhibits invasion and promotes apoptosis of human trophoblast cells by targeting the estrogen receptor alpha gene. Mol Med Rep. 2015;12(2):2701–6.  https://doi.org/10.3892/mmr.2015.3724.CrossRefPubMedGoogle Scholar
  72. 72.
    Kumar P, Luo Y, Tudela C, Alexander JM, Mendelson CR. The c-Myc-regulated microRNA-17~92 (miR-17~92) and miR-106a~363 clusters target hCYP19A1 and hGCM1 to inhibit human trophoblast differentiation. Mol Cell Biol. 2013;33(9):1782–96.  https://doi.org/10.1128/mcb.01228-12.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Wang Y, Zhang Y, Wang H, Wang J, Pan Z, Luo S. Aberrantly up-regulated miR-20a in pre-eclampsic placenta compromised the proliferative and invasive behaviors of trophoblast cells by targeting forkhead box protein A1. Int J Biol Sci. 2014;10(9):973–82.  https://doi.org/10.7150/ijbs.9088.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Li P, Guo W, Du L, Zhao J, Wang Y, Liu L, et al. microRNA-29b contributes to pre-eclampsia through its effects on apoptosis, invasion and angiogenesis of trophoblast cells. Clin Sci (Lond). 2013;124(1):27–40.  https://doi.org/10.1042/cs20120121.CrossRefGoogle Scholar
  75. 75.
    Sun M, Chen H, Liu J, Tong C, Meng T. MicroRNA-34a inhibits human trophoblast cell invasion by targeting MYC. BMC Cell Biol. 2015;16:21.  https://doi.org/10.1186/s12860-015-0068-2.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Zou Y, Jiang Z, Yu X, Zhang Y, Sun M, Wang W, et al. MiR-101 regulates apoptosis of trophoblast HTR-8/SVneo cells by targeting endoplasmic reticulum (ER) protein 44 during preeclampsia. J Hum Hypertens. 2014;28(10):610–6.  https://doi.org/10.1038/jhh.2014.35.CrossRefPubMedGoogle Scholar
  77. 77.
    Li Q, Pan Z, Wang X, Gao Z, Ren C, Yang W. miR-125b-1-3p inhibits trophoblast cell invasion by targeting sphingosine-1-phosphate receptor 1 in preeclampsia. Biochem Biophys Res Commun. 2014;453(1):57–63.  https://doi.org/10.1016/j.bbrc.2014.09.059.CrossRefPubMedGoogle Scholar
  78. 78.
    Tamaru S, Mizuno Y, Tochigi H, Kajihara T, Okazaki Y, Okagaki R, et al. MicroRNA-135b suppresses extravillous trophoblast-derived HTR-8/SVneo cell invasion by directly down regulating CXCL12 under low oxygen conditions. Biochem Biophys Res Commun. 2015;461(2):421–6.  https://doi.org/10.1016/j.bbrc.2015.04.055.CrossRefPubMedGoogle Scholar
  79. 79.
    TM L, Lu W, Zhao LJ. MicroRNA-137 affects proliferation and migration of placenta trophoblast cells in preeclampsia by targeting ERRalpha. Reprod Sci. 2016.  https://doi.org/10.1177/1933719116650754.
  80. 80.
    Dai Y, Qiu Z, Diao Z, Shen L, Xue P, Sun H, et al. MicroRNA-155 inhibits proliferation and migration of human extravillous trophoblast derived HTR-8/SVneo cells via down-regulating cyclin D1. Placenta. 2012;33(10):824–9.  https://doi.org/10.1016/j.placenta.2012.07.012.CrossRefPubMedGoogle Scholar
  81. 81.
    Bai Y, Yang W, Yang HX, Liao Q, Ye G, Fu G, et al. Downregulated miR-195 detected in preeclamptic placenta affects trophoblast cell invasion via modulating ActRIIA expression. PLoS One. 2012;7(6):e38875.  https://doi.org/10.1371/journal.pone.0038875.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Yu Y, Wang L, Liu T, Guan H. MicroRNA-204 suppresses trophoblast-like cell invasion by targeting matrix metalloproteinase-9. Biochem Biophys Res Commun. 2015;463(3):285–91.  https://doi.org/10.1016/j.bbrc.2015.05.052.CrossRefPubMedGoogle Scholar
  83. 83.
    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.  https://doi.org/10.1096/fj.09-149724.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Zhang Y, Fei M, Xue G, Zhou Q, Jia Y, Li L, 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.  https://doi.org/10.1111/j.1582-4934.2011.01291.x.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Luo R, Shao X, Xu P, Liu Y, Wang Y, Zhao Y, et al. MicroRNA-210 contributes to preeclampsia by downregulating potassium channel modulatory factor 1. Hypertension. 2014;64(4):839–45.  https://doi.org/10.1161/hypertensionaha.114.03530.CrossRefPubMedGoogle Scholar
  86. 86.
    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.  https://doi.org/10.1371/journal.pone.0067760.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Fu G, Ye G, Nadeem L, Ji L, Manchanda T, Wang Y, 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.  https://doi.org/10.1161/hypertensionaha.111.203489.CrossRefPubMedGoogle Scholar
  88. 88.
    Luo L, Ye G, Nadeem L, Fu G, Yang BB, Honarparvar E, et al. MicroRNA-378a-5p promotes trophoblast cell survival, migration and invasion by targeting Nodal. J Cell Sci. 2012;125(Pt 13):3124–32.  https://doi.org/10.1242/jcs.096412. CrossRefPubMedGoogle Scholar
  89. 89.
    Xie L, Mouillet JF, Chu T, Parks WT, Sadovsky E, Knofler M, et al. C19MC microRNAs regulate the migration of human trophoblasts. Endocrinology. 2014;155(12):4975–85.  https://doi.org/10.1210/en.2014-1501.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Ding J, Huang F, Wu G, Han T, Xu F, Weng D, et al. MiR-519d-3p suppresses invasion and migration of trophoblast cells via targeting MMP-2. PLoS One. 2015;10(3):e0120321.  https://doi.org/10.1371/journal.pone.0120321.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Gao WL, Liu M, Yang Y, Yang H, Liao Q, Bai 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.  https://doi.org/10.4161/rna.20807.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Toshihiro Takizawa
    • 1
    Email author
  • Akihide Ohkuchi
    • 2
  • Shigeki Matsubara
    • 2
  • Toshiyuki Takeshita
    • 3
  • Shigeru Saito
    • 4
  1. 1.Department of Molecular Medicine and AnatomyNippon Medical SchoolTokyoJapan
  2. 2.Department of Obstetrics and GynecologyJichi Medical UniversityTochigiJapan
  3. 3.Department of Obstetrics and GynecologyNippon Medical SchoolTokyoJapan
  4. 4.Department of Obstetrics and Gynecology, Faculty of MedicineUniversity of ToyamaToyamaJapan

Personalised recommendations