MicroRNA regulation in the genesis of fetal growth restriction

Zabanova E.A., Kuznetsova N.B., Skurat T.P., Butenko E.V.

1) Rostov State Medical University, Ministry of Health of Russia, Rostov-on-Don, Russia; 2) Southern Federal University, Rostov-on-Don, Russia
MicroRNA is a class of short non-coding RNAs that carry out epigenetic regulation of many biological processes, including the course of pregnancy. More than 500 microRNAs associated with the formation and functioning of the placenta are presently known. The expression level of these microRNAs may be an indicator of placental changes during pregnancy. A number of placenta-specific microRNAs detected in maternal plasma can be regarded as potential non-invasive markers of maternal and fetal health. The data available in the modern scientific literature on changes in the expression of placenta-specific microRNAs circulating in the plasma of a pregnant woman with fetal growth restriction are analyzed. MicroRNAs can play an important, but currently not fully investigated role in the initiation of gestational complications. The use of microRNAs in the prediction and treatment of diseases and pregnancy complications is a promising area that requires further investigation.

Keywords

microRNA
fetal growth restriction
placenta
pregnancy complications
preeclampsia

References

  1. Unterscheider J., Daly S., Geary M.P., Kennelly M.M., McAuliffe F.M., O’Donoghue K., et al. Optimizing the definition of intrauterine growth restriction: the multicenter prospective PORTO Study. Am J Obstet Gynecol. 2013; 208(4): 290.e1-6. doi:10.1016/j.ajog.2013.02.007.
  2. Стрижаков А.Н., Игнатко И.В., Тимохина Е.В., Белоцерковцева Л.Д. Синдром задержки роста плода: патогенез, диагностика, лечение, акушерская тактика. М.: ГЭОТАР-Медиа, 2014. 120 с. [Strizhakov A.N., Ignatko I.V., Timokhina E.V., Belotserkovtseva L.D. Fetal growth retardation syndrome: pathogenesis, diagnosis, treatment, obstetric tactics. M.: GEOTAR-Media, 2014. 120 p. (in Russian)]. https://www.rosmedlib.ru/book/ISBN9785970431566.html
  3. American College of Obstetricians and Gynecologists. ACOG Practice bulletin no. 134: fetal growth restriction. Obstet Gynecol. 2013; 121(5): 1122–33. doi:10.1097/01.AOG.0000429658.85846.f9.
  4. Bidarimath M., Khalaj K., Wessels J.M., Tayade C. MicroRNAs, immune cells and pregnancy. Cell Mol Immunol. 2014; 11(6): 538–47. doi:10.1038/cmi.2014.45
  5. Hong X., Luense L.J., McGinnis L.K., Nothnick W.B., Christenson L.K. Dicer1 is essential for female fertility and normal development of the female reproductive system. 2008; 149(12): 6207–12. doi:10.1210/en.2008-0294
  6. Hudson T.J., Anderson W., Artez A., Barker A.D., Bell C., Bernabé R.R., et al. International network of cancer genome projects. International Cancer Genome Consortium. Nature. 2010; 464(7291): 993–8. doi:10.1038/nature08987.
  7. Enquobahrie D.A., Abetew D.F., Sorensen T.K., Willoughby D., Chidambaram K., Williams M.A. Placental microRNA expression in pregnancies complicated by preeclampsia. Am J Obstet Gynecol. 2011; 204(2): 178.e12-21. doi:10.1016/j.ajog.2010.09.004.
  8. Mayor-Lynn K., Toloubeydokhti T., Cruz A.C., Chegini N. Expression profile of microRNAs and mRNAs in human placentas from pregnancies complicated by preeclampsia and preterm labor. Reprod Sci. 2011; 18(1): 46–56. doi:10.1177/1933719110374115.
  9. Gilad S., Meiri E., Yogev Y., Benjamin S., Lebanony D., Yerushalmi N., et al. Serum microRNAs are promising novel biomarkers. PLoS One. 2008; 3(9): e3148. doi:10.1371/journal.pone.0003148.
  10. Tsochandaridis M., Nasca L., Toga C., Levy-Mozziconacci A. Circulating microRNAs as clinical biomarkers in the predictions of pregnancy complications. Biomed Res Int. 2015; 2015: 294954. doi:10.1155/2015/294954
  11. Morales-Prieto D.M., Chaiwangyen W., Ospina-Prieto S., Schneider U., Herrmann J., Gruhn B., et al. MicroRNA expression profiles of trophoblastic cells. Placenta. 2012; 33(9): 725–34. doi:10.1016/j.placenta.2012.05.009.
  12. Chim S.S., Shing T.K., Hung E.C., Leung T.Y., Lau T.K., Chiu R.W., et al. Detection and characterization of placental microRNAs in maternal plasma. Clin Chem. 2008; 54(3): 482–90. doi:10.1373/clinchem.2007.097972.
  13. Mouillet J.F., Chu T., Hubel C.A., Nelson D.M., Parks W.T., Sadovsky Y. The levels of hypoxia-regulated microRNAs in plasma of pregnant women with fetal growth restriction. Placenta. 2010; 31(9): 781–784. doi:10.1016/j.placenta.2010.07.001.
  14. Luo S.S., Ishibashi O., Ishikawa G., Ishikawa T., Katayama A., Mishima T. Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol Reprod. 2009; 81(4): 717–29. doi:10.1095/biolreprod.108.075481.
  15. Donker R.B., Mouillet J.F., Chu T., Hubel C.A., Stolz D.B., Morelli A.E., et al. The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes. Mol Hum Reprod. 2012; 18(8): 417–24. doi:10.1093/molehr/gas013
  16. Ouyang Y., Mouillet J.F., Coyne C.B., Sadovsky Y. Review: placenta-specific microRNAs in exosomes - good things come in nano-packages. Placenta. 2013; 35 Suppl: S69–S73. doi:10.1016/j.placenta.2013.11.002
  17. Gu Y., Sun J., Groome L.J., Wang Y. Differential miRNA expression profiles between the first and third trimester human placentas. Am J Physiol Endocrinol Metab. 2013; 304(8): E836–E843. doi:10.1152/ajpendo.00660.2012
  18. Li H., Guo L., Wu Q., Lu J., Ge Q., Lu Z. A comprehensive survey of maternal plasma miRNAs expression profiles using high-throughput sequencing. Clin Chim Acta. 2012; 413(5–6): 568–76. doi:10.1016/j.cca.2011.11.026.
  19. Низяева Н.В., Кан Н.Е., Тютюнник В.Л., Ломова Н.А., Наговицына М.Н., Прозоровская К.Н., Щёголев А.И. МикроРНК как важные диагностичеcкие предвестники развития акушерской патологии. Вестник РАМН. 2015; 70 (4): 484–92. [Nizyaeva N.V., Kan N.E., Tyutyunnik V.L., Lomova N.A.,Nagovitsyna M.N., Prozorovskaya K.N., Shchyogolev A.I. MicroRNAs As An Important Precursors of Diagnostic Obstetric Pathology. Vestnik Rossiiskoi Akademii Meditsinskikh Nauk/ Annals of the Russian Academy of Medical Sciences. 2015; 70(4): 484–92. (in Russian)]. doi:10.15690/vramn.v70.i4.1416.
  20. Mouillet J.F., Chu T., Nelson D.M., Mishima T., Sadovsky Y. MiR-205 silences MED1 in hypoxic primary human trophoblasts. FASEB J. 2010; 24(6): 2030–9. doi:10.1096/fj.09-149724.
  21. Luo L., Ye G., Nadeem L., Fu G., Yang B.B., Honarparvar E., et al. MicroRNA-378a-5p promotes trophoblast cell survival, migration and invasion by targeting Nodal. J Cell Sci. 2012; 125(Pt13): 3124–32. doi:10.1242/jcs.096412.
  22. Pineles B.L., Romero R., Montenegro D., Tarca A.L., Han Y.M., Kim Y.M., 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.doi: 10.1016/j.ajog.2007.01.008
  23. Zhu X.M., Han T., Sargent I.L., Yin G.W., Yao Y.Q. Differential expression profile of microRNAs in human placentas from preeclamptic pregnancies vs normal pregnancies. Am J Obstet Gynecol. 2009; 200(6): 661.e1–7. doi:10.1016/j.ajog.2008.12.045.
  24. Ura B., Feriotto G., Monasta L., Bilel S., Zweyer M., Celeghini C. Potential role of circulating microRNAs as early markers of preeclampsia. Taiwan J Obstet Gynecol. 2014; 53(2): 232–4. doi:10.1016/j.tjog.2014.03.001.
  25. Choi S.Y., Yun J., Lee O.J., Han H.S., Yeo M.K., Lee M.A., et al. MicroRNA expression profiles in placenta with severe preeclampsia using a PNA-based microarray. Placenta. 2013; 34(9): 799–804. doi:10.1016/j.placenta.2013.06.006.
  26. Chan S.Y., Loscalzo J. MicroRNA-210: a unique and pleiotropic hypoxamir. Cell Cycle. 2010; 9(6): 1072–83. doi:10.4161/cc.9.6.11006
  27. Kelly T.J., Souza A.L., Clish C.B., 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): 2696–2706. doi:10.1128/MCB.01242-10
  28. Тимофеева А.В., Гусар В.А., Прозоровская К.Н. , Балашов И.С., Ломова Н.А., Ганичкина М.Б., Амирасланов Э.Ю., Волочаева М.В., Низяева Н.В., Боровиков П.И., Франкевич В.Е., Тютюнник В.Л., Кан Н.Е., Бобров М.Ю., Сухих Г.Т. Идентификация ассоциированных с преэклампсией микроРНК методом глубокого секвенирования и количественной полимеразной цепной реакции в реальном времени. Акушерство и гинекология. 2016; 8: 60–70. [Timofeeva A.V., Gusar V.A., Prozorovskaya K.N., Balashov I.S., Lomova N.A., Ganichkina M.B., Amiraslanov E.Yu., Volochaeva M.V., Nizyaeva N.V., Borovikov P.I., Frankevich V.E., Tyutyunnik V.L., Kan N.E., Bobrov M.Yu., Sukhikh G.T. Identification of preeclampsia-related miRNA by a deep sequencing technique and a real-time quantitative PCR. Akusherstvo i ginekologiya/Obstetrics and Gynecology. 2016; (8): 60–70. (in Russian)]. doi:10.18565/aig.2016.8.60-70
  29. Thamotharan S., Chu A., Kempf K., Janzen C., Grogan T., Elashoff D.A., et al. Differential microRNA expression in human placentas of term intra-uterine growth restriction that regulates target genes mediating angiogenesis and amino acid transport. PLoS One. 2017; 12(5): e0176493. doi:10.1371/journal.pone.0176493
  30. Maccani M.A., Padbury J.F., Marsit C.J. miR-16 and miR-21 expression in the placenta is associated with fetal growth. PLoS One. 2011; 6(6): e21210. doi:10.1371/journal.pone.0021210
  31. Cindrova-Davies T., Herrera E.A., Niu Y., Kingdom J., Giussani D.A., Burton G.J. Reduced cystathionine γ-lyase and increased miR-21 expression are associated with increased vascular resistance in growth-restricted pregnancies: hydrogen sulfide as a placental vasodilator. Am J Pathol. 2013; 182(4): 1448–58. doi:10.1016/j.ajpath.2013.01.001
  32. Whitehead C.L., Teh W.T., Walker S.P., Leung C., Larmour L., Tong S. Circulating MicroRNAs in maternal blood as potential biomarkers for fetal hypoxia in-utero. PLoS One. 2013; 8(11): e78487. doi:10.1371/journal.pone.0078487
  33. Tang Q., Wu W., Xu X., Huang L., Gao Q., Chen H., et al. miR-141 contributes to fetal growth restriction by regulating PLAG1 expression. PLoS One. 2013; 8(3): e58737. doi: 10.1371/journal.pone.0058737
  34. Saha S., Chakraborty S., Bhattacharya A., Biswas A., Ain R. MicroRNA regulation of Transthyretin in trophoblast differentiation and Intra-Uterine Growth Restriction. Sci Rep. 2017; 7(1): 16548. doi:10.1038/s41598-017-16566-0
  35. Айламазян Э.К., Кулаков В.И., Радзинский В.Е., Савельева Г.М., ред. Акушерство: национальное руководство. М.: ГЭОТАР-Медиа; 2014. 1200 с. [Ailamazyan E.K., Kulakov V.I., Radzinsky V.E., Savelyeva G.M., ed. Obstetrics: national leadership. M.: GEOTAR-Media; 2014. 1200 p. (in Russian)]. https://books.google.ru/books?id=oUaKHGBILuQC
  36. Forbes K., Farrokhnia F., Aplin J.D., Westwood M. Dicer-dependent miRNAs provide an endogenous restraint on cytotrophoblast proliferation. Placenta. 2012; 33(7): 581–5. doi:10.1016/j.placenta.2012.03.006.
  37. Song G.Y., Song W.W., Han Y., Wang D., Na Q. Characterization of the role of microRNA-517a expression in low birth weight infants. J Dev Orig Health Dis. 2013; 4(6): 522-6. doi:10.1017/S204017441300024X.
  38. Dai Y., Diao Z., Sun H., Li R., Qiu Z., Hu Y. MicroRNA-155 is involved in the remodelling of human-trophoblast-derived HTR-8/SVneo cells induced by lipopolysaccharides. Hum Reprod. 2011; 26(7): 1882–91. doi:10.1093/humrep/der118.
  39. Wang D., Na Q., Song W.W., Song G.Y. Altered Expression of miR-518b and miR-519a in the placenta is associated with low fetal birth weight. Am J Perinatol. 2014; 31(9): 729-34. doi:10.1055/s-0033-1361832.
  40. Liu M., Wang Y., Lu H., Wang H., Shi X., Shao X., et al. miR-518b enhances human trophoblast cell proliferation through targeting rap1b and activating ras-MAPK signal. Front Endocrinol (Lausanne). 2018; 9:100. doi:10.3389/fendo.2018.00100.
  41. Huang L., Shen Z., Xu Q., Huang X., Chen Q., Li D. Increased levels of microRNA-424 are associated with the pathogenesis of fetal growth restriction. Placenta. 2013; 34(7): 624–7. doi:10.1016/j.placenta.2013.04.009.
  42. Бурлев В.А., Павлович С.В. Ангиогенез и ангиогенные факторы роста в регуляции репродуктивной системы у женщин. Проблемы репродукции. 1999; 5: 6–13. [Burlev V.A., Pavlovich S.V. Angiogenesis and angiogenic growth factors in the regulation of the reproductive system in women. Problemy reproduktsii/Russian Journal of Human Reproduction. 1999; 5: 6–13. (in Russian)]
  43. Hromadnikova I., Kotlabova K., Hympanova L., Krofta L. Cardiovascular and cerebrovascular disease associated microRNAs are dysregulated in placental tissues affected with gestational hypertension, preeclampsia and I=intrauterine growth restriction. PLoS One. 2015; 10(9): e0138383. doi:10.1371/journal.pone.0138383
  44. Wen H., Chen L., He J., Lin J. MicroRNA expression profiles and networks in placentas complicated with selective intrauterine growth restriction. Mol Med Rep. 2017; 16(5): 6650–6673. doi:10.3892/mmr.2017.7462
  45. Hromadnikova I., Kotlabova K., Ivankova K., Krofta L. First trimester screening of circulating C19MC microRNAs and the evaluation of their potential to predict the onset of preeclampsia and IUGR. PLoS One. 2017;12(2): e0171756. doi:10.1371/journal.pone.0171756

Received 16.04.2019

Accepted 19.04.2019

About the Authors

Ekaterina A. Zabanova, Postgraduate at the Department of Simulation education of RostSMU.
344022, 29 Nahichevansky ave., Rostov-on-Don, Russian Federation. Phone: +7(918)566-88-25, e-mail:rock-fe@mail.ru.
Natalia B. Kuznetsova, Doctor of Medical Sciences, Professor at the Department of Simulation education of RostSMU.
344022, 29 Nahichevansky ave., Rostov-on-Don, Russian Federation. Phone: +7(928)770-97-62, e-mail:lauranb@inbox.ru .
Tatiana P. Shkurat., Doctor of Biological Sciences, Full Professor, Director of Research Institute of Biology of SFedU.
344090, 194/1 Stachki ave., Rostov-on-Don, Russian Federation. Phone: +7(863)243-38-85, e-mail:tshkurat@sfedu.ru .
Elena V. Butenko, Candidate of Biological Sciences, Associate Professor at the Department of genetics of Academy of Biology and Biotechnologies of SFedU.
344090, 194/1 Stachki ave., Rostov-on-Don, Russian Federation. Phone: +7(909)420-22-23, e-mail:evbutenko@sfedu.ru

For citation: Zabanova E.A., Kuznetsova N.B., Skurat T.P., Butenko E.V. MicroRNA regulation in the genesis of fetal growth restriction.
Akusherstvo i Ginekologiya/ Obstetrics and gynecology. 2019; 12: 5-11. (In Russian).
https://dx.doi.org/10.18565/aig.2019.12.5-11

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