Skip to main content

Advertisement

SpringerLink
Log in

Circulating levels of specific members of chromosome 19 microRNA cluster are associated with preeclampsia development

  • Maternal-Fetal Medicine
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Purpose

To perform serum microRNA expression profiling to identify members of chromosome 19 miRNA cluster involved in preeclampsia development.

Methods

Serum chromosome 19 miRNA cluster microRNA expression profiling was evaluated at 12, 16, and 20 gestational weeks and at the time of preeclampsia diagnosis, in women who developed preeclampsia (WWD-PE; n = 16) and controls (n = 18) using TaqMan low density array plates.

Results

A total of 51 chromosome 19 microRNA cluster members were evaluated. The circulating hsa-miRs 512-3p, 518f-3p, 520c-3p, and 520d-3p, were differentially expressed between groups (P < 0.05). Compared with controls, serum levels of hsa-miR-518f-3p at 20 GW were useful for identifying WWD-Mild-PE (P = 0.035) and WWD-Severe-PE (P = 0.007).

Conclusions

Serum hsa-miRs 512-3p, 518f-3p, 520c-3p, and 520d-3p, are differentially expressed between WWD-PE and controls and their role in the development of preeclampsia should be investigated further.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Aslam MI (2009) MicroRNAs are novel biomarkers of colorectal cancer. Br J Surg 96(7):702–710

    Article  CAS  PubMed  Google Scholar 

  2. Maccani MA (2009) Epigenetics in the placenta. Am J Reprod Immunol (New York, NY: 1989) 62(2):78–89

    Article  CAS  Google Scholar 

  3. Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6(5):376–385. https://doi.org/10.1038/nrm1644

    Article  CAS  PubMed  Google Scholar 

  4. Ji L, Brkic J, Liu M, Fu G, Peng C, Wang YL (2013) Placental trophoblast cell differentiation: physiological regulation and pathological relevance to preeclampsia. Mol Aspects Med 34(5):981–1023. https://doi.org/10.1016/j.mam.2012.12.008

    Article  CAS  PubMed  Google Scholar 

  5. Enquobahrie DA, Abetew DF, Sorensen TK, Willoughby D, Chidambaram K, Williams MA (2011) Placental microRNA expression in pregnancies complicated by preeclampsia. Am J Obstet Gynecol 204(2):178 e112-121. https://doi.org/10.1016/j.ajog.2010.09.004

    Article  Google Scholar 

  6. Fu G, Brkic J, Hayder H, Peng C (2013) MicroRNAs in human placental development and pregnancy complications. Int J Mol Sci 14(3):5519–5544. https://doi.org/10.3390/ijms14035519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pineles BL, Romero R, Montenegro D, Tarca AL, Han YM, Kim YM, Draghici S, Espinoza J, Kusanovic JP, Mittal P, Hassan SS, Kim CJ (2007) Distinct subsets of microRNAs are expressed differentially in the human placentas of patients with preeclampsia. Am J Obstet Gynecol 196 e261-266(3):261. https://doi.org/10.1016/j.ajog.2007.01.008

    Google Scholar 

  8. Chen DB, Wang W (2013) Human placental microRNAs and preeclampsia. Biol Reprod 88(5):130. https://doi.org/10.1095/biolreprod.113.107805

    Article  PubMed  PubMed Central  Google Scholar 

  9. Doridot L, Miralles F, Barbaux S, Vaiman D (2013) Trophoblasts, invasion, and microRNA. Front Genet 4:248. https://doi.org/10.3389/fgene.2013.00248

    Article  PubMed  PubMed Central  Google Scholar 

  10. Morales-Prieto DM, Ospina-Prieto S, Chaiwangyen W, Schoenleben M, Markert UR (2013) Pregnancy-associated miRNA-clusters. J Reprod Immunol 97(1):51–61. https://doi.org/10.1016/j.jri.2012.11.001

    Article  CAS  PubMed  Google Scholar 

  11. Ouyang Y, Mouillet JF, Coyne CB, Sadovsky Y (2014) Review: Placenta-specific microRNAs in exosomes—good things come in nano-packages. Placenta 35(Suppl):S69–S73. https://doi.org/10.1016/j.placenta.2013.11.002

    Article  CAS  PubMed  Google Scholar 

  12. Gu Y, Sun J, Groome LJ, Wang Y (2013) Differential miRNA expression profiles between the first and third trimester human placentas. Am J Physiol Endocrinol Metab 304(8):E836–E843. https://doi.org/10.1152/ajpendo.00660.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Donker RB, Mouillet JF, Chu T, Hubel CA, Stolz DB, Morelli AE, Sadovsky Y (2012) The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes. Mol Hum Reprod 18(8):417–424. https://doi.org/10.1093/molehr/gas013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Bullerdiek J, Flor I (2012) Exosome-delivered microRNAs of “chromosome 19 microRNA cluster” as immunomodulators in pregnancy and tumorigenesis. Mol Cytogenet 5(1):27. https://doi.org/10.1186/1755-8166-5-27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Xu P, Zhao Y, Liu M, Wang Y, Wang H, Li YX, Zhu X, Yao Y, Qiao J, Ji L, Wang YL (2014) Variations of microRNAs in human placentas and plasma from preeclamptic pregnancy. Hypertension 63(6):1276–1284. https://doi.org/10.1161/HYPERTENSIONAHA.113.02647

    Article  CAS  PubMed  Google Scholar 

  16. Mouillet JF, Chu T, Hubel CA, Nelson DM, Parks WT, Sadovsky Y (2010) The levels of hypoxia-regulated microRNAs in plasma of pregnant women with fetal growth restriction. Placenta 31(9):781–784. https://doi.org/10.1016/j.placenta.2010.07.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Li H, Ge Q, Guo L, Lu Z (2013) Maternal plasma miRNAs expression in preeclamptic pregnancies. Biomed Res Int 2013:970265. https://doi.org/10.1155/2013/970265

    PubMed  PubMed Central  Google Scholar 

  18. Wu L, Zhou H, Lin H, Qi J, Zhu C, Gao Z, Wang H (2012) Circulating microRNAs are elevated in plasma from severe preeclamptic pregnancies. Reproduction 143(3):389–397. https://doi.org/10.1530/REP-11-0304

    Article  CAS  PubMed  Google Scholar 

  19. Yang Q, Lu J, Wang S, Li H, Ge Q, Lu Z (2011) Application of next-generation sequencing technology to profile the circulating microRNAs in the serum of preeclampsia versus normal pregnant women. Clin Chim Acta Int J Clin Chem 412(23–24):2167–2173. https://doi.org/10.1016/j.cca.2011.07.029

    Article  CAS  Google Scholar 

  20. Ura B, Feriotto G, Monasta L, Bilel S, Zweyer M, Celeghini C (2014) Potential role of circulating microRNAs as early markers of preeclampsia. Taiwan J Obstet Gynecol 53(2):232–234. https://doi.org/10.1016/j.tjog.2014.03.001

    Article  PubMed  Google Scholar 

  21. Herzog EM, Eggink AJ, Willemsen SP, Slieker RC, Wijnands KPJ, Felix JF, Chen J, Stubbs A, van der Spek PJ, van Meurs JB, Steegers-Theunissen RPM (2017) Early- and late-onset preeclampsia and the tissue-specific epigenome of the placenta and newborn. Placenta 58:122–132. https://doi.org/10.1016/j.placenta.2017.08.070

    Article  CAS  PubMed  Google Scholar 

  22. Garza-Veloz I, Castruita-De la Rosa C, Cortes-Flores R, Martinez-Gaytan V, Rivera-Munoz JE, Garcia-Mayorga EA, Meza-Lamas E, Rojas-Martinez A, Ortiz-Lopez R, Martinez-Fierro ML (2011) No association between polymorphisms/haplotypes of the vascular endothelial growth factor gene and preeclampsia. BMC Pregnancy Childbirth 11:35. https://doi.org/10.1186/1471-2393-11-35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Martinez-Fierro ML, Garza-Veloz I, Carrillo-Sanchez K, Martinez-Gaytan V, Cortes-Flores R, Ochoa-Torres MA, Guerrero GG, Rodriguez-Sanchez IP, Cancela-Murrieta CO, Zamudio-Osuna M, Badillo-Almaraz JI, Castruita-De la Rosa C (2014) Expression levels of seven candidate genes in human peripheral blood mononuclear cells and their association with preeclampsia. Hypertens Pregnancy 33(2):191–203. https://doi.org/10.3109/10641955.2013.853777

    Article  CAS  PubMed  Google Scholar 

  24. Morales-Prieto DM, Chaiwangyen W, Ospina-Prieto S, Schneider U, Herrmann J, Gruhn B, Markert UR (2012) MicroRNA expression profiles of trophoblastic cells. Placenta 33(9):725–734. https://doi.org/10.1016/j.placenta.2012.05.009

    Article  CAS  PubMed  Google Scholar 

  25. Sheikh AM, Small HY, Currie G, Delles C (2016) Systematic review of micro-RNA expression in pre-eclampsia identifies a number of common pathways associated with the disease. PLoS ONE 11(8):e0160808. https://doi.org/10.1371/journal.pone.0160808

    Article  PubMed  PubMed Central  Google Scholar 

  26. Hromadnikova I, Kotlabova K, Ivankova K, Krofta L (2017) First trimester screening of circulating C19MC microRNAs and the evaluation of their potential to predict the onset of preeclampsia and IUGR. PLoS ONE 12(2):e0171756. https://doi.org/10.1371/journal.pone.0171756

    Article  PubMed  PubMed Central  Google Scholar 

  27. Luque A, Farwati A, Crovetto F, Crispi F, Figueras F, Gratacos E, Aran JM (2014) Usefulness of circulating microRNAs for the prediction of early preeclampsia at first-trimester of pregnancy. Sci Rep 4:4882. https://doi.org/10.1038/srep04882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hromadnikova I, Kotlabova K, Ondrackova M, Kestlerova A, Novotna V, Hympanova L, Doucha J, Krofta L (2013) Circulating C19MC microRNAs in preeclampsia, gestational hypertension, and fetal growth restriction. Mediat Inflamm 2013:186041. https://doi.org/10.1155/2013/186041

    Google Scholar 

Download references

Acknowledgements

The authors thank all of the study participants. We are grateful to the clinical staff of the Urban Health Center of Zacatecas “José Castro Villagrana” and the Hospital de la Mujer Zacatecana for their invaluable assistance in patient recruitment. We also gratefully acknowledge the support of Dr. Raymundo Orozco-Covarrubias, Dr. José Luis Durán-Aguayo, Dr. Martín Cardona-Domínguez, Dr. Rosbel Vázquez Castro, and Dr. Raúl Hernández-León (SSZ) in patient enrolment. The invaluable accompaniment and support of Dr. Pug MF throughout the work will always be acknowledged: we will always remember you.

Author information

Authors and Affiliations

  1. Unidad Academica de Medicina Humana y Ciencias de la Salud, Molecular Medicine Laboratory, Universidad Autonoma de Zacatecas, Carretera Zacatecas-Guadalajara km. 6, Ejido la Escondida, Zacatecas, CP 98160, Mexico

    Margarita L. Martinez-Fierro, Idalia Garza-Veloz, Cristina Gutierrez-Arteaga, Jose I. Badillo-Almaraz & Yolanda Ortiz-Castro

  2. School of Medicine, University of Colima, Colima, Mexico

    Ivan Delgado-Enciso

  3. Unidad Academica de Ciencias Quimicas, Laboratory of Cell and Molecular Biology, Universidad Autonoma de Zacatecas, Zacatecas, Mexico

    Olga Y. Barbosa-Cisneros

  4. Laboratorio de Sintesis Asimetrica y Bioenergetica (LSAyB), Universidad Autonoma de Zacatecas, Zacatecas, Mexico

    Virginia Flores-Morales

  5. Laboratorio de Investigacion en Farmacologia, Universidad Autonoma de Zacatecas, Zacatecas, Mexico

    Gloria P. Hernandez-Delgadillo

  6. Centro de Biotecnologia-FEMSA, Tecnologico de Monterrey, Monterrey, Mexico

    Maria R. Rocha-Pizaña

  7. Departamento de Genetica, School of Medicine, Universidad Autonoma de Nuevo Leon, Monterrey, Nuevo Leon, Mexico

    Iram P. Rodriguez-Sanchez

  8. Unidad Academica de Ingenieria Electrica, Bioengineering Laboratory, Universidad Autonoma de Zacatecas, Zacatecas, Mexico

    Jose M. Ortiz-Rodriguez, Rodrigo Castañeda-Miranda & Luis O. Solis-Sanchez

Authors
  1. Margarita L. Martinez-Fierro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Idalia Garza-Veloz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cristina Gutierrez-Arteaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ivan Delgado-Enciso
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Olga Y. Barbosa-Cisneros
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Virginia Flores-Morales
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gloria P. Hernandez-Delgadillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria R. Rocha-Pizaña
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Iram P. Rodriguez-Sanchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jose I. Badillo-Almaraz
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jose M. Ortiz-Rodriguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Rodrigo Castañeda-Miranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Luis O. Solis-Sanchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Yolanda Ortiz-Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors participated throughout the study and during the preparation of the manuscript, as follows: Protocol/project development: MLM-F, VF-M, YO-C. Data collection or management: MLM-F, IG-V, CG-A, OYB-C, IPR-S, RC-M. Data analysis: MLM-F, CG-A, ID-E, JIB-A, JMO-R, LOS-S. Manuscript writing/editing/approval: MLM-F, IG-V, CG-A, ID-E, OYB-C, VF-M, GPH-D, MRR-P, IPR-S, RC-M, JMO-R, LOS-S, JIB-A, YO-C.

Corresponding author

Correspondence to Margarita L. Martinez-Fierro.

Ethics declarations

Conflict of interest

The authors report no conflicts of interest.

Funding

This work was funded in part by the following CONACYT Grants to M.L.M.F: -SEP-CB-2009-01-0128567, -FOMIX M0024-2013-01-203220, -SS/IMSS/ISSSTE-2010-138721, -SS/IMSS/ISSSTE-2012-01-181124, and -INFR-225520, and to I.GV: INFR-2015-01-254106.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martinez-Fierro, M.L., Garza-Veloz, I., Gutierrez-Arteaga, C. et al. Circulating levels of specific members of chromosome 19 microRNA cluster are associated with preeclampsia development. Arch Gynecol Obstet 297, 365–371 (2018). https://doi.org/10.1007/s00404-017-4611-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00404-017-4611-6

Keywords

Search

Navigation