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MicroRNAs in placental health and disease
Open accessAbstract
MicroRNAs (miRNAs) constitute a large family of small noncoding RNAs that are encoded by the genomes of most organisms. They regulate gene expression through posttranscriptional mechanisms to attenuate protein output in various genetic networks. The discovery of miRNAs has transformed our understanding of gene regulation and sparked intense efforts intended to harness their potential as diagnostic markers and therapeutic tools. Over the last decade, a flurry of studies has shed light on placental miRNAs but has also raised many questions regarding the scope of their biologic action. Moreover, the recognition that miRNAs of placental origin are released continually in the maternal circulation throughout pregnancy suggested that circulating miRNAs might serve as biomarkers for placental function during pregnancy. Although this generated much enthusiasm, recently recognized challenges have delayed the application of miRNA-based biomarkers and therapeutics in clinical practice. In this review, we summarize key findings in the field and discuss current knowledge related to miRNAs in the context of placental biology.
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“The human placenta expresses a wide variety of non-coding RNAs (398), but few data are available regarding their responsiveness to hypoxia.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [398]
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Cites
MicroRNAs: Target Recognition and Regulatory Functions
Bartel, D. P. (2009) · Cell · doi:10.1016/j.cell.2009.01.002 · Cited by 20,068
Tissue-based map of the human proteome
Uhlén, M., Fagerberg, L., Hallström, B. M., Lindskog, C., Oksvold, P., Mardinoglu, A., Sivertsson, Å., Kampf, C., Sjöstedt, E., Asplund, A., et al. (2015) · Science · doi:10.1126/science.1260419 · Cited by 15,286
The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14
Lee, R. C., Feinbaum, R. L., & Ambros, V. (1993) · Cell · doi:10.1016/0092-8674(93)90529-y · Cited by 12,948
Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., & Lötvall, J. O. (2007) · Nature Cell Biology · doi:10.1038/ncb1596 · Cited by 12,834
Lewis, B. P., Burge, C. B., & Bartel, D. P. (2005) · Cell · doi:10.1016/j.cell.2004.12.035 · Cited by 11,855
Circulating microRNAs as stable blood-based markers for cancer detection
Mitchell, P. S., Parkin, R. K., Kroh, E. M., Fritz, B. R., Wyman, S. K., Pogosova-Agadjanyan, E. L., Peterson, A., Noteboom, J., O'Briant, K. C., Allen, A., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804549105 · Cited by 7,969
Regulation of microRNA biogenesis
Ha, M., & Kim, V. N. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3838 · Cited by 5,462
Prediction of Mammalian MicroRNA Targets
Lewis, B. P., Shih, I.-H., Jones-Rhoades, M. W., Bartel, D. P., & Burge, C. B. (2003) · Cell · doi:10.1016/s0092-8674(03)01018-3 · Cited by 5,199
miRBase: annotating high confidence microRNAs using deep sequencing data
Kozomara, A., & Griffiths-Jones, S. (2014) · Nucleic Acids Research · doi:10.1093/nar/gkt1181 · Cited by 5,073
Role for a bidentate ribonuclease in the initiation step of RNA interference
Bernstein, E., Caudy, A. A., Hammond, S. M., & Hannon, G. J. (2001) · Nature · doi:10.1038/35053110 · Cited by 5,018
Cited by
Sorted by citations
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717
Update of syncytiotrophoblast derived extracellular vesicles in normal pregnancy and preeclampsia
Tannetta, D., Masliukaitė, I., Vatish, M., Redman, C. W. G., & Sargent, I. L. (2016) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2016.08.008 · Cited by 212
“008 lipids and miRNAs (recently reviewed by (Tannetta and Sargent, 2013; Tannetta et al., 2014; Mouillet et al., 2015), whilst in PE both qualitative and quantitative differences in shed STBEV have been found, such as changes in the size of EV released and the molecular”
BackgroundInfluentialLapehn, S., & Paquette, A. G. (2022) · Current Environmental Health Reports · doi:10.1007/s40572-022-00354-8 · Cited by 166
“Identification of placenta-specific microRNAs secreted into the maternal blood from exosomes is an area of growing interest as a noninvasive biomarker for pregnancy health [17].”
BackgroundMicroRNAs: crucial regulators of placental development
Hayder, H., O’Brien, J. A., Nadeem, U., & Peng, C. (2018) · Reproduction · doi:10.1530/rep-17-0603 · Cited by 160
Yang, L., Semmes, E. C., Ovies, C., Megli, C., Permar, S. R., Gilner, J. B., & Coyne, C. B. (2022) · eLife · doi:10.7554/elife.79794 · Cited by 132
“To further confirm that TOs and DOs recapitulated their tissues of origin, we profiled the expression of three members of the chromosome 19 microRNA family (C19MC), which are specifically expressed in the human placenta (Mouillet et al., 2015).”
BackgroundSelf-citationPrimary Human Placental Trophoblasts are Permissive for Zika Virus (ZIKV) Replication
Aagaard, K. M., Lahon, A., Suter, M., Arya, R. P., Seferovic, M. D., Vogt, M. B., Hu, M., Stossi, F., Mancini, M. A., Harris, R. A., et al. (2017) · Scientific Reports · doi:10.1038/srep41389 · Cited by 127
“Since C19MC miRNAs and miR-21 may modulate viral replication and inflammatory responses 29–33 , we sought to characterize the expression of the miRNAs in primary human tropho-blasts following ZIKV infection using qPCR.”
Ghafourian, M., Mahdavi, R., Jonoush, Z. A., Sadeghi, M., Ghadiri, N., Farzaneh, M., & Salehi, A. M. (2022) · Cell Communication and Signaling · doi:10.1186/s12964-022-00853-z · Cited by 133
“More than one thousand miRNAs are identified, which are expressed by different layers of the human placenta [106].”
BackgroundSyncytiotrophoblast extracellular vesicles – Circulating biopsies reflecting placental health
Tannetta, D., Collett, G. P., Vatish, M., Redman, C. W. G., & Sargent, I. L. (2016) · Placenta · doi:10.1016/j.placenta.2016.11.008 · Cited by 119
Defense and infection of the human placenta
Heerema‐McKenney, A. (2018) · Apmis · doi:10.1111/apm.12847 · Cited by 120
“to maternal cells distant from the placenta (1, 2, 45).”
BackgroundPlacental programming of neuropsychiatric disease
Kratimenos, P., & Penn, A. A. (2019) · Pediatric Research · doi:10.1038/s41390-019-0405-9 · Cited by 115
Ouyang, Y., Bayer, A., Chu, T., Tyurin, V. A., Kagan, V. E., Morelli, A. E., Coyne, C. B., & Sadovsky, Y. (2016) · Placenta · doi:10.1016/j.placenta.2016.09.008 · Cited by 109
Self-citationNiu, Z., Han, T., Sun, X.-L., Luan, L., Gou, W., & Zhu, X. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.11.568 · Cited by 102
A Dormant Microbial Component in the Development of Preeclampsia
Kell, D. B., & Kenny, L. C. (2016) · Frontiers in Medicine · doi:10.3389/fmed.2016.00060 · Cited by 101
MicroRNAs: New Players in the Pathobiology of Preeclampsia
Bounds, K. R., Chiasson, V. L., Pan, L. J., Gupta, S., & Chatterjee, P. (2017) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2017.00060 · Cited by 100
Imprinted MicroRNA Gene Clusters in the Evolution, Development, and Functions of Mammalian Placenta
Malnou, C. E., Umlauf, D., Mouysset, M., & Cavaillé, J. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2018.00706 · Cited by 100
Preeclampsia: novel insights from global RNA profiling of trophoblast subpopulations
Gormley, M. J., Ona, K., Kapidzic, M., Garrido‐Gómez, T., Zdravkovic, T., & Fisher, S. J. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.03.017 · Cited by 99
Sex at the interface: the origin and impact of sex differences in the developing human placenta
Braun, A. E., Mitchel, O. R., Gonzalez, T. L., Sun, T., Flowers, A. E., Pisarska, M. D., & Winn, V. D. (2022) · Biology of Sex Differences · doi:10.1186/s13293-022-00459-7 · Cited by 94
“Sex differences in microRNA in human placenta Consisting of single-stranded non-coding RNA molecules approximately 22 nucleotides in length [94], microRNAs (miRNAs) regulate mRNA transcription and translation [95].”
BackgroundImpacts of bisphenol A (BPA) and phthalate exposures on epigenetic outcomes in the human placenta
Strakovsky, R. S., & Schantz, S. L. (2018) · Current Zoology · doi:10.1093/eep/dvy022 · Cited by 94
“miRs are small non-coding RNAs that post-transcriptionally regulate gene expression, and several miR clusters within the placenta have been shown to regulate placental development and function (reviewed in [42]).”
BackgroundBiró, O., Alasztics, B., Molvarec, A., Joó, J. G., Nagy, B., & Rigó, J. J. (2017) · Pregnancy Hypertension · doi:10.1016/j.preghy.2017.09.002 · Cited by 87
“More than one thousand miRNAs are expressed by different layers of the human placenta, some of which are primate-specific and only present in placental and stem cells [19].”
BackgroundPregnancy immune tolerance at the maternal-fetal interface
Li, X., Zhou, J., Fang, M., & Yu, B. (2020) · International Reviews of Immunology · doi:10.1080/08830185.2020.1777292 · Cited by 88
Second trimester extracellular microRNAs in maternal blood and fetal growth: An exploratory study
Rodosthenous, R. S., Burris, H. H., Sanders, A. P., Just, A. C., Dereix, A. E., Svensson, K., Solano, M., Téllez‐Rojo, M. M., Wright, R. O., & Baccarelli, A. (2017) · Epigenetics · doi:10.1080/15592294.2017.1358345 · Cited by 85
“mal and abnormal placentas, and were detected in maternal blood EVs as well.(6) In addition, a few studies have identified microRNAs that were differentially expressed in placentas from pregnancies complicated by fetal growth restriction.”
BackgroundPlacental outcomes of phthalate exposure
Warner, G. R., Dettogni, R. S., Bagchi, I. C., Flaws, J. A., & Graceli, J. B. (2021) · Reproductive Toxicology · doi:10.1016/j.reprotox.2021.05.001 · Cited by 84
Poirier, C., Desgagné, V., Guérin, R., & Bouchard, L. (2017) · Current Diabetes Reports · doi:10.1007/s11892-017-0856-5 · Cited by 79
Genome-wide microRNA expression profiling in placentae from frozen-thawed blastocyst transfer
Hiura, H., Hattori, H., Kobayashi, N., Okae, H., Chiba, H., Miyauchi, N., Kitamura, A., Kikuchi, H., Yoshida, H., & Arima, T. (2017) · Clinical Epigenetics · doi:10.1186/s13148-017-0379-6 · Cited by 75
“Abnormal expression of miRNAs has been observed in pregnancy-associated diseases and recurrent pregnancy loss [13, 14].”
BackgroundFallen, S., Baxter, D. H., Wu, X., Kim, T., Shynlova, O. P., Lee, M. Y., Scherler, K., Lye, S. J., Hood, L., & Wang, K. (2018) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13570 · Cited by 73
“The miRNAs in these clusters have been implicated in placenta development.(20) The chromosome 14 microRNA cluster (C14MC) is located at the imprinted, maternally expressed DLK-DIO3 region on the human chromosome 14q32 and is the largest known miRNA cluster with 52 miRNA precursors (miRBase, www.”
BackgroundMicroRNAs: Small molecules with a large impact on pre‐eclampsia
Hemmatzadeh, M., Shomali, N., Yousefzadeh, Y., Mohammadi, H., Ghasemzadeh, A., & Yousefi, M. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.29286 · Cited by 67
Pillay, P., Vatish, M., Duarte, R. A. B., Moodley, J., & Mackraj, I. (2019) · International Journal of Nanomedicine · doi:10.2147/ijn.s208865 · Cited by 73
Circulating MicroRNAs as Biomarkers of Gestational Diabetes Mellitus: Updates and Perspectives
Guarino, E., Poggi, C. D., Grieco, G. E., Cenci, V., Ceccarelli, E., Crisci, I., Sebastiani, G., & Dotta, F. (2018) · International Journal of Endocrinology · doi:10.1155/2018/6380463 · Cited by 68
Placenta-Derived MicroRNAs in the Pathophysiology of Human Pregnancy
Xu, P., Ma, Y., Wu, H., & Wang, Y. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.646326 · Cited by 67
Progress in the understanding of the etiology and predictability of fetal growth restriction
Tang, L. P., He, G., Liu, X., & Xu, W. (2017) · Reproduction · doi:10.1530/rep-16-0287 · Cited by 63
“Although C14MC produces many groups of miRNAs in the placenta, most of them are considered nonfunctional and the function of others remain unknown (Mouillet et al. 2015).”
BackgroundMiRNA‐548c‐5p downregulates inflammatory response in preeclampsia via targeting PTPRO
Wang, Z., Wang, P., Wang, Z., Qin, Z., Xiu, X., Xu, D., Zhang, X., & Wang, Y. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27758 · Cited by 60
Pre-eclampsia predictive ability of maternal miR-125b: a clinical and experimental study
Licini, C., Avellini, C., Picchiassi, E., Mensa’, E., Fantone, S., Ramini, D., Tersigni, C., Tossetta, G., Castellucci, C., Tarquini, F., et al. (2020) · Translational research · doi:10.1016/j.trsl.2020.07.011 · Cited by 61
FLT1 and transcriptome-wide polyadenylation site (PAS) analysis in preeclampsia
Ashar-Patel, A., Kaymaz, Y., Rajakumar, A., Bailey, J. A., Karumanchi, S. A., & Moore, M. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-11639-6 · Cited by 61
Addo, K., Palakodety, N., Hartwell, H. J., Tingare, A., & Fry, R. C. (2020) · Toxicology Reports · doi:10.1016/j.toxrep.2020.08.002 · Cited by 59
Identification of microRNAs in skeletal muscle associated with lung cancer cachexia
van de Worp, W. R. P. H., Schols, A. M. W. J., Dingemans, A. C., den Kamp, C. M. O., Degens, J. H. R. J., KELDERS, M. C. J. M., Coort, S. L., Woodruff, H. C., Kratassiouk, G., Harel‐Bellan, A., et al. (2019) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12512 · Cited by 56
“C19MC is one of the largest miRNA clusters in human genome.(52,53) The miRNAs of the C19MC are expressed from the paternal chromosome and promote pluripotent stem cell phenotype,(52) and their activity towards promoting stem cell survival has been implicated in muscle mass maintenance.”
BackgroundEndogenous and exogenous miR-520c-3p modulates CD44-mediated extravillous trophoblast invasion
Takahashi, H., Ohkuchi, A., Kuwata, T., Usui, R., Baba, Y., Suzuki, H., Kyi, T. T. C., Matsubara, S., Saito, S., & Takizawa, T. (2016) · Placenta · doi:10.1016/j.placenta.2016.12.016 · Cited by 54
MiRNAs in the Peri-Implantation Period: Contribution to Embryo–Maternal Communication in Pigs
Kaczmarek, M. M., Szuszkiewicz, J., Guzewska, M. M., & Przygrodzka, E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21062229 · Cited by 53
“To date, miRNAs have been shown to change significantly throughout the course of many diseases and physiological conditions, including pregnancy disorders [89].”
BackgroundMicroRNA-Mediated Gene Regulatory Mechanisms in Mammalian Female Reproductive Health
Gebremedhn, S., Ali, A., Hossain, M. M., Hoelker, M., Salilew‐Wondim, D., Anthony, R. V., & Tesfaye, D. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020938 · Cited by 52
“Chromosome 14 miRNA cluster (C14MC) produces 63 mature miRNAs in humans, which are highly expressed in the placenta [107].”
BackgroundProsthetic joint infections in the elderly.
Powers, K., Terpenning, M. S., Voice, R. A., & Kauffman, C. A. (1990) · PubMed · Cited by 52
miR-142-3p as a biomarker of blastocyst implantation failure - A pilot study
Borges, E., Setti, A. S., Braga, D. P. A. F., Geraldo, M. V., Figueira, R. D. C. S., & Iaconelli, A. (2016) · JBRA · doi:10.5935/1518-0557.20160039 · Cited by 49
“They were first described in the nematode Caenorhabditis elegans (Lee et al. 1993; Wightman et al. 1993) and later found in the genomes of protists, plants, animals, and viruses (Mouillet et al., 2015).”
BackgroundHayder, H., Shan, Y., Chen, Y., O’Brien, J. A., & Peng, C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.995462 · Cited by 50
“They are also reported to be dysregulated in many pregnancy-related diseases including PE (Fu et al., 2013a; Bidarimath et al., 2014; Mouillet et al., 2015; Munaut et al., 2016; Cai et al., 2017; Carreras-Badosa et al., 2017; Lykoudi et al., 2018; Ali et al., 2021).”
BackgroundMicroRNA-Mediated Control of Inflammation and Tolerance in Pregnancy
Kamity, R., Sharma, S., & Hanna, N. N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00718 · Cited by 51
“A previous study reported the deletion of the miR379/410 cluster (from C14MC) without consequence (84).”
BackgroundLi, L., Huang, X., He, Z., Xiong, Y., & Fang, Q. (2019) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14335 · Cited by 48
Fitzgerald, W., Gomez‐Lopez, N., Erez, O., Romero, R. J., & Margolis, L. B. (2018) · American Journal of Reproductive Immunology · doi:10.1111/aji.12860 · Cited by 49
Vrachnis, N., Loukas, N., Vrachnis, D. N., Antonakopoulos, N., Zygouris, D., Kοlialexi, A., Pergialiotis, V., Iavazzo, C. R., Mastorakos, G. P., & Iliodromiti, Z. (2021) · Nutrients · doi:10.3390/nu13072426 · Cited by 49
“In addition, altered placental micro-RNA expression has the potential to affect fetal growth by affecting placental development and function [11,12].”
BackgroundPlacental miR-340 mediates vulnerability to activity based anorexia in mice
Schroeder, M., Jakovcevski, M., Polacheck, T., Drori, Y., Luoni, A., Röh, S., Zaugg, J., Ben‐Dor, S., Albrecht, C., & Chen, A. (2018) · Nature Communications · doi:10.1038/s41467-018-03836-2 · Cited by 44
“d−f Fetus weight was similar in control and PNS offspring (d), but placental weight was reduced by PNS only in females (twoway ANOVA Fint(1,18)= 4.”
BackgroundInfluentialGu, H., Chen, L., Xue, J., Huang, T., Wei, X., Liu, D., Ma, W., Cao, S., & Yuan, Z. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.10.110 · Cited by 46
Balaguer, N., Moreno, I., Herrero, M., Gonzáléz-Monfort, M., Vilella, F., & Simón, C. (2019) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2019.02.047 · Cited by 45
The expression level of C19MC miRNAs in early pregnancy and in response to viral infection
Dumont, T., Mouillet, J., Bayer, A., Gardner, C. L., Klimstra, W. B., Wolf, D. G., Yagel, S., Balmir, F., Binstock, A., Sanfilippo, J. S., et al. (2017) · Placenta · doi:10.1016/j.placenta.2017.03.011 · Cited by 42
Self-citationKowalczyk, A., Gajda, A., Ruzycka-Ayoush, M., Targońska, A., Mosieniak, G., Głogowski, M., Szumera‐Ciećkiewicz, A., Prochorec‐Sobieszek, M., Bamburowicz‐Klimkowska, M., Nowicka, A. M., et al. (2023) · Analytical Chemistry · doi:10.1021/acs.analchem.3c00772 · Cited by 41
MicroRNAs in Uteroplacental Vascular Dysfunction
Hu, X., & Zhang, L. (2019) · Cells · doi:10.3390/cells8111344 · Cited by 45
“Not surprisingly, dysregulated expression of uteroplacental miRNAs has been demonstrated in both preeclampsia and IUGR, implicating their potential roles in the pathogenesis of these complications [15,18,19].”
BackgroundDiabetes in Pregnancy and MicroRNAs: Promises and Limitations in Their Clinical Application
Ibarra, A., Guedes, B. V., Brito‐Casillas, Y., & Wägner, A. M. (2018) · Non-Coding RNA · doi:10.3390/ncrna4040032 · Cited by 39
“The human placenta also expresses numerous types of miRNA species (reviewed in Reference [33]), which are encoded at all but chromosome Y [34].”
BackgroundLégaré, C., Clément, A., Desgagné, V., Thibeault, K., White, F., Guay, S., Arsenault, B. J., Scott, M. S., Jacques, P., Perron, P., et al. (2022) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-021-00883-1 · Cited by 38
“Studies support that microRNAs (miRNAs) regulate embryonic and fetal growth and development as well as maternal metabolic adaptations and maintenance of pregnancy [1, 2].”
BackgroundLin, X., Yang, P., Reece, E. A., & Yang, P. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.04.008 · Cited by 36
Cirkovic, A. M., Stanisavljevic, D. M., Milin-Lazovic, J. S., Rajović, N., Pavlovic, V. R., Milicevic, O. S., Savic, M. D., Kostic, J., Aleksic, N., Milic, N., et al. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.782845 · Cited by 37
“This results in pathologic remodeling of the placental arterioles, which become narrow, with reduced flow and sclerotic changes in the arteriolar walls (Mouillet et al., 2015).”
BackgroundInfluentialPrecise Personalized Medicine in Gynecology Cancer and Infertility
Zhang, P.-Y., & Yu, Y. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00382 · Cited by 34
Diagnostic Potential of MicroRNAs as Biomarkers in the Detection of Preeclampsia
Horňáková, A., Kolková, Z., Holubeková, V., Loderer, D., Lasabová, Z., Biringer, K., & Halášová, E. (2020) · Genetic Testing and Molecular Biomarkers · doi:10.1089/gtmb.2019.0264 · Cited by 34
“Several studies have explored the importance of miRNA-regulated gene expression in the physiological process of placental development, as well as in the pathogenesis of PE (Fu et al. , 2013; Mouillet et al. , 2015; Wang et al. , 2016b; Gormley et al. , 2017).”
Identifying miRNA regulatory mechanisms in preeclampsia by systems biology approaches
Biró, O., Nagy, B., & Rigó, J. J. (2016) · Hypertension in Pregnancy · doi:10.1080/10641955.2016.1239736 · Cited by 33
“the regulation of placental development and are essential for normal physiology (10).”
BackgroundJoshi, A. S., Azuma, R., Akumuo, R. C., Goetzl, L. M., & Pinney, S. E. (2019) · International Journal of Obesity · doi:10.1038/s41366-019-0485-y · Cited by 34
Smith, M., Pillman, K. A., Jankovic‐Karasoulos, T., McAninch, D., Wan, Q., Bogias, K. J., McCullough, D., Bianco‐Miotto, T., Breen, J., & Roberts, C. T. (2021) · RNA Biology · doi:10.1080/15476286.2021.1963105 · Cited by 33
Associations of maternal and placental extracellular vesicle miRNA with preeclampsia
Aharon, A., Rebibo-Sabbah, A., Ahmad, R. S., Dangot, A., Bar-Lev, T. H., Brenner, B., Halberthal-Cohen, A., David, C. B., Weiner, Z., & Solt, I. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1080419 · Cited by 33
“…2013; Mitchell et al., 2015) suggests that the relevant mechanism is apparently a non-random process (Diehl et al., 2012; Boon and Vickers, 2013; Niu et al., 2018) related to EVs as a source of miRNAs that promote GVCs. Previously, we demonstrated that EVs from women with GVCs contain higher…”
BackgroundPaquette, A. G., Chu, T., Wu, X., Wang, K., Price, N. D., & Sadovsky, Y. (2018) · Placenta · doi:10.1016/j.placenta.2018.10.004 · Cited by 31
“Selected C19MC miRNA species also hinder trophoblast differentiation [20], and regulate the migration of extravillous trophoblasts by targeting specific transcripts related to cellular movement [5,21].”
BackgroundSelf-citationMeng, M., Cheng, Y. K. Y., Wu, L., Chaemsaithong, P., Leung, B. W., Chim, S. S. C., Sahota, D. S., Li, W., Poon, L. C., Wang, C. C., et al. (2020) · Placenta · doi:10.1016/j.placenta.2020.02.002 · Cited by 31
Medina, L., Castillo, C., Liempi, A. I., Guerrero-Muñoz, J., Rojas-Pirela, M., Maya, J. D., Humberto Prieto, E., & Kemmerling, U. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.595250 · Cited by 31
“Moreover, epigenetic and genetic defects in miRNAs and their processing machinery are a common hallmark of infection and diseases that include pregnancy-specific pathologies such as preeclampsia (17, 38).”
BackgroundHan, S., Chen, Y., Gao, Y. L., Sun, B., & Kong, Y. (2018) · Experimental Eye Research · doi:10.1016/j.exer.2018.09.010 · Cited by 30
Serum miRNA biomarker discovery for placenta accreta spectrum
Chen, S., Pang, D., Li, Y., Zhou, J., Liu, Y., Yang, S., Liang, K., & Yu, B. (2020) · Placenta · doi:10.1016/j.placenta.2020.09.068 · Cited by 30
Data-Driven Medicine in the Diagnosis and Treatment of Infertility
de Santiago, I., & Polański, Ł. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11216426 · Cited by 32
“…as non-coding RNAs, where some authors propose the use of non-coding RNAs and microRNAs as being predictive of male infertility [45,46], placental function during pregnancy [47], and of circulating small non-coding RNAs in the first trimester [48] as a non-invasive diagnostic tool for preeclampsia.”
BackgroundOgoyama, M., Ohkuchi, A., Takahashi, H., Zhao, D., Matsubara, S., & Takizawa, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031237 · Cited by 29
“, placenta-associated miRNAs), there are two other placenta-associated miRNA clusters in chromosome 19: the chromosome-19 miRNA cluster (designated as C19MC; 46 miRNA precursors) and the miR-371-3 cluster (three miRNA precursors in the vicinity of C19MC) [84,85].”
BackgroundInfluentialA blood-based miRNA signature for early non-invasive diagnosis of preeclampsia
Bao, S., Zhou, T., Yan, C., Bao, J., Yang, F., Chao, S., Zhou, M., & Xu, Z. (2022) · BMC Medicine · doi:10.1186/s12916-022-02495-x · Cited by 29
Elevated microRNA-34a contributes to trophoblast cell apoptosis in preeclampsia by targeting BCL-2
Guo, M., Zhao, X., Yuan, X., & Li, P. (2017) · Journal of Human Hypertension · doi:10.1038/jhh.2017.65 · Cited by 29
Distinct microRNA profiles for complete hydatidiform moles at risk of malignant progression
Lin, L. H., Maestá, I., Laurent, J. D. S., Hasselblatt, K. T., Horowitz, N. S., GOLDSTEIN, D. P., Quade, B. J., Sun, S. Y., Braga, A., Fisher, R. A., et al. (2020) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.09.048 · Cited by 29
Tang, M., Bai, L., Wan, Z., Wan, S., Xiang, Y., Qian, Y., Cui, L., You, J., Hu, X., Qu, F., et al. (2021) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2021.06.012 · Cited by 27
“In the placenta, at least 500 different miRNAs have been identified.(14) These miRNAs are involved in placental”
BackgroundMiura, K., 東島, 愛., Murakami, Y., Fuchi, N., Tsukamoto, O., Abe, S., Hasegawa, Y., Miura, S., & Masuzaki, H. (2016) · Reproductive Sciences · doi:10.1177/1933719116653837 · Cited by 25
“plasma may reflect the condition of placental abruption.(18-21) If prenatal prediction of placental abruption can be provided by monitoring the circulating pattern of cell-free C19MC miRNAs in maternal plasma, it will enable a reduction in both fetal and maternal mortalities from this condition.”
BackgroundmicroRNA signatures associated with fetal growth restriction: a systematic review
Kochhar, P., Vukku, M., Rajashekhar, R., & Mukhopadhyay, A. (2021) · European Journal of Clinical Nutrition · doi:10.1038/s41430-021-01041-x · Cited by 26
Peiris, H. N., Vaswani, K., Almughlliq, F. B., Koh, Y. Q., & Mitchell, M. D. (2016) · Placenta · doi:10.1016/j.placenta.2016.12.013 · Cited by 24
Saha, S., Chakraborty, S., Bhattacharya, A., Biswas, A., & Ain, R. (2017) · Scientific Reports · doi:10.1038/s41598-017-16566-0 · Cited by 24
Awamleh, Z., & Han, V. K. M. (2020) · Pregnancy Hypertension · doi:10.1016/j.preghy.2020.01.002 · Cited by 24
Sundrani, D. P., Karkhanis, A. R., & Joshi, S. (2021) · Systems Biology in Reproductive Medicine · doi:10.1080/19396368.2020.1858994 · Cited by 24
“These placental extracellular miRNAs are derived primarily from the trophoblast layer, which lines the human placental villi (Mouillet et al. 2015).”
BackgroundZolfaghari, M. A., Motavalli, R., Soltani‐Zangbar, M. S., Parhizkar, F., Danaii, S., Maleki, L. A., Noori, M., Dolati, S., Ahmadi, M., Kafil, H. S., et al. (2021) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2021.103317 · Cited by 23
Whigham, C., MacDonald, T. M., Walker, S. P., Hiscock, R. J., Hannan, N. J., Pritchard, N., Cannon, P., Nguyen, T. V., Miranda, M., Tong, S. Y. C., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-73783-w · Cited by 21
Yao, P., Hu, G., & Niu, H. (2021) · Biochemical Genetics · doi:10.1007/s10528-021-10095-2 · Cited by 22
The inter- and multi- generational epigenetic alterations induced by maternal cadmium exposure
Lawless, L., Xie, L., & Zhang, K. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1148906 · Cited by 24
“Within the placenta, miRNAs are involved in regulating trophoblast differentiation, migration, invasion, and vasculogenesis (Mouillet et al., 2015; Hayder et al., 2018).”
BackgroundTimofeeva, A. V., Fedorov, I. S., Вячеславовна, С. Ю., Ivanets, T. Y., & Sukhikh, G. T. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24098006 · Cited by 21
Cell-free nucleic acids in prenatal diagnosis and pregnancy-associated diseases.
Nagy, B. (2019) · PubMed Central · Cited by 19
Xu, N., Zhou, X., Shi, W., Ye, M., Cao, X., Chen, S., & Xu, C. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.893744 · Cited by 19
“Approximately 600 miRNAs are expressed in the human placenta and play key roles in placental development and function by regulating the expressions of genes involved in trophoblast proliferation, differentiation, invasion, migration, apoptosis, and angiogenesis (Mouillet et al., 2015; Chen et al., 2021).”
BackgroundPisarska, M. D., Akhlaghpour, M., Lee, B., Barlow, G. M., Xu, N., Wang, E. T., Mackey, A. J., Farber, C. R., Rich, S. S., Rotter, J. I., et al. (2016) · Prenatal Diagnosis · doi:10.1002/pd.4936 · Cited by 19
Non‐coding RNAs and their cross‐talks impacting reproductive health of women
Jain, N., Gupta, P., Sahoo, S., & Mallick, B. (2021) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1695 · Cited by 19
“Not surprisingly, the human placenta expresses a large number of miRNAs, particularly in trophoblasts, indicating their importance in fetal development (Mouillet et al., 2015).”
BackgroundPrats‐Puig, A., Xargay‐Torrent, S., Carreras‐Badosa, G., Mas‐Parés, B., Bassols, J., Petry, C. J., Girardot, M., de Zegher, F., Ibáñez, L., Dunger, D. B., et al. (2019) · International Journal of Obesity · doi:10.1038/s41366-019-0450-9 · Cited by 18
HMGA2 is regulated by LIN28 and BRCA1 in human placental cells†
West, R. C., McWhorter, E. S., Ali, A., Goetzmann, L. N., Russ, J. E., Gonzalez-Berrios, C. L., Anthony, R. V., Bouma, G. J., & Winger, Q. A. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy183 · Cited by 17
Placental extracellular vesicles promote cardiomyocyte maturation and fetal heart development
Jeyarajah, M. J., Patterson, V. S., Bhattad, G. J., Zhao, L., Whitehead, S. N., & Renaud, S. J. (2024) · Communications Biology · doi:10.1038/s42003-024-06938-4 · Cited by 17
Fetal microchimerism by mode of delivery: a prospective cohort study
Shree, R. S., Harrington, W., Kanaan, S. B., Forsyth, A. M., Cousin, E. M., López, A. M. A., Nelson, J. L., & Gammill, H. S. (2018) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.15432 · Cited by 18
Liu, B., Liu, L., Cui, S., Qi, Y. A., & Wang, T. (2021) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.14732 · Cited by 17
“At present, at least 500 different miRNAs are known to be expressed in placental trophoblast cells, but the biological significance of most miRNAs is still unclear.(6) Recent studies have shown that the disorder of miRNA in placental tissues is related to the pathogenesis of PE.”
BackgroundSex differences in microRNA expression in first and third trimester human placenta
Flowers, A. E., Gonzalez, T. L., Joshi, N. V., Eisman, L. E., Clark, E. L., Buttle, R. A., Sauro, E., DiPentino, R., Lin, Y., Wu, D., et al. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab221 · Cited by 18
“miRNAs generally cause target messenger RNA to be degraded, or prevent translation to protein [13]; small changes in miRNA expression can result in multi-fold changes in gene expression [14].”
BackgroundMaternal paraben exposure and intra-pair thyroid-stimulating hormone difference in twin neonates
Hu, L., Mei, H., Cai, X., Hu, X.-J., Duan, Z., Liu, J., Tan, Y., Yang, P., Xiao, H., & Zhou, A. (2023) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2023.114502 · Cited by 16
Maternal plasma mRNA species in fetal heart defects: a potential for molecular screening
Curti, A., Lapucci, C., Berto, S., Prandstraller, D., Perolo, A., Rizzo, N., & Farina, A. (2016) · Prenatal Diagnosis · doi:10.1002/pd.4853 · Cited by 16
“miRNAs are released into the extracellular systemic circulation via exosomes(7) and have also been isolated in maternal plasma as has recently been reported.(8) It is worth noting that both circulating mRNA and miRNA species have recently been evaluated for their possible association with CHDs.”
BackgroundEvaluation of circulating miRNAs during late pregnancy in the mare
Loux, S. C., Scoggin, K. E. S., Bruemmer, J. E., Canisso, I. F., Troedsson, M. H. T., Squires, E. L., & Ball, B. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175045 · Cited by 16
Increased fetal microchimerism in immune and stem cell subsets in preeclampsia
McCartney, S. A., Kolarova, T. R., Kanaan, S. B., Chae, A., Laughney, C. I., Nelson, J. L., Gammill, H. S., & Shree, R. S. (2022) · American Journal of Reproductive Immunology · doi:10.1111/aji.13666 · Cited by 15
Physiopathology of late-onset fetal growth restriction
Júnior, E. A., Zamarian, A. C. P., Caetano, A. C. R., Peixoto, A. B., & Nardozza, L. M. M. (2021) · Minerva Obstetrics and Gynecology · doi:10.23736/s2724-606x.21.04771-7 · Cited by 15
kshv-mir-k12-1-5p promotes cell growth and metastasis by targeting SOCS6 in Kaposi’s sarcoma cells
Zhang, J., Pu, X., & Xiong, Y. (2019) · Cancer Management and Research · doi:10.2147/cmar.s198411 · Cited by 15
“They can also serve as cancer diagnostic markers and potential therapeutic targets.(15) One study showed that miR-143/145 was an upregulated miRNA biomarker, while miR-221/222, miR-155, and the let-7 family were downregulated in KS.”
BackgroundAwamleh, Z., & Han, V. K. M. (2020) · Molecular Biology Reports · doi:10.1007/s11033-020-05705-y · Cited by 15
Metadata
- Authors
- Mouillet, J.-F., Ouyang, Y., Coyne, C. B., & Sadovsky, Y.
- Affiliations
- University of Pittsburgh (US)
- Corresponding author
- Sadovsky, Yoel
- Venue
- American Journal of Obstetrics and Gynecology
- Publisher
- Elsevier BV
- Published
- 2015-10
- Volume
- 213
- Issue
- 4
- Pages
- S163-S172
- ISSN
- 0002-9378 (ISSN-L)
- PMC
- PMC4592520
- OpenAlex
- W2128949071
- Cited by
- 195
- References
- 157
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 13 · 2023: 20 · 2022: 25 · 2021: 25 · 2020: 23 · 2019: 18 · 2018: 19 · 2017: 19 · 2016: 15
- FWCI
- 2.61
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- American Journal of Obstetrics and Gynecology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Pennsylvania Department of Health
- National Institutes of Health (0863906)
- National Institute of Allergy and Infectious Diseases (R01AI081759)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21HD071707, R01HD065893, R01HD075665)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- microRNA, placenta, placental function, placental disease, circulating microRNAs, pregnancy, biomarkers, post-transcriptional regulation, non-coding RNA, miRNA-based therapy
- MeSH terms
- Extracellular Space, Female, Humans, Placenta Diseases, Pregnancy, Biomarkers, MicroRNAs
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