First trimester screening of circulating C19MC microRNAs and the evaluation of their potential to predict the onset of preeclampsia and IUGR
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
28182660
PubMed Central
PMC5300267
DOI
10.1371/journal.pone.0171756
PII: PONE-D-16-36781
Knihovny.cz E-zdroje
- MeSH
- biologické markery krev MeSH
- dospělí MeSH
- lidé MeSH
- mikro RNA krev MeSH
- prediktivní hodnota testů MeSH
- preeklampsie krev diagnóza MeSH
- prenatální diagnóza metody MeSH
- první trimestr těhotenství krev MeSH
- růstová retardace plodu krev diagnóza MeSH
- stanovení celkové genové exprese MeSH
- studie případů a kontrol MeSH
- těhotenství MeSH
- Check Tag
- dospělí MeSH
- lidé MeSH
- těhotenství MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- biologické markery MeSH
- mikro RNA MeSH
OBJECTIVES: A nested case control study of a longitudinal cohort comparing pregnant women enrolled at 10 to 13 gestational weeks was carried out to evaluate risk assessment for preeclampsia and IUGR based on circulating placental specific C19MC microRNAs in early pregnancy. METHODS: The expression of placental specific C19MC microRNAs (miR-516b-5p, miR-517-5p, miR-518b, miR-520a-5p, miR-520h, and miR-525-5p) was determined in plasma samples from pregnancies that subsequently developed preeclampsia (n = 21), IUGR (n = 18), and 58 normal pregnancies using real-time PCR and comparative Ct method relative to synthetic Caenorhabditis elegans microRNA (cel-miR-39). RESULTS: Circulating C19MC microRNAs were up-regulated (miR-517-5p, p = 0.005; miR-518b, p = 0.013; miR-520h, p = 0.021) or showed a trend toward up-regulation in patients destined to develop preeclampsia (miR-520a-5p, p = 0.067; miR-525-5p, p = 0.073). MiR-517-5p had the best predictive performance for preeclampsia with a sensitivity of 42.9%, a specificity of 86.2%, a PPV of 52.9% and a NPV of 80.6%. The combination of all examined circulating C19MC microRNAs had no advantage over using only the miR-517-5p biomarker to predict the occurrence of preeclampsia (a sensitivity of 20.6%, a specificity of 90.8%, a PPV of 44.8%, and a NPV of 76.0%). CONCLUSIONS: Up-regulation of miR-517-5p, miR-518b and miR-520h was associated with a risk of later development of preeclampsia. First trimester screening of extracellular miR-517-5p identified a proportion of women with subsequent preeclampsia. No circulating C19MC microRNA biomarkers were identified that could predict later occurrence of IUGR.
Zobrazit více v PubMed
Lai EC. MicroRNAs are complementary to 3´UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet. 2002;30:175–205. PubMed
Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116: 281–297. PubMed
Hromadnikova I. Extracellular nucleic acids in maternal circulation as potential biomarkers for placental insufficiency. DNA Cell Biol. 2012;31: 1221–1232. 10.1089/dna.2011.1530 PubMed DOI PMC
Luque A, Farwati A, Crovetto F, Crispi F, Figueras F, Gratacós E, et al. Usefulness of circulating microRNAs for the prediction of early preeclampsia at first-trimester of pregnancy. Sci Rep. 2014;4: 4882 10.1038/srep04882 PubMed DOI PMC
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: 232–234. 10.1016/j.tjog.2014.03.001 PubMed DOI
Winger EE, Reed JL, Ji X. First Trimester Pbmc Microrna Predicts Adverse Pregnancy Outcome. Am J Reprod Immunol. 2014;72: 515–526. 10.1111/aji.12287 PubMed DOI
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: 160–167. 10.1016/j.jmoldx.2011.11.003 PubMed DOI
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. Mediators Inflamm. 2013: 186041 10.1155/2013/186041 PubMed DOI PMC
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: e113735 10.1371/journal.pone.0113735 PubMed DOI PMC
Winger EE, Reed JL, Ji X. First-trimester maternal cell microRNA is a superior pregnancy marker to immunological testing for predicting adverse pregnancy outcome. J Reprod Immunol. 2015;110: 22–35. 10.1016/j.jri.2015.03.005 PubMed DOI
Hromadnikova I, Kotlabova K, Hympanova L, Krofta L. Gestational hypertension, preeclampsia and intrauterine growth restriction induce dysregulation of cardiovascular and cerebrovascular disease associated microRNAs in maternal whole peripheral blood. Thromb Res. 2016;137: 126–40. 10.1016/j.thromres.2015.11.032 PubMed DOI
ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Obstet Gynecol. 2002;99: 159–167. PubMed
Vyas S, Nicolaides KH, Bower S, Campbell S. Middle cerebral artery flow velocity waveforms in fetal hypoxaemia. Br J Obstet Gynaecol. 1990;97: 797–803. PubMed
Arbeille P, Body G, Saliba E, Tranquart F, Berson M, Roncin A, et al. Fetal cerebral circulation assessment by Doppler ultrasound in normal and pathological pregnancies. Eur J Obstet Gynecol Reprod Biol. 1988;29: 261–273. PubMed
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25: 402–408. 10.1006/meth.2001.1262 PubMed DOI
Cnattingius S, Reilly M, Pawitan Y, Lichtenstein P. Maternal and fetal genetic factors account for most of familial aggregation of preeclampsia: a population-based Swedish cohort study. Am J Med Genet A. 2004;130A: 365–371. 10.1002/ajmg.a.30257 PubMed DOI
Yliniemi A, Makikallio K, Korpimaki T, Kouru H, Marttala J, Ryynanen M. Combination of PAPPA, fhCGβ, AFP, PlGF, sTNFR1, and Maternal Characteristics in Prediction of Early-onset Preeclampsia. Clin Med Insights Reprod Health. 2015;9: 13–20. 10.4137/CMRH.S21865 PubMed DOI PMC
Noguer-Dance M, Abu-Amero S, Al-Khtib M, Lefèvre A, Coullin P, Moore GE, et al. The primate-specific microRNA gene cluster (C19MC) is imprinted in the placenta. Hum Mol Genet. 2010;19: 3566–3582. 10.1093/hmg/ddq272 PubMed DOI
Bentwich I, Avniel A, Karov Y, Aharonov R, Gilad S, Barad O, et al. Identification of hundreds of conserved and non-conserved human microRNAs. Nat Genet. 2005;37: 766–770. 10.1038/ng1590 PubMed DOI
Zhang R, Wang YQ, Su B. Molecular evolution of a primate-specific microRNA family. Mol Biol Evol. 2008;25: 1493–1502. 10.1093/molbev/msn094 PubMed DOI
Bortolin-Cavaillé ML, Dance M, Weber M, Cavaillé J. C19MC microRNAs are processed from introns of large Pol-II, non-protein-coding transcripts. Nucleic Acids Res. 2009;37: 3464–3473. 10.1093/nar/gkp205 PubMed DOI PMC
Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007;129: 1401–1414. 10.1016/j.cell.2007.04.040 PubMed DOI PMC
Liang Y, Ridzon D, Wong L, Chen C. Characterization of microRNA expression profiles in normal human tissue. BMC Genomics. 2007;8: 166 10.1186/1471-2164-8-166 PubMed DOI PMC
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: 610–621. 10.1101/gr.7179508 PubMed DOI PMC
Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S, et al. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol. 2008;10: 202–210. 10.1038/ncb1681 PubMed DOI
Li M, Lee KF, Lu Y, Clarke I, Shih D, Eberhart C, et al. Frequent amplification of a chr19q13.41 microRNA polycistron in aggressive primitive neuroectodermal brain tumors. Cancer Cell. 2009;16: 533–546. 10.1016/j.ccr.2009.10.025 PubMed DOI PMC
Rippe V, Dittberner L, Lorenz VN, Drieschner N, Nimzyk R, Sendt W, et al. The two stem cell microRNA gene clusters C19MC and miR-371-3 are activated by specific chromosomal rearrangements in a subgroup of thyroid adenomas. PLoS One. 2010;5: e9485 10.1371/journal.pone.0009485 PubMed DOI PMC
Ouyang Y, Mouillet JF, Coyne CB, Sadovsky Y. Review: placenta-specific microRNAs in exosomes—good things come in nano-packages. Placenta. 2014;35, Suppl: S69–73. PubMed PMC
Donker RB, Mouillet JF, Chu T, Hubel CA, Stolz DB, Morelli AE, et al. The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes. Mol Hum Reprod. 2012;18: 417–424. 10.1093/molehr/gas013 PubMed DOI PMC
Luo SS, Ishibashi O, Ishikawa G, Ishikawa T, Katayama A, Mishima T, et al. Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol Reprod. 2009;81: 717–729. 10.1095/biolreprod.108.075481 PubMed DOI
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: 185–191. 10.1016/j.jri.2011.02.006 PubMed DOI
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: 1767–1771. 10.1373/clinchem.2010.147660 PubMed DOI
Morales-Prieto DM, Ospina-Prieto S, Chaiwangyen W, Schoenleben M, Markert UR. Pregnancy-associated miRNA-clusters. J Reprod Immunol. 2013;97: 51–61. 10.1016/j.jri.2012.11.001 PubMed DOI
Gilad S, Meiri E, Yogev Y, Benjamin S, Lebanony D, Yerushalmi N, et al. Serum microRNAs are promising novel biomarkers. PLoS One. 2008;3: e3148 10.1371/journal.pone.0003148 PubMed DOI PMC
Ong CY, Liao AW, Spencer K, Munim S, Nicolaides KH. First trimester maternal serum free beta human chorionic gonadotrophin and pregnancy associated plasma protein A as predictors of pregnancy complications. BJOG. 2000;107: 1265–1270. PubMed
Smith GC, Stenhouse EJ, Crossley JA, Aitken DA, Cameron AD, Connor JM. Early pregnancy levels of pregnancy-associated plasma protein a and the risk of intrauterine growth restriction, premature birth, preeclampsia, and stillbirth. J Clin Endocrinol Metab. 2002;87: 1762–1767. 10.1210/jcem.87.4.8430 PubMed DOI
Spencer K, Cowans NJ, Chefetz I, Tal J, Meiri H. First-trimester maternal serum PP-13, PAPP-A and second-trimester uterine artery Doppler pulsatility index as markers of pre-eclampsia. Ultrasound Obstet Gynecol. 2007;29: 128–134. 10.1002/uog.3876 PubMed DOI
Canini S, Prefumo F, Pastorino D, Crocetti L, Afflitto CG, Venturini PL, et al. Association between birth weight and first-trimester free beta-human chorionic gonadotropin and pregnancy-associated plasma protein A. Fertil Steril. 2008;89: 174–178. 10.1016/j.fertnstert.2007.02.024 PubMed DOI
Spencer K, Cowans NJ, Nicolaides KH. Low levels of maternal serum PAPP-A in the first trimester and the risk of pre-eclampsia. Prenat Diagn. 2008;28: 7–10. 10.1002/pd.1890 PubMed DOI
Kusanovic JP, Romero R, Chaiworapongsa T, Erez O, Mittal P, Vaisbuch E, et al. A prospective cohort study of the value of maternal plasma concentrations of angiogenic and anti-angiogenic factors in early pregnancy and midtrimester in the identification of patients destined to develop preeclampsia. J Matern Fetal Neonatal Med. 2009;22: 1021–1038. 10.3109/14767050902994754 PubMed DOI PMC
Pihl K, Larsen T, Laursen I, Krebs L, Christiansen M. First trimester maternal serum pregnancy-specific beta-1-glycoprotein (SP1) as a marker of adverse pregnancy outcome. Prenat Diagn. 2009;29: 1256–1261. 10.1002/pd.2408 PubMed DOI
Wortelboer EJ, Koster MP, Cuckle HS, Stoutenbeek PH, Schielen PC, Visser GH. First-trimester placental protein 13 and placental growth factor: markers for identification of women destined to develop early-onset pre-eclampsia. BJOG. 2010;117: 1384–1389 10.1111/j.1471-0528.2010.02690.x PubMed DOI
Chambers AE, Griffin C, Naif SA, Mills I, Mills WE, Syngelaki A, et al. Quantitative ELISAs for serum soluble LHCGR and hCG-LHCGR complex: potential diagnostics in first trimester pregnancy screening for stillbirth, Down's syndrome, preterm delivery and preeclampsia. Reprod Biol Endocrinol. 2012;10: 113 10.1186/1477-7827-10-113 PubMed DOI PMC
Tal R. The role of hypoxia and hypoxia-inducible factor-1alpha in preeclampsia pathogenesis. Biol Reprod. 2012;87: 134 10.1095/biolreprod.112.102723 PubMed DOI
Karahasanovic A, Sørensen S, Nilas L. First trimester pregnancy-associated plasma protein A and human chorionic gonadotropin-beta in early and late pre-eclampsia. Clin Chem Lab Med. 2014;52: 521–525. 10.1515/cclm-2013-0338 PubMed DOI
Poon LC, Nicolaides KH. First-trimester maternal factors and biomarker screening for preeclampsia. Prenat Diagn. 2014;34: 618–627. 10.1002/pd.4397 PubMed DOI
Scazzocchio E, Crovetto F, Triunfo S, Gratacós E, Figueras F. Validation of a first-trimester screening model for pre-eclampsia in an unselected population. Ultrasound Obstet Gynecol. 2016. [Epub ahead of print] PubMed
Crovetto F, Triunfo S, Crispi F, Rodriguez-Sureda V, Roma E, Dominguez C, et al. First trimester screening with specific algorithms for early and late onset fetal growth restriction. Ultrasound Obstet Gynecol. 2016. [Epub ahead of print] PubMed
Leslie K, Thilaganathan B, Papageorghiou A. Early prediction and prevention of pre-eclampsia. Best Pract Res Clin Obstet Gynaecol. 2011;25: 343–354. 10.1016/j.bpobgyn.2011.01.002 PubMed DOI
Keung MH, Chan LS, Kwok HH, Wong RN, Yue PY. Role of microRNA-520h in 20(R)-ginsenoside-Rg3-mediated angiosuppression. J Ginseng Res. 2016;40: 151–159. 10.1016/j.jgr.2015.07.002 PubMed DOI PMC
Vaupel P, Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev. 2007;26: 225–239. 10.1007/s10555-007-9055-1 PubMed DOI
Zhang M, Zhou S, Zhang L, Zhang J, Cai H, Zhu J, et al. miR-518b is down-regulated, and involved in cell proliferation and invasion by targeting Rap1b in esophageal squamous cell carcinoma. FEBS Lett. 2012;586: 3508–3521. 10.1016/j.febslet.2012.08.007 PubMed DOI
Frische EW, Zwartkruis FJ. Rap1, a mercenary among the Ras-like GTPases. Dev Biol. 2010;340: 1–9. 10.1016/j.ydbio.2009.12.043 PubMed DOI
Ribeiro-Neto F, Urbani J, Lemee N, Lou L, Altschuler DL. On the mitogenic properties of Rap1b: cAMP-induced G(1)/S entry requires activated and phosphorylated Rap1b. Proc Natl Acad Sci U S A. 2002;99: 5418–5423. 10.1073/pnas.082122499 PubMed DOI PMC
Wang F, Xue X, Wei J, An Y, Yao J, Cai H, et al. hsa-miR-520h downregulates ABCG2 in pancreatic cancer cells to inhibit migration, invasion, and side populations. Br J Cancer. 2010;103: 567–574. 10.1038/sj.bjc.6605724 PubMed DOI PMC
Su CM, Wang MY, Hong CC, Chen HA, Su YH, Wu CH, et al. miR-520h is crucial for DAPK2 regulation and breast cancer progression. Oncogene. 2016;35: 1134–1142. 10.1038/onc.2015.168 PubMed DOI
Cheng N, Brantley DM, Chen J. The ephrins and Eph receptors in angiogenesis. Cytokine Growth Factor Rev. 2002;13: 75–85. PubMed
Héroult M, Schaffner F, Augustin HG. Eph receptor and ephrin ligand-mediated interactions during angiogenesis and tumor progression. Exp Cell Res. 2006;312: 642–650. 10.1016/j.yexcr.2005.10.028 PubMed DOI
Kuijper S, Turner CJ, Adams RH. Regulation of angiogenesis by Eph-ephrin interactions. Trends Cardiovasc Med. 2007;17: 145–151. 10.1016/j.tcm.2007.03.003 PubMed DOI
Chang YW, Chen MW, Chiu CF, Hong CC, Cheng CC, Hsiao M, et al. Arsenic trioxide inhibits CXCR4-mediated metastasis by interfering miR-520h/PP2A/NF-κB signaling in cervical cancer. Ann Surg Oncol. 2014;21 Suppl 4: S687–S695. PubMed
Rubin JB. Chemokine signaling in cancer: one hump or two? Semin Cancer Biol. 2009;19: 116–122. 10.1016/j.semcancer.2008.10.001 PubMed DOI PMC
Teicher BA, Fricker SP. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res. 2010;16: 2927–2931. 10.1158/1078-0432.CCR-09-2329 PubMed DOI
Li YM, Pan Y, Wei Y, Cheng X, Zhou BP, Tan M, et al. Upregulation of CXCR4 is essential for HER2-mediated tumor metastasis. Cancer Cell. 2004;6: 459–469. 10.1016/j.ccr.2004.09.027 PubMed DOI
Portilho DM, Alves MR, Kratassiouk G, Roche S, Magdinier F, de Santana EC, et al. miRNA expression in control and FSHD fetal human muscle biopsies. PLoS One. 2015;10: e0116853 10.1371/journal.pone.0116853 PubMed DOI PMC
Wang D, Song W, Na Q. The emerging roles of placenta-specific microRNAs in regulating trophoblast proliferation during the first trimester. Aust N Z J Obstet Gynaecol. 2012;52: 565–570. 10.1111/j.1479-828X.2012.01481.x PubMed DOI
Morales-Prieto DM, Chaiwangyen W, Ospina-Prieto S, Schneider U, Herrmann J, Gruhn B, et al. MicroRNA expression profiles of trophoblastic cells. Placenta. 2012;33: 725–734. 10.1016/j.placenta.2012.05.009 PubMed DOI
Flor I, Neumann A, Freter C, Helmke BM, Langenbuch M, Rippe V, et al. Abundant expression and hemimethylation of C19MC in cell cultures from placenta-derived stromal cells. Biochem Biophys Res Commun. 2012;422: 411–416. 10.1016/j.bbrc.2012.05.004 PubMed DOI
Merkerova M, Vasikova A, Belickova M, Bruchova H. MicroRNA expression profiles in umbilical cord blood cell lineages. Stem Cells Dev. 2010;19: 17–26. 10.1089/scd.2009.0071 PubMed DOI
Gu Y, Sun J, Groome LJ, Wang Y. Differential miRNA expression profiles between the first and third trimester human placentas. Am J Physiol Endocrinol Metab. 2013;304: E836–E843. 10.1152/ajpendo.00660.2012 PubMed DOI PMC
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: e21072 10.1371/journal.pone.0021072 PubMed DOI PMC
Higashijima A, Miura K, Mishima H, Kinoshita A, Jo O, Abe S, et al. Characterization of placenta-specific microRNAs in fetal growth restriction pregnancy. Prenat Diagn. 2013;33: 214–222. 10.1002/pd.4045 PubMed DOI
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: 1276–1284. 10.1161/HYPERTENSIONAHA.113.02647 PubMed DOI
Ishibashi O, Ohkuchi A, Ali MM, Kurashina R, Luo SS, Ishikawa T, et al. Hydroxysteroid (17-β) dehydrogenase 1 is dysregulated by miR-210 and miR-518c that are aberrantly expressed in preeclamptic placentas: a novel marker for predicting preeclampsia. Hypertension. 2012;59: 265–273. 10.1161/HYPERTENSIONAHA.111.180232 PubMed DOI
Nelson DM. Apoptotic changes occur in syncytiotrophoblast of human placental villi where fibrin type fibrinoid is deposited at discontinuities in the villous trophoblast. Placenta. 1996;17: 387–391. PubMed
Oudejans CB, Tjoa ML, Westerman BA, Mulders MA, Van Wijk IJ, Van Vugt JM. Circulating trophoblast in maternal blood. Prenat Diagn. 2003;23: 111–116. 10.1002/pd.539 PubMed DOI
Huppertz B, Kingdom JC. Apoptosis in the trophoblast—role of apoptosis in placental morphogenesis. J Soc Gynecol Investig. 2004;11: 353–362. 10.1016/j.jsgi.2004.06.002 PubMed DOI
Orozco AF, Bischoff FZ, Horne C, Popek E, Simpson JL, Lewis DE. Hypoxia-induced membrane-bound apoptotic DNA particles: potential mechanism of fetal DNA in maternal plasma. Ann N Y Acad Sci. 2006;1075: 57–62. 10.1196/annals.1368.007 PubMed DOI
Lo YM, Corbetta N, Chamberlain PF, Rai V, Sargent IL, Redman CW, Wainscoat JS. Presence of fetal DNA in maternal plasma and serum. Lancet. 1997;350: 485–487. 10.1016/S0140-6736(97)02174-0 PubMed DOI
Lo YM, Hjelm NM, Fidler C, Sargent IL, Murphy MF, Chamberlain PF, et al. Prenatal diagnosis of fetal RhD status by molecular analysis of maternal plasma. N Engl J Med. 1998;339: 1734–1738. 10.1056/NEJM199812103392402 PubMed DOI
Ng EK, Tsui NB, Lau TK, Leung TN, Chiu RW, Panesar NS, et al. mRNA of placental origin is readily detectable in maternal plasma. Proc Natl Acad Sci U S A. 2003;100: 4748–4753. 10.1073/pnas.0637450100 PubMed DOI PMC
Sedlackova L, Spacek M, Holler E, Imryskova Z, Hromadnikova I. Heat-shock protein expression in leukemia.Tumour Biol. 2011;32: 33–44. 10.1007/s13277-010-0088-7 PubMed DOI
Sedlackova L, Sosna A, Vavrincova P, Frýdl J, Guerriero V, Raynes DA, Hromadnikova I. Heat shock protein gene expression profile may differentiate between rheumatoid arthritis, osteoarthritis, and healthy controls. Scand J Rheumatol. 2011;40: 354–357. 10.3109/03009742.2011.552522 PubMed DOI
Thompson LP, Pence L, Pinkas G, Song H, Telugu BP. Placental Hypoxia During Early Pregnancy Causes Maternal Hypertension and Placental Insufficiency in the Hypoxic Guinea Pig Model. Biol Reprod. 2016. pii: biolreprod.116.142273. [Epub ahead of print] PubMed PMC
DiFederico E, Genbacev O, Fisher SJ. Preeclampsia is associated with widespread apoptosis of placental cytotrophoblasts within the uterine wall. Am J Pathol. 1999;155: 293–301. 10.1016/S0002-9440(10)65123-1 PubMed DOI PMC
Reddy A, Zhong XY, Rusterholz C, Hahn S, Holzgreve W, Redman CW, Sargent IL. The effect of labour and placental separation on the shedding of syncytiotrophoblast microparticles, cell-free DNA and mRNA in normal pregnancy and pre-eclampsia. Placenta. 2008;29: 942–949. 10.1016/j.placenta.2008.08.018 PubMed DOI
Whitley GS, Dash PR, Ayling LJ, Prefumo F, Thilaganathan B, Cartwright JE. Increased apoptosis in first trimester extravillous trophoblasts from pregnancies at higher risk of developing preeclampsia. Am J Pathol. 2007;170: 1903–1909. 10.2353/ajpath.2007.070006 PubMed DOI PMC
Mouillet JF, Chu T, Hubel CA, Nelson DM, Parks WT, Sadovsky Y. The levels of hypoxia-regulated microRNAs in plasma of pregnant women with fetal growth restriction. Placenta. 2010;31: 781–784. 10.1016/j.placenta.2010.07.001 PubMed DOI PMC
Mouillet JF, Chu T, Nelson DM, Mishima T, Sadovsky Y. MiR-205 silences MED1 in hypoxic primary human trophoblasts. FASEB J. 2010;24: 2030–2039. 10.1096/fj.09-149724 PubMed DOI PMC
Huppertz B. Oxygenation of the placenta and its role in pre-eclampsia. Pregnancy Hypertens. 2014;4: 244–245. PubMed