Expression profile of C19MC microRNAs in placental tissue of patients with preterm prelabor rupture of membranes and spontaneous preterm birth

The aim of the study was to demonstrate that preterm birth (PTB) is associated with altered C19MC microRNA expression profile in placental tissues. Gene expression of 15 placental specific microRNAs (miR-512-5p, miR-515-5p, miR-516-5p, miR-517-5p, miR-518b, miR-518f-5p, miR-519a, miR-519d, miR-519e-5p, miR-520a-5p, miR-520h, miR-524-5p, miR-525-5p, miR-526a and miR-526b-5p) was compared between groups: 34 spontaneous PTB, 108 preterm prelabor rupture of membranes (PPROM) and 20 term in labor pregnancies. Correlation between variables including relative microRNA quantification in placental tissues and the gestational age at delivery, white blood cell (WBC) count at admission and serum levels of C-reactive protein at admission in patients with PPROM and PTB was determined. Expression profile of microRNAs was different between PPROM and term in labor pregnancies, PTB and term in labor pregnancies, and between gestational age-matched PPROM and PTB groups. When compared with term in labor pregnancies, while C19MC microRNAs showed a downregulation in PPROM pregnancies (miR-525-5p), in PTB pregnancies C19MC microRNAs were upregulated (miR-515-5p, miR-516-5p, miR-518b, miR-518f-5p, miR-519a, miR-519e-5p, miR-520a-5p, miR-520h, and miR-526b-5p) or showed a trend to upregulation (miR-519d and miR-526a). In comparison to PTB pregnancies, the PPROM group demonstrated a significant portion of downregulated C19MC microRNAs (miR-516-5p, miR-517-5p, miR-518b, miR-518f-5p, miR-519a, miR-519d, miR-519e-5p, miR-520a-5p, miR-520h, miR-525-5p, miR-526a and miR-526b-5p). In the group of PPROM pregnancies, a weak negative correlation between the gestational age at delivery and microRNA gene expression in placental tissue for all examined C19MC microRNAs was observed. PTB pregnancies showed a positive correlation (miR-512-5p, miR-515-5p, miR-519e-5p) or a trend to positive correlation (miR-516-5p, miR-518b, miR-520h) between particular C19MC microRNAs and maternal WBC count at admission. Our study demonstrates that upregulation of C19MC microRNAs is a characteristic phenomenon of PTB. PPROM pregnancies have a tendency to produce lower levels of miR-525-5p. All examined C19MC microRNAs displayed decreased expression with advancing gestational age in PPROM group.

[1]  B. Mercer.  Preterm premature rupture of the membranes. , 2003, Obstetrics and gynecology.

[2]  R. Wong,et al.  Role of microRNA-520h in 20(R)-ginsenoside-Rg3-mediated angiosuppression , 2015, Journal of ginseng research.

[3]  B. Jacobsson,et al.  Intraamniotic Inflammation in Women with Preterm Prelabor Rupture of Membranes , 2015, PloS one.

[4]  V. Novotna,et al.  Expression profile of C19MC microRNAs in placental tissue in pregnancy-related complications. , 2015, DNA and cell biology.

[5]  M. Elovitz,et al.  Can microRNA profiling in maternal blood identify women at risk for preterm birth? , 2015, American journal of obstetrics and gynecology.

[6]  A. Harel-Bellan,et al.  miRNA Expression in Control and FSHD Fetal Human Muscle Biopsies , 2015, PloS one.

[7]  A. Just,et al.  microRNA expression in the cervix during pregnancy is associated with length of gestation , 2015, Epigenetics.

[8]  C. Taner,et al.  Can platelet count and mean platelet volume during the first trimester of pregnancy predict preterm premature rupture of membranes? , 2015, The journal of obstetrics and gynaecology research.

[9]  Fateeva Lv,et al.  Serum β-human chorionic gonadotropin and interleukin-1 as diagnostic biomarkers for the premature rupture of membranes and chorioamnionitis. , 2014, Biomedical reports.

[10]  G. Saade,et al.  Expression of 8‐oxoguanine Glycosylase in Human Fetal Membranes , 2014, American journal of reproductive immunology.

[11]  Robert N. Taylor,et al.  Histological evidence of oxidative stress and premature senescence in preterm premature rupture of the human fetal membranes recapitulated in vitro. , 2014, The American journal of pathology.

[12]  Laura M. Heiser,et al.  Distinct cervical microRNA profiles are present in women destined to have a preterm birth. , 2014, American journal of obstetrics and gynecology.

[13]  Y. Sadovsky,et al.  Review: placenta-specific microRNAs in exosomes - good things come in nano-packages. , 2014, Placenta.

[14]  J. Kingdom,et al.  Preeclampsia Is Associated with Alterations in the p53-Pathway in Villous Trophoblast , 2014, PloS one.

[15]  M. Lappas,et al.  Circulating RNA coding genes regulating apoptosis in maternal blood in severe early onset fetal growth restriction and pre-eclampsia , 2013, Journal of Perinatology.

[16]  K. Yoshiura,et al.  Characterization of placenta‐specific microRNAs in fetal growth restriction pregnancy , 2013, Prenatal diagnosis.

[17]  E. Sheiner,et al.  Can leukocyte count during the first trimester of pregnancy predict later gestational complications? , 2013, Archives of Gynecology and Obstetrics.

[18]  O. Wolkenhauer,et al.  MicroRNA Cancer Regulation: Advanced Concepts, Bioinformatics and Systems Biology Tools , 2013 .

[19]  Weiwei Song,et al.  The emerging roles of placenta‐specific microRNAs in regulating trophoblast proliferation during the first trimester , 2012, The Australian & New Zealand journal of obstetrics & gynaecology.

[20]  F. Cetani,et al.  The microRNA cluster C19MC is deregulated in parathyroid tumours. , 2012, Journal of molecular endocrinology.

[21]  B. LaMarca.  Endothelial dysfunction. An important mediator in the pathophysiology of hypertension during pre-eclampsia. , 2012, Minerva ginecologica.

[22]  Massimo Negrini,et al.  In hepatocellular carcinoma miR‐519d is up‐regulated by p53 and DNA hypomethylation and targets CDKN1A/p21, PTEN, AKT3 and TIMP2 , 2012, The Journal of pathology.

[23]  J. Bullerdiek,et al.  The dark side of a success story: microRNAs of the C19MC cluster in human tumours , 2012, The Journal of pathology.

[24]  Xin Luo,et al.  The expression of pentraxin 3 and tumor necrosis factor-alpha is increased in preeclamptic placental tissue and maternal serum , 2012, Inflammation Research.

[25]  Gynecologists.  ACOG practice bulletin no. 127: Management of preterm labor. , 2012, Obstetrics and gynecology.

[26]  Lida Moghaddam Banaem,et al.  Maternal serum C‐reactive protein in early pregnancy and occurrence of preterm premature rupture of membranes and preterm birth , 2012, The journal of obstetrics and gynaecology research.

[27]  M. Roncalli,et al.  MicroRNA profiling of hepatocarcinogenesis identifies C19MC cluster as a novel prognostic biomarker in hepatocellular carcinoma , 2012, Liver international : official journal of the International Association for the Study of the Liver.

[28]  Robert N. Taylor,et al.  Short Fetal Leukocyte Telomere Length and Preterm Prelabor Rupture of the Membranes , 2012, PloS one.

[29]  B. Gruhn,et al.  MicroRNA expression profiles of trophoblastic cells. , 2011, Placenta.

[30]  B. Trink,et al.  Phospho-ΔNp63α is a key regulator of the cisplatin-induced microRNAome in cancer cells , 2011, Cell Death and Differentiation.

[31]  Carmen J. Marsit,et al.  miR-16 and miR-21 Expression in the Placenta Is Associated with Fetal Growth , 2011, PloS one.

[32]  N. Seki,et al.  Restoration of miR-517a expression induces cell apoptosis in bladder cancer cell lines. , 2011, Oncology reports.

[33]  I. Hromadnikova,et al.  Placental-specific microRNA in maternal circulation--identification of appropriate pregnancy-associated microRNAs with diagnostic potential. , 2011, Journal of reproductive immunology.

[34]  L. Kooistra,et al.  Maternal selenium status during early gestation and risk for preterm birth , 2011, Canadian Medical Association Journal.

[35]  D. Enquobahrie,et al.  Placental microRNA expression in pregnancies complicated by preeclampsia. , 2011, American journal of obstetrics and gynecology.

[36]  N. Chegini,et al.  Expression Profile of MicroRNAs and mRNAs in Human Placentas From Pregnancies Complicated by Preeclampsia and Preterm Labor , 2011, Reproductive Sciences.

[37]  K. Yokoyama,et al.  Early pregnancy blood lead levels and the risk of premature rupture of the membranes. , 2010, Reproductive toxicology.

[38]  L. Pastore,et al.  miR‐519d Overexpression Is Associated With Human Obesity , 2010, Obesity.

[39]  J. Keelan.  Pharmacological inhibition of inflammatory pathways for the prevention of preterm birth. , 2010, Journal of reproductive immunology.

[40]  M. Tosun,et al.  Maternal and umbilical serum levels of interleukin-6, interleukin-8, and tumor necrosis factor-α in normal pregnancies and in pregnancies complicated by preeclampsia , 2010, The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians.

[41]  J. Cavaille,et al.  The primate-specific microRNA gene cluster (C19MC) is imprinted in the placenta. , 2010, Human molecular genetics.

[42]  W. Andrews,et al.  Diagnosis and management of clinical chorioamnionitis. , 2010, Clinics in perinatology.

[43]  Jörn Bullerdiek,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 , 2010, PloS one.

[44]  Robert N. Taylor,et al.  Chorioamnionitis--a complex pathophysiologic syndrome. , 2010, Placenta.

[45]  M. Belickova,et al.  MicroRNA expression profiles in umbilical cord blood cell lineages. , 2010, Stem cells and development.

[46]  V. P. Collins,et al.  Frequent amplification of a chr19q13.41 microRNA polycistron in aggressive primitive neuroectodermal brain tumors. , 2009, Cancer cell.

[47]  T. Takizawa,et al.  Human Villous Trophoblasts Express and Secrete Placenta-Specific MicroRNAs into Maternal Circulation via Exosomes1 , 2009, Biology of reproduction.

[48]  Junli Zhao,et al.  Differential expression of microRNAs in the placentae of Chinese patients with severe pre-eclampsia , 2009, Clinical chemistry and laboratory medicine.

[49]  T. Han,et al.  Differential expression profile of microRNAs in human placentas from preeclamptic pregnancies vs normal pregnancies. , 2009, American journal of obstetrics and gynecology.

[50]  J. Cavaille,et al.  C19MC microRNAs are processed from introns of large Pol-II, non-protein-coding transcripts , 2009, Nucleic acids research.

[51]  S. Drăghici,et al.  Expression patterns of microRNAs in the chorioamniotic membranes: a role for microRNAs in human pregnancy and parturition , 2009, The Journal of pathology.

[52]  G. Mor.  Inflammation and Pregnancy , 2008, Annals of the New York Academy of Sciences.

[53]  Wenbin Ye,et al.  The Effect of Central Loops in miRNA:MRE Duplexes on the Efficiency of miRNA-Mediated Gene Regulation , 2008, PloS one.

[54]  Saroj Saigal,et al.  An overview of mortality and sequelae of preterm birth from infancy to adulthood , 2008, The Lancet.

[55]  Roberto Romero,et al.  Epidemiology and causes of preterm birth , 2008, The Lancet.

[56]  François Goffinet,et al.  Prevention of preterm delivery. , 2007, The New England journal of medicine.

[57]  F. Lee,et al.  Low maternal serum levels of pregnancy-associated plasma protein-A during the first trimester are associated with subsequent preterm delivery with preterm premature rupture of membranes. , 2007, Taiwanese journal of obstetrics & gynecology.

[58]  S. Drăghici,et al.  Differential expression of microRNAs with progression of gestation and inflammation in the human chorioamniotic membranes. , 2007, American journal of obstetrics and gynecology.

[59]  Yu Liang,et al.  BMC Genomics , 2007 .

[60]  S. Drăghici,et al.  BASIC SCIENCE: OBSTETRICS , 2022 .

[61]  Tsuyoshi Saito,et al.  Proteomic analysis of mechanisms of hypoxia-induced apoptosis in trophoblastic cells , 2006, International journal of medical sciences.

[62]  R. Romero,et al.  The preterm parturition syndrome , 2006, BJOG : an international journal of obstetrics and gynaecology.

[63]  Hyun Joon Kim,et al.  Altered gene expression of caspase-10, death receptor-3 and IGFBP-3 in preeclamptic placentas. , 2006, Molecules and cells.

[64]  Mark Schluchter,et al.  Chronic conditions, functional limitations, and special health care needs of school-aged children born with extremely low-birth-weight in the 1990s. , 2005, JAMA.

[65]  N. Uldbjerg,et al.  Preterm delivery , 2005, Acta obstetricia et gynecologica Scandinavica.

[66]  H. Simhan,et al.  Preterm premature rupture of membranes: diagnosis, evaluation and management strategies , 2005, BJOG : an international journal of obstetrics and gynaecology.

[67]  Stavros Petrou,et al.  The economic consequences of preterm birth duringthe first 10 years of life , 2005, BJOG : an international journal of obstetrics and gynaecology.

[68]  A. LaCroix,et al.  Risk Factors Associated with Acute Pyelonephritis in Healthy Women , 2005, Annals of Internal Medicine.

[69]  F. Menacker,et al.  Infant mortality statistics from the 2002 period: linked birth/infant death data set. , 2004, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[70]  T. Artimani.  VAGINAL FLUID HCG LEVELS FOR DETECTING PREMATURE RUPTURE OF MEMBRANES , 2004 .

[71]  Jane Henderson,et al.  The impact of preterm birth on hospital inpatient admissions and costs during the first 5 years of life. , 2003, Pediatrics.

[72]  L. Doyle,et al.  Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. , 2003, JAMA.

[73]  A. Bhutta,et al.  Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. , 2002, JAMA.

[74]  F. Speleman,et al.  Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes , 2002, Genome Biology.

[75]  H. Silver,et al.  Etiology and epidemiology of preterm premature rupture of the membranes. , 2001, Clinics in perinatology.

[76]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[77]  C. Lockwood,et al.  Plasma levels of thrombin-antithrombin complexes predict preterm premature rupture of the fetal membranes. , 2001 .

[78]  R. Wapner,et al.  Does transvaginal ultrasound of the cervix predict preterm premature rupture of membranes in a high‐risk population? , 2001, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[79]  J. Krieger,et al.  AMNIOTIC FLUID INTERLEUKIN‐6 AND PRETERM DELIVERY: A REVIEW , 2000, Obstetrics and gynecology.

[80]  J. Hauth,et al.  Intrauterine infection and preterm delivery. , 2000, The New England journal of medicine.

[81]  A. Fanaroff,et al.  Outcomes of children of extremely low birthweight and gestational age in the 1990s. , 2000, Seminars in neonatology : SN.

[82]  A. Hartikainen,et al.  Evaluation of a rapid strip test for insulin-like growth factor binding protein-1 in the diagnosis of ruptured fetal membranes. , 1996, Clinica chimica acta; international journal of clinical chemistry.

[83]  S. Kenyon,et al.  Preterm premature rupture of membranes. , 2012, Archivos argentinos de pediatria.

[84]  R. Romero,et al.  Risk factors for the development of preterm premature rupture of the membranes after arrest of preterm labor. , 1995, American journal of obstetrics and gynecology.

[85]  R. Woolson,et al.  Risks for premature rupture of amniotic membranes. , 1993, International journal of epidemiology.

[86]  E. Lieberman,et al.  Cigarettes, coffee, and preterm premature rupture of the membranes. , 1993, American journal of epidemiology.

[87]  J. Iams,et al.  Etiology of preterm premature rupture of membranes. , 1992, Obstetrics and gynecology clinics of North America.

[88]  S. Gabbe,et al.  Risk Factors for Preterm Premature Rupture of the Fetal Membranes , 1990, American journal of perinatology.

[89]  M. Swain,et al.  Vaginal pH: A marker of preterm premature rupture of the membranes , 1989, Obstetrics and gynecology.

[90]  A. Sarandakou,et al.  Vaginal fluid prolactin: a reliable marker for the diagnosis of prematurely ruptured membranes. Comparison with vaginal fluid alpha-fetoprotein and placental lactogen. , 1989, European journal of obstetrics, gynecology, and reproductive biology.

[91]  M. Pupkin,et al.  Etiology of Preterm Premature Rupture of the Membranes , 1986, Clinical obstetrics and gynecology.

[92]  M C McCormick,et al.  The contribution of low birth weight to infant mortality and childhood morbidity. , 1985, The New England journal of medicine.

[93]  R. Naeye,et al.  CAUSES AND CONSEQUENCES OF PREMATURE RUPTURE OF FETAL MEMBRANES , 1980, The Lancet.

[94]  O. Itelson,et al.  [Premature rupture of fetal membranes]. , 1969, Harefuah.

[95]  S. Callender,et al.  Effect of corticosteroids and gluten-free diet on absorption of iron inidiopathic steatorrhoea and coeliac disease. , 1960, Lancet.

[96]  S. Cavkaytar,et al.  Placental apoptosis in preeclampsia, intrauterine growth retardation, and HELLP syndrome: an immunohistochemical study with caspase-3 and bcl-2. , 2013, Clinical and experimental obstetrics & gynecology.

[97]  O. Wolkenhauer,et al.  MicroRNA Cancer Regulation , 2013, Advances in Experimental Medicine and Biology.

[98]  J. Martin,et al.  Births: final data for 2009. , 2011, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[99]  Setting Oxfordshire,et al.  The economic consequences of preterm birth during the first 10 years of life , 2005 .

[100]  S. Fujimoto,et al.  Rapid diagnosis of premature rupture of membranes using a new kit employing anti-AFP monoclonal antibody , 2004, Archives of Gynecology and Obstetrics.

[101]  A. Fanaroff,et al.  Outcomes of children of extremely low birthweight and gestational age in the 1990's. , 1999, Early human development.

[102]  M. Hannah,et al.  Fetal Fibronectin as a Predictor of Preterm Birth: An Overview , 1998, American journal of perinatology.

[103]  S. Fujimoto,et al.  Diagnosis of preterm premature rupture of the membranes using a newly developed AFP monoclonal antibody test kit. , 1995, European journal of obstetrics, gynecology, and reproductive biology.

[104]  G. Meeks.  Management of premature rupture of membranes. , 1982, Journal of the Mississippi State Medical Association.

[105]  A. Lembet.  Premature rupture of the membranes. , 1979, British medical journal.