Maternal Obesity Affects Fetal Neurodevelopmental and Metabolic Gene Expression: A Pilot Study

One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying molecular mechanisms are poorly understood. We performed a global gene expression analysis of mid-trimester amniotic fluid cell-free fetal RNA i...

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Published inPloS one Vol. 9; no. 2; p. e88661
Main Authors Edlow, Andrea G., Vora, Neeta L., Hui, Lisa, Wick, Heather C., Cowan, Janet M., Bianchi, Diana W.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 18.02.2014
Public Library of Science (PLoS)
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Abstract One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying molecular mechanisms are poorly understood. We performed a global gene expression analysis of mid-trimester amniotic fluid cell-free fetal RNA in obese versus lean pregnant women. This prospective pilot study included eight obese (BMI≥30) and eight lean (BMI<25) women undergoing clinically indicated mid-trimester genetic amniocentesis. Subjects were matched for gestational age and fetal sex. Fetuses with abnormal karyotype or structural anomalies were excluded. Cell-free fetal RNA was extracted from amniotic fluid and hybridized to whole genome expression arrays. Genes significantly differentially regulated in 8/8 obese-lean pairs were identified using paired t-tests with the Benjamini-Hochberg correction (false discovery rate of <0.05). Biological interpretation was performed with Ingenuity Pathway Analysis and the BioGPS gene expression atlas. In fetuses of obese pregnant women, 205 genes were significantly differentially regulated. Apolipoprotein D, a gene highly expressed in the central nervous system and integral to lipid regulation, was the most up-regulated gene (9-fold). Apoptotic cell death was significantly down-regulated, particularly within nervous system pathways involving the cerebral cortex. Activation of the transcriptional regulators estrogen receptor, FOS, and STAT3 was predicted in fetuses of obese women, suggesting a pro-estrogenic, pro-inflammatory milieu. Maternal obesity affects fetal neurodevelopmental and metabolic gene expression as early as the second trimester. These findings may have implications for postnatal neurodevelopmental and metabolic abnormalities described in the offspring of obese women.
AbstractList Objective One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying molecular mechanisms are poorly understood. We performed a global gene expression analysis of mid-trimester amniotic fluid cell-free fetal RNA in obese versus lean pregnant women. Methods This prospective pilot study included eight obese (BMI[greater than or equal to]30) and eight lean (BMI<25) women undergoing clinically indicated mid-trimester genetic amniocentesis. Subjects were matched for gestational age and fetal sex. Fetuses with abnormal karyotype or structural anomalies were excluded. Cell-free fetal RNA was extracted from amniotic fluid and hybridized to whole genome expression arrays. Genes significantly differentially regulated in 8/8 obese-lean pairs were identified using paired t-tests with the Benjamini-Hochberg correction (false discovery rate of <0.05). Biological interpretation was performed with Ingenuity Pathway Analysis and the BioGPS gene expression atlas. Results In fetuses of obese pregnant women, 205 genes were significantly differentially regulated. Apolipoprotein D, a gene highly expressed in the central nervous system and integral to lipid regulation, was the most up-regulated gene (9-fold). Apoptotic cell death was significantly down-regulated, particularly within nervous system pathways involving the cerebral cortex. Activation of the transcriptional regulators estrogen receptor, FOS, and STAT3 was predicted in fetuses of obese women, suggesting a pro-estrogenic, pro-inflammatory milieu. Conclusion Maternal obesity affects fetal neurodevelopmental and metabolic gene expression as early as the second trimester. These findings may have implications for postnatal neurodevelopmental and metabolic abnormalities described in the offspring of obese women.
One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying molecular mechanisms are poorly understood. We performed a global gene expression analysis of mid-trimester amniotic fluid cell-free fetal RNA in obese versus lean pregnant women. This prospective pilot study included eight obese (BMI[greater than or equal to]30) and eight lean (BMI<25) women undergoing clinically indicated mid-trimester genetic amniocentesis. Subjects were matched for gestational age and fetal sex. Fetuses with abnormal karyotype or structural anomalies were excluded. Cell-free fetal RNA was extracted from amniotic fluid and hybridized to whole genome expression arrays. Genes significantly differentially regulated in 8/8 obese-lean pairs were identified using paired t-tests with the Benjamini-Hochberg correction (false discovery rate of <0.05). Biological interpretation was performed with Ingenuity Pathway Analysis and the BioGPS gene expression atlas. In fetuses of obese pregnant women, 205 genes were significantly differentially regulated. Apolipoprotein D, a gene highly expressed in the central nervous system and integral to lipid regulation, was the most up-regulated gene (9-fold). Apoptotic cell death was significantly down-regulated, particularly within nervous system pathways involving the cerebral cortex. Activation of the transcriptional regulators estrogen receptor, FOS, and STAT3 was predicted in fetuses of obese women, suggesting a pro-estrogenic, pro-inflammatory milieu. Maternal obesity affects fetal neurodevelopmental and metabolic gene expression as early as the second trimester. These findings may have implications for postnatal neurodevelopmental and metabolic abnormalities described in the offspring of obese women.
One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying molecular mechanisms are poorly understood. We performed a global gene expression analysis of mid-trimester amniotic fluid cell-free fetal RNA in obese versus lean pregnant women.OBJECTIVEOne in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying molecular mechanisms are poorly understood. We performed a global gene expression analysis of mid-trimester amniotic fluid cell-free fetal RNA in obese versus lean pregnant women.This prospective pilot study included eight obese (BMI≥30) and eight lean (BMI<25) women undergoing clinically indicated mid-trimester genetic amniocentesis. Subjects were matched for gestational age and fetal sex. Fetuses with abnormal karyotype or structural anomalies were excluded. Cell-free fetal RNA was extracted from amniotic fluid and hybridized to whole genome expression arrays. Genes significantly differentially regulated in 8/8 obese-lean pairs were identified using paired t-tests with the Benjamini-Hochberg correction (false discovery rate of <0.05). Biological interpretation was performed with Ingenuity Pathway Analysis and the BioGPS gene expression atlas.METHODSThis prospective pilot study included eight obese (BMI≥30) and eight lean (BMI<25) women undergoing clinically indicated mid-trimester genetic amniocentesis. Subjects were matched for gestational age and fetal sex. Fetuses with abnormal karyotype or structural anomalies were excluded. Cell-free fetal RNA was extracted from amniotic fluid and hybridized to whole genome expression arrays. Genes significantly differentially regulated in 8/8 obese-lean pairs were identified using paired t-tests with the Benjamini-Hochberg correction (false discovery rate of <0.05). Biological interpretation was performed with Ingenuity Pathway Analysis and the BioGPS gene expression atlas.In fetuses of obese pregnant women, 205 genes were significantly differentially regulated. Apolipoprotein D, a gene highly expressed in the central nervous system and integral to lipid regulation, was the most up-regulated gene (9-fold). Apoptotic cell death was significantly down-regulated, particularly within nervous system pathways involving the cerebral cortex. Activation of the transcriptional regulators estrogen receptor, FOS, and STAT3 was predicted in fetuses of obese women, suggesting a pro-estrogenic, pro-inflammatory milieu.RESULTSIn fetuses of obese pregnant women, 205 genes were significantly differentially regulated. Apolipoprotein D, a gene highly expressed in the central nervous system and integral to lipid regulation, was the most up-regulated gene (9-fold). Apoptotic cell death was significantly down-regulated, particularly within nervous system pathways involving the cerebral cortex. Activation of the transcriptional regulators estrogen receptor, FOS, and STAT3 was predicted in fetuses of obese women, suggesting a pro-estrogenic, pro-inflammatory milieu.Maternal obesity affects fetal neurodevelopmental and metabolic gene expression as early as the second trimester. These findings may have implications for postnatal neurodevelopmental and metabolic abnormalities described in the offspring of obese women.CONCLUSIONMaternal obesity affects fetal neurodevelopmental and metabolic gene expression as early as the second trimester. These findings may have implications for postnatal neurodevelopmental and metabolic abnormalities described in the offspring of obese women.
Objective One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying molecular mechanisms are poorly understood. We performed a global gene expression analysis of mid-trimester amniotic fluid cell-free fetal RNA in obese versus lean pregnant women. Methods This prospective pilot study included eight obese (BMI≥30) and eight lean (BMI<25) women undergoing clinically indicated mid-trimester genetic amniocentesis. Subjects were matched for gestational age and fetal sex. Fetuses with abnormal karyotype or structural anomalies were excluded. Cell-free fetal RNA was extracted from amniotic fluid and hybridized to whole genome expression arrays. Genes significantly differentially regulated in 8/8 obese-lean pairs were identified using paired t-tests with the Benjamini-Hochberg correction (false discovery rate of <0.05). Biological interpretation was performed with Ingenuity Pathway Analysis and the BioGPS gene expression atlas. Results In fetuses of obese pregnant women, 205 genes were significantly differentially regulated. Apolipoprotein D, a gene highly expressed in the central nervous system and integral to lipid regulation, was the most up-regulated gene (9-fold). Apoptotic cell death was significantly down-regulated, particularly within nervous system pathways involving the cerebral cortex. Activation of the transcriptional regulators estrogen receptor, FOS, and STAT3 was predicted in fetuses of obese women, suggesting a pro-estrogenic, pro-inflammatory milieu. Conclusion Maternal obesity affects fetal neurodevelopmental and metabolic gene expression as early as the second trimester. These findings may have implications for postnatal neurodevelopmental and metabolic abnormalities described in the offspring of obese women.
One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying molecular mechanisms are poorly understood. We performed a global gene expression analysis of mid-trimester amniotic fluid cell-free fetal RNA in obese versus lean pregnant women.This prospective pilot study included eight obese (BMI≥30) and eight lean (BMI<25) women undergoing clinically indicated mid-trimester genetic amniocentesis. Subjects were matched for gestational age and fetal sex. Fetuses with abnormal karyotype or structural anomalies were excluded. Cell-free fetal RNA was extracted from amniotic fluid and hybridized to whole genome expression arrays. Genes significantly differentially regulated in 8/8 obese-lean pairs were identified using paired t-tests with the Benjamini-Hochberg correction (false discovery rate of <0.05). Biological interpretation was performed with Ingenuity Pathway Analysis and the BioGPS gene expression atlas.In fetuses of obese pregnant women, 205 genes were significantly differentially regulated. Apolipoprotein D, a gene highly expressed in the central nervous system and integral to lipid regulation, was the most up-regulated gene (9-fold). Apoptotic cell death was significantly down-regulated, particularly within nervous system pathways involving the cerebral cortex. Activation of the transcriptional regulators estrogen receptor, FOS, and STAT3 was predicted in fetuses of obese women, suggesting a pro-estrogenic, pro-inflammatory milieu.Maternal obesity affects fetal neurodevelopmental and metabolic gene expression as early as the second trimester. These findings may have implications for postnatal neurodevelopmental and metabolic abnormalities described in the offspring of obese women.
One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying molecular mechanisms are poorly understood. We performed a global gene expression analysis of mid-trimester amniotic fluid cell-free fetal RNA in obese versus lean pregnant women. This prospective pilot study included eight obese (BMI≥30) and eight lean (BMI<25) women undergoing clinically indicated mid-trimester genetic amniocentesis. Subjects were matched for gestational age and fetal sex. Fetuses with abnormal karyotype or structural anomalies were excluded. Cell-free fetal RNA was extracted from amniotic fluid and hybridized to whole genome expression arrays. Genes significantly differentially regulated in 8/8 obese-lean pairs were identified using paired t-tests with the Benjamini-Hochberg correction (false discovery rate of <0.05). Biological interpretation was performed with Ingenuity Pathway Analysis and the BioGPS gene expression atlas. In fetuses of obese pregnant women, 205 genes were significantly differentially regulated. Apolipoprotein D, a gene highly expressed in the central nervous system and integral to lipid regulation, was the most up-regulated gene (9-fold). Apoptotic cell death was significantly down-regulated, particularly within nervous system pathways involving the cerebral cortex. Activation of the transcriptional regulators estrogen receptor, FOS, and STAT3 was predicted in fetuses of obese women, suggesting a pro-estrogenic, pro-inflammatory milieu. Maternal obesity affects fetal neurodevelopmental and metabolic gene expression as early as the second trimester. These findings may have implications for postnatal neurodevelopmental and metabolic abnormalities described in the offspring of obese women.
Objective One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying molecular mechanisms are poorly understood. We performed a global gene expression analysis of mid-trimester amniotic fluid cell-free fetal RNA in obese versus lean pregnant women. Methods This prospective pilot study included eight obese (BMI≥30) and eight lean (BMI<25) women undergoing clinically indicated mid-trimester genetic amniocentesis. Subjects were matched for gestational age and fetal sex. Fetuses with abnormal karyotype or structural anomalies were excluded. Cell-free fetal RNA was extracted from amniotic fluid and hybridized to whole genome expression arrays. Genes significantly differentially regulated in 8/8 obese-lean pairs were identified using paired t-tests with the Benjamini-Hochberg correction (false discovery rate of <0.05). Biological interpretation was performed with Ingenuity Pathway Analysis and the BioGPS gene expression atlas. Results In fetuses of obese pregnant women, 205 genes were significantly differentially regulated. Apolipoprotein D, a gene highly expressed in the central nervous system and integral to lipid regulation, was the most up-regulated gene (9-fold). Apoptotic cell death was significantly down-regulated, particularly within nervous system pathways involving the cerebral cortex. Activation of the transcriptional regulators estrogen receptor, FOS, and STAT3 was predicted in fetuses of obese women, suggesting a pro-estrogenic, pro-inflammatory milieu. Conclusion Maternal obesity affects fetal neurodevelopmental and metabolic gene expression as early as the second trimester. These findings may have implications for postnatal neurodevelopmental and metabolic abnormalities described in the offspring of obese women.
Audience Academic
Author Hui, Lisa
Cowan, Janet M.
Bianchi, Diana W.
Edlow, Andrea G.
Wick, Heather C.
Vora, Neeta L.
AuthorAffiliation 3 Department of Pathology and Laboratory Medicine, Tufts Medical Center, Boston, Massachusetts, United States of America
Virgen Macarena University Hospital, School of Medicine, University of Seville, Spain
2 Department of Computer Science, Tufts University, Medford, Massachusetts, United States of America
1 Mother Infant Research Institute, Tufts Medical Center, Boston, Massachusetts, United States of America
AuthorAffiliation_xml – name: 1 Mother Infant Research Institute, Tufts Medical Center, Boston, Massachusetts, United States of America
– name: 3 Department of Pathology and Laboratory Medicine, Tufts Medical Center, Boston, Massachusetts, United States of America
– name: Virgen Macarena University Hospital, School of Medicine, University of Seville, Spain
– name: 2 Department of Computer Science, Tufts University, Medford, Massachusetts, United States of America
Author_xml – sequence: 1
  givenname: Andrea G.
  surname: Edlow
  fullname: Edlow, Andrea G.
– sequence: 2
  givenname: Neeta L.
  surname: Vora
  fullname: Vora, Neeta L.
– sequence: 3
  givenname: Lisa
  surname: Hui
  fullname: Hui, Lisa
– sequence: 4
  givenname: Heather C.
  surname: Wick
  fullname: Wick, Heather C.
– sequence: 5
  givenname: Janet M.
  surname: Cowan
  fullname: Cowan, Janet M.
– sequence: 6
  givenname: Diana W.
  surname: Bianchi
  fullname: Bianchi, Diana W.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24558408$$D View this record in MEDLINE/PubMed
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Cites_doi 10.1093/humrep/deh117
10.1289/ehp.00108s3511
10.1093/humrep/deg320
10.1016/j.bbadis.2009.08.007
10.1016/j.ajog.2006.06.077
10.1007/s00439-012-1195-x
10.2202/1544-6115.1034
10.1038/sj.ijo.0803741
10.4049/jimmunol.1002971
10.1373/clinchem.2006.084350
10.1111/j.1464-5491.1994.tb00252.x
10.1152/ajpregu.00310.2010
10.1152/ajpcell.00385.2007
10.1179/1476830512Y.0000000035
10.1001/jama.2012.39
10.1159/000115355
10.1007/s00439-010-0923-3
10.1186/gb-2004-5-10-r80
10.1016/j.neuroscience.2009.04.073
10.1056/NEJMra0708473
10.1097/AOG.0b013e318293d70b
10.1542/peds.2004-1808
10.1093/clinchem/47.10.1867
10.1016/j.neulet.2009.03.038
10.1097/PDM.0b013e31815bcdb6
10.1017/S1368980007000596
10.1016/j.jmoldx.2011.05.008
10.1186/1475-2840-8-8
10.1038/oby.2007.621
10.1371/journal.pone.0005870
10.1136/jmg.2003.015784
10.1093/aje/kwk030
10.1007/s10995-012-0964-4
10.1194/jlr.M001206
10.1034/j.1600-0412.2003.00090.x
10.1016/j.nbd.2009.04.002
10.1097/AOG.0b013e31823d4150
10.1073/pnas.071056198
10.1046/j.1471-4159.2003.01866.x
10.1016/j.ijdevneu.2009.08.005
10.1111/j.2517-6161.1995.tb02031.x
10.1002/(SICI)1096-9861(19980622)396:1<39::AID-CNE4>3.0.CO;2-J
10.1038/ijo.2012.143
10.1073/pnas.0400782101
10.1007/s00404-005-0068-0
10.1002/pd.2850
10.1097/CCO.0b013e328331a7a4
10.1093/aje/kwm291
10.1038/sj.onc.1203551
10.1002/pd.2732
10.3945/ajcn.110.001057
10.1152/physrev.00007.2010
10.1373/clinchem.2006.076083
10.1002/uog.6117
10.1016/S0920-9964(01)00378-4
10.1073/pnas.0903909106
10.1096/fj.00-0530fje
10.1542/peds.2011-2583
10.1016/S0006-3223(02)01976-5
10.1016/j.bbadis.2012.04.005
10.1093/bioinformatics/btg227
10.1016/j.cell.2006.01.044
10.1016/j.nurx.2006.05.005
10.1001/jama.293.7.836
10.1111/j.1471-4159.2009.06031.x
10.1056/NEJM197104222841604
10.1186/gb-2009-10-11-r130
ContentType Journal Article
Copyright COPYRIGHT 2014 Public Library of Science
2014 Edlow et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2014 Edlow et al 2014 Edlow et al
Copyright_xml – notice: COPYRIGHT 2014 Public Library of Science
– notice: 2014 Edlow et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Competing Interests: The authors have declared that no competing interests exist.
Current address: Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, University of North Carolina-Chapel Hill, NC, United States of America
Current address: Department of Perinatal Medicine, Mercy Hospital for Women, Heidelberg, VIC, Australia
Conceived and designed the experiments: AGE NLV DWB. Performed the experiments: AGE NLV. Analyzed the data: AGE HCW DWB. Contributed reagents/materials/analysis tools: AGE NLV LH JMC DWB. Wrote the paper: AGE LH DWB. Revised the manuscript critically for important intellectual content: AGE NLV LH HCW JMC DWB.
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References R Romero (ref77) 2006; 195
SY Kim (ref2) 2007; 15
P Pavlidis (ref26) 2003; 19
RC Gentleman (ref33) 2004; 5
Y Benjamini (ref35) 1995; 57
NE Olson (ref78) 2006; 3
I Peter (ref29) 2008; 17
R Tanda (ref7) 2013; 17
PB Larrabee (ref13) 2005; 293
L Hui (ref31) 2013; 121
GJ Morton (ref64) 2010; 91
P Krakowiak (ref10) 2012; 129
DA Lawlor (ref6) 2007; 165
O Lapaire (ref30) 2007; 53
T Hirano (ref68) 2000; 19
C Wu (ref44) 2009; 10
SP Mahadik (ref50) 2002; 58
ref45
MP Patel (ref56) 2009; 21
S Vijayaraghavan (ref73) 1994; 79
ref42
MJ Heerwagen (ref75) 2010; 299
XY Zhong (ref19) 2006; 273
CL White (ref55) 2009; 35
AJ Blaschke (ref59) 1998; 396
SN Hinkle (ref11) 2012; 36
DK Slonim (ref15) 2009; 106
CJ Greenhill (ref67) 2011; 186
AH Clementi (ref70) 2009; 1792
JA Armitage (ref76) 2008; 36
YH Neggers (ref9) 2003; 82
JL Pennings (ref41) 2011; 31
W Min (ref66) 2009; 8
L Hui (ref32) 2013
WA Baker (ref72) 1994; 11
DW Bianchi (ref18) 2001; 47
RR Newbold (ref62) 2011; 94
T Kislinger (ref40) 2006; 125
FM Lun (ref20) 2007; 53
U Heikura (ref8) 2008; 167
J Kosacka (ref47) 2009; 162
X He (ref46) 2009; 455
EK Stachowiak (ref58) 2012; 16
ref37
ref36
D Rice (ref60) 2000; 108 Suppl 3
MD Niculescu (ref57) 2009; 27
CM Boney (ref4) 2005; 115
AG Edlow (ref25) 2012; 1822
R Gentleman (ref34) 2005; 4
LJ Massingham (ref27) 2011; 13
Z Liu (ref74) 2001; 15
ref38
G Perdomo (ref71) 2010; 51
E Rassart (ref43) 2000; 1482
PD Gluckman (ref3) 2008; 359
EA Thomas (ref51) 2001; 98
PS Crespo (ref5) 2007; 10
AI Su (ref39) 2004; 101
L Hui (ref14) 2012; 119
L Hui (ref17) 2012; 131
C Ordonez (ref52) 2006; 21
NE Hastings (ref65) 2007; 293
AL Herbst (ref61) 1971; 284
J Guibert (ref23) 2003; 18
WS Kim (ref54) 2009; 109
M Durchdewald (ref63) 2009; 24
KM Flegal (ref1) 2012; 307
A Rodriguez (ref12) 2008; 32
E Flori (ref22) 2004; 19
H Masuzaki (ref24) 2004; 41
EA Thomas (ref53) 2003; 54
K Koide (ref16) 2011; 129
SL Kirk (ref69) 2009; 4
JA Dietz (ref28) 2011; 31
MM Khan (ref48) 2003; 86
G Makrydimas (ref21) 2008; 32
KH Choi (ref49) 2009; 34
References_xml – volume: 19
  start-page: 723
  year: 2004
  ident: ref22
  article-title: Circulating cell-free fetal DNA in maternal serum appears to originate from cyto- and syncytio-trophoblastic cells. Case report
  publication-title: Hum Reprod
  doi: 10.1093/humrep/deh117
– ident: ref37
– volume: 108 Suppl 3
  start-page: 511
  year: 2000
  ident: ref60
  article-title: Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models
  publication-title: Environ Health Perspect
  doi: 10.1289/ehp.00108s3511
– volume: 18
  start-page: 1733
  year: 2003
  ident: ref23
  article-title: Kinetics of SRY gene appearance in maternal serum: detection by real time PCR in early pregnancy after assisted reproductive technique
  publication-title: Hum Reprod
  doi: 10.1093/humrep/deg320
– volume: 1792
  start-page: 1062
  year: 2009
  ident: ref70
  article-title: Loss of Kupffer cells in diet-induced obesity is associated with increased hepatic steatosis, STAT3 signaling, and further decreases in insulin signaling
  publication-title: Biochim Biophys Acta
  doi: 10.1016/j.bbadis.2009.08.007
– volume: 195
  start-page: 360
  year: 2006
  ident: ref77
  article-title: High-dimensional biology in obstetrics and gynecology: functional genomics in microarray studies
  publication-title: Am J Obstet Gynecol
  doi: 10.1016/j.ajog.2006.06.077
– volume: 131
  start-page: 1751
  year: 2012
  ident: ref17
  article-title: Novel neurodevelopmental information revealed in amniotic fluid supernatant transcripts from fetuses with trisomies 18 and 21
  publication-title: Hum Genet
  doi: 10.1007/s00439-012-1195-x
– volume: 4
  start-page: Article2
  year: 2005
  ident: ref34
  article-title: Reproducible research: a bioinformatics case study
  publication-title: Stat Appl Genet Mol Biol
  doi: 10.2202/1544-6115.1034
– volume: 32
  start-page: 550
  year: 2008
  ident: ref12
  article-title: Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts
  publication-title: Int J Obes (Lond)
  doi: 10.1038/sj.ijo.0803741
– volume: 186
  start-page: 1199
  year: 2011
  ident: ref67
  article-title: IL-6 trans-signaling modulates TLR4-dependent inflammatory responses via STAT3
  publication-title: J Immunol
  doi: 10.4049/jimmunol.1002971
– volume: 24
  start-page: 1451
  year: 2009
  ident: ref63
  article-title: The transcription factor Fos: a Janus-type regulator in health and disease
  publication-title: Histol Histopathol
– volume: 53
  start-page: 796
  year: 2007
  ident: ref20
  article-title: Epigenetic analysis of RASSF1A gene in cell-free DNA in amniotic fluid
  publication-title: Clin Chem
  doi: 10.1373/clinchem.2006.084350
– volume: 11
  start-page: 947
  year: 1994
  ident: ref72
  article-title: Apolipoprotein D gene polymorphism: a new genetic marker for type 2 diabetic subjects in Nauru and south India
  publication-title: Diabet Med
  doi: 10.1111/j.1464-5491.1994.tb00252.x
– volume: 299
  start-page: R711
  year: 2010
  ident: ref75
  article-title: Maternal obesity and fetal metabolic programming: a fertile epigenetic soil
  publication-title: Am J Physiol Regul Integr Comp Physiol
  doi: 10.1152/ajpregu.00310.2010
– volume: 293
  start-page: C1824
  year: 2007
  ident: ref65
  article-title: Atherosclerosis-prone hemodynamics differentially regulates endothelial and smooth muscle cell phenotypes and promotes pro-inflammatory priming
  publication-title: Am J Physiol Cell Physiol
  doi: 10.1152/ajpcell.00385.2007
– ident: ref36
– volume: 16
  start-page: 96
  year: 2012
  ident: ref58
  article-title: Maternal obesity affects gene expression and cellular development in fetal brains
  publication-title: Nutr Neurosci
  doi: 10.1179/1476830512Y.0000000035
– volume: 1482
  start-page: 185
  year: 2000
  ident: ref43
  article-title: Apolipoprotein D. Biochim Biophys Acta
– volume: 307
  start-page: 491
  year: 2012
  ident: ref1
  article-title: Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010
  publication-title: JAMA
  doi: 10.1001/jama.2012.39
– volume: 36
  start-page: 73
  year: 2008
  ident: ref76
  article-title: Developmental origins of obesity and the metabolic syndrome: the role of maternal obesity
  publication-title: Front Horm Res
  doi: 10.1159/000115355
– volume: 129
  start-page: 295
  year: 2011
  ident: ref16
  article-title: Transcriptomic analysis of cell-free fetal RNA suggests a specific molecular phenotype in trisomy 18
  publication-title: Hum Genet
  doi: 10.1007/s00439-010-0923-3
– volume: 5
  start-page: R80
  year: 2004
  ident: ref33
  article-title: Bioconductor: open software development for computational biology and bioinformatics
  publication-title: Genome Biol
  doi: 10.1186/gb-2004-5-10-r80
– volume: 162
  start-page: 282
  year: 2009
  ident: ref47
  article-title: Apolipoproteins D and E3 exert neurotrophic and synaptogenic effects in dorsal root ganglion cell cultures
  publication-title: Neuroscience
  doi: 10.1016/j.neuroscience.2009.04.073
– volume: 359
  start-page: 61
  year: 2008
  ident: ref3
  article-title: Effect of in utero and early-life conditions on adult health and disease
  publication-title: N Engl J Med
  doi: 10.1056/NEJMra0708473
– volume: 121
  start-page: 1248
  year: 2013
  ident: ref31
  article-title: Global gene expression analysis of term amniotic fluid cell-free fetal RNA
  publication-title: Obstet Gynecol
  doi: 10.1097/AOG.0b013e318293d70b
– volume: 79
  start-page: 568
  year: 1994
  ident: ref73
  article-title: Apolipoprotein-D polymorphism: a genetic marker for obesity and hyperinsulinemia
  publication-title: J Clin Endocrinol Metab
– volume: 115
  start-page: e290
  year: 2005
  ident: ref4
  article-title: Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus
  publication-title: Pediatrics
  doi: 10.1542/peds.2004-1808
– volume: 47
  start-page: 1867
  year: 2001
  ident: ref18
  article-title: Large amounts of cell-free fetal DNA are present in amniotic fluid
  publication-title: Clin Chem
  doi: 10.1093/clinchem/47.10.1867
– volume: 455
  start-page: 183
  year: 2009
  ident: ref46
  article-title: Apolipoprotein D modulates F2-isoprostane and 7-ketocholesterol formation and has a neuroprotective effect on organotypic hippocampal cultures after kainate-induced excitotoxic injury
  publication-title: Neurosci Lett
  doi: 10.1016/j.neulet.2009.03.038
– volume: 21
  start-page: 361
  year: 2006
  ident: ref52
  article-title: Apolipoprotein D expression in substantia nigra of Parkinson disease
  publication-title: Histol Histopathol
– volume: 17
  start-page: 185
  year: 2008
  ident: ref29
  article-title: Cell-free DNA fragmentation patterns in amniotic fluid identify genetic abnormalities and changes due to storage
  publication-title: Diagn Mol Pathol
  doi: 10.1097/PDM.0b013e31815bcdb6
– volume: 10
  start-page: 1121
  year: 2007
  ident: ref5
  article-title: Metabolic syndrome in childhood
  publication-title: Public Health Nutr
  doi: 10.1017/S1368980007000596
– volume: 13
  start-page: 565
  year: 2011
  ident: ref27
  article-title: Proof of concept study to assess fetal gene expression in amniotic fluid by nanoarray PCR
  publication-title: J Mol Diagn
  doi: 10.1016/j.jmoldx.2011.05.008
– volume: 8
  start-page: 8
  year: 2009
  ident: ref66
  article-title: The signal transduction pathway of PKC/NF-kappa B/c-fos may be involved in the influence of high glucose on the cardiomyocytes of neonatal rats
  publication-title: Cardiovasc Diabetol
  doi: 10.1186/1475-2840-8-8
– volume: 15
  start-page: 986
  year: 2007
  ident: ref2
  article-title: Trends in pre-pregnancy obesity in nine states, 1993–2003
  publication-title: Obesity (Silver Spring)
  doi: 10.1038/oby.2007.621
– volume: 4
  start-page: e5870
  year: 2009
  ident: ref69
  article-title: Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0005870
– volume: 41
  start-page: 289
  year: 2004
  ident: ref24
  article-title: Detection of cell free placental DNA in maternal plasma: direct evidence from three cases of confined placental mosaicism
  publication-title: J Med Genet
  doi: 10.1136/jmg.2003.015784
– volume: 165
  start-page: 418
  year: 2007
  ident: ref6
  article-title: Epidemiologic evidence for the fetal overnutrition hypothesis: findings from the mater-university study of pregnancy and its outcomes
  publication-title: Am J Epidemiol
  doi: 10.1093/aje/kwk030
– volume: 17
  start-page: 222
  year: 2013
  ident: ref7
  article-title: The Impact of Prepregnancy Obesity on Children's Cognitive Test Scores
  publication-title: Matern Child Health J
  doi: 10.1007/s10995-012-0964-4
– volume: 51
  start-page: 1298
  year: 2010
  ident: ref71
  article-title: A role of apolipoprotein D in triglyceride metabolism
  publication-title: J Lipid Res
  doi: 10.1194/jlr.M001206
– volume: 82
  start-page: 235
  year: 2003
  ident: ref9
  article-title: Maternal prepregnancy body mass index and psychomotor development in children
  publication-title: Acta Obstet Gynecol Scand
  doi: 10.1034/j.1600-0412.2003.00090.x
– volume: 35
  start-page: 3
  year: 2009
  ident: ref55
  article-title: Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: contributions of maternal diet
  publication-title: Neurobiol Dis
  doi: 10.1016/j.nbd.2009.04.002
– volume: 119
  start-page: 111
  year: 2012
  ident: ref14
  article-title: The amniotic fluid transcriptome: a source of novel information about human fetal development
  publication-title: Obstet Gynecol
  doi: 10.1097/AOG.0b013e31823d4150
– volume: 98
  start-page: 4066
  year: 2001
  ident: ref51
  article-title: Increased CNS levels of apolipoprotein D in schizophrenic and bipolar subjects: implications for the pathophysiology of psychiatric disorders
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.071056198
– volume: 86
  start-page: 1089
  year: 2003
  ident: ref48
  article-title: Antipsychotic drugs differentially modulate apolipoprotein D in rat brain
  publication-title: J Neurochem
  doi: 10.1046/j.1471-4159.2003.01866.x
– volume: 27
  start-page: 627
  year: 2009
  ident: ref57
  article-title: High fat diet-induced maternal obesity alters fetal hippocampal development
  publication-title: Int J Dev Neurosci
  doi: 10.1016/j.ijdevneu.2009.08.005
– ident: ref45
– volume: 57
  start-page: 289
  year: 1995
  ident: ref35
  article-title: Controlling the false discovery rate: a practical and powerful approach to multiple testing
  publication-title: J Roy Statist Soc Ser B (Methodological)
  doi: 10.1111/j.2517-6161.1995.tb02031.x
– volume: 34
  start-page: 450
  year: 2009
  ident: ref49
  article-title: Expression profiles of schizophrenia susceptibility genes during human prefrontal cortical development
  publication-title: J Psychiatry Neurosci
– volume: 396
  start-page: 39
  year: 1998
  ident: ref59
  article-title: Programmed cell death is a universal feature of embryonic and postnatal neuroproliferative regions throughout the central nervous system
  publication-title: J Comp Neurol
  doi: 10.1002/(SICI)1096-9861(19980622)396:1<39::AID-CNE4>3.0.CO;2-J
– volume: 36
  start-page: 1312
  year: 2012
  ident: ref11
  article-title: Associations between maternal prepregnancy body mass index and child neurodevelopment at 2 years of age
  publication-title: Int J Obes (Lond)
  doi: 10.1038/ijo.2012.143
– volume: 101
  start-page: 6062
  year: 2004
  ident: ref39
  article-title: A gene atlas of the mouse and human protein-encoding transcriptomes
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.0400782101
– volume: 273
  start-page: 221
  year: 2006
  ident: ref19
  article-title: Cell-free foetal DNA in maternal plasma does not appear to be derived from the rich pool of cell-free foetal DNA in amniotic fluid
  publication-title: Arch Gynecol Obstet
  doi: 10.1007/s00404-005-0068-0
– volume: 31
  start-page: 1153
  year: 2011
  ident: ref41
  article-title: Integrative data mining to identify novel candidate serum biomarkers for pre-eclampsia screening
  publication-title: Prenat Diagn
  doi: 10.1002/pd.2850
– volume: 21
  start-page: 516
  year: 2009
  ident: ref56
  article-title: Targeting the Bcl-2
  publication-title: Curr Opin Oncol
  doi: 10.1097/CCO.0b013e328331a7a4
– volume: 167
  start-page: 169
  year: 2008
  ident: ref8
  article-title: Variations in prenatal sociodemographic factors associated with intellectual disability: a study of the 20-year interval between two birth cohorts in northern Finland
  publication-title: Am J Epidemiol
  doi: 10.1093/aje/kwm291
– volume: 19
  start-page: 2548
  year: 2000
  ident: ref68
  article-title: Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors
  publication-title: Oncogene
  doi: 10.1038/sj.onc.1203551
– volume: 31
  start-page: 598
  year: 2011
  ident: ref28
  article-title: Comparison of extraction techniques for amniotic fluid supernatant demonstrates improved yield of cell-free fetal RNA
  publication-title: Prenat Diagn
  doi: 10.1002/pd.2732
– volume: 94
  start-page: 1939S
  year: 2011
  ident: ref62
  article-title: Developmental exposure to endocrine-disrupting chemicals programs for reproductive tract alterations and obesity later in life
  publication-title: Am J Clin Nutr
  doi: 10.3945/ajcn.110.001057
– volume: 91
  start-page: 389
  year: 2010
  ident: ref64
  article-title: Leptin and the central nervous system control of glucose metabolism
  publication-title: Physiol Rev
  doi: 10.1152/physrev.00007.2010
– ident: ref38
– volume: 53
  start-page: 405
  year: 2007
  ident: ref30
  article-title: Cell-free fetal DNA in amniotic fluid: unique fragmentation signatures in euploid and aneuploid fetuses
  publication-title: Clin Chem
  doi: 10.1373/clinchem.2006.076083
– volume: 32
  start-page: 594
  year: 2008
  ident: ref21
  article-title: Cell-free fetal DNA in celomic fluid
  publication-title: Ultrasound Obstet Gynecol
  doi: 10.1002/uog.6117
– year: 2013
  ident: ref32
  article-title: Global gene expression analysis of amniotic fluid cell-free RNA from recipient twins with twin-twin transfusion syndrome
  publication-title: Prenat Diagn
– volume: 58
  start-page: 55
  year: 2002
  ident: ref50
  article-title: Elevated plasma level of apolipoprotein D in schizophrenia and its treatment and outcome
  publication-title: Schizophr Res
  doi: 10.1016/S0920-9964(01)00378-4
– volume: 106
  start-page: 9425
  year: 2009
  ident: ref15
  article-title: Functional genomic analysis of amniotic fluid cell-free mRNA suggests that oxidative stress is significant in Down syndrome fetuses
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.0903909106
– ident: ref42
– volume: 15
  start-page: 1329
  year: 2001
  ident: ref74
  article-title: Apolipoprotein D interacts with the long-form leptin receptor: a hypothalamic function in the control of energy homeostasis
  publication-title: FASEB J
  doi: 10.1096/fj.00-0530fje
– volume: 129
  start-page: e1121
  year: 2012
  ident: ref10
  article-title: Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders
  publication-title: Pediatrics
  doi: 10.1542/peds.2011-2583
– volume: 54
  start-page: 136
  year: 2003
  ident: ref53
  article-title: Apolipoprotein D levels are elevated in prefrontal cortex of subjects with Alzheimer's disease: no relation to apolipoprotein E expression or genotype
  publication-title: Biol Psychiatry
  doi: 10.1016/S0006-3223(02)01976-5
– volume: 1822
  start-page: 1970
  year: 2012
  ident: ref25
  article-title: Tracking fetal development through molecular analysis of maternal biofluids
  publication-title: Biochim Biophys Acta
  doi: 10.1016/j.bbadis.2012.04.005
– volume: 19
  start-page: 1620
  year: 2003
  ident: ref26
  article-title: The effect of replication on gene expression microarray experiments
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btg227
– volume: 125
  start-page: 173
  year: 2006
  ident: ref40
  article-title: Global survey of organ and organelle protein expression in mouse: combined proteomic and transcriptomic profiling
  publication-title: Cell
  doi: 10.1016/j.cell.2006.01.044
– volume: 3
  start-page: 373
  year: 2006
  ident: ref78
  article-title: The microarray data analysis process: from raw data to biological significance
  publication-title: NeuroRx
  doi: 10.1016/j.nurx.2006.05.005
– volume: 293
  start-page: 836
  year: 2005
  ident: ref13
  article-title: Global gene expression analysis of the living human fetus using cell-free messenger RNA in amniotic fluid
  publication-title: JAMA
  doi: 10.1001/jama.293.7.836
– volume: 109
  start-page: 1053
  year: 2009
  ident: ref54
  article-title: Apolipoprotein-D expression is increased during development and maturation of the human prefrontal cortex
  publication-title: J Neurochem
  doi: 10.1111/j.1471-4159.2009.06031.x
– volume: 284
  start-page: 878
  year: 1971
  ident: ref61
  article-title: Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women
  publication-title: N Engl J Med
  doi: 10.1056/NEJM197104222841604
– volume: 10
  start-page: R130
  year: 2009
  ident: ref44
  article-title: BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources
  publication-title: Genome Biol
  doi: 10.1186/gb-2009-10-11-r130
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Snippet One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity. Underlying...
Objective One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity....
Objective One in three pregnant women in the United States is obese. Their offspring are at increased risk for neurodevelopmental and metabolic morbidity....
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SubjectTerms Abnormalities
Acids
Adult
Age
Amniocentesis
Amniotic fluid
Analysis
Apolipoproteins
Apoptosis
Biology
Body mass
Body mass index
Cell death
Central nervous system
Cerebral cortex
Cerebrum
Computational Biology
Epigenetics
Estrogens
Female
Fetus - embryology
Fetus - metabolism
Fetuses
Fos protein
Gene expression
Gene Expression Regulation, Developmental
Genes
Genomes
Genomics
Gestational age
Gynecology
Humans
Hybridization
Inflammation
Karyotypes
Laboratories
Medicine
Metabolic syndrome
Middle Aged
Molecular modelling
Morbidity
Mothers
Nervous System - embryology
Neurodevelopmental disorders
Obesity
Obstetrics
Offspring
Oligonucleotide Array Sequence Analysis
Organ Specificity
Pilot Projects
Pregnancy
Pregnancy Trimester, Second
Pregnant women
Regulators
Ribonucleic acid
RNA
Rodents
Signal transduction
Stat3 protein
Studies
Transcription activation
Womens health
Xenoestrogens
Young Adult
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Title Maternal Obesity Affects Fetal Neurodevelopmental and Metabolic Gene Expression: A Pilot Study
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Volume 9
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