Sex differences in gene regulatory networks during mid-gestational brain development

dc.contributorSistema FMUSP-HC: Faculdade de Medicina da Universidade de São Paulo (FMUSP) e Hospital das Clínicas da FMUSP
dc.contributor.authorTOLEDO, Victor Hugo Calegari de
dc.contributor.authorFELTRIN, Arthur Sant'Anna
dc.contributor.authorBARBOSA, Andre Rocha
dc.contributor.authorTAHIRA, Ana Carolina
dc.contributor.authorBRENTANI, Helena
dc.date.accessioned2022-10-26T14:35:48Z
dc.date.available2022-10-26T14:35:48Z
dc.date.issued2022
dc.description.abstractNeurodevetopmental disorders differ considerably between males and females, and fetal brain development is one of the most critical periods to determine risk for these disorders. Transcriptomic studies comparing male and female fetal brain have demonstrated that the highest difference in gene expression occurs in sex chromosomes, but several autossomal genes also demonstrate a slight difference that has not been yet explored. In order to investigate biological pathways underlying fetal brain sex differences, we applied medicine network principles using integrative methods such as co-expression networks (CEMiTool) and regulatory networks (netZoo). The pattern of gene expression from genes in the same pathway tend to reflect biologically relevant phenomena. In this study, network analysis of fetal brain expression reveals regulatory differences between males and females. Integrating two different bioinformatics tools, our results suggest that biological processes such as cell cycle, cell differentiation, energy metabolism and extracellular matrix organization are consistently sex-biased. MSET analysis demonstrates that these differences are relevant to neurodevelopmental disorders, including autism.eng
dc.description.indexPubMedeng
dc.identifier.citationFRONTIERS IN HUMAN NEUROSCIENCE, v.16, article ID 955607, 21p, 2022
dc.identifier.doi10.3389/fnhum.2022.955607
dc.identifier.issn1662-5161
dc.identifier.urihttps://observatorio.fm.usp.br/handle/OPI/49354
dc.language.isoeng
dc.publisherFRONTIERS MEDIA SAeng
dc.relation.ispartofFrontiers in Human Neuroscience
dc.rightsopenAccesseng
dc.rights.holderCopyright FRONTIERS MEDIA SAeng
dc.subjectneurodevelopmental disorderseng
dc.subjectsex differenceseng
dc.subjectfetal brain developmenteng
dc.subjectgene regulatory networkseng
dc.subjectsystems biologyeng
dc.subjectautism spectrum disorder (ASD)eng
dc.subject.othertranscription factoreng
dc.subject.otherexpressioneng
dc.subject.othercancereng
dc.subject.otherdifferentiationeng
dc.subject.othercellseng
dc.subject.otherneurogenesiseng
dc.subject.otherphosphorylationeng
dc.subject.othermitochondriaeng
dc.subject.otherarchitectureeng
dc.subject.othermetabolismeng
dc.subject.wosNeuroscienceseng
dc.subject.wosPsychologyeng
dc.titleSex differences in gene regulatory networks during mid-gestational brain developmenteng
dc.typearticleeng
dc.type.categoryoriginal articleeng
dc.type.versionpublishedVersioneng
dspace.entity.typePublication
hcfmusp.affiliation.countryEstados Unidos
hcfmusp.affiliation.countryisous
hcfmusp.author.externalFELTRIN, Arthur Sant'Anna:Univ Fed ABC, Ctr Matemat Comp & Cognicao, Santo Andre, Brazil
hcfmusp.author.externalBARBOSA, Andre Rocha:Lieber Inst Brain Dev, Baltimore, MD USA
hcfmusp.author.externalTAHIRA, Ana Carolina:Inst Butantan, Lab Expressao Genica, Dept Parasitol, Sao Paulo, Brazil
hcfmusp.citation.scopus1
hcfmusp.contributor.author-fmusphcVICTOR HUGO CALEGARI DE TOLEDO
hcfmusp.contributor.author-fmusphcHELENA PAULA BRENTANI
hcfmusp.description.articlenumber955607
hcfmusp.description.volume16
hcfmusp.origemWOS
hcfmusp.origem.pubmed36061507
hcfmusp.origem.scopus2-s2.0-85137186549
hcfmusp.origem.wosWOS:000847942200001
hcfmusp.publisher.cityLAUSANNEeng
hcfmusp.publisher.countrySWITZERLANDeng
hcfmusp.relation.referenceAbe H, 2012, P NATL ACAD SCI USA, V109, P8734, DOI 10.1073/pnas.1206418109eng
hcfmusp.relation.referenceAddis R, 2014, BIOL SEX DIFFER, V5, DOI 10.1186/s13293-014-0018-2eng
hcfmusp.relation.referenceAlberini CM, 2009, PHYSIOL REV, V89, P121, DOI 10.1152/physrev.00017.2008eng
hcfmusp.relation.referenceArber S, 2000, CELL, V101, P485, DOI 10.1016/S0092-8674(00)80859-4eng
hcfmusp.relation.referenceAscenzi M, 2017, DEV NEUROBIOL, V77, P1023, DOI 10.1002/dneu.22495eng
hcfmusp.relation.referenceAuger AP, 2003, J NEUROENDOCRINOL, V15, P622, DOI 10.1046/j.1365-2826.2003.01041.xeng
hcfmusp.relation.referenceBale TL, 2016, DIALOGUES CLIN NEURO, V18, P459eng
hcfmusp.relation.referenceBarber MJ, 2007, PHYS REV E, V76, DOI 10.1103/PhysRevE.76.066102eng
hcfmusp.relation.referenceBehar TN, 1996, J NEUROSCI, V16, P1808eng
hcfmusp.relation.referenceBenatti P, 2016, ONCOTARGET, V7, P1633, DOI 10.18632/oncotarget.6453eng
hcfmusp.relation.referenceBorras C, 2003, FREE RADICAL BIO MED, V34, P546, DOI 10.1016/S0891-5849(02)01356-4eng
hcfmusp.relation.referenceKummer KK, 2021, CYTOKINE, V144, DOI 10.1016/j.cyto.2021.155582eng
hcfmusp.relation.referenceLam M, 2019, NAT GENET, V51, P1670, DOI 10.1038/s41588-019-0512-xeng
hcfmusp.relation.referenceLandeira BS, 2018, CEREB CORTEX, V28, P538, DOI 10.1093/cercor/bhw387eng
hcfmusp.relation.referenceLangfelder P, 2008, BMC BIOINFORMATICS, V9, DOI 10.1186/1471-2105-9-559eng
hcfmusp.relation.referenceLarsen KB, 2010, J HISTOCHEM CYTOCHEM, V58, P669, DOI 10.1369/jhc.2010.955757eng
hcfmusp.relation.referenceLee PH, 2019, CELL, V179, P1469, DOI 10.1016/j.cell.2019.11.020eng
hcfmusp.relation.referenceLiberzon A, 2015, CELL SYST, V1, P417, DOI 10.1016/j.cels.2015.12.004eng
hcfmusp.relation.referenceLoke H, 2015, INT J BIOCHEM CELL B, V65, P139, DOI 10.1016/j.biocel.2015.05.024eng
hcfmusp.relation.referenceLong KTRER, 2022, FRONT CELL NEUROSCI, V15, DOI 10.3389/fncel.2021.804649eng
hcfmusp.relation.referenceLopes-Ramos CM, 2021, CANCER RES, V81, P5401, DOI 10.1158/0008-5472.CAN-21-0730eng
hcfmusp.relation.referenceO'Brien H.E., 2018, FIGSHARE FILESET, DOI [10.6084/m9.figshare.6881825, DOI 10.6084/M9.FIGSHARE.6881825]eng
hcfmusp.relation.referenceLopes-Ramos CM, 2020, CELL REP, V31, DOI 10.1016/j.celrep.2020.107795eng
hcfmusp.relation.referenceLopes-Ramos CM, 2018, CANCER RES, V78, P5538, DOI 10.1158/0008-5472.CAN-18-0454eng
hcfmusp.relation.referenceLove MI, 2014, GENOME BIOL, V15, DOI 10.1186/s13059-014-0550-8eng
hcfmusp.relation.referenceMahler N, 2017, PLOS GENET, V13, DOI 10.1371/journal.pgen.1006402eng
hcfmusp.relation.referenceMarchetto MC, 2017, MOL PSYCHIATR, V22, P820, DOI 10.1038/mp.2016.95eng
hcfmusp.relation.referenceMaschietto M, 2017, SCI REP-UK, V7, DOI 10.1038/srep44547eng
hcfmusp.relation.referenceMay T, 2019, CURR OPIN NEUROL, V32, P622, DOI 10.1097/WCO.0000000000000714eng
hcfmusp.relation.referenceMayes J S, 2004, Obes Rev, V5, P197, DOI 10.1111/j.1467-789X.2004.00152.xeng
hcfmusp.relation.referenceMcCarthy MM, 2016, PHILOS T R SOC B, V371, DOI 10.1098/rstb.2015.0106eng
hcfmusp.relation.referenceMcrae JF, 2017, NATURE, V542, P433, DOI 10.1038/nature21062eng
hcfmusp.relation.referenceO'Brien HE, 2018, GENOME BIOL, V19, DOI 10.1186/s13059-018-1567-1eng
hcfmusp.relation.referenceMichoel T, 2009, BMC SYST BIOL, V3, DOI 10.1186/1752-0509-3-49eng
hcfmusp.relation.referenceMiranda A, 2018, BRAIN BEHAV, V8, DOI 10.1002/brb3.920eng
hcfmusp.relation.referenceMitchell AM, 2017, BRAIN BEHAV IMMUN, V60, P32, DOI 10.1016/j.bbi.2016.06.015eng
hcfmusp.relation.referenceNakashima A, 2008, MOL CELL BIOL, V28, P4080, DOI 10.1128/MCB.02168-07eng
hcfmusp.relation.referenceNayernia Z, 2014, ANTIOXID REDOX SIGN, V20, P2815, DOI 10.1089/ars.2013.5703eng
hcfmusp.relation.referenceOCKNER RK, 1979, J CLIN INVEST, V64, P172, DOI 10.1172/JCI109437eng
hcfmusp.relation.referenceOjeda J, 2019, FRONT SYNAPTIC NEURO, V11, DOI 10.3389/fnsyn.2019.00033eng
hcfmusp.relation.referenceOliva M, 2020, SCIENCE, V369, P1331, DOI 10.1126/science.aba3066eng
hcfmusp.relation.referenceOrth M, 2012, CHOLESTEROL, DOI 10.1155/2012/292598eng
hcfmusp.relation.referencePadi M, 2018, NPJ SYST BIOL APPL, V4, DOI 10.1038/s41540-018-0052-5eng
hcfmusp.relation.referenceParry DA, 2013, AM J HUM GENET, V93, P1135, DOI 10.1016/j.ajhg.2013.10.027eng
hcfmusp.relation.referencePaulsen BD, 2012, CELL TRANSPLANT, V21, P1547, DOI 10.3727/096368911X600957eng
hcfmusp.relation.referencePlatig J, 2016, PLOS COMPUT BIOL, V12, DOI 10.1371/journal.pcbi.1005033eng
hcfmusp.relation.referenceShi L, 2016, SCI REP-UK, V6, DOI 10.1038/srep21181eng
hcfmusp.relation.referencePolioudakis D, 2019, NEURON, V103, P785, DOI 10.1016/j.neuron.2019.06.011eng
hcfmusp.relation.referenceRAY PF, 1995, J REPROD FERTIL, V104, P165eng
hcfmusp.relation.referenceReczek CR, 2017, ANNU REV CANC BIOL, V1, P79, DOI 10.1146/annurev-cancerbio-041916-065808eng
hcfmusp.relation.referenceReick M, 2001, SCIENCE, V293, P506, DOI 10.1126/science.1060699eng
hcfmusp.relation.referenceReinius B, 2009, MOL PSYCHIATR, V14, P988, DOI 10.1038/mp.2009.79eng
hcfmusp.relation.referenceRitchie ME, 2015, NUCLEIC ACIDS RES, V43, DOI 10.1093/nar/gkv007eng
hcfmusp.relation.referenceRitchie SJ, 2018, CEREB CORTEX, V28, P2959, DOI 10.1093/cercor/bhy109eng
hcfmusp.relation.referenceRodic S, 2018, INT J CANCER, V142, P440, DOI 10.1002/ijc.31069eng
hcfmusp.relation.referenceRubin JB, 2020, BIOL SEX DIFFER, V11, DOI 10.1186/s13293-020-00291-xeng
hcfmusp.relation.referenceRusso PST, 2018, BMC BIOINFORMATICS, V19, DOI 10.1186/s12859-018-2053-1eng
hcfmusp.relation.referenceSilaidos C, 2018, BIOL SEX DIFFER, V9, DOI 10.1186/s13293-018-0193-7eng
hcfmusp.relation.referenceSaito K, 2009, P NATL ACAD SCI USA, V106, P8350, DOI 10.1073/pnas.0903541106eng
hcfmusp.relation.referenceSanders SJ, 2015, NEURON, V87, P1215, DOI 10.1016/j.neuron.2015.09.016eng
hcfmusp.relation.referenceSantos-Terra J, 2021, INT J DEV NEUROSCI, V81, P545, DOI 10.1002/jdn.10141eng
hcfmusp.relation.referenceSementchenko VI, 2000, ONCOGENE, V19, P6533, DOI 10.1038/sj.onc.1204034eng
hcfmusp.relation.referenceShanware NP, 2013, ANNU REV PHARMACOL, V53, P89, DOI 10.1146/annurev-pharmtox-010611-134717eng
hcfmusp.relation.referenceSimoes SN, 2015, BMC BIOINFORMATICS, V16, DOI 10.1186/1471-2105-16-S19-S9eng
hcfmusp.relation.referenceSkinner MK, 2010, DIFFERENTIATION, V80, P1, DOI 10.1016/j.diff.2010.02.003eng
hcfmusp.relation.referenceSmedley D, 2009, BMC GENOMICS, V10, DOI 10.1186/1471-2164-10-22eng
hcfmusp.relation.referenceSokpor G, 2022, FRONT NEUROSCI-SWITZ, V16, DOI 10.3389/fnins.2022.824802eng
hcfmusp.relation.referenceSonawane AR, 2017, CELL REP, V21, P1077, DOI 10.1016/j.celrep.2017.10.001eng
hcfmusp.relation.referenceStahl EA, 2019, NAT GENET, V51, P793, DOI 10.1038/s41588-019-0397-8eng
hcfmusp.relation.referenceStark MJ, 2011, PLACENTA, V32, P865, DOI 10.1016/j.placenta.2011.08.010eng
hcfmusp.relation.referenceSubramanian A, 2005, P NATL ACAD SCI USA, V102, P15545, DOI 10.1073/pnas.0506580102eng
hcfmusp.relation.referenceBroere-Brown ZA, 2016, BIOL SEX DIFFER, V7, DOI 10.1186/s13293-016-0119-1eng
hcfmusp.relation.referenceSun Y, 2001, CELL, V104, P365, DOI 10.1016/S0092-8674(01)00224-0eng
hcfmusp.relation.referenceSupek F, 2011, PLOS ONE, V6, DOI 10.1371/journal.pone.0021800eng
hcfmusp.relation.referenceSzklarczyk D, 2019, NUCLEIC ACIDS RES, V47, pD607, DOI 10.1093/nar/gky1131eng
hcfmusp.relation.referenceTahira AC, 2019, AM J MED GENET B, V180, P390, DOI 10.1002/ajmg.b.32704eng
hcfmusp.relation.referenceTaverna E, 2014, ANNU REV CELL DEV BI, V30, P465, DOI 10.1146/annurev-cellbio-101011-155801eng
hcfmusp.relation.referenceUhl M, 2022, FRONT MOL NEUROSCI, V15, DOI 10.3389/fnmol.2022.818390eng
hcfmusp.relation.referenceVeenstra TD, 2021, PROTEOMICS, V21, DOI 10.1002/pmic.202000235eng
hcfmusp.relation.referenceVerdin H, 2014, ORPHANET J RARE DIS, V9, DOI 10.1186/1750-1172-9-26eng
hcfmusp.relation.referenceWeirauch MT, 2014, CELL, V158, P1431, DOI 10.1016/j.cell.2014.08.009eng
hcfmusp.relation.referenceWerling DM, 2016, NAT COMMUN, V7, DOI 10.1038/ncomms10717eng
hcfmusp.relation.referenceBurke KJ, 2019, FRONT CELL NEUROSCI, V13, DOI 10.3389/fncel.2019.00221eng
hcfmusp.relation.referenceYang ZF, 2014, MOL CELL BIOL, V34, P3194, DOI 10.1128/MCB.00492-12eng
hcfmusp.relation.referenceYokogawa T, 2000, J BIOL CHEM, V275, P19913, DOI 10.1074/jbc.M908473199eng
hcfmusp.relation.referenceYu GC, 2012, OMICS, V16, P284, DOI 10.1089/omi.2011.0118eng
hcfmusp.relation.referenceZhang Y, 2002, J BIOL CHEM, V277, P28065, DOI 10.1074/jbc.C100767200eng
hcfmusp.relation.referenceZiats MN, 2013, MOL AUTISM, V4, DOI 10.1186/2040-2392-4-10eng
hcfmusp.relation.referenceCai CM, 2007, MOL ENDOCRINOL, V21, P1835, DOI 10.1210/me.2006-0480eng
hcfmusp.relation.referenceCardinale DA, 2018, FRONT PHYSIOL, V9, DOI 10.3389/fphys.2018.01133eng
hcfmusp.relation.referenceClifton VL, 2010, GROWTH HORM IGF RES, V20, P39, DOI 10.1016/j.ghir.2009.07.004eng
hcfmusp.relation.referenceDang CV, 2010, CANCER RES, V70, P859, DOI 10.1158/0008-5472.CAN-09-3556eng
hcfmusp.relation.referenceDemontis D, 2019, NAT GENET, V51, P63, DOI 10.1038/s41588-018-0269-7eng
hcfmusp.relation.referenceDenley MCS, 2018, FRONT NEUROSCI-SWITZ, V12, DOI 10.3389/fnins.2018.00245eng
hcfmusp.relation.referenceDeverman BE, 2009, NEURON, V64, P61, DOI 10.1016/j.neuron.2009.09.002eng
hcfmusp.relation.referenceEisinger BE, 2013, BMC NEUROSCI, V14, DOI 10.1186/1471-2202-14-147eng
hcfmusp.relation.referenceErnst C, 2016, TRENDS NEUROSCI, V39, P290, DOI 10.1016/j.tins.2016.03.001eng
hcfmusp.relation.referenceErta M, 2012, INT J BIOL SCI, V8, P1254, DOI 10.7150/ijbs.4679eng
hcfmusp.relation.referenceFame RM, 2021, FRONT CELL DEV BIOL, V9, DOI 10.3389/fcell.2021.780207eng
hcfmusp.relation.referenceFink G, 2018, AM J EPIDEMIOL, V187, P2324, DOI 10.1093/aje/kwy141eng
hcfmusp.relation.referenceFlames N, 2009, NATURE, V458, P885, DOI 10.1038/nature07929eng
hcfmusp.relation.referenceFritz V, 2010, ONCOGENE, V29, P4369, DOI 10.1038/onc.2010.182eng
hcfmusp.relation.referenceGaiteri C, 2014, GENES BRAIN BEHAV, V13, P13, DOI 10.1111/gbb.12106eng
hcfmusp.relation.referenceGaljaard S, 2019, BIOL SEX DIFFER, V10, DOI 10.1186/s13293-019-0261-7eng
hcfmusp.relation.referenceGlass K, 2014, BMC SYST BIOL, V8, DOI 10.1186/s12918-014-0118-yeng
hcfmusp.relation.referenceGlass K, 2013, PLOS ONE, V8, DOI 10.1371/journal.pone.0064832eng
hcfmusp.relation.referenceGrandori C, 2000, ANNU REV CELL DEV BI, V16, P653, DOI 10.1146/annurev.cellbio.16.1.653eng
hcfmusp.relation.referenceGrove J, 2019, NAT GENET, V51, P431, DOI 10.1038/s41588-019-0344-8eng
hcfmusp.relation.referenceGurgen D, 2013, HYPERTENSION, V61, P730, DOI 10.1161/HYPERTENSIONAHA.111.00276eng
hcfmusp.relation.referenceGur RC, 2017, J NEUROSCI RES, V95, P189, DOI 10.1002/jnr.23830eng
hcfmusp.relation.referenceGutierrez-Adan A, 2006, REPROD DOMEST ANIM, V41, P54, DOI 10.1111/j.1439-0531.2006.00769.xeng
hcfmusp.relation.referenceHeiden MGV, 2009, SCIENCE, V324, P1029, DOI 10.1126/science.1160809eng
hcfmusp.relation.referenceHoward DM, 2019, NAT NEUROSCI, V22, P343, DOI 10.1038/s41593-018-0326-7eng
hcfmusp.relation.referenceIlyas Muhammad, 2020, F1000Res, V9, DOI 10.12688/f1000research.16315.1eng
hcfmusp.relation.referenceInoue M, 2017, DEVELOPMENT, V144, P385, DOI 10.1242/dev.136382eng
hcfmusp.relation.referenceJagasia R, 2009, J NEUROSCI, V29, P7966, DOI 10.1523/JNEUROSCI.1054-09.2009eng
hcfmusp.relation.referenceJakovcevski I, 2005, J NEUROSCI, V25, P10064, DOI 10.1523/JNEUROSCI.2324-05.2005eng
hcfmusp.relation.referenceJansen IE, 2019, NAT GENET, V51, P404, DOI 10.1038/s41588-018-0311-9eng
hcfmusp.relation.referenceJezek P, 2010, INT J BIOCHEM CELL B, V42, P604, DOI 10.1016/j.biocel.2009.11.008eng
hcfmusp.relation.referenceKalebic N, 2020, TRENDS NEUROSCI, V43, P843, DOI 10.1016/j.tins.2020.07.009eng
hcfmusp.relation.referenceKang HJ, 2011, NATURE, V478, P483, DOI 10.1038/nature10523eng
hcfmusp.relation.referenceKaraismailoglu S, 2013, J TURK-GER GYNECOL A, V14, P163, DOI 10.5152/jtgga.2013.86836eng
hcfmusp.relation.referenceKim JW, 2004, MOL CELL BIOL, V24, P5923, DOI 10.1128/MCB.24.13.5923-5936.2004eng
hcfmusp.relation.referenceKnobloch Marlen, 2017, Brain Plast, V3, P61, DOI 10.3233/BPL-160035eng
hcfmusp.relation.referenceKostovic I, 2019, NEUROIMAGE, V188, P743, DOI 10.1016/j.neuroimage.2018.12.043eng
hcfmusp.scopus.lastupdate2024-05-10
relation.isAuthorOfPublication26dcca7a-26f5-459a-bb2f-5b850a0acde4
relation.isAuthorOfPublication302b2020-cbc3-4a79-8697-ece1308a4bdc
relation.isAuthorOfPublication.latestForDiscovery26dcca7a-26f5-459a-bb2f-5b850a0acde4
Arquivos
Pacote Original
Agora exibindo 1 - 1 de 1
Carregando...
Imagem de Miniatura
Nome:
art_TOLEDO_Sex_differences_in_gene_regulatory_networks_during_midgestational_2022.PDF
Tamanho:
2.65 MB
Formato:
Adobe Portable Document Format
Descrição:
publishedVersion (English)