Sex differences in gene regulatory networks during mid-gestational brain development
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Citações na Scopus
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Tipo de produção
article
Data de publicação
2022
Título da Revista
ISSN da Revista
Título do Volume
Editora
FRONTIERS MEDIA SA
Autores
FELTRIN, Arthur Sant'Anna
BARBOSA, Andre Rocha
TAHIRA, Ana Carolina
Citação
FRONTIERS IN HUMAN NEUROSCIENCE, v.16, article ID 955607, 21p, 2022
Resumo
Neurodevetopmental 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.
Palavras-chave
neurodevelopmental disorders, sex differences, fetal brain development, gene regulatory networks, systems biology, autism spectrum disorder (ASD)
Referências
- Abe H, 2012, P NATL ACAD SCI USA, V109, P8734, DOI 10.1073/pnas.1206418109
- Addis R, 2014, BIOL SEX DIFFER, V5, DOI 10.1186/s13293-014-0018-2
- Alberini CM, 2009, PHYSIOL REV, V89, P121, DOI 10.1152/physrev.00017.2008
- Arber S, 2000, CELL, V101, P485, DOI 10.1016/S0092-8674(00)80859-4
- Ascenzi M, 2017, DEV NEUROBIOL, V77, P1023, DOI 10.1002/dneu.22495
- Auger AP, 2003, J NEUROENDOCRINOL, V15, P622, DOI 10.1046/j.1365-2826.2003.01041.x
- Bale TL, 2016, DIALOGUES CLIN NEURO, V18, P459
- Barber MJ, 2007, PHYS REV E, V76, DOI 10.1103/PhysRevE.76.066102
- Behar TN, 1996, J NEUROSCI, V16, P1808
- Benatti P, 2016, ONCOTARGET, V7, P1633, DOI 10.18632/oncotarget.6453
- Borras C, 2003, FREE RADICAL BIO MED, V34, P546, DOI 10.1016/S0891-5849(02)01356-4
- Kummer KK, 2021, CYTOKINE, V144, DOI 10.1016/j.cyto.2021.155582
- Lam M, 2019, NAT GENET, V51, P1670, DOI 10.1038/s41588-019-0512-x
- Landeira BS, 2018, CEREB CORTEX, V28, P538, DOI 10.1093/cercor/bhw387
- Langfelder P, 2008, BMC BIOINFORMATICS, V9, DOI 10.1186/1471-2105-9-559
- Larsen KB, 2010, J HISTOCHEM CYTOCHEM, V58, P669, DOI 10.1369/jhc.2010.955757
- Lee PH, 2019, CELL, V179, P1469, DOI 10.1016/j.cell.2019.11.020
- Liberzon A, 2015, CELL SYST, V1, P417, DOI 10.1016/j.cels.2015.12.004
- Loke H, 2015, INT J BIOCHEM CELL B, V65, P139, DOI 10.1016/j.biocel.2015.05.024
- Long KTRER, 2022, FRONT CELL NEUROSCI, V15, DOI 10.3389/fncel.2021.804649
- Lopes-Ramos CM, 2021, CANCER RES, V81, P5401, DOI 10.1158/0008-5472.CAN-21-0730
- O'Brien H.E., 2018, FIGSHARE FILESET, DOI [10.6084/m9.figshare.6881825, DOI 10.6084/M9.FIGSHARE.6881825]
- Lopes-Ramos CM, 2020, CELL REP, V31, DOI 10.1016/j.celrep.2020.107795
- Lopes-Ramos CM, 2018, CANCER RES, V78, P5538, DOI 10.1158/0008-5472.CAN-18-0454
- Love MI, 2014, GENOME BIOL, V15, DOI 10.1186/s13059-014-0550-8
- Mahler N, 2017, PLOS GENET, V13, DOI 10.1371/journal.pgen.1006402
- Marchetto MC, 2017, MOL PSYCHIATR, V22, P820, DOI 10.1038/mp.2016.95
- Maschietto M, 2017, SCI REP-UK, V7, DOI 10.1038/srep44547
- May T, 2019, CURR OPIN NEUROL, V32, P622, DOI 10.1097/WCO.0000000000000714
- Mayes J S, 2004, Obes Rev, V5, P197, DOI 10.1111/j.1467-789X.2004.00152.x
- McCarthy MM, 2016, PHILOS T R SOC B, V371, DOI 10.1098/rstb.2015.0106
- Mcrae JF, 2017, NATURE, V542, P433, DOI 10.1038/nature21062
- O'Brien HE, 2018, GENOME BIOL, V19, DOI 10.1186/s13059-018-1567-1
- Michoel T, 2009, BMC SYST BIOL, V3, DOI 10.1186/1752-0509-3-49
- Miranda A, 2018, BRAIN BEHAV, V8, DOI 10.1002/brb3.920
- Mitchell AM, 2017, BRAIN BEHAV IMMUN, V60, P32, DOI 10.1016/j.bbi.2016.06.015
- Nakashima A, 2008, MOL CELL BIOL, V28, P4080, DOI 10.1128/MCB.02168-07
- Nayernia Z, 2014, ANTIOXID REDOX SIGN, V20, P2815, DOI 10.1089/ars.2013.5703
- OCKNER RK, 1979, J CLIN INVEST, V64, P172, DOI 10.1172/JCI109437
- Ojeda J, 2019, FRONT SYNAPTIC NEURO, V11, DOI 10.3389/fnsyn.2019.00033
- Oliva M, 2020, SCIENCE, V369, P1331, DOI 10.1126/science.aba3066
- Orth M, 2012, CHOLESTEROL, DOI 10.1155/2012/292598
- Padi M, 2018, NPJ SYST BIOL APPL, V4, DOI 10.1038/s41540-018-0052-5
- Parry DA, 2013, AM J HUM GENET, V93, P1135, DOI 10.1016/j.ajhg.2013.10.027
- Paulsen BD, 2012, CELL TRANSPLANT, V21, P1547, DOI 10.3727/096368911X600957
- Platig J, 2016, PLOS COMPUT BIOL, V12, DOI 10.1371/journal.pcbi.1005033
- Shi L, 2016, SCI REP-UK, V6, DOI 10.1038/srep21181
- Polioudakis D, 2019, NEURON, V103, P785, DOI 10.1016/j.neuron.2019.06.011
- RAY PF, 1995, J REPROD FERTIL, V104, P165
- Reczek CR, 2017, ANNU REV CANC BIOL, V1, P79, DOI 10.1146/annurev-cancerbio-041916-065808
- Reick M, 2001, SCIENCE, V293, P506, DOI 10.1126/science.1060699
- Reinius B, 2009, MOL PSYCHIATR, V14, P988, DOI 10.1038/mp.2009.79
- Ritchie ME, 2015, NUCLEIC ACIDS RES, V43, DOI 10.1093/nar/gkv007
- Ritchie SJ, 2018, CEREB CORTEX, V28, P2959, DOI 10.1093/cercor/bhy109
- Rodic S, 2018, INT J CANCER, V142, P440, DOI 10.1002/ijc.31069
- Rubin JB, 2020, BIOL SEX DIFFER, V11, DOI 10.1186/s13293-020-00291-x
- Russo PST, 2018, BMC BIOINFORMATICS, V19, DOI 10.1186/s12859-018-2053-1
- Silaidos C, 2018, BIOL SEX DIFFER, V9, DOI 10.1186/s13293-018-0193-7
- Saito K, 2009, P NATL ACAD SCI USA, V106, P8350, DOI 10.1073/pnas.0903541106
- Sanders SJ, 2015, NEURON, V87, P1215, DOI 10.1016/j.neuron.2015.09.016
- Santos-Terra J, 2021, INT J DEV NEUROSCI, V81, P545, DOI 10.1002/jdn.10141
- Sementchenko VI, 2000, ONCOGENE, V19, P6533, DOI 10.1038/sj.onc.1204034
- Shanware NP, 2013, ANNU REV PHARMACOL, V53, P89, DOI 10.1146/annurev-pharmtox-010611-134717
- Simoes SN, 2015, BMC BIOINFORMATICS, V16, DOI 10.1186/1471-2105-16-S19-S9
- Skinner MK, 2010, DIFFERENTIATION, V80, P1, DOI 10.1016/j.diff.2010.02.003
- Smedley D, 2009, BMC GENOMICS, V10, DOI 10.1186/1471-2164-10-22
- Sokpor G, 2022, FRONT NEUROSCI-SWITZ, V16, DOI 10.3389/fnins.2022.824802
- Sonawane AR, 2017, CELL REP, V21, P1077, DOI 10.1016/j.celrep.2017.10.001
- Stahl EA, 2019, NAT GENET, V51, P793, DOI 10.1038/s41588-019-0397-8
- Stark MJ, 2011, PLACENTA, V32, P865, DOI 10.1016/j.placenta.2011.08.010
- Subramanian A, 2005, P NATL ACAD SCI USA, V102, P15545, DOI 10.1073/pnas.0506580102
- Broere-Brown ZA, 2016, BIOL SEX DIFFER, V7, DOI 10.1186/s13293-016-0119-1
- Sun Y, 2001, CELL, V104, P365, DOI 10.1016/S0092-8674(01)00224-0
- Supek F, 2011, PLOS ONE, V6, DOI 10.1371/journal.pone.0021800
- Szklarczyk D, 2019, NUCLEIC ACIDS RES, V47, pD607, DOI 10.1093/nar/gky1131
- Tahira AC, 2019, AM J MED GENET B, V180, P390, DOI 10.1002/ajmg.b.32704
- Taverna E, 2014, ANNU REV CELL DEV BI, V30, P465, DOI 10.1146/annurev-cellbio-101011-155801
- Uhl M, 2022, FRONT MOL NEUROSCI, V15, DOI 10.3389/fnmol.2022.818390
- Veenstra TD, 2021, PROTEOMICS, V21, DOI 10.1002/pmic.202000235
- Verdin H, 2014, ORPHANET J RARE DIS, V9, DOI 10.1186/1750-1172-9-26
- Weirauch MT, 2014, CELL, V158, P1431, DOI 10.1016/j.cell.2014.08.009
- Werling DM, 2016, NAT COMMUN, V7, DOI 10.1038/ncomms10717
- Burke KJ, 2019, FRONT CELL NEUROSCI, V13, DOI 10.3389/fncel.2019.00221
- Yang ZF, 2014, MOL CELL BIOL, V34, P3194, DOI 10.1128/MCB.00492-12
- Yokogawa T, 2000, J BIOL CHEM, V275, P19913, DOI 10.1074/jbc.M908473199
- Yu GC, 2012, OMICS, V16, P284, DOI 10.1089/omi.2011.0118
- Zhang Y, 2002, J BIOL CHEM, V277, P28065, DOI 10.1074/jbc.C100767200
- Ziats MN, 2013, MOL AUTISM, V4, DOI 10.1186/2040-2392-4-10
- Cai CM, 2007, MOL ENDOCRINOL, V21, P1835, DOI 10.1210/me.2006-0480
- Cardinale DA, 2018, FRONT PHYSIOL, V9, DOI 10.3389/fphys.2018.01133
- Clifton VL, 2010, GROWTH HORM IGF RES, V20, P39, DOI 10.1016/j.ghir.2009.07.004
- Dang CV, 2010, CANCER RES, V70, P859, DOI 10.1158/0008-5472.CAN-09-3556
- Demontis D, 2019, NAT GENET, V51, P63, DOI 10.1038/s41588-018-0269-7
- Denley MCS, 2018, FRONT NEUROSCI-SWITZ, V12, DOI 10.3389/fnins.2018.00245
- Deverman BE, 2009, NEURON, V64, P61, DOI 10.1016/j.neuron.2009.09.002
- Eisinger BE, 2013, BMC NEUROSCI, V14, DOI 10.1186/1471-2202-14-147
- Ernst C, 2016, TRENDS NEUROSCI, V39, P290, DOI 10.1016/j.tins.2016.03.001
- Erta M, 2012, INT J BIOL SCI, V8, P1254, DOI 10.7150/ijbs.4679
- Fame RM, 2021, FRONT CELL DEV BIOL, V9, DOI 10.3389/fcell.2021.780207
- Fink G, 2018, AM J EPIDEMIOL, V187, P2324, DOI 10.1093/aje/kwy141
- Flames N, 2009, NATURE, V458, P885, DOI 10.1038/nature07929
- Fritz V, 2010, ONCOGENE, V29, P4369, DOI 10.1038/onc.2010.182
- Gaiteri C, 2014, GENES BRAIN BEHAV, V13, P13, DOI 10.1111/gbb.12106
- Galjaard S, 2019, BIOL SEX DIFFER, V10, DOI 10.1186/s13293-019-0261-7
- Glass K, 2014, BMC SYST BIOL, V8, DOI 10.1186/s12918-014-0118-y
- Glass K, 2013, PLOS ONE, V8, DOI 10.1371/journal.pone.0064832
- Grandori C, 2000, ANNU REV CELL DEV BI, V16, P653, DOI 10.1146/annurev.cellbio.16.1.653
- Grove J, 2019, NAT GENET, V51, P431, DOI 10.1038/s41588-019-0344-8
- Gurgen D, 2013, HYPERTENSION, V61, P730, DOI 10.1161/HYPERTENSIONAHA.111.00276
- Gur RC, 2017, J NEUROSCI RES, V95, P189, DOI 10.1002/jnr.23830
- Gutierrez-Adan A, 2006, REPROD DOMEST ANIM, V41, P54, DOI 10.1111/j.1439-0531.2006.00769.x
- Heiden MGV, 2009, SCIENCE, V324, P1029, DOI 10.1126/science.1160809
- Howard DM, 2019, NAT NEUROSCI, V22, P343, DOI 10.1038/s41593-018-0326-7
- Ilyas Muhammad, 2020, F1000Res, V9, DOI 10.12688/f1000research.16315.1
- Inoue M, 2017, DEVELOPMENT, V144, P385, DOI 10.1242/dev.136382
- Jagasia R, 2009, J NEUROSCI, V29, P7966, DOI 10.1523/JNEUROSCI.1054-09.2009
- Jakovcevski I, 2005, J NEUROSCI, V25, P10064, DOI 10.1523/JNEUROSCI.2324-05.2005
- Jansen IE, 2019, NAT GENET, V51, P404, DOI 10.1038/s41588-018-0311-9
- Jezek P, 2010, INT J BIOCHEM CELL B, V42, P604, DOI 10.1016/j.biocel.2009.11.008
- Kalebic N, 2020, TRENDS NEUROSCI, V43, P843, DOI 10.1016/j.tins.2020.07.009
- Kang HJ, 2011, NATURE, V478, P483, DOI 10.1038/nature10523
- Karaismailoglu S, 2013, J TURK-GER GYNECOL A, V14, P163, DOI 10.5152/jtgga.2013.86836
- Kim JW, 2004, MOL CELL BIOL, V24, P5923, DOI 10.1128/MCB.24.13.5923-5936.2004
- Knobloch Marlen, 2017, Brain Plast, V3, P61, DOI 10.3233/BPL-160035
- Kostovic I, 2019, NEUROIMAGE, V188, P743, DOI 10.1016/j.neuroimage.2018.12.043