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

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