Atypical genomic cortical patterning in autism with poor early language outcome.


Journal

Science advances
ISSN: 2375-2548
Titre abrégé: Sci Adv
Pays: United States
ID NLM: 101653440

Informations de publication

Date de publication:
03 Sep 2021
Historique:
entrez: 13 9 2021
pubmed: 14 9 2021
medline: 14 9 2021
Statut: ppublish

Résumé

Cortical regionalization develops via genomic patterning along anterior-posterior (A-P) and dorsal-ventral (D-V) gradients. Here, we find that normative A-P and D-V genomic patterning of cortical surface area (SA) and thickness (CT), present in typically developing and autistic toddlers with good early language outcome, is absent in autistic toddlers with poor early language outcome. Autistic toddlers with poor early language outcome are instead specifically characterized by a secondary and independent genomic patterning effect on CT. Genes involved in these effects can be traced back to midgestational A-P and D-V gene expression gradients and different prenatal cell types (e.g., progenitor cells and excitatory neurons), are functionally important for vocal learning and human-specific evolution, and are prominent in prenatal coexpression networks enriched for high-penetrance autism risk genes. Autism with poor early language outcome may be explained by atypical genomic cortical patterning starting in prenatal development, which may detrimentally affect later regional functional specialization and circuit formation.

Identifiants

pubmed: 34516910
doi: 10.1126/sciadv.abh1663
pmc: PMC8442861
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

eabh1663

Subventions

Organisme : Medical Research Council
ID : MR/M009041/1
Pays : United Kingdom
Organisme : NIDCD NIH HHS
ID : R01 DC016385
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH110558
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH118281
Pays : United States

Références

Mol Syst Biol. 2015 Dec 14;11(12):841
pubmed: 26668231
N Engl J Med. 2015 Feb 26;372(9):793-5
pubmed: 25635347
Nat Neurosci. 2019 Oct;22(10):1624-1634
pubmed: 31551593
Cell. 2016 Mar 10;164(6):1269-1276
pubmed: 26967292
Neuron. 2012 Feb 9;73(3):537-52
pubmed: 22325205
Hum Brain Mapp. 2017 Dec;38(12):5931-5942
pubmed: 28898497
Mol Psychiatry. 2019 Oct;24(10):1435-1450
pubmed: 30617272
Bioinformatics. 2008 Jul 1;24(13):1547-8
pubmed: 18467348
Nat Neurosci. 2018 Sep;21(9):1251-1259
pubmed: 30082915
Neuron. 2014 Sep 3;83(5):1131-43
pubmed: 25155956
Cell. 2013 Nov 21;155(5):1008-21
pubmed: 24267887
Autism Res. 2013 Dec;6(6):468-78
pubmed: 24124067
Brain Behav Immun. 2012 Mar;26(3):383-92
pubmed: 21906670
J Autism Dev Disord. 2000 Jun;30(3):205-23
pubmed: 11055457
J Pediatr. 2021 Sep;236:179-188
pubmed: 33915154
PLoS Comput Biol. 2011 Jan 20;7(1):e1001057
pubmed: 21283776
Neuron. 2007 Oct 25;56(2):252-69
pubmed: 17964244
Nat Rev Genet. 2015 Aug;16(8):441-58
pubmed: 26149713
Nature. 2015 Apr 2;520(7545):51-6
pubmed: 25807484
Science. 2018 Dec 14;362(6420):
pubmed: 30545855
Nat Commun. 2015 Mar 10;6:6404
pubmed: 25752243
Science. 1988 Jul 8;241(4862):170-6
pubmed: 3291116
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
Bioinformatics. 2015 May 15;31(10):1584-91
pubmed: 25583121
Pediatrics. 2015 Oct;136 Suppl 1:S60-81
pubmed: 26430170
Autism. 2008 Sep;12(5):487-511
pubmed: 18805944
Nat Commun. 2019 Mar 4;10(1):1022
pubmed: 30833582
N Engl J Med. 2014 Mar 27;370(13):1209-1219
pubmed: 24670167
IEEE Trans Med Imaging. 2007 Apr;26(4):518-29
pubmed: 17427739
Nature. 2012 Sep 20;489(7416):391-399
pubmed: 22996553
Neuroimage. 1999 Feb;9(2):179-94
pubmed: 9931268
Science. 2018 Aug 17;361(6403):709-712
pubmed: 30115809
Nature. 2017 Oct 11;550(7675):204-213
pubmed: 29022597
Neurobiol Dis. 2010 May;38(2):148-53
pubmed: 19765659
Nat Neurosci. 2018 Dec;21(12):1680-1688
pubmed: 30482947
Neuroimage. 2016 Jan 1;124(Pt B):1149-1154
pubmed: 25937488
Nature. 2011 May 25;474(7351):380-4
pubmed: 21614001
Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):11050-5
pubmed: 10984517
Mol Autism. 2013 Oct 03;4(1):36
pubmed: 24090431
Nature. 2014 Apr 10;508(7495):199-206
pubmed: 24695229
Nat Commun. 2019 Jun 3;10(1):2396
pubmed: 31160561
Genome Biol. 2004;5(10):R80
pubmed: 15461798
Cell. 2017 Jun 15;169(7):1177-1186
pubmed: 28622505
Mol Psychiatry. 2019 Jan;24(1):88-107
pubmed: 29934544
Nature. 2015 Jul 16;523(7560):337-41
pubmed: 26030524
Elife. 2020 Nov 23;9:
pubmed: 33226336
Brain Res. 2011 Mar 22;1380:138-45
pubmed: 20920490
Neuroimage. 2011 May 15;56(2):455-75
pubmed: 20656037
Neuroimage. 2010 Oct 15;53(1):85-93
pubmed: 20621657
Nature. 2016 Dec 15;540(7633):423-427
pubmed: 27919067
Science. 2018 Dec 14;362(6420):
pubmed: 30545854
Neuroimage. 2006 Aug 1;32(1):180-94
pubmed: 16651008
Cell. 2011 Jul 22;146(2):247-61
pubmed: 21784246
Neuron. 2015 Apr 22;86(2):567-77
pubmed: 25864635
Trends Neurosci. 2020 May;43(5):326-342
pubmed: 32353336
BMC Bioinformatics. 2008 Dec 29;9:559
pubmed: 19114008
Proc Natl Acad Sci U S A. 2014 Oct 21;111(42):E4468-77
pubmed: 25294932
Science. 2019 May 17;364(6441):685-689
pubmed: 31097668
IEEE Trans Med Imaging. 2001 Jan;20(1):70-80
pubmed: 11293693
Science. 2018 Dec 14;362(6420):
pubmed: 30545856
PLoS Genet. 2012;8(3):e1002592
pubmed: 22457638
Proc Natl Acad Sci U S A. 2015 Dec 15;112(50):15462-7
pubmed: 26575625
Front Neurosci. 2017 Jan 05;10:601
pubmed: 28105001
Science. 2012 Mar 30;335(6076):1634-6
pubmed: 22461613
Neuroimage. 2004;23 Suppl 1:S69-84
pubmed: 15501102
Neuron. 2019 Sep 4;103(5):785-801.e8
pubmed: 31303374
Neuron. 2019 Sep 25;103(6):980-1004
pubmed: 31557462
Cell. 2020 Feb 6;180(3):568-584.e23
pubmed: 31981491
Proc Natl Acad Sci U S A. 2016 Dec 20;113(51):14662-14667
pubmed: 27930330
Neuroimage. 1999 Feb;9(2):195-207
pubmed: 9931269
Proc Natl Acad Sci U S A. 2013 Oct 15;110(42):17089-94
pubmed: 24082094
BMC Mol Biol. 2006 Jan 31;7:3
pubmed: 16448564

Auteurs

Michael V Lombardo (MV)

Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, Italy.
Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.

Lisa Eyler (L)

Department of Psychiatry, University of California, San Diego, La Jolla, CA, USA.
VISN 22 Mental Illness Research, Education, and Clinical Center, VA San Diego Healthcare System, San Diego, CA, USA.

Tiziano Pramparo (T)

Autism Center of Excellence, Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA.

Vahid H Gazestani (VH)

Autism Center of Excellence, Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA.

Donald J Hagler (DJ)

Center for Multimodal Imaging and Genetics, University of California, San Diego, La Jolla, CA, USA.
Department of Radiology, University of California, San Diego, La Jolla, CA, USA.

Chi-Hua Chen (CH)

Department of Psychiatry, University of California, San Diego, La Jolla, CA, USA.

Anders M Dale (AM)

Center for Multimodal Imaging and Genetics, University of California, San Diego, La Jolla, CA, USA.
Department of Radiology, University of California, San Diego, La Jolla, CA, USA.
Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA.

Jakob Seidlitz (J)

Department of Child and Adolescent Psychiatry and Behavioral Science, Children's Hospital of Philadelphia, Philadelphia, PA, USA.
Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA.

Richard A I Bethlehem (RAI)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.
Department of Psychiatry, University of Cambridge, Cambridge, UK.

Natasha Bertelsen (N)

Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, Italy.
Center for Mind/Brain Sciences, University of Trento, Rovereto, Italy.

Cynthia Carter Barnes (CC)

Autism Center of Excellence, Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA.

Linda Lopez (L)

Autism Center of Excellence, Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA.

Kathleen Campbell (K)

Autism Center of Excellence, Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA.
Department of Pediatrics, University of Utah, Salt Lake City, UT, USA.

Nathan E Lewis (NE)

Department of Pediatrics, University of California, San Diego, La Jolla, CA, USA.
Department of Bioengineering, University of California, San Diego, La Jolla, CA, USA.
Novo Nordisk Foundation Center for Biosustainability at the University of California, San Diego, La Jolla, CA, USA.

Karen Pierce (K)

Autism Center of Excellence, Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA.

Eric Courchesne (E)

Autism Center of Excellence, Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA.

Classifications MeSH