Non-coding structural variation differentially impacts attention-deficit hyperactivity disorder (ADHD) gene networks in African American vs Caucasian children.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
17 09 2020
Historique:
received: 10 01 2020
accepted: 16 06 2020
entrez: 18 9 2020
pubmed: 19 9 2020
medline: 22 12 2020
Statut: epublish

Résumé

Previous studies of attention-deficit hyperactivity disorder (ADHD) have suggested that structural variants (SVs) play an important role but these were mainly studied in subjects of European ancestry and focused on coding regions. In this study, we sought to address the role of SVs in non-European populations and outside of coding regions. To that end, we generated whole genome sequence (WGS) data on 875 individuals, including 205 ADHD cases and 670 non-ADHD controls. The ADHD cases included 116 African Americans (AA) and 89 of European Ancestry (EA) with SVs in comparison with 408 AA and 262 controls, respectively. Multiple SVs and target genes that associated with ADHD from previous studies were identified or replicated, and novel recurrent ADHD-associated SV loci were discovered. We identified clustering of non-coding SVs around neuroactive ligand-receptor interaction pathways, which are involved in neuronal brain function, and highly relevant to ADHD pathogenesis and regulation of gene expression related to specific ADHD phenotypes. There was little overlap (around 6%) in the genes impacted by SVs between AA and EA. These results suggest that SVs within non-coding regions may play an important role in ADHD development and that WGS could be a powerful discovery tool for studying the molecular mechanisms of ADHD.

Identifiants

pubmed: 32943653
doi: 10.1038/s41598-020-71307-0
pii: 10.1038/s41598-020-71307-0
pmc: PMC7499198
doi:

Substances chimiques

RNA, Untranslated 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

15252

Références

Polanczyk, G. V., Willcutt, E. G., Salum, G. A., Kieling, C. & Rohde, L. A. ADHD prevalence estimates across three decades: an updated systematic review and meta-regression analysis. Int. J. Epidemiol. 43, 434–442. https://doi.org/10.1093/ije/dyt261 (2014).
doi: 10.1093/ije/dyt261 pubmed: 24464188 pmcid: 4817588
Visser, S. N. et al. Trends in the parent-report of health care provider-diagnosed and medicated attention-deficit/hyperactivity disorder: United States, 2003–2011. J. Am. Acad. Child Adolesc. Psychiatry 53, 34–46. https://doi.org/10.1016/j.jaac.2013.09.001 (2014).
doi: 10.1016/j.jaac.2013.09.001 pubmed: 24342384
Barbaresi, W. J. et al. Mortality, ADHD, and psychosocial adversity in adults with childhood ADHD: a prospective study. Pediatrics 131, 637–644. https://doi.org/10.1542/peds.2012-2354 (2013).
doi: 10.1542/peds.2012-2354 pubmed: 23460687 pmcid: 3821174
Elia, J. et al. Genome-wide copy number variation study associates metabotropic glutamate receptor gene networks with attention deficit hyperactivity disorder. Nat. Genet. 44, 78–84. https://doi.org/10.1038/ng.1013 (2011).
doi: 10.1038/ng.1013 pubmed: 22138692 pmcid: 4310555
Lantieri, F., Glessner, J. T., Hakonarson, H., Elia, J. & Devoto, M. Analysis of GWAS top hits in ADHD suggests association to two polymorphisms located in genes expressed in the cerebellum. Am. J. Med. Genet. B Neuropsychiatr. Genet. 153B, 1127–1133. https://doi.org/10.1002/ajmg.b.31110 (2010).
doi: 10.1002/ajmg.b.31110 pubmed: 20607790
Connolly, J. J., Glessner, J. T., Elia, J. & Hakonarson, H. ADHD & pharmacotherapy: past, present and future: a review of the changing landscape of drug therapy for attention deficit hyperactivity disorder. Ther. Innov. Regul. Sci. 49, 632–642. https://doi.org/10.1177/2168479015599811 (2015).
doi: 10.1177/2168479015599811 pubmed: 26366330 pmcid: 4564067
Acosta, M. T., Arcos-Burgos, M. & Muenke, M. Attention deficit/hyperactivity disorder (ADHD): complex phenotype, simple genotype?. Genet. Med. 6, 1–15. https://doi.org/10.1097/01.GIM.0000110413.07490.0B (2004).
doi: 10.1097/01.GIM.0000110413.07490.0B pubmed: 14726804
Akutagava-Martins, G. C., Rohde, L. A. & Hutz, M. H. Genetics of attention-deficit/hyperactivity disorder: an update. Expert. Rev. Neurother. 16, 145–156. https://doi.org/10.1586/14737175.2016.1130626 (2016).
doi: 10.1586/14737175.2016.1130626 pubmed: 26651394
Glessner, J. T. et al. Copy number variation meta-analysis reveals a novel duplication at 9p24 associated with multiple neurodevelopmental disorders. Genome Med. 9, 106. https://doi.org/10.1186/s13073-017-0494-1 (2017).
doi: 10.1186/s13073-017-0494-1 pubmed: 29191242 pmcid: 5709845
Glessner, J. T., Connolly, J. J. & Hakonarson, H. Rare genomic deletions and duplications and their role in neurodevelopmental disorders. Curr. Top. Behav. Neurosci. 12, 345–360. https://doi.org/10.1007/7854_2011_179 (2012).
doi: 10.1007/7854_2011_179 pubmed: 22241247
Zhang, F. & Lupski, J. R. Non-coding genetic variants in human disease. Hum. Mol. Genet 24, R102-110. https://doi.org/10.1093/hmg/ddv259 (2015).
doi: 10.1093/hmg/ddv259 pubmed: 26152199 pmcid: 4572001
Bulayeva, K. et al. Genomic structural variants are linked with intellectual disability. J. Neural. Transm (Vienna) 122, 1289–1301. https://doi.org/10.1007/s00702-015-1366-8 (2015).
doi: 10.1007/s00702-015-1366-8
Demontis, D. et al. Discovery of the first genome-wide significant risk loci for attention deficit/hyperactivity disorder. Nat. Genet 51, 63–75. https://doi.org/10.1038/s41588-018-0269-7 (2019).
doi: 10.1038/s41588-018-0269-7 pubmed: 30478444
Zhang, L. et al. ADHDgene: a genetic database for attention deficit hyperactivity disorder. Nucleic Acids Res 40, D1003-1009. https://doi.org/10.1093/nar/gkr992 (2012).
doi: 10.1093/nar/gkr992 pubmed: 22080511
Thevenon, J. et al. 12p13.33 microdeletion including ELKS/ERC1, a new locus associated with childhood apraxia of speech. Eur. J. Hum. Genet 21, 82–88. https://doi.org/10.1038/ejhg.2012.116 (2013).
doi: 10.1038/ejhg.2012.116 pubmed: 22713806
Khadka, S. et al. Multivariate Imaging Genetics Study of MRI Gray Matter Volume and SNPs Reveals Biological Pathways Correlated with Brain Structural Differences in Attention Deficit Hyperactivity Disorder. Front Psychiatry 7, 128. https://doi.org/10.3389/fpsyt.2016.00128 (2016).
doi: 10.3389/fpsyt.2016.00128 pubmed: 27504100 pmcid: 4959119
Lima Lde, A. et al. An integrative approach to investigate the respective roles of single-nucleotide variants and copy-number variants in Attention-Deficit/Hyperactivity Disorder. Sci Rep 6, 22851. https://doi.org/10.1038/srep22851 (2016).
doi: 10.1038/srep22851 pubmed: 26947246
Kun-Rodrigues, C. et al. A systematic screening to identify de novo mutations causing sporadic early-onset Parkinson’s disease. Hum Mol Genet 24, 6711–6720. https://doi.org/10.1093/hmg/ddv376 (2015).
doi: 10.1093/hmg/ddv376 pubmed: 26362251 pmcid: 4634375
Mahmoudi, E. & Cairns, M. J. MiR-137: an important player in neural development and neoplastic transformation. Mol. Psychiatry 22, 44–55. https://doi.org/10.1038/mp.2016.150 (2017).
doi: 10.1038/mp.2016.150 pubmed: 27620842
Tovo-Rodrigues, L. et al. DRD4 rare variants in Attention-Deficit/Hyperactivity Disorder (ADHD): further evidence from a birth cohort study. PLoS ONE 8, e85164. https://doi.org/10.1371/journal.pone.0085164 (2013).
doi: 10.1371/journal.pone.0085164 pubmed: 24391992 pmcid: 3877354
Stankiewicz, P. et al. Haploinsufficiency of the chromatin remodeler BPTF causes syndromic developmental and speech delay, postnatal microcephaly, and dysmorphic features. Am. J. Hum. Genet. 101, 503–515. https://doi.org/10.1016/j.ajhg.2017.08.014 (2017).
doi: 10.1016/j.ajhg.2017.08.014 pubmed: 28942966 pmcid: 5630163
Popp, B. et al. Exome Pool-Seq in neurodevelopmental disorders. Eur. J. Hum. Genet. 25, 1364–1376. https://doi.org/10.1038/s41431-017-0022-1 (2017).
doi: 10.1038/s41431-017-0022-1 pubmed: 29158550 pmcid: 5865117
Polina, E. R. et al. ADHD diagnosis may influence the association between polymorphisms in nicotinic acetylcholine receptor genes and tobacco smoking. Neuromol. Med. 16, 389–397. https://doi.org/10.1007/s12017-013-8286-2 (2014).
doi: 10.1007/s12017-013-8286-2
Franke, B. et al. The genetics of attention deficit/hyperactivity disorder in adults, a review. Mol Psychiatry 17, 960–987. https://doi.org/10.1038/mp.2011.138 (2012).
doi: 10.1038/mp.2011.138 pubmed: 22105624
Kim, J. I. et al. The GRIN2B and GRIN2A Gene Variants Are Associated With Continuous Performance Test Variables in ADHD. J Atten Disord https://doi.org/10.1177/1087054716649665 (2016).
doi: 10.1177/1087054716649665 pubmed: 28030984
Neale, B. M. et al. Meta-analysis of genome-wide association studies of attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 49, 884–897. https://doi.org/10.1016/j.jaac.2010.06.008 (2010).
doi: 10.1016/j.jaac.2010.06.008 pubmed: 20732625 pmcid: 2928252
Mehta, C. M., Gruen, J. R. & Zhang, H. A method for integrating neuroimaging into genetic models of learning performance. Genet Epidemiol 41, 4–17. https://doi.org/10.1002/gepi.22025 (2017).
doi: 10.1002/gepi.22025 pubmed: 27859682
Shelley-Tremblay, J. F. & Rosen, L. A. Attention deficit hyperactivity disorder: an evolutionary perspective. J. Genet. Psychol. 157, 443–453 (1996).
doi: 10.1080/00221325.1996.9914877
Calkins, M. E. et al. The Philadelphia Neurodevelopmental Cohort: constructing a deep phenotyping collaborative. J. Child. Psychol. Psychiatry 56, 1356–1369. https://doi.org/10.1111/jcpp.12416 (2015).
doi: 10.1111/jcpp.12416 pubmed: 25858255 pmcid: 4598260
Chen, X. et al. Manta: rapid detection of structural variants and indels for germline and cancer sequencing applications. Bioinformatics 32, 1220–1222. https://doi.org/10.1093/bioinformatics/btv710 (2016).
doi: 10.1093/bioinformatics/btv710 pubmed: 26647377

Auteurs

Yichuan Liu (Y)

Center for Applied Genomics, Children's Hospital of Philadelphia, 3615 Civic Center Blvd, Abramson Building, Philadelphia, PA, 19104, USA.

Xiao Chang (X)

Center for Applied Genomics, Children's Hospital of Philadelphia, 3615 Civic Center Blvd, Abramson Building, Philadelphia, PA, 19104, USA.

Huiqi Qu (H)

Center for Applied Genomics, Children's Hospital of Philadelphia, 3615 Civic Center Blvd, Abramson Building, Philadelphia, PA, 19104, USA.

Joseph Glessner (J)

Center for Applied Genomics, Children's Hospital of Philadelphia, 3615 Civic Center Blvd, Abramson Building, Philadelphia, PA, 19104, USA.

Lifeng Tian (L)

Center for Applied Genomics, Children's Hospital of Philadelphia, 3615 Civic Center Blvd, Abramson Building, Philadelphia, PA, 19104, USA.

Dong Li (D)

Center for Applied Genomics, Children's Hospital of Philadelphia, 3615 Civic Center Blvd, Abramson Building, Philadelphia, PA, 19104, USA.

Haijun Qiu (H)

Center for Applied Genomics, Children's Hospital of Philadelphia, 3615 Civic Center Blvd, Abramson Building, Philadelphia, PA, 19104, USA.

Patrick M A Sleiman (PMA)

Center for Applied Genomics, Children's Hospital of Philadelphia, 3615 Civic Center Blvd, Abramson Building, Philadelphia, PA, 19104, USA. sleimanp@email.chop.edu.
Division of Human Genetics, Department of Pediatrics, The Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA. sleimanp@email.chop.edu.

Hakon Hakonarson (H)

Center for Applied Genomics, Children's Hospital of Philadelphia, 3615 Civic Center Blvd, Abramson Building, Philadelphia, PA, 19104, USA. hakonarson@email.chop.edu.
Department of Human Genetics, Children's Hospital of Philadelphia, Philadelphia, PA, USA. hakonarson@email.chop.edu.
Division of Human Genetics, Department of Pediatrics, The Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA. hakonarson@email.chop.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH