Home LiteratureArticle Details
PMID: 28990594 Published · ppublish English Journal Article Meta-Analysis

The Gene Encoding Protocadherin 9 (PCDH9), a Novel Risk Factor for Major Depressive Disorder.

Xiao X, Zheng F, Chang H, Ma Y, Yao YG, Luo XJ, Li M

Abstract

Genomic analyses have identified only a handful of robust risk loci for major depressive disorder (MDD). In addition to the published genome-wide significant genes, it is believed that there are undiscovered 'treasures' underlying the current MDD genome-wide association studies (GWASs) and gene expression data sets, and digging into these data will allow better understanding of the illness and development of new therapeutic approaches. For this purpose, we performed a meta-analytic study combining three MDD GWAS data sets (23andMe, CONVERGE, and PGC), and then conducted independent replications of significant loci in two additional samples. The genome-wide significant variants then underwent explorative analyses on MDD-related phenotypes, cognitive function alterations, and gene expression in brains. In the discovery meta-analysis, a previously unidentified single-nucleotide polymorphism (SNP) rs9540720 in the PCDH9 gene was genome-wide significantly associated with MDD (p=1.69 × 10-8 in a total of 89 610 cases and 246 603 controls), and the association was further strengthened when additional replication samples were included (p=1.20 × 10-8 in a total of 136 115 cases and 355 275 controls). The risk SNP was also associated with multiple MDD-related phenotypes and cognitive function impairment in diverse samples. Intriguingly, the risk allele of rs9540720 predicted lower PCDH9 expression, consistent with the diagnostic analysis results that PCDH9 mRNA expression levels in the brain and peripheral blood tissues were reduced in MDD patients compared with healthy controls. These convergent lines of evidence suggest that PCDH9 is likely a novel risk gene for MDD. Our study highlights the necessity and importance of excavating the public data sets to explore risk genes for MDD, and this approach is also applicable to other complex diseases.

MeSH Terms
Adolescent Adult Alleles Brain/metabolism Cadherins/biosynthesis,blood,genetics Case-Control Studies Child Cognitive Dysfunction/complications,genetics Depressive Disorder, Major/blood,complications,genetics,psychology Female Genetic Predisposition to Disease/genetics Genome-Wide Association Study Humans Male Polymorphism, Single Nucleotide/genetics Protocadherins Young Adult
Chemicals
Cadherins PCDH9 protein, human Protocadherins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Xiao Xiao
Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences and Yunnan Province, Kunming Institute of Zoology, Kunming, Yunnan, China.
Zheng Fanfan
Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, Beijing, China.
Chang Hong
Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences and Yunnan Province, Kunming Institute of Zoology, Kunming, Yunnan, China.
Ma Yina
State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China.
Yao Yong-Gang
Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences and Yunnan Province, Kunming Institute of Zoology, Kunming, Yunnan, China. | Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China.
Luo Xiong-Jian
Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences and Yunnan Province, Kunming Institute of Zoology, Kunming, Yunnan, China.
Li Ming ORCID
Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences and Yunnan Province, Kunming Institute of Zoology, Kunming, Yunnan, China. | Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China.
References (77)
77 references, click to expand
  1. Efficient replication of over 180 genetic associations with self-reported medical data.
    PLoS One. 2011;6(8):e23473 PMID: 21858135
  2. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication.
    Arch Gen Psychiatry. 2005 Jun;62(6):593-602 PMID: 15939837
  3. Distinct profiles of neurocognitive function in unmedicated unipolar depression and bipolar II depression.
    Biol Psychiatry. 2007 Oct 15;62(8):917-24 PMID: 17825802
  4. The protocadherin 17 gene affects cognition, personality, amygdala structure and function, synapse development and risk of major mood disorders.
    Mol Psychiatry. 2018 Feb;23 (2):400-412 PMID: 28070120
  5. Altered expression of genes involved in ATP biosynthesis and GABAergic neurotransmission in the ventral prefrontal cortex of suicides with and without major depression.
    Mol Psychiatry. 2009 Feb;14(2):175-89 PMID: 17938633
  6. Genetic variability in the regulation of gene expression in ten regions of the human brain.
    Nat Neurosci. 2014 Oct;17 (10 ):1418-1428 PMID: 25174004
  7. Genomic studies of mood disorders -- the brain as a muscle?
    Genome Biol. 2005;6(4):215 PMID: 15833130
  8. Molecular and Genetic Characterization of Depression: Overlap with other Psychiatric Disorders and Aging.
    Mol Neuropsychiatry. 2015 May;1(1):1-12 PMID: 26213687
  9. Convergent integration of animal model and human studies of bipolar disorder (manic-depressive illness).
    Curr Opin Pharmacol. 2010 Oct;10(5):594-600 PMID: 20817606
  10. Genome-wide association-, replication-, and neuroimaging study implicates HOMER1 in the etiology of major depression.
    Biol Psychiatry. 2010 Sep 15;68(6):578-85 PMID: 20673876
  11. Evidence of AS3MTd2d3-Associated Variants within 10q24.32-33 in the Genetic Risk of Major Affective Disorders.
    Mol Neuropsychiatry. 2017 Feb;2(4):213-218 PMID: 28277567
  12. Shared Genetics and Couple-Associated Environment Are Major Contributors to the Risk of Both Clinical and Self-Declared Depression.
    EBioMedicine. 2016 Dec;14 :161-167 PMID: 27838479
  13. Large-scale genome-wide association analysis of bipolar disorder identifies a new susceptibility locus near ODZ4.
    Nat Genet. 2011 Sep 18;43(10):977-83 PMID: 21926972
  14. Protocadherin 17 regulates presynaptic assembly in topographic corticobasal Ganglia circuits.
    Neuron. 2013 Jun 5;78(5):839-54 PMID: 23684785
  15. Distribution of protocadherin 9 protein in the developing mouse nervous system.
    Neuroscience. 2012 Dec 6;225:88-104 PMID: 22982106
  16. Biological insights from 108 schizophrenia-associated genetic loci.
    Nature. 2014 Jul 24;511(7510):421-7 PMID: 25056061
  17. Transethnic meta-analysis of genomewide association studies.
    Genet Epidemiol. 2011 Dec;35(8):809-22 PMID: 22125221
  18. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.
    Genome Biol. 2013 Apr 25;14(4):R36 PMID: 23618408
  19. Web-based, participant-driven studies yield novel genetic associations for common traits.
    PLoS Genet. 2010 Jun 24;6(6):e1000993 PMID: 20585627
  20. Gene expression in major depressive disorder.
    Mol Psychiatry. 2016 Mar;21(3):339-47 PMID: 26008736
  21. The genetics of depression: a review.
    Biol Psychiatry. 2006 Jul 15;60(2):84-92 PMID: 16300747
  22. Identification of IL6 as a susceptibility gene for major depressive disorder.
    Sci Rep. 2016 Aug 09;6:31264 PMID: 27502736
  23. Meta-analysis of genome-wide association studies of anxiety disorders.
    Mol Psychiatry. 2016 Oct;21(10 ):1391-9 PMID: 26754954
  24. Childhood intelligence is heritable, highly polygenic and associated with FNBP1L.
    Mol Psychiatry. 2014 Feb;19(2):253-8 PMID: 23358156
  25. Intelligence.
    Annu Rev Psychol. 2012;63:453-82 PMID: 21943169
  26. Genetic effects influencing risk for major depressive disorder in China and Europe.
    Transl Psychiatry. 2017 Mar 28;7(3):e1074 PMID: 28350396
  27. Childhood IQ in relation to later psychiatric disorder: evidence from a Danish birth cohort study.
    Br J Psychiatry. 2005 Aug;187:180-1 PMID: 16055831
  28. Interaction of the 5-HTTLPR and childhood trauma influences memory bias in healthy individuals.
    J Affect Disord. 2015 Nov 1;186:83-9 PMID: 26232751
  29. Clinical factors associated with treatment resistance in major depressive disorder: results from a European multicenter study.
    J Clin Psychiatry. 2007 Jul;68(7):1062-70 PMID: 17685743
  30. Sparse whole-genome sequencing identifies two loci for major depressive disorder.
    Nature. 2015 Jul 30;523(7562):588-91 PMID: 26176920
  31. Genetic Mapping in Mice Reveals the Involvement of Pcdh9 in Long-Term Social and Object Recognition and Sensorimotor Development.
    Biol Psychiatry. 2015 Oct 1;78(7):485-95 PMID: 25802080
  32. Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis.
    Nat Genet. 2010 Jul;42(7):579-89 PMID: 20581827
  33. The Sequence Alignment/Map format and SAMtools.
    Bioinformatics. 2009 Aug 15;25(16):2078-9 PMID: 19505943
  34. Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies.
    Genomics. 2011 Aug;98(2):152-3 PMID: 21651976
  35. The epidemiology of depression across cultures.
    Annu Rev Public Health. 2013;34:119-38 PMID: 23514317
  36. Convergent Functional Genomics of bipolar disorder: from animal model pharmacogenomics to human genetics and biomarkers.
    Neurosci Biobehav Rev. 2007;31(6):897-903 PMID: 17614132
  37. Genetic risk profiles for depression and anxiety in adult and elderly cohorts.
    Mol Psychiatry. 2011 Jul;16(7):773-83 PMID: 20567237
  38. A human-specific AS3MT isoform and BORCS7 are molecular risk factors in the 10q24.32 schizophrenia-associated locus.
    Nat Med. 2016 Jun;22(6):649-56 PMID: 27158905
  39. Genome-wide association study of recurrent major depressive disorder in two European case-control cohorts.
    Mol Psychiatry. 2010 Jun;15(6):589-601 PMID: 19107115
  40. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci.
    Nat Genet. 2010 Dec;42(12):1118-25 PMID: 21102463
  41. Candidate genes, pathways and mechanisms for bipolar (manic-depressive) and related disorders: an expanded convergent functional genomics approach.
    Mol Psychiatry. 2004 Nov;9(11):1007-29 PMID: 15314610
  42. The Genetic Architecture of Major Depressive Disorder in Han Chinese Women.
    JAMA Psychiatry. 2017 Feb 1;74(2):162-168 PMID: 28002544
  43. Linking "big" personality traits to anxiety, depressive, and substance use disorders: a meta-analysis.
    Psychol Bull. 2010 Sep;136(5):768-821 PMID: 20804236
  44. Genetic studies of major depressive disorder: why are there no genome-wide association study findings and what can we do about it?
    Biol Psychiatry. 2014 Oct 1;76(7):510-2 PMID: 25201436
  45. Polygenic dissection of diagnosis and clinical dimensions of bipolar disorder and schizophrenia.
    Mol Psychiatry. 2014 Sep;19(9):1017-1024 PMID: 24280982
  46. The genetic relationship of personality to major depression and schizophrenia.
    Neurotox Res. 2004;6(1):43-50 PMID: 15184104
  47. A genome-wide association meta-analysis of preschool internalizing problems.
    J Am Acad Child Adolesc Psychiatry. 2014 Jun;53(6):667-676.e7 PMID: 24839885
  48. Genome-wide association study of major recurrent depression in the U.K. population.
    Am J Psychiatry. 2010 Aug;167(8):949-57 PMID: 20516156
  49. The Genotype-Tissue Expression (GTEx) project.
    Nat Genet. 2013 Jun;45(6):580-5 PMID: 23715323
  50. Epidemiology of major depressive disorder: results from the National Epidemiologic Survey on Alcoholism and Related Conditions.
    Arch Gen Psychiatry. 2005 Oct;62(10):1097-106 PMID: 16203955
  51. Genome-wide association study identifies 74 loci associated with educational attainment.
    Nature. 2016 May 11;533(7604):539-42 PMID: 27225129
  52. A mega-analysis of genome-wide association studies for major depressive disorder.
    Mol Psychiatry. 2013 Apr;18(4):497-511 PMID: 22472876
  53. GWAS of 126,559 individuals identifies genetic variants associated with educational attainment.
    Science. 2013 Jun 21;340(6139):1467-71 PMID: 23722424
  54. A variant of the neuronal amino acid transporter SLC6A15 is associated with ACTH and cortisol responses and cognitive performance in unipolar depression.
    Int J Neuropsychopharmacol. 2013 Feb;16(1):83-90 PMID: 22475622
  55. Genome-wide association study of recurrent early-onset major depressive disorder.
    Mol Psychiatry. 2011 Feb;16(2):193-201 PMID: 20125088
  56. Influence of BCL2 gene in major depression susceptibility and antidepressant treatment outcome.
    J Affect Disord. 2014 Feb;155:288-94 PMID: 24321200
  57. The neuronal transporter gene SLC6A15 confers risk to major depression.
    Neuron. 2011 Apr 28;70(2):252-65 PMID: 21521612
  58. The stanley neuropathology consortium integrative database: a novel, web-based tool for exploring neuropathological markers in psychiatric disorders and the biological processes associated with abnormalities of those markers.
    Neuropsychopharmacology. 2010 Jan;35(2):473-82 PMID: 19829293
  59. Temporal dynamics and genetic control of transcription in the human prefrontal cortex.
    Nature. 2011 Oct 26;478(7370):519-23 PMID: 22031444
  60. Convergent functional genomics of schizophrenia: from comprehensive understanding to genetic risk prediction.
    Mol Psychiatry. 2012 Sep;17(9):887-905 PMID: 22584867
  61. Genetic foundations of human intelligence.
    Hum Genet. 2009 Jul;126(1):215-32 PMID: 19294424
  62. Capturing heterogeneity in gene expression studies by surrogate variable analysis.
    PLoS Genet. 2007 Sep;3(9):1724-35 PMID: 17907809
  63. Convergent lines of evidence support CAMKK2 as a schizophrenia susceptibility gene.
    Mol Psychiatry. 2014 Jul;19(7):774-83 PMID: 23958956
  64. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks.
    Nat Protoc. 2012 Mar 01;7(3):562-78 PMID: 22383036
  65. PLINK: a tool set for whole-genome association and population-based linkage analyses.
    Am J Hum Genet. 2007 Sep;81(3):559-75 PMID: 17701901
  66. Genome-wide association study of major depressive disorder: new results, meta-analysis, and lessons learned.
    Mol Psychiatry. 2012 Jan;17(1):36-48 PMID: 21042317
  67. Childhood IQ and adult mental disorders: a test of the cognitive reserve hypothesis.
    Am J Psychiatry. 2009 Jan;166(1):50-7 PMID: 19047325
  68. Postmortem brain tissue for drug discovery in psychiatric research.
    Schizophr Bull. 2009 Nov;35(6):1031-3 PMID: 19783604
  69. Influence of parental and grandparental major depressive disorder on behavior problems in early childhood: a three-generation study.
    J Am Acad Child Adolesc Psychiatry. 2008 Jan;47(1):53-60 PMID: 18174825
  70. Genetic epidemiology of major depression: review and meta-analysis.
    Am J Psychiatry. 2000 Oct;157(10):1552-62 PMID: 11007705
  71. Functional annotation of noncoding sequence variants.
    Nat Methods. 2014 Mar;11(3):294-6 PMID: 24487584
  72. SNOMAD (Standardization and NOrmalization of MicroArray Data): web-accessible gene expression data analysis.
    Bioinformatics. 2002 Nov;18(11):1540-1 PMID: 12424128
  73. Further evidence for the association between LRP8 and schizophrenia.
    Schizophr Res. 2017 May 8;:null PMID: 28495490
  74. Public health significance of neuroticism.
    Am Psychol. 2009 May-Jun;64(4):241-56 PMID: 19449983
  75. Poor replication of candidate genes for major depressive disorder using genome-wide association data.
    Mol Psychiatry. 2011 May;16(5):516-32 PMID: 20351714
  76. Identification of 15 genetic loci associated with risk of major depression in individuals of European descent.
    Nat Genet. 2016 Sep;48(9):1031-6 PMID: 27479909
  77. Genetic variants associated with subjective well-being, depressive symptoms, and neuroticism identified through genome-wide analyses.
    Nat Genet. 2016 Jun;48(6):624-33 PMID: 27089181
Article Info
Journal
Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
Abbr.
Neuropsychopharmacology
ISSN
1740-634X
Published
2018-00-00
Epub
2017-00-09
Pages
1128-1137
Language
English
Region
England
NLM ID
8904907
PMCID
PMC5854803
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]