Complete Sequence of the 22q11.2 Allele in 1,053 Subjects with 22q11.2 Deletion Syndrome Reveals Modifiers of Conotruncal Heart Defects

Y.J. Zhao, A. Diacou, H.R. Johnston, F.I. Musfee, D.M. McDonald-McGinn, D. McGinn, T.B. Crowley, G.M. Repetto, A. Swillen, J. Breckpot, J.R. Vermeesch, W.R. Kates, M.C. Digilio, M. Unolt, B. Marino, M. Pontillo, M. Armando, F. Di Fabio, S. Vicari, M. van den BreeH. Moss, M.J. Owen, K.C. Murphy, C.M. Murphy, D. Murphy, K. Schoch, V. Shashi, F. Tassone, T.J. Simon, R.J. Shprintzen, L. Campbell, N. Philip, D. Heine-Suner, S. Garcia-Minaur, L. Fernandez, C.E. Bearden, C. Vingerhoets, T. van Amelsvoort, S. Eliez, M. Schneider, J.A.S. Vorstman, D. Gothelf, E. Zackai, A.J. Agopian, R.E. Gur, A.S. Bassett, B.S. Emanuel, E. Goldmuntz, L.E. Mitchell, T. Wang, International 22q11.2 Brain and Behavior Consortium, B.E. Morrow*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

The 22q11.2 deletion syndrome (22q11.2DS) results from non-allelic homologous recombination between low-copy repeats termed LCR22. About 60%-70% of individuals with the typical 3 megabase (Mb) deletion from LCR22A-D have congenital heart disease, mostly of the conotruncal type (CTD), whereas others have normal cardiac anatomy. In this study, we tested whether variants in the hemizygous LCR22A-D region are associated with risk for CTDs on the basis of the sequence of the 22q11.2 region from 1,053 22q11.2DS individuals. We found a significant association (FDR p < 0.05) of the CTD subset with 62 common variants in a single linkage disequilibrium (LD) block in a 350 kb interval harboring CRKL. A total of 45 of the 62 variants were associated with increased risk for CTDs (odds ratio [OR) ranges: 1.64-4.75). Associations of four variants were replicated in a meta-analysis of three genome-wide association studies of CTDs in affected individuals without 22q11.2DS. One of the replicated variants, rs178252, is located in an open chromatin region and resides in the double-elite enhancer, GH22J020947, that is predicted to regulate CRKL (CRK-like proto-oncogene, cytoplasmic adaptor) expression. Approximately 23% of patients with nested LCR22C-D deletions have CTDs, and inactivation of Crkl in mice causes CTDs, thus implicating this gene as a modifier. Rs178252 and rs6004160 are expression quantitative trait loci (eQTLs) of CRKL. Furthermore, set-based tests identified an enhancer that is predicted to target CRKL and is significantly associated with CTD risk (GH22J020946, sequence kernal association test (SKAT) p = 7.21 x 10(-5)) in the 22q11.2DS cohort. These findings suggest that variance in CTD penetrance in the 22q11.2DS population can be explained in part by variants affecting CRKL expression.
Original languageEnglish
Pages (from-to)26-40
Number of pages15
JournalAmerican Journal of Human Genetics
Volume106
Issue number1
DOIs
Publication statusPublished - 2 Jan 2020

Keywords

  • association
  • cardio-facial syndrome
  • crkl
  • ii deficiency
  • low-copy repeats
  • molecular definition
  • prediction
  • prevalence
  • tbx1 haploinsufficiency
  • variants
  • LOW-COPY REPEATS
  • VARIANTS
  • II DEFICIENCY
  • PREVALENCE
  • MOLECULAR DEFINITION
  • CRKL
  • PREDICTION
  • TBX1 HAPLOINSUFFICIENCY
  • ASSOCIATION
  • CARDIO-FACIAL SYNDROME

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