[en] Intellectual developmental disorder with autism and dysmorphic facies (IDDADF) is a rare syndromic intellectual disability (ID) caused by homozygous disruption of PDZD8 (PDZ domain-containing protein 8), an integral endoplasmic reticulum (ER) protein. All four previously identified IDDADF cases exhibit autistic behavior, with autism spectrum disorder (ASD) diagnosed in three cases. To determine whether autistic behavior is a common outcome of PDZD8 disruption, we studied a third family with biallelic mutation of PDZD8 (family C) and further characterized PDZD8-deficient (Pdzd8tm1b) mice that exhibit stereotyped motor behavior relevant to ASD.
METHODS: Homozygosity mapping, whole-exome sequencing, and cosegregation analysis were used to identify the PDZD8 variant responsible for IDDADF, including diagnoses of ASD, in consanguineous family C. To assess the in vivo effect of PDZD8 disruption on social responses and related phenotypes, behavioral, structural magnetic resonance imaging, and microscopy analyses were conducted on the Pdzd8tm1b mouse line. Metabolic activity was profiled using sealed metabolic cages.
RESULTS: The discovery of a third family with IDDADF caused by biallelic disruption of PDZD8 permitted identification of a core clinical phenotype consisting of developmental delay, ID, autism, and facial dysmorphism. In addition to impairments in social recognition and social odor discrimination, Pdzd8tm1b mice exhibit increases in locomotor activity (dark phase only) and metabolic rate (both lights-on and dark phases), and decreased plasma triglyceride in males. In the brain, Pdzd8tm1b mice exhibit increased levels of accessory olfactory bulb volume, primary olfactory cortex volume, dendritic spine density, and ER stress- and mitochondrial fusion-related transcripts, as well as decreased levels of cerebellar nuclei volume and adult neurogenesis.
LIMITATIONS: The total number of known cases of PDZD8-related IDDADF remains low. Some mouse experiments in the study did not use balanced numbers of males and females. The assessment of ER stress and mitochondrial fusion markers did not extend beyond mRNA levels.
CONCLUSIONS: Our finding that the Pdzd8tm1b mouse model and all six known cases of IDDADF exhibit autistic behavior, with ASD diagnosed in five cases, identifies this trait as a common outcome of biallelic disruption of PDZD8 in humans and mice. Other abnormalities exhibited by Pdzd8tm1b mice suggest that the range of comorbidities associated with PDZD8 deficiency may be wider than presently recognized.
Disciplines :
Neurology
Author, co-author :
Pantiru, Andreea D ; School of Biomedical Sciences, University of Leeds, Leeds, LS2 9JT, UK ; Division of Neuroscience, School of Biological Sciences, University of Manchester, Manchester, M13 9PT, UK
Van de Sompele, Stijn ; Center for Medical Genetics, Ghent University Hospital, Ghent, Belgium ; Department of Biomolecular Medicine, Ghent University, Ghent, Belgium
Ligneul, Clemence ; Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neuroscience, University of Oxford, Oxford, OX1 3SR, UK
Chatelain, Camille ; Centre Hospitalier Universitaire de Liège - CHU > > Service de génétique
Barrea, Christophe ; Centre Hospitalier Universitaire de Liège - CHU > > Service de pédiatrie
Lerch, Jason P ; Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neuroscience, University of Oxford, Oxford, OX1 3SR, UK
Filippi, Beatrice M ; School of Biomedical Sciences, University of Leeds, Leeds, LS2 9JT, UK
Alkan, Serpil ; Centre Hospitalier Universitaire de Liège - CHU > > Service de pédiatrie (CHR)
De Baere, Elfride ; Center for Medical Genetics, Ghent University Hospital, Ghent, Belgium ; Department of Biomolecular Medicine, Ghent University, Ghent, Belgium
Johnston, Jamie ; School of Biomedical Sciences, University of Leeds, Leeds, LS2 9JT, UK
Clapcote, Steven J ; School of Biomedical Sciences, University of Leeds, Leeds, LS2 9JT, UK. S.J.Clapcote@leeds.ac.uk
Language :
English
Title :
Autistic behavior is a common outcome of biallelic disruption of PDZD8 in humans and mice.
BBSRC - Biotechnology and Biological Sciences Research Council MRC - Medical Research Council
Funding text :
We thank the family who participated in this study for their full cooperation. We also thank Tim Munsey and Simon Futers (University of Leeds) for technical assistance, and Chris Inglehearn, Manir Ali, Lee Roberts (University of Leeds), Michelle Stewart (MRC Harwell), Abeer Al Sayegh (Sultan Qaboos University Hospital, Oman), and Aisha Al Shamsi (Tawam Hospital, UAE) for helpful advice.This research was supported by grants from the Medical Research Council (MR/R014736/1 to SJC) and the Biotechnology and Biological Sciences Research Council (BB/R019401/1 to SJC and JJ). ADP was supported by a PhD scholarship from the Emma Reid and Leslie Reid Scholarships and Fellowships Fund.
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