Uncovering the Neurogenetic Program of 2q37 Syndrome by Integrative Genomics and Cerebral Organoids
Joshua Fedorko1, Fumihiro Watanabe2, Jaime Imitola2
1Laboratory for Neural Stem Cells and Functional Neurogenetics, Division of Multiple Sclerosis and Neuroimmunology and Comprehensive MS Center, University of Connecticut Health Center, Farmington, CT 06030. Frank H. Netter SOM, 2Laboratory for Neural Stem Cells and Functional Neurogenetics, Division of Multiple Sclerosis and Neuroimmunology and Comprehensive MS Center, University of Connecticut Health Center, Farmington, CT 06030.
Objective:

To perform a  deep genomic analysis of the entire 2q37 segment to find genes involved in neuronal dysfunction.

Background:
2q37 deletion syndrome  is a rare syndrome characterized by multiple phenotypic features including bone, cardiovascular alterations, neurodevelopmental including autism and microcephaly. Despite attempts to define genotype-phenotype correlation, the genes responsible for neurological phenotypes are unknown. In the past,  we identified a 486kb deletion in a patient with microcephaly and hypoplasia of the corpus callosum pointing to a  genomic region in distal 2q37 with multiple CNS genes.
Design/Methods:

We use the Allen brain Atlas developmental  framework from 8 weeks to 40 years of age. Guilt-by association survey of genomic neighbors by pearson correlation of RNAseq data. We used the Decipher Clinical genome database to correlate the reported genomic alterations of selected genes.  We use human cerebral organoids to perform scRNAseq and confocal imaging of immunohistochemistry to examine expression to confirm candidates  in cerebral organoids at 70 days in culture.

Results:
We performed clustering of more than 80 genes that showed four different developmental clusters that correlated with increased expression in the human brain, we found PTMA, KIF1A and SEPT2 showing high expression in all data sets and in a variety of neuronal cell types from interneurons to neuroepithelial cells using scRNAseq. Organoid staining with IHC showed that PTMA and SEPT2 had high expression  in cortical progenitors The expression pattern in the cortex shows that many of the highly expressed genes in 2q37are expressed in  inhibitory neurons and may explain the hyperexcitability seen in 2q37 patients. We found an increased number of single nucleotide variants in KIF1A associated with multiple neurological phenotypes
Conclusions:

The results showed that KIF1A, SEPT2 and PTMA are genes with high confidence to play a distinct function in brain development and 2q37 deletion syndrome.

10.1212/WNL.0000000000206503