Whole genome sequencing identifies associations for nonsyndromic sagittal craniosynostosis with the intergenic region of BMP2 and noncoding RNA gene LINC01428

April 2024

Authors:
Anthony M. Musolf, Cristina M. Justice, Zeynep Erdogan-Yildirim, Seppe Goovaerts, Araceli Cuellar, John R. Shaffer, Mary L. Marazita, Peter Claes, Seth M. Weinberg, Jae Li, Craig Senders, Marike Zwienenberg, Emil Simeonov, Radka Kaneva, Tony Roscioli, Lorena Di Pietro, Marta Barba, Wanda Lattanzi, Michael L. Cunningham, Paul A. Romitti & Simeon A. Boyadjiev

Abstract:
“Craniosynostosis (CS) is a major birth defect resulting from premature fusion of cranial sutures. Nonsyndromic CS occurs more frequently than syndromic CS, with sagittal nonsyndromic craniosynostosis (sNCS) presenting as the most common CS phenotype. Previous genome-wide association and targeted sequencing analyses of sNCS have identified multiple associated loci, with the strongest association on chromosome 20. Herein, we report the first whole-genome sequencing study of sNCS using 63 proband-parent trios. Sequencing data for these trios were analyzed using the transmission disequilibrium test (TDT) and rare variant TDT (rvTDT) to identify high-risk rare gene variants. Sequencing data were also examined for copy number variants (CNVs) and de novo variants. TDT analysis identified a highly significant locus at 20p12.3, localized to the intergenic region between BMP2 and the noncoding RNA gene LINC01428. Three variants (rs6054763, rs6054764, rs932517) were identified as potential causal variants due to their probability of being transcription factor binding sites, deleterious combined annotation dependent depletion scores, and high minor allele enrichment in probands. Morphometric analysis of cranial vault shape in an unaffected cohort validated the effect of these three single nucleotide variants (SNVs) on dolichocephaly. No genome-wide significant rare variants, de novo loci, or CNVs were identified. Future efforts to identify risk variants for sNCS should include sequencing of larger and more diverse population samples and increased omics analyses, such as RNA-seq and ATAC-seq. “

Sage Science Products:
PippinHT was used to size select whole genome libraries for Oxford Nanopore Promethion sequencing.

Methods Excerpt:
“…3–5 µg of genomic DNA was sheared using a Megaruptor 3 (Diagenode) and purified using Ampure XP beads. Sheared DNA was size selected using the PippinHT instrument (Sage Science) with a target range of 16–20 kb fragments. Next, 1 µg of fragmented, purified, and size-selected DNA in a volume of 47 µl was used in the SQK-LSK109 library preparation protocol per manufacturer’s instructions (Oxford Nanopore Technologies). DNA was end-repaired using the NEBNext FFPE DNA Repair Mix and NEBNext Ultra II End Repair/dA-tailing modules, followed by purification with AMPure XP beads (1:1 vol ratio) and elution to a final volume of 60 µl. Adapters were ligated, and the final library resuspended in Long Fragment Buffer (Oxford Nanopore Technologies). The resulting final library yield was 1.2–2.2 µg per specimen. Libraries were loaded onto PromethION Flowcells (R9.4.1) with 20 femtomolar (fM) loading. After 24 h, all specimens were nuclease washed and reloaded with 20 fM of library. Total sequencing run time was 72 h.”

Author Affiliations:
Statistical Genetics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health (NIH), Baltimore, MD
Neurobehavioral Clinical Research Section, Social and Behavioral Research Branch, National Human Genome Research Institute, National Institutes of Health (NIH), Bethesda, MD
Center for Craniofacial and Dental Genetics, Department of Oral and Craniofacial Sciences, School of Dental Medicine, University of Pittsburgh, Pittsburgh, PA
Department of Human Genetics, KU Leuven, Leuven, Belgium
Department of Electrical Engineering, ESAT-PSI, KU Leuven, Leuven, Belgium
Medical Imaging Research Center, University Hospitals Leuven, Leuven, Belgium
Department of Pediatrics, University of California Davis, Sacramento, CA
Department of Human Genetics, School of Public Health, University of Pittsburgh, Pittsburgh, PA
Bioinformatics Core, Genome Center, University of California Davis, Davis, CA
Department of Otolaryngology, Head and Neck Surgery, University of California Davis, Sacramento, CA
Department of Neurosurgery, University of California Davis, Sacramento, CA
Pediatric Clinic, Alexandrovska University Hospital, Medical University of Sofia, 1431, Sofia, Bulgaria
Molecular Medicine Center, Department of Medical Chemistry and Biochemistry, Medical Faculty, Medical University of Sofia, 1431, Sofia, Bulgaria
Neuroscience Research Australia, University of New South Wales, Sydney, Australia
Department of Life Sciences and Public Health, Università Cattolica del Sacro Cuore, 00168, Rome, Italy
Fondazione Policlinico Universitario A. Gemelli, IRCCS, 00168, Rome, Italy
Seattle Children’s Craniofacial Center, Center of Developmental Biology and Regenerative Medicine and Division of Craniofacial Medicine, Department of Pediatrics, University of Washington, Seattle, WA
Department of Epidemiology, College of Public Health, The University of Iowa, Iowa City, IA

Nature Scientific Reports
DOI:10.1038/s41598-024-58343-w

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