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A variant near DHCR24 associates with microstructural properties of white matter and peripheral lipid metabolism in adolescents

Molecular Psychiatry volume 26, pages 3795–3805 (2021)Cite this article

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Abstract

Visceral adiposity has been associated with altered microstructural properties of white matter in adolescents. Previous evidence suggests that circulating phospholipid PC(16:0/2:0) may mediate this association. To investigate the underlying biology, we performed a genome-wide association study (GWAS) of the shared variance of visceral fat, PC(16:0/2:0), and white matter microstructure in 872 adolescents from the Saguenay Youth Study. We further studied the metabolomic profile of the GWAS-lead variant in 931 adolescents. Visceral fat and white matter microstructure were assessed with magnetic resonance imaging. Circulating metabolites were quantified with serum lipidomics and metabolomics. We identified a genome-wide significant association near DHCR24 (Seladin-1) encoding a cholesterol-synthesizing enzyme (rs588709, p = 3.6 × 10−8); rs588709 was also associated nominally with each of the three traits (white matter microstructure: p = 2.1 × 10−6, PC(16:0/2:0): p = 0.005, visceral fat: p = 0.010). We found that the metabolic profile associated with rs588709 resembled that of a TM6SF2 variant impacting very low-density lipoprotein (VLDL) secretion and was only partially similar to that of a HMGCR variant. This suggests that the effect of rs588709 on VLDL lipids may arise due to altered phospholipid rather than cholesterol metabolism. The rs588709 was also nominally associated with circulating concentrations of omega-3 fatty acids in interaction with visceral fat and PC(16:0/2:0), and these fatty acid measures showed robust associations with white matter microstructure. Overall, the present study provides evidence that the DHCR24 locus may link peripheral metabolism to brain microstructure, an association with implications for cognitive impairment.

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Fig. 1: The genome-wide significant locus on chromosome 1 near DHCR24.
Fig. 2: Expression of DHCR24 during lifespan.
Fig. 3: The effects of the DHCR24 rs588709-G on particle concentration of 14 lipoprotein subclasses and the lipid fractions within the 14 subclasses.
Fig. 4: The effects of the DHCR24 rs588709-G on lipoprotein particle size, apolipoproteins, cholesterol, triglycerides, phospholipids, amino acids, and glycoprotein acetylation.
Fig. 5: The overall similarities of the metabolomic effects of DHCR24 rs588709-G versus TM6SF2 rs58542926-T or HMGCR rs12916-T.

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Acknowledgements

The authors thank the following individuals for their contributions in data acquisition and storage in the SYS: Manon Bernard (database architect, The Hospital for Sick Children), Hélène Simard and her team of research assistants (Cégep de Jonquière), and Jacynthe Tremblay and her team of research nurses (Chicoutimi Hospital). The authors thank all participants who took part in the Saguenay Youth Study. The Genotype-Tissue Expression (GTEx) Project was supported by the Common Fund of the Office of the Director of the National Institutes of Health, and by NCI, NHGRI, NHLBI, NIDA, NIMH, and NINDS. The data used for the analyses described in this manuscript were obtained from the GTEx Portal on 04/01/2019 and dbGaP accession number phs000424.v7.p2 on 04/01/2019.

Funding

The Saguenay Youth Study has been funded by the Canadian Institutes of Health Research (TP and ZP), Heart and Stroke Foundation of Canada (ZP), Canadian Foundation for Innovation (ZP), and National Institutes for Health (ZP).

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Authors and Affiliations

  1. The Hospital for Sick Children, University of Toronto, Toronto, ON, Canada

    Eeva Sliz, Jean Shin, Catriona Syme & Zdenka Pausova

  2. Departments of Physiology and Nutritional Sciences, University of Toronto, Toronto, ON, Canada

    Eeva Sliz, Jean Shin, Catriona Syme & Zdenka Pausova

  3. Center for Life-Course Health Research and Computational Medicine, Faculty of Medicine, University of Oulu, and Biocenter Oulu, Oulu, Finland

    Eeva Sliz

  4. Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, ON, Canada

    Yash Patel, Nadine Parker & Tomas Paus

  5. Department of Health Sciences, Université du Québec à Chicoutimi, Chicoutimi, QC, Canada

    Louis Richer

  6. Clinical Lipidology and rare lipid disorders Unit, Community Genetic Medicine Center, Department of Medicine, Université de Montréal, ECOGENE-21, Chicoutimi, QC, Canada

    Daniel Gaudet

  7. Neural Regeneration Laboratory, Ottawa Institute of Systems Biology, University of Ottawa, Ottawa, ON, Canada

    Steffany Bennett

  8. Departments of Psychology and Psychiatry, University of Toronto, Toronto, ON, Canada

    Tomas Paus

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Sliz, E., Shin, J., Syme, C. et al. A variant near DHCR24 associates with microstructural properties of white matter and peripheral lipid metabolism in adolescents. Mol Psychiatry 26, 3795–3805 (2021). https://doi.org/10.1038/s41380-019-0640-9

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