IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-53689-1.html
   My bibliography  Save this article

Genetic risk factors underlying white matter hyperintensities and cortical atrophy

Author

Listed:
  • Yash Patel

    (Toronto
    Toronto)

  • Jean Shin

    (Toronto
    Toronto)

  • Eeva Sliz

    (University of Oulu)

  • Ariana Tang

    (Toronto
    Toronto)

  • Aniket Mishra

    (UMR1219)

  • Rui Xia

    (The University of Texas Health Science Center at Houston)

  • Edith Hofer

    (Statistik und Dokumentation
    Medical University of Graz)

  • Hema Sekhar Reddy Rajula

    (UMR1219)

  • Ruiqi Wang

    (Boston University School of Public Health)

  • Frauke Beyer

    (UMR1219
    Max Planck Institute for Human Cognitive and Brain Sciences)

  • Katrin Horn

    (Statistics and Epidemiology; Leipzig University)

  • Max Riedl

    (Statistics and Epidemiology; Leipzig University)

  • Jing Yu

    (Erasmus MC University Medical Center Rotterdam
    Erasmus MC University Medical Center Rotterdam)

  • Henry Völzke

    (University Medicine Greifswald)

  • Robin Bülow

    (University Medicine Greifswald)

  • Uwe Völker

    (University Medicine Greifswald)

  • Stefan Frenzel

    (University Medicine Greifswald)

  • Katharina Wittfeld

    (University Medicine Greifswald)

  • Sandra Auwera

    (University Medicine Greifswald
    Site Rostock/Greifswald)

  • Thomas H. Mosley

    (The University of Mississippi Medical Center)

  • Vincent Bouteloup

    (UMR1219
    Pôle Santé Publique)

  • Jean-Charles Lambert

    (University of Lille)

  • Geneviève Chêne

    (UMR1219
    CHU de Bordeaux)

  • Carole Dufouil

    (UMR1219)

  • Christophe Tzourio

    (UMR1219
    CHU de Bordeaux)

  • Jean-François Mangin

    (Baobab)

  • Rebecca F. Gottesman

    (National Institute of Neurological Disorders and Stroke Intramural Research Program)

  • Myriam Fornage

    (The University of Texas Health Science Center at Houston)

  • Reinhold Schmidt

    (Medical University of Graz)

  • Qiong Yang

    (Boston University School of Public Health)

  • Veronica Witte

    (Max Planck Institute for Human Cognitive and Brain Sciences)

  • Markus Scholz

    (Statistics and Epidemiology; Leipzig University)

  • Markus Loeffler

    (Statistics and Epidemiology; Leipzig University
    Leipzig Research Centre for Civilization Diseases; Leipzig University)

  • Gennady V. Roshchupkin

    (Erasmus MC University Medical Center Rotterdam
    Erasmus MC University Medical Center Rotterdam)

  • M. Arfan Ikram

    (Erasmus MC University Medical Center Rotterdam)

  • Hans J. Grabe

    (University Medicine Greifswald
    University Medicine Greifswald)

  • Sudha Seshadri

    (University of Texas)

  • Stephanie Debette

    (UMR1219
    Institute for Neurodegenerative Diseases)

  • Tomas Paus

    (University of Montreal
    University of Montreal
    McGill University
    ECOGENE-21)

  • Zdenka Pausova

    (Toronto
    Toronto
    University of Montreal
    ECOGENE-21)

Abstract

White matter hyperintensities index structural abnormalities in the cerebral white matter, including axonal damage. The latter may promote atrophy of the cerebral cortex, a key feature of dementia. Here, we report a study of 51,065 individuals from 10 cohorts demonstrating that higher white matter hyperintensity volume associates with lower cortical thickness. The meta-GWAS of white matter hyperintensities-associated cortical ‘atrophy’ identifies 20 genome-wide significant loci, and enrichment in genes specific to vascular cell types, astrocytes, and oligodendrocytes. White matter hyperintensities-associated cortical ‘atrophy’ showed positive genetic correlations with vascular-risk traits and plasma biomarkers of neurodegeneration, and negative genetic correlations with cognitive functioning. 15 of the 20 loci regulated the expression of 54 genes in the cerebral cortex that, together with their co-expressed genes, were enriched in biological processes of axonal cytoskeleton and intracellular transport. The white matter hyperintensities-cortical thickness associations were most pronounced in cortical regions with higher expression of genes specific to excitatory neurons with long-range axons traversing through the white matter. The meta-GWAS-based polygenic risk score predicts vascular and all-cause dementia in an independent sample of 500,348 individuals. Thus, the genetics of white matter hyperintensities-related cortical atrophy involves vascular and neuronal processes and increases dementia risk.

Suggested Citation

  • Yash Patel & Jean Shin & Eeva Sliz & Ariana Tang & Aniket Mishra & Rui Xia & Edith Hofer & Hema Sekhar Reddy Rajula & Ruiqi Wang & Frauke Beyer & Katrin Horn & Max Riedl & Jing Yu & Henry Völzke & Rob, 2024. "Genetic risk factors underlying white matter hyperintensities and cortical atrophy," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53689-1
    DOI: 10.1038/s41467-024-53689-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-53689-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-53689-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Muralidharan Sargurupremraj & Hideaki Suzuki & Xueqiu Jian & Chloé Sarnowski & Tavia E. Evans & Joshua C. Bis & Gudny Eiriksdottir & Saori Sakaue & Natalie Terzikhan & Mohamad Habes & Wei Zhao & Nicol, 2020. "Cerebral small vessel disease genomics and its implications across the lifespan," Nature Communications, Nature, vol. 11(1), pages 1-18, December.
    2. Michael J. Hawrylycz & Ed S. Lein & Angela L. Guillozet-Bongaarts & Elaine H. Shen & Lydia Ng & Jeremy A. Miller & Louie N. van de Lagemaat & Kimberly A. Smith & Amanda Ebbert & Zackery L. Riley & Chr, 2012. "An anatomically comprehensive atlas of the adult human brain transcriptome," Nature, Nature, vol. 489(7416), pages 391-399, September.
    3. Tian Ge & Chia-Yen Chen & Yang Ni & Yen-Chen Anne Feng & Jordan W. Smoller, 2019. "Polygenic prediction via Bayesian regression and continuous shrinkage priors," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    4. Rebecca D. Hodge & Trygve E. Bakken & Jeremy A. Miller & Kimberly A. Smith & Eliza R. Barkan & Lucas T. Graybuck & Jennie L. Close & Brian Long & Nelson Johansen & Osnat Penn & Zizhen Yao & Jeroen Egg, 2019. "Conserved cell types with divergent features in human versus mouse cortex," Nature, Nature, vol. 573(7772), pages 61-68, September.
    5. Hanchuan Peng & Peng Xie & Lijuan Liu & Xiuli Kuang & Yimin Wang & Lei Qu & Hui Gong & Shengdian Jiang & Anan Li & Zongcai Ruan & Liya Ding & Zizhen Yao & Chao Chen & Mengya Chen & Tanya L. Daigle & R, 2021. "Morphological diversity of single neurons in molecularly defined cell types," Nature, Nature, vol. 598(7879), pages 174-181, October.
    6. Christiaan A de Leeuw & Joris M Mooij & Tom Heskes & Danielle Posthuma, 2015. "MAGMA: Generalized Gene-Set Analysis of GWAS Data," PLOS Computational Biology, Public Library of Science, vol. 11(4), pages 1-19, April.
    7. Vassily Trubetskoy & Antonio F. Pardiñas & Ting Qi & Georgia Panagiotaropoulou & Swapnil Awasthi & Tim B. Bigdeli & Julien Bryois & Chia-Yen Chen & Charlotte A. Dennison & Lynsey S. Hall & Max Lam & K, 2022. "Mapping genomic loci implicates genes and synaptic biology in schizophrenia," Nature, Nature, vol. 604(7906), pages 502-508, April.
    8. Gibran Hemani & Kate Tilling & George Davey Smith, 2017. "Orienting the causal relationship between imprecisely measured traits using GWAS summary data," PLOS Genetics, Public Library of Science, vol. 13(11), pages 1-22, November.
    9. Benjamin B. Sun & Joshua Chiou & Matthew Traylor & Christian Benner & Yi-Hsiang Hsu & Tom G. Richardson & Praveen Surendran & Anubha Mahajan & Chloe Robins & Steven G. Vasquez-Grinnell & Liping Hou & , 2023. "Plasma proteomic associations with genetics and health in the UK Biobank," Nature, Nature, vol. 622(7982), pages 329-338, October.
    10. Mitja I. Kurki & Juha Karjalainen & Priit Palta & Timo P. Sipilä & Kati Kristiansson & Kati M. Donner & Mary P. Reeve & Hannele Laivuori & Mervi Aavikko & Mari A. Kaunisto & Anu Loukola & Elisa Lahtel, 2023. "FinnGen provides genetic insights from a well-phenotyped isolated population," Nature, Nature, vol. 613(7944), pages 508-518, January.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Abolfazl Doostparast Torshizi & Dongnhu T. Truong & Liping Hou & Bart Smets & Christopher D. Whelan & Shuwei Li, 2024. "Proteogenomic network analysis reveals dysregulated mechanisms and potential mediators in Parkinson’s disease," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Ruoyu Tian & Tian Ge & Hyeokmoon Kweon & Daniel B. Rocha & Max Lam & Jimmy Z. Liu & Kritika Singh & Daniel F. Levey & Joel Gelernter & Murray B. Stein & Ellen A. Tsai & Hailiang Huang & Christopher F., 2024. "Whole-exome sequencing in UK Biobank reveals rare genetic architecture for depression," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Eva-Maria Stauffer & Richard A. I. Bethlehem & Lena Dorfschmidt & Hyejung Won & Varun Warrier & Edward T. Bullmore, 2023. "The genetic relationships between brain structure and schizophrenia," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Andras Gezsi & Sandra Auwera & Hannu Mäkinen & Nora Eszlari & Gabor Hullam & Tamas Nagy & Sarah Bonk & Rubèn González-Colom & Xenia Gonda & Linda Garvert & Teemu Paajanen & Zsofia Gal & Kevin Kirchner, 2024. "Unique genetic and risk-factor profiles in clusters of major depressive disorder-related multimorbidity trajectories," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Max Lam & Chia-Yen Chen & W. David Hill & Charley Xia & Ruoyu Tian & Daniel F. Levey & Joel Gelernter & Murray B. Stein & Alexander S. Hatoum & Hailiang Huang & Anil K. Malhotra & Heiko Runz & Tian Ge, 2022. "Collective genomic segments with differential pleiotropic patterns between cognitive dimensions and psychopathology," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    6. Jiwoo Lee & Sakari Jukarainen & Antti Karvanen & Padraig Dixon & Neil M. Davies & George Davey Smith & Pradeep Natarajan & Andrea Ganna, 2023. "Quantifying the causal impact of biological risk factors on healthcare costs," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    7. Anders Mälarstig & Felix Grassmann & Leo Dahl & Marios Dimitriou & Dianna McLeod & Marike Gabrielson & Karl Smith-Byrne & Cecilia E. Thomas & Tzu-Hsuan Huang & Simon K. G. Forsberg & Per Eriksson & Mi, 2023. "Evaluation of circulating plasma proteins in breast cancer using Mendelian randomisation," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    8. Tuomo Hartonen & Bradley Jermy & Hanna Sõnajalg & Pekka Vartiainen & Kristi Krebs & Andrius Vabalas & Tuija Leino & Hanna Nohynek & Jonas Sivelä & Reedik Mägi & Mark Daly & Hanna M. Ollila & Lili Mila, 2023. "Nationwide health, socio-economic and genetic predictors of COVID-19 vaccination status in Finland," Nature Human Behaviour, Nature, vol. 7(7), pages 1069-1083, July.
    9. Mattia Cordioli & Andrea Corbetta & Hanna Maria Kariis & Sakari Jukarainen & Pekka Vartiainen & Tuomo Kiiskinen & Matteo Ferro & Markus Perola & Mikko Niemi & Samuli Ripatti & Kelli Lehto & Lili Milan, 2024. "Socio-demographic and genetic risk factors for drug adherence and persistence across 5 common medication classes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. Bingxin Zhao & Yujue Li & Zirui Fan & Zhenyi Wu & Juan Shu & Xiaochen Yang & Yilin Yang & Xifeng Wang & Bingxuan Li & Xiyao Wang & Carlos Copana & Yue Yang & Jinjie Lin & Yun Li & Jason L. Stein & Joa, 2024. "Eye-brain connections revealed by multimodal retinal and brain imaging genetics," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    11. Dmitrii Usoltsev & Nikita Kolosov & Oxana Rotar & Alexander Loboda & Maria Boyarinova & Ekaterina Moguchaya & Ekaterina Kolesova & Anastasia Erina & Kristina Tolkunova & Valeriia Rezapova & Ivan Molot, 2024. "Complex trait susceptibilities and population diversity in a sample of 4,145 Russians," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    12. Tingting Bo & Jie Li & Ganlu Hu & Ge Zhang & Wei Wang & Qian Lv & Shaoling Zhao & Junjie Ma & Meng Qin & Xiaohui Yao & Meiyun Wang & Guang-Zhong Wang & Zheng Wang, 2023. "Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    13. Mattia Marchi & Anne Alkema & Charley Xia & Chris H. L. Thio & Li-Yu Chen & Winni Schalkwijk & Gian M. Galeazzi & Silvia Ferrari & Luca Pingani & Hyeokmoon Kweon & Sara Evans-Lacko & W. David Hill & M, 2024. "Investigating the impact of poverty on mental illness in the UK Biobank using Mendelian randomization," Nature Human Behaviour, Nature, vol. 8(9), pages 1771-1783, September.
    14. Catherine M. Francis & Matthias E. Futschik & Jian Huang & Wenjia Bai & Muralidharan Sargurupremraj & Alexander Teumer & Monique M. B. Breteler & Enrico Petretto & Amanda S. R. Ho & Philippe Amouyel &, 2022. "Genome-wide associations of aortic distensibility suggest causality for aortic aneurysms and brain white matter hyperintensities," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    15. Yunfeng Huang & Dora Bodnar & Chia-Yen Chen & Gabriela Sanchez-Andrade & Mark Sanderson & Jun Shi & Katherine G. Meilleur & Matthew E. Hurles & Sebastian S. Gerety & Ellen A. Tsai & Heiko Runz, 2023. "Rare genetic variants impact muscle strength," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    16. Biao Zhang & Shuqin Zhang & Shihua Zhang, 2024. "Whole brain alignment of spatial transcriptomics between humans and mice with BrainAlign," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    17. Chachrit Khunsriraksakul & Qinmengge Li & Havell Markus & Matthew T. Patrick & Renan Sauteraud & Daniel McGuire & Xingyan Wang & Chen Wang & Lida Wang & Siyuan Chen & Ganesh Shenoy & Bingshan Li & Xue, 2023. "Multi-ancestry and multi-trait genome-wide association meta-analyses inform clinical risk prediction for systemic lupus erythematosus," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    18. Danielle Rasooly & Gina M. Peloso & Alexandre C. Pereira & Hesam Dashti & Claudia Giambartolomei & Eleanor Wheeler & Nay Aung & Brian R. Ferolito & Maik Pietzner & Eric H. Farber-Eger & Quinn Stanton , 2023. "Genome-wide association analysis and Mendelian randomization proteomics identify drug targets for heart failure," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    19. Eamon Fitzgerald & Mojun Shen & Hannah Ee Juen Yong & Zihan Wang & Irina Pokhvisneva & Sachin Patel & Nicholas O’Toole & Shiao-Yng Chan & Yap Seng Chong & Helen Chen & Peter D. Gluckman & Jerry Chan &, 2023. "Hofbauer cell function in the term placenta associates with adult cardiovascular and depressive outcomes," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    20. Santiago Diaz-Torres & Samantha Sze-Yee Lee & Luis M. García-Marín & Adrian I. Campos & Garreth Lingham & Jue-Sheng Ong & David A. Mackey & Kathryn P. Burdon & Michael Hunter & Xianjun Dong & Stuart M, 2024. "Uncovering genetic loci and biological pathways associated with age-related cataracts through GWAS meta-analysis," Nature Communications, Nature, vol. 15(1), pages 1-10, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53689-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.