. 2021 Sep;53(9):1276-1282.

doi: 10.1038/s41588-021-00921-z. Epub 2021 Sep 7.

A genome-wide association study with 1,126,563 individuals identifies new risk loci for Alzheimer's disease

Douglas P Wightman¹, Iris E Jansen¹, Jeanne E Savage¹, Alexey A Shadrin^{2

3}, Shahram Bahrami^{2

3

4}, Dominic Holland⁵, Arvid Rongve^{6

7}, Sigrid Børte^{3

8

9}, Bendik S Winsvold^{9

10

11}, Ole Kristian Drange^{12

13}, Amy E Martinsen^{3

9

10}, Anne Heidi Skogholt^{9

14}, Cristen Willer¹⁵, Geir Bråthen^{16

17

18}, Ingunn Bosnes^{12

19}, Jonas Bille Nielsen^{9

15

20}, Lars G Fritsche²¹, Laurent F Thomas^{9

14}, Linda M Pedersen¹⁰, Maiken E Gabrielsen⁹, Marianne Bakke Johnsen^{3

8

9}, Tore Wergeland Meisingset^{16

17}, Wei Zhou^{22

23}, Petroula Proitsi²⁴, Angela Hodges²⁴, Richard Dobson^{25

26

27

28

29}, Latha Velayudhan²⁴, Karl Heilbron³⁰, Adam Auton³⁰; 23andMe Research Team; Julia M Sealock^{31

32}, Lea K Davis^{31

32}, Nancy L Pedersen³³, Chandra A Reynolds³⁴, Ida K Karlsson^{33

35}, Sigurdur Magnusson³⁶, Hreinn Stefansson³⁶, Steinunn Thordardottir³⁷, Palmi V Jonsson^{37

38}, Jon Snaedal³⁷, Anna Zettergren³⁹, Ingmar Skoog^{39

40}, Silke Kern^{39

40}, Margda Waern^{39

41}, Henrik Zetterberg^{42

43

44

45}, Kaj Blennow^{44

45}, Eystein Stordal^{12

19}, Kristian Hveem^{9

46}, John-Anker Zwart^{3

9

10}, Lavinia Athanasiu^{2

4}, Per Selnes⁴⁷, Ingvild Saltvedt^{16

18}, Sigrid B Sando^{16

17}, Ingun Ulstein⁴⁸, Srdjan Djurovic^{49

50}, Tormod Fladby^{3

47}, Dag Aarsland^{24

51}, Geir Selbæk^{3

48

52}, Stephan Ripke^{23

53

54}, Kari Stefansson³⁶, Ole A Andreassen^#^{2

3

4}, Danielle Posthuma^#^{55

56}

Collaborators, Affiliations

Collaborators

23andMe Research Team:
Michelle Agee, Stella Aslibekyan, Elizabeth Babalola, Robert K Bell, Jessica Bielenberg, Katarzyna Bryc, Emily Bullis, Briana Cameron, Daniella Coker, Gabriel Cuellar Partida, Devika Dhamija, Sayantan Das, Sarah L Elson, Teresa Filshtein, Kipper Fletez-Brant, Pierre Fontanillas, Will Freyman, Pooja M Gandhi, Barry Hicks, David A Hinds, Karen E Huber, Ethan M Jewett, Yunxuan Jiang, Aaron Kleinman, Katelyn Kukar, Vanessa Lane, Keng-Han Lin, Maya Lowe, Marie K Luff, Jey C McCreight, Matthew H McIntyre, Kimberly F McManus, Steven J Micheletti, Meghan E Moreno, Joanna L Mountain, Sahar V Mozaffari, Priyanka Nandakumar, Elizabeth S Noblin, Jared O'Connell, Aaron A Petrakovitz, G David Poznik, Morgan Schumacher, Anjali J Shastri, Janie F Shelton, Jingchunzi Shi, Suyash Shringarpure, Chao Tian, Vinh Tran, Joyce Y Tung, Xin Wang, Wei Wang, Catherine H Weldon, Peter Wilton

Affiliations

¹ Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU Amsterdam, Amsterdam, the Netherlands.
² NORMENT Centre, University of Oslo, Oslo, Norway.
³ Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
⁴ Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.
⁵ Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA.
⁶ Department of Research and Innovation, Helse Fonna, Haugesund Hospital, Haugesund, Norway.
⁷ The University of Bergen, Institute of Clinical Medicine (K1), Bergen, Norway.
⁸ Research and Communication Unit for Musculoskeletal Health (FORMI), Department of Research, Innovation and Education, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway.
⁹ K. G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway.
¹⁰ Department of Research, Innovation and Education, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway.
¹¹ Department of Neurology, Oslo University Hospital, Oslo, Norway.
¹² Department of Mental Health, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway.
¹³ Division of Mental Health Care, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway.
¹⁴ Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway.
¹⁵ Department of Internal Medicine, Division of Cardiovascular Medicine, University of Michigan, Ann Arbor, MI, USA.
¹⁶ Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology, Trondheim, Norway.
¹⁷ Department of Neurology and Clinical Neurophysiology, University Hospital of Trondheim, Trondheim, Norway.
¹⁸ Department of Geriatrics, St. Olav's Hospital, Trondheim University Hospital, Trondheim, Norway.
¹⁹ Department of Psychiatry, Hospital Namsos, Nord-Trøndelag Health Trust, Namsos, Norway.
²⁰ Department of Epidemiology Research, Statens Serum Institut, Copenhagen, Denmark.
²¹ Center for Statistical Genetics, Department of Biostatistics, University of Michigan, Ann Arbor, MI, USA.
²² Department of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI, USA.
²³ Analytic and Translational Genetics Unit, Massachusetts General Hospital, Boston, MA, USA.
²⁴ Institute of Psychiatry Psychology and Neurosciences, King's College London, London, UK.
²⁵ Department of Biostatistics and Health Informatics, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, UK.
²⁶ NIHR Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London, London, UK.
²⁷ Health Data Research UK London, University College London, London, UK.
²⁸ Institute of Health Informatics, University College London, London, UK.
²⁹ NIHR Biomedical Research Centre at University College London Hospitals NHS Foundation Trust, London, UK.
³⁰ 23andMe Inc., Sunnyvale, CA, USA.
³¹ Division of Genetic Medicine, Department of Medicine Vanderbilt University Medical Center Nashville, Nashville, TN, USA.
³² Vanderbilt Genetics Institute, Vanderbilt University Medical Center, Nashville, TN, USA.
³³ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
³⁴ Department of Psychology, University of California-Riverside, Riverside, CA, USA.
³⁵ Institute of Gerontology and Aging Research Network - Jönköping (ARN-J), School of Health and Welfare, Jönköping University, Jönköping, Sweden.
³⁶ deCODE Genetics/Amgen, Reykjavik, Iceland.
³⁷ Department of Geriatric Medicine, Landspitali University Hospital, Reykjavik, Iceland.
³⁸ Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
³⁹ Neuropsychiatric Epidemiology Unit, Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, the Sahlgrenska Academy, Centre for Ageing and Health (AGECAP) at the University of Gothenburg, Gothenburg, Sweden.
⁴⁰ Region Västra Götaland, Sahlgrenska University Hospital, Psychiatry, Cognition and Old Age Psychiatry Clinic, Gothenburg, Sweden.
⁴¹ Region Västra Götaland, Sahlgrenska University Hospital, Psychosis Clinic, Gothenburg, Sweden.
⁴² Department of Neurodegenerative Disease, UCL Institute of Neurology, London, UK.
⁴³ UK Dementia Research Institute at UCL, London, UK.
⁴⁴ Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden.
⁴⁵ Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden.
⁴⁶ HUNT Research Center, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway.
⁴⁷ Department of Neurology, Akershus University Hospital, Lørenskog, Norway.
⁴⁸ Department of Geriatric Medicine, Oslo University Hospital, Oslo, Norway.
⁴⁹ Department of Medical Genetics, Oslo University Hospital, Oslo, Norway.
⁵⁰ NORMENT, Department of Clinical Science, University of Bergen, Bergen, Norway.
⁵¹ Centre of Age-Related Medicine, Stavanger University Hospital, Stavanger, Norway.
⁵² Norwegian National Advisory Unit on Ageing and Health, Vestfold Hospital Trust, Tønsberg, Norway.
⁵³ Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
⁵⁴ Department of Psychiatry and Psychotherapy, Charité-Universitätsmedizin, Berlin, Germany.
⁵⁵ Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU Amsterdam, Amsterdam, the Netherlands. d.posthuma@vu.nl.
⁵⁶ Department of Child and Adolescent Psychiatry and Pediatric Psychology, Section Complex Trait Genetics, Amsterdam Neuroscience, Vrije Universiteit Medical Center, Amsterdam University Medical Center, Amsterdam, the Netherlands. d.posthuma@vu.nl.

^# Contributed equally.

PMID: 34493870
PMCID: PMC10243600
DOI: 10.1038/s41588-021-00921-z

A genome-wide association study with 1,126,563 individuals identifies new risk loci for Alzheimer's disease

Douglas P Wightman et al. Nat Genet. 2021 Sep.

. 2021 Sep;53(9):1276-1282.

doi: 10.1038/s41588-021-00921-z. Epub 2021 Sep 7.

Authors

Collaborators

23andMe Research Team:
Michelle Agee, Stella Aslibekyan, Elizabeth Babalola, Robert K Bell, Jessica Bielenberg, Katarzyna Bryc, Emily Bullis, Briana Cameron, Daniella Coker, Gabriel Cuellar Partida, Devika Dhamija, Sayantan Das, Sarah L Elson, Teresa Filshtein, Kipper Fletez-Brant, Pierre Fontanillas, Will Freyman, Pooja M Gandhi, Barry Hicks, David A Hinds, Karen E Huber, Ethan M Jewett, Yunxuan Jiang, Aaron Kleinman, Katelyn Kukar, Vanessa Lane, Keng-Han Lin, Maya Lowe, Marie K Luff, Jey C McCreight, Matthew H McIntyre, Kimberly F McManus, Steven J Micheletti, Meghan E Moreno, Joanna L Mountain, Sahar V Mozaffari, Priyanka Nandakumar, Elizabeth S Noblin, Jared O'Connell, Aaron A Petrakovitz, G David Poznik, Morgan Schumacher, Anjali J Shastri, Janie F Shelton, Jingchunzi Shi, Suyash Shringarpure, Chao Tian, Vinh Tran, Joyce Y Tung, Xin Wang, Wei Wang, Catherine H Weldon, Peter Wilton

Affiliations

¹ Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU Amsterdam, Amsterdam, the Netherlands.
² NORMENT Centre, University of Oslo, Oslo, Norway.
³ Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
⁴ Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.
⁵ Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA.
⁶ Department of Research and Innovation, Helse Fonna, Haugesund Hospital, Haugesund, Norway.
⁷ The University of Bergen, Institute of Clinical Medicine (K1), Bergen, Norway.
⁸ Research and Communication Unit for Musculoskeletal Health (FORMI), Department of Research, Innovation and Education, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway.
⁹ K. G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway.
¹⁰ Department of Research, Innovation and Education, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway.
¹¹ Department of Neurology, Oslo University Hospital, Oslo, Norway.
¹² Department of Mental Health, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway.
¹³ Division of Mental Health Care, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway.
¹⁴ Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway.
¹⁵ Department of Internal Medicine, Division of Cardiovascular Medicine, University of Michigan, Ann Arbor, MI, USA.
¹⁶ Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology, Trondheim, Norway.
¹⁷ Department of Neurology and Clinical Neurophysiology, University Hospital of Trondheim, Trondheim, Norway.
¹⁸ Department of Geriatrics, St. Olav's Hospital, Trondheim University Hospital, Trondheim, Norway.
¹⁹ Department of Psychiatry, Hospital Namsos, Nord-Trøndelag Health Trust, Namsos, Norway.
²⁰ Department of Epidemiology Research, Statens Serum Institut, Copenhagen, Denmark.
²¹ Center for Statistical Genetics, Department of Biostatistics, University of Michigan, Ann Arbor, MI, USA.
²² Department of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI, USA.
²³ Analytic and Translational Genetics Unit, Massachusetts General Hospital, Boston, MA, USA.
²⁴ Institute of Psychiatry Psychology and Neurosciences, King's College London, London, UK.
²⁵ Department of Biostatistics and Health Informatics, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, UK.
²⁶ NIHR Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London, London, UK.
²⁷ Health Data Research UK London, University College London, London, UK.
²⁸ Institute of Health Informatics, University College London, London, UK.
²⁹ NIHR Biomedical Research Centre at University College London Hospitals NHS Foundation Trust, London, UK.
³⁰ 23andMe Inc., Sunnyvale, CA, USA.
³¹ Division of Genetic Medicine, Department of Medicine Vanderbilt University Medical Center Nashville, Nashville, TN, USA.
³² Vanderbilt Genetics Institute, Vanderbilt University Medical Center, Nashville, TN, USA.
³³ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
³⁴ Department of Psychology, University of California-Riverside, Riverside, CA, USA.
³⁵ Institute of Gerontology and Aging Research Network - Jönköping (ARN-J), School of Health and Welfare, Jönköping University, Jönköping, Sweden.
³⁶ deCODE Genetics/Amgen, Reykjavik, Iceland.
³⁷ Department of Geriatric Medicine, Landspitali University Hospital, Reykjavik, Iceland.
³⁸ Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
³⁹ Neuropsychiatric Epidemiology Unit, Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, the Sahlgrenska Academy, Centre for Ageing and Health (AGECAP) at the University of Gothenburg, Gothenburg, Sweden.
⁴⁰ Region Västra Götaland, Sahlgrenska University Hospital, Psychiatry, Cognition and Old Age Psychiatry Clinic, Gothenburg, Sweden.
⁴¹ Region Västra Götaland, Sahlgrenska University Hospital, Psychosis Clinic, Gothenburg, Sweden.
⁴² Department of Neurodegenerative Disease, UCL Institute of Neurology, London, UK.
⁴³ UK Dementia Research Institute at UCL, London, UK.
⁴⁴ Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden.
⁴⁵ Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden.
⁴⁶ HUNT Research Center, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway.
⁴⁷ Department of Neurology, Akershus University Hospital, Lørenskog, Norway.
⁴⁸ Department of Geriatric Medicine, Oslo University Hospital, Oslo, Norway.
⁴⁹ Department of Medical Genetics, Oslo University Hospital, Oslo, Norway.
⁵⁰ NORMENT, Department of Clinical Science, University of Bergen, Bergen, Norway.
⁵¹ Centre of Age-Related Medicine, Stavanger University Hospital, Stavanger, Norway.
⁵² Norwegian National Advisory Unit on Ageing and Health, Vestfold Hospital Trust, Tønsberg, Norway.
⁵³ Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
⁵⁴ Department of Psychiatry and Psychotherapy, Charité-Universitätsmedizin, Berlin, Germany.
⁵⁵ Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU Amsterdam, Amsterdam, the Netherlands. d.posthuma@vu.nl.
⁵⁶ Department of Child and Adolescent Psychiatry and Pediatric Psychology, Section Complex Trait Genetics, Amsterdam Neuroscience, Vrije Universiteit Medical Center, Amsterdam University Medical Center, Amsterdam, the Netherlands. d.posthuma@vu.nl.

^# Contributed equally.

PMID: 34493870
PMCID: PMC10243600
DOI: 10.1038/s41588-021-00921-z

Erratum in

Author Correction: A genome-wide association study with 1,126,563 individuals identifies new risk loci for Alzheimer's disease.
Wightman DP, Jansen IE, Savage JE, Shadrin AA, Bahrami S, Holland D, Rongve A, Børte S, Winsvold BS, Drange OK, Martinsen AE, Skogholt AH, Willer C, Bråthen G, Bosnes I, Nielsen JB, Fritsche LG, Thomas LF, Pedersen LM, Gabrielsen ME, Johnsen MB, Meisingset TW, Zhou W, Proitsi P, Hodges A, Dobson R, Velayudhan L, Heilbron K, Auton A; 23andMe Research Team; Sealock JM, Davis LK, Pedersen NL, Reynolds CA, Karlsson IK, Magnusson S, Stefansson H, Thordardottir S, Jonsson PV, Snaedal J, Zettergren A, Skoog I, Kern S, Waern M, Zetterberg H, Blennow K, Stordal E, Hveem K, Zwart JA, Athanasiu L, Selnes P, Saltvedt I, Sando SB, Ulstein I, Djurovic S, Fladby T, Aarsland D, Selbæk G, Ripke S, Stefansson K, Andreassen OA, Posthuma D. Wightman DP, et al. Nat Genet. 2021 Dec;53(12):1722. doi: 10.1038/s41588-021-00977-x. Nat Genet. 2021. PMID: 34773122 No abstract available.
Author Correction: A genome-wide association study with 1,126,563 individuals identifies new risk loci for Alzheimer's disease.
Wightman DP, Jansen IE, Savage JE, Shadrin AA, Bahrami S, Holland D, Rongve A, Børte S, Winsvold BS, Drange OK, Martinsen AE, Skogholt AH, Willer C, Bråthen G, Bosnes I, Nielsen JB, Fritsche LG, Thomas LF, Pedersen LM, Gabrielsen ME, Johnsen MB, Meisingset TW, Zhou W, Proitsi P, Hodges A, Dobson R, Velayudhan L, Heilbron K, Auton A; 23andMe Research Team; Sealock JM, Davis LK, Pedersen NL, Reynolds CA, Karlsson IK, Magnusson S, Stefansson H, Thordardottir S, Jonsson PV, Snaedal J, Zettergren A, Skoog I, Kern S, Waern M, Zetterberg H, Blennow K, Stordal E, Hveem K, Zwart JA, Athanasiu L, Selnes P, Saltvedt I, Sando SB, Ulstein I, Djurovic S, Fladby T, Aarsland D, Selbæk G, Ripke S, Stefansson K, Andreassen OA, Posthuma D. Wightman DP, et al. Nat Genet. 2022 Jul;54(7):1062. doi: 10.1038/s41588-022-01126-8. Nat Genet. 2022. PMID: 35726068 No abstract available.

Abstract

Late-onset Alzheimer's disease is a prevalent age-related polygenic disease that accounts for 50-70% of dementia cases. Currently, only a fraction of the genetic variants underlying Alzheimer's disease have been identified. Here we show that increased sample sizes allowed identification of seven previously unidentified genetic loci contributing to Alzheimer's disease. This study highlights microglia, immune cells and protein catabolism as relevant to late-onset Alzheimer's disease, while identifying and prioritizing previously unidentified genes of potential interest. We anticipate that these results can be included in larger meta-analyses of Alzheimer's disease to identify further genetic variants that contribute to Alzheimer's pathology.

PubMed Disclaimer

Conflict of interest statement

Competing Interests Statement

All other authors declare no competing interests.

Figures

**Figure 1:**
A Manhattan plot of the meta-analysis results highlighting 38 loci, including 7 previously unidentified regions. Only variants with a P< 0.0005 are displayed. The *APOE* region cannot be fully observed because the y-axis is limited to the top variant in the second most significant locus, *-log10*(1×10⁻⁶⁰), in order to display the less significant variants. The red line represents genome wide significance (5×10⁻⁸). The P-values were identified through a meta-analysis (two-sided test) of summary statistics generated by linear/logistic regressions (two-sided test) and were not adjusted for multiple testing. The previously unidentified loci are highlighted in green and indicated by the assigned gene name. The *TNIP1*/*HAVCR2* regions and the *NTN5*/*LILRB2* regions are close enough together that they cannot be visually distinguished at this scale but are different genomic risk loci.

See this image and copyright information in PMC

Comment in

Genome-wide association study identifies new risk loci for Alzheimer disease.
Lemprière S. Lemprière S. Nat Rev Neurol. 2021 Nov;17(11):659. doi: 10.1038/s41582-021-00575-9. Nat Rev Neurol. 2021. PMID: 34599319 No abstract available.

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A genome-wide association study with 1,126,563 individuals identifies new risk loci for Alzheimer's disease

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A genome-wide association study with 1,126,563 individuals identifies new risk loci for Alzheimer's disease

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Erratum in

Abstract

Conflict of interest statement

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