Common Genetic Variation Indicates Separate Causes for Periventricular and Deep White Matter Hyperintensities.
| Title: | Common Genetic Variation Indicates Separate Causes for Periventricular and Deep White Matter Hyperintensities. |
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| Authors: | Armstrong NJ; Mathematics and Statistics, Murdoch University, Perth, Australia (N.J.A.).; Mather KA; Centre for Healthy Brain Ageing, School of Psychiatry (K.A.M., W.W., H.B., J.J., A.T., J.T., P.S.S.), University of New South Wales, Sydney, Australia.; Neuroscience Research Australia, Sydney, Australia (K.A.M., P.R.S., A.T.).; Sargurupremraj M; University Bordeaux, Inserm, Bordeaux Population Health Research Center, France (M.S., C.T., S.D.).; Knol MJ; Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands (M.J.K., D.V., N.A., G.V.R., M.W.V., C.M.v.D., M.A.I., H.H.H.A.).; Malik R; Institute for Stroke and Dementia Research (ISD), University Hospital, Ludwig-Maximilians-Universität LMU Munich, Germany (R.M., M.D.).; Satizabal CL; Glenn Biggs Institute for Alzheimer's & Neurodegenerative Diseases, UT Health San Antonio, San Antonio, TX (C.L.S., S.S.).; The Framingham Heart Study, MA (C.L.S., A.S.B., J.R.R., S.S.).; Department of Neurology (C.L.S., A.S.B., J.R.R., S.S.), Boston University School of Medicine, MA.; Yanek LR; GeneSTAR Research Program (L.R.Y., B.G.K., L.C.B., P.A.N.), Johns Hopkins University School of Medicine, Baltimore, MD.; Wen W; Centre for Healthy Brain Ageing, School of Psychiatry (K.A.M., W.W., H.B., J.J., A.T., J.T., P.S.S.), University of New South Wales, Sydney, Australia.; Gudnason VG; Icelandic Heart Association, Kopavogur (V.G.G., S.S.).; University of Iceland, Reykjavik, Iceland (V.G.G., A.V.S.).; Dueker ND; Dr. John T. Macdonald Foundation Department of Human Genetics (R.L.S.), University of Miami, FL.; Elliott LT; Department of Statistics and Actuarial Science, Simon Fraser University, Burnaby, BC, Canada (L.T.E.).; Wellcome Centre for Integrative Neuroimaging (WIN FMRIB) (L.T.E., F.A.-A., L.G., M.J., S.M.S.), University of Oxford, United Kingdom.; Hofer E; Clinical Division of Neurogeriatrics, Department of Neurology, Medical University of Graz, Austria (E.H., R.S.).; Institute for Medical Informatics, Statistics and Documentation, Medical University of Graz, Austria (E.H.).; Bis J; Cardiovascular Health Research Unit, Department of Medicine, University of Washington, Seattle, WA (J.B., B.P., W.L.).; Jahanshad N; Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Marina del Rey (N.J., P.M.T.).; Li S; Department of Biostatistics, Boston University School of Public Health, Boston, MA (S.L., M.A.L., A.S.B., Q.Y.).; Logue MA; Department of Psychiatry and Biomedical Genetics Section (M.A.L.), Boston University School of Medicine, MA.; Department of Biostatistics, Boston University School of Public Health, Boston, MA (S.L., M.A.L., A.S.B., Q.Y.).; National Center for PTSD: Behavioral Science Division, VA Boston Healthcare System, Boston, MA (M.A.L.).; Luciano M; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, United Kingdom (M.L., I.J.D., D.C.M.L., M.E.B., J.M.W.).; Scholz M; Institute for Medical Informatics, Statistics and Epidemiology (M.S.).; Smith AV; University of Iceland, Reykjavik, Iceland (V.G.G., A.V.S.).; Trompet S; Department of Internal Medicine, Section of Gerontology and Geriatrics (S.T.), Leiden University Medical Center, the Netherlands.; Department of Cardiology (S.T.), Leiden University Medical Center, the Netherlands.; Vojinovic D; Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands (M.J.K., D.V., N.A., G.V.R., M.W.V., C.M.v.D., M.A.I., H.H.H.A.).; Xia R; Brown Foundation Institute of Molecular Medicine, McGovern Medical School, University of Texas Health Science Center at Houston, TX (R.X., M.F.).; Alfaro-Almagro F; Wellcome Centre for Integrative Neuroimaging (WIN FMRIB) (L.T.E., F.A.-A., L.G., M.J., S.M.S.), University of Oxford, United Kingdom.; Ames D; National Ageing Research Institute, Parkville, Victoria, Australia (D.A.).; Academic Unit for Psychiatry of Old Age, University of Melbourne, St George's Hospital, Kew, Australia (D.A.).; Amin N; Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands (M.J.K., D.V., N.A., G.V.R., M.W.V., C.M.v.D., M.A.I., H.H.H.A.).; Amouyel P; Lille University, Inserm, Institut Pasteur de Lille, RID-AGE - Risk Factors and Molecular Determinants of Aging-Related Diseases and Labex Distalz, France (P.A.).; Lille University, Inserm, CHU Lille, Institut Pasteur de Lille, RID-AGE (P.A.).; Beiser AS; The Framingham Heart Study, MA (C.L.S., A.S.B., J.R.R., S.S.).; Department of Neurology (C.L.S., A.S.B., J.R.R., S.S.), Boston University School of Medicine, MA.; Department of Biostatistics, Boston University School of Public Health, Boston, MA (S.L., M.A.L., A.S.B., Q.Y.).; Brodaty H; Centre for Healthy Brain Ageing, School of Psychiatry (K.A.M., W.W., H.B., J.J., A.T., J.T., P.S.S.), University of New South Wales, Sydney, Australia.; Dementia Centre for Research Collaboration (H.B.), University of New South Wales, Sydney, Australia.; Deary IJ; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, United Kingdom (M.L., I.J.D., D.C.M.L., M.E.B., J.M.W.).; Fennema-Notestine C; Department of Psychiatry (C.F.-N.), University of California, San Diego, La Jolla, CA.; Center for Behavior Genetics of Aging (C.F.-N.), University of California, San Diego, La Jolla, CA.; Gampawar PG; Gottfried Schatz Research Center (for Cell Signaling, Metabolism and Aging), Medical University of Graz, Austria (P.G.G., H.S.).; Gottesman R; Department of Neurology, Cerebrovascular and stroke Division (R.G.), Johns Hopkins University School of Medicine, Baltimore, MD.; Griffanti L; Wellcome Centre for Integrative Neuroimaging (WIN FMRIB) (L.T.E., F.A.-A., L.G., M.J., S.M.S.), University of Oxford, United Kingdom.; Jack CR Jr; Department of Radiology, Mayo Clinic, Rochester, MN (C.R.J.J.).; Jenkinson M; Wellcome Centre for Integrative Neuroimaging (WIN FMRIB) (L.T.E., F.A.-A., L.G., M.J., S.M.S.), University of Oxford, United Kingdom.; Jiang J; Centre for Healthy Brain Ageing, School of Psychiatry (K.A.M., W.W., H.B., J.J., A.T., J.T., P.S.S.), University of New South Wales, Sydney, Australia.; Kral BG; GeneSTAR Research Program (L.R.Y., B.G.K., L.C.B., P.A.N.), Johns Hopkins University School of Medicine, Baltimore, MD.; Kwok JB; School of Medical Sciences (J.B.K., P.R.S.), University of New South Wales, Sydney, Australia.; Brain and Mind Centre - The University of Sydney, Camperdown, NSW, Australia (J.B.K.).; Lampe L; Department of Neurology, Max-Planck-Institute for Human Cognitive and Brain Sciences, Leipzig, Germany (L.L., V.A.W.).; C M Liewald D; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, United Kingdom (M.L., I.J.D., D.C.M.L., M.E.B., J.M.W.).; Maillard P; Imaging of Dementia and Aging (IDeA) Laboratory, Department of Neurology, University of California-Davis, Davis, CA (P.M.).; Marchini J; Statistical Genetics and Methods at Regeneron Pharmaceuticals, Inc, New York, NY (J.M.).; Bastin ME; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, United Kingdom (M.L., I.J.D., D.C.M.L., M.E.B., J.M.W.).; Centre for Clinical Brain Sciences, Edinburgh Imaging, Centre for Cognitive Ageing, University of Edinburgh, United Kingdom (M.E.B., J.M.W.).; Mazoyer B; Institut des Maladies Neurodégénératives, University of Bordeaux, France (B.M.).; Pirpamer L; Clinical Division of Neurogeriatrics, Department of Neurology, Medical University of Graz, Austria (L.P.).; Rafael Romero J; The Framingham Heart Study, MA (C.L.S., A.S.B., J.R.R., S.S.).; Department of Neurology (C.L.S., A.S.B., J.R.R., S.S.), Boston University School of Medicine, MA.; Roshchupkin GV; Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands (M.J.K., D.V., N.A., G.V.R., M.W.V., C.M.v.D., M.A.I., H.H.H.A.).; Department of Radiology and Nuclear Medicine (G.V.R., M.W.V., H.H.H.A.).; Schofield PR; School of Medical Sciences (J.B.K., P.R.S.), University of New South Wales, Sydney, Australia.; Neuroscience Research Australia, Sydney, Australia (K.A.M., P.R.S., A.T.).; Schroeter ML; LIFE Research Center for Civilization Disease, Leipzig, Germany (M.S.).; Department of Neurology, Max-Planck-Institute for Human Cognitive and Brain Sciences, Leipzig, Germany (M.L.S., A.V.).; Day Clinic for Cognitive Neurology, University Hospital Leipzig, Germany (M.L.S., A.V.).; Stott DJ; Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary and Life Sciences, University of Glasgow, United Kingdom (D.J.S.).; Thalamuthu A; Centre for Healthy Brain Ageing, School of Psychiatry (K.A.M., W.W., H.B., J.J., A.T., J.T., P.S.S.), University of New South Wales, Sydney, Australia.; Neuroscience Research Australia, Sydney, Australia (K.A.M., P.R.S., A.T.).; Trollor J; Centre for Healthy Brain Ageing, School of Psychiatry (K.A.M., W.W., H.B., J.J., A.T., J.T., P.S.S.), University of New South Wales, Sydney, Australia.; Department of Developmental Disability Neuropsychiatry, School of Psychiatry (J.T.), University of New South Wales, Sydney, Australia.; Tzourio C; University Bordeaux, Inserm, Bordeaux Population Health Research Center, France (M.S., C.T., S.D.).; CHU de Bordeaux, Public Health Department, Medical information Department, Bordeaux, France (C.T.).; van der Grond J; Department of Radiology (J.v.d.G.), Leiden University Medical Center, the Netherlands.; Vernooij MW; Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands (M.J.K., D.V., N.A., G.V.R., M.W.V., C.M.v.D., M.A.I., H.H.H.A.).; Department of Radiology and Nuclear Medicine (G.V.R., M.W.V., H.H.H.A.).; Witte VA; Collaborative Research Center 1052 Obesity Mechanisms, Faculty of Medicine, University of Leipzig, Germany (V.A.W).; Department of Neurology, Max-Planck-Institute for Human Cognitive and Brain Sciences, Leipzig, Germany (L.L., V.A.W.).; Wright MJ; Queensland Brain Institute (M.J.W.), The University of Queensland, St Lucia, QLD, Australia.; Centre for Advanced Imaging (M.J.W.), The University of Queensland, St Lucia, QLD, Australia.; Yang Q; Department of Biostatistics, Boston University School of Public Health, Boston, MA (S.L., M.A.L., A.S.B., Q.Y.).; Morris Z; Neuroradiology Department, Department of Clinical Neurosciences, Western General Hospital, Edinburgh, United Kingdom (Z.M.).; Siggurdsson S; Glenn Biggs Institute for Alzheimer's & Neurodegenerative Diseases, UT Health San Antonio, San Antonio, TX (C.L.S., S.S.).; The Framingham Heart Study, MA (C.L.S., A.S.B., J.R.R., S.S.).; Department of Neurology (C.L.S., A.S.B., J.R.R., S.S.), Boston University School of Medicine, MA.; Psaty B; Cardiovascular Health Research Unit, Department of Medicine, University of Washington, Seattle, WA (J.B., B.P., W.L.).; Villringer A; Department of Neurology, Max-Planck-Institute for Human Cognitive and Brain Sciences, Leipzig, Germany (M.L.S., A.V.).; Day Clinic for Cognitive Neurology, University Hospital Leipzig, Germany (M.L.S., A.V.).; Schmidt H; Gottfried Schatz Research Center (for Cell Signaling, Metabolism and Aging), Medical University of Graz, Austria (P.G.G., H.S.).; Haberg AK; Department of Neuromedicine and Movement Science (A.K.H.), Norwegian University of Science and Technology, Trondheim, Norway.; Department of Radiology and Nuclear Medicine (A.K.H.), Norwegian University of Science and Technology, Trondheim, Norway.; van Duijn CM; Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands (M.J.K., D.V., N.A., G.V.R., M.W.V., C.M.v.D., M.A.I., H.H.H.A.).; Nuffield Department of Population Health (C.M.v.D.), University of Oxford, United Kingdom.; Jukema JW; Department of Cardiology (J.W.J.), Leiden University Medical Center, the Netherlands.; Einthoven Laboratory for Experimental Vascular Medicine, LUMC, Leiden, the Netherlands (J.W.J.).; Dichgans M; Institute for Stroke and Dementia Research (ISD), University Hospital, Ludwig-Maximilians-Universität LMU Munich, Germany (R.M., M.D.).; German Center for Neurodegenerative Diseases, Munich, Germany (M.D.).; Munich Cluster for Systems Neurology (SyNergy), Germany (M.D.).; Sacco RL; Department of Public Health Sciences, Miller School of Medicine (R.L.S.), University of Miami, FL.; Department of Neurology, Miller School of Medicine (R.L.S.), University of Miami, FL.; Evelyn F. McKnight Brain Institute, Department of Neurology (R.L.S.), University of Miami, FL.; Wright CB; National Institute of Neurological Disorders and Stroke (C.B.W.), National Institutes of Health, Bethesda, MD.; Kremen WS; Center for Behavior Genetics of Aging (W.S.K.), University of California, San Diego, La Jolla, CA.; Department of Psychiatry (W.S.K.), University of California, San Diego, La Jolla, CA.; Becker LC; GeneSTAR Research Program (L.R.Y., B.G.K., L.C.B., P.A.N.), Johns Hopkins University School of Medicine, Baltimore, MD.; Thompson PM; Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Marina del Rey (N.J., P.M.T.).; Mosley TH; Department of Geriatric Medicine, Memory Impairment and Neurodegenerative Dementia (MIND) Center, University of Mississippi Medical Center, Jackson (T.H.M.).; Wardlaw JM; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, United Kingdom (M.L., I.J.D., D.C.M.L., M.E.B., J.M.W.).; Centre for Clinical Brain Sciences, Edinburgh Imaging, Centre for Cognitive Ageing, University of Edinburgh, United Kingdom (M.E.B., J.M.W.).; Ikram MA; Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands (M.J.K., D.V., N.A., G.V.R., M.W.V., C.M.v.D., M.A.I., H.H.H.A.).; Adams HHH; Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, the Netherlands (M.J.K., D.V., N.A., G.V.R., M.W.V., C.M.v.D., M.A.I., H.H.H.A.).; Department of Radiology and Nuclear Medicine (G.V.R., M.W.V., H.H.H.A.).; Department of Clinical Genetics, Erasmus MC, Rotterdam, the Netherlands (H.H.H.A.).; Seshadri S; Icelandic Heart Association, Kopavogur (V.G.G., S.S.).; Sachdev PS; Centre for Healthy Brain Ageing, School of Psychiatry (K.A.M., W.W., H.B., J.J., A.T., J.T., P.S.S.), University of New South Wales, Sydney, Australia.; Neuropsychiatric Institute, Prince of Wales Hospital, Sydney, Australia (P.S.S.).; Smith SM; Wellcome Centre for Integrative Neuroimaging (WIN FMRIB) (L.T.E., F.A.-A., L.G., M.J., S.M.S.), University of Oxford, United Kingdom.; Launer L; Laboratory of Epidemiology and Population Sciences, National Institute on Aging, Intramural Research Program (L.L.), National Institutes of Health, Bethesda, MD.; Longstreth W; Cardiovascular Health Research Unit, Department of Medicine, University of Washington, Seattle, WA (J.B., B.P., W.L.).; DeCarli C; Alzheimer's Disease Center and Imaging of Dementia and Aging (IDeA) Laboratory, Department of Neurology and Center for Neuroscience University of California at Davis (C.D.).; Schmidt R; Clinical Division of Neurogeriatrics, Department of Neurology, Medical University of Graz, Austria (E.H., R.S.).; Fornage M; Brown Foundation Institute of Molecular Medicine, McGovern Medical School, University of Texas Health Science Center at Houston, TX (R.X., M.F.).; Human Genetics Center, School of Public Health UT, Houston, TX (M.F.).; Debette S; University Bordeaux, Inserm, Bordeaux Population Health Research Center, France (M.S., C.T., S.D.).; Department of Neurology, CHU de Bordeaux (University Hospital), Bordeaux, France (S.D.).; Nyquist PA; GeneSTAR Research Program (L.R.Y., B.G.K., L.C.B., P.A.N.), Johns Hopkins University School of Medicine, Baltimore, MD.; Departments of Neurology, Critical Care Medicine, Neurosurgery (P.A.N.), Johns Hopkins University School of Medicine, Baltimore, MD.; Critical Care Medicine Department (P.A.N.), National Institutes of Health, Bethesda, MD. |
| Source: | Stroke [Stroke] 2020 Jul; Vol. 51 (7), pp. 2111-2121. Date of Electronic Publication: 2020 Jun 10. |
| Publication Type: | Journal Article; Meta-Analysis; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't |
| Language: | English |
| Journal Info: | Publisher: Lippincott Williams & Wilkins Country of Publication: United States NLM ID: 0235266 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1524-4628 (Electronic) Linking ISSN: 00392499 NLM ISO Abbreviation: Stroke Subsets: MEDLINE |
| Imprint Name(s): | Publication: 1998- : Baltimore, Md. : Lippincott Williams & Wilkins; Original Publication: Dallas : American Heart Association |
| MeSH Terms: | Brain/*pathology ; Cerebral Small Vessel Diseases/*genetics ; Cerebral Small Vessel Diseases/*pathology ; Genetic Predisposition to Disease/*genetics ; White Matter/*pathology; Brain/diagnostic imaging ; Cerebral Small Vessel Diseases/diagnostic imaging ; White Matter/diagnostic imaging ; Aged ; Female ; Genome-Wide Association Study ; Humans ; Male ; Middle Aged |
| Abstract: | Background and Purpose: Periventricular white matter hyperintensities (WMH; PVWMH) and deep WMH (DWMH) are regional classifications of WMH and reflect proposed differences in cause. In the first study, to date, we undertook genome-wide association analyses of DWMH and PVWMH to show that these phenotypes have different genetic underpinnings.; Methods: Participants were aged 45 years and older, free of stroke and dementia. We conducted genome-wide association analyses of PVWMH and DWMH in 26,654 participants from CHARGE (Cohorts for Heart and Aging Research in Genomic Epidemiology), ENIGMA (Enhancing Neuro-Imaging Genetics Through Meta-Analysis), and the UKB (UK Biobank). Regional correlations were investigated using the genome-wide association analyses -pairwise method. Cross-trait genetic correlations between PVWMH, DWMH, stroke, and dementia were estimated using LDSC.; Results: In the discovery and replication analysis, for PVWMH only, we found associations on chromosomes 2 (NBEAL), 10q23.1 (TSPAN14/FAM231A), and 10q24.33 (SH3PXD2A). In the much larger combined meta-analysis of all cohorts, we identified ten significant regions for PVWMH: chromosomes 2 (3 regions), 6, 7, 10 (2 regions), 13, 16, and 17q23.1. New loci of interest include 7q36.1 (NOS3) and 16q24.2. In both the discovery/replication and combined analysis, we found genome-wide significant associations for the 17q25.1 locus for both DWMH and PVWMH. Using gene-based association analysis, 19 genes across all regions were identified for PVWMH only, including the new genes: CALCRL (2q32.1), KLHL24 (3q27.1), VCAN (5q27.1), and POLR2F (22q13.1). Thirteen genes in the 17q25.1 locus were significant for both phenotypes. More extensive genetic correlations were observed for PVWMH with small vessel ischemic stroke. There were no associations with dementia for either phenotype.; Conclusions: Our study confirms these phenotypes have distinct and also shared genetic architectures. Genetic analyses indicated PVWMH was more associated with ischemic stroke whilst DWMH loci were implicated in vascular, astrocyte, and neuronal function. Our study confirms these phenotypes are distinct neuroimaging classifications and identifies new candidate genes associated with PVWMH only. |
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| Grant Information: | P41 EB015922 United States EB NIBIB NIH HHS; MC_QA137853 United Kingdom MRC_ Medical Research Council; MR/R024065/1 United Kingdom MRC_ Medical Research Council; MR/N027558/1 United Kingdom MRC_ Medical Research Council; U54 EB020403 United States EB NIBIB NIH HHS; G0701120 United Kingdom MRC_ Medical Research Council; MR/L023784/2 United Kingdom MRC_ Medical Research Council; R01 NS062059 United States NS NINDS NIH HHS; MR/M013111/1 United Kingdom MRC_ Medical Research Council; G1001245 United Kingdom MRC_ Medical Research Council; J-0901 United Kingdom PUK_ Parkinson's UK; R56 AG058854 United States AG NIA NIH HHS; G0700704 United Kingdom MRC_ Medical Research Council; United Kingdom WT_ Wellcome Trust; MC_PC_17228 United Kingdom MRC_ Medical Research Council; BB/F019394/1 United Kingdom BB_ Biotechnology and Biological Sciences Research Council; R01 AG022381 United States AG NIA NIH HHS; R01 AG050595 United States AG NIA NIH HHS; R01 AG059874 United States AG NIA NIH HHS |
| Contributed Indexing: | Keywords: brain; genome-wide association study; neuroimaging; risk factors; white matter |
| Entry Date(s): | Date Created: 20200611 Date Completed: 20201104 Latest Revision: 20260509 |
| Update Code: | 20260509 |
| PubMed Central ID: | PMC7365038 |
| DOI: | 10.1161/STROKEAHA.119.027544 |
| PMID: | 32517579 |
| Database: | MEDLINE |
Journal Article; Meta-Analysis; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't