Impact of Y chromosome loss on the risk of Parkinson's disease and progressionResearch in context
Summary: Background: Loss of Y chromosome (LOY), an age-related somatic mutation, is associated with various age-related diseases, but its role in the onset and progression of Parkinson's disease (PD) remains unclear. This study investigated the relationship between blood LOY levels and the ri...
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2025-07-01
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| author | Junhao Wang Xinyi Chen Wenxuan Du Cha Lin Yu Liao Jean-Christophe Corvol Jodi Maple-Grødem Meghan C. Campbell Alexis Elbaz Suzanne Lesage Alexis Brice Michael A. Schwarzschild Pille Taba Sulev Kõks Guido Alves Ole-Bjørn Tysnes Joel S. Perlmutter Baijayanta Maiti Jacobus J. van Hilten Roger A. Barker Caroline H. Williams-Gray Clemens R. Scherzer Ganqiang Liu Ganqiang Liu Rebecca R. Valentino Zhixiang Liao Joseph J. Locascio Jean-Christophe Corvol Xianjun Dong Jodi Maple-Grødem Meghan C. Campbell Alexis Elbaz Suzanne Lesage Alexis Brice Graziella Mangone John H. Growdon Albert Y. Hung Michael A. Schwarzchild Michael T. Hayes Anne-Marie Wills Todd M. Herrington Bernard Ravian Ira Shoulson Pille Taba Sulev Kõks Thomas G. Beach Florence Cormier-Dequaire Guido Alves Ole-Bjørn Tysnes Joel S. Perlmutter Peter Heutink Jacobus J. van Hilten Meike Kasten Brit Mollenhauer Claudia Trenkwalder Christine Klein Roger A. Barker Caroline H. Williams-Gray Johan Marinus Clemens R. Scherzer |
| author_facet | Junhao Wang Xinyi Chen Wenxuan Du Cha Lin Yu Liao Jean-Christophe Corvol Jodi Maple-Grødem Meghan C. Campbell Alexis Elbaz Suzanne Lesage Alexis Brice Michael A. Schwarzschild Pille Taba Sulev Kõks Guido Alves Ole-Bjørn Tysnes Joel S. Perlmutter Baijayanta Maiti Jacobus J. van Hilten Roger A. Barker Caroline H. Williams-Gray Clemens R. Scherzer Ganqiang Liu Ganqiang Liu Rebecca R. Valentino Zhixiang Liao Joseph J. Locascio Jean-Christophe Corvol Xianjun Dong Jodi Maple-Grødem Meghan C. Campbell Alexis Elbaz Suzanne Lesage Alexis Brice Graziella Mangone John H. Growdon Albert Y. Hung Michael A. Schwarzchild Michael T. Hayes Anne-Marie Wills Todd M. Herrington Bernard Ravian Ira Shoulson Pille Taba Sulev Kõks Thomas G. Beach Florence Cormier-Dequaire Guido Alves Ole-Bjørn Tysnes Joel S. Perlmutter Peter Heutink Jacobus J. van Hilten Meike Kasten Brit Mollenhauer Claudia Trenkwalder Christine Klein Roger A. Barker Caroline H. Williams-Gray Johan Marinus Clemens R. Scherzer |
| author_sort | Junhao Wang |
| collection | DOAJ |
| description | Summary: Background: Loss of Y chromosome (LOY), an age-related somatic mutation, is associated with various age-related diseases, but its role in the onset and progression of Parkinson's disease (PD) remains unclear. This study investigated the relationship between blood LOY levels and the risk of PD onset and progression. Methods: We estimated the LOY level for each male participant based on genome-wide arrays or whole genome sequencing data. We performed Cox proportional hazards regression analysis among 222,598 male participants in the UK Biobank and linear mixed model analysis involving 2574 male individuals with PD across 14 cohorts, encompassing 19,562 visits. In the Parkinson's Progression Markers Initiative (PPMI) cohort, we further compared brain structure using T1-weighted magnetic resonance imaging (MRI) scans, and carried out brain network functional connectivity analysis based on resting-state functional MRI (rs-fMRI) datasets. Additionally, we assessed the LOY status in single-nucleus RNA sequencing (snRNA-seq) data, which included 1,303,531 cells from 279 post-mortem samples across five brain regions, and performed temporal dynamic gene expression analysis. Findings: Male participants with LOY had a slightly higher risk of developing PD during follow-up (HR = 1·16, 95% CI = 1·01–1·34, P = 0·04). Among males affected by PD, LOY carriers experienced accelerated neurodegenerative progression, manifesting as more rapid motor impairment (P = 0·0072) and cognitive decline (P = 0·0005) compared to non-LOY carriers. Patients with PD carrying LOY also exhibited decreased network functional connectivity in certain brain regions. Notably, LOY cells were particularly enriched in microglia/immune and vascular/epithelial cells, and a subset of genes in LOY-Mic P2RY12 cells were associated with PD progression. Interpretation: This data-driven study highlights the potential association of LOY with the onset and progression of PD through the analysis of multi-scale data, including clinical phenotypes, brain neuroimaging maps, and molecular profiles from single-nucleus transcriptome across multi-brain regions. These findings suggest that LOY may be an accomplice to the onset and progression of PD. Funding: G.L.'s work is supported by the Shenzhen Fundamental Research Program (JCYJ20240813151132042), National Natural Science Foundation of China (32270701, 32470708), Young Talent Recruitment Project of Guangdong (2019QN01Y139), the Science and Technology Planning Project of Guangdong Province (2023B1212060018) and Shenzhen Key Laboratory for Systems Medicine in Inflammatory Diseases (ZDSYS20220606100803007). This study is supported by High-performance Computing Public Platform (Shenzhen Campus) of Sun Yat-sen University. C.R.S.'s work is supported by NIH grants NINDS/NIA R01NS115144, the U.S. Department of Defense, and the American Parkinson Disease Association Center for Advanced Parkinson Research. C.R.S.'s research work was funded in part by Aligning Science Across Parkinson's 000301 through the Michael J. Fox Foundation for Parkinson's Research (MJFF). The study was made possible in part by a philanthropic support for Illumina MEGA chip genotyping (to Brigham & Women's Hospital and C.R.S.). CHWG received funding support from an RCUK/UKRI Research Innovation Fellowship awarded by the Medical Research Council (MR/R007446/1; MR/W029235/1) and from the NIHR Cambridge Biomedical Research Centre (NIHR203312). The views expressed are those of the author(s) and not necessarily those of the NIHR or the Department of Health and Social Care. For the purpose of open access, the author has applied a CC BY public copyright licence to all Author Accepted Manuscripts arising from this submission. |
| format | Article |
| id | doaj-art-db90516e00bf40548d1b456b69d5aec2 |
| institution | OA Journals |
| issn | 2352-3964 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | EBioMedicine |
| spelling | doaj-art-db90516e00bf40548d1b456b69d5aec22025-08-20T02:34:53ZengElsevierEBioMedicine2352-39642025-07-0111710576910.1016/j.ebiom.2025.105769Impact of Y chromosome loss on the risk of Parkinson's disease and progressionResearch in contextJunhao Wang0Xinyi Chen1Wenxuan Du2Cha Lin3Yu Liao4Jean-Christophe Corvol5Jodi Maple-Grødem6Meghan C. Campbell7Alexis Elbaz8Suzanne Lesage9Alexis Brice10Michael A. Schwarzschild11Pille Taba12Sulev Kõks13Guido Alves14Ole-Bjørn Tysnes15Joel S. Perlmutter16Baijayanta Maiti17Jacobus J. van Hilten18Roger A. Barker19Caroline H. Williams-Gray20Clemens R. Scherzer21Ganqiang Liu22Ganqiang LiuRebecca R. ValentinoZhixiang LiaoJoseph J. LocascioJean-Christophe CorvolXianjun DongJodi Maple-GrødemMeghan C. CampbellAlexis ElbazSuzanne LesageAlexis BriceGraziella MangoneJohn H. GrowdonAlbert Y. HungMichael A. SchwarzchildMichael T. HayesAnne-Marie WillsTodd M. HerringtonBernard RavianIra ShoulsonPille TabaSulev KõksThomas G. BeachFlorence Cormier-DequaireGuido AlvesOle-Bjørn TysnesJoel S. PerlmutterPeter HeutinkJacobus J. van HiltenMeike KastenBrit MollenhauerClaudia TrenkwalderChristine KleinRoger A. BarkerCaroline H. Williams-GrayJohan MarinusClemens R. ScherzerShenzhen Key Laboratory of Systems Medicine in Inflammatory Diseases, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Guangming District, Shenzhen, Guangdong, 518107, China; Neurobiology Research Center, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Shenzhen, Guangdong, 518107, ChinaShenzhen Key Laboratory of Systems Medicine in Inflammatory Diseases, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Guangming District, Shenzhen, Guangdong, 518107, China; Neurobiology Research Center, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Shenzhen, Guangdong, 518107, ChinaShenzhen Key Laboratory of Systems Medicine in Inflammatory Diseases, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Guangming District, Shenzhen, Guangdong, 518107, China; Neurobiology Research Center, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Shenzhen, Guangdong, 518107, ChinaShenzhen Key Laboratory of Systems Medicine in Inflammatory Diseases, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Guangming District, Shenzhen, Guangdong, 518107, China; Neurobiology Research Center, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Shenzhen, Guangdong, 518107, ChinaShenzhen Key Laboratory of Systems Medicine in Inflammatory Diseases, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Guangming District, Shenzhen, Guangdong, 518107, China; Neurobiology Research Center, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Shenzhen, Guangdong, 518107, ChinaSorbonne Université, Institut du Cerveau – Paris Brain Institute - ICM, Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Assistance Publique Hôpitaux de Paris, Département de Neurologie et de Génétique, Hôpital Pitié-Salpêtrière, F-75013, Paris, FranceThe Centre for Movement Disorders, Centre for Brain Health, Stavanger University Hospital, 4011, Stavanger, Norway; Department of Chemistry, Bioscience and Environmental Engineering, University of Stavanger, 4021, Stavanger, NorwayDepartments of Neurology and Radiology, Washington University School of Medicine, St. Louis, MO, 63110, USAUniversité Paris-Saclay, UVSQ, Inserm, Gustave Roussy, CESP, 94805, Villejuif, FranceSorbonne Université, Institut du Cerveau – Paris Brain Institute - ICM, Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Assistance Publique Hôpitaux de Paris, Département de Neurologie et de Génétique, Hôpital Pitié-Salpêtrière, F-75013, Paris, FranceSorbonne Université, Institut du Cerveau – Paris Brain Institute - ICM, Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Assistance Publique Hôpitaux de Paris, Département de Neurologie et de Génétique, Hôpital Pitié-Salpêtrière, F-75013, Paris, FranceDepartment of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, 02114, USADepartment of Neurology and Neurosurgery, Institute of Clinical Medicine, University of Tartu, Tartu, 50406, Estonia; Neurology Clinic, Tartu University Hospital, Tartu, 50406, EstoniaCentre for Molecular Medicine and Innovative Therapeutics, Murdoch University, Murdoch, Perth, 6150, WA, Australia; Perron Institute for Neurological and Translational Science, Nedlands, WA, 6009, AustraliaThe Centre for Movement Disorders, Centre for Brain Health, Stavanger University Hospital, 4011, Stavanger, Norway; Department of Chemistry, Bioscience and Environmental Engineering, University of Stavanger, 4021, Stavanger, Norway; Department of Neurology, Stavanger University Hospital, 4068, Stavanger, NorwayDepartment of Neurology, Haukeland University Hospital, 5020, Bergen, Norway; Department of Clinical Medicine, University of Bergen, 5020, NorwayDepartments of Neurology and Radiology, Washington University School of Medicine, St. Louis, MO, 63110, USA; Departments of Radiology and Neuroscience, Washington University School of Medicine, St. Louis, MO, 63110, USA; Program of Physical Therapy and Program of Occupational Therapy, Washington University School of Medicine, St. Louis, MO, 63110, USADepartments of Neurology and Radiology, Washington University School of Medicine, St. Louis, MO, 63110, USADepartment of Neurology, Leiden University Medical Center, Albinusdreef 2, 2333, ZA, Leiden, the NetherlandsJohn Van Geest Centre for Brain Repair, Department of Clinical Neurosciences, University of Cambridge, Cambridge, CB2 0PY, UK; Wellcome - MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge, CB2 0AW, UKJohn Van Geest Centre for Brain Repair, Department of Clinical Neurosciences, University of Cambridge, Cambridge, CB2 0PY, UKStephen & Denise Adams Center for Parkinson's Disease Research of Yale School of Medicine, New Haven, CT, 06510, USA; APDA Center for Parkinson Precision Medicine, Yale, New Haven, CT, 06510, USA; Department of Neurology, Yale, New Haven, CT, 06510, USA; Department of Genetics, Yale, New Haven, CT, 06510, USAShenzhen Key Laboratory of Systems Medicine in Inflammatory Diseases, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Guangming District, Shenzhen, Guangdong, 518107, China; Neurobiology Research Center, School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Shenzhen, Guangdong, 518107, China; Guangdong Provincial Key Laboratory of Brain Function and Disease, Guangzhou, 510080, China; Corresponding author. School of Medicine, Shenzhen Campus of Sun Yat-sen University, No. 66, Gongchang Road, Guangming District, Shenzhen, Guangdong, 518107, China.Summary: Background: Loss of Y chromosome (LOY), an age-related somatic mutation, is associated with various age-related diseases, but its role in the onset and progression of Parkinson's disease (PD) remains unclear. This study investigated the relationship between blood LOY levels and the risk of PD onset and progression. Methods: We estimated the LOY level for each male participant based on genome-wide arrays or whole genome sequencing data. We performed Cox proportional hazards regression analysis among 222,598 male participants in the UK Biobank and linear mixed model analysis involving 2574 male individuals with PD across 14 cohorts, encompassing 19,562 visits. In the Parkinson's Progression Markers Initiative (PPMI) cohort, we further compared brain structure using T1-weighted magnetic resonance imaging (MRI) scans, and carried out brain network functional connectivity analysis based on resting-state functional MRI (rs-fMRI) datasets. Additionally, we assessed the LOY status in single-nucleus RNA sequencing (snRNA-seq) data, which included 1,303,531 cells from 279 post-mortem samples across five brain regions, and performed temporal dynamic gene expression analysis. Findings: Male participants with LOY had a slightly higher risk of developing PD during follow-up (HR = 1·16, 95% CI = 1·01–1·34, P = 0·04). Among males affected by PD, LOY carriers experienced accelerated neurodegenerative progression, manifesting as more rapid motor impairment (P = 0·0072) and cognitive decline (P = 0·0005) compared to non-LOY carriers. Patients with PD carrying LOY also exhibited decreased network functional connectivity in certain brain regions. Notably, LOY cells were particularly enriched in microglia/immune and vascular/epithelial cells, and a subset of genes in LOY-Mic P2RY12 cells were associated with PD progression. Interpretation: This data-driven study highlights the potential association of LOY with the onset and progression of PD through the analysis of multi-scale data, including clinical phenotypes, brain neuroimaging maps, and molecular profiles from single-nucleus transcriptome across multi-brain regions. These findings suggest that LOY may be an accomplice to the onset and progression of PD. Funding: G.L.'s work is supported by the Shenzhen Fundamental Research Program (JCYJ20240813151132042), National Natural Science Foundation of China (32270701, 32470708), Young Talent Recruitment Project of Guangdong (2019QN01Y139), the Science and Technology Planning Project of Guangdong Province (2023B1212060018) and Shenzhen Key Laboratory for Systems Medicine in Inflammatory Diseases (ZDSYS20220606100803007). This study is supported by High-performance Computing Public Platform (Shenzhen Campus) of Sun Yat-sen University. C.R.S.'s work is supported by NIH grants NINDS/NIA R01NS115144, the U.S. Department of Defense, and the American Parkinson Disease Association Center for Advanced Parkinson Research. C.R.S.'s research work was funded in part by Aligning Science Across Parkinson's 000301 through the Michael J. Fox Foundation for Parkinson's Research (MJFF). The study was made possible in part by a philanthropic support for Illumina MEGA chip genotyping (to Brigham & Women's Hospital and C.R.S.). CHWG received funding support from an RCUK/UKRI Research Innovation Fellowship awarded by the Medical Research Council (MR/R007446/1; MR/W029235/1) and from the NIHR Cambridge Biomedical Research Centre (NIHR203312). The views expressed are those of the author(s) and not necessarily those of the NIHR or the Department of Health and Social Care. For the purpose of open access, the author has applied a CC BY public copyright licence to all Author Accepted Manuscripts arising from this submission.http://www.sciencedirect.com/science/article/pii/S2352396425002130Parkinson's diseaseLOYOnsetProgression |
| spellingShingle | Junhao Wang Xinyi Chen Wenxuan Du Cha Lin Yu Liao Jean-Christophe Corvol Jodi Maple-Grødem Meghan C. Campbell Alexis Elbaz Suzanne Lesage Alexis Brice Michael A. Schwarzschild Pille Taba Sulev Kõks Guido Alves Ole-Bjørn Tysnes Joel S. Perlmutter Baijayanta Maiti Jacobus J. van Hilten Roger A. Barker Caroline H. Williams-Gray Clemens R. Scherzer Ganqiang Liu Ganqiang Liu Rebecca R. Valentino Zhixiang Liao Joseph J. Locascio Jean-Christophe Corvol Xianjun Dong Jodi Maple-Grødem Meghan C. Campbell Alexis Elbaz Suzanne Lesage Alexis Brice Graziella Mangone John H. Growdon Albert Y. Hung Michael A. Schwarzchild Michael T. Hayes Anne-Marie Wills Todd M. Herrington Bernard Ravian Ira Shoulson Pille Taba Sulev Kõks Thomas G. Beach Florence Cormier-Dequaire Guido Alves Ole-Bjørn Tysnes Joel S. Perlmutter Peter Heutink Jacobus J. van Hilten Meike Kasten Brit Mollenhauer Claudia Trenkwalder Christine Klein Roger A. Barker Caroline H. Williams-Gray Johan Marinus Clemens R. Scherzer Impact of Y chromosome loss on the risk of Parkinson's disease and progressionResearch in context EBioMedicine Parkinson's disease LOY Onset Progression |
| title | Impact of Y chromosome loss on the risk of Parkinson's disease and progressionResearch in context |
| title_full | Impact of Y chromosome loss on the risk of Parkinson's disease and progressionResearch in context |
| title_fullStr | Impact of Y chromosome loss on the risk of Parkinson's disease and progressionResearch in context |
| title_full_unstemmed | Impact of Y chromosome loss on the risk of Parkinson's disease and progressionResearch in context |
| title_short | Impact of Y chromosome loss on the risk of Parkinson's disease and progressionResearch in context |
| title_sort | impact of y chromosome loss on the risk of parkinson s disease and progressionresearch in context |
| topic | Parkinson's disease LOY Onset Progression |
| url | http://www.sciencedirect.com/science/article/pii/S2352396425002130 |
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