Genetic landscape of Parkinson’s disease and related diseases in Luxembourg

LANDOULSI, Zied; PACHCHEK, Sinthuja; BOBBILI, Dheeraj Reddy; PAVELKA, Lukas; MAY, Patrick; KRÜGER, Rejko; NCER-PD consortium

doi:10.3389/fnagi.2023.1282174

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Genetic landscape of Parkinson’s disease and related diseases in Luxembourg

LANDOULSI, Zied; PACHCHEK, Sinthuja; BOBBILI, Dheeraj Reddy et al.

2023 • In Frontiers in Aging Neuroscience, 15

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https://hdl.handle.net/10993/59072

DOI
10.3389/fnagi.2023.1282174

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Keywords :

Cognitive Neuroscience; Aging; Parkinson's disease; Parkinsonism; Genetics; Luxembourg

Abstract :

[en] Objectives: To explore the genetic architecture of PD in the Luxembourg Parkinson’s Study including cohorts of healthy people and patients with Parkinson’s disease (PD) and atypical parkinsonism (AP).Methods: 809 healthy controls, 680 PD and 103 AP were genotyped using the Neurochip array. We screened and validated rare single nucleotide variants (SNVs) and copy number variants (CNVs) within seven PD-causing genes (LRRK2, SNCA, VPS35, PRKN, PARK7, PINK1 and ATP13A2). Polygenic risk scores (PRSs) were generated using the latest genome-wide association study for PD. We then estimated the role of common variants in PD risk by applying gene-set-specific PRSs.Results: We identified 60 rare SNVs in seven PD-causing genes, nine of which were pathogenic in LRRK2, PINK1 and PRKN. Eleven rare CNVs were detected in PRKN including seven duplications and four deletions. The majority of PRKN SNVs and CNVs carriers were heterozygous and not differentially distributed between cases and controls. The PRSs were significantly associated with PD and identified specific molecular pathways related to protein metabolism and signal transduction as drivers of PD risk.Conclusion: We performed a comprehensive genetic characterization of the deep-phenotyped individuals of the Luxembourgish Parkinson’s Study. Heterozygous SNVs and CNVs in PRKN were not associated with higher PD risk. In particular, we reported novel digenic variants in PD related genes and rare LRRK2 SNVs in AP patients. Our findings will help future studies to unravel the genetic complexity of PD.

Research center :

Luxembourg Centre for Systems Biomedicine (LCSB): Bioinformatics Core (R. Schneider Group)
Luxembourg Centre for Systems Biomedicine (LCSB): Clinical & Experimental Neuroscience (Krüger Group)
LIH - Luxembourg Institute of Health
ULHPC - University of Luxembourg: High Performance Computing

Disciplines :

Genetics & genetic processes
Neurology

Author, co-author :

LANDOULSI, Zied ^✱; University of Luxembourg > Luxembourg Centre for Systems Biomedicine (LCSB) > Bioinformatics Core

PACHCHEK, Sinthuja ^✱; University of Luxembourg > Luxembourg Centre for Systems Biomedicine (LCSB) > Translational Neuroscience

BOBBILI, Dheeraj Reddy ; University of Luxembourg > Luxembourg Centre for Systems Biomedicine (LCSB) > Bioinformatics Core

PAVELKA, Lukas ; University of Luxembourg

MAY, Patrick ^✱; University of Luxembourg > Luxembourg Centre for Systems Biomedicine (LCSB) > Bioinformatics Core

KRÜGER, Rejko ^✱; University of Luxembourg > Luxembourg Centre for Systems Biomedicine (LCSB) > Translational Neuroscience ; Centre Hospitalier de Luxembourg (CHL) > Parkinson Research Clinic ; Luxembourg Institute of Health (LIH) > Transversal Translational Medicine

NCER-PD consortium

^✱ These authors have contributed equally to this work.

External co-authors :

Language :

English

Title :

Genetic landscape of Parkinson’s disease and related diseases in Luxembourg

Publication date :

20 December 2023

Journal title :

Frontiers in Aging Neuroscience

eISSN :

1663-4365

Publisher :

Frontiers Media SA

Volume :

Peer reviewed :

Peer Reviewed verified by ORBi

Focus Area :

Systems Biomedicine

Development Goals :

3. Good health and well-being

Additional URL :

https://www.frontiersin.org/articles/10.3389/fnagi.2023.1282174/full

FnR Project :

FNR11264123 - Ncer-pd, 2015 (01/01/2015-30/11/2020) - Rejko Krüger

Funders :

FNR - Fonds National de la Recherche [LU]

Funding number :

FNR/P13/6682797; C17/BM/11676395; FNR11250962; PRIDE17/12244779/PARK-QC

Funding text :

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The National Centre of Excellence in Research on Parkinson’s Disease (NCER-PD) is funded by the Luxembourg National Research Fund (FNR/NCER13/BM/11264123), the PEARL program (FNR/P13/6682797 to RK), MotaSYN (12719684 to RK), MAMaSyn (to RK), MiRisk-PD (C17/BM/11676395 to RK and PM), the FNR/DFG Core INTER (ProtectMove, FNR11250962 to PM and ZL), and the PARK-QC DTU (PRIDE17/12244779/PARK-QC to RK and SP).

Commentary :

NCER-PD consortium member Geeta Acharya, Gloria Aguayo, Myriam Alexandre, Wim Ammerlann, Katy Beaumont, Camille Bellora, Jessica Calmes, Lorieza Castillo, Gessica Contesotto, Daniela Esteves, Guy Fagherazzi, Jean-Yves Ferrand, Manon Gantenbein, Marijus Giraitis, Jérôme Graas, Gaël Hammot, Anne-Marie Hanff, Estelle Henry, Michael Heymann, Alexander Hundt, Sonja Jónsdóttir, Jochen Klucken, Rejko Krüger, Pauline Lambert, Victoria Lorentz, Paula Cristina Lupu, Guilherme Marques, Deborah Mcintyre, Chouaib Mediouni, Myriam Menster, Maura Minelli, Ulf Nehrbass, Fozia Noor, Magali Perquin, Rosalina Ramos Lima, Eduardo Rosales, Estelle Sandt, Margaux Schmitt, Amir Sharify, Kate Sokolowska, Hermann Thien, Johanna Trouet, Olena Tsurkalenko, Michel Vaillant, Mesele Valenti, Luxembourg Institute of Health, Strassen, Luxembourg; Muhammad Ali, Giuseppe Arena, Rudi Balling, Michele Bassis, Regina Becker, Ibrahim Boussaad, Kathrin Brockmann, Piotr Gawron, Soumyabrata Ghosh, Enrico Glaab, Elisa Gómez De Lope, Valentin Groues, Anne Grünewald, Wei Gu, Linda Hansen, Michael Heneka, Sascha Herzinger, Jacek Jaroslaw Lebioda, Yohan Jaroz, Quentin Klopfenstein, Jochen Klucken, Rejko Krüger, Zied Landoulsi, Tainá M. Marques, Patricia Martins Conde, Patrick May, Francoise Meisch, Michel Mittelbronn, Michel Mittelbronn, Sarah Nickels, Marek Ostaszewski, Clarissa P. C. Gomes, Sinthuja Pachchek, Claire Pauly, Laure Pauly, Lukas Pavelka, Armin Rauschenberger, Rajesh Rawal, Dheeraj Reddy Bobbili, Kirsten Roomp, Isabel Rosety, Stefano Sapienza, Venkata Satagopam, Sabine Schmitz, Reinhard Schneider, Jens Schwamborn, Ekaterina Soboleva, Rebecca Ting Jiin Loo, Christophe Trefois, Carlos Vega, Maharshi Vyas, Paul Wilmes, Evi Wollscheid-Lengeling, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg; Guy Berchem, Nico Diederich, Marijus Giraitis, Linda Hansen, Jochen Klucken, Rejko Krüger, Laura Longhino, Romain Nati, Beatrice Nicolai, Claire Pauly, Lukas Pavelka, Elodie Thiry, Liliana Vilas Boas, Gelani Zelimkhanov, Centre Hospitalier de Luxembourg, Strassen, Luxembourg; Michel Mittelbronn, Friedrich Mühlschlegel, Laboratoire National de Santé, Dudelange, Luxembourg; Alexandre Bisdorff, Rene Dondelinger, Centre Hospitalier Emile Mayrisch, Esch-sur-Alzette, Luxembourg; Sylvia Herbrink, Centre Hospitalier du Nord, Ettelbrück, Luxembourg; Roseline Lentz, Parkinson Luxembourg Association, Leudelange, Luxembourg; Michele Hu, Oxford Parkinson’s Disease Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom; Richard Wade-Martins, Oxford Parkinson’s Disease Centre, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom; Clare Mackay, Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, Oxford, United Kingdom; Daniela Berg, Kathrin Brockmann, Thomas Gasser, Inga Liepelt, Center of Neurology and Hertie Institute for Clinical Brain Research, Department of Neurodegenerative Diseases, University Hospital Tübingen, Tübingen, Germany; Brit Mollenhauer, Paracelsus-Elena-Klinik, Kassel, Germany; Katrin Marcus, Ruhr-University of Bochum, Bochum, Germany; Robert Liszka, Westpfalz-Klinikum GmbH, Kaiserslautern, Germany; Walter Maetzler, Department of Neurology, University Medical Center Schleswig-Holstein, Kiel, Germany; Mariella Graziano, Association of Physiotherapists in Parkinson’s Disease Europe, Esch-sur-Alzette, Luxembourg; Nadine Jacoby, Private Practice, Ettelbruck, Luxembourg; Jean-Paul Nicolay, Private Practice, Luxembourg, Luxembourg.

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Bibliography

Ahmad A. Nkosi D. Iqbal M. A. (2023). PARK2 microdeletion or duplications have been implicated in different neurological disorders including early onset Parkinson disease. Genes 14:600. doi: 10.3390/genes14030600, PMID: 36980871
Anandhan A. Jacome M. S. Lei S. Hernandez-Franco P. Pappa A. Panayiotidis M. I. et al. (2017). Metabolic dysfunction in Parkinson’s disease: bioenergetics, redox homeostasis and central carbon metabolism. Brain Res. Bull. 133, 12–30. doi: 10.1016/j.brainresbull.2017.03.009, PMID: 28341600
Arena G. Valente E. M. (2017). PINK1 in the limelight: multiple functions of an eclectic protein in human health and disease: functions of PINK1 in human pathology. J. Pathol. 241, 251–263. doi: 10.1002/path.4815, PMID: 27701735
Baker M. Litvan I. Houlden H. Adamson J. Dickson D. Perez-Tur J. et al. (1999). Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Hum. Mol. Genet. 8, 711–715. doi: 10.1093/hmg/8.4.711
Bandres-Ciga S. Saez-Atienzar S. Kim J. J. Makarious M. B. Faghri F. Diez-Fairen M. et al. (2020). Large-scale pathway specific polygenic risk and transcriptomic community network analysis identifies novel functional pathways in Parkinson disease. Acta Neuropathol. 140, 341–358. doi: 10.1007/s00401-020-02181-3, PMID: 32601912
Blauwendraat C. Faghri F. Pihlstrom L. Geiger J. T. Elbaz A. Lesage S. et al. (2017). NeuroChip, an updated version of the NeuroX genotyping platform to rapidly screen for variants associated with neurological diseases. Neurobiol. Aging 57, 247.e9–247.e13. doi: 10.1016/j.neurobiolaging.2017.05.009, PMID: 28602509
Blauwendraat C. Nalls M. A. Singleton A. B. (2020). The genetic architecture of Parkinson’s disease. Lancet Neurol. 19, 170–178. doi: 10.1016/S1474-4422(19)30287-X
Bloem B. R. Okun M. S. Klein C. (2021). Parkinson’s disease. Lancet 397, 2284–2303. doi: 10.1016/S0140-6736(21)00218-X
Castelo Rueda M. P. Raftopoulou A. Gögele M. Borsche M. Emmert D. Fuchsberger C. et al. (2021). Frequency of heterozygous parkin (PRKN) variants and penetrance of Parkinson’s disease risk markers in the population-based CHRIS cohort. Front. Neurol. 12:706145. doi: 10.3389/fneur.2021.706145, PMID: 34434164
Chang C. C. Chow C. C. Tellier L. C. Vattikuti S. Purcell S. M. Lee J. J. (2015). Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaSci 4:7. doi: 10.1186/s13742-015-0047-8, PMID: 25722852
Choi S. W. García-González J. Ruan Y. Wu H. M. Porras C. Johnson J. et al. (2023). PRSet: pathway-based polygenic risk score analyses and software. PLoS Genet. 19:e1010624. doi: 10.1371/journal.pgen.1010624, PMID: 36749789
Choi S. W. O’Reilly P. F. (2019). PRSice-2: polygenic risk score software for biobank-scale data. GigaScience 8:giz082. doi: 10.1093/gigascience/giz082, PMID: 31307061
Collins R. L. Brand H. Karczewski K. J. Zhao X. Alföldi J. Francioli L. C. et al. (2020). A structural variation reference for medical and population genetics. Nature 581, 444–451. doi: 10.1038/s41586-020-2287-8, PMID: 32461652
Correia Guedes L. Ferreira J. J. Rosa M. M. Coelho M. Bonifati V. Sampaio C. (2010). Worldwide frequency of G2019S LRRK2 mutation in Parkinson’s disease: a systematic review. Parkinsonism Relat. Disord. 16, 237–242. doi: 10.1016/j.parkreldis.2009.11.004, PMID: 19945904
Dächsel J. C. Mata I. F. Ross O. A. Taylor J. P. Lincoln S. J. Hinkle K. M. et al. (2006). Digenic parkinsonism: investigation of the synergistic effects of PRKN and LRRK2. Neurosci. Lett. 410, 80–84. doi: 10.1016/j.neulet.2006.06.068, PMID: 17095157
Das S. Forer L. Schönherr S. Sidore C. Locke A. E. Kwong A. et al. (2016). Next-generation genotype imputation service and methods. Nat. Genet. 48, 1284–1287. doi: 10.1038/ng.3656, PMID: 27571263
Dehestani M. Liu H. Gasser T. (2021). Polygenic risk scores contribute to personalized medicine of Parkinson’s disease. JPM 11:1030. doi: 10.3390/jpm11101030, PMID: 34683174
Dorsey E. R. Bloem B. R. (2018). The Parkinson pandemic—a call to action. JAMA Neurol. 75:9. doi: 10.1001/jamaneurol.2017.3299
Elfferich P. Verleun-Mooijman M. C. Maat-Kievit J. A. van de Warrenburg B. P. C. Abdo W. F. Eshuis S. A. et al. (2011). Breakpoint mapping of 13 large parkin deletions/duplications reveals an exon 4 deletion and an exon 7 duplication as founder mutations. Neurogenetics 12, 263–271. doi: 10.1007/s10048-011-0302-9, PMID: 21993715
Funayama M. Li Y. Tsoi T. Lam C. Ohi T. Yazawa S. et al. (2008). Familial parkinsonism with digenic parkin and PINK1 mutations. Mov. Disord. 23, 1461–1465. doi: 10.1002/mds.22143
Gilman S. Wenning G. K. Low P. A. Brooks D. J. Mathias C. J. Trojanowski J. Q. et al. (2008). Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71, 670–676. doi: 10.1212/01.wnl.0000324625.00404.15, PMID: 18725592
Haugarvoll K. Wszolek Z. K. (2009). Clinical features of LRRK2 parkinsonism. Parkinsonism Relat. Disord. 15, S205–S208. doi: 10.1016/S1353-8020(09)70815-6
Hayashida A. Li Y. Yoshino H. Daida K. Ikeda A. Ogaki K. et al. (2021). The identified clinical features of Parkinson’s disease in homo-, heterozygous and digenic variants of PINK1. Neurobiol. Aging 97, 146.e1–146.e13. doi: 10.1016/j.neurobiolaging.2020.06.017, PMID: 32713623
Healy D. G. Falchi M. O’Sullivan S. S. Bonifati V. Durr A. Bressman S. et al. (2008). Phenotype, genotype, and worldwide genetic penetrance of LRRK2-associated Parkinson’s disease: a case-control study. Lancet Neurol. 7, 583–590. doi: 10.1016/S1474-4422(08)70117-0, PMID: 18539534
Hipp G. Vaillant M. Diederich N. J. Roomp K. Satagopam V. P. Banda P. et al. (2018). The Luxembourg Parkinson’s study: a comprehensive approach for stratification and early diagnosis. Front. Aging Neurosci. 10:326. doi: 10.3389/fnagi.2018.00326, PMID: 30420802
Huttenlocher J. Stefansson H. Steinberg S. Helgadottir H. T. Sveinbjörnsdóttir S. Riess O. et al. (2015). Heterozygote carriers for CNVs in PARK2 are at increased risk of Parkinson’s disease. Hum. Mol. Genet. 24, 5637–5643. doi: 10.1093/hmg/ddv277
Ioannidis N. M. Rothstein J. H. Pejaver V. Middha S. McDonnell S. K. Baheti S. et al. (2016). REVEL: an ensemble method for predicting the pathogenicity of rare missense variants. Am. J. Hum. Genet. 99, 877–885. doi: 10.1016/j.ajhg.2016.08.016, PMID: 27666373
Jabbari E. Koga S. Valentino R. R. Reynolds R. H. Ferrari R. Tan M. M. X. et al. (2021). Genetic determinants of survival in progressive supranuclear palsy: a genome-wide association study. Lancet Neurol. 20, 107–116. doi: 10.1016/S1474-4422(20)30394-X, PMID: 33341150
Karczewski K. J. Francioli L. C. Tiao G. Cummings B. B. Alföldi J. Wang Q. et al. (2020). The mutational constraint spectrum quantified from variation in 141,456 humans. Nature 581, 434–443. doi: 10.1038/s41586-020-2308-7, PMID: 32461654
Karimi-Moghadam A. Charsouei S. Bell B. Jabalameli M. R. (2018). Parkinson disease from mendelian forms to genetic susceptibility: new molecular insights into the neurodegeneration process. Cell. Mol. Neurobiol. 38, 1153–1178. doi: 10.1007/s10571-018-0587-4, PMID: 29700661
Kay D. M. Stevens C. F. Hamza T. H. Montimurro J. S. Zabetian C. P. Factor S. A. et al. (2010). A comprehensive analysis of deletions, multiplications, and copy number variations in PARK2. Neurology 75, 1189–1194. doi: 10.1212/WNL.0b013e3181f4d832, PMID: 20876472
Kilarski L. L. Pearson J. P. Newsway V. Majounie E. Knipe M. D. W. Misbahuddin A. et al. (2012). Systematic review and UK-based study of PARK2 (parkin), PINK1, PARK7 (DJ-1) and LRRK2 in early-onset Parkinson’s disease: PARK2, PINK1, PARK7, LRRK2 in EOPD. Mov. Disord. 27, 1522–1529. doi: 10.1002/mds.25132, PMID: 22956510
Kim S. Y. Seong M. W. Jeon B. S. Kim S. Y. Ko H. S. Kim J. Y. et al. (2012). Phase analysis identifies compound heterozygous deletions of the PARK2 gene in patients with early-onset Parkinson disease. Clin. Genet. 82, 77–82. doi: 10.1111/j.1399-0004.2011.01693.x, PMID: 21534944
Klein C. Lohmann-Hedrich K. Rogaeva E. Schlossmacher M. G. Lang A. E. (2007). Deciphering the role of heterozygous mutations in genes associated with parkinsonism. Lancet Neurol. 6, 652–662. doi: 10.1016/S1474-4422(07)70174-6
Kouri N. Ross O. A. Dombroski B. Younkin C. S. Serie D. J. Soto-Ortolaza A. et al. (2015). Genome-wide association study of corticobasal degeneration identifies risk variants shared with progressive supranuclear palsy. Nat. Commun. 6:7247. doi: 10.1038/ncomms8247, PMID: 26077951
La Cognata V. Morello G. D’Agata V. Cavallaro S. (2017). Copy number variability in Parkinson’s disease: assembling the puzzle through a systems biology approach. Hum. Genet. 136, 13–37. doi: 10.1007/s00439-016-1749-4, PMID: 27896429
Landrum M. J. Lee J. M. Riley G. R. Jang W. Rubinstein W. S. Church D. M. et al. (2014). ClinVar: public archive of relationships among sequence variation and human phenotype. Nucleic Acids Res. 42, D980–D985. doi: 10.1093/nar/gkt1113
Langston R. G. Cookson M. R. (2020). Pathways of protein synthesis and degradation in PD pathogenesis. Prog. Brain Res. 252, 217–270. doi: 10.1016/bs.pbr.2020.01.002
Lesage S. Brice A. (2009). Parkinson’s disease: from monogenic forms to genetic susceptibility factors. Hum. Mol. Genet. 18, R48–R59. doi: 10.1093/hmg/ddp012
Lewis C. M. Vassos E. (2020). Polygenic risk scores: from research tools to clinical instruments. Genome Med. 12:44. doi: 10.1186/s13073-020-00742-5, PMID: 32423490
Litvan I. Agid Y. Calne D. Campbell G. Dubois B. Duvoisin R. C. et al. (1996). Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop*. Neurology 47, 1–9. doi: 10.1212/WNL.47.1.1
Litvan I. Bhatia K. P. Burn D. J. Goetz C. G. Lang A. E. McKeith I. et al. (2003). SIC task force appraisal of clinical diagnostic criteria for parkinsonian disorders. Mov. Disord. 18, 467–486. doi: 10.1002/mds.10459
Liu X. Cheng R. Ye X. Verbitsky M. Kisselev S. Mejia-Santana H. et al. (2013). Increased rate of sporadic and recurrent rare genic copy number variants in Parkinson’s disease among Ashkenazi Jews. Mol. Genet. Genomic Med. 1, 142–154. doi: 10.1002/mgg3.18, PMID: 24073418
Lubbe S. J. Bustos B. I. Hu J. Krainc D. Joseph T. Hehir J. et al. (2021). Assessing the relationship between monoallelic PRKN mutations and Parkinson’s risk. Hum. Mol. Genet. 30, 78–86. doi: 10.1093/hmg/ddaa273, PMID: 33448283
MacDonald J. R. Ziman R. Yuen R. K. C. Feuk L. Scherer S. W. (2014). The database of genomic variants: a curated collection of structural variation in the human genome. Nucl. Acids Res. 42, D986–D992. doi: 10.1093/nar/gkt958, PMID: 24174537
Macnee M. Pérez-Palma E. Brünger T. Klöckner C. Platzer K. Stefanski A. et al. (2023). CNV-ClinViewer: enhancing the clinical interpretation of large copy-number variants online. Bioinformatics 39:btad290. doi: 10.1093/bioinformatics/btad290, PMID: 37104749
Makarious M. B. Lake J. Pitz V. Ye Fu A. Guidubaldi J. L. Solsberg C. W. et al. (2023). Large-scale rare variant burden testing in Parkinson’s disease. Brain 146, 4622–4632. doi: 10.1093/brain/awad214, PMID: 37348876
Manichaikul A. Mychaleckyj J. C. Rich S. S. Daly K. Sale M. Chen W.-M. (2010). Robust relationship inference in genome-wide association studies. Bioinformatics 26, 2867–2873. doi: 10.1093/bioinformatics/btq559, PMID: 20926424
Mata I. F. (2004). Parkin genetics: one model for Parkinson’s disease. Hum. Mol. Genet. 13, 127R–133R. doi: 10.1093/hmg/ddh089
McKeith I. G. Dickson D. W. Lowe J. Emre M. O’Brien J. T. Feldman H. et al. (2005). Diagnosis and management of dementia with Lewy bodies: third report of the DLB consortium. Neurology 65, 1863–1872. doi: 10.1212/01.wnl.0000187889.17253.b1
Menon P. J. Sambin S. Criniere-Boizet B. Courtin T. Casse F. Tesson C. et al. (2023). Genotype-Phenotype correlation in Parkin-Parkinson’s disease (P3-11.012). Presented at the 2023 Annual Meeting Abstracts, Lippincott Williams & Wilkins, p. 2970.
Myers A. J. Kaleem M. Marlowe L. Pittman A. M. Lees A. J. Fung H. C. et al. (2005). The H1c haplotype at the MAPT locus is associated with Alzheimer’s disease. Hum. Mol. Genet. 14, 2399–2404. doi: 10.1093/hmg/ddi241, PMID: 16000317
Nalls M. A. Blauwendraat C. Vallerga C. L. Heilbron K. Bandres-Ciga S. Chang D. et al. (2019). Identification of novel risk loci, causal insights, and heritable risk for Parkinson’s disease: a meta-analysis of genome-wide association studies. Lancet Neurol. 18, 1091–1102. doi: 10.1016/S1474-4422(19)30320-5, PMID: 31701892
Neary D. Snowden J. S. Gustafson L. Passant U. Stuss D. Black S. et al. (1998). Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 51, 1546–1554. doi: 10.1212/WNL.51.6.1546
Pachchek S. Landoulsi Z. Pavelka L. Schulte C. Buena-Atienza E. Gross C. et al. (2023). Accurate long-read sequencing identified GBA1 as major risk factor in the Luxembourgish Parkinson’s study. NPJ Parkinsons Dis 9:156. doi: 10.1038/s41531-023-00595-w
Pankratz N. Dumitriu A. Hetrick K. N. Sun M. Latourelle J. C. Wilk J. B. et al. (2011). Copy number variation in familial Parkinson disease. PLoS One 6:e20988. doi: 10.1371/journal.pone.0020988, PMID: 21829596
Pavelka L. Rauschenberger A. Landoulsi Z. Pachchek S. May P. Glaab E. et al. (2022). Publisher correction: age at onset as stratifier in idiopathic Parkinson’s disease – effect of ageing and polygenic risk score on clinical phenotypes. NPJ Parkinsons Dis. 8:112. doi: 10.1038/s41531-022-00378-9
Pennings M. Meijer R. P. P. Gerrits M. Janssen J. Pfundt R. De Leeuw N. et al. (2023). Copy number variants from 4800 exomes contribute to ~7% of genetic diagnoses in movement disorders, muscle disorders and neuropathies. Eur. J. Hum. Genet. 31, 654–662. doi: 10.1038/s41431-023-01312-0, PMID: 36781956
Pittman A. M. (2005). Linkage disequilibrium fine mapping and haplotype association analysis of the tau gene in progressive supranuclear palsy and corticobasal degeneration. J. Med. Genet. 42, 837–846. doi: 10.1136/jmg.2005.031377
Rentzsch P. Witten D. Cooper G. M. Shendure J. Kircher M. (2019). CADD: predicting the deleteriousness of variants throughout the human genome. Nucleic Acids Res. 47, D886–D894. doi: 10.1093/nar/gky1016, PMID: 30371827
Sardi S. P. Cedarbaum J. M. Brundin P. (2018). Targeted therapies for Parkinson’s disease: from genetics to the clinic: targeted therapies for PD. Mov. Disord. 33, 684–696. doi: 10.1002/mds.27414, PMID: 29704272
Sarihan E. I. Pérez-Palma E. Niestroj L. Loesch D. Inca-Martinez M. Horimoto A. R. V. R. et al. (2021). Genome-wide analysis of copy number variation in Latin American Parkinson’s disease patients. Mov. Disord. 36, 434–441. doi: 10.1002/mds.28353, PMID: 33150996
Schüle B. Hatchwell E. Eis P. S. Langston J. W. (2015). Comparative genomic hybridization solves a 14-year-old PARKIN mystery. Ann. Neurol. 78, 663–664. doi: 10.1002/ana.24478, PMID: 26179350
Shu L. Zhang Y. Sun Q. Pan H. Tang B. (2019). A comprehensive analysis of population differences in LRRK2 variant distribution in Parkinson’s disease. Front. Aging Neurosci. 11:13. doi: 10.3389/fnagi.2019.00013, PMID: 30760999
Skipper L. Wilkes K. Toft M. Baker M. Lincoln S. Hulihan M. et al. (2004). Linkage disequilibrium and association of MAPT H1 in Parkinson disease. Am. J. Hum. Genet. 75, 669–677. doi: 10.1086/424492, PMID: 15297935
Tang B. Xiong H. Sun P. Zhang Y. Wang D. Hu Z. et al. (2006). Association of PINK1 and DJ-1 confers digenic inheritance of early-onset Parkinson’s disease. Hum. Mol. Genet. 15, 1816–1825. doi: 10.1093/hmg/ddl104, PMID: 16632486
The 1000 Genomes Project Consortium (2012). An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56–65. doi: 10.1038/nature11632, PMID: 23128226
Toft M. Ross O. A. (2010). Copy number variation in Parkinson’s disease. Genome Med. 2:62. doi: 10.1186/gm183, PMID: 20828427
Wang K. Li M. Hadley D. Liu R. Glessner J. Grant S. F. A. et al. (2007). PennCNV: an integrated hidden Markov model designed for high-resolution copy number variation detection in whole-genome SNP genotyping data. Genome Res. 17, 1665–1674. doi: 10.1101/gr.6861907, PMID: 17921354
Wang K. Li M. Hakonarson H. (2010). ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38:e164. doi: 10.1093/nar/gkq603, PMID: 20601685
Wen Y. Zhou Y. Jiao B. Shen L. (2021). Genetics of progressive supranuclear palsy: a review. JPD 11, 93–105. doi: 10.3233/JPD-202302, PMID: 33104043
Yu E. Rudakou U. Krohn L. Mufti K. Ruskey J. A. Asayesh F. et al. (2021). Analysis of heterozygous PRKN variants and copy-number variations in Parkinson’s disease. Mov. Disord. 36, 178–187. doi: 10.1002/mds.28299, PMID: 32970363
Zabetian C. P. Hutter C. M. Factor S. A. Nutt J. G. Higgins D. S. Griffith A. et al. (2007). Association analysis of MAPT H1 haplotype and subhaplotypes in Parkinson’s disease. Ann. Neurol. 62, 137–144. doi: 10.1002/ana.21157, PMID: 17514749