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Abstract

Summary Background

An understanding of the genetic mechanisms underlying diseases in ancestrally diverse populations is an important step towards development of targeted treatments. Research in African and African admixed populations can enable mapping of complex traits, because of their genetic diversity, extensive population substructure, and distinct linkage disequilibrium patterns. We aimed to do a comprehensive genome-wide assessment in African and African admixed individuals to better understand the genetic architecture of Parkinson's disease in these underserved populations.

Methods

We performed a genome-wide association study (GWAS) in people of African and African admixed ancestry with and without Parkinson's disease. Individuals were included from several cohorts that were available as a part of the Global Parkinson's Genetics Program, the International Parkinson's Disease Genomics Consortium Africa, and 23andMe. A diagnosis of Parkinson's disease was confirmed clinically by a movement disorder specialist for every individual in each cohort, except for 23andMe, in which it was self-reported based on clinical diagnosis. We characterised ancestry-specific risk, differential haplotype structure and admixture, coding and structural genetic variation, and enzymatic activity.

Findings

We included 197 918 individuals (1488 cases and 196 430 controls) in our genome-wide analysis. We identified a novel common risk factor for Parkinson's disease (overall meta-analysis odds ratio for risk of Parkinson's disease 1·58 [95% CI 1·37–1·80], p=2·397 × 10−14) and age at onset at the GBA1 locus, rs3115534-G (age at onset β=–2·00 [SE=0·57], p=0·0005, for African ancestry; and β=–4·15 [0·58], p=0·015, for African admixed ancestry), which was rare in non-African or non-African admixed populations. Downstream short-read and long-read whole-genome sequencing analyses did not reveal any coding or structural variant underlying the GWAS signal. The identified signal seems to be associated with decreased glucocerebrosidase activity.

Interpretation

Our study identified a novel genetic risk factor in GBA1 in people of African ancestry, which has not been seen in European populations, and it could be a major mechanistic basis of Parkinson's disease in African populations. This population-specific variant exerts substantial risk on Parkinson's disease as compared with common variation identified through GWAS and it was found to be present in 39% of the cases assessed in this study. This finding highlights the importance of understanding ancestry-specific genetic risk in complex diseases, a particularly crucial point as the Parkinson's disease field moves towards targeted treatments in clinical trials. The distinctive genetics of African populations highlights the need for equitable inclusion of ancestrally diverse groups in future trials, which will be a valuable step towards gaining insights into novel genetic determinants underlying the causes of Parkinson's disease. This finding opens new avenues towards RNA-based and other therapeutic strategies aimed at reducing lifetime risk of Parkinson's disease.

Funding

The Global Parkinson's Genetics Program, which is funded by the Aligning Science Across Parkinson's initiative, and The Michael J Fox Foundation for Parkinson's Research.

Details

Title
Identification of genetic risk loci and causal insights associated with Parkinson's disease in African and African admixed populations: a genome-wide association study
Author
Rizig, Mie 1 ; Bandres-Ciga, Sara 2 ; Makarious, Mary B 3 ; Ojo, Oluwadamilola Omolara 4 ; Peter Wild Crea 5 ; Oladunni, Victoria Abiodun 6 ; Levine, Kristin S 7 ; Sani Atta Abubakar 8 ; Achoru, Charles Obiora 9 ; Vitale, Dan 10 ; Olaleye Akinmola Adeniji 11 ; Osigwe Paul Agabi 4 ; Koretsky, Mathew J 2 ; Agulanna, Uchechi 12 ; Hall, Deborah A 13 ; Akinyemi, Rufus Olusola 14 ; Xie, Tao 15 ; Ali, Mohammed Wulgo 16 ; Shamim, Ejaz A 17 ; Ani-Osheku, Ifeyinwa 18 ; Padmanaban, Mahesh 15 ; Ohwotemu, Michael Arigbodi 19 ; Standaert, David G 20 ; Abiodun Hamzat Bello 21 ; Dean, Marissa N 20 ; Erameh, Cyril Oshomah 22 ; Elsayed, Inas 23 ; Temitope Hannah Farombi 24 ; Okunoye, Olaitan 1 ; Fawale, Michael Bimbola 25 ; Billingsley, Kimberley J 5 ; Imarhiagbe, Frank Aiwansoba 26 ; Pilar Alvarez Jerez 27 ; Iwuozo, Emmanuel Uzodinma 28 ; Baker, Breeana 2 ; Morenikeji Adeyoyin Komolafe 25 ; Malik, Laksh 2 ; Nwani, Paul Osemeke 29 ; Daida, Kensuke 5 ; Nwazor, Ernest Okwundu 30 ; Miano-Burkhardt, Abigail 5 ; Yakub Wilberforce Nyandaiti 31 ; Zih-Hua Fang 32 ; Yahaya Olugbo Obiabo 33 ; Kluss, Jillian H 34 ; Olanike Adedoyin Odeniyi 35 ; Hernandez, Dena G 34 ; Odiase, Francis Ehidiamen 26 ; Tayebi, Nahid 36 ; Francis Ibe Ojini 4 ; Sidranksy, Ellen 36 ; Onwuegbuzie, Gerald Awele 37 ; D'Souza, Andrea M 36 ; Godwin Osawaru Osaigbovo 9 ; Berhe, Bahafta 36 ; Osemwegie, Nosakhare 38 ; Reed, Xylena 2 ; Oshinaike, Olajumoke Olufemi 39 ; Leonard, Hampton L 7 ; Otubogun, Folajimi Morenikeji 40 ; Alvarado, Chelsea X 7 ; Oyakhire, Shyngle Imiewan 41 ; Ozomma, Simon Izuchukwu 42 ; Samuel, Sarah Chabiri 31 ; Taiwo, Funmilola Tolulope 24 ; Wahab, Kolawole Wasiu 43 ; Yusuf Agboola Zubair 41 ; Iwaki, Hirotaka 7 ; Jonggeol Jeffrey Kim 5 ; Morris, Huw R 1 ; Hardy, John 44 ; Nalls, Mike A 10 ; Heilbron, Karl 45 ; Norcliffe-Kaufmann, Lucy 45 ; Okubadejo, Njideka; Ojo, Oluwadamilola; Oladunni Abiodun; Achoru, Charles; Agabi, Osigwe; Akinyemi, Rufus; Ali, Mohammed; Arigbodi, Ohwotemu; Bello, Abiodun; Erameh, Cyril; Farombi, Temitope; Fawale, Michael; Imarhiagbe, Frank; Iwuozo, Emmanuel; Komolafe, Morenikeji; Nwani, Paul; Nwazor, Ernest; Nyandaiti, Yakub; Yahaya Obiabo; Odeniyi, Olanike; Odiase, Francis; Ojini, Francis; Onwuegbuzie, Gerald; Godwin Osaigbovo; Oshinaike, Olajumoke; Otubogun, Folajimi; Oyakhire, Shyngle; Ozomma, Simon; Samuel, Sarah; Taiwo, Funmilola; Wahab, Kolawole; Zubair, Yusuf; Daniel Gams Massi; Eric Gueumekane Bila lamou; Nfor, Leonard Njamnshi; Magnerou, Mélanie Annick; Fogoum, Yannick Fogang; Shalash, Ali; El-FawaI, Hassan; Khedr, Eman; Gharib Fawi; Eltantawi, Mohamed A; Salama, Mohamed; El-Jaafary, Shaimaa; Hamed, Sharifa; Abenet Tafesse Mengesha; Biniyam Alemayehu Ayele; Dereje Melka Oda; Yared Zenebe Zewde; Yohanesse Debebe Gelan; AkpaIu, Albert; Charway-Felli, Augustina; Sarfo, Fred Stephen; Adjei, Patrick; Obese, Vida; Bocoum, Abdoulaye; Koita, Abdou; Guinto, Cheick Oumar; Coulibaly, Toumany; Maiga, Youssoufa; Kone, Zaynab; Bell, Abiodun; Adebowale, Akintunde A; Akpekpe, John; lyagba, Alagoma; Ali Mohammed Wulgo; Arabambi, Babawale; Agu, Christian; Franklin Dike; Ishola, Ismail; Kehinde Abiodun; Ekenze, Oluchi; Paul Agabi Osigwe; Salisu Balarabe; Sani Abubakar; Williams, Uduak; Fall, Maouly; Diop, Alassane Mamadou; Ewodo Touna Hilaire Dominique; Mochan, Andre; Modi, Girish; Dindayal, Saiesha; Eman Ali Awadelkareem; Dahawi, Maha; Mosab Ali Awadelkareem; Misbah, Sarah; Brighton Mushengez; Kimambo, Henrika; Msango, Leonard; Adebayo, Philip; OKeng, Kigocha; Diekker, Marieke; URassa, Sarah; Gouider, Riadh; Mouna Ben Djebara; Gargouri, Amina; Kacem, Imen; Nasri, Amina; Mrabet, Saloua; Sghaier, Ikram; Mkada, Imen; Atadzhanov, Masharip; Chishimba, Lorraine; Fatumah Jama; Houlden, Henry; Singleton, Andrew; Nalls, Mike; Ejaz Shamim; Cabell Jonas; Williamson, Jared; Rosenbaum, Marc; Davis, Staci; Dean, Marissa; Cromer, Candace; Smith, Jenna; Ruffrage, Lauren; Richardson, Joseph; Sipma, Rebeka; Padmanaban, Manesh; Warren, Natalie; Mercado, Tomas; Disbrow, Elizabeth; Chauppeta, Brian; Thomas-Dean, Fermine; Toms, Jamie; Lofton, Katelyn; Rawls, Ashley; Rizer, Kyle; Black, Nieci; Solle, Justin; O'Grady, Alyssa; Sherer, Todd; Fiske, Brian; Blauwendraat, Cornelis 5 ; Njideka Ulunma Okubadejo 46 ; A Nazlı Başak; Ai Huey Tan; Noyce, Alastair; Akpalu, Albert; Espay, Alberto; Martínez-Carrasco, Alejandro; Medina, Alex; Zimprich, Alexander; Brice, Alexis; Karimova, Altynay; Hernandez, Alvaro; Illarionova, Anastasia; Quattrone, Andrea; Singleton, Andrew B; Sobering, Andrew K; Vinuela, Angel; Arinola Sanyaolu; Schumacher-Schuh, Artur F; Kishore, Asha; Ahmad-Annuar, Azlina; Bashayer Al Mubarak; Tang, Beisha; Benjamin Pizarro Galleguillos; Jeon, Beomseok; Siddiqi, Bernadette; Casey, Bradford; Mollenhauer, Brit; Carroll, Camille; Rieder, Carlos; Pantazis, Caroline B; Comart, Charisse; Chin-Hsien, Lin; Klein, Christine; Bale, Claire; Shepherd, Claire E; Wegel, Claire; Martinez-Ramirez, Daniel; Hall, Deborah; Hernandez, Dena; Divya, K P; Nguyen, Duan; Fon, Edward A; Dadiotis, Efthymios; Riley, Ekemini; Iakovenko, Elena; Stafford, Ellie; Gatto, Emilia M; Valente, Enza Maria; Eva-Juliane Vollstedt; Faghri, Faraz; Genc, Gencer; Xiromerisiou, Georgia; Hadjigorgiou, Georgios; Chan, Germaine Hiu-Fai; Arboleda, Gonzalo; Kaishibayeva, Gulnaz; Höglinger, Günter; Hampton, Leonard; Madoev, Harutyun; Chen, Honglei; Wu, Hsiu-Chuan; Shang, Huifang; Mata, Ignacio F; Ignacio Juan Keller Sarmiento; Dagklis, Ioannis; Tarnanas, Ioannis; Aasly, Jan O; Hoenicka, Janet; Corvol, Jean-Christophe; Jia Nee Foo; Guo, Jifeng; Junker, Johanna; Carr, Jonathan; Jonggeol Jeff Kim; Orozco, Jorge; Jankovic, Joseph; Shulman, Joshua; Hunter, Julie; Solle, Justin C; Murphy, Kaileigh; Nuytemans, Karen; Kieburtz, Karl; Lohmann, Katja; Marek, Kenneth; Mok, Kin Ying; Kumar, Kishore; Levine, Kristin; Chahine, Lana M; Lange, Lara M; Pihlstrøm, Lasse; Screven, Laurel; Stefanis, Leonidas; Shulman, Lisa; Marsili, Luca; Parnetti, Lucilla; Kuhl, Maggie; Funayama, Manabu; Sharma, Manu; Tan, Manuela; Kauffman, Marcelo; Miranda, Marcelo; Bustamante, Maria Leonor; Stamelou, Maria; Maria Teresa Periñan Tocino; Cornejo-Olivas, Mario; Marlene Jimenez del Rio; Koretsky, Mathew; Rodriguez-Violante, Mayela; Ellis, Melina; Avenali, Micol; Rentería, Miguel E; Inca-Martines, Miguel z; Mohamed Ibrahim Norlinah; Umair, Muhammad; Ip, Nancy; Louie, Naomi; Cheung, Nelson Yuk-Fai; Mencacci, Niccolò Emanuele; Wood, Nicholas; Williams, Nigel; Hattori, Nobutaka; Nor Azian Abdul Murad; Norlinah Mohamed Ibrahim; Oury Monchi; Çakmak, Özgür Öztop; Patricio Öztop Çakmak Öztop Çakmak; Lewis, Patrick Alfryn; Pastor, Pau; Reyes-Pérez, Paula; Awad, Paula Saffie; Chana, Pedro; Chan, Phillip; Pin-Jui Kung; Chan, Piu; Pal, Pramod; Prashanth Lingappa Kukkle; Ojha, Rajeev; Kaiyrzhanov, Rauan; Krüger, Rejko; Amouri, Rim; Weil, Rimona; Rajan, Roopa; Alcalay, Roy; Wu, Ruey-Meei; Borgohain, Rupam; Samia Ben Sassi; Khachatryan, Samson; El-Sadig, Sarah; Wu, Serena; Groppa, Sergio; Azmin, Shahrul; Shen-Yang, Lim; Ur-Rehman, Shoaib; Ertan, Sibel; Stott, Simon; Jasaitye, Simona; Chowdhury, Sohini; Dumanis, Sonya; Bardien, Soraya; Lubbe, Steven; Koks, Sulev; Dey, Sumit; Foroud, Tatiana; Fon, Ted; Beach, Thomas; Gasser, Thomas; Anderson, Tim; Nguyen, Toan; Schirinzi, Tommaso; Shiraishi, Tomotaka; Pitcher, Toni; Tumas, Vitor; Mohamed, Wael; Kamel, Walaa A; Luo, Wei; Zhou, Xiaopu; Zewde, Yared Z; Song, Yeajin; Wen, Yi; Wu, Yihru; Kim, Yun Joong; Tavadyan, Zaruhi

 Department of Neuromuscular Diseases, UCL Queen Square Institute of Neurology, London, UK 
 Center for Alzheimer's and Related Dementias, National Institute on Aging and National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA 
 UCL Movement Disorders Centre, University College London, London, UK; Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA 
 College of Medicine, University of Lagos, Idi Araba, Lagos State, Nigeria 
 Center for Alzheimer's and Related Dementias, National Institute on Aging and National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA; Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA 
 General Hospital, Isolo, Lagos State, Nigeria 
 Center for Alzheimer's and Related Dementias, National Institute on Aging and National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA; Data Tecnica International, Washington, DC, USA 
 Ahmadu Bello University, Zaria, Kaduna State, Nigeria 
 Jos University Teaching Hospital, Jos, Plateau State, Nigeria 
10  Data Tecnica International, Washington, DC, USA 
11  Federal Medical Centre, Abeokuta, Ogun State, Nigeria 
12  Lagos University Teaching Hospital, Idi Araba, Lagos State, Nigeria 
13  Department of Neurological Sciences, Rush University Medical Center, Chicago, IL, USA 
14  Neuroscience and Ageing Research Unit, Institute for Advanced Medical Research and Training, College of Medicine, University of Ibadan, Ibadan, Oyo State, Nigeria 
15  Department of Neurology, University of Chicago Medicine, Chicago, IL, USA 
16  Federal Teaching Hospital Gombe, Gombe State, Nigeria 
17  Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA; Kaiser Permanente Mid-Atlantic States, Largo, MD, USA; MidAtlantic Permanente Research Institute, Rockville, MD, USA 
18  Asokoro District Hospital, Asokoro, Abuja, Nigeria 
19  Delta State University, Abraka, Delta State, Nigeria 
20  Department of Neurology, University of Alabama at Birmingham, Birmingham, AL, USA 
21  University of Ilorin Teaching Hospital, Ilorin, Kwara State, Nigeria 
22  Irrua Specialist Teaching Hospital, Irrua, Edo State, Nigeria 
23  Faculty of Pharmacy, University of Gezira, Wadmadani, Sudan 
24  University College Hospital, Ibadan, Oyo State, Nigeria 
25  Obafemi Awolowo University, Ile-Ife, Osun State, Nigeria 
26  University of Benin, Benin City, Edo State, Nigeria 
27  Department of Neuromuscular Diseases, UCL Queen Square Institute of Neurology, London, UK; Center for Alzheimer's and Related Dementias, National Institute on Aging and National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA 
28  Benue State University, Makurdi, Benue State, Nigeria 
29  Nnamdi Azikiwe University Teaching Hospital, Nnewi, Anambra State, Nigeria 
30  Rivers State University Teaching Hospital, Port Harcourt, Rivers State, Nigeria 
31  University of Maiduguri Teaching Hospital, Maiduguri, Borno State, Nigeria 
32  German Center for Neurodegenerative Diseases, Tuebingen, Germany 
33  Federal University of Health Sciences, Otukpo, Benue State, Nigeria 
34  Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA 
35  General Hospital, Lagos Island, Lagos State, Nigeria 
36  Medical Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA 
37  University of Abuja, Abuja, Federal Capital Territory, Nigeria 
38  University of Port Harcourt, Port Harcourt, Rivers State, Nigeria 
39  Lagos State University College of Medicine, Ikeja, Lagos State, Nigeria 
40  Federal Medical Center, Ebute Metta, Lagos State, Nigeria 
41  National Hospital, Abuja, Federal Capital Territory, Nigeria 
42  University of Calabar Teaching Hospital, Calabar, Cross River State, Nigeria 
43  University of Ilorin Teaching Hospital, Ilorin, Kwara State, Nigeria; University of Ilorin, Ilorin, Kwara State, Nigeria 
44  Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, London, UK 
45  23andMe, Sunnyvale, CA, USA 
46  College of Medicine, University of Lagos, Idi Araba, Lagos State, Nigeria; Lagos University Teaching Hospital, Idi Araba, Lagos State, Nigeria 
Pages
1015-1025
Section
Articles
Publication year
2023
Publication date
Nov 2023
Publisher
Elsevier Limited
ISSN
14744422
e-ISSN
14744465
Source type
Scholarly Journal
Language of publication
English
ProQuest document ID
2881756112
Copyright
©2023. Elsevier Ltd