SARS-CoV-2 susceptibility and COVID-19 disease severity are associated with genetic variants affecting gene expression in a variety of tissues
Matteo D’Antonio(University of California San Diego), Jennifer Nguyen(University of California San Diego), Timothy D. Arthur(University of California San Diego), Hiroko Matsui(University of California San Diego), Agnieszka D’Antonio‐Chronowska(University of California San Diego), Kelly A. Frazer(University of California San Diego), Benjamin M. Neale, Mark J. Daly, Andrea Ganna, Christine Stevens, Gita A. Pathak, Shea J. Andrews, Masahiro Kanai, Mattia Cordioli, Andrea Ganna, Juha Karjalainen, Gita A. Pathak, Renato Polimanti, Shea J. Andrews, Mattia Cordioli, Matti Pirinen, Masahiro Kanai, Nadia V. Harerimana, Kumar Veerapen, Brooke Wolford, Huy Nguyen(University of California San Diego), Matthew Solomonson, Christine Stevens, Rachel G. Liao, Karolina Chwiałkowska, Amy Trankiem, Mary K. Balaconis, Caroline Hayward, Anne Richmond, Archie Campbell, Marcela Morris, Chloe Fawns‐Ritchie, Joseph Glessner, Douglas M. Shaw, Xiao Chang, Hannah Polikowski, Petty E. Lauren, Hung‐Hsin Chen, Wanying Zhu, Håkon Håkonarson, David J. Porteous, Jennifer E. Below(University of California San Diego), K.E. North, Joseph B. McCormick, Paul R. H. J. Timmers, James F. Wilson, Albert Tenesa, Kenton D’Mellow, Shona M. Kerr, Mari E.K. Niemi, Mattia Cordioli, Lindokuhle Nkambul, Kathrin Aprile von Hohenstaufen, Ali Sobh, Madonna M. Eltoukhy, Amr M. Yassen, M. Hegazy, Kamal Okasha, Mohammed Eid, Hanteera S. Moahmed, Doaa Shahin, Yasser M. El‐Sherbiny, Tamer Elhadidy, Mohamed S. Abd Elghafar, Jehan J. El‐Jawhari, Attia A. S. Mohamed, Marwa H. Elnagdy, Amr Samir, Mahmoud Abdel-Aziz, Walid T. Khafaga, Walaa M. El-Lawaty, Mohamed Torky, Mohamed El‐Shanshory, Chiara Batini, Paul H. Lee, Nick Shrine, Alexander T. Williams, Martin D. Tobin, Anna L. Guyatt, Catherine John, Richard Packer, Altaf Ali, Robert C. Free, Xueyang Wang, Louise V. Wain, Edward J. Hollox, Laura D. Venn, Catherine Bee, Emma L. Adams, Mari E.K. Niemi, Ahmadreza Niavarani, Mattia Cordioli, Lindokuhle Nkambul, Bahareh Sharififard, Rasoul Aliannejad, Ali Amirsavadkouhi, Zeinab Naderpour, Hengameh Ansari Tadi, Afshar Etemadi-Aleagha, Saeideh Ahmadi, Seyed Behrooz Mohseni Moghaddam, Alireza Adamsara, Morteza Saeedi, Hamed Abdollahi, Abdolmajid Hosseini, Pajaree Chariyavilaskul, Monpat Chamnanphon, Thitima B. Suttichet, Vorasuk Shotelersuk, Monnat Pongpanich, Chureerat Phokaew, Wanna Chetruengchai, Watsamon Jantarabenjakul, Opass Putchareon, Pattama Torvorapanit, Thanyawee Puthanakit, Pintip Suchartlikitwong, Nattiya Hirankarn, Voraphoj Nilaratanakul, Pimpayao Sodsai, Ben Brumpton, Kristian Hveem, Cristen J. Willer, Brooke Wolford, Wei Zhou, Tormod Rogne, Erik Solligård, Bjørn Olav Åsvold, Malak Abedalthagafi, Manal Alaamery, Saleh A. Alqahtani, Dona Baraka, Fawz Al Harthi, Ebtehal Alsolm, Leen Abu Safieh, Albandary M. Alowayn, Fatimah Alqubaishi, Amal Al Mutairi, Serghei Mangul, Abdulraheem Alshareef, Mona Sawaji, Mansour Almutairi, Nora Aljawini, Nour Albesher, Yaseen M. Arabi, Ebrahim Mahmoud, Amin Khattab, Roaa T. Halawani, Ziab Z. Alahmadey, Jehad K. Albakri, Walaa A. Felemban, Bandar A. Suliman, Rana Hasanato, Laila Alawdah, Jahad Alghamdi, Deema AlZahrani, Sameera Aljohani, Hani Al-Afghani, May Alrashed, Nouf AlDhawi, Hadeel AlBardis, Sarah Alkwai, Moneera Alswailm, Faisal A. Almalki, Maha Albeladi, Iman Almohammed, Eman Barhoush, Anoud Albader, Salam Massadeh, Abdulaziz Almalik, Sara Jeza Alotaibi, Bader Alghamdi, Junghyun Jung, Mohammad Fawzy, Yunsung Lee, Per Magnus, Lill-Iren S. Trogstad, Øyvind Helgeland, Jennifer R. Harris, Massimo Mangino, Tim D. Spector, Duncan Emma, Sandra Smieszek, Bartlomiej Przychodzen, Christos Polymeropoulos, Vasilios M. Polymeropoulos, Mihael H. Polymeropoulos, Israel Fernández‐Cadenas, Jordi Pérez‐Tur, Laia Llucià‐Carol, Natàlia Cullell, Elena Muiño, Jara Cárcel‐Márquez, Marta L. DeDiego, L. Lloret Iglesias, Anna M. Planas, Àlex Soriano, Verónica Rico, Daiana Agüero, Josep Lluís Bedini, Francisco Lozano, Carlos Domingo, Verónica Robles, Francisca Ruíz-Jaén, Leonardo Márquez, Juan Manuel López Gómez, Eliécer Coto, Guillermo M. Albaiceta, Marta García‐Clemente, David Dalmau, María J. Arranz, Beatriz Dietl, Alex Serra-Llovich, Pere Soler, Roger Colobrán, Andrea Martín‐Nalda, Alba Parra-Martínez, David Bernardo, Silvia Rojo, Aida Fiz‐López, Elisa Arribas‐Rodríguez, Paloma Cal‐Sabater, Tomás Segura, Esther González-Villa, Gemma Serrano‐Heras, Joan Martí‐Fábregas, Elena Jiménez‐Xarrié, Alicia de Felipe Mimbrera, Jaime Masjuán, Sebastián García‐Madrona, Anna Domínguez-Mayoral, Joan Montaner Villalonga, Paloma Menéndez-Valladares, Daniel I. Chasman, Julie E. Buring, Paul M. Ridker, Franco Giulianini, Howard D. Sesso, JoAnn E. Manson, Xiao Chang, Joseph R. Glessner, Håkon Håkonarson, Caroline Hayward, Anne Richmond, David J. Porteous, Archie Campbell, Chloe Fawns‐Ritchie, Carolina Medina‐Gómez, André G. Uitterlinden, M. Arfan Ikram, Kati Kristiansson, Sami Koskelainen, Markus Perola, Kati Donner, Katja Kivinen, Aarno Palotie, Samuli Ripatti, Sanni Ruotsalainen, Mari Kaunisto, FinnGen, Tomoko Nakanishi, Guillaume Butler‐Laporte, Vincenzo Forgetta, David Morrison, Biswarup Ghosh, Lætitia Laurent, Alexandre Bélisle, Danielle Henry, Tala Abdullah, Olumide Adeleye, Noor Mamlouk, Nofar Kimchi, Zaman Afrasiabi, Nardin Rezk Branka Vulesevic, Meriem Bouab, Charlotte Guzman, Louis Petitjean, Chris Tselios, Xiaoqing Xue, Erwin Schurr, Jonathan Afilalo, Marc Afilalo, Maureen Oliveira, Bluma Brenner, Pierre Lepage, Jiannis Ragoussis, Daniel Auld, Nathalie Brassard, Madéleine Durand, Michaël Chassé, Daniel E. Kaufmann, G. Mark Lathrop, Vincent Mooser, J. Brent Richards, Rui Li, Darin Adra, Souad Rahmouni, Michel Georges, Michel Moutschen, Benoît Misset, Gilles Darcis, Julien Guiot, Julien Guntz, Samira Azarzar, Stéphanie Gofflot, Y Beguin, Sabine Claassen, Olivier Malaise, Pascale Huynen, Christelle Meuris, Marie Thys, Jessica Jacques, Philippe Léonard, Frédéric Frippiat, Jean‐Baptiste Giot, Anne-Sophie Sauvage, Christian Von Frenckell, Yasmine Belhaj, Bernard Lambermont, Mari E.K. Niemi, Mattia Cordioli, Sara Pigazzini, Lindokuhle Nkambule, Michelle Daya, Jonathan Shortt, Nicholas Rafaels, Stephen J. Wicks, Kristy Crooks, Kathleen C. Barnes, Christopher R. Gignoux, Sameer Chavan, Triin Laisk, Kristi Läll, Maarja Lepamets, Reedik Mägi, Tõnu Esko, Ene Reimann, Lili Milani, Helene Alavere, Kristjan Metsalu, Mairo Puusepp, Andres Metspalu, Paul Naaber, Edward Laane, Jaana Pesukova, Pärt Peterson, Kai Kisand, Jekaterina Tabri, Raili Allos, Kati Hensen, Joel Starkopf, Inge Ringmets, Anu Tamm, Anne Kallaste, Pierre–Yves Bochud, Carlo Rivolta, Stéphanie Bibert, Mathieu Quinodoz, Dhryata Kamdar, Noémie Boillat‐Blanco, Semira Gonseth, Werner C. Albrich, Noémie Suh, Dionysios Neofytos, Véronique Erard, Cathy Voide, FHoGID, RegCOVID, P-PredictUs, SeroCOVID, CRiPSI, Rafael de Cid, Iván Galván‐Femenía, Natàlia Blay, Anna Carreras, Beatriz Cortés, Xavier Farré, Lauro Sumoy, Vı́ctor Moreno, Josep M. Mercader, Marta Guindo-Martínez, David Torrents, Manolis Kogevinas, Judith García‐Aymerich, Gemma Castaño‐Vinyals, Carlota Dobaño, Alessandra Renieri, Francesca Mari, Chiara Fallerini, Sergio Daga, Elisa Benetti, Margherita Baldassarri, Francesca Fava, Elisa Frullanti, Floriana Valentino, Gabriella Doddato, Annarita Giliberti, Rossella Tita, Sara Amitrano, Mirella Bruttini, Susanna Croci, Ilaria Meloni, Maria Antonietta Mencarelli, Caterina Lo Rizzo, Anna Maria Pinto, Giada Beligni, Andréa Tommasi, Laura Di Sarno, Maria Palmieri, Miriam Lucia Carriero, Diana Alaverdian, Stefano Busani, Raffaele Bruno, Marco Vecchia, Mary Ann Belli, Nicola Picchiotti, Maurizio Sanarico, Marco Gori, Simone Furini, Stefania Mantovani, Serena Ludovisi, Mario U. Mondelli, Francesco Castelli, Eugenia Quirós-Roldán, Melania Degli Antoni(University of California San Diego), Isabella Zanella, Massimo Vaghi, Stefano Rusconi, Matteo Siano(University of California San Diego), Francesca Montagnani, Arianna Emiliozzi, Massimiliano Fabbiani, Barbara Rossetti, Elena Bargagli, Laura Bergantini, Miriana d’Alessandro, Paolo Cameli, David Bennett, Federico Anedda, Simona Marcantonio, Sabino Scolletta, Federico Franchi, Maria Antonietta Mazzei, Susanna Guerrini, Edoardo Conticini, Luca Cantarini, Bruno Frediani, Danilo Tacconi, Chiara Spertilli, Marco Feri, Alice Donati, Raffaele Scala, Luca Guidelli, Genni Spargi, Marta Corridi, Cesira Nencioni, Leonardo Croci, Maria Bandini, Gian Piero Caldarelli, Paolo Piacentini, Elena Desanctis, Silvia Cappelli, Anna Canaccini, Agnese Verzuri, Valentina Anemoli, Agostino Ognibene, Alessandro Pancrazzi, Maria Lorubbio, Antonella d’Arminio Monforte, Federica Gaia Miraglia, Massimo Girardis, Sophie Venturelli, Andrea Cossarizza, Andrea Antinori, Alessandra Vergori, Arianna Gabrieli, Agostino Riva, Daniela Francisci, Elisabetta Schiaroli, Francesco Paciosi, Pier Giorgio Scotton, Francesca Andretta, Sandro Panese, Renzo Scaggiante, Francesca Gatti, Saverio Giuseppe Parisi, Stefano Baratti, Matteo Della Monica(University of California San Diego), Carmelo Piscopo, Mario Capasso, Roberta Russo, Immacolata Andolfo, Achille Iolascon, Giuseppe Fiorentino, Massimo Carella, Marco Castori, Giuseppe Merla, Gabriella Maria Squeo, Filippo Aucella, Pamela Raggi, Carmen Marciano, Rita Perna, Matteo Bassetti(University of California San Diego), Antonio Di Biagio(University of California San Diego), Maurizio Sanguinetti, Luca Masucci, Serafina Valente, Marco Mandalà, Alessia Giorli, Lorenzo Salerni, Patrizia Zucchi, Pierpaolo Parravicini, E. Menatti, Tullio Trotta, Ferdinando Giannattasio, Gabriella Coiro, Fabio Lena, Domenico Coviello, Cristina Mussini, Enrico Martinelli, Sandro Mancarella, Luisa Tavecchia, Lia Crotti, Chiara Gabbi, Marco Rizzi, F Maggiolo, Diego Ripamonti, Tiziana Bachetti, Maria Teresa La Rovere, Simona Sarzi Braga, Maurizio Bussotti, Stefano Ceri, Pietro Pinoli, Francesco Raimondi, Filippo Biscarini, Alessandra Stella, Kristina Zguro, Katia Capitani, Claudia Suardi, Mari E.K. Niemi, Mattia Cordioli, Sara Pigazzini, Simona Dei, Gianfranco Parati, Sabrina Ravaglia, Rosangela Artuso, Mattia Cordioli, Sara Pigazzini, Lindokuhle Nkambule, Giordano Bottà, Paolo Di Domenico, Ilaria Rancan, A. Bianchi, Davide Romani, Paola Bergomi, E Catena, Riccardo Colombo, Marco Tanfoni, Antonella Vincenti, Claudio Ferri, Davide Grassi, G Pessina, Mario Tumbarello, Massimo Di Pietro, Sabrina Ravaglia, Sauro Luchi, Chiara Barbieri, Donatella Acquilini, Elena Andreucci, Francesco Paciosi, Francesco Vladimiro Segala, Giusy Tiseo, Marco Falcone, Mirjam Lista, Monica Poscente, Oreste De Vivo, Paola Petrocelli, Alessandra Guarnaccia, Silvia Baroni, Albert V. Smith, Andrew P. Boughton, Kevin Li, Jonathon LeFaive, Aubrey Annis, Anne E. Justice, Tooraj Mirshahi, Geetha Chittoor, Navya Shilpa Josyula, Jack A. Kosmicki, Manuel A. R. Ferreira, Joseph B. Leader, Dave J. Carey, Matthew C. Gass, Julie Horowitz, Michael Cantor, Ashish Yadav, Aris Baras, Gonçalo R. Abecasis, David A. van Heel, Karen A. Hunt, Dan Mason(University of California San Diego), Qin Qin Huang, Sarah Finer, Bhavi Trivedi, Chris Griffiths, Hilary C. Martin, John Wright, Richard C. Trembath, Nicole Soranzo, Jing Hua Zhao, Adam S. Butterworth, John Danesh, Emanuele Di Angelantonio, Lude Franke Marike Boezen, Patrick Deelen, Annique Claringbould, Esteban Lopera, Robert Warmerdam, Judith M. Vonk, Irene V. van Blokland, Pauline Lanting, Anil P. S. Ori, Brooke Wolford Sebastian Zöllner, Jiongming Wang, Andrew F. Beck, Gina M. Peloso, Yuk‐Lam Ho, Yan V. Sun(Cancer Genetics (United States)), Jennifer E. Huffman, Christopher J. O’Donnell, Kelly Cho, Philip S. Tsao(University of California San Diego), J. Michael Gaziano, Michel G. Nivard, Eco J. C. de Geus, Meike Bartels, Jouke Jan Hottenga, Scott T. Weiss, Elizabeth W. Karlson, Jordan W. Smoller, Robert C. Green, Yen‐Chen Anne Feng, Josep M. Mercader, Shawn N. Murphy, James B. Meigs, Ann E. Woolley, Emma Perez, Daniel J. Rader, Anurag Verma, Marylyn D. Ritchie, Binglan Li, Shefali S. Verma, Anastasia Lucas, Yuki Bradford, Hugo Zeberg, Robert Frithiof, Michael Hultström, Mari E.K. Niemi, Mattia Cordioli, Sara Pigazzini, Miklós Lipcsey, Lindo Nkambul, Nicolas Tardif, Olav Rooyackers, Jonathan Grip, Tomislav Maričić, Tomoko Nakanishi, Guillaume Butler‐Laporte, Vincenzo Forgetta, J. Brent Richards, Konrad J. Karczewski, Elizabeth G. Atkinson, Masahiro Kanai, Kristin Tsuo, Nikolas Baya, Patrick Turley, Rahul Gupta, Shawneequa Callier, Raymond K. Walters, Duncan S. Palmer, Gopal Sarma, Matthew Solomonson, Nathan Cheng, Wenhan Lu, Sam Bryant, Claire Churchhouse, Caroline Cusick, Jacqueline I. Goldstein, Daniel L. King, Wei Zhou, Cotton Seed, Hilary K. Finucane, Alicia R. Martin, Sam Bryant, F. Kyle Satterstrom, Daniel J. Wilson, Jacob Armstrong, Justine Rudkin, Gavin Band, Sarah G. Earle, Shang‐Kuan Lin, Nicolas Arning, Derrick W. Crook, David Wyllie, Anne Marie O’Connell, Chris C.A. Spencer, Nils Koelling, Mark J. Caulfield, Richard H. Scott, Tom Fowler, Loukas Moutsianas, Athanasios Kousathanas, Dorota Pasko, Susan Walker, Augusto Rendon, Alexander Stuckey, Christopher A. Odhams, Daniel R. Rhodes, G. C. Chan, Prabhu Arumugam, Catherine A. Ball, Eurie L. Hong, Kristin A. Rand, Ahna R. Girshick, Harendra Guturu, Asher Haug Baltzell, Genevieve Roberts, Danny Park, Marie V. Coignet, Shannon McCurdy, Spencer C. Knight, Raghavendran Partha, Brooke Rhead, Miao Zhang, Nathan Berkowitz, Michael Gaddis, Keith Noto, Luong Ruiz, Miloš Pavlović, Laura Sloofman, Shea J. Andrews, Alexander W. Charney, Noam D. Beckmann, Eric E. Schadt, Daniel M. Jordan, Ryan C. Thompson, Kyle Gettler, Noura S. Abul‐Husn, Steven Ascolillo, Joseph D. Buxbaum, Kumardeep Chaudhary, Judy H. Cho, Yuval Itan, Eimear E. Kenny, Gillian M. Belbin, Stuart C. Sealfon, Robert Sebra, Irene Salib, Brett Collins, Tess Levy, Bari Britvan, Katherine Keller, Lara Tang, Michael Peruggia, Liam L. Hiester, Kristi Niblo, Alexandra Aksentijevich, Alexander Labkowsky, Avromie Karp, Menachem Zlatopolsky, Michael Preuß, Ruth J. F. Loos, Girish N. Nadkarni, Ron Do, Clive Hoggart(University of California San Diego), Sam Choi, Slayton J. Underwood, Paul F. O’Reilly, Laura M. Huckins, Marissa Zyndorf
Cited by 47Open Access
Abstract
Variability in SARS-CoV-2 susceptibility and COVID-19 disease severity between individuals is partly due to genetic factors. Here, we identify 4 genomic loci with suggestive associations for SARS-CoV-2 susceptibility and 19 for COVID-19 disease severity. Four of these 23 loci likely have an ethnicity-specific component. Genome-wide association study (GWAS) signals in 11 loci colocalize with expression quantitative trait loci (eQTLs) associated with the expression of 20 genes in 62 tissues/cell types (range: 1:43 tissues/gene), including lung, brain, heart, muscle, and skin as well as the digestive system and immune system. We perform genetic fine mapping to compute 99% credible SNP sets, which identify 10 GWAS loci that have eight or fewer SNPs in the credible set, including three loci with one single likely causal SNP. Our study suggests that the diverse symptoms and disease severity of COVID-19 observed between individuals is associated with variants across the genome, affecting gene expression levels in a wide variety of tissue types.
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