SARS-CoV-2 susceptibility and COVID-19 disease severity are associated with genetic variants affecting gene expression in a variety of tissues.

D'Antonio, Matteo; Nguyen, Jennifer P; Arthur, Timothy D; Matsui, Hiroko; COVID-19 Host Genetics Initiative; D'Antonio-Chronowska, Agnieszka; Frazer, Kelly A

doi:10.1016/j.celrep.2021.110020

Article (Scientific journals)

SARS-CoV-2 susceptibility and COVID-19 disease severity are associated with genetic variants affecting gene expression in a variety of tissues.

D'Antonio, Matteo; Nguyen, Jennifer P; Arthur, Timothy D et al.

2021 • In Cell Reports, 37 (7), p. 110020

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/308412

DOI
10.1016/j.celrep.2021.110020

PubMed
34762851

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Keywords :

COVID-19; GWAS; SARS-CoV-2; colocalization; eQTL; COVID-19/genetics; Chromosome Mapping/methods; Computational Biology/methods; Databases, Genetic; Ethnicity/genetics; Gene Expression/genetics; Gene Expression Profiling/methods; Genetic Predisposition to Disease/genetics; Genetic Variation/genetics; Genome-Wide Association Study/methods; Humans; Organ Specificity/genetics; Polymorphism, Single Nucleotide/genetics; Quantitative Trait Loci/genetics; SARS-CoV-2/genetics; SARS-CoV-2/pathogenicity; Severity of Illness Index; Transcriptome/genetics; Chromosome Mapping; Computational Biology; Ethnic Groups; Gene Expression; Gene Expression Profiling; Genetic Predisposition to Disease; Genetic Variation; Genome-Wide Association Study; Organ Specificity; Polymorphism, Single Nucleotide; Quantitative Trait Loci; Transcriptome; Biochemistry, Genetics and Molecular Biology (all); General Biochemistry, Genetics and Molecular Biology

Abstract :

[en] 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.

Disciplines :

Immunology & infectious disease

Author, co-author :

D'Antonio, Matteo; Department of Pediatrics, University of California, San Diego, La Jolla, CA 92093, USA. Electronic address: madantonio@health.ucsd.edu

Nguyen, Jennifer P; Department of Biomedical Informatics, University of California, San Diego, La Jolla, CA 92093, USA, Bioinformatics and Systems Biology Graduate Program, University of California, San Diego, La Jolla, CA 92093, USA

Arthur, Timothy D; Department of Biomedical Informatics, University of California, San Diego, La Jolla, CA 92093, USA, Biomedical Sciences Graduate Program, University of California, San Diego, La Jolla, CA 92093, USA

Matsui, Hiroko; Institute of Genomic Medicine, University of California San Diego, 9500 Gilman Dr, La Jolla, CA 92093, USA

COVID-19 Host Genetics Initiative

D'Antonio-Chronowska, Agnieszka; Department of Pediatrics, University of California, San Diego, La Jolla, CA 92093, USA

Frazer, Kelly A; Department of Pediatrics, University of California, San Diego, La Jolla, CA 92093, USA, Institute of Genomic Medicine, University of California San Diego, 9500 Gilman Dr, La Jolla, CA 92093, USA. Electronic address: kafrazer@health.ucsd.edu

Other collaborator :

Moutschen, Michel ; Centre Hospitalier Universitaire de Liège - CHU > > Service des maladies infectieuses - médecine interne

Language :

English

Title :

SARS-CoV-2 susceptibility and COVID-19 disease severity are associated with genetic variants affecting gene expression in a variety of tissues.

Publication date :

2021

Journal title :

Cell Reports

eISSN :

2211-1247

Publisher :

Elsevier B.V., United States

Volume :

Issue :

Pages :

110020

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S2211124721015023?httpAccept=text/xml

Funders :

NIH - National Institutes of Health [US-MD]
NHGRI - National Human Genome Research Institute [US-MD]
UCSD - University of California, San Diego [US-CA]

Funding text :

This work was supported by Emergency COVID-19 Seed Award from the Tobacco-Related Disease Research Program of the University of California , grant R00RG2716 , and by the NHGRI CEGS grant RM1HG011558 . J.P.N. and T.D.A. were supported by an NIH training grant ( T15LM011271 ).

Commentary :

A complete list of the members of the COVID-19 Host Genetics Initiative and their affiliations is provided at https://docs.google.com/spreadsheets/d/1cp9pFeFUxXz5WMjRFv4X-AM1Hlc0iXYJa1rorSSj2Dc.

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Bibliography

Ahn, D., Prince, A., Participation of the IL-10RB Related Cytokines, IL-22 and IFN-λ in Defense of the Airway Mucosal Barrier. Front. Cell. Infect. Microbiol., 10, 2020, 300.
Alasoo, K., Rodrigues, J., Mukhopadhyay, S., Knights, A.J., Mann, A.L., Kundu, K., Hale, C., Dougan, G., Gaffney, D.J., Gaffney, D.J., HIPSCI Consortium. Shared genetic effects on chromatin and gene expression indicate a role for enhancer priming in immune response. Nat. Genet. 50 (2018), 424–431.
Aragam, K.G., Chaffin, M., Levinson, R.T., McDermott, G., Choi, S.H., Shoemaker, M.B., Haas, M.E., Weng, L.C., Lindsay, M.E., Smith, J.G., et al., GRADE Investigators. Phenotypic Refinement of Heart Failure in a National Biobank Facilitates Genetic Discovery. Circulation, 2018, 10.1161/CIRCULATIONAHA.118.035774 Published online November 11, 2018.
Astle, W.J., Elding, H., Jiang, T., Allen, D., Ruklisa, D., Mann, A.L., Mead, D., Bouman, H., Riveros-Mckay, F., Kostadima, M.A., et al. The Allelic Landscape of Human Blood Cell Trait Variation and Links to Common Complex Disease. Cell 167 (2016), 1415–1429.e19.
Atkins, J.L., Masoli, J.A.H., Delgado, J., Pilling, L.C., Kuo, C.L., Kuchel, G.A., Melzer, D., Preexisting Comorbidities Predicting COVID-19 and Mortality in the UK Biobank Community Cohort. J. Gerontol. A Biol. Sci. Med. Sci. 75 (2020), 2224–2230.
Baker, M., Litvan, I., Houlden, H., Adamson, J., Dickson, D., Perez-Tur, J., Hardy, J., Lynch, T., Bigio, E., Hutton, M., Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Hum. Mol. Genet. 8 (1999), 711–715.
Banerjee, S., Gusho, E., Gaughan, C., Dong, B., Gu, X., Holvey-Bates, E., Talukdar, M., Li, Y., Weiss, S.R., Sicheri, F., et al. OAS-RNase L innate immune pathway mediates the cytotoxicity of a DNA-demethylating drug. Proc. Natl. Acad. Sci. USA 116 (2019), 5071–5076.
Barnkob, M.B., Pottegård, A., Støvring, H., Haunstrup, T.M., Homburg, K., Larsen, R., Hansen, M.B., Titlestad, K., Aagaard, B., Møller, B.K., Barington, T., Reduced prevalence of SARS-CoV-2 infection in ABO blood group O. Blood Adv. 4 (2020), 4990–4993.
Bentham, J., Morris, D.L., Graham, D.S.C., Pinder, C.L., Tombleson, P., Behrens, T.W., Martín, J., Fairfax, B.P., Knight, J.C., Chen, L., et al. Genetic association analyses implicate aberrant regulation of innate and adaptive immunity genes in the pathogenesis of systemic lupus erythematosus. Nat. Genet. 47 (2015), 1457–1464.
Birdwell, L.D., Zalinger, Z.B., Li, Y., Wright, P.W., Elliott, R., Rose, K.M., Silverman, R.H., Weiss, S.R., Activation of RNase L by Murine Coronavirus in Myeloid Cells Is Dependent on Basal Oas Gene Expression and Independent of Virus-Induced Interferon. J. Virol. 90 (2016), 3160–3172.
Bonder, M.J., Smail, C., Gloudemans, M.J., Frésard, L., Jakubosky, D., D'Antonio, M., Li, X., Ferraro, N.M., Carcamo-Orive, I., Mirauta, B., et al. HipSci Consortium iPSCORE consortium Undiagnosed Diseases Network, PhLiPS consortium. Identification of rare and common regulatory variants in pluripotent cells using population-scale transcriptomics. Nat. Genet. 53 (2021), 313–321.
Buil, A., Brown, A.A., Lappalainen, T., Viñuela, A., Davies, M.N., Zheng, H.F., Richards, J.B., Glass, D., Small, K.S., Durbin, R., et al. Gene-gene and gene-environment interactions detected by transcriptome sequence analysis in twins. Nat. Genet. 47 (2015), 88–91.
Chen, L., Ge, B., Casale, F.P., Vasquez, L., Kwan, T., Garrido-Martín, D., Watt, S., Yan, Y., Kundu, K., Ecker, S., et al. Genetic Drivers of Epigenetic and Transcriptional Variation in Human Immune Cells. Cell 167 (2016), 1398–1414.e24.
Chu, X., Pan, C.M., Zhao, S.X., Liang, J., Gao, G.Q., Zhang, X.M., Yuan, G.Y., Li, C.G., Xue, L.Q., Shen, M., et al., China Consortium for Genetics of Autoimmune Thyroid Disease. A genome-wide association study identifies two new risk loci for Graves’ disease. Nat. Genet. 43 (2011), 897–901.
COVID-19 Host Genetics Initiative. The COVID-19 Host Genetics Initiative, a global initiative to elucidate the role of host genetic factors in susceptibility and severity of the SARS-CoV-2 virus pandemic. Eur. J. Hum. Genet. 28 (2020), 715–718.
COVID-19 Host Genetics Initiative. Mapping the human genetic architecture of COVID-19. Nature, 2021, 10.1038/s41586-021-03767-x Published online July 8, 2021.
Cummings, M.J., Baldwin, M.R., Abrams, D., Jacobson, S.D., Meyer, B.J., Balough, E.M., Aaron, J.G., Claassen, J., Rabbani, L.E., Hastie, J., et al. Epidemiology, clinical course, and outcomes of critically ill adults with COVID-19 in New York City: a prospective cohort study. Lancet 395 (2020), 1763–1770.
DeBoever, C., Li, H., Jakubosky, D., Benaglio, P., Reyna, J., Olson, K.M., Huang, H., Biggs, W., Sandoval, E., D'Antonio, M., et al. Large-Scale Profiling Reveals the Influence of Genetic Variation on Gene Expression in Human Induced Pluripotent Stem Cells. Cell Stem Cell 20 (2017), 533–546.e7.
Duncan, C.J., Mohamad, S.M., Young, D.F., Skelton, A.J., Leahy, T.R., Munday, D.C., Butler, K.M., Morfopoulou, S., Brown, J.R., Hubank, M., et al. Human IFNAR2 deficiency: Lessons for antiviral immunity. Sci. Transl. Med., 7, 2015, 307ra154.
Ellinghaus, D., Degenhardt, F., Bujanda, L., Buti, M., Albillos, A., Invernizzi, P., Fernández, J., Prati, D., Baselli, G., Asselta, R., et al., Severe Covid-19 GWAS Group. Genomewide Association Study of Severe Covid-19 with Respiratory Failure. N. Engl. J. Med. 383 (2020), 1522–1534.
Fan, J., Wang, H., Ye, G., Cao, X., Xu, X., Tan, W., Zhang, Y., Letter to the Editor: Low-density lipoprotein is a potential predictor of poor prognosis in patients with coronavirus disease 2019. Metabolism, 107, 2020, 154243.
Ghoreschi, K., Augustin, M., Baraliakos, X., Krönke, G., Schneider, M., Schreiber, S., Schulze-Koops, H., Zeißig, S., Thaçi, D., TYK2 inhibition and its potential in the treatment of chronic inflammatory immune diseases. J. Dtsch. Dermatol. Ges. 19 (2021), 1409–1420.
Giambartolomei, C., Vukcevic, D., Schadt, E.E., Franke, L., Hingorani, A.D., Wallace, C., Plagnol, V., Bayesian test for colocalisation between pairs of genetic association studies using summary statistics. PLoS Genet., 10, 2014, e1004383.
Gilly, A., Suveges, D., Kuchenbaecker, K., Pollard, M., Southam, L., Hatzikotoulas, K., Farmaki, A.E., Bjornland, T., Waples, R., Appel, E.V.R., et al. Cohort-wide deep whole genome sequencing and the allelic architecture of complex traits. Nat. Commun., 9, 2018, 4674.
GTEx Consortium. The GTEx Consortium atlas of genetic regulatory effects across human tissues. Science 369 (2020), 1318–1330.
Guan, W.J., Ni, Z.Y., Hu, Y., Liang, W.H., Ou, C.Q., He, J.X., Liu, L., Shan, H., Lei, C.L., Hui, D.S.C., et al., China Medical Treatment Expert Group for Covid-19. Clinical Characteristics of Coronavirus Disease 2019 in China. N. Engl. J. Med. 382 (2020), 1708–1720.
Gutierrez-Arcelus, M., Lappalainen, T., Montgomery, S.B., Buil, A., Ongen, H., Yurovsky, A., Bryois, J., Giger, T., Romano, L., Planchon, A., et al. Passive and active DNA methylation and the interplay with genetic variation in gene regulation. eLife, 2, 2013, e00523.
Horowitz, J.E., Kosmicki, J.A., Damask, A., Sharma, D., Roberts, G.H.L., Justice, A.E., Banerjee, N., Coignet, M.V., Yadav, A., Leader, J.B., et al. Common genetic variants identify targets for COVID-19 and individuals at high risk of severe disease. medRxiv, 2021.
Hu, X., Chen, D., Wu, L., He, G., Ye, W., Declined serum high density lipoprotein cholesterol is associated with the severity of COVID-19 infection. Clin. Chim. Acta 510 (2020), 105–110.
Huang, C., Wang, Y., Li, X., Ren, L., Zhao, J., Hu, Y., Zhang, L., Fan, G., Xu, J., Gu, X., et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395 (2020), 497–506.
Jones, E.Y., Fugger, L., Strominger, J.L., Siebold, C., MHC class II proteins and disease: a structural perspective. Nat. Rev. Immunol. 6 (2006), 271–282.
Karczewski, K.J., Francioli, L.C., Tiao, G., Cummings, B.B., Alföldi, J., Wang, Q., Collins, R.L., Laricchia, K.M., Ganna, A., Birnbaum, D.P., et al., Genome Aggregation Database Consortium. The mutational constraint spectrum quantified from variation in 141,456 humans. Nature 581 (2020), 434–443.
Kerimov, N., Hayhurst, J.D., Peikova, K., Manning, J.R., Walter, P., Kolberg, L., Samoviča, M., Sakthivel, M.P., Kuzmin, I., Trevanion, S.J., et al. eQTL Catalogue: a compendium of uniformly processed human gene expression and splicing QTLs. Nat. Genet. 53 (2021), 1290–1299.
Koolen, D.A., Vissers, L.E., Pfundt, R., de Leeuw, N., Knight, S.J., Regan, R., Kooy, R.F., Reyniers, E., Romano, C., Fichera, M., et al. A new chromosome 17q21.31 microdeletion syndrome associated with a common inversion polymorphism. Nat. Genet. 38 (2006), 999–1001.
Kulminski, A.M., Huang, J., Loika, Y., Arbeev, K.G., Bagley, O., Yashkin, A., Duan, M., Culminskaya, I., Strong impact of natural-selection-free heterogeneity in genetics of age-related phenotypes. Aging (Albany NY) 10 (2018), 492–514.
Lappalainen, T., Sammeth, M., Friedländer, M.R., ’t Hoen, P.A., Monlong, J., Rivas, M.A., Gonzàlez-Porta, M., Kurbatova, N., Griebel, T., Ferreira, P.G., et al., Geuvadis Consortium. Transcriptome and genome sequencing uncovers functional variation in humans. Nature 501 (2013), 506–511.
Larson, N.B., Bell, E.J., Decker, P.A., Pike, M., Wassel, C.L., Tsai, M.Y., Pankow, J.S., Tang, W., Hanson, N.Q., Alexander, K., et al. ABO blood group associations with markers of endothelial dysfunction in the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis 251 (2016), 422–429.
Laurent, E.M.N., Sofianatos, Y., Komarova, A., Gimeno, J.-P., Samavarchi Tehrani, P., Kim, D.-K., Abdouni, H., Duhamel, M., Cassonnet, P., Knapp, J.J., et al. Global BioID-based SARS-CoV-2 proteins proximal interactome unveils novel ties between viral polypeptides and host factors involved in multiple COVID19-associated mechanisms. bioRxiv, 2020, 10.1101/2020.08.28.272955.
Li, M., Wang, L., Shi, D.C., Foo, J.N., Zhong, Z., Khor, C.C., Lanzani, C., Citterio, L., Salvi, E., Yin, P.R., et al. Genome-Wide Meta-Analysis Identifies Three Novel Susceptibility Loci and Reveals Ethnic Heterogeneity of Genetic Susceptibility for IgA Nephropathy. J. Am. Soc. Nephrol. 31 (2020), 2949–2963.
Mackey, K., Ayers, C.K., Kondo, K.K., Saha, S., Advani, S.M., Young, S., Spencer, H., Rusek, M., Anderson, J., Veazie, S., et al. Racial and Ethnic Disparities in COVID-19-Related Infections, Hospitalizations, and Deaths : A Systematic Review. Ann. Intern. Med. 174 (2021), 362–373.
Mahajan, A., Taliun, D., Thurner, M., Robertson, N.R., Torres, J.M., Rayner, N.W., Payne, A.J., Steinthorsdottir, V., Scott, R.A., Grarup, N., et al. Fine-mapping type 2 diabetes loci to single-variant resolution using high-density imputation and islet-specific epigenome maps. Nat. Genet. 50 (2018), 1505–1513.
Mandala, V.S., McKay, M.J., Shcherbakov, A.A., Dregni, A.J., Kolocouris, A., Hong, M., Structure and drug binding of the SARS-CoV-2 envelope protein transmembrane domain in lipid bilayers. Nat. Struct. Mol. Biol. 27 (2020), 1202–1208.
Manichaikul, A., Wang, X.Q., Sun, L., Dupuis, J., Borczuk, A.C., Nguyen, J.N., Raghu, G., Hoffman, E.A., Onengut-Gumuscu, S., Farber, E.A., et al. Genome-wide association study of subclinical interstitial lung disease in MESA. Respir. Res., 18, 2017, 97.
Melzer, D., Perry, J.R., Hernandez, D., Corsi, A.M., Stevens, K., Rafferty, I., Lauretani, F., Murray, A., Gibbs, J.R., Paolisso, G., et al. A genome-wide association study identifies protein quantitative trait loci (pQTLs). PLoS Genet., 4, 2008, e1000072.
Meyts, I., Casanova, J.L., Viral infections in humans and mice with genetic deficiencies of the type I IFN response pathway. Eur. J. Immunol. 51 (2021), 1039–1061.
Muise, A.M., Walters, T., Wine, E., Griffiths, A.M., Turner, D., Duerr, R.H., Regueiro, M.D., Ngan, B.Y., Xu, W., Sherman, P.M., et al. Protein-tyrosine phosphatase sigma is associated with ulcerative colitis. Curr. Biol. 17 (2007), 1212–1218.
Myers, A.J., Kaleem, M., Marlowe, L., Pittman, A.M., Lees, A.J., Fung, H.C., Duckworth, J., Leung, D., Gibson, A., Morris, C.M., et al. The H1c haplotype at the MAPT locus is associated with Alzheimer's disease. Hum. Mol. Genet. 14 (2005), 2399–2404.
Myers, T.A., Chanock, S.J., Machiela, M.J., LDlinkR: An R Package for Rapidly Calculating Linkage Disequilibrium Statistics in Diverse Populations. Front. Genet., 11, 2020, 157.
Nédélec, Y., Sanz, J., Baharian, G., Szpiech, Z.A., Pacis, A., Dumaine, A., Grenier, J.C., Freiman, A., Sams, A.J., Hebert, S., et al. Genetic Ancestry and Natural Selection Drive Population Differences in Immune Responses to Pathogens. Cell 167 (2016), 657–669.e21.
Oriol, R., Mollicone, R., Coullin, P., Dalix, A.M., Candelier, J.J., Genetic regulation of the expression of ABH and Lewis antigens in tissues. APMIS Suppl 27 (1992), 28–38.
Pairo-Castineira, E., Clohisey, S., Klaric, L., Bretherick, A.D., Rawlik, K., Pasko, D., Walker, S., Parkinson, N., Fourman, M.H., Russell, C.D., et al. GenOMICC Investigators ISARIC4C Investigators COVID-19 Human Genetics Initiative 23andMe Investigators BRACOVID Investigators, Gen-COVID Investigators. Genetic mechanisms of critical illness in COVID-19. Nature 591 (2021), 92–98.
Pedersen, S.F., Ho, Y.C., SARS-CoV-2: a storm is raging. J. Clin. Invest. 130 (2020), 2202–2205.
Quach, H., Rotival, M., Pothlichet, J., Loh, Y.E., Dannemann, M., Zidane, N., Laval, G., Patin, E., Harmant, C., Lopez, M., et al. Genetic Adaptation and Neandertal Admixture Shaped the Immune System of Human Populations. Cell 167 (2016), 643–656.e17.
Quinlan, A.R., BEDTools: The Swiss-Army Tool for Genome Feature Analysis. Curr. Protoc. Bioinformatics 47 (2014), 11.12–11.34.
Richardson, S., Hirsch, J.S., Narasimhan, M., Crawford, J.M., McGinn, T., Davidson, K.W., Barnaby, D.P., Becker, L.B., Chelico, J.D., Cohen, S.L., et al., the Northwell COVID-19 Research Consortium. Presenting Characteristics, Comorbidities, and Outcomes Among 5700 Patients Hospitalized With COVID-19 in the New York City Area. JAMA 323 (2020), 2052–2059.
Roche, P.A., Furuta, K., The ins and outs of MHC class II-mediated antigen processing and presentation. Nat. Rev. Immunol. 15 (2015), 203–216.
Sakornsakolpat, P., Prokopenko, D., Lamontagne, M., Reeve, N.F., Guyatt, A.L., Jackson, V.E., Shrine, N., Qiao, D., Bartz, T.M., Kim, D.K., et al. SpiroMeta Consortium, International COPD Genetics Consortium. Genetic landscape of chronic obstructive pulmonary disease identifies heterogeneous cell-type and phenotype associations. Nat. Genet. 51 (2019), 494–505.
Samavarchi-Tehrani, P., Abdouni, H., Knight, J.D.R., Astori, A., Samson, R., Lin, Z.-Y., Kim, D.-K., Knapp, J.J., St-Germain, J., Go, C.D., et al. A SARS-CoV-2 – host proximity interactome. bioRxiv, 2020, 10.1101/2020.09.03.282103.
Sawai, H., Nishida, N., Khor, S.S., Honda, M., Sugiyama, M., Baba, N., Yamada, K., Sawada, N., Tsugane, S., Koike, K., et al. Genome-wide association study identified new susceptible genetic variants in HLA class I region for hepatitis B virus-related hepatocellular carcinoma. Sci. Rep., 8, 2018, 7958.
Schmiedel, B.J., Singh, D., Madrigal, A., Valdovino-Gonzalez, A.G., White, B.M., Zapardiel-Gonzalo, J., Ha, B., Altay, G., Greenbaum, J.A., McVicker, G., et al. Impact of Genetic Polymorphisms on Human Immune Cell Gene Expression. Cell 175 (2018), 1701–1715.e1716.
Schmiedel, B.J., Chandra, V., Rocha, J., Gonzalez-Colin, C., Bhattacharyya, S., Madrigal, A., Ottensmeier, C.H., Ay, F., Vijayanand, P., COVID-19 genetic risk variants are associated with expression of multiple genes in diverse immune cell types. bioRxiv, 2020, 10.1101/2020.12.01.407429.
Shouval, D.S., Biswas, A., Goettel, J.A., McCann, K., Conaway, E., Redhu, N.S., Mascanfroni, I.D., Al Adham, Z., Lavoie, S., Ibourk, M., et al. Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity 40 (2014), 706–719.
Skipper, L., Wilkes, K., Toft, M., Baker, M., Lincoln, S., Hulihan, M., Ross, O.A., Hutton, M., Aasly, J., Farrer, M., Linkage disequilibrium and association of MAPT H1 in Parkinson disease. Am. J. Hum. Genet. 75 (2004), 669–677.
Snijders Blok, L., Vino, A., den Hoed, J., Underhill, H.R., Monteil, D., Li, H., Reynoso Santos, F.J., Chung, W.K., Amaral, M.D., Schnur, R.E., et al. Heterozygous variants that disturb the transcriptional repressor activity of FOXP4 cause a developmental disorder with speech/language delays and multiple congenital abnormalities. Genet. Med. 23 (2021), 534–542.
Theusch, E., Chen, Y.I., Rotter, J.I., Krauss, R.M., Medina, M.W., Genetic variants modulate gene expression statin response in human lymphoblastoid cell lines. BMC Genomics, 21, 2020, 555.
Thomas, S., The Structure of the Membrane Protein of SARS-CoV-2 Resembles the Sugar Transporter SemiSWEET. Pathog. Immun. 5 (2020), 342–363.
Wallace, C., Eliciting priors and relaxing the single causal variant assumption in colocalisation analyses. PLoS Genet., 16, 2020, e1008720.
Wang, G., Zhang, Q., Zhao, X., Dong, H., Wu, C., Wu, F., Yu, B., Lv, J., Zhang, S., Wu, G., et al. Low high-density lipoprotein level is correlated with the severity of COVID-19 patients: an observational study. Lipids Health Dis., 19, 2020, 204.
Webb, A., Miller, B., Bonasera, S., Boxer, A., Karydas, A., Wilhelmsen, K.C., Role of the tau gene region chromosome inversion in progressive supranuclear palsy, corticobasal degeneration, and related disorders. Arch. Neurol. 65 (2008), 1473–1478.
Wei, X., Zeng, W., Su, J., Wan, H., Yu, X., Cao, X., Tan, W., Wang, H., Hypolipidemia is associated with the severity of COVID-19. J. Clin. Lipidol. 14 (2020), 297–304.
Worldometer. COVID-19 CORONAVIRUS PANDEMIC. 2021 https://www.worldometers.info/coronavirus/.
Wu, Y., Byrne, E.M., Zheng, Z., Kemper, K.E., Yengo, L., Mallett, A.J., Yang, J., Visscher, P.M., Wray, N.R., Genome-wide association study of medication-use and associated disease in the UK Biobank. Nat. Commun., 10, 2019, 1891.
Yang, T., Li, H., Thakur, A., Chen, T., Xue, J., Li, D., Chen, M., FOXP4 modulates tumor growth and independently associates with miR-138 in non-small cell lung cancer cells. Tumour Biol. 36 (2015), 8185–8191.
Yang, G.H., Fontaine, D.A., Lodh, S., Blumer, J.T., Roopra, A., Davis, D.B., TCF19 Impacts a Network of Inflammatory and DNA Damage Response Genes in the Pancreatic β-Cell. Metabolites, 11, 2021, 513.
Young, A.M.H., Kumasaka, N., Calvert, F., Hammond, T.R., Knights, A., Panousis, N., Park, J.S., Schwartzentruber, J., Liu, J., Kundu, K., et al. A map of transcriptional heterogeneity and regulatory variation in human microglia. Nat. Genet. 53 (2021), 861–868.
Zeberg, H., Pääbo, S., A genomic region associated with protection against severe COVID-19 is inherited from Neandertals. Proc. Natl. Acad. Sci. USA, 118, 2021 e2026309118.
Zeng, Z., Liu, H., Xu, H., Lu, H., Yu, Y., Xu, X., Yu, M., Zhang, T., Tian, X., Xi, H., et al., HBVstudy consortium. Genome-wide association study identifies new loci associated with risk of HBV infection and disease progression. BMC Med. Genomics, 14, 2021, 84.
Zhao, S.X., Liu, W., Liang, J., Gao, G.Q., Zhang, X.M., Yao, Y., Wang, H.N., Yuan, F.F., Xue, L.Q., Ma, Y.R., et al., China Consortium for the Genetics of Autoimmune Thyroid Disease. Assessment of Molecular Subtypes in Thyrotoxic Periodic Paralysis and Graves Disease Among Chinese Han Adults: A Population-Based Genome-Wide Association Study. JAMA Netw. Open, 2, 2019, e193348.
Zhou, Z.H., Chen, G., Deng, C., Tang, J.M., Xie, L., Zhou, H.Y., Ye, X., Zhang, D.K., Shi, R.Q., Tian, D., et al. TCF19 contributes to cell proliferation of non-small cell lung cancer by inhibiting FOXO1. Cell Biol. Int, 2019, 10.1002/cbin.11189 Published online May 29, 2019.
Zhou, F., Yu, T., Du, R., Fan, G., Liu, Y., Liu, Z., Xiang, J., Wang, Y., Song, B., Gu, X., et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet 395 (2020), 1054–1062.
Zhou, S., Butler-Laporte, G., Nakanishi, T., Morrison, D.R., Afilalo, J., Afilalo, M., Laurent, L., Pietzner, M., Kerrison, N., Zhao, K., et al. A Neanderthal OAS1 isoform protects individuals of European ancestry against COVID-19 susceptibility and severity. Nat. Med. 27 (2021), 659–667.