1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biomedical Data Science
  4. Volume 6, 2023
  5. Article

Annual Review of Biomedical Data Science

Volume 6, 2023

Human Genomics of COVID-19 Pneumonia: Contributions of Rare and Common Variants

Abstract

SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2) infection is silent or benign in most infected individuals, but causes hypoxemic COVID-19 pneumonia in about 10% of cases. We review studies of the human genetics of life-threatening COVID-19 pneumonia, focusing on both rare and common variants. Large-scale genome-wide association studies have identified more than 20 common loci robustly associated with COVID-19 pneumonia with modest effect sizes, some implicating genes expressed in the lungs or leukocytes. The most robust association, on chromosome 3, concerns a haplotype inherited from Neanderthals. Sequencing studies focusing on rare variants with a strong effect have been particularly successful, identifying inborn errors of type I interferon (IFN) immunity in 1–5% of unvaccinated patients with critical pneumonia, and their autoimmune phenocopy, autoantibodies against type I IFN, in another 15–20% of cases. Our growing understanding of the impact of human genetic variation on immunity to SARS-CoV-2 is enabling health systems to improve protection for individuals and populations.

Keyword(s): COVID-19 pneumonia, GWAS, inborn errors of immunity, SARS-CoV-2, type I interferons
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biodatasci-020222-021705
2023-08-10
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/biodatasci/6/1/annurev-biodatasci-020222-021705.html?itemId=/content/journals/10.1146/annurev-biodatasci-020222-021705&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Dong E, Du H, Gardner L. 2020. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect. Dis. 20:533–34
     [Google Scholar]
  2. 2.
    Zhang Q, Bastard P, COVID Hum. Genet. Effort, Cobat A, Casanova JL 2022. Human genetic and immunological determinants of critical COVID-19 pneumonia. Nature 603:587–98
     [Google Scholar]
  3. 3.
    O'Driscoll M, Ribeiro Dos Santos G, Wang L, Cummings DAT, Azman AS et al. 2021. Age-specific mortality and immunity patterns of SARS-CoV-2. Nature 590:140–45
     [Google Scholar]
  4. 4.
    COVID-19 Forecast. Team 2022. Variation in the COVID-19 infection-fatality ratio by age, time, and geography during the pre-vaccine era: a systematic analysis. Lancet 399:1469–88
     [Google Scholar]
  5. 5.
    Bennett TD, Moffitt RA, Hajagos JG, Amor B, Anand A et al. 2021. Clinical characterization and prediction of clinical severity of SARS-CoV-2 infection among US adults using data from the US National COVID Cohort Collaborative. JAMA Netw. Open 4:e2116901
     [Google Scholar]
  6. 6.
    Takahashi T, Ellingson MK, Wong P, Israelow B, Lucas C et al. 2020. Sex differences in immune responses that underlie COVID-19 disease outcomes. Nature 588:315–20
     [Google Scholar]
  7. 7.
    Navaratnam AV, Gray WK, Day J, Wendon J, Briggs TWR. 2021. Patient factors and temporal trends associated with COVID-19 in-hospital mortality in England: an observational study using administrative data. Lancet Respir. Med. 9:397–406
     [Google Scholar]
  8. 8.
    Ricoca Peixoto V, Vieira A, Aguiar P, Sousa P, Carvalho C et al. 2021. Determinants for hospitalisations, intensive care unit admission and death among 20,293 reported COVID-19 cases in Portugal, March to April 2020. Eur. Surveill. 26:332001059
     [Google Scholar]
  9. 9.
    Williamson EJ, Walker AJ, Bhaskaran K, Bacon S, Bates C et al. 2020. Factors associated with COVID-19-related death using OpenSAFELY. Nature 584:430–36
     [Google Scholar]
  10. 10.
    Sancho-Shimizu V, Brodin P, Cobat A, Biggs CM, Toubiana J et al. 2021. SARS-CoV-2-related MIS-C: a key to the viral and genetic causes of Kawasaki disease?. J. Exp. Med. 218:6e20210446
     [Google Scholar]
  11. 11.
    Ahmad F, Ahmed A, Rajendraprasad SS, Loranger A, Gupta S et al. 2021. Multisystem inflammatory syndrome in adults: a rare sequela of SARS-CoV-2 infection. Int. J. Infect. Dis. 108:209–11
     [Google Scholar]
  12. 12.
    Arkin LM, Moon JJ, Tran JM, Asgari S, O'Farrelly C et al. 2021. From your nose to your toes: a review of severe acute respiratory syndrome coronavirus 2 pandemic–associated pernio. J. Investig. Dermatol. 141:2791–96
     [Google Scholar]
  13. 13.
    Brodin P, Casari G, Townsend L, O'Farrelly C, Tancevski I et al. 2022. Studying severe long COVID to understand post-infectious disorders beyond COVID-19. Nat. Med. 28:879–82
     [Google Scholar]
  14. 14.
    Moghadas SM, Vilches TN, Zhang K, Wells CR, Shoukat A et al. 2021. The impact of vaccination on coronavirus disease 2019 (COVID-19) outbreaks in the United States. Clin. Infect. Dis. 73:2257–64
     [Google Scholar]
  15. 15.
    Davies NG, Jarvis CI, Group CC-W, Edmunds WJ, Jewell NP et al. 2021. Increased mortality in community-tested cases of SARS-CoV-2 lineage B.1.1.7. Nature 593:270–74
     [Google Scholar]
  16. 16.
    Nyberg T, Twohig KA, Harris RJ, Seaman SR, Flannagan J et al. 2021. Risk of hospital admission for patients with SARS-CoV-2 variant B.1.1.7: cohort analysis. BMJ 373:n1412
     [Google Scholar]
  17. 17.
    Patone M, Thomas K, Hatch R, Tan PS, Coupland C et al. 2021. Mortality and critical care unit admission associated with the SARS-CoV-2 lineage B.1.1.7 in England: an observational cohort study. Lancet Infect. Dis. 21:1518–28
     [Google Scholar]
  18. 18.
    Twohig KA, Nyberg T, Zaidi A, Thelwall S, Sinnathamby MA et al. 2022. Hospital admission and emergency care attendance risk for SARS-CoV-2 delta (B.1.617.2) compared with alpha (B.1.1.7) variants of concern: a cohort study. Lancet Infect. Dis. 22:35–42
     [Google Scholar]
  19. 19.
    Wolter N, Jassat W, Walaza S, Welch R, Moultrie H et al. 2022. Early assessment of the clinical severity of the SARS-CoV-2 omicron variant in South Africa: a data linkage study. Lancet 399:437–46
     [Google Scholar]
  20. 20.
    Harvey WT, Carabelli AM, Jackson B, Gupta RK, Thomson EC et al. 2021. SARS-CoV-2 variants, spike mutations and immune escape. Nat. Rev. Microbiol. 19:409–24
     [Google Scholar]
  21. 21.
    Kuhlmann C, Mayer CK, Claassen M, Maponga T, Burgers WA et al. 2022. Breakthrough infections with SARS-CoV-2 omicron despite mRNA vaccine booster dose. Lancet 399:625–26
     [Google Scholar]
  22. 22.
    Bergwerk M, Gonen T, Lustig Y, Amit S, Lipsitch M et al. 2021. Covid-19 breakthrough infections in vaccinated health care workers. N. Engl. J. Med. 385:1474–84
     [Google Scholar]
  23. 23.
    Casanova JL, Abel L. 2022. From rare disorders of immunity to common determinants of infection: following the mechanistic thread. Cell 185:3086–103
     [Google Scholar]
  24. 24.
    Casanova JL, Abel L. 2021. Mechanisms of viral inflammation and disease in humans. Science 374:1080–86
     [Google Scholar]
  25. 25.
    Gibbs KD, Schott BH, Ko DC. 2022. The awesome power of human genetics of infectious disease. Annu. Rev. Genet. 56:41–62
     [Google Scholar]
  26. 26.
    Alcais A, Quintana-Murci L, Thaler DS, Schurr E, Abel L, Casanova JL. 2010. Life-threatening infectious diseases of childhood: single-gene inborn errors of immunity?. Ann. N. Y. Acad. Sci. 1214:18–33
     [Google Scholar]
  27. 27.
    Kwiatkowski DP. 2005. How malaria has affected the human genome and what human genetics can teach us about malaria. Am. J. Hum. Genet. 77:171–92
     [Google Scholar]
  28. 28.
    Meyts I, Bosch B, Bolze A, Boisson B, Itan Y et al. 2016. Exome and genome sequencing for inborn errors of immunity. J. Allergy Clin. Immunol. 138:957–69
     [Google Scholar]
  29. 29.
    Tangye SG, Al-Herz W, Bousfiha A, Cunningham-Rundles C, Franco JL et al. 2022. Human inborn errors of immunity: 2022 update on the classification from the International Union of Immunological Societies Expert Committee. J. Clin. Immunol. 42:71473–507
     [Google Scholar]
  30. 30.
    Casanova JL, Abel L. 2020. The human genetic determinism of life-threatening infectious diseases: genetic heterogeneity and physiological homogeneity?. Hum. Genet. 139:681–94
     [Google Scholar]
  31. 31.
    Casanova JL, Abel L. 2021. Lethal infectious diseases as inborn errors of immunity: toward a synthesis of the germ and genetic theories. Annu. Rev. Pathol. Mech. Dis. 16:23–50
     [Google Scholar]
  32. 32.
    Martinez-Barricarte R, Markle JG, Ma CS, Deenick EK, Ramirez-Alejo N et al. 2018. Human IFN-g immunity to mycobacteria is governed by both IL-12 and IL-23. Sci. Immunol. 3:30eaau6759
     [Google Scholar]
  33. 33.
    Bustamante J. 2020. Mendelian susceptibility to mycobacterial disease: recent discoveries. Hum. Genet. 139:993–1000
     [Google Scholar]
  34. 34.
    Rosain J, Kong XF, Martinez-Barricarte R, Oleaga-Quintas C, Ramirez-Alejo N et al. 2019. Mendelian susceptibility to mycobacterial disease: 2014–2018 update. Immunol. Cell Biol. 97:360–67
     [Google Scholar]
  35. 35.
    Zhang SY. 2020. Herpes simplex virus encephalitis of childhood: inborn errors of central nervous system cell-intrinsic immunity. Hum. Genet. 139:911–18
     [Google Scholar]
  36. 36.
    Bastard P, Manry J, Chen J, Rosain J, Seeleuthner Y et al. 2021. Herpes simplex encephalitis in a patient with a distinctive form of inherited IFNAR1 deficiency. J. Clin. Investig. 131:1e139980
     [Google Scholar]
  37. 37.
    Boisson-Dupuis S. 2020. The monogenic basis of human tuberculosis. Hum. Genet. 139:1001–9
     [Google Scholar]
  38. 38.
    Boisson-Dupuis S, Ramirez-Alejo N, Li Z, Patin E, Rao G et al. 2018. Tuberculosis and impaired IL-23-dependent IFN-g immunity in humans homozygous for a common TYK2 missense variant. Sci. Immunol. 3:30eaau8714
     [Google Scholar]
  39. 39.
    Kerner G, Laval G, Patin E, Boisson-Dupuis S, Abel L et al. 2021. Human ancient DNA analyses reveal the high burden of tuberculosis in Europeans over the last 2,000 years. Am. J. Hum. Genet. 108:517–24
     [Google Scholar]
  40. 40.
    Kerner G, Ramirez-Alejo N, Seeleuthner Y, Yang R, Ogishi M et al. 2019. Homozygosity for TYK2 P1104A underlies tuberculosis in about 1% of patients in a cohort of European ancestry. PNAS 116:10430–34
     [Google Scholar]
  41. 41.
    COVID-19 Host Genet. Initiat 2020. 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. 28:715–18
     [Google Scholar]
  42. 42.
    Casanova JL, Su HC, COVID Hum. Genet. Effort 2020. A global effort to define the human genetics of protective immunity to SARS-CoV-2 infection. Cell 181:1194–99
     [Google Scholar]
  43. 43.
    COVID-19 Host Genet. Initiat 2022. A first update on mapping the human genetic architecture of COVID-19. Nature 608:E1–10
     [Google Scholar]
  44. 44.
    Kousathanas A, Pairo-Castineira E, Rawlik K, Stuckey A, Odhams CA et al. 2022. Whole-genome sequencing reveals host factors underlying critical COVID-19. Nature 607:97–103
     [Google Scholar]
  45. 45.
    Severe Covid-19 GWAS Group, Ellinghaus D, Degenhardt F, Bujanda L, Buti M et al. 2020. Genomewide association study of severe Covid-19 with respiratory failure. N. Engl. J. Med. 383:1522–34
     [Google Scholar]
  46. 46.
    Zeberg H, Paabo S. 2020. The major genetic risk factor for severe COVID-19 is inherited from Neanderthals. Nature 587:610–12
     [Google Scholar]
  47. 47.
    Pairo-Castineira E, Clohisey S, Klaric L, Bretherick AD, Rawlik K et al. 2021. Genetic mechanisms of critical illness in COVID-19. Nature 591:92–98
     [Google Scholar]
  48. 48.
    COVID-19 Host Genet. Initiat 2021. Mapping the human genetic architecture of COVID-19. Nature 600:472–77
     [Google Scholar]
  49. 49.
    Downes DJ, Cross AR, Hua P, Roberts N, Schwessinger R et al. 2021. Identification of LZTFL1 as a candidate effector gene at a COVID-19 risk locus. Nat. Genet. 53:1606–15
     [Google Scholar]
  50. 50.
    Horowitz JE, Kosmicki JA, Damask A, Sharma D, Roberts GHL et al. 2022. Genome-wide analysis provides genetic evidence that ACE2 influences COVID-19 risk and yields risk scores associated with severe disease. Nat. Genet. 54:382–92
     [Google Scholar]
  51. 51.
    Dendrou CA, Cortes A, Shipman L, Evans HG, Attfield KE et al. 2016. Resolving TYK2 locus genotype-to-phenotype differences in autoimmunity. Sci. Transl. Med. 8:363ra149
     [Google Scholar]
  52. 52.
    Huffman JE, Butler-Laporte G, Khan A, Pairo-Castineira E, Drivas TG et al. 2022. Multi-ancestry fine mapping implicates OAS1 splicing in risk of severe COVID-19. Nat. Genet. 54:125–27
     [Google Scholar]
  53. 53.
    Zeberg H, Paabo S. 2021. A genomic region associated with protection against severe COVID-19 is inherited from Neandertals. PNAS 118:9e2026309118
     [Google Scholar]
  54. 54.
    Dong B, Xu L, Zhou A, Hassel BA, Lee X et al. 1994. Intrinsic molecular activities of the interferon-induced 2–5A-dependent RNase. J. Biol. Chem. 269:14153–58
     [Google Scholar]
  55. 55.
    Schwartz SL, Conn GL. 2019. RNA regulation of the antiviral protein 2′-5′-oligoadenylate synthetase. WIREs RNA 10:e1534
     [Google Scholar]
  56. 56.
    Bonnevie-Nielsen V, Field LL, Lu S, Zheng DJ, Li M et al. 2005. Variation in antiviral 2′,5′-oligoadenylate synthetase (2′5′AS) enzyme activity is controlled by a single-nucleotide polymorphism at a splice-acceptor site in the OAS1 gene. Am. J. Hum. Genet. 76:623–33
     [Google Scholar]
  57. 57.
    Fadista J, Kraven LM, Karjalainen J, Andrews SJ, Geller F et al. 2021. Shared genetic etiology between idiopathic pulmonary fibrosis and COVID-19 severity. eBioMedicine 65:103277
     [Google Scholar]
  58. 58.
    Shrine N, Guyatt AL, Erzurumluoglu AM, Jackson VE, Hobbs BD et al. 2019. New genetic signals for lung function highlight pathways and chronic obstructive pulmonary disease associations across multiple ancestries. Nat. Genet. 51:481–93
     [Google Scholar]
  59. 59.
    Hobbs BD, de Jong K, Lamontagne M, Bosse Y, Shrine N et al. 2017. Genetic loci associated with chronic obstructive pulmonary disease overlap with loci for lung function and pulmonary fibrosis. Nat. Genet. 49:426–32
     [Google Scholar]
  60. 60.
    Fingerlin TE, Murphy E, Zhang W, Peljto AL, Brown KK et al. 2013. Genome-wide association study identifies multiple susceptibility loci for pulmonary fibrosis. Nat. Genet. 45:613–20
     [Google Scholar]
  61. 61.
    Gordon DE, Hiatt J, Bouhaddou M, Rezelj VV, Ulferts S et al. 2020. Comparative host-coronavirus protein interaction networks reveal pan-viral disease mechanisms. Science 370:6521abe9403
     [Google Scholar]
  62. 62.
    Ciancanelli MJ, Huang SX, Luthra P, Garner H, Itan Y et al. 2015. Life-threatening influenza and impaired interferon amplification in human IRF7 deficiency. Science 348:448–53
     [Google Scholar]
  63. 63.
    Hernandez N, Melki I, Jing H, Habib T, Huang SSY et al. 2018. Life-threatening influenza pneumonitis in a child with inherited IRF9 deficiency. J. Exp. Med. 215:2567–85
     [Google Scholar]
  64. 64.
    Lim HK, Huang SXL, Chen J, Kerner G, Gilliaux O et al. 2019. Severe influenza pneumonitis in children with inherited TLR3 deficiency. J. Exp. Med. 216:2038–56
     [Google Scholar]
  65. 65.
    Abolhassani H, Vosughimotlagh A, Asano T, Landegren N, Boisson B et al. 2022. X-linked TLR7 deficiency underlies critical COVID-19 pneumonia in a male patient with ataxia-telangiectasia. J. Clin. Immunol. 42:1–9
     [Google Scholar]
  66. 66.
    Schmidt A, Peters S, Knaus A, Sabir H, Hamsen F et al. 2021. TBK1 and TNFRSF13B mutations and an autoinflammatory disease in a child with lethal COVID-19. npj Genom. Med. 6:55
     [Google Scholar]
  67. 67.
    Zhang Q, Matuozzo D, Le Pen J, Lee D, Moens L et al. 2022. Recessive inborn errors of type I IFN immunity in children with COVID-19 pneumonia. J. Exp. Med. 219:8e20220131
     [Google Scholar]
  68. 68.
    Khanmohammadi S, Rezaei N, Khazaei M, Shirkani A. 2022. A case of autosomal recessive interferon alpha/beta receptor alpha chain (IFNAR1) deficiency with severe COVID-19. J. Clin. Immunol. 42:19–24
     [Google Scholar]
  69. 69.
    Abolhassani H, Landegren N, Bastard P, Materna M, Modaresi M et al. 2022. Inherited IFNAR1 deficiency in a child with both critical COVID-19 pneumonia and multisystem inflammatory syndrome. J. Clin. Immunol. 42:471–83
     [Google Scholar]
  70. 70.
    Butler-Laporte G, Povysil G, Kosmicki JA, Cirulli ET, Drivas T et al. 2022. Exome-wide association study to identify rare variants influencing COVID-19 outcomes: results from the Host Genetics Initiative. PLOS Genet. 18:e1010367
     [Google Scholar]
  71. 71.
    Kosmicki JA, Horowitz JE, Banerjee N, Lanche R, Marcketta A et al. 2021. Pan-ancestry exome-wide association analyses of COVID-19 outcomes in 586,157 individuals. Am. J. Hum. Genet. 108:1350–55
     [Google Scholar]
  72. 72.
    Povysil G, Butler-Laporte G, Shang N, Wang C, Khan A et al. 2021. Rare loss-of-function variants in type I IFN immunity genes are not associated with severe COVID-19. J. Clin. Investig. 131:14e147834
     [Google Scholar]
  73. 73.
    Zhang Q, Cobat A, Bastard P, Notarangelo LD, Su HC et al. 2021. Association of rare predicted loss-of-function variants of influenza-related type I IFN genes with critical COVID-19 pneumonia. J. Clin. Investig. 131:15e152474
     [Google Scholar]
  74. 74.
    Matuozzo D, Talouarn E, Marchal A, Zhang P, Manry J et al. 2023. Rare predicted loss-of-function variants of type I IFN immunity genes are associated with life-threatening COVID-19. Genome Med. 15:22
     [Google Scholar]
  75. 75.
    Li J, Lei WT, Zhang P, Rapaport F, Seeleuthner Y et al. 2021. Biochemically deleterious human NFKB1 variants underlie an autosomal dominant form of common variable immunodeficiency. J. Exp. Med. 218:11e20210566
     [Google Scholar]
  76. 76.
    Koning R, Bastard P, Casanova JL, Brouwer MC, van de Beek D, Amsterdam U.M.C. COVID-19 Biobank Investig 2021. Autoantibodies against type I interferons are associated with multi-organ failure in COVID-19 patients. Intensive Care Med. 47:704–6
     [Google Scholar]
  77. 77.
    Lamborn IT, Jing H, Zhang Y, Drutman SB, Abbott JK et al. 2017. Recurrent rhinovirus infections in a child with inherited MDA5 deficiency. J. Exp. Med. 214:1949–72
     [Google Scholar]
  78. 78.
    Fallerini C, Daga S, Mantovani S, Benetti E, Picchiotti N et al. 2021. Association of Toll-like receptor 7 variants with life-threatening COVID-19 disease in males: findings from a nested case-control study. eLife 10:e67569
     [Google Scholar]
  79. 79.
    Mantovani S, Daga S, Fallerini C, Baldassarri M, Benetti E et al. 2022. Rare variants in Toll-like receptor 7 results in functional impairment and downregulation of cytokine-mediated signaling in COVID-19 patients. Genes Immun. 23:51–56
     [Google Scholar]
  80. 80.
    Pessoa NL, Bentes AA, de Carvalho AL, de Souza Silva TB, Alves PA et al. 2021. Case report: hepatitis in a child infected with SARS-CoV-2 presenting Toll-like receptor 7 Gln11Leu single nucleotide polymorphism. Virol. J. 18:180
     [Google Scholar]
  81. 81.
    Solanich X, Vargas-Parra G, van der Made CI, Simons A, Schuurs-Hoeijmakers J et al. 2021. Genetic screening for TLR7 variants in young and previously healthy men with severe COVID-19. Front. Immunol. 12:719115
     [Google Scholar]
  82. 82.
    van der Made CI, Simons A, Schuurs-Hoeijmakers J, van den Heuvel G, Mantere T et al. 2020. Presence of genetic variants among young men with severe COVID-19. JAMA 324:663–73
     [Google Scholar]
  83. 83.
    Casanova JL, Abel L. 2015. Disentangling inborn and acquired immunity in human twins. Cell 160:13–15
     [Google Scholar]
  84. 84.
    Nakanishi T, Pigazzini S, Degenhardt F, Cordioli M, Butler-Laporte G et al. 2021. Age-dependent impact of the major common genetic risk factor for COVID-19 on severity and mortality. J. Clin. Investig. 131:23e152386
     [Google Scholar]
  85. 85.
    Cruz R, Almeida SD, Heredia ML, Quintela I, Ceballos FC et al. 2022. Novel genes and sex differences in COVID-19 severity. Hum. Mol. Genet. 31:223789–806
     [Google Scholar]
  86. 86.
    Bartleson JM, Radenkovic D, Covarrubias AJ, Furman D, Winer DA, Verdin E. 2021. SARS-CoV-2, COVID-19 and the ageing immune system. Nat. Aging 1:769–82
     [Google Scholar]
  87. 87.
    Splunter MV, Perdijk O, Fick-Brinkhof H, Floris-Vollenbroek EG, Meijer B et al. 2019. Plasmacytoid dendritic cell and myeloid dendritic cell function in ageing: a comparison between elderly and young adult women. PLOS ONE 14:e0225825
     [Google Scholar]
  88. 88.
    Schultze JL, Aschenbrenner AC. 2021. COVID-19 and the human innate immune system. Cell 184:1671–92
     [Google Scholar]
  89. 89.
    Stark GR, Darnell JE Jr. 2012. The JAK-STAT pathway at twenty. Immunity 36:503–14
     [Google Scholar]
  90. 90.
    Pierce CA, Sy S, Galen B, Goldstein DY, Orner E et al. 2021. Natural mucosal barriers and COVID-19 in children. JCI Insight 6:9e148694
     [Google Scholar]
  91. 91.
    Andreakos E, Abel L, Vinh DC, Kaja E, Drolet BA et al. 2022. A global effort to dissect the human genetic basis of resistance to SARS-CoV-2 infection. Nat. Immunol. 23:159–64
     [Google Scholar]
  92. 92.
    Martinez-Sanz J, Jimenez D, Martinez-Campelo L, Cruz R, Vizcarra P et al. 2021. Role of ACE2 genetic polymorphisms in susceptibility to SARS-CoV-2 among highly exposed but non infected healthcare workers. Emerg. Microbes Infect. 10:493–96
     [Google Scholar]
  93. 93.
    Reukers DFM, van Boven M, Meijer A, Rots N, Reusken C et al. 2022. High infection secondary attack rates of severe acute respiratory syndrome coronavirus 2 in Dutch households revealed by dense sampling. Clin. Infect. Dis. 74:52–58
     [Google Scholar]
  94. 94.
    Tournamille C, Colin Y, Cartron JP, Le Van Kim C. 1995. Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat. Genet. 10:224–28
     [Google Scholar]
  95. 95.
    Dean M, Carrington M, Winkler C, Huttley GA, Smith MW et al. 1996. Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Science 273:1856–62
     [Google Scholar]
  96. 96.
    Liu R, Paxton WA, Choe S, Ceradini D, Martin SR et al. 1996. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367–77
     [Google Scholar]
  97. 97.
    Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C et al. 1996. Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382:722–25
     [Google Scholar]
  98. 98.
    Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X et al. 2003. Human susceptibility and resistance to Norwalk virus infection. Nat. Med. 9:548–53
     [Google Scholar]
  99. 99.
    Shelton JF, Shastri AJ, Ye C, Weldon CH, Filshtein-Sonmez T et al. 2021. Trans-ancestry analysis reveals genetic and nongenetic associations with COVID-19 susceptibility and severity. Nat. Genet. 53:801–8
     [Google Scholar]
  100. 100.
    Gutierrez-Valencia M, Leache L, Librero J, Jerico C, Enguita German M, Garcia-Erce JA 2022. ABO blood group and risk of COVID-19 infection and complications: a systematic review and meta-analysis. Transfusion 62:493–505
     [Google Scholar]
  101. 101.
    Cooling L. 2015. Blood groups in infection and host susceptibility. Clin. Microbiol. Rev. 28:801–70
     [Google Scholar]
  102. 102.
    Cheng Y, Cheng G, Chui CH, Lau FY, Chan PK et al. 2005. ABO blood group and susceptibility to severe acute respiratory syndrome. JAMA 293:1450–51
     [Google Scholar]
  103. 103.
    Roberts GHL, Partha R, Rhead B, Knight SC, Park DS et al. 2022. Expanded COVID-19 phenotype definitions reveal distinct patterns of genetic association and protective effects. Nat. Genet. 54:374–81
     [Google Scholar]
  104. 104.
    Biering SB, Sarnik SA, Wang E, Zengel JR, Leist SR et al. 2022. Genome-wide bidirectional CRISPR screens identify mucins as host factors modulating SARS-CoV-2 infection. Nat. Genet. 54:1078–89
     [Google Scholar]
  105. 105.
    Grodzki M, Bluhm AP, Schaefer M, Tagmount A, Russo M et al. 2022. Genome-scale CRISPR screens identify host factors that promote human coronavirus infection. Genome Med. 14:10
     [Google Scholar]
  106. 106.
    Zhu Y, Feng F, Hu G, Wang Y, Yu Y et al. 2021. A genome-wide CRISPR screen identifies host factors that regulate SARS-CoV-2 entry. Nat. Commun. 12:961
     [Google Scholar]
  107. 107.
    Wang R, Simoneau CR, Kulsuptrakul J, Bouhaddou M, Travisano KA et al. 2021. Genetic screens identify host factors for SARS-CoV-2 and common cold coronaviruses. Cell 184:106–19.e14
     [Google Scholar]
  108. 108.
    Schneider WM, Luna JM, Hoffmann HH, Sanchez-Rivera FJ, Leal AA et al. 2021. Genome-scale identification of SARS-CoV-2 and pan-coronavirus host factor networks. Cell 184:120–32.e14
     [Google Scholar]
  109. 109.
    Wei J, Alfajaro MM, DeWeirdt PC, Hanna RE, Lu-Culligan WJ et al. 2021. Genome-wide CRISPR screens reveal host factors critical for SARS-CoV-2 infection. Cell 184:76–91.e13
     [Google Scholar]
  110. 110.
    Daniloski Z, Jordan TX, Wessels HH, Hoagland DA, Kasela S et al. 2021. Identification of required host factors for SARS-CoV-2 infection in human cells. Cell 184:92–105.e16
     [Google Scholar]
  111. 111.
    Baggen J, Persoons L, Vanstreels E, Jansen S, Van Looveren D et al. 2021. Genome-wide CRISPR screening identifies TMEM106B as a proviral host factor for SARS-CoV-2. Nat. Genet. 53:435–44
     [Google Scholar]
  112. 112.
    Rebendenne A, Roy P, Bonaventure B, Chaves Valadao AL, Desmarets L et al. 2022. Bidirectional genome-wide CRISPR screens reveal host factors regulating SARS-CoV-2, MERS-CoV and seasonal HCoVs. Nat. Genet. 54:1090–102
     [Google Scholar]
  113. 113.
    Andreakos E, Abel L, Vinh DC, Kaja E, Drolet BA et al. 2021. A global effort to dissect the human genetic basis of resistance to SARS-CoV-2 infection. Nat. Immunol. 23:159–64
     [Google Scholar]
  114. 114.
    Bastard P, Gervais A, Le Voyer T, Rosain J, Philippot Q et al. 2021. Autoantibodies neutralizing type I IFNs are present in ∼4% of uninfected individuals over 70 years old and account for ∼20% of COVID-19 deaths. Sci. Immunol. 6:62eabl4340
     [Google Scholar]
  115. 115.
    Bastard P, Rosen LB, Zhang Q, Michailidis E, Hoffmann HH et al. 2020. Autoantibodies against type I IFNs in patients with life-threatening COVID-19. Science 370:6515abd4585
     [Google Scholar]
  116. 116.
    Puel A, Bastard P, Bustamante J, Casanova JL. 2022. Human autoantibodies underlying infectious diseases. J. Exp. Med. 219:4e20211387
     [Google Scholar]
  117. 117.
    Ku CL, Chi CY, von Bernuth H, Doffinger R. 2020. Autoantibodies against cytokines: phenocopies of primary immunodeficiencies?. Hum. Genet. 139:783–94
     [Google Scholar]
  118. 118.
    Pozzetto B, Mogensen KE, Tovey MG, Gresser I. 1984. Characteristics of autoantibodies to human interferon in a patient with varicella-zoster disease. J. Infect. Dis. 150:707–13
     [Google Scholar]
  119. 119.
    Goncalves D, Mezidi M, Bastard P, Perret M, Saker K et al. 2021. Antibodies against type I interferon: detection and association with severe clinical outcome in COVID-19 patients. Clin. Transl. Immunol. 10:e1327
     [Google Scholar]
  120. 120.
    Shaw ER, Rosen LB, Cheng A, Dobbs K, Delmonte OM et al. 2021. Temporal dynamics of anti-type I interferon autoantibodies in COVID-19 patients. Clin. Infect. Dis. 75:1e1192–94
     [Google Scholar]
  121. 121.
    Savvateeva E, Filippova M, Valuev-Elliston V, Nuralieva N, Yukina M et al. 2021. Microarray-based detection of antibodies against SARS-CoV-2 proteins, common respiratory viruses and type I interferons. Viruses 13:122553
     [Google Scholar]
  122. 122.
    Troya J, Bastard P, Planas-Serra L, Ryan P, Ruiz M et al. 2021. Neutralizing autoantibodies to type I IFNs in >10% of patients with severe COVID-19 pneumonia hospitalized in Madrid, Spain. J. Clin. Immunol. 41:914–22
     [Google Scholar]
  123. 123.
    van der Wijst MGP, Vazquez SE, Hartoularos GC, Bastard P, Grant T et al. 2021. Type I interferon autoantibodies are associated with systemic immune alterations in patients with COVID-19. Sci. Transl. Med. 13:eabh2624
     [Google Scholar]
  124. 124.
    Vazquez SE, Bastard P, Kelly K, Gervais A, Norris PJ et al. 2021. Neutralizing autoantibodies to type I interferons in COVID-19 convalescent donor plasma. J. Clin. Immunol. 41:1169–71
     [Google Scholar]
  125. 125.
    Wang EY, Mao T, Klein J, Dai Y, Huck JD et al. 2021. Diverse functional autoantibodies in patients with COVID-19. Nature 595:283–88
     [Google Scholar]
  126. 126.
    Abers MS, Rosen LB, Delmonte OM, Shaw E, Bastard P et al. 2021. Neutralizing type-I interferon autoantibodies are associated with delayed viral clearance and intensive care unit admission in patients with COVID-19. Immunol. Cell Biol. 99:917–21
     [Google Scholar]
  127. 127.
    Chauvineau-Grenier A, Bastard P, Servajean A, Gervais A, Rosain J et al. 2021. Autoantibodies neutralizing type I interferons in 20% of COVID-19 deaths in a French hospital. Res. Sq. rs.3.rs-915062/v1. https://doi.org/10.21203/rs.3.rs-915062/v1
  128. 128.
    Solanich X, Rigo-Bonnin R, Gumucio VD, Bastard P, Rosain J et al. 2021. Pre-existing autoantibodies neutralizing high concentrations of type I interferons in almost 10% of COVID-19 patients admitted to intensive care in Barcelona. J. Clin. Immunol. 41:81733–44
     [Google Scholar]
  129. 129.
    Raadsen MP, Gharbharan A, Jordans CCE, Mykytyn AZ, Lamers MM et al. 2022. Interferon-α2 auto-antibodies in convalescent plasma therapy for COVID-19. J. Clin. Immunol. 42:232–39
     [Google Scholar]
  130. 130.
    Chang SE, Feng A, Meng W, Apostolidis SA, Mack E et al. 2021. New-onset IgG autoantibodies in hospitalized patients with COVID-19. Nat. Commun. 12:5417
     [Google Scholar]
  131. 131.
    Ziegler CGK, Miao VN, Owings AH, Navia AW, Tang Y et al. 2021. Impaired local intrinsic immunity to SARS-CoV-2 infection in severe COVID-19. Cell 184:4713–33.e22
     [Google Scholar]
  132. 132.
    Acosta-Ampudia Y, Monsalve DM, Rojas M, Rodriguez Y, Gallo JE et al. 2021. COVID-19 convalescent plasma composition and immunological effects in severe patients. J. Autoimmun. 118:102598
     [Google Scholar]
  133. 133.
    Carapito R, Li R, Helms J, Carapito C, Gujja S et al. 2022. Identification of driver genes for critical forms of COVID-19 in a deeply phenotyped young patient cohort. Sci. Transl. Med. 14:eabj7521
     [Google Scholar]
  134. 134.
    Eto S, Nukui Y, Tsumura M, Nakagama Y, Kashimada K et al. 2022. Neutralizing type I interferon autoantibodies in Japanese patients with severe COVID-19. J. Clin. Immunol. 42:1360–70
     [Google Scholar]
  135. 135.
    Manry J, Bastard P, Gervais A, Le Voyer T, Rosain J et al. 2022. The risk of COVID-19 death is much greater and age dependent with type I IFN autoantibodies. PNAS 119:e2200413119
     [Google Scholar]
  136. 136.
    Bastard P, Orlova E, Sozaeva L, Levy R, James A et al. 2021. Preexisting autoantibodies to type I IFNs underlie critical COVID-19 pneumonia in patients with APS-1. J. Exp. Med. 218:7e20210554
     [Google Scholar]
  137. 137.
    Lopez J, Mommert M, Mouton W, Pizzorno A, Brengel-Pesce K et al. 2021. Early nasal type I IFN immunity against SARS-CoV-2 is compromised in patients with autoantibodies against type I IFNs. J. Exp. Med. 218:10e20211211
     [Google Scholar]
  138. 138.
    Sposito B, Broggi A, Pandolfi L, Crotta S, Clementi N et al. 2021. The interferon landscape along the respiratory tract impacts the severity of COVID-19. Cell 184:4953–68.e16
     [Google Scholar]
  139. 139.
    Bastard P, Zhang Q, Zhang SY, Jouanguy E, Casanova JL. 2022. Type I interferons and SARS-CoV-2: from cells to organisms. Curr. Opin. Immunol. 74:172–82
     [Google Scholar]
  140. 140.
    Bastard P, Vazquez S, Liu J, Laurie MT, Wang CY et al. 2022. Vaccine breakthrough hypoxemic COVID-19 pneumonia in patients with auto-Abs neutralizing type I IFNs. Sci. Immunol. In press
    [Google Scholar]
  141. 141.
    Zhang Q, Pizzorno A, Miorin L, Bastard P, Gervais A et al. 2022. Autoantibodies against type I IFNs in patients with critical influenza pneumonia. J. Exp. Med. 219:11e20220514
     [Google Scholar]
  142. 142.
    Busnadiego I, Abela IA, Frey PM, Hofmaenner DA, Scheier TC et al. 2022. Critically ill COVID-19 patients with neutralizing autoantibodies against type I interferons have increased risk of herpesvirus disease. PLOS Biol. 20:e3001709
     [Google Scholar]
  143. 143.
    Mathian A, Breillat P, Dorgham K, Bastard P, Charre C et al. 2022. Lower disease activity but higher risk of severe COVID-19 and herpes zoster in patients with systemic lupus erythematosus with pre-existing autoantibodies neutralising IFN-α. Ann. Rheum. Dis. 81:1695–703
     [Google Scholar]
  144. 144.
    Sun S, Wang Y, Maslov AY, Dong X, Vijg J. 2022. SomaMutDB: a database of somatic mutations in normal human tissues. Nucleic Acids Res. 50:D1100–8
     [Google Scholar]
  145. 145.
    Levy R, Zhang P, Bastard P, Dorgham K, Melki I et al. 2021. Monoclonal antibody–mediated neutralization of SARS-CoV-2 in an IRF9-deficient child. PNAS 118:45e2114390118
     [Google Scholar]
  146. 146.
    de Prost N, Bastard P, Arrestier R, Fourati S, Mahevas M et al. 2021. Plasma exchange to rescue patients with autoantibodies against type I interferons and life-threatening COVID-19 pneumonia. J. Clin. Immunol. 41:536–44
     [Google Scholar]
  147. 147.
    Vinh DC, Abel L, Bastard P, Cheng MP, Condino-Neto A et al. 2021. Harnessing type I IFN immunity against SARS-CoV-2 with early administration of IFN-β. J. Clin. Immunol. 41:71425–42
     [Google Scholar]
  148. 148.
    Khera AV, Chaffin M, Aragam KG, Haas ME, Roselli C et al. 2018. Genome-wide polygenic scores for common diseases identify individuals with risk equivalent to monogenic mutations. Nat. Genet. 50:1219–24
     [Google Scholar]
  149. 149.
    Huang QM, Zhang PD, Li ZH, Zhou JM, Liu D et al. 2022. Genetic risk and chronic obstructive pulmonary disease independently predict the risk of incident severe COVID-19. Ann. Am. Thorac. Soc. 19:58–65
     [Google Scholar]
  150. 150.
    Kaiser J. 2021. DNA test to predict odds of severe COVID-19 draws scrutiny. Science 372:1139
     [Google Scholar]
  151. 151.
    Tangye SG, COVID Hum. Genet. Effort Consort 2023. Impact of SARS-CoV-2 infection and COVID-19 on patients with inborn errors of immunity. J. Allergy Clin. Immunol. 151:818–31
     [Google Scholar]
  152. 152.
    Lee D, Le Pen J, Yatim A, Dong B, Aquino Y et al. 2022. Inborn errors of OAS–RNase L in SARS-CoV-2–related multisystem inflammatory syndrome in children. Science 379:6632abo3627
     [Google Scholar]
  153. 153.
    Chou J, Platt CD, Habiballah S, Nguyen AA, Elkins M et al. 2021. Mechanisms underlying genetic susceptibility to multisystem inflammatory syndrome in children (MIS-C). J. Allergy Clin. Immunol. 148:732–38.e1
     [Google Scholar]
  154. 154.
    Lee PY, Platt CD, Weeks S, Grace RF, Maher G et al. 2020. Immune dysregulation and multisystem inflammatory syndrome in children (MIS-C) in individuals with haploinsufficiency of SOCS1. J. Allergy Clin. Immunol. 146:1194–200.e1
     [Google Scholar]
  155. 155.
    Bolze A, Mogensen TH, Zhang SY, Abel L, Andreakos E et al. 2022. Decoding the human genetic and immunological basis of COVID-19 mRNA vaccine–induced myocarditis. J. Clin. Immunol. 42:1354–59
     [Google Scholar]
  156. 156.
    Namkoong H, Edahiro R, Takano T, Nishihara H, Shirai Y et al. 2022. DOCK2 is involved in the host genetics and biology of severe COVID-19. Nature 609:754–60
     [Google Scholar]
  157. 157.
    Ostendorf BN, Patel MA, Bilanovic J, Hoffmann HH, Carrasco SE et al. 2022. Common human genetic variants of APOE impact murine COVID-19 mortality. Nature 611:346–51
     [Google Scholar]
  158. 158.
    Herrera-Esposito D, de Los Campos G. 2022. Age-specific rate of severe and critical SARS-CoV-2 infections estimated with multi-country seroprevalence studies. BMC Infect. Dis. 22:311
     [Google Scholar]
  159. 159.
    Asano T, Boisson B, Onodi F, Matuozzo D, Moncada-Velez M et al. 2021. X-linked recessive TLR7 deficiency in ∼1% of men under 60 years old with life-threatening COVID-19. Sci. Immunol. 6:eabl4348
     [Google Scholar]
  160. 160.
    Zhang Q, Bastard P, Liu Z, Le Pen J, Moncada-Velez M et al. 2020. Inborn errors of type I IFN immunity in patients with life-threatening COVID-19. Science 370:6515eabd4570
     [Google Scholar]
/content/journals/10.1146/annurev-biodatasci-020222-021705
Loading
Human Genomics of COVID-19 Pneumonia: Contributions of Rare and Common Variants
Annual Review of Biomedical Data Science 6, 465 (2023); https://doi.org/10.1146/annurev-biodatasci-020222-021705
/content/journals/10.1146/annurev-biodatasci-020222-021705
/content/journals/10.1146/annurev-biodatasci-020222-021705
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error