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1. Inborn errors of type I IFN immunity in patients with life-threatening COVID-19

Author

Zhang, Q, Liu, Z, Moncada-Velez, M, Chen, J, Ogishi, M, Bigio, B, Yang, R, Arias, AA, Zhou, Q, Han, JE, Ugurbil, AC, Zhang, P, Rapaport, F, Li, J, Spaan, AN, Boisson, B, Boisson-Dupuis, S, Bustamante, J, Puel, A, Ciancanelli, MJ, Zhang, SY, Béziat, V, Jouanguy, E, Abel, L, Cobat, A, Casanova, JL, Bastard, P, Korol, C, Rosain, J, Philippot, Q, Chbihi, M, Lorenzo, L, Bizien, L, Neehus, AL, Kerner, G, Seeleuthner, Y, Manry, J, Le Voyer, T, Le Pen, J, Schneider, WM, Razooky, BS, Hoffmann, HH, Michailidis, E, Rice, CM, Sabli, IKD, Hodeib, S, Sancho-Shimizu, V, Bilguvar, K, Ye, J, Maniatis, T, Bolze, A, Zhang, Y, Notarangelo, LD, Su, HC, Onodi, F, Korniotis, S, Karpf, L, Soumelis, V, Bonnet-Madin, L, Amara, A, Dorgham, K, Gorochov, G, Smith, N, Duffy, D, Moens, L, Meyts, I, Zhang, Q, Liu, Z, Moncada-Velez, M, Chen, J, Ogishi, M, Bigio, B, Yang, R, Arias, AA, Zhou, Q, Han, JE, Ugurbil, AC, Zhang, P, Rapaport, F, Li, J, Spaan, AN, Boisson, B, Boisson-Dupuis, S, Bustamante, J, Puel, A, Ciancanelli, MJ, Zhang, SY, Béziat, V, Jouanguy, E, Abel, L, Cobat, A, Casanova, JL, Bastard, P, Korol, C, Rosain, J, Philippot, Q, Chbihi, M, Lorenzo, L, Bizien, L, Neehus, AL, Kerner, G, Seeleuthner, Y, Manry, J, Le Voyer, T, Le Pen, J, Schneider, WM, Razooky, BS, Hoffmann, HH, Michailidis, E, Rice, CM, Sabli, IKD, Hodeib, S, Sancho-Shimizu, V, Bilguvar, K, Ye, J, Maniatis, T, Bolze, A, Zhang, Y, Notarangelo, LD, Su, HC, Onodi, F, Korniotis, S, Karpf, L, Soumelis, V, Bonnet-Madin, L, Amara, A, Dorgham, K, Gorochov, G, Smith, N, Duffy, D, Moens, L, and Meyts, I

Abstract

Clinical outcome upon infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) ranges from silent infection to lethal coronavirus disease 2019 (COVID-19). We have found an enrichment in rare variants predicted to be loss-of-function (LOF) at the 13 human loci known to govern Toll-like receptor 3 (TLR3)- and interferon regulatory factor 7 (IRF7)-dependent type I interferon (IFN) immunity to influenza virus in 659 patients with life-threatening COVID-19 pneumonia relative to 534 subjects with asymptomatic or benign infection. By testing these and other rare variants at these 13 loci, we experimentally defined LOF variants underlying autosomal-recessive or autosomal-dominant deficiencies in 23 patients (3.5%) 17 to 77 years of age. We show that human fibroblasts with mutations affecting this circuit are vulnerable to SARS-CoV-2. Inborn errors of TLR3- and IRF7-dependent type I IFN immunity can underlie life-threatening COVID-19 pneumonia in patients with no prior severe infection.

Published
2020

2. Autoantibodies against type I IFNs in patients with life-threatening COVID-19

Author

Bastard, P, Rosen, LB, Zhang, Q, Michailidis, E, Hoffmann, HH, Zhang, Y, Dorgham, K, Philippot, Q, Rosain, J, Béziat, V, Manry, J, Shaw, E, Haljasmägi, L, Peterson, P, Lorenzo, L, Bizien, L, Trouillet-Assant, S, Dobbs, K, de Jesus, AA, Belot, A, Kallaste, A, Catherinot, E, Tandjaoui-Lambiotte, Y, Le Pen, J, Kerner, G, Bigio, B, Seeleuthner, Y, Yang, R, Bolze, A, Spaan, AN, Delmonte, OM, Abers, MS, Aiuti, A, Casari, G, Lampasona, V, Piemonti, L, Ciceri, F, Bilguvar, K, Lifton, RP, Vasse, M, Smadja, DM, Migaud, M, Hadjadj, J, Terrier, B, Duffy, D, Quintana-Murci, L, van de Beek, D, Roussel, L, Vinh, DC, Tangye, SG, Haerynck, F, Dalmau, D, Martinez-Picado, J, Brodin, P, Nussenzweig, MC, Boisson-Dupuis, S, Rodríguez-Gallego, C, Vogt, G, Mogensen, TH, Oler, AJ, Gu, J, Burbelo, PD, Cohen, JI, Biondi, A, Bettini, LR, DÁngio, M, Bonfanti, P, Rossignol, P, Mayaux, J, Rieux-Laucat, F, Husebye, ES, Fusco, F, Ursini, MV, Imberti, L, Sottini, A, Paghera, S, Quiros-Roldan, E, Rossi, C, Castagnoli, R, Montagna, D, Licari, A, Marseglia, GL, Duval, X, Ghosn, J, Tsang, JS, Goldbach-Mansky, R, Kisand, K, Lionakis, MS, Puel, A, Zhang, SY, Holland, SM, Gorochov, G, Jouanguy, E, Rice, CM, Cobat, A, Notarangelo, LD, Abel, L, Su, HC, Casanova, JL, Arias, AA, Bastard, P, Rosen, LB, Zhang, Q, Michailidis, E, Hoffmann, HH, Zhang, Y, Dorgham, K, Philippot, Q, Rosain, J, Béziat, V, Manry, J, Shaw, E, Haljasmägi, L, Peterson, P, Lorenzo, L, Bizien, L, Trouillet-Assant, S, Dobbs, K, de Jesus, AA, Belot, A, Kallaste, A, Catherinot, E, Tandjaoui-Lambiotte, Y, Le Pen, J, Kerner, G, Bigio, B, Seeleuthner, Y, Yang, R, Bolze, A, Spaan, AN, Delmonte, OM, Abers, MS, Aiuti, A, Casari, G, Lampasona, V, Piemonti, L, Ciceri, F, Bilguvar, K, Lifton, RP, Vasse, M, Smadja, DM, Migaud, M, Hadjadj, J, Terrier, B, Duffy, D, Quintana-Murci, L, van de Beek, D, Roussel, L, Vinh, DC, Tangye, SG, Haerynck, F, Dalmau, D, Martinez-Picado, J, Brodin, P, Nussenzweig, MC, Boisson-Dupuis, S, Rodríguez-Gallego, C, Vogt, G, Mogensen, TH, Oler, AJ, Gu, J, Burbelo, PD, Cohen, JI, Biondi, A, Bettini, LR, DÁngio, M, Bonfanti, P, Rossignol, P, Mayaux, J, Rieux-Laucat, F, Husebye, ES, Fusco, F, Ursini, MV, Imberti, L, Sottini, A, Paghera, S, Quiros-Roldan, E, Rossi, C, Castagnoli, R, Montagna, D, Licari, A, Marseglia, GL, Duval, X, Ghosn, J, Tsang, JS, Goldbach-Mansky, R, Kisand, K, Lionakis, MS, Puel, A, Zhang, SY, Holland, SM, Gorochov, G, Jouanguy, E, Rice, CM, Cobat, A, Notarangelo, LD, Abel, L, Su, HC, Casanova, JL, and Arias, AA

Abstract

Interindividual clinical variability in the course of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection is vast. We report that at least 101 of 987 patients with life-threatening coronavirus disease 2019 (COVID-19) pneumonia had neutralizing immunoglobulin G (IgG) autoantibodies (auto-Abs) against interferon-w (IFN-w) (13 patients), against the 13 types of IFN-a (36), or against both (52) at the onset of critical disease; a few also had auto-Abs against the other three type I IFNs. The auto-Abs neutralize the ability of the corresponding type I IFNs to block SARS-CoV-2 infection in vitro. These auto-Abs were not found in 663 individuals with asymptomatic or mild SARS-CoV-2 infection and were present in only 4 of 1227 healthy individuals. Patients with auto-Abs were aged 25 to 87 years and 95 of the 101 were men. A B cell autoimmune phenocopy of inborn errors of type I IFN immunity accounts for life-threatening COVID-19 pneumonia in at least 2.6% of women and 12.5% of men.

Published
2020

3. Auto-antibodies against type I IFNs in patients with life-threatening COVID-19

Author

Universitat Rovira i Virgili, Bastard P; Rosen LB; Zhang Q; Michailidis E; Hoffmann HH; Zhang Y; Dorgham K; Philippot Q; Rosain J; Béziat V; Manry J; Shaw E; Haljasmägi L; Peterson P; Lorenzo L; Bizien L; Trouillet-Assant S; Dobbs K; de Jesus AA; Belot A; Kallaste A; Catherinot E; Tandjaoui-Lambiotte Y; Le Pen J; Kerner G; Bigio B; Seeleuthner Y; Yang R; Bolze A; Spaan AN; Delmonte OM; Abers MS; Aiuti A; Casari G; Lampasona V; Piemonti L; Ciceri F; Bilguvar K; Lifton RP; Vasse M; Smadja DM; Migaud M; Hadjadj J; Terrier B; Duffy D; Quintana-Murci L; van de Beek D; Roussel L; Vinh DC; Tangye SG; Haerynck F; Dalmau D; Martinez-Picado J; Brodin P; Nussenzweig MC; Boisson-Dupuis S; Rodríguez-Gallego C; Vogt G; Mogensen TH; Oler AJ; Gu J; Burbelo PD; Cohen J; Biondi A; Bettini LR; D'Angio M; Bonfanti P; Rossignol P; Mayaux J; Rieux-Laucat F; Husebye ES; Fusco F; Ursini MV; Imberti L; Sottini A; Paghera S; Quiros-Roldan E; Rossi C; Castagnoli R; Montagna D; Licari A; Marseglia GL; Duval X; Ghosn J; HGID Lab; NIAID-USUHS Immune Response to COVID Group; COVID Clinicians; COVID-STORM Clinicians; Imagine COVID Group; French COVID Cohort Study Group; Milieu Intérieur Consortium; CoV-Contact Cohort; Amsterdam UMC Covid-19 Biobank; COVID Human Genetic Effort; Tsang JS; Goldbach-Mansky R; Kisand K; Lionakis MS; Puel A; Zhang SY; Holland SM; Gorochov G; Jouanguy E; Rice CM; Cobat A; Notarangelo LD; Abel L; Su HC; Casanova JL, Universitat Rovira i Virgili, and Bastard P; Rosen LB; Zhang Q; Michailidis E; Hoffmann HH; Zhang Y; Dorgham K; Philippot Q; Rosain J; Béziat V; Manry J; Shaw E; Haljasmägi L; Peterson P; Lorenzo L; Bizien L; Trouillet-Assant S; Dobbs K; de Jesus AA; Belot A; Kallaste A; Catherinot E; Tandjaoui-Lambiotte Y; Le Pen J; Kerner G; Bigio B; Seeleuthner Y; Yang R; Bolze A; Spaan AN; Delmonte OM; Abers MS; Aiuti A; Casari G; Lampasona V; Piemonti L; Ciceri F; Bilguvar K; Lifton RP; Vasse M; Smadja DM; Migaud M; Hadjadj J; Terrier B; Duffy D; Quintana-Murci L; van de Beek D; Roussel L; Vinh DC; Tangye SG; Haerynck F; Dalmau D; Martinez-Picado J; Brodin P; Nussenzweig MC; Boisson-Dupuis S; Rodríguez-Gallego C; Vogt G; Mogensen TH; Oler AJ; Gu J; Burbelo PD; Cohen J; Biondi A; Bettini LR; D'Angio M; Bonfanti P; Rossignol P; Mayaux J; Rieux-Laucat F; Husebye ES; Fusco F; Ursini MV; Imberti L; Sottini A; Paghera S; Quiros-Roldan E; Rossi C; Castagnoli R; Montagna D; Licari A; Marseglia GL; Duval X; Ghosn J; HGID Lab; NIAID-USUHS Immune Response to COVID Group; COVID Clinicians; COVID-STORM Clinicians; Imagine COVID Group; French COVID Cohort Study Group; Milieu Intérieur Consortium; CoV-Contact Cohort; Amsterdam UMC Covid-19 Biobank; COVID Human Genetic Effort; Tsang JS; Goldbach-Mansky R; Kisand K; Lionakis MS; Puel A; Zhang SY; Holland SM; Gorochov G; Jouanguy E; Rice CM; Cobat A; Notarangelo LD; Abel L; Su HC; Casanova JL

Abstract

Interindividual clinical variability in the course of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection is vast. We report that at least 101 of 987 patients with life-threatening coronavirus disease 2019 (COVID-19) pneumonia had neutralizing immunoglobulin G (IgG) autoantibodies (auto-Abs) against interferon-omega (IFN-omega) (13 patients), against the 13 types of IFN-alpha (36), or against both (52) at the onset of critical disease; a few also had auto-Abs against the other three type I IFNs. The auto-Abs neutralize the ability of the corresponding type I IFNs to block SARS-CoV-2 infection in vitro. These auto-Abs were not found in 663 individuals with asymptomatic or mild SARS-CoV-2 infection and were present in only 4 of 1227 healthy individuals. Patients with auto-Abs were aged 25 to 87 years and 95 of the 101 were men. A B cell autoimmune phenocopy of inborn errors of type I IFN immunity accounts for lifethreatening COVID-19 pneumonia in at least 2.6% of women and 12.5% of men.

Published
2020

4. Inborn errors of type I IFN immunity in patients with life-threatening COVID-19

Author

Universitat Rovira i Virgili, Zhang Q, Bastard P, Liu Z, Le Pen J, Moncada-Velez M, Chen J, Ogishi M, Sabli IKD, Hodeib S, Korol C, Rosain J, Bilguvar K, Ye J, Bolze A, Bigio B, Yang R, Arias AA, Zhou Q, Zhang Y, Onodi F, Korniotis S, Karpf L, Philippot Q, Chbihi M, Bonnet-Madin L, Dorgham K, Smith N, Schneider WM, Razooky BS, Hoffmann HH, Michailidis E, Moens L, Han JE, Lorenzo L, Bizien L, Meade P, Neehus AL, Ugurbil AC, Corneau A, Kerner G, Zhang P, Rapaport F, Seeleuthner Y, Manry J, Masson C, Schmitt Y, Schlüter A, Le Voyer T, Khan T, Li J, Fellay J, Roussel L, Shahrooei M, Alosaimi MF, Mansouri D, Al-Saud H, Al-Mulla F, Almourfi F, Al-Muhsen SZ, Alsohime F, Al Turki S, Hasanato R, van de Beek D, Biondi A, Bettini LR, D'Angio M, Bonfanti P, Imberti L, Sottini A, Paghera S, Quiros-Roldan E, Rossi C, Oler AJ, Tompkins MF, Alba C, Vandernoot I, Goffard JC, Smits G, Migeotte I, Haerynck F, Soler-Palacin P, Martin-Nalda A, Colobran R, Morange PE, Keles S, Çölkesen F, Ozcelik T, Yasar KK, Senoglu S, Karabela ?N, Gallego CR, Novelli G, Hraiech S, Tandjaoui-Lambiotte Y, Duval X, Laouénan C,, Snow AL, Dalgard CL, Milner J, Vinh DC, Mogensen TH, Marr N, Spaan AN, Boisson B, Boisson-Dupuis S, Bustamante J, Puel A, Ciancanelli M, Meyts I, Maniatis T, Soumelis V, Amara A, Nussenzweig M, García-Sastre A, Krammer F, Pujol A, Duffy D, Lifton R, Zhang SY, Gorochov G, Béziat V, Jouanguy E, Sancho-Shimizu V, Rice CM, Abel L, Notarangelo LD, Cobat A, Su HC, Casanova JL COVID-STORM Clinicians, COVID Clinicians, Imagine COVID Group, French COVID Cohort Study Group, CoV-Contact Cohort, Amsterdam UMC Covid-19, Biobank, COVID Human Genetic Effort, NIAID-USUHS, TAGC COVID Immunity Group, Universitat Rovira i Virgili, and Zhang Q, Bastard P, Liu Z, Le Pen J, Moncada-Velez M, Chen J, Ogishi M, Sabli IKD, Hodeib S, Korol C, Rosain J, Bilguvar K, Ye J, Bolze A, Bigio B, Yang R, Arias AA, Zhou Q, Zhang Y, Onodi F, Korniotis S, Karpf L, Philippot Q, Chbihi M, Bonnet-Madin L, Dorgham K, Smith N, Schneider WM, Razooky BS, Hoffmann HH, Michailidis E, Moens L, Han JE, Lorenzo L, Bizien L, Meade P, Neehus AL, Ugurbil AC, Corneau A, Kerner G, Zhang P, Rapaport F, Seeleuthner Y, Manry J, Masson C, Schmitt Y, Schlüter A, Le Voyer T, Khan T, Li J, Fellay J, Roussel L, Shahrooei M, Alosaimi MF, Mansouri D, Al-Saud H, Al-Mulla F, Almourfi F, Al-Muhsen SZ, Alsohime F, Al Turki S, Hasanato R, van de Beek D, Biondi A, Bettini LR, D'Angio M, Bonfanti P, Imberti L, Sottini A, Paghera S, Quiros-Roldan E, Rossi C, Oler AJ, Tompkins MF, Alba C, Vandernoot I, Goffard JC, Smits G, Migeotte I, Haerynck F, Soler-Palacin P, Martin-Nalda A, Colobran R, Morange PE, Keles S, Çölkesen F, Ozcelik T, Yasar KK, Senoglu S, Karabela ?N, Gallego CR, Novelli G, Hraiech S, Tandjaoui-Lambiotte Y, Duval X, Laouénan C,, Snow AL, Dalgard CL, Milner J, Vinh DC, Mogensen TH, Marr N, Spaan AN, Boisson B, Boisson-Dupuis S, Bustamante J, Puel A, Ciancanelli M, Meyts I, Maniatis T, Soumelis V, Amara A, Nussenzweig M, García-Sastre A, Krammer F, Pujol A, Duffy D, Lifton R, Zhang SY, Gorochov G, Béziat V, Jouanguy E, Sancho-Shimizu V, Rice CM, Abel L, Notarangelo LD, Cobat A, Su HC, Casanova JL COVID-STORM Clinicians, COVID Clinicians, Imagine COVID Group, French COVID Cohort Study Group, CoV-Contact Cohort, Amsterdam UMC Covid-19, Biobank, COVID Human Genetic Effort, NIAID-USUHS, TAGC COVID Immunity Group

Abstract

Clinical outcome upon infection with SARS-CoV-2 ranges from silent infection to lethal COVID-19. We have found an enrichment in rare variants predicted to be loss-of-function (LOF) at the 13 human loci known to govern TLR3- and IRF7-dependent type I interferon (IFN) immunity to influenza virus, in 659 patients with life-threatening COVID-19 pneumonia, relative to 534 subjects with asymptomatic or benign infection. By testing these and other rare variants at these 13 loci, we experimentally define LOF variants in 23 patients (3.5%), aged 17 to 77 years, underlying autosomal recessive or dominant deficiencies. We show that human fibroblasts with mutations affecting this pathway are vulnerable to SARS-CoV-2. Inborn errors of TLR3- and IRF7-dependent type I IFN immunity can underlie life-threatening COVID-19 pneumonia in patients with no prior severe infection.Copyright © 2020, American Association for the Advancement of Science.

Published
2020

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