Auto-antibodies to type I IFNs can underlie adverse reactions to yellow fever live attenuated vaccine

Paul Bastard; Eleftherios Michailidis; Hans-Heinrich Hoffmann; Marwa Chbihi; Tom Le Voyer; Jeremie Rosain; Quentin Philippot; Yoann Seeleuthner; Adrian Gervais; Marie Materna; Patricia Mouta Nunes de Oliveira; Maria de Lourdes S. Maia; Ana Paula Dinis Ano Bom; Tamiris Azamor; Deborah Araujo da Conceicao; Ekaterini Goudouris; Akira Homma; Gunther Slesak; Johannes Schaefer; Bali Pulendran; Joseph D. Miller; Ralph Huits; Rui Yang; Lindsey B. Rosen; Lucy Bizien; Lazaro Lorenzo; Maya Chrabieh; Lucia Erazo; Flore Rozenberg; Mohamed Maxime Jeljeli; Vivien Beziat; Steven M. Holland; Aurelie Cobat; Luigi D. Notarangelo; Helen C. Su; Rafi Ahmed; Anne Puel; Shen-Ying Zhang; Laurent Abel; Stephen J. Seligman; Qian Zhang; Margaret R. MacDonald; Emmanuelle Jouanguy; Charles M. Rice; Jean-Laurent Casanova

doi:10.1084/jem.20202486

Auto-antibodies to type I IFNs can underlie adverse reactions to yellow fever live attenuated vaccine

Paul Bastard, Eleftherios Michailidis, Hans-Heinrich Hoffmann, Marwa Chbihi, Tom Le Voyer, Jeremie Rosain, Quentin Philippot, Yoann Seeleuthner, Adrian Gervais, Marie Materna, Patricia Mouta Nunes de Oliveira, Maria de Lourdes S. Maia, Ana Paula Dinis Ano Bom, Tamiris Azamor, Deborah Araujo da Conceicao, Ekaterini Goudouris, Akira Homma, Gunther Slesak, Johannes Schaefer, Bali PulendranJoseph D. Miller, Ralph Huits, Rui Yang, Lindsey B. Rosen, Lucy Bizien, Lazaro Lorenzo, Maya Chrabieh, Lucia Erazo, Flore Rozenberg, Mohamed Maxime Jeljeli, Vivien Beziat, Steven M. Holland, Aurelie Cobat, Luigi D. Notarangelo, Helen C. Su, Rafi Ahmed, Anne Puel, Shen-Ying Zhang, Laurent Abel, Stephen J. Seligman, Qian Zhang, Margaret R. MacDonald, Emmanuelle Jouanguy, Charles M. Rice, Jean-Laurent Casanova

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Abstract

Yellow fever virus (YFV) live attenuated vaccine can, in rare cases, cause life-threatening disease, typically in patients with no previous history of severe viral illness. Autosomal recessive (AR) complete IFNAR1 deficiency was reported in one 12-yr-old patient. Here, we studied seven other previously healthy patients aged 13 to 80 yr with unexplained life-threatening YFV vaccine-associated disease. One 13-yr-old patient had AR complete IFNAR2 deficiency. Three other patients vaccinated at the ages of 47, 57, and 64 yr had high titers of circulating auto-Abs against at least 14 of the 17 individual type I IFNs. These antibodies were recently shown to underlie at least 10% of cases of life-threatening COVID-19 pneumonia. The auto-Abs were neutralizing in vitro, blocking the protective effect of IFN-α2 against YFV vaccine strains. AR IFNAR1 or IFNAR2 deficiency and neutralizing auto-Abs against type I IFNs thus accounted for more than half the cases of life-threatening YFV vaccine-associated disease studied here. Previously healthy subjects could be tested for both predispositions before anti-YFV vaccination.

Original language	English
Article number	e20202486
Journal	Journal of Experimental Medicine
Volume	218
Issue number	4
Number of pages	16
DOIs	https://doi.org/10.1084/jem.20202486
Publication status	Published - 2021

Keywords

Adolescent
Adult
Aged
Antibodies, Neutralizing/immunology
Autoantibodies/immunology
Autoimmune Diseases/genetics
COVID-19/genetics
Female
Genetic Diseases, Inborn/genetics
HEK293 Cells
Humans
Interferon-alpha/genetics
Male
Middle Aged
Receptor, Interferon alpha-beta/deficiency
SARS-CoV-2/genetics
Vaccines, Attenuated/genetics
Yellow Fever Vaccine/adverse effects
Yellow fever virus/genetics

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2021jemee20202486Final published version, 3.08 MBLicence: CC BY-NC-SA

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Bastard, P., Michailidis, E., Hoffmann, H.-H., Chbihi, M., Le Voyer, T., Rosain, J., Philippot, Q., Seeleuthner, Y., Gervais, A., Materna, M., Nunes de Oliveira, P. M., Maia, M. D. L. S., Ano Bom, A. P. D., Azamor, T., da Conceicao, D. A., Goudouris, E., Homma, A., Slesak, G., Schaefer, J., ... Casanova, J.-L. (2021). Auto-antibodies to type I IFNs can underlie adverse reactions to yellow fever live attenuated vaccine. Journal of Experimental Medicine, 218(4), Article e20202486. https://doi.org/10.1084/jem.20202486

@article{8a36a32d045146f7931f107cf7f38428,

title = "Auto-antibodies to type I IFNs can underlie adverse reactions to yellow fever live attenuated vaccine",

abstract = "Yellow fever virus (YFV) live attenuated vaccine can, in rare cases, cause life-threatening disease, typically in patients with no previous history of severe viral illness. Autosomal recessive (AR) complete IFNAR1 deficiency was reported in one 12-yr-old patient. Here, we studied seven other previously healthy patients aged 13 to 80 yr with unexplained life-threatening YFV vaccine-associated disease. One 13-yr-old patient had AR complete IFNAR2 deficiency. Three other patients vaccinated at the ages of 47, 57, and 64 yr had high titers of circulating auto-Abs against at least 14 of the 17 individual type I IFNs. These antibodies were recently shown to underlie at least 10% of cases of life-threatening COVID-19 pneumonia. The auto-Abs were neutralizing in vitro, blocking the protective effect of IFN-α2 against YFV vaccine strains. AR IFNAR1 or IFNAR2 deficiency and neutralizing auto-Abs against type I IFNs thus accounted for more than half the cases of life-threatening YFV vaccine-associated disease studied here. Previously healthy subjects could be tested for both predispositions before anti-YFV vaccination.",

keywords = "Adolescent, Adult, Aged, Antibodies, Neutralizing/immunology, Autoantibodies/immunology, Autoimmune Diseases/genetics, COVID-19/genetics, Female, Genetic Diseases, Inborn/genetics, HEK293 Cells, Humans, Interferon-alpha/genetics, Male, Middle Aged, Receptor, Interferon alpha-beta/deficiency, SARS-CoV-2/genetics, Vaccines, Attenuated/genetics, Yellow Fever Vaccine/adverse effects, Yellow fever virus/genetics",

author = "Paul Bastard and Eleftherios Michailidis and Hans-Heinrich Hoffmann and Marwa Chbihi and {Le Voyer}, Tom and Jeremie Rosain and Quentin Philippot and Yoann Seeleuthner and Adrian Gervais and Marie Materna and {Nunes de Oliveira}, {Patricia Mouta} and Maia, {Maria de Lourdes S.} and {Ano Bom}, {Ana Paula Dinis} and Tamiris Azamor and {da Conceicao}, {Deborah Araujo} and Ekaterini Goudouris and Akira Homma and Gunther Slesak and Johannes Schaefer and Bali Pulendran and Miller, {Joseph D.} and Ralph Huits and Rui Yang and Rosen, {Lindsey B.} and Lucy Bizien and Lazaro Lorenzo and Maya Chrabieh and Lucia Erazo and Flore Rozenberg and Jeljeli, {Mohamed Maxime} and Vivien Beziat and Holland, {Steven M.} and Aurelie Cobat and Notarangelo, {Luigi D.} and Su, {Helen C.} and Rafi Ahmed and Anne Puel and Shen-Ying Zhang and Laurent Abel and Seligman, {Stephen J.} and Qian Zhang and MacDonald, {Margaret R.} and Emmanuelle Jouanguy and Rice, {Charles M.} and Jean-Laurent Casanova",

note = "FTX; OGOA; (CC BY-NC-SA 4.0)",

year = "2021",

doi = "10.1084/jem.20202486",

language = "English",

volume = "218",

journal = "Journal of Experimental Medicine",

publisher = "Rockefeller University Press",

number = "4",

}

Bastard, P, Michailidis, E, Hoffmann, H-H, Chbihi, M, Le Voyer, T, Rosain, J, Philippot, Q, Seeleuthner, Y, Gervais, A, Materna, M, Nunes de Oliveira, PM, Maia, MDLS, Ano Bom, APD, Azamor, T, da Conceicao, DA, Goudouris, E, Homma, A, Slesak, G, Schaefer, J, Pulendran, B, Miller, JD, Huits, R, Yang, R, Rosen, LB, Bizien, L, Lorenzo, L, Chrabieh, M, Erazo, L, Rozenberg, F, Jeljeli, MM, Beziat, V, Holland, SM, Cobat, A, Notarangelo, LD, Su, HC, Ahmed, R, Puel, A, Zhang, S-Y, Abel, L, Seligman, SJ, Zhang, Q, MacDonald, MR, Jouanguy, E, Rice, CM & Casanova, J-L 2021, 'Auto-antibodies to type I IFNs can underlie adverse reactions to yellow fever live attenuated vaccine', Journal of Experimental Medicine, vol. 218, no. 4, e20202486. https://doi.org/10.1084/jem.20202486

TY - JOUR

T1 - Auto-antibodies to type I IFNs can underlie adverse reactions to yellow fever live attenuated vaccine

AU - Bastard, Paul

AU - Michailidis, Eleftherios

AU - Hoffmann, Hans-Heinrich

AU - Chbihi, Marwa

AU - Le Voyer, Tom

AU - Rosain, Jeremie

AU - Philippot, Quentin

AU - Seeleuthner, Yoann

AU - Gervais, Adrian

AU - Materna, Marie

AU - Nunes de Oliveira, Patricia Mouta

AU - Maia, Maria de Lourdes S.

AU - Ano Bom, Ana Paula Dinis

AU - Azamor, Tamiris

AU - da Conceicao, Deborah Araujo

AU - Goudouris, Ekaterini

AU - Homma, Akira

AU - Slesak, Gunther

AU - Schaefer, Johannes

AU - Pulendran, Bali

AU - Miller, Joseph D.

AU - Huits, Ralph

AU - Yang, Rui

AU - Rosen, Lindsey B.

AU - Bizien, Lucy

AU - Lorenzo, Lazaro

AU - Chrabieh, Maya

AU - Erazo, Lucia

AU - Rozenberg, Flore

AU - Jeljeli, Mohamed Maxime

AU - Beziat, Vivien

AU - Holland, Steven M.

AU - Cobat, Aurelie

AU - Notarangelo, Luigi D.

AU - Su, Helen C.

AU - Ahmed, Rafi

AU - Puel, Anne

AU - Zhang, Shen-Ying

AU - Abel, Laurent

AU - Seligman, Stephen J.

AU - Zhang, Qian

AU - MacDonald, Margaret R.

AU - Jouanguy, Emmanuelle

AU - Rice, Charles M.

AU - Casanova, Jean-Laurent

N1 - FTX; OGOA; (CC BY-NC-SA 4.0)

PY - 2021

Y1 - 2021

N2 - Yellow fever virus (YFV) live attenuated vaccine can, in rare cases, cause life-threatening disease, typically in patients with no previous history of severe viral illness. Autosomal recessive (AR) complete IFNAR1 deficiency was reported in one 12-yr-old patient. Here, we studied seven other previously healthy patients aged 13 to 80 yr with unexplained life-threatening YFV vaccine-associated disease. One 13-yr-old patient had AR complete IFNAR2 deficiency. Three other patients vaccinated at the ages of 47, 57, and 64 yr had high titers of circulating auto-Abs against at least 14 of the 17 individual type I IFNs. These antibodies were recently shown to underlie at least 10% of cases of life-threatening COVID-19 pneumonia. The auto-Abs were neutralizing in vitro, blocking the protective effect of IFN-α2 against YFV vaccine strains. AR IFNAR1 or IFNAR2 deficiency and neutralizing auto-Abs against type I IFNs thus accounted for more than half the cases of life-threatening YFV vaccine-associated disease studied here. Previously healthy subjects could be tested for both predispositions before anti-YFV vaccination.

AB - Yellow fever virus (YFV) live attenuated vaccine can, in rare cases, cause life-threatening disease, typically in patients with no previous history of severe viral illness. Autosomal recessive (AR) complete IFNAR1 deficiency was reported in one 12-yr-old patient. Here, we studied seven other previously healthy patients aged 13 to 80 yr with unexplained life-threatening YFV vaccine-associated disease. One 13-yr-old patient had AR complete IFNAR2 deficiency. Three other patients vaccinated at the ages of 47, 57, and 64 yr had high titers of circulating auto-Abs against at least 14 of the 17 individual type I IFNs. These antibodies were recently shown to underlie at least 10% of cases of life-threatening COVID-19 pneumonia. The auto-Abs were neutralizing in vitro, blocking the protective effect of IFN-α2 against YFV vaccine strains. AR IFNAR1 or IFNAR2 deficiency and neutralizing auto-Abs against type I IFNs thus accounted for more than half the cases of life-threatening YFV vaccine-associated disease studied here. Previously healthy subjects could be tested for both predispositions before anti-YFV vaccination.

KW - Adolescent

KW - Adult

KW - Aged

KW - Antibodies, Neutralizing/immunology

KW - Autoantibodies/immunology

KW - Autoimmune Diseases/genetics

KW - COVID-19/genetics

KW - Female

KW - Genetic Diseases, Inborn/genetics

KW - HEK293 Cells

KW - Humans

KW - Interferon-alpha/genetics

KW - Male

KW - Middle Aged

KW - Receptor, Interferon alpha-beta/deficiency

KW - SARS-CoV-2/genetics

KW - Vaccines, Attenuated/genetics

KW - Yellow Fever Vaccine/adverse effects

KW - Yellow fever virus/genetics

U2 - 10.1084/jem.20202486

DO - 10.1084/jem.20202486

M3 - A1: Web of Science-article

C2 - 33544838

VL - 218

JO - Journal of Experimental Medicine

JF - Journal of Experimental Medicine

IS - 4

M1 - e20202486

ER -

Auto-antibodies to type I IFNs can underlie adverse reactions to yellow fever live attenuated vaccine

Abstract

Keywords

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