Lack of association between classical HLA genes and asymptomatic SARS-CoV-2 infection

NIAID-USUHS COVID Study Group; COVID Human Genetic Effort; COVIDeF Study Group; French COVID Cohort Study Group; CoV-Contact Cohort; COVID-STORM Clinicians; COVID Clinicians; Orchestra Working Group; Amsterdam UMC Covid-19 Biobank

doi:10.1016/j.xhgg.2024.100300

Lack of association between classical HLA genes and asymptomatic SARS-CoV-2 infection

NIAID-USUHS COVID Study Group, COVID Human Genetic Effort, COVIDeF Study Group, French COVID Cohort Study Group, CoV-Contact Cohort, COVID-STORM Clinicians, COVID Clinicians, Orchestra Working Group, Amsterdam UMC Covid-19 Biobank

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

Human genetic studies of critical COVID-19 pneumonia have revealed the essential role of type I interferon-dependent innate immunity to SARS-CoV-2 infection. Conversely, an association between the HLA-B∗15:01 allele and asymptomatic SARS-CoV-2 infection in unvaccinated individuals was recently reported, suggesting a contribution of pre-existing T cell-dependent adaptive immunity. We report a lack of association of classical HLA alleles, including HLA-B∗15:01, with pre-omicron asymptomatic SARS-CoV-2 infection in unvaccinated participants in a prospective population-based study in the United States (191 asymptomatic vs. 945 symptomatic COVID-19 cases). Moreover, we found no such association in the international COVID Human Genetic Effort cohort (206 asymptomatic vs. 574 mild or moderate COVID-19 cases and 1,625 severe or critical COVID-19 cases). Finally, in the Human Challenge Characterisation study, the three HLA-B∗15:01 individuals infected with SARS-CoV-2 developed symptoms. As with other acute primary infections studied, no classical HLA alleles favoring an asymptomatic course of SARS-CoV-2 infection were identified.

Original language	English
Article number	100300
Journal	Human Genetics and Genomics Advances
Volume	5
Issue number	3
DOIs	https://doi.org/10.1016/j.xhgg.2024.100300
State	Published - Jul 18 2024

Keywords

COVID-19
HLA
association
asymptomatic infection
population stratification

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10.1016/j.xhgg.2024.100300

Cite this

NIAID-USUHS COVID Study Group, COVID Human Genetic Effort, COVIDeF Study Group, French COVID Cohort Study Group, CoV-Contact Cohort, COVID-STORM Clinicians, COVID Clinicians, Orchestra Working Group, & Amsterdam UMC Covid-19 Biobank (2024). Lack of association between classical HLA genes and asymptomatic SARS-CoV-2 infection. Human Genetics and Genomics Advances, 5(3), Article 100300. https://doi.org/10.1016/j.xhgg.2024.100300

@article{53917196357f4ace93305e05b19f401c,

title = "Lack of association between classical HLA genes and asymptomatic SARS-CoV-2 infection",

abstract = "Human genetic studies of critical COVID-19 pneumonia have revealed the essential role of type I interferon-dependent innate immunity to SARS-CoV-2 infection. Conversely, an association between the HLA-B∗15:01 allele and asymptomatic SARS-CoV-2 infection in unvaccinated individuals was recently reported, suggesting a contribution of pre-existing T cell-dependent adaptive immunity. We report a lack of association of classical HLA alleles, including HLA-B∗15:01, with pre-omicron asymptomatic SARS-CoV-2 infection in unvaccinated participants in a prospective population-based study in the United States (191 asymptomatic vs. 945 symptomatic COVID-19 cases). Moreover, we found no such association in the international COVID Human Genetic Effort cohort (206 asymptomatic vs. 574 mild or moderate COVID-19 cases and 1,625 severe or critical COVID-19 cases). Finally, in the Human Challenge Characterisation study, the three HLA-B∗15:01 individuals infected with SARS-CoV-2 developed symptoms. As with other acute primary infections studied, no classical HLA alleles favoring an asymptomatic course of SARS-CoV-2 infection were identified.",

keywords = "COVID-19, HLA, association, asymptomatic infection, population stratification",

author = "{NIAID-USUHS COVID Study Group} and {COVID Human Genetic Effort} and {COVIDeF Study Group} and {French COVID Cohort Study Group} and {CoV-Contact Cohort} and {COVID-STORM Clinicians} and {COVID Clinicians} and {Orchestra Working Group} and {Amsterdam UMC Covid-19 Biobank} and Astrid Marchal and Cirulli, {Elizabeth T.} and Iva Neveux and Evangelos Bellos and Thwaites, {Ryan S.} and {Schiabor Barrett}, {Kelly M.} and Yu Zhang and Ivana Nemes-Bokun and Mariya Kalinova and Andrew Catchpole and Tangye, {Stuart G.} and Spaan, {Andr{\'a}s N.} and Lack, {Justin B.} and Jade Ghosn and Charles Burdet and Guy Gorochov and Florence Tubach and Pierre Hausfater and Laurent Abel and Alessandro Aiuti and Saleh Al-Muhsen and Fahd Al-Mulla and Ali Amara and Anderson, {Mark S.} and Evangelos Andreakos and Arias, {Andr{\'e}s A.} and Arkin, {Lisa M.} and Feldman, {Hagit Baris} and Paul Bastard and Alexandre Belot and Biggs, {Catherine M.} and Dusan Bogunovic and Alexandre Bolze and Anastasiia Bondarenko and Alessandro Borghesi and Bousfiha, {Ahmed A.} and Petter Brodin and Yenan Bryceson and Butte, {Manish J.} and Casanova, {Jean Laurent} and Giorgio Casari and John Christodoulou and Aur{\'e}lie Cobat and Roger Colobran and Antonio Condino-Neto and Constantinescu, {Stefan N.} and Cooper, {Megan A.} and Dalgard, {Clifton L.} and Murkesh Desai and Drolet, {Beth A.} and Xavier Duval and {El Baghdadi}, Jamila and Philippine Eloy and Sara Espinosa-Padilla and Jacques Fellay and Carlos Flores and Franco, {Jos{\'e} Luis} and Antoine Froidure and Gregersen, {Peter K.} and Bodo Grimbacher and Filomeen Haerynck and David Hagin and Rabih Halwani and Lennart Hammarstr{\"o}m and Heath, {James R.} and Hsieh, {Elena W.Y.} and Eystein Husebye and Kohsuke Imai and Yuval Itan and Emmanuelle Jouanguy and El{\.z}bieta Kaja and Timokratis Karamitros and Kai Kisand and Ku, {Cheng Lung} and Lau, {Yu Lung} and Yun Ling and Lucas, {Carrie L.} and Tom Maniatis and Davood Mansouri and L{\'a}szl{\'o} Mar{\'o}di and France Mentr{\'e} and Isabelle Meyts and Milner, {Joshua D.} and Kristina Mironska and Mogensen, {Trine H.} and Tomohiro Morio and Ng, {Lisa F.P.} and Notarangelo, {Luigi D.} and Antonio Novelli and Giuseppe Novelli and Cliona O'Farrelly and Satoshi Okada and Keisuke Okamoto and Tayfun {\"O}z{\c c}elik and Qiang Pan-Hammarstr{\"o}m and Pape, {Jean W.} and {Perez de Diego}, Rebeca and Jordi Perez-Tur and Perlin, {David S.} and Graziano Pesole and Planas, {Anna M.} and Carolina Prando and Aurora Pujol and Anne Puel and Lluis Quintana-Murci and Sathishkumar Ramaswamy and Laurent Renia and Igor Resnick and Carlos Rodr{\'i}guez-Gallego and Vanessa Sancho-Shimizu and Anna Sediva and Sepp{\"a}nen, {Mikko R.J.} and Mohammad Shahrooei and Anna Shcherbina and Ondrej Slaby and Snow, {Andrew L.} and Pere Soler-Palac{\'i}n and Vassili Soumelis and Ivan Tancevski and Tayoun, {Ahmad Abou} and Temel, {{\c S}ehime G{\"u}ls{\"u}n} and Christian Thorball and Pierre Tiberghien and Sophie Trouillet-Assant and Turvey, {Stuart E.} and Uddin, {K. M.Furkan} and Uddin, {Mohammed J.} and {van de Beek}, Diederik and Vinh, {Donald C.} and {von Bernuth}, Horst and Joost Wauters and Mayana Zatz and Pawel Zawadzki and Qian Zhang and Zhang, {Shen Ying} and Serge Bureau and Yannick Vacher and Anne Gysembergh-Houal and Lauren Demerville and Abla Benleulmi-Chaachoua and Sebastien Abad and Radhiya Abassi and Abdelrafie Abdellaoui and Abdelkrim Abdelmalek and Hendy Abdoul and Helene Abergel and Fariza Abeud and Sophie Abgrall and Noemie Abisror and Marylise Adechian and Nordine Aderdour and Admane, {Hakeem Farid} and Frederic Adnet and Sara Afritt and Helene Agostini and Claire Aguilar and Sophie Agut and Aiello, {Tommaso Francesco} and Kaci, {Marc Ait} and Oufella, {Hafid Ait} and Gokula Ajeenthiravasan and Virginie Alauzy and Fanny Alby-Laurent and Lucie Allard and Alyanakian, {Marie Alexandra} and Borrero, {Blanca Amador} and Sabrina Amam and Lucile Amrouche and Marc Andronikof and Dany Anglicheau and Nadia Anguel and Djillali Annane and Mohammed Aounzou and Caroline Aparicio and Gladys Aratus and Arlet, {Jean Benoit} and Jeremy Arzoine and Elisabeth Aslangul and Mona Assefi and Adeline Aubry and Laetitia Audiffred and Etienne Audureau and Auger, {Christelle Nathalie} and Auregan, {Jean Charles} and Celine Awotar and Milla, {Sonia Ayllon} and Delphine Azan and Laurene Azemar and Billal Azzouguen and Elrufaai, {Marwa Bachir} and A{\"i}da Badsi and Prissile Bakouboula and Coline Balcerowiak and Fanta Balde and Elodie Baldivia and Bangamingo, {Eliane Flore} and Amandine Baptiste and Fanny Baran-Marszak and Caroline Barau and Nathalie Barget",

note = "Publisher Copyright: {\textcopyright} 2024 The Author(s)",

year = "2024",

month = jul,

day = "18",

doi = "10.1016/j.xhgg.2024.100300",

language = "English",

volume = "5",

journal = "Human Genetics and Genomics Advances",

issn = "2666-2477",

number = "3",

}

NIAID-USUHS COVID Study Group, COVID Human Genetic Effort, COVIDeF Study Group, French COVID Cohort Study Group, CoV-Contact Cohort, COVID-STORM Clinicians, COVID Clinicians, Orchestra Working Group & Amsterdam UMC Covid-19 Biobank 2024, 'Lack of association between classical HLA genes and asymptomatic SARS-CoV-2 infection', Human Genetics and Genomics Advances, vol. 5, no. 3, 100300. https://doi.org/10.1016/j.xhgg.2024.100300

TY - JOUR

T1 - Lack of association between classical HLA genes and asymptomatic SARS-CoV-2 infection

AU - NIAID-USUHS COVID Study Group

AU - COVID Human Genetic Effort

AU - COVIDeF Study Group

AU - French COVID Cohort Study Group

AU - CoV-Contact Cohort

AU - COVID-STORM Clinicians

AU - COVID Clinicians

AU - Orchestra Working Group

AU - Amsterdam UMC Covid-19 Biobank

AU - Marchal, Astrid

AU - Cirulli, Elizabeth T.

AU - Neveux, Iva

AU - Bellos, Evangelos

AU - Thwaites, Ryan S.

AU - Schiabor Barrett, Kelly M.

AU - Zhang, Yu

AU - Nemes-Bokun, Ivana

AU - Kalinova, Mariya

AU - Catchpole, Andrew

AU - Tangye, Stuart G.

AU - Spaan, András N.

AU - Lack, Justin B.

AU - Ghosn, Jade

AU - Burdet, Charles

AU - Gorochov, Guy

AU - Tubach, Florence

AU - Hausfater, Pierre

AU - Abel, Laurent

AU - Aiuti, Alessandro

AU - Al-Muhsen, Saleh

AU - Al-Mulla, Fahd

AU - Amara, Ali

AU - Anderson, Mark S.

AU - Andreakos, Evangelos

AU - Arias, Andrés A.

AU - Arkin, Lisa M.

AU - Feldman, Hagit Baris

AU - Bastard, Paul

AU - Belot, Alexandre

AU - Biggs, Catherine M.

AU - Bogunovic, Dusan

AU - Bolze, Alexandre

AU - Bondarenko, Anastasiia

AU - Borghesi, Alessandro

AU - Bousfiha, Ahmed A.

AU - Brodin, Petter

AU - Bryceson, Yenan

AU - Butte, Manish J.

AU - Casanova, Jean Laurent

AU - Casari, Giorgio

AU - Christodoulou, John

AU - Cobat, Aurélie

AU - Colobran, Roger

AU - Condino-Neto, Antonio

AU - Constantinescu, Stefan N.

AU - Cooper, Megan A.

AU - Dalgard, Clifton L.

AU - Desai, Murkesh

AU - Drolet, Beth A.

AU - Duval, Xavier

AU - El Baghdadi, Jamila

AU - Eloy, Philippine

AU - Espinosa-Padilla, Sara

AU - Fellay, Jacques

AU - Flores, Carlos

AU - Franco, José Luis

AU - Froidure, Antoine

AU - Gregersen, Peter K.

AU - Grimbacher, Bodo

AU - Haerynck, Filomeen

AU - Hagin, David

AU - Halwani, Rabih

AU - Hammarström, Lennart

AU - Heath, James R.

AU - Hsieh, Elena W.Y.

AU - Husebye, Eystein

AU - Imai, Kohsuke

AU - Itan, Yuval

AU - Jouanguy, Emmanuelle

AU - Kaja, Elżbieta

AU - Karamitros, Timokratis

AU - Kisand, Kai

AU - Ku, Cheng Lung

AU - Lau, Yu Lung

AU - Ling, Yun

AU - Lucas, Carrie L.

AU - Maniatis, Tom

AU - Mansouri, Davood

AU - Maródi, László

AU - Mentré, France

AU - Meyts, Isabelle

AU - Milner, Joshua D.

AU - Mironska, Kristina

AU - Mogensen, Trine H.

AU - Morio, Tomohiro

AU - Ng, Lisa F.P.

AU - Notarangelo, Luigi D.

AU - Novelli, Antonio

AU - Novelli, Giuseppe

AU - O'Farrelly, Cliona

AU - Okada, Satoshi

AU - Okamoto, Keisuke

AU - Özçelik, Tayfun

AU - Pan-Hammarström, Qiang

AU - Pape, Jean W.

AU - Perez de Diego, Rebeca

AU - Perez-Tur, Jordi

AU - Perlin, David S.

AU - Pesole, Graziano

AU - Planas, Anna M.

AU - Prando, Carolina

AU - Pujol, Aurora

AU - Puel, Anne

AU - Quintana-Murci, Lluis

AU - Ramaswamy, Sathishkumar

AU - Renia, Laurent

AU - Resnick, Igor

AU - Rodríguez-Gallego, Carlos

AU - Sancho-Shimizu, Vanessa

AU - Sediva, Anna

AU - Seppänen, Mikko R.J.

AU - Shahrooei, Mohammad

AU - Shcherbina, Anna

AU - Slaby, Ondrej

AU - Snow, Andrew L.

AU - Soler-Palacín, Pere

AU - Soumelis, Vassili

AU - Tancevski, Ivan

AU - Tayoun, Ahmad Abou

AU - Temel, Şehime Gülsün

AU - Thorball, Christian

AU - Tiberghien, Pierre

AU - Trouillet-Assant, Sophie

AU - Turvey, Stuart E.

AU - Uddin, K. M.Furkan

AU - Uddin, Mohammed J.

AU - van de Beek, Diederik

AU - Vinh, Donald C.

AU - von Bernuth, Horst

AU - Wauters, Joost

AU - Zatz, Mayana

AU - Zawadzki, Pawel

AU - Zhang, Qian

AU - Zhang, Shen Ying

AU - Bureau, Serge

AU - Vacher, Yannick

AU - Gysembergh-Houal, Anne

AU - Demerville, Lauren

AU - Benleulmi-Chaachoua, Abla

AU - Abad, Sebastien

AU - Abassi, Radhiya

AU - Abdellaoui, Abdelrafie

AU - Abdelmalek, Abdelkrim

AU - Abdoul, Hendy

AU - Abergel, Helene

AU - Abeud, Fariza

AU - Abgrall, Sophie

AU - Abisror, Noemie

AU - Adechian, Marylise

AU - Aderdour, Nordine

AU - Admane, Hakeem Farid

AU - Adnet, Frederic

AU - Afritt, Sara

AU - Agostini, Helene

AU - Aguilar, Claire

AU - Agut, Sophie

AU - Aiello, Tommaso Francesco

AU - Kaci, Marc Ait

AU - Oufella, Hafid Ait

AU - Ajeenthiravasan, Gokula

AU - Alauzy, Virginie

AU - Alby-Laurent, Fanny

AU - Allard, Lucie

AU - Alyanakian, Marie Alexandra

AU - Borrero, Blanca Amador

AU - Amam, Sabrina

AU - Amrouche, Lucile

AU - Andronikof, Marc

AU - Anglicheau, Dany

AU - Anguel, Nadia

AU - Annane, Djillali

AU - Aounzou, Mohammed

AU - Aparicio, Caroline

AU - Aratus, Gladys

AU - Arlet, Jean Benoit

AU - Arzoine, Jeremy

AU - Aslangul, Elisabeth

AU - Assefi, Mona

AU - Aubry, Adeline

AU - Audiffred, Laetitia

AU - Audureau, Etienne

AU - Auger, Christelle Nathalie

AU - Auregan, Jean Charles

AU - Awotar, Celine

AU - Milla, Sonia Ayllon

AU - Azan, Delphine

AU - Azemar, Laurene

AU - Azzouguen, Billal

AU - Elrufaai, Marwa Bachir

AU - Badsi, Aïda

AU - Bakouboula, Prissile

AU - Balcerowiak, Coline

AU - Balde, Fanta

AU - Baldivia, Elodie

AU - Bangamingo, Eliane Flore

AU - Baptiste, Amandine

AU - Baran-Marszak, Fanny

AU - Barau, Caroline

AU - Barget, Nathalie

PY - 2024/7/18

Y1 - 2024/7/18

N2 - Human genetic studies of critical COVID-19 pneumonia have revealed the essential role of type I interferon-dependent innate immunity to SARS-CoV-2 infection. Conversely, an association between the HLA-B∗15:01 allele and asymptomatic SARS-CoV-2 infection in unvaccinated individuals was recently reported, suggesting a contribution of pre-existing T cell-dependent adaptive immunity. We report a lack of association of classical HLA alleles, including HLA-B∗15:01, with pre-omicron asymptomatic SARS-CoV-2 infection in unvaccinated participants in a prospective population-based study in the United States (191 asymptomatic vs. 945 symptomatic COVID-19 cases). Moreover, we found no such association in the international COVID Human Genetic Effort cohort (206 asymptomatic vs. 574 mild or moderate COVID-19 cases and 1,625 severe or critical COVID-19 cases). Finally, in the Human Challenge Characterisation study, the three HLA-B∗15:01 individuals infected with SARS-CoV-2 developed symptoms. As with other acute primary infections studied, no classical HLA alleles favoring an asymptomatic course of SARS-CoV-2 infection were identified.

AB - Human genetic studies of critical COVID-19 pneumonia have revealed the essential role of type I interferon-dependent innate immunity to SARS-CoV-2 infection. Conversely, an association between the HLA-B∗15:01 allele and asymptomatic SARS-CoV-2 infection in unvaccinated individuals was recently reported, suggesting a contribution of pre-existing T cell-dependent adaptive immunity. We report a lack of association of classical HLA alleles, including HLA-B∗15:01, with pre-omicron asymptomatic SARS-CoV-2 infection in unvaccinated participants in a prospective population-based study in the United States (191 asymptomatic vs. 945 symptomatic COVID-19 cases). Moreover, we found no such association in the international COVID Human Genetic Effort cohort (206 asymptomatic vs. 574 mild or moderate COVID-19 cases and 1,625 severe or critical COVID-19 cases). Finally, in the Human Challenge Characterisation study, the three HLA-B∗15:01 individuals infected with SARS-CoV-2 developed symptoms. As with other acute primary infections studied, no classical HLA alleles favoring an asymptomatic course of SARS-CoV-2 infection were identified.

KW - COVID-19

KW - HLA

KW - association

KW - asymptomatic infection

KW - population stratification

UR - http://www.scopus.com/inward/record.url?scp=85195515679&partnerID=8YFLogxK

U2 - 10.1016/j.xhgg.2024.100300

DO - 10.1016/j.xhgg.2024.100300

M3 - Article

C2 - 38678364

AN - SCOPUS:85195515679

SN - 2666-2477

VL - 5

JO - Human Genetics and Genomics Advances

JF - Human Genetics and Genomics Advances

IS - 3

M1 - 100300

ER -

Lack of association between classical HLA genes and asymptomatic SARS-CoV-2 infection

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