BIK polymorphism and proteasome regulation unveil host risk factor for severe influenza

S Sourabh Soni (Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center) S Soner Yildiz (Department of Microbiology, Icahn School of Medicine at Mount Sinai) E Emma Kaitlynn Allen (Department of Immunology, St. Jude Children’s Research Hospital) H Hans Petersen (Chronic Obstructive Pulmonary Disease Program, Lovelace Respiratory Research Institute) M Mark Peeples (Center for Vaccines and Immunity, Abigail Wexner Research Institute at Nationwide Children’s Hospital) S Sara El Zahed (Department of Microbiology, Icahn School of Medicine at Mount Sinai) L Lorena Rosas (Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center) V Vandana Anang (Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center) L Laura Antonescu (Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center) R Richard Seonghun Nho (Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center) A Ana Lucia Mora (Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center) J Jeffrey Craig Horowitz (Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center) M Mauricio Rojas (Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center) R Rafael Andrés Medina (Pathology Advanced Translational Research Unit, Department of Pathology and Laboratory Medicine Emory Vaccine Center, Emory University School of Medicine) P Paul Glyndwr Thomas (Department of Immunology, St. Jude Children’s Research Hospital) A Adolfo García-Sastre Y Yohannes Tesfaigzi (Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School) Y Yohannes Afework Mebratu (Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center)

Abstract

Influenza A viruses (IAVs) pose a significant public health threat, with host factors playing a crucial role in disease severity. We investigated the role of Bcl-2-interacting killer (BIK) in IAV infection using cellular and mouse models, and influenza-infected human cohort. In airway epithelial cells (AECs), BIK deficiency impaired viral replication, while BIK restoration enhanced it. Conversely, airway-specific BIK overexpression in mice increased viral load, inflammation, and mortality, whereas BIK suppression conferred protection. Critically, a genetic variation (rs738276) in the BIK gene, influencing BIK expression, correlates with altered viral replication in air–liquid interface differentiated primary normal human bronchial epithelial cells and influenza severity in humans. Mechanistically, we demonstrate that IAV nucleoprotein (NP) suppresses β5, a subunit of the proteasome, leading to increased BIK levels and enhanced viral replication. Conversely, β5 treatment dampened BIK levels and protected mice from IAV-induced morbidity and mortality. Furthermore, BIK interacts with NP, disrupting the Bcl-2/NP interaction and promoting viral replication. Our findings uncover an IAV–BIK–β5 axis that governs viral replication, suggesting that targeting BIK or β5 may offer therapeutic strategies against influenza.

Article Details

Volume / Issue Vol. 122, Issue 28
Published July 15, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (18)

S

Sourabh Soni

Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center

S

Soner Yildiz

Department of Microbiology, Icahn School of Medicine at Mount Sinai

E

Emma Kaitlynn Allen

Department of Immunology, St. Jude Children’s Research Hospital

H

Hans Petersen

Chronic Obstructive Pulmonary Disease Program, Lovelace Respiratory Research Institute

M

Mark Peeples

Center for Vaccines and Immunity, Abigail Wexner Research Institute at Nationwide Children’s Hospital

S

Sara El Zahed

Department of Microbiology, Icahn School of Medicine at Mount Sinai

L

Lorena Rosas

Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center

V

Vandana Anang

Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center

L

Laura Antonescu

Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center

R

Richard Seonghun Nho

Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center

A

Ana Lucia Mora

Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center

J

Jeffrey Craig Horowitz

Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center

M

Mauricio Rojas

Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center

R

Rafael Andrés Medina

Pathology Advanced Translational Research Unit, Department of Pathology and Laboratory Medicine Emory Vaccine Center, Emory University School of Medicine

P

Paul Glyndwr Thomas

Department of Immunology, St. Jude Children’s Research Hospital

A

Adolfo García-Sastre

Y

Yohannes Tesfaigzi

Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School

Y

Yohannes Afework Mebratu

Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center