Deficiency in platelet 12-lipoxygenase exacerbates inflammation and disease severity during SARS-CoV-2 infection

A Ana Claudia dos S. P. Andrade (Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) E Emile Lacasse (Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) I Isabelle Dubuc (Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) L Leslie Gudimard (Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) A Annie Gravel (Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) F Florian Puhm (Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) G Gabriel Campolina-Silva (Division of Reproduction, mother and youth health, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) C Celso Queiroz-Junior (Morphology Department, Universidade Federal de Minas Gerais) I Isabelle Allaeys (Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) J Julien Prunier (Division of Endocrinology and Nephrology, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) O Oumaima Azeggouar Wallen (Centre de recherche de l’Institut Universitaire de cardiologie et pneumologie de Québec, Division of pneumology, Faculty of medicine, Université Laval) Élizabeth Dumais (Centre de recherche de l’Institut Universitaire de cardiologie et pneumologie de Québec, Division of pneumology, Faculty of medicine, Université Laval) C Clémence Belleannée (Division of Reproduction, mother and youth health, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) A Arnaud Droit N Nicolas Flamand (Centre de recherche de l’Institut Universitaire de cardiologie et pneumologie de Québec, Division of pneumology, Faculty of medicine, Université Laval) Éric Boilard (Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval) L Louis Flamand (Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval)

Abstract

Platelets, known for maintaining blood balance, also participate in antimicrobial defense. Upon severeacute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection, platelets become hyperactivated, releasing molecules such as cytokines, granule contents, and bioactive lipids. The key effector biolipids produced by platelets include 12-hydroxyeicosatetraenoic acid (12-HETE) and 12-hydroxyeicosatrienoic acid (12-HETrE), produced by 12-lipoxygenase (12-LOX), and prostaglandins and thromboxane, produced by cyclooxygenase-1. While prostaglandin E2 and thromboxane B2 were previously associated with lung inflammation in severe COVID-19, the role of platelet 12-LOX in SARS-CoV-2 infection remains unclear. Using mice deficient for platelets’ 12-LOX, we report that SARS-CoV-2 infection resulted in higher lung inflammation characterized by histopathological tissue analysis, increased leukocyte infiltrates, and cytokine production relative to wild-type mice. In addition, distinct platelet and lung transcriptomic changes, including alterations in NOD-like receptor (NLR) family pyrin domain-containing 1 (NLRP1) inflammasome-related gene expression, were observed. Mass spectrometry lipidomic analysis in 12-LOX-deficient-infected mice revealed significant changes in bioactive lipid content, including reduced levels of 12-HETrE that inversely correlated with disease severity. Finally, platelet 12-LOX deficiency was associated with increased morbidity and lower survival rates relative to wild type (WT) mice. Overall, this study highlights the complex interplay between 12-LOX-related lipid metabolism and inflammatory responses during SARS-CoV-2 infection. The findings provide valuable insights into potential therapeutic targets aimed at mitigating severe outcomes, emphasizing the pivotal role of platelet enzymes in the host response to viral infections.

Article Details

Volume / Issue Vol. 122, Issue 12
Published March 25, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (17)

A

Ana Claudia dos S. P. Andrade

Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

E

Emile Lacasse

Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

I

Isabelle Dubuc

Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

L

Leslie Gudimard

Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

A

Annie Gravel

Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

F

Florian Puhm

Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

G

Gabriel Campolina-Silva

Division of Reproduction, mother and youth health, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

C

Celso Queiroz-Junior

Morphology Department, Universidade Federal de Minas Gerais

I

Isabelle Allaeys

Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

J

Julien Prunier

Division of Endocrinology and Nephrology, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

O

Oumaima Azeggouar Wallen

Centre de recherche de l’Institut Universitaire de cardiologie et pneumologie de Québec, Division of pneumology, Faculty of medicine, Université Laval

Élizabeth Dumais

Centre de recherche de l’Institut Universitaire de cardiologie et pneumologie de Québec, Division of pneumology, Faculty of medicine, Université Laval

C

Clémence Belleannée

Division of Reproduction, mother and youth health, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

A

Arnaud Droit

N

Nicolas Flamand

Centre de recherche de l’Institut Universitaire de cardiologie et pneumologie de Québec, Division of pneumology, Faculty of medicine, Université Laval

Éric Boilard

Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval

L

Louis Flamand

Division of Infectious and Immune Diseases, Centre de Recherche du Centre Hospitalier Universitaire de Québec-Université Laval