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1. Serum Interleukin-26 Is a New Biomarker for Disease Activity Assessment in Systemic Lupus Erythematosus

Author

Benoit Brilland, Maxime Bach-Bunner, Christopher Nunes Gomes, Vincent Larochette, Etienne Foucher, Marc Plaisance, Patrick Saulnier, Nathalie Costedoat-Chalumeau, Pascale Ghillani, Cristina Belizna, Yves Delneste, Jean-François Augusto, and Pascale Jeannin

Subjects
IL-26, SLEDAI, Proteinuria, anti-DNA antibodies, complement consumption, systemic lupus erythematosus, Immunologic diseases. Allergy, RC581-607
Abstract

ObjectiveInterleukin-26 (IL-26) has a unique ability to activate innate immune cells due to its binding to circulating double-stranded DNA. High levels of IL-26 have been reported in patients with chronic inflammation. We aimed to investigate IL-26 levels in patients with systemic lupus erythematosus (SLE).MethodsIL-26 serum levels were quantified by ELISA for 47 healthy controls and 109 SLE patients previously enrolled in the PLUS study. Performance of IL-26 levels and classical markers (autoantibodies or complement consumption) to identify an active SLE disease (SLE disease activity index (SLEDAI) score > 4) were compared.ResultsIL-26 levels were significantly higher in SLE patients than in controls (4.04 ± 11.66 and 0.74 ± 2.02 ng/mL; p = 0.005). IL-26 levels were also significantly higher in patients with active disease than those with inactive disease (33.08 ± 21.06 vs 1.10 ± 3.80 ng/mL, p < 0.0001). IL-26 levels correlated with SLEDAI score and the urine protein to creatinine ratio (uPCR) (p < 0.001). Patients with high IL-26 levels had higher SLEDAI score, anti-DNA antibodies levels, and uPCR (p < 0.05). They presented more frequently with C3 or C4 complement consumption. Lastly, IL-26 showed stronger performance than classical markers (complement consumption or autoantibodies) for active disease identification.ConclusionsOur results suggest that, in addition to classical SLE serological markers, the measurement of IL-26 levels may be a useful biomarker for active disease identification in SLE patients.

Published
2021
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2. IL-26, a Cytokine With Roles in Extracellular DNA-Induced Inflammation and Microbial Defense

Author

Vincent Larochette, Charline Miot, Caroline Poli, Elodie Beaumont, Philippe Roingeard, Helmut Fickenscher, Pascale Jeannin, and Yves Delneste

Subjects
IL-26, inflammation, kinocidin, soluble PRM, DNA carrier, Immunologic diseases. Allergy, RC581-607
Abstract

Interleukin 26 (IL-26) is the most recently identified member of the IL-20 cytokine subfamily, and is a novel mediator of inflammation overexpressed in activated or transformed T cells. Novel properties have recently been assigned to IL-26, owing to its non-conventional cationic, and amphipathic features. IL-26 binds to DNA released from damaged cells and, as a carrier molecule for extracellular DNA, links DNA to inflammation. This observation suggests that IL-26 may act both as a driver and an effector of inflammation, leading to the establishment of a deleterious amplification loop and, ultimately, sustained inflammation. Thus, IL-26 emerges as an important mediator in local immunity/inflammation. The dysregulated expression and extracellular DNA carrier capacity of IL-26 may have profound consequences for the chronicity of inflammation. IL-26 also exhibits direct antimicrobial properties. This review summarizes recent advances on the biology of IL-26 and discusses its roles as a novel kinocidin.

Published
2019
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3. IL-26 inhibits hepatitis C virus replication in hepatocytes

Author

Élodie Beaumont, Vincent Larochette, Laurence Preisser, Charline Miot, Pascale Pignon, Simon Blanchard, Björn-Thore Hansen, Jonathan Dauvé, Caroline Poli, Minna M. Poranen, Patricia Lamourette, Marc Plaisance, Alain Morel, Helmut Fickenscher, Pascale Jeannin, Philippe Roingeard, Yves Delneste, Molecular and Integrative Biosciences Research Programme, University of Helsinki, Biosciences, Molecular and Translational Virology, Morphogénèse et antigénicité du VIH et du virus des Hépatites (MAVIVH - U1259 Inserm - CHRU Tours ), Centre Hospitalier Régional Universitaire de Tours (CHRU Tours)-Université de Tours (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire d'Angers (CHU Angers), PRES Université Nantes Angers Le Mans (UNAM), Centre de Recherche en Cancérologie et Immunologie Intégrée Nantes-Angers (CRCI2NA ), Université d'Angers (UA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Nantes Université - UFR de Médecine et des Techniques Médicales (Nantes Univ - UFR MEDECINE), Nantes Université - pôle Santé, Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Nantes Université - pôle Santé, Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ), Christian-Albrechts University of Kiel, Institut de Cancérologie de l'Ouest [Angers/Nantes] (UNICANCER/ICO), UNICANCER, Helsingin yliopisto = Helsingfors universitet = University of Helsinki, Institut de Biologie et de Technologies de Saclay (IBITECS), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, and Blanchard, Simon

Subjects
MECHANISM, hepatitis C virus, Il-26, DEFENSE, INCREASES, [SDV]Life Sciences [q-bio], DEPENDENT RNA-POLYMERASE, Hepacivirus, Virus Replication, Antiviral Agents, ANTIMICROBIAL PEPTIDE LL-37, Antiviral defense, INFECTION, Viral replication, Humans, Hepatology, Interleukins, DNA, INTERLEUKIN-10, Hepatitis C, [SDV] Life Sciences [q-bio], CATHELICIDIN, 3121 General medicine, internal medicine and other clinical medicine, CELLS, Hepatocytes, Cytokines
Abstract

Publisher Copyright: © 2021 European Association for the Study of the Liver Background & Aims: Interleukin-26 (IL-26) is a proinflammatory cytokine that has properties atypical for a cytokine, such as direct antibacterial activity and DNA-binding capacity. We previously observed an accumulation of IL-26 in fibrotic and inflammatory lesions in the livers of patients with chronic HCV infection and showed that infiltrating CD3+ lymphocytes were the principal source of IL-26. Surprisingly, IL-26 was also detected in the cytoplasm of hepatocytes from HCV-infected patients, even though these cells do not produce IL-26, even when infected with HCV. Based on this observation and possible interactions between IL-26 and nucleic acids, we investigated the possibility that IL-26 controlled HCV infection independently of the immune system. Methods: We evaluated the ability of IL-26 to interfere with HCV replication in hepatocytes and investigated the mechanisms by which IL-26 exerts its antiviral activity. Results: We showed that IL-26 penetrated HCV-infected hepatocytes, where it interacted directly with HCV double-stranded RNA replication intermediates, thereby inhibiting viral replication. IL-26 interfered with viral RNA-dependent RNA polymerase activity, preventing the de novo synthesis of viral genomic single-stranded RNA. Conclusions: These findings reveal a new role for IL-26 in direct protection against HCV infection, independently of the immune system, and increase our understanding of the antiviral defense mechanisms controlling HCV infection. Future studies should evaluate the possible use of IL-26 for treating other chronic disorders caused by RNA viruses, for which few treatments are currently available, or emerging RNA viruses. Lay summary: This study sheds new light on the body's arsenal for controlling hepatitis C virus (HCV) infection and identifies interleukin-26 (IL-26) as an antiviral molecule capable of blocking HCV replication. IL-26, which has unique biochemical and structural characteristics, penetrates infected hepatocytes and interacts directly with viral RNA, thereby blocking viral replication. IL-26 is, therefore, a new player in antiviral defenses, operating independently of the immune system. It is of considerable potential interest for treating HCV infection and other chronic disorders caused by RNA viruses for which few treatments are currently available, and for combating emerging RNA viruses.

Published
2022
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4. Immune Properties of HSP70

Author

Vincent Larochette, Pascale Jeannin, Yves Delneste, Innate Immunity and Immunotherapy (CRCINA-ÉQUIPE 7), Centre de Recherche en Cancérologie et Immunologie Nantes-Angers (CRCINA), Université d'Angers (UA)-Université de Nantes (UN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Université d'Angers (UA)-Université de Nantes (UN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre hospitalier universitaire de Nantes (CHU Nantes), Bernardo, Elizabeth, Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Nantes - UFR de Médecine et des Techniques Médicales (UFR MEDECINE), Université de Nantes (UN)-Université de Nantes (UN)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Centre National de la Recherche Scientifique (CNRS)-Université d'Angers (UA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Nantes - UFR de Médecine et des Techniques Médicales (UFR MEDECINE), and Université de Nantes (UN)-Université de Nantes (UN)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Centre National de la Recherche Scientifique (CNRS)-Université d'Angers (UA)

Subjects
0301 basic medicine, Innate immune system, Relative efficacy, media_common.quotation_subject, Endocytic cycle, [SDV.CAN]Life Sciences [q-bio]/Cancer, Biology, Acquired immune system, 3. Good health, Hsp70, 03 medical and health sciences, 030104 developmental biology, 0302 clinical medicine, Immune system, [SDV.CAN] Life Sciences [q-bio]/Cancer, 030220 oncology & carcinogenesis, Immunology, Internalization, Receptor, media_common
Abstract

International audience; In addition to their conventional chaperon activity, numerous studies have reported that heat shock protein 70 (HSP0) exhibit immune properties and especially the capacity (i) to induce the presentation and cross-presentation of associated or client proteins and, (ii) to control myeloid cell activation. Several studies were focused on the identification of HSP70-binding elements that contribute to their immune properties. A general consensus was reached on the nature of the endocytic receptors involved in the internalization of extracellular HSP70 with belong, for most of them, to the innate immunity receptor family. However, the nature of signaling receptors recruited by HSP70 remains unclear, because the stim-ulatory versus regulatory properties of HSP70 remains a subject of debate. Nevertheless, these unique immune properties allowed developing innovative pro-phylactic and therapeutic vaccines, especially in the treatment of cancers and chronic viral infections. Although HSP70 constitute potent vaccine vehicles in different preclinical models, clinical studies remain disappointing. The fact that the immune properties of HSP70 have not been totally clarified may explain their relative efficacy in human. In this review are presented the main immune properties of HSP70 related to the HSP70-binding elements identified to date, and discuss our current knowledge on their intrinsic immune properties.

Published
2018
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5. IL-26 Confers Proinflammatory Properties to Extracellular DNA

Author

Pascale Jeannin, Pascale Pignon, Jean François Subra, Ariel Savina, Jean-François Augusto, Alain Morel, Alain Chevailler, Simon Blanchard, Christophe Créminon, Yves Delneste, Helmut Fickenscher, Jonathan Dauvé, Clement Adam, Vincent Larochette, Vincent Procaccio, Laurence Preisser, Anne Croue, Caroline Poli, Centre de Recherche en Cancérologie et Immunologie Nantes-Angers (CRCINA), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Nantes - UFR de Médecine et des Techniques Médicales (UFR MEDECINE), Université de Nantes (UN)-Université de Nantes (UN)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Centre National de la Recherche Scientifique (CNRS)-Université d'Angers (UA), Laboratoire d'Immunologie et d'Allergologie, Centre Hospitalier Universitaire d'Angers (CHU Angers), PRES Université Nantes Angers Le Mans (UNAM)-PRES Université Nantes Angers Le Mans (UNAM), Service de Néphrologie-Dialyse-Transplantation [Angers], Université d'Angers (UA)-Centre Hospitalier Universitaire d'Angers (CHU Angers), Institut de Cancérologie de l'Ouest [Angers/Nantes] (UNICANCER/ICO), UNICANCER, Laboratoire Roche SAS [Boulogne Billancourt], Laboratoire d'Immunologie et d'Allergologie, CHU d'Angers, PRES Université Nantes Angers Le Mans (UNAM), Physiopathologie Cardiovasculaire et Mitochondriale (MITOVASC), Université d'Angers (UA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Département de Biochimie et Génétique [Angers], Département de Pathologie Cellulaire et Tissulaire [Angers], Laboratoire d'Etudes et de Recherches en Immunoanalyses (LERI), Service de Pharmacologie et Immunoanalyse (SPI), Médicaments et Technologies pour la Santé (MTS), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Médicaments et Technologies pour la Santé (MTS), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institute for Infection Medicine [Kiel, Germany], Christian-Albrechts-Universität zu Kiel (CAU)- University Medical Center Schleswig-Holstein, none, Université d'Angers (UA)-Université de Nantes (UN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre hospitalier universitaire de Nantes (CHU Nantes), MitoVasc - Physiopathologie Cardiovasculaire et Mitochondriale (MITOVASC), and Bernardo, Elizabeth

Subjects
0301 basic medicine, Adult, Male, Programmed cell death, Adolescent, Protein Conformation, medicine.medical_treatment, Immunology, Myocytes, Smooth Muscle, [SDV.CAN]Life Sciences [q-bio]/Cancer, Inflammation, Biology, Kidney, Autoantigens, Extracellular Traps, Monocytes, Proinflammatory cytokine, 03 medical and health sciences, Young Adult, 0302 clinical medicine, Glomerulonephritis, [SDV.CAN] Life Sciences [q-bio]/Cancer, medicine, Immunology and Allergy, Humans, Secretion, Computer Simulation, Cells, Cultured, Aged, Aged, 80 and over, Innate immune system, Interleukins, Membrane Proteins, Neutrophil extracellular traps, DNA, Middle Aged, Molecular biology, 3. Good health, Cell biology, 030104 developmental biology, Cytokine, Female, medicine.symptom, Inflammation Mediators, Extracellular Space, Intracellular, 030215 immunology, Protein Binding
Abstract

In physiological conditions, self-DNA released by dying cells is not detected by intracellular DNA sensors. In chronic inflammatory disorders, unabated inflammation has been associated with a break in innate immune tolerance to self-DNA. However, extracellular DNA has to complex with DNA-binding molecules to gain access to intracellular DNA sensors. IL-26 is a member of the IL-10 cytokine family, overexpressed in numerous chronic inflammatory diseases, in which biological activity remains unclear. We demonstrate in this study that IL-26 binds to genomic DNA, mitochondrial DNA, and neutrophil extracellular traps, and shuttles them in the cytosol of human myeloid cells. As a consequence, IL-26 allows extracellular DNA to trigger proinflammatory cytokine secretion by monocytes, in a STING- and inflammasome-dependent manner. Supporting these biological properties, IL-10–based modeling predicts two DNA-binding domains, two amphipathic helices, and an in-plane membrane anchor in IL-26, which are structural features of cationic amphipathic cell-penetrating peptides. In line with these properties, patients with active autoantibody-associated vasculitis, a chronic relapsing autoimmune inflammatory disease associated with extensive cell death, exhibit high levels of both circulating IL-26 and IL-26–DNA complexes. Moreover, in patients with crescentic glomerulonephritis, IL-26 is expressed by renal arterial smooth muscle cells and deposits in necrotizing lesions. Accordingly, human primary smooth cells secrete IL-26 in response to proinflammatory cytokines. In conclusion, IL-26 is a unique cationic protein more similar to a soluble pattern recognition receptor than to conventional cytokines. IL-26 expressed in inflammatory lesions confers proinflammatory properties to DNA released by dying cells, setting up a positive amplification loop between extensive cell death and unabated inflammation.

Published
2016
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