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Heterogeneity of Polymorphonuclear Neutrophils in HIV-1 Infection. Study of SIV-Infected Cynomolgus Macaque Model

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Heterogeneity of Polymorphonuclear Neutrophils in HIV-1 Infection. Study of SIV-Infected Cynomolgus Macaque Model Heterogeneity of polymorphonuclear neutrophils in HIV-1 infection. Study of SIV-infected cynomolgus macaque model. Julien Lemaitre To cite this version: Julien Lemaitre. Heterogeneity of polymorphonuclear neutrophils in HIV-1 infection. Study of SIV- infected cynomolgus macaque model.. Innate immunity. Université Paris Saclay (COmUE), 2019. English. NNT : 2019SACLS267. tel-02955513 HAL Id: tel-02955513 https://tel.archives-ouvertes.fr/tel-02955513 Submitted on 2 Oct 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Heterogeneity of polymorphonuclear neutrophils in HIV-1 infection Study of SIV-infected cynomolgus 2019SACLS267 macaque model : NNT Thèse de doctorat de l'Université Paris-Saclay préparée à l’Université Paris-Sud École doctorale n°569 Innovation thérapeutique : du fondamental à l’appliqué (ITFA) Spécialité : Immunologie Thèse présentée et soutenue à Fontenay-aux-Roses, le 13 septembre 2019, par Monsieur Julien Lemaitre Composition du Jury : Sylvie Chollet-Martin Professeur–Praticien hospitalier, GHPNVS-INSERM (UMR-996) Présidente Véronique Witko-Sarsat Directeur de recherche, Institut Cochin-INSERM (UMR-1016) Rapporteur Pierre Delobel Professeur–Praticien hospitalier, CPTP-CHU de Toulouse Rapporteur INSERM (UMR-1043) Mirko Paiardini Professeur assistant, Yerkes National Primate Research Center Examinateur Emory University School of Medicine Olivier Lambotte Professeur–Praticien hospitalier, CHU du Kremlin Bicêtre-INSERM Directeur de thèse (UMR-1184) Anne-Sophie Beignon Chargé de recherche, CEA-CNRS-INSERM (UMR-1184) Co-Directeur de thèse Table of Content Forewords: brief history of a zoonosis ___________________________________________ 8 Introduction_______________________________________________________________ 10 I. The unsolved chronic inflammation in HIV-1 infection ____________________________ 10 II. Causes of chronic inflammation in treated HIV-infection and consequences __________ 13 A. HIV infection as a chronic inflammatory disease ________________________________________ 13 B. Failure of antiretroviral treatments to resolve inflammation ______________________________ 15 1) Reservoirs and pharmacological sanctuaries maintain immune stimulation ________________ 15 i. HIV persistence in cellular and tissue reservoirs ____________________________________ 15 ii. Pharmacological sanctuaries as a source of chronic inflammation _____________________ 18 2) Maintenance of type I interferon response under cART ________________________________ 19 C. Unrestored mucosal immune response under cART _____________________________________ 20 D. Co-factors associated with amplification of inflammation _________________________________ 25 1) Co-infections as additional sources of inflammation ___________________________________ 25 i. Tuberculosis strongly activates immune cells ______________________________________ 25 ii. Cytomegalovirus modulates neutrophils responses _________________________________ 26 iii. Viral hepatitis co-infections and liver fibrosis ______________________________________ 27 2) Lifestyle and inflammation _______________________________________________________ 28 E. Consequences of chronic inflammation _______________________________________________ 30 F. Resolution of chronic inflammation by natural hosts _____________________________________ 33 III. Neutrophils plasticity in response to inflammation _______________________________ 37 A. Neutrophil life from granulopoiesis to efferocytosis _____________________________________ 37 1) Feedback loop of neutrophils production ___________________________________________ 37 2) Differentiation and maturation of neutrophils _______________________________________ 39 3) Circadian cycle orchestrates neutrophils circulation and tissue migration _________________ 41 4) Anti-microbial function of neutrophils ______________________________________________ 42 5) Neutrophil compartmentalization and death to control inflammation ____________________ 44 B. Heterogeneity and function of neutrophils in chronic inflammation ________________________ 46 1) Auto-immune diseases __________________________________________________________ 46 2) Cancers ______________________________________________________________________ 48 3) Tuberculosis ___________________________________________________________________ 49 4) Neutrophils in chronic viral infections ______________________________________________ 51 C. Neutrophils in HIV infection ________________________________________________________ 53 1) Dynamic of neutrophils in HIV infection_____________________________________________ 53 i. HIV infection and neutropenia __________________________________________________ 53 1 ii. Mucosal neutrophils in HIV infection ____________________________________________ 54 2) Neutrophil function in HIV infection _______________________________________________ 54 i. Neutrophil’s antiviral response _________________________________________________ 54 ii. Dual role in HIV acquisition and protection _______________________________________ 55 iii. Neutrophils function and chronic inflammation ____________________________________ 56 Methodology ______________________________________________________________ 59 I. General objectives _________________________________________________________ 59 II. Study model ______________________________________________________________ 62 III. Principles of mass cytometry ________________________________________________ 64 Results ___________________________________________________________________ 67 I. Mass cytometry reveals the immaturity of circulating neutrophils during SIV infection __ 67 A. Summary________________________________________________________________________ 67 B. Manuscript ______________________________________________________________________ 67 II. Immature CD10- neutrophils exert immunostimulatory function during primary and chronic SIV infection __________________________________________________________________ 80 A. Summary________________________________________________________________________ 80 B. Manuscript ______________________________________________________________________ 82 1) Abstract ______________________________________________________________________ 83 2) Introduction ___________________________________________________________________ 84 3) Material and method ___________________________________________________________ 85 4) Results _______________________________________________________________________ 88 5) Discussion ____________________________________________________________________ 94 III. Unpublished results: tissue neutrophils heterogeneity in cynomolgus macaques______ 101 A. Introduction ____________________________________________________________________ 101 B. Material and method _____________________________________________________________ 101 C. Preliminary results _______________________________________________________________ 102 Discussion and perspectives _________________________________________________ 106 I. Validation of experimental approach _________________________________________ 106 II. Discussion ______________________________________________________________ 107 III. Perspectives _____________________________________________________________ 109 References _______________________________________________________________ 113 2 List of figures Figure 1: Major causes of chronic inflammation in HIV-infected patients under cART and association with non-AIDS-related diseases. Figure 2: Gut CD4+ T cell depletion and lymph node histopathology during HIV-1 infection Figure 3: Persistence of viral reservoir and residual replication are associated to poor antiretroviral drugs distribution. Figure 4: Neutrophils infiltrate gut during HIV infection. Figure 5: Translocated microbial products reach secondary lymphoid tissues and drive distant inflammation. Figure 6: Incidences of non-AIDS-related comorbidities. Figure 7: Mechanisms involve in control of chronic inflammation by natural hosts. Figure 8: Regulation of neutrophils production and circulation. Figure 9: Neutrophil differentiation in human bone marrow. Figure 10: Pattern recognition receptors sensing viruses in human neutrophils. Figure 11: Dynamic of viral replication along with CD4+ T cells and CD8+ T cells in SIVmac251- infected cynomolgus macaques. Figure 12: Mass cytometry operation and data analysis. 3 List of abbreviations 3TC: Lamivudine FDC: Follicular dendritic cell AAV: Antibody-associated vasculitis fMLP: N-formylmethionine-leucyl- phenylalanine ACPA: Anti-citrullinated protein antibodies FTC: Emtricitabine ADCC: Antibody-dependent cellular cytotoxicity G-CSF: Granulocyte-colony stimulating factor ADCP: Antibody-dependent cellular G-MDSC: Granulocytic-myeloid-derived phagocytosis suppressive cell AGM: African green monkey GALT: Gut-associated lymphoid tissue AIDS : Acquired immunodeficiency syndrome GM-CSF: Granulocyte-monocyte colony stimulating factor ANRS: Agence nationale de recherche sur le sida et les hépatites virales GMP: Granulocyte-monocyte
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