Differential and sequential immunomodulatory role of neutrophils and Ly6C^hi inflammatory monocytes during antiviral antibody therapy

References

• Dibo M, Battocchio EC, dos SSantos SSouza LM, et al. Antibody Therapy for the Control of Viral Diseases: An Update. CPB. 2019 Oct 28;20(13):1108–1121.
   Web of Science ®Google Scholar
• Salazar G, Zhang N, Fu T-M, et al. Antibody therapies for the prevention and treatment of viral infections. NPJ Vaccines. 2017;2:19.
   PubMed Web of Science ®Google Scholar
• Lu LL, Suscovich TJ, Fortune SM, et al. Beyond binding: antibody effector functions in infectious diseases. Nat Rev Immunol. 2018 Jan;18(1):46–61.
   PubMed Web of Science ®Google Scholar
• Pelegrin M, Naranjo-Gomez M, Piechaczyk M. Antiviral monoclonal antibodies: can they be more than simple neutralizing agents? Trends Microbiol 2015 Oct;23(10):653–665.
   PubMed Web of Science ®Google Scholar
• Naranjo-Gomez M, Pelegrin M. Vaccinal effect of HIV-1 antibody therapy: current opinion in HIV and AIDS. 2019 Jul;14(4):325–333.
   Google Scholar
• Niessl J, Baxter AE, Mendoza P, et al. Combination anti-HIV-1 antibody therapy is associated with increased virus-specific T cell immunity. Nat Med. 2020 Feb;26(2):222–227.
   PubMed Web of Science ®Google Scholar
• Schoofs T, Klein F, Braunschweig M, et al. HIV-1 therapy with monoclonal antibody 3BNC117 elicits host immune responses against HIV-1. Science. 2016 May 20;352(6288):997–1001.
   PubMed Web of Science ®Google Scholar
• Bournazos S, Klein F, Pietzsch J, et al. Broadly neutralizing anti-HIV-1 antibodies require Fc effector functions for in vivo activity. Cell. 2014 Sept;158(6):1243–1253.
   Google Scholar
• Earnest JT, Basore K, Roy V, et al. Neutralizing antibodies against mayaro virus require Fc effector functions for protective activity. J Exp Med. 2019 Oct 7;216(10):2282–2301.
   PubMed Web of Science ®Google Scholar
• Fox JM, Roy V, Gunn BM, et al. Optimal therapeutic activity of monoclonal antibodies against chikungunya virus requires Fc-FcγR interaction on monocytes. Sci Immunol. 2019 Feb 22;4(32):eaav5062.
   PubMed Web of Science ®Google Scholar
• Gunn BM, Yu W-H, Karim MM, et al. A role for Fc function in therapeutic monoclonal antibody-mediated protection against Ebola virus. Cell Host & Microbe. 2018 Aug;24(2):221–233.e5.
   PubMed Web of Science ®Google Scholar
• Lambour J, Naranjo-Gomez M, Piechaczyk M, et al. Converting monoclonal antibody-based immunotherapies from passive to active: bringing immune complexes into play. Emerg Microbes Infect. 2016 Aug 17;5(8):e92.
   Google Scholar
• Michaud H-A, Gomard T, Gros L, et al. A crucial role for infected-cell/antibody immune complexes in the enhancement of endogenous antiviral immunity by short passive immunotherapy. PLoS Pathog. 2010 Jun 10;6(6):e1000948.
   Web of Science ®Google Scholar
• Nasser R, Pelegrin M, Michaud H-A, et al. Long-lasting protective antiviral immunity induced by passive immunotherapies requires both neutralizing and effector functions of the administered monoclonal antibody. J Virol. 2010 Oct;84(19):10169–10181.
   Web of Science ®Google Scholar
• Celis E, Chang TW. HBsAg-serum protein complexes stimulate immune T lymphocytes more efficiently than do pure HBsAg. Hepatology 1984 Dec;4(6):1116–1123.
   Web of Science ®Google Scholar
• Yamamoto T, Iwamoto N, Yamamoto H, et al. Polyfunctional CD4+ T-cell induction in neutralizing antibody-triggered control of simian immunodeficiency virus infection. J Virol. 2009 Jun;83(11):5514–5524.
   Web of Science ®Google Scholar
• Bournazos S, Corti D, Virgin HW, et al. Fc-optimized antibodies elicit CD8 immunity to viral respiratory infection. Nature. 2020 Oct; 588(7838):485–490.
   PubMed Web of Science ®Google Scholar
• Naranjo-Gomez M, Lambour J, Piechaczyk M, et al. Neutrophils are essential for induction of vaccine-like effects by antiviral monoclonal antibody immunotherapies. JCI Insight. 2018 May;3(9):e97339.
   Web of Science ®Google Scholar
• Wang X-Y, Wang B, Wen Y-M. From therapeutic antibodies to immune complex vaccines. NPJ Vaccines. 2019 Dec;4(1):2.
   Web of Science ®Google Scholar
• Wen Y-M, Mu L, Shi Y. Immunoregulatory functions of immune complexes in vaccine and therapy. EMBO Mol Med. 2016;8(10):1120–1133.
   PubMed Web of Science ®Google Scholar
• Mantovani A, Cassatella MA, Costantini C, et al. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011 Jul 25;11(8):519–531.
   PubMed Web of Science ®Google Scholar
• Tecchio C, Cassatella MA. Neutrophil-derived chemokines on the road to immunity. Semin Immunol. 2016 Apr;28(2):119–128.
   PubMed Web of Science ®Google Scholar
• Tamassia N, Bianchetto-Aguilera F, Arruda-Silva F, et al. Cytokine production by human neutrophils: revisiting the « dark side of the moon ». Eur J Clin Invest. 2018 May 17;e12952.
   Web of Science ®Google Scholar
• Stegelmeier AA, van Vloten JP, Mould RC, et al. Myeloid cells during viral infections and inflammation. Viruses. 2019 Feb 19;11(2):168.
   Web of Science ®Google Scholar
• Portis JL, Czub S, Garon CF, et al. Neurodegenerative disease induced by the wild mouse ecotropic retrovirus is markedly accelerated by long terminal repeat and gag-pol sequences from nondefective Friend murine leukemia virus. J Virol. 1990 Apr;64(4):1648–1656.
   Web of Science ®Google Scholar
• Gros L, Dreja H, Fiser AL, et al. Induction of long-term protective antiviral endogenous immune response by short neutralizing monoclonal antibody treatment. J Virol. 2005 May;79(10):6272–6280.
   Web of Science ®Google Scholar
• McAtee FJ, Portis JL. Monoclonal antibodies specific for wild mouse neurotropic retrovirus: detection of comparable levels of virus replication in mouse strains susceptible and resistant to paralytic disease. J Virol. 1985 Dec;56(3):1018–1022.
   Web of Science ®Google Scholar
• Chesebro B, Collins JK, Wehrly K, et al. Expression of cell surface Friend virus gp70 does not block reinfection by ecotropic murine leukemia viruses. Virology (Auckl) 1981 Nov;115(1):125–129.
   Google Scholar
• Tipton TRW, Mockridge CI, French RR, et al. Anti-mouse FcγRIV antibody 9E9 also blocks FcγRIII in vivo. Blood. 2015 Dec 10;126(24):2643–2645.
   Web of Science ®Google Scholar
• Gros L, Pelegrin M, Michaud H-A, et al. Endogenous cytotoxic T-cell response contributes to the long-term antiretroviral protection induced by a short period of antibody-based immunotherapy of neonatally infected mice. J Virol. 2008 Feb;82(3):1339–1349.
   Web of Science ®Google Scholar
• Pelegrin M, Marin M, Oates A, et al. Immunotherapy of a viral disease by in vivo production of therapeutic monoclonal antibodies. Hum Gene Ther. 2000 Jul 1;11(10):1407–1415.
   Web of Science ®Google Scholar
• Wang Y, Jönsson F. Expression, role, and regulation of neutrophil Fcγ receptors. Front Immunol. 2019 Aug 27;10:1958.
   PubMed Web of Science ®Google Scholar
• Nimmerjahn F, Bruhns P, Horiuchi K, et al. FcgammaRIV: a novel FcR with distinct IgG subclass specificity. Immunity. 2005 Jul;23(1):41–51.
   PubMed Web of Science ®Google Scholar
• Naranjo-Gomez M, Cahen M, Lambour J, et al. Immunomodulatory role of NK cells during antiviral antibody therapy. Vaccines (Basel). 2021 Feb 8;9(2):137.
   Web of Science ®Google Scholar
• Yoshida T, Kobayashi M, Li X-D, et al. Inhibitory effect of glycyrrhizin on the neutrophil-dependent increase of R5 HIV replication in cultures of macrophages. Immunol Cell Biol. 2009 Oct;87(7):554–558.
   Web of Science ®Google Scholar
• Hokeness KL, Kuziel WA, Biron CA, et al. Monocyte chemoattractant protein-1 and CCR2 interactions Are required for IFN- / -induced inflammatory responses and antiviral defense in liver. The Journal of Immunology. 2005 Feb 1;174(3):1549–1556.
   Web of Science ®Google Scholar
• Miller AL, Bowlin TL, Lukacs NW. Respiratory syncytial virus–induced chemokine production: linking viral replication to chemokine production in vitro and in vivo. J Infect Dis. 2004 Apr 15;189(8):1419–1430.
   Web of Science ®Google Scholar
• Rubio N, Sanz-Rodriguez F. Induction of the CXCL1 (KC) chemokine in mouse astrocytes by infection with the murine encephalomyelitis virus of theiler. Virology (Auckl) 2007 Feb;358(1):98–108.
   Google Scholar
• Seo S-U, Kwon H-J, Ko H-J, et al. Type I interferon signaling regulates Ly6C(hi) monocytes and neutrophils during acute viral pneumonia in mice. PLoS Pathog 2011 Feb;7(2):e1001304.
   PubMed Web of Science ®Google Scholar
• Wareing MD, Lyon AB, Lu B, et al. Chemokine expression during the development and resolution of a pulmonary leukocyte response to influenza A virus infection in mice. Journal of Leukocyte Biology. 2004 Oct;76(4):886–895.
   PubMed Web of Science ®Google Scholar
• Dahal LN, Dou L, Hussain K, et al. STING activation reverses lymphoma-mediated resistance to antibody immunotherapy. Cancer Res. 2017 Jul 1;77(13):3619–3631.
   Web of Science ®Google Scholar
• Lehmann B, Biburger M, Brückner C, et al. Tumor location determines tissue-specific recruitment of tumor-associated macrophages and antibody-dependent immunotherapy response. Sci Immunol. 2017 Jan 6;2(7):eaah6413.
   PubMed Web of Science ®Google Scholar
• Pricop L, Redecha P, Teillaud JL, et al. Differential modulation of stimulatory and inhibitory Fc gamma receptors on human monocytes by Th1 and Th2 cytokines. J Immunol. 2001 Jan 1;166(1):531–537.
   PubMed Web of Science ®Google Scholar
• Bruhns P. Properties of mouse and human IgG receptors and their contribution to disease models. Blood. 2012 Jun 14;119(24):5640–5649.
   PubMed Web of Science ®Google Scholar
• Zhang J, Liu J, Yuan Y, et al. Two waves of pro-inflammatory factors are released during the influenza A virus (IAV)-driven pulmonary immunopathogenesis. Sant AJ, éditeur. PLoS Pathog. 2020 Feb 26;16(2):e1008334.
   Web of Science ®Google Scholar
• Nimmerjahn F, Lux A, Albert H, et al. Fc RIV deletion reveals its central role for IgG2a and IgG2b activity in vivo. Proc Natl Acad Sci USA. 2010 Nov 9;107(45):19396–19401.
   Web of Science ®Google Scholar
• Otten MA, van der Bij GJ, Verbeek SJ, et al. Experimental antibody therapy of liver metastases reveals functional redundancy between Fc gammaRI and Fc gammaRIV. J Immunol. 2008 Nov 15;181(10):6829–6836.
   Web of Science ®Google Scholar
• Simpson TR, Li F, Montalvo-Ortiz W, et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J Exp Med. 2013 Aug 26;210(9):1695–1710.
   PubMed Web of Science ®Google Scholar
• DiLillo DJ, Ravetch JV. Differential Fc-receptor engagement drives an anti-tumor vaccinal effect. Cell. 2015 May 21;161(5):1035–1045.
   PubMed Web of Science ®Google Scholar
• Jakus Z, Németh T, Verbeek JS, et al. Critical but overlapping role of FcgammaRIII and FcgammaRIV in activation of murine neutrophils by immobilized immune complexes. J Immunol. 2008 Jan 1;180(1):618–629.
   Web of Science ®Google Scholar
• Syed SN, Konrad S, Wiege K, et al. Both FcgammaRIV and FcgammaRIII are essential receptors mediating type II and type III autoimmune responses via FcRgamma-LAT-dependent generation of C5a. Eur J Immunol. 2009 Dec;39(12):3343–3356.
   Web of Science ®Google Scholar
• Czarniecki CW. The role of tumor necrosis factor in viral disease. Antiviral Research. 1993 Dec;22(4):223–258.
   Web of Science ®Google Scholar
• Hildenbrand B, Lorenzen D, Sauer B, et al. IFN-y enhances T(H)1 polarisation of monocyte-derived dendritic cells matured with clinical-grade cytokines using serum-free conditions. Anticancer Res 2008 Jun;28(3A):1467–1476.
   Web of Science ®Google Scholar
• Jin P, Zhao Y, Liu H, et al. Interferon-γ and tumor necrosis factor-α polarize bone marrow stromal cells uniformly to a Th1 phenotype. Sci Rep. 2016 Sep;6(1):26345.
   Web of Science ®Google Scholar
• Uciechowski P, Dempke WCM. Interleukin-6: A masterplayer in the cytokine network. Oncology. 2020;98(3):131–137.
   PubMed Web of Science ®Google Scholar
• Wang JP, Kurt-Jones EA, Shin OS, et al. Varicella-Zoster virus activates inflammatory cytokines in human monocytes and macrophages via toll-like receptor 2. J Virol. 2005 Oct 15;79(20):12658–12666.
   PubMed Web of Science ®Google Scholar
• Lok LSC, Dennison TW, Mahbubani KM, et al. Phenotypically distinct neutrophils patrol uninfected human and mouse lymph nodes. Proc Natl Acad Sci USA. 2019 Sept 17;116(38):19083–9.
   PubMed Web of Science ®Google Scholar
• Meinderts SM, Baker G, van Wijk S, et al. Neutrophils acquire antigen-presenting cell features after phagocytosis of IgG-opsonized erythrocytes. Blood Advances. 2019 Jun 11;3(11):1761–1773.
   Web of Science ®Google Scholar
• Vono M, Lin A, Norrby-Teglund A, et al. Neutrophils acquire the capacity for antigen presentation to memory CD4+ T cells in vitro and ex vivo. Blood. 2017 Apr 6;129(14):1991–2001.
   PubMed Web of Science ®Google Scholar
• Wessel AW, Kose N, Bombardi RG, et al. Antibodies targeting epitopes on the cell-surface form of NS1 protect against zika virus infection during pregnancy. Nat Commun. 2020 Dec;11(1):5278.
   Web of Science ®Google Scholar
• Johnson RF, Bagci U, Keith L, et al. 3B11-N, a monoclonal antibody against MERS-CoV, reduces lung pathology in rhesus monkeys following intratracheal inoculation of MERS-CoV Jordan-n3/2012. Virology (Auckl) 2016 Mar;490:49–58.
   Google Scholar
• Zost SJ, Gilchuk P, Case JB, et al. Potently neutralizing and protective human antibodies against SARS-CoV-2. Nature. 2020 Aug;584(7821):443–449.
   PubMed Web of Science ®Google Scholar
• Bournazos S, DiLillo DJ, Goff AJ, et al. Differential requirements for FcγR engagement by protective antibodies against Ebola virus. Proc Natl Acad Sci USA. 2019 Oct 1;116(40):20054–20062.
   PubMed Web of Science ®Google Scholar
• Chen TF, Sazinsky SL, Houde D, et al. Engineering aglycosylated IgG variants with wild-type or improved binding affinity to human Fc gamma RIIA and Fc gamma RIIIAs. Journal of Molecular Biology. 2017 Aug;429(16):2528–2541.
   Web of Science ®Google Scholar