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Emerging Microbes & Infections Volume 5, 2016 - Issue 1
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Non-neutralizing protective antibodies

Converting monoclonal antibody-based immunotherapies from passive to active: bringing immune complexes into play

Jennifer Lambour‘Equipe Labellisée par la Ligue Contre le Cancer’ - Institut de Génétique Moléculaire de Montpellier, UMR 5535, CNRS, 34293 Montpellier Cedex 5, France; Université de Montpellier, 34090Montpellier, France
,
Mar Naranjo-Gomez‘Equipe Labellisée par la Ligue Contre le Cancer’ - Institut de Génétique Moléculaire de Montpellier, UMR 5535, CNRS, 34293 Montpellier Cedex 5, France; Université de Montpellier, 34090Montpellier, France
,
Marc Piechaczyk‘Equipe Labellisée par la Ligue Contre le Cancer’ - Institut de Génétique Moléculaire de Montpellier, UMR 5535, CNRS, 34293 Montpellier Cedex 5, France; Université de Montpellier, 34090Montpellier, France
&
Mireia Pelegrin‘Equipe Labellisée par la Ligue Contre le Cancer’ - Institut de Génétique Moléculaire de Montpellier, UMR 5535, CNRS, 34293 Montpellier Cedex 5, France; Université de Montpellier, 34090Montpellier, FranceCorrespondence[email protected]
Pages 1-9 | Received 15 Jun 2016, Accepted 14 Jul 2016, Published online: 25 Jan 2019

  • IraniV,GuyAJ,AndrewD,BeesonJG,RamslandPA,RichardsJS.Molecular properties of human IgG subclasses and their implications for designing therapeutic monoclonal antibodies against infectious diseases.Mol Immunol2015; 67:171–182.
  • VacchelliE,EggermontA,GalonJet al.Trial watch: monoclonal antibodies in cancer therapy.Oncoimmunology2013; 2:e22789.
  • BornholdtZA,TurnerHL,MurinCDet al.Isolation of potent neutralizing antibodies from a survivor of the 2014 Ebola virus outbreak.Science2016; 351:1078–1083.
  • CortiD,MisasiJ,MulanguSet al.Protective monotherapy against lethal Ebola virus infection by a potently neutralizing antibody.Science2016; 351:1339–1342.
  • CortiD,ZhaoJ,PedottiMet al.Prophylactic and postexposure efficacy of a potent human monoclonal antibody against MERS coronavirus.Proc Natl Acad Sci USA2015; 112:10473–10478.
  • JohnsonRF,BagciU,KeithLet al.3B11-N, a monoclonal antibody against MERS-CoV, reduces lung pathology in rhesus monkeys following intratracheal inoculation of MERS-CoV Jordan-n3/2012.Virology2016; 490:49–58.
  • QiuX,WongG,AudetJet al.Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp.Nature2014; 514:47–53.
  • BarouchDH,WhitneyJB,MoldtBet al.Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIV-infected rhesus monkeys.Nature2013; 503:224–228.
  • BerryJD,GaudetRG.Antibodies in infectious diseases: polyclonals, monoclonals and niche biotechnology.N Biotechnol2011; 28:489–501.
  • BothL,BanyardAC,van DolleweerdC,WrightE,MaJK,FooksAR.Monoclonal antibodies for prophylactic and therapeutic use against viral infections.Vaccine2013; 31:1553–1559.
  • CortiD,LanzavecchiaA.Broadly neutralizing antiviral antibodies.Annu Rev Immunol2013; 31:705–742.
  • de JongYP,DornerM,MommersteegMCet al.Broadly neutralizing antibodies abrogate established hepatitis C virus infection.Sci Transl Med2014; 6:254ra129.
  • DejnirattisaiW,WongwiwatW,SupasaSet al.A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus.Nat Immunol2015; 16:170–177.
  • FlegoM,AscioneA,CianfrigliaM,VellaS.Clinical development of monoclonal antibody-based drugs in HIV and HCV diseases.BMC Med2013; 11:4.
  • FlyakAI,IlinykhPA,MurinCDet al.Mechanism of human antibody-mediated neutralization of Marburg virus.Cell2015; 160:893–903.
  • FlyakAI,ShenX,MurinCDet al.Cross-reactive and potent neutralizing antibody responses in human survivors of natural Ebolavirus infection.Cell2015; 164:392–405.
  • GautamR,NishimuraY,PeguAet al.A single injection of anti-HIV-1 antibodies protects against repeated SHIV challenges.Nature2016; 533:105–109.
  • HessellAJ,JaworskiJP,EpsonEet al.Early short-term treatment with neutralizing human monoclonal antibodies halts SHIV infection in infant macaques.Nat Med2016; 22:362–368.
  • KrawczykA,ArndtMA,Grosse-HovestLet al.Overcoming drug-resistant herpes simplex virus (HSV) infection by a humanized antibody.Proc Natl Acad Sci USA2013; 110:6760–6765.
  • MarascoWA,SuiJ.The growth and potential of human antiviral monoclonal antibody therapeutics.Nat Biotechnol2007; 25:1421–1434.
  • TanY,NgQ,JiaQ,KwangJ,HeF.A novel humanized antibody neutralizes H5N1 influenza virus via two different mechanisms.J Virol2015; 89:3712–3722.
  • WilliamsKL,Sukupolvi-PettyS,BeltramelloMet al.Therapeutic efficacy of antibodies lacking Fcgamma receptor binding against lethal dengue virus infection is due to neutralizing potency and blocking of enhancing antibodies [corrected].PLoS Pathog2013; 9:e1003157.
  • CaskeyM,KleinF,LorenziJCet al.Viraemia suppressed in HIV-1-infected humans by broadly neutralizing antibody 3BNC117.Nature2015; 522:487–491.
  • LynchRM,BoritzE,CoatesEEet al.Virologic effects of broadly neutralizing antibody VRC01 administration during chronic HIV-1 infection.Sci Transl Med2015; 7:319ra206.
  • BruhnsP,JonssonF.Mouse and human FcR effector functions.Immunol Rev2015; 268:25–51.
  • PinceticA,BournazosS,DiLilloDJet al.Type I and type II Fc receptors regulate innate and adaptive immunity.Nat Immunol2014; 15:707–716.
  • EulerZ,AlterG.Exploring the potential of monoclonal antibody therapeutics for HIV-1 eradication.AIDS Res Hum Retroviruses2014; 31:13–24.
  • HessellAJ,HaigwoodNL.Neutralizing antibodies and control of HIV: moves and countermoves.Curr HIV/AIDS Rep2012; 9:64–72.
  • SuB,MoogC.Which antibody functions are important for an HIV vaccine?Front Immunol2014; 5:289.
  • NimmerjahnF,GordanS,LuxA.FcgammaR dependent mechanisms of cytotoxic, agonistic, and neutralizing antibody activities.Trends Immunol2015; 36:325–336.
  • MalbecM,PorrotF,RuaRet al.Broadly neutralizing antibodies that inhibit HIV-1 cell to cell transmission.J Exp Med2013; 210:2813–2821.
  • BruhnsP.Properties of mouse and human IgG receptors and their contribution to disease models.Blood2012; 119:5640–5649.
  • GetahunA,HeymanB.How antibodies act as natural adjuvants.Immunol Lett2006; 104:38–45.
  • HeymanB.Antibodies as natural adjuvants.Curr Top Microbiol Immunol2014; 382:201–219.
  • HjelmF,CarlssonF,GetahunA,HeymanB.Antibody-mediated regulation of the immune response.Scand J Immunol2006; 64:177–184.
  • NimmerjahnF,RavetchJV.Fcgamma receptors as regulators of immune responses.Nat Rev Immunol2008; 8:34–47.
  • SchwabI,NimmerjahnF.Intravenous immunoglobulin therapy: how does IgG modulate the immune system?Nat Rev Immunol2013; 13:176–189.
  • BradyLJ.Antibody-mediated immunomodulation: a strategy to improve host responses against microbial antigens.Infect Immun2005; 73:671–678.
  • PelegrinM,Naranjo-GomezM,PiechaczykM.Antiviral monoclonal antibodies: can they be more than simple neutralizing agents?Trends Microbiol2015; 23:653–665.
  • GrosL,DrejaH,FiserAL,PlaysM,PelegrinM,PiechaczykM.Induction of long-term protective antiviral endogenous immune response by short neutralizing monoclonal antibody treatment.J Virol2005; 79:6272–6280.
  • GrosL,PelegrinM,MichaudHAet 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 Virol2008; 82:1339–1349.
  • GrosL,PelegrinM,PlaysM,PiechaczykM.Efficient mother-to-child transfer of antiretroviral immunity in the context of preclinical monoclonal antibody-based immunotherapy.J Virol2006; 80:10191–10200.
  • MichaudHA,GomardT,GrosLet al.A crucial role for infected-cell/antibody immune complexes in the enhancement of endogenous antiviral immunity by short passive immunotherapy.PLoS Pathog2010; 6:e1000948.
  • NasserR,PelegrinM,MichaudHAet al.Long-lasting protective antiviral immunity induced by passive immunotherapies requires both neutralizing and effector functions of the administered monoclonal antibody.J Virol2010; 84:10169–10181.
  • NasserR,PelegrinM,PlaysM,GrosL,PiechaczykM.Control of regulatory T cells is necessary for vaccine-like effects of antiviral immunotherapy by monoclonal antibodies.Blood2013; 121:1102–1111.
  • Boyoglu-BarnumS,ChirkovaT,ToddSOet al.Prophylaxis with a respiratory syncytial virus (RSV) anti-G protein monoclonal antibody shifts the adaptive immune response to RSV rA2-line19F infection from Th2 to Th1 in BALB/c mice.J Virol2014; 88:10569–10583.
  • BossartKN,GeisbertTW,FeldmannHet al.A neutralizing human monoclonal antibody protects african green monkeys from hendra virus challenge.Sci Transl Med2011; 3:105ra103.
  • GeisbertTW,MireCE,GeisbertJBet al.Therapeutic treatment of Nipah virus infection in nonhuman primates with a neutralizing human monoclonal antibody.Sci Transl Med2014; 6:242ra282.
  • JaworskiJP,KobieJ,BrowerZet al.Neutralizing polyclonal IgG present during acute infection prevents rapid disease onset in simian-human immunodeficiency virus SHIVSF162P3-infected infant rhesus macaques.J Virol2013; 87:10447–10459.
  • NgCT,JaworskiJP,JayaramanPet al.Passive neutralizing antibody controls SHIV viremia and enhances B cell responses in infant macaques.Nat Med2010; 16:1117–1119.
  • WatkinsJD,SiddappaNB,LakhasheSKet al.An anti-HIV-1 V3 loop antibody fully protects cross-clade and elicits T-cell immunity in macaques mucosally challenged with an R5 clade C SHIV.PLoS One2011; 6:e18207.
  • SchoofsT,KleinF,BraunschweigMet al.HIV-1 therapy with monoclonal antibody 3BNC117 elicits hoost immune responses against HIV-1.Science2016; 352:997–1001.
  • BournazosS,KleinF,PietzschJ,SeamanMS,NussenzweigMC,RavetchJV.Broadly neutralizing anti-HIV-1 antibodies require Fc effector functions for in vivo activity.Cell2014; 158:1243–1253.
  • Halper-StrombergA,LuCL,KleinFet al.Broadly neutralizing antibodies and viral inducers decrease rebound from HIV-1 latent reservoirs in humanized mice.Cell2014; 158:989–999.
  • CelisE,ChangTW.HBsAg-serum protein complexes stimulate immune T lymphocytes more efficiently than do pure HBsAg.Hepatology1984; 4:1116–1123.
  • ZhengBJ,ZhouJ,QuDet al.Selective functional deficit in dendritic cell—T cell interaction is a crucial mechanism in chronic hepatitis B virus infection.J Viral Hepat2004; 11:217–224.
  • VillingerF,MayneAE,BostikPet al.Evidence for antibody-mediated enhancement of simian immunodeficiency virus (SIV) Gag antigen processing and cross presentation in SIV-infected rhesus macaques.J Virol2003; 77:10–24.
  • YamamotoT,IwamotoN,YamamotoHet al.Polyfunctional CD4+ T-cell induction in neutralizing antibody-triggered control of simian immunodeficiency virus infection.J Virol2009; 83:5514–5524.
  • PoschW,CardinaudS,HamimiCet al.Antibodies attenuate the capacity of dendritic cells to stimulate HIV-specific cytotoxic T lymphocytes.J Allergy Clin Immunol2012; 130:1368–1374 e1362.
  • XuDZ,HuangKL,ZhaoKet al.Vaccination with recombinant HBsAg-HBIG complex in healthy adults.Vaccine2005; 23:2658–2664.
  • YaoX,ZhengB,ZhouJet al.Therapeutic effect of hepatitis B surface antigen-antibody complex is associated with cytolytic and non-cytolytic immune responses in hepatitis B patients.Vaccine2007; 25:1771–1779.
  • XuDZ,ZhaoK,GuoLMet al.A randomized controlled phase IIb trial of antigen-antibody immunogenic complex therapeutic vaccine in chronic hepatitis B patients.PLoS One2008; 3:e2565.
  • LiuH,GengS,WangBet al.Immuno-potentiating pathway of HBsAg-HBIG immunogenic complex visualized.Hum Vaccin Immunother2015; 12:77–84.
  • LeonB,Ballesteros-TatoA,RandallTD,LundFE.Prolonged antigen presentation by immune complex-binding dendritic cells programs the proliferative capacity of memory CD8 T cells.J Exp Med2014; 211:1637–1655.
  • KruijsenD,BakkersMJ,van UdenNOet al.Serum antibodies critically affect virus-specific CD4+/CD8+ T cell balance during respiratory syncytial virus infections.J Immunol2010; 185:6489–6498.
  • DuhanV,KhairnarV,FriedrichSKet al.Virus-specific antibodies allow viral replication in the marginal zone, thereby promoting CD8(+) T-cell priming and viral control.Sci Rep2016; 6:19191.
  • BachmannMF,HunzikerL,ZinkernagelRM,StorniT,KopfM.Maintenance of memory CTL responses by T helper cells and CD40-CD40 ligand: antibodies provide the key.Eur J Immunol2004; 34:317–326.
  • BergthalerA,FlatzL,VerschoorAet al.Impaired antibody response causes persistence of prototypic T cell-contained virus.PLoS Biol2009; 7:e80.
  • TerresG,WolinsW.Enhanced immunological sensitization of mice by the simultaneous injection of antigen and specific antiserum. I. Effect of varying the amount of antigen used relative to the antiserum.J Immunol1961; 86:361–368.
  • WenYM,QuD,ZhouSH.Antigen-antibody complex as therapeutic vaccine for viral hepatitis B.Int Rev Immunol1999; 18:251–258.
  • BasalpA,CirakogluB,BermekE.Enhancement of the immune response to hepatitis B virus vaccine by antigen specific IgM.Immunol Lett2000; 73:1–6.
  • ZhengBJ,NgMH,HeLFet al.Therapeutic efficacy of hepatitis B surface antigen-antibodies-recombinant DNA composite in HBsAg transgenic mice.Vaccine2001; 19:4219–4225.
  • LuM,YaoX,XuYet al.Combination of an antiviral drug and immunomodulation against hepadnaviral infection in the woodchuck model.J Virol2008; 82:2598–2603.
  • McCluskieMJ,WenYM,DiQ,DavisHL.Immunization against hepatitis B virus by mucosal administration of antigen-antibody complexes.Viral Immunol1998; 11:245–252.
  • HioeCE,ViscianoML,KumarRet al.The use of immune complex vaccines to enhance antibody responses against neutralizing epitopes on HIV-1 envelope gp120.Vaccine2009; 28:352–360.
  • KumarR,TuenM,LiH,TseDB,HioeCE.Improving immunogenicity of HIV-1 envelope gp120 by glycan removal and immune complex formation.Vaccine2011; 29:9064–9074.
  • KumarR,TuenM,LiuJet al.Elicitation of broadly reactive antibodies against glycan-modulated neutralizing V3 epitopes of HIV-1 by immune complex vaccines.Vaccine2013; 31:5413–5421.
  • KruijsenD,EinarsdottirHK,SchijfMAet al.Intranasal administration of antibody-bound respiratory syncytial virus particles efficiently primes virus-specific immune responses in mice.J Virol2013; 87:7550–7557.
  • RandallRE,YoungDF,SouthernJA.Immunization with solid matrix-antibody-antigen complexes containing surface or internal virus structural proteins protects mice from infection with the paramyxovirus, simian virus 5.J Gen Virol1988; 69:2517–2526.
  • RandallRE,YoungDF.Solid matrix-antibody-antigen complexes induce antigen-specific CD8+ cells that clear a persistent paramyxovirus infection.J Virol1991; 65:719–726.
  • XuDZ,WangXY,ShenXLet al.Results of a phase III clinical trial with an HBsAg-HBIG immunogenic complex therapeutic vaccine for chronic hepatitis B patients: experiences and findings.J Hepatol2013; 59:450–456.
  • BerzofskyJA,BensussanA,CeaseKBet al.Antigenic peptides recognized by T lymphocytes from AIDS viral envelope-immune humans.Nature1988; 334:706–708.
  • KumarR,ViscianoML,LiH,HioeC.Targeting a neutralizing epitope of HIV envelope Gp120 by immune complex vaccine.J AIDS Clin Res2012; S8:pii: 5512.
  • TsouchnikasG,ZlatkovicJ,JarmerJet al.Immunization with immune complexes modulates the fine specificity of antibody responses to a flavivirus antigen.J Virol2015; 89:7970–7978.
  • RivalC,SamyE,SetiadyY,TungK.Cutting edge: Ly49C/I(-) neonatal NK cells predispose newborns to autoimmune ovarian disease induced by maternal autoantibody.J Immunol2013; 191:2865–2869.
  • RivalC,SetiadyY,SamyET,HarakalJ,TungKS.The unique neonatal NK cells: a critical component required for neonatal autoimmune disease induction by maternal autoantibody.Front Immunol2014; 5:242.
  • WielandA,ShashidharamurthyR,KamphorstAOet al.Antibody effector functions mediated by Fcgamma-receptors are compromised during persistent viral infection.Immunity2015; 42:367–378.
  • YamadaDH,ElsaesserH,LuxAet al.Suppression of Fcgamma-receptor-mediated antibody effector function during persistent viral infection.Immunity2015; 42:379–390.
  • MoirS,FauciAS.B cells in HIV infection and disease.Nat Rev Immunol2009; 9:235–245.
  • LiuP,OvermanRG,YatesNLet al.Dynamic antibody specificities and virion concentrations in circulating immune complexes in acute to chronic HIV-1 infection.J Virol2011; 85:11196–11207.
  • RivaE,MaggiF,AbbruzzeseFet al.Immune complexed (IC) hepatitis C virus (HCV) in chronically and acutely HCV-infected patients.Med Microbiol Immunol2009; 198:13–18.
  • AcostaEG,BartenschlagerR.Paradoxical role of antibodies in dengue virus infections: considerations for prophylactic vaccine development.Expert Rev Vaccines2016; 15:467–482.
  • HalsteadSB.Dengue antibody-dependent enhancement: knowns and unknowns.Microbiol Spectr2014 doi:10.1128/microbiolspec.AID-0022-2014.
  • HalsteadSB,MahalingamS,MarovichMA,UbolS,MosserDM.Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes.Lancet Infect Dis2010; 10:712–722.
  • UbolS,HalsteadSB.How innate immune mechanisms contribute to antibody-enhanced viral infections.Clin Vaccine Immunol2010; 17:1829–1835.
  • TsaiTT,ChuangYJ,LinYSet al.Antibody-dependent enhancement infection facilitates dengue virus-regulated signaling of IL-10 production in monocytes.PLoS Negl Trop Dis2014; 8:e3320.
  • PerreauM,PantaleoG,KremerEJ.Activation of a dendritic cell-T cell axis by Ad5 immune complexes creates an improved environment for replication of HIV in T cells.J Exp Med2008; 205:2717–2725.
  • BengschB,MartinB,ThimmeR.Restoration of HBV-specific CD8+ T cell function by PD-1 blockade in inactive carrier patients is linked to T cell differentiation.J Hepatol2014; 61:1212–1219.
  • GardinerD,LalezariJ,LawitzEet al.A randomized, double-blind, placebo-controlled assessment of BMS-936558, a fully human monoclonal antibody to programmed death-1 (PD-1), in patients with chronic hepatitis C virus infection.PLoS One2013; 8:e63818.
  • SharmaP,AllisonJP.Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential.Cell2015; 161:205–214.
  • ShermanAC,TrehanpatiN,DaucherMet al.Augmentation of hepatitis B virus-specific cellular immunity with programmed death receptor-1/programmed death receptor-L1 blockade in hepatitis B virus and HIV/hepatitis B virus coinfected patients treated with adefovir.AIDS Res Hum Retroviruses2013; 29:665–672.

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