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Review

Pros and Cons of the Immunogenicity of Monoclonal Antibodies in Cancer Treatment: A Lesson from Autoimmune Diseases

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Pages 241-254 | Received 15 Jun 2018, Accepted 05 Nov 2018, Published online: 16 Jan 2019

References

  • Wofsy D . Strategies for treating autoimmune disease with monoclonal antibodies . West J. Med.143 ( 6 ), 804 – 809 ( 1985 ).
  • Osbourn J , JermutusL , DuncanA . Current methods for the generation of human antibodies for the treatment of autoimmune diseases . Drug Discov. Today.8 ( 18 ), 845 – 851 ( 2003 ).
  • Weiner LM . Fully human therapeutic monoclonal antibodies . J. Immunother.29 ( 1 ), 1 – 9 ( 2006 ).
  • Harding FA , SticklerMM , RazoJ , DuBridgeRB . The immunogenicity of humanized and fully human antibodies: residual immunogenicity resides in the CDR regions . MAbs2 ( 3 ), 256 – 265 ( 2010 ).
  • Laptoš T , OmerselJ . The importance of handling high-value biologicals: physico-chemical instability and immunogenicity of monoclonal antibodies . Exp. Ther. Med.15 ( 4 ), 3161 – 3168 ( 2018 ).
  • Yamane-Ohnuki N , SatohM . Production of therapeutic antibodies with controlled fucosylation . MAbs1 ( 3 ), 230 – 236 ( 2009 ).
  • Li W , ZhuZ , ChenW , FengY , DimitrovDS . Crystallizable fragment glycoengineering for therapeutic antibodies development . Front. Immunol.8 , 1554 ( 2017 ).
  • Homann A , RöckendorfN , KrommingaA , FreyA , JappeU . B cell epitopes on infliximab identified by oligopeptide microarray with unprocessed patient sera . J. Transl. Med.13 , 339 ( 2015 ).
  • Homann A , RöckendorfN , KrommingaA , FreyA , Platts-MillsTA , JappeU . Glycan and peptide IgE epitopes of the TNF-alpha blockers infliximab and adalimumab – precision diagnostics by cross-reactivity immune profiling of patient sera . Theranostics7 ( 19 ), 4699 – 4709 ( 2017 ).
  • Chung CH , MirakhurB , ChanEet al. Cetuximab-induced anaphylaxis and IgE specific for galactose-alpha-1,3-galactose . N. Engl. J. Med.358 ( 11 ), 1109 – 1117 ( 2008 ).
  • Lee C , JeongM , LeeJJet al. Glycosylation profile and biological activity of Remicade® compared with Flixabi® and Remsima® . MAbs9 ( 6 ), 968 – 977 ( 2017 ).
  • Liu JK . The history of monoclonal antibody development – progress, remaining challenges and future innovations . Ann. Med. Surg. (Lond.)3 ( 4 ), 113 – 116 ( 2014 ).
  • McKeage K . A review of CT-P13: an infliximab biosimilar . BioDrugs28 ( 3 ), 313 – 321 ( 2014 ).
  • Jacobs I , EwesuedoR , LulaS , ZacharchukC . Biosimilars for the treatment of cancer: a systematic review of published evidence . BioDrugs31 ( 1 ), 1 – 36 ( 2017 ).
  • Vulto AG , JaquezOA . The process defines the product: what really matters in biosimilar design and production?Rheumatology56 ( Suppl. 4 ), iv14 – iv29 ( 2017 ).
  • J⊘rgensen KK , OlsenIC , GollGLet al. NOR-SWITCH study group. Switching from originator infliximab to biosimilar CT-P13 compared with maintained treatment with originator infliximab (NOR-SWITCH): a 52-week, randomised, double-blind, non-inferiority trial . Lancet389 ( 10086 ), 2304 – 2316 ( 2017 ).
  • Glintborg B , S⊘rensenIJ , LoftAGet al. A nationwide non-medical switch from originator infliximab to biosimilar CT-P13 in 802 patients with inflammatory arthritis: 1-year clinical outcomes from the DANBIO registry . Ann. Rheum. Dis.76 ( 8 ), 1426 – 1431 ( 2017 ).
  • Ben-Horin S , YavzoriM , BenharIet al. Cross-immunogenicity: antibodies to infliximab in Remicade-treated patients with IBD similarly recognise the biosimilar Remsima . Gut65 ( 7 ), 1132 – 1138 ( 2016 ).
  • Talotta R , BerziA , DoriaAet al. The immunogenicity of branded and biosimilar infliximab in rheumatoid arthritis according to Th9-related responses . Int. J. Mol. Sci.18 ( 10 ), pii: E2127 ( 2017 ).
  • Li E , LobainaE . Application of the FDA biosimilar extrapolation framework to make off-label determinations . J. Manag. Care Spec. Pharm.23 ( 12 ), 1227 – 1232 ( 2017 ).
  • Vultaggio A , PetroniG , PratesiSet al. How the immune system responds to therapeutic biological agents . J. Int. Med. Res.44 ( 1 Suppl. ), 38 – 42 ( 2016 ).
  • Passey C , SuryawanshiS , SanghaviK , GuptaM . Reporting, visualization, and modeling of immunogenicity data to assess its impact on pharmacokinetics, efficacy, and safety of monoclonal antibodies . AAPS J.20 ( 2 ), 35 ( 2018 ).
  • Krishna M , NadlerSG . Immunogenicity to biotherapeutics - the role of anti-drug immune complexes . Front. Immunol.7 , 21 ( 2016 ).
  • Talotta R , BerziA , AtzeniFet al. Paradoxical expansion of Th1 and Th17 lymphocytes in rheumatoid arthritis following infliximab treatment: a possible explanation for a lack of clinical response . J. Clin. Immunol.35 ( 6 ), 550 – 557 ( 2015 ).
  • Talotta R , BerziA , AtzeniF , Dell’AcquaD , Sarzi PuttiniP , TrabattoniD . Evaluation of Th9 lymphocytes in peripheral blood of rheumatoid arthritis patients and correlation with anti-tumor necrosis factor therapy: results from an in vitro pivotal study . Reumatismo68 ( 2 ), 83 – 89 ( 2016 ).
  • Vultaggio A , NenciniF , PratesiSet al. ABIRISK Consortium. IL-10-producing infliximab-specific T cells regulate the antidrug T cell response in exposed patients . J. Immunol.199 ( 4 ), 1283 – 1289 ( 2017 ).
  • Torres MJ , ChavesP , DoñaIet al. T-cell involvement in delayed-type hypersensitivity reactions to infliximab . J. Allergy Clin. Immunol.128 ( 6 ), 1365 – 1367 ( 2011 ).
  • Zeltser R , ValleL , TanckC , HolystMM , RitchlinC , GaspariAA . Clinical, histological, and immunophenotypic characteristics of injection site reactions associated with etanercept: a recombinant tumor necrosis factor alpha receptor: Fc fusion protein . Arch. Dermatol.137 ( 7 ), 893 – 899 ( 2001 ).
  • Yin L , ChenX , ViciniP , RupB , HicklingTP . Therapeutic outcomes, assessments, risk factors and mitigation efforts of immunogenicity of therapeutic protein products . Cell. Immunol.295 ( 2 ), 118 – 126 ( 2015 ).
  • Jahn EM , SchneiderCK . How to systematically evaluate immunogenicity of therapeutic proteins – regulatory considerations . N. Biotechnol.25 ( 5 ), 280 – 286 ( 2009 ).
  • Aikawa NE , Freire de CarvalhoJ , SilvaCAA , BonfàE . Immunogenicity of anti-TNF-alpha agents in autoimmune diseases . Clin. Rev. Allerg. Immunol.38 , 82 – 89 ( 2010 ).
  • Finn OJ . Immuno-oncology: understanding the function and dysfunction of the immune system in cancer . Ann. Oncol.23 ( Suppl. 8 ), viii6 – viii9 ( 2012 ).
  • Passarelli A , MannavolaF , StucciLS , TucciM , SilvestrisF . Immune system and melanoma biology: a balance between immunosurveillance and immune escape . Oncotarget8 ( 62 ), 106132 – 106142 ( 2017 ).
  • Tarbell KV , EgenJG . Breaking self-tolerance during autoimmunity and cancer immunity: myeloid cells and type I IFN response regulation . J. Leukoc. Biol. doi:10.1002/JLB.3MIR1017-400R ( 2018 ) ( Epub ahead of print ).
  • Thorsson V , GibbsDL , BrownSDet al. The immune landscape of cancer . Immunity pii: S1074-7613(18)30121-3 ( 2018 ).
  • Zarour HM . Reversing T-cell dysfunction and exhaustion in cancer . Clin. Cancer Res.22 ( 8 ), 1856 – 1864 ( 2016 ).
  • Mojic M , TakedaK , HayakawaY . The dark side of IFN-γ: its role in promoting cancer immunoevasion . Int. J. Mol. Sci.19 ( 1 ), pii: E89 ( 2017 ).
  • Aras S , ZaidiMR . TAMeless traitors: macrophages in cancer progression and metastasis . Br. J. Cancer117 ( 11 ), 1583 – 1591 ( 2017 ).
  • Krstic J , TrivanovicD , JaukovicA , SantibanezJF , BugarskiD . Metabolic plasticity of stem cells and macrophages in cancer . Front. Immunol.8 , 939 ( 2017 ).
  • Yaacoub K , PedeuxR , TarteK , GuilladeuxT . Role of tumor microenvironment in regulating apoptosis and cancer progression . Cancer Lett.378 , 150 – 159 ( 2016 ).
  • Xiaojuan Liu , HyunwooKwon , ZihaiLi , Yang-xinFu . Is CD47 an innate immune checkpoint for tumor evasion?J. Hematol. Oncol.10 , 12 ( 2017 ).
  • Gurusamy D , CleverD , EilR , RestifoNP . Novel ‘elements’ of immune suppression within the tumor microenvironment . Cancer Immunol. Res.5 ( 6 ), 426 – 433 ( 2017 ).
  • Koury J , LuceroM , CatoCet al. Immunotherapies: exploiting the immune system for cancer treatment . J. Immunol. Res. published online 2018: 9585614 ( 2018 ).
  • Cuesta-Mateos C , Alcaraz-SernaA , Somovilla-CrespoB , Muñoz-CallejaC . Monoclonal antibody therapies for hematological malignancies: not just lineage-specific targets . Front. Immunol.8 , 1936 ( 2018 ).
  • Spinelli FR , ValesiniG . Immunogenicity of anti-tumour necrosis factor drugs in rheumatic diseases . Clin. Exp. Rheumatol.31 ( 6 ), 954 – 963 ( 2013 ).
  • Cassinotti A , TravisS . Incidence and clinical significance of immunogenicity to infliximab in Crohn’s disease: a critical systematic review . Inflamm. Bowel Dis.15 ( 8 ), 1264 – 1275 ( 2009 ).
  • Dunn N , JutoA , RynerMet al. Rituximab in multiple sclerosis: frequency and clinical relevance of anti-drug antibodies . Mult. Scler.24 ( 9 ), 1224 – 1233 ( 2017 ).
  • Blair HA , DugganST . Belimumab: a review in systemic lupus erythematosus . Drugs78 ( 3 ), 355 – 366 ( 2018 ).
  • Atzeni F , TalottaR , SalaffiFet al. Immunogenicity and autoimmunity during anti-TNF therapy . Autoimmun. Rev.12 ( 7 ), 703 – 708 ( 2013 ).
  • van Brummelen EM , RosW , WolbinkG , BeijnenJH , SchellensJH . Antidrug antibody formation in oncology: clinical relevance and challenges . Oncologist21 ( 10 ), 1260 – 1268 ( 2016 ).
  • Ogawa Y , OguraM , SuzukiTet al. A phase I/II study of ofatumumab (GSK1841157) in Japanese and Korean patients with relapsed or refractory B-cell chronic lymphocytic leukemia . Int. J. Hematol.98 ( 2 ), 164 – 170 ( 2013 ).
  • Czuczman MS , FayadL , DelwailVet al. 405 Study Investigators. Ofatumumab monotherapy in rituximab-refractory follicular lymphoma: results from a multicenter study . Blood119 ( 16 ), 3698 – 3704 ( 2012 ).
  • A Phase 1 safety, pharmacokinetic and pharmacodynamic study of the Anti-A5B1 integrin monoclonal antibody PF-04605412 administered intravenously to adult patients with advanced or metastatic solid tumors . ClinicalTrials.gov Identifier: NCT00915278 .
  • Li G , ZhangL , ChenEet al. Dual functional monoclonal antibody PF-04605412 targets integrin alpha5beta1 and elicits potent antibody-dependent cellular cytotoxicity . Cancer Res.70 ( 24 ), 10243 – 10254 ( 2010 ).
  • Yoshino T , YamazakiK , GotohMet al. Safety and pharmacokinetics of second-line ramucirumab plus FOLFIRI in Japanese patients with metastatic colorectal carcinoma . Anticancer Res.35 ( 7 ), 4003 – 4007 ( 2015 ).
  • Mok CC . Rituximab for the treatment of rheumatoid arthritis: an update . Drug Des. Devel. Ther.8 , 87 – 100 ( 2013 ).
  • Sedykh SE , PrinzVV , BunevaVN , NevinskyGA . Bispecific antibodies: design, therapy, perspectives . Drug Des. Devel. Ther.12 , 195 – 208 ( 2018 ).
  • Ott MG , MarméF , MoldenhauerGet al. Humoral response to catumaxomab correlates with clinical outcome: results of the pivotal Phase II/III study in patients with malignant ascites . Int. J. Cancer130 ( 9 ), 2195 – 203 ( 2012 ).
  • Firer MA , GellermanG . Targeted drug delivery for cancer therapy: the other side of antibodies . J. Hematol. Oncol.5 , 70 ( 2012 ).
  • Mazor R , OndaM , PastanI . Immunogenicity of therapeutic recombinant immunotoxins . Immunol. Rev.270 ( 1 ), 152 – 164 ( 2016 ).
  • Jordaan S , AkinrinmadeOA , NachreinerTet al. Updates in the development of immunoRNases for the selective killing of tumor cells . Biomedicines6 ( 1 ), pii: E28 ( 2018 ).
  • Bannas P , HambachJ , Koch-NolteF . Nanobodies and nanobody-based human heavy chain antibodies as antitumor therapeutics . Front. Immunol.8 , 1603 ( 2017 ).
  • Gallo P , GonçalvesR , MosserDM . The influence of IgG density and macrophage Fc (gamma) receptor cross-linking on phagocytosis and IL-10 production . Immunol. Lett.133 ( 2 ), 70 – 77 ( 2010 ).
  • Kovaleva M , JohnsonK , StevenJ , BarelleCJ , PorterA . Therapeutic potential of shark anti-ICOSL VNAR domains is exemplified in a murine model of autoimmune non-infectious uveitis . Front. Immunol.8 , 1121 ( 2017 ).
  • Iezzi ME , PolicastroL , WerbajhS , PodhajcerO , CanzianiGA . Single-domain antibodies and the promise of modular targeting in cancer imaging and treatment . Front. Immunol.9 , 273 ( 2018 ).
  • Finco D , GrimaldiC , FortMet al. Cytokine release assays: current practices and future directions . Cytokine66 ( 2 ), 143 – 155 ( 2014 ).
  • Brennan FR , KiesslingA . Translational immunotoxicology of immunomodulatory monoclonal antibodies . Drug Discov. Today Technol.21–22 , 85 – 93 ( 2016 ).
  • Hünig T . The rise and fall of the CD28 superagonist TGN1412 and its return as TAB08: a personal account . FEBS J.283 ( 18 ), 3325 – 3334 ( 2016 ).
  • Peipp M , van de WinkelJG , ValeriusT . Molecular engineering to improve antibodies’ anti-lymphoma activity . Best Pract. Res. Clin. Haematol.24 ( 2 ), 217 – 229 ( 2011 ).
  • Pereira NA , ChanKF , LinPC , SongZ . The ‘less-is-more’ in therapeutic antibodies: afucosylated anti-cancer antibodies with enhanced antibody-dependent cellular cytotoxicity . MAbs10 ( 5 ), 693 – 711 ( 2018 ).
  • Idusogie EE , WongPY , PrestaLGet al. Engineered antibodies with increased activity to recruit complement . J. Immunol.166 , 2571 – 2575 ( 2001 ).
  • Kuriakose A , ChirmuleN , NairP . Immunogenicity of biotherapeutics: causes and association with posttranslational modifications . J. Immunol. Res.2016 , 1298473 ( 2016 ).
  • Everds NE , TarrantJM . Unexpected hematologic effects of biotherapeutics in nonclinical species and in humans . Toxicol. Pathol.41 ( 2 ), 280 – 302 ( 2013 ).
  • Kronenberg S , HusarE , SchubertCet al. Comparative assessment of immune complex-mediated hypersensitivity reactions with biotherapeutics in the non-human primate: critical parameters, safety and lessons for future studies . Regul. Toxicol. Pharmacol.88 , 125 – 137 ( 2017 ).
  • Todoric J , AntonucciL , KarinM . Targeting inflammation in cancer prevention and therapy . Cancer Prev. Res. (Phila).9 ( 12 ), 895 – 905 ( 2016 ).
  • Dhanji S , TseK , TehHS . The low affinity Fc receptor for IgG functions as an effective cytolytic receptor for self-specific CD8 T cells . J. Immunol.174 ( 3 ), 1253 – 1258 ( 2005 ).
  • Krishnan S , WarkeVG , NambiarMP , TsokosGC , FarberDL . The FcR gamma subunit and Syk kinase replace the CD3 zeta-chain and ZAP-70 kinase in the TCR signaling complex of human effector CD4 T cells . J. Immunol.170 ( 8 ), 4189 – 4195 ( 2003 ).
  • Asadzadeh Z , MohammadiH , SafarzadehEet al. The paradox of Th17 cell functions in tumor immunity . Cell. Immunol.322 , 15 – 25 ( 2017 ).
  • Nedoszytko B , Sokołowska-WojdyłoM , RenkeJet al. The role of regulatory T cells and genes involved in their differentiation in pathogenesis of selected inflammatory and neoplastic skin diseases . Part III: Polymorphisms of Genes Involved in Tregs’ Activation and Function. Postepy Dermatol Alergol . 34 ( 6 ), 517 – 525 ( 2017 ).
  • Romagnoli G , WiedermannM , HübnerFet al. Morphological evaluation of tumor-infiltrating lymphocytes (TILs) to investigate invasive breast cancer immunogenicity, reveal lymphocytic networks and help relapse prediction: a retrospective study . Int. J. Mol. Sci.18 ( 9 ), pii: E1936 ( 2017 ).
  • Benedetti R , Dell’AversanaC , GiorgioC , AstorriR , AltucciL . Breast cancer vaccines: new insights . Front. Endocrinol. (Lausanne)8 , 270 ( 2017 ).
  • Angelova AL , BarfM , GeletnekyK , UnterbergA , RommelaereJ . Immunotherapeutic potential of oncolytic H-1 parvovirus: hints of glioblastoma microenvironment conversion towards immunogenicity . Viruses9 ( 12 ), pii: E382 ( 2017 ).

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