. 2017 Oct; 8:1245.
doi: 10.3389/fimmu.2017.01245.

Therapeutic Antibodies: What Have We Learnt from Targeting CD20 and Where Are We Going?

Michael J E Marshall 1 Richard J Stopforth 1 Mark S Cragg 1 
  • PMID: 29046676
  •     245 References
  •     52 citations


Therapeutic monoclonal antibodies (mAbs) have become one of the fastest growing classes of drugs in recent years and are approved for the treatment of a wide range of indications, from cancer to autoimmune disease. Perhaps the best studied target is the pan B-cell marker CD20. Indeed, the first mAb to receive approval by the Food and Drug Administration for use in cancer treatment was the CD20-targeting mAb rituximab (Rituxan®). Since its approval for relapsed/refractory non-Hodgkin's lymphoma in 1997, rituximab has been licensed for use in the treatment of numerous other B-cell malignancies, as well as autoimmune conditions, including rheumatoid arthritis. Despite having a significant impact on the treatment of these patients, the exact mechanisms of action of rituximab remain incompletely understood. Nevertheless, numerous second- and third-generation anti-CD20 mAbs have since been developed using various strategies to enhance specific effector functions thought to be key for efficacy. A plethora of knowledge has been gained during the development and testing of these mAbs, and this knowledge can now be applied to the design of novel mAbs directed to targets beyond CD20. As we enter the "post-rituximab" era, this review will focus on the lessons learned thus far through investigation of anti-CD20 mAb. Also discussed are current and future developments relating to enhanced effector function, such as the ability to form multimers on the target cell surface. These strategies have potential applications not only in oncology but also in the improved treatment of autoimmune disorders and infectious diseases. Finally, potential approaches to overcoming mechanisms of resistance to anti-CD20 therapy are discussed, chiefly involving the combination of anti-CD20 mAbs with various other agents to resensitize patients to treatment.

Keywords: Fc engineering; Fc gamma receptors; anti-CD20; combination therapies; isotype; monoclonal antibody; resistance.

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Federico Alberici, Rona M Smith, +19 authors, David R W Jayne.
J Allergy Clin Immunol, 2016 Oct 27; 139(5). PMID: 27780742
Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer.
José Baselga, Javier Cortés, +12 authors, CLEOPATRA Study Group.
N Engl J Med, 2011 Dec 14; 366(2). PMID: 22149875    Free PMC article.
Highly Cited.
Antagonistic human FcγRIIB (CD32B) antibodies have anti-tumor activity and overcome resistance to antibody therapy in vivo.
Ali Roghanian, Ingrid Teige, +29 authors, Mark S Cragg.
Cancer Cell, 2015 Apr 16; 27(4). PMID: 25873171
Optimization of antibody binding to FcgammaRIIa enhances macrophage phagocytosis of tumor cells.
John O Richards, Sher Karki, +3 authors, John R Desjarlais.
Mol Cancer Ther, 2008 Aug 30; 7(8). PMID: 18723496
Alemtuzumab compared with chlorambucil as first-line therapy for chronic lymphocytic leukemia.
Peter Hillmen, Aleksander B Skotnicki, +5 authors, Jiri Mayer.
J Clin Oncol, 2007 Nov 07; 25(35). PMID: 17984186
Highly Cited.
Trastuzumab in the Treatment of Breast Cancer.
Sofia Maximiano, Paulo Magalhães, Mara Pereira Guerreiro, Manuel Morgado.
BioDrugs, 2016 Feb 20; 30(2). PMID: 26892619
Structural analysis of Fc/FcγR complexes: a blueprint for antibody design.
Jose M M Caaveiro, Masato Kiyoshi, Kouhei Tsumoto.
Immunol Rev, 2015 Oct 27; 268(1). PMID: 26497522
An acquired defect in IgG-dependent phagocytosis explains the impairment in antibody-mediated cellular depletion in Lupus.
Anupama Ahuja, Lino L Teichmann, +3 authors, Mark J Shlomchik.
J Immunol, 2011 Aug 30; 187(7). PMID: 21873531    Free PMC article.
Complement-mediated lysis by anti-CD20 mAb correlates with segregation into lipid rafts.
Mark S Cragg, Suzanne M Morgan, +5 authors, Martin J Glennie.
Blood, 2002 Oct 24; 101(3). PMID: 12393541
Trastuzumab emtansine versus treatment of physician's choice for pretreated HER2-positive advanced breast cancer (TH3RESA): a randomised, open-label, phase 3 trial.
Ian E Krop, Sung-Bae Kim, +7 authors, TH3RESA study collaborators.
Lancet Oncol, 2014 May 06; 15(7). PMID: 24793816
Highly Cited.
Construction and characterization of a bispecific anti-CD20 antibody with potent antitumor activity against B-cell lymphoma.
Bohua Li, Xunming Zhang, +7 authors, Yajun Guo.
Cancer Res, 2010 Jul 16; 70(15). PMID: 20631068
Internalization of rituximab and the efficiency of B Cell depletion in rheumatoid arthritis and systemic lupus erythematosus.
Venkat Reddy, Geraldine Cambridge, +3 authors, Maria Leandro.
Arthritis Rheumatol, 2015 Apr 29; 67(8). PMID: 25916583    Free PMC article.
Obinutuzumab plus chlorambucil in patients with CLL and coexisting conditions.
Valentin Goede, Kirsten Fischer, +20 authors, Michael Hallek.
N Engl J Med, 2014 Jan 10; 370(12). PMID: 24401022
Highly Cited.
Fc optimization of therapeutic antibodies enhances their ability to kill tumor cells in vitro and controls tumor expansion in vivo via low-affinity activating Fcgamma receptors.
Jeffrey B Stavenhagen, Sergey Gorlatov, +8 authors, Scott Koenig.
Cancer Res, 2007 Sep 19; 67(18). PMID: 17875730
Veltuzumab, an anti-CD20 mAb for the treatment of non-Hodgkin's lymphoma, chronic lymphocytic leukemia and immune thrombocytopenic purpura.
Cannon Milani, Jorge Castillo.
Curr Opin Mol Ther, 2009 Mar 31; 11(2). PMID: 19330725
High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R.
R L Shields, A K Namenuk, +9 authors, L G Presta.
J Biol Chem, 2000 Nov 30; 276(9). PMID: 11096108
Highly Cited.
Use of 90Y-ibritumomab tiuxetan in non-Hodgkin's lymphoma.
Robert Marcus.
Semin Oncol, 2005 Mar 24; 32(1 Suppl 1). PMID: 15786024
Depletion of the C3 component of complement enhances the ability of rituximab-coated target cells to activate human NK cells and improves the efficacy of monoclonal antibody therapy in an in vivo model.
Siao-Yi Wang, Suresh Veeramani, +5 authors, George J Weiner.
Blood, 2009 Oct 07; 114(26). PMID: 19805620    Free PMC article.
Differential Fc-Receptor Engagement Drives an Anti-tumor Vaccinal Effect.
David J DiLillo, Jeffrey V Ravetch.
Cell, 2015 May 16; 161(5). PMID: 25976835    Free PMC article.
Highly Cited.
Chronic lymphocytic leukaemia cells are efficiently killed by an anti-CD20 monoclonal antibody selected for improved engagement of FcgammaRIIIA/CD16.
Christophe de Romeuf, Charles-Antoine Dutertre, +13 authors, Hélène Merle-Béral.
Br J Haematol, 2008 Feb 28; 140(6). PMID: 18302712
Ocaratuzumab, an Fc-engineered antibody demonstrates enhanced antibody-dependent cell-mediated cytotoxicity in chronic lymphocytic leukemia.
Carolyn M Cheney, Deborah M Stephens, +10 authors, John C Byrd.
MAbs, 2014 Mar 07; 6(3). PMID: 24594909    Free PMC article.
Antigenic modulation limits the efficacy of anti-CD20 antibodies: implications for antibody selection.
Stephen A Beers, Ruth R French, +13 authors, Mark S Cragg.
Blood, 2010 Mar 13; 115(25). PMID: 20223920
Highly Cited.
Long-term outcome of patients in the LNH-98.5 trial, the first randomized study comparing rituximab-CHOP to standard CHOP chemotherapy in DLBCL patients: a study by the Groupe d'Etudes des Lymphomes de l'Adulte.
Bertrand Coiffier, Catherine Thieblemont, +11 authors, Hervé Tilly.
Blood, 2010 Jun 16; 116(12). PMID: 20548096    Free PMC article.
Highly Cited.
NK-cell activation and antibody-dependent cellular cytotoxicity induced by rituximab-coated target cells is inhibited by the C3b component of complement.
Siao-Yi Wang, Emilian Racila, Ronald P Taylor, George J Weiner.
Blood, 2007 Nov 21; 111(3). PMID: 18024795    Free PMC article.
The IgG Fc contains distinct Fc receptor (FcR) binding sites: the leukocyte receptors Fc gamma RI and Fc gamma RIIa bind to a region in the Fc distinct from that recognized by neonatal FcR and protein A.
B D Wines, M S Powell, +2 authors, P M Hogarth.
J Immunol, 2000 May 09; 164(10). PMID: 10799893
The novel tribody [(CD20)(2)xCD16] efficiently triggers effector cell-mediated lysis of malignant B cells.
P Glorius, A Baerenwaldt, +12 authors, M Peipp.
Leukemia, 2012 Jun 05; 27(1). PMID: 22660187
Olaratumab: First Global Approval.
Matt Shirley.
Drugs, 2016 Dec 21; 77(1). PMID: 27995580
Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity.
S Krapp, Y Mimura, +2 authors, P Sondermann.
J Mol Biol, 2003 Jan 16; 325(5). PMID: 12527303
Highly Cited.
Antibodies to watch in 2017.
Janice M Reichert.
MAbs, 2016 Dec 15; 9(2). PMID: 27960628    Free PMC article.
Highly Cited.
FcγR dependent mechanisms of cytotoxic, agonistic, and neutralizing antibody activities.
Falk Nimmerjahn, Sina Gordan, Anja Lux.
Trends Immunol, 2015 May 20; 36(6). PMID: 25981969
Highly Cited. Review.
Antibody effector functions mediated by Fcγ-receptors are compromised during persistent viral infection.
Andreas Wieland, Rangaiah Shashidharamurthy, +9 authors, Rafi Ahmed.
Immunity, 2015 Feb 15; 42(2). PMID: 25680276    Free PMC article.
Complement activation determines the therapeutic activity of rituximab in vivo.
Nicola Di Gaetano, Elena Cittera, +6 authors, Josée Golay.
J Immunol, 2003 Jul 23; 171(3). PMID: 12874252
Highly Cited.
Activating Fc γ receptors contribute to the antitumor activities of immunoregulatory receptor-targeting antibodies.
Yannick Bulliard, Rose Jolicoeur, +6 authors, Jennifer L Brogdon.
J Exp Med, 2013 Jul 31; 210(9). PMID: 23897982    Free PMC article.
Highly Cited.
Phase I clinical study of pertuzumab, a novel HER dimerization inhibitor, in patients with advanced cancer.
David B Agus, Michael S Gordon, +9 authors, Gwen Fyfe.
J Clin Oncol, 2005 Feb 09; 23(11). PMID: 15699478
Effective phagocytosis of low Her2 tumor cell lines with engineered, aglycosylated IgG displaying high FcγRIIa affinity and selectivity.
Sang Taek Jung, William Kelton, +5 authors, George Georgiou.
ACS Chem Biol, 2012 Oct 04; 8(2). PMID: 23030766
Combined glyco- and protein-Fc engineering simultaneously enhance cytotoxicity and half-life of a therapeutic antibody.
Céline Monnet, Sylvie Jorieux, +10 authors, Alexandre Fontayne.
MAbs, 2014 Feb 05; 6(2). PMID: 24492301    Free PMC article.
The discovery and development of brentuximab vedotin for use in relapsed Hodgkin lymphoma and systemic anaplastic large cell lymphoma.
Peter D Senter, Eric L Sievers.
Nat Biotechnol, 2012 Jul 12; 30(7). PMID: 22781692
Highly Cited.
Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cell-mediated B-cell cytotoxicity.
Ekkehard Mössner, Peter Brünker, +22 authors, Pablo Umaña.
Blood, 2010 Mar 03; 115(22). PMID: 20194898    Free PMC article.
Highly Cited.
FcR gamma chain deletion results in pleiotrophic effector cell defects.
T Takai, M Li, +2 authors, J V Ravetch.
Cell, 1994 Feb 11; 76(3). PMID: 8313472
Highly Cited.
OX40 engagement depletes intratumoral Tregs via activating FcγRs, leading to antitumor efficacy.
Yannick Bulliard, Rose Jolicoeur, +3 authors, Jennifer L Brogdon.
Immunol Cell Biol, 2014 Apr 16; 92(6). PMID: 24732076
Highly Cited.
Immune complex-mediated antigen presentation induces tumor immunity.
Khadija Rafiq, Amy Bergtold, Raphael Clynes.
J Clin Invest, 2002 Jul 03; 110(1). PMID: 12093890    Free PMC article.
Development and Characterization of Monoclonal Antibodies Specific for Mouse and Human Fcγ Receptors.
Alison L Tutt, Sonya James, +24 authors, Mark S Cragg.
J Immunol, 2015 Oct 30; 195(11). PMID: 26512139
Fc Engineering to Improve the Function of Therapeutic Antibodies.
Futa Mimoto, Taichi Kuramochi, +2 authors, Kunihiro Hattori.
Curr Pharm Biotechnol, 2016 Aug 25; 17(15). PMID: 27552846
Novel antibodies targeting immune regulatory checkpoints for cancer therapy.
Chern Siang Lee, Mark Cragg, Martin Glennie, Peter Johnson.
Br J Clin Pharmacol, 2013 May 25; 76(2). PMID: 23701301    Free PMC article.
Cutting Edge: IgE Plays an Active Role in Tumor Immunosurveillance in Mice.
Elisa A Nigro, Anna T Brini, +9 authors, Luca Vangelista.
J Immunol, 2016 Aug 28; 197(7). PMID: 27566822
Safety and activity of PD1 blockade by pidilizumab in combination with rituximab in patients with relapsed follicular lymphoma: a single group, open-label, phase 2 trial.
Jason R Westin, Fuliang Chu, +19 authors, Sattva S Neelapu.
Lancet Oncol, 2013 Dec 18; 15(1). PMID: 24332512    Free PMC article.
Highly Cited.
Immunotherapy with FBTA05 (Bi20), a trifunctional bispecific anti-CD3 x anti-CD20 antibody and donor lymphocyte infusion (DLI) in relapsed or refractory B-cell lymphoma after allogeneic stem cell transplantation: study protocol of an investigator-driven, open-label, non-randomized, uncontrolled, dose-escalating Phase I/II-trial.
Raymund Buhmann, Stanglmaier Michael, +3 authors, Hans-Jochem Kolb.
J Transl Med, 2013 Jul 03; 11. PMID: 23815981    Free PMC article.
Antibody Distance from the Cell Membrane Regulates Antibody Effector Mechanisms.
Kirstie L S Cleary, H T Claude Chan, +2 authors, Mark S Cragg.
J Immunol, 2017 Apr 14; 198(10). PMID: 28404636    Free PMC article.
Off-label use of rituximab for systemic lupus erythematosus in Europe.
Monica Rydén-Aulin, Dimitrios Boumpas, +30 authors, Ronald van Vollenhoven.
Lupus Sci Med, 2016 Sep 22; 3(1). PMID: 27651920    Free PMC article.
Antibody-Dependent Phagocytosis of Tumor Cells by Macrophages: A Potent Effector Mechanism of Monoclonal Antibody Therapy of Cancer.
Nuray Gül, Marjolein van Egmond.
Cancer Res, 2015 Nov 18; 75(23). PMID: 26573795
Obinutuzumab induces superior B-cell cytotoxicity to rituximab in rheumatoid arthritis and systemic lupus erythematosus patient samples.
Venkat Reddy, Christian Klein, +4 authors, Maria J Leandro.
Rheumatology (Oxford), 2017 Apr 14; 56(7). PMID: 28407142    Free PMC article.
Engineered antibodies of IgG1/IgG3 mixed isotype with enhanced cytotoxic activities.
Akito Natsume, Mika In, +8 authors, Rinpei Niwa.
Cancer Res, 2008 May 17; 68(10). PMID: 18483271
Rituximab therapy in hematologic malignancy patients with circulating blood tumor cells: association with increased infusion-related side effects and rapid blood tumor clearance.
J C Byrd, J K Waselenko, +6 authors, C A White.
J Clin Oncol, 1999 Mar 10; 17(3). PMID: 10071268
Inducing tumor immunity through the selective engagement of activating Fcgamma receptors on dendritic cells.
Alexis M Kalergis, Jeffrey V Ravetch.
J Exp Med, 2002 Jun 19; 195(12). PMID: 12070293    Free PMC article.
Highly Cited.
CD20 as a target for therapeutic type I and II monoclonal antibodies.
Stephen A Beers, Claude H T Chan, +2 authors, Martin J Glennie.
Semin Hematol, 2010 Mar 31; 47(2). PMID: 20350657
PI3Kδ inhibition elicits anti-leukemic effects through Bim-dependent apoptosis.
M J Carter, K L Cox, +7 authors, M S Cragg.
Leukemia, 2016 Nov 16; 31(6). PMID: 27843137    Free PMC article.
Rituximab infusion promotes rapid complement depletion and acute CD20 loss in chronic lymphocytic leukemia.
Adam D Kennedy, Paul V Beum, +6 authors, Ronald P Taylor.
J Immunol, 2004 Feb 24; 172(5). PMID: 14978136
Necitumumab, a fully human IgG1 mAb directed against the EGFR for the potential treatment of cancer.
Rodrigo Dienstmann, Josep Tabernero.
Curr Opin Investig Drugs, 2010 Dec 15; 11(12). PMID: 21154125
Combination of ibrutinib with rituximab, cyclophosphamide, doxorubicin, vincristine, and prednisone (R-CHOP) for treatment-naive patients with CD20-positive B-cell non-Hodgkin lymphoma: a non-randomised, phase 1b study.
Anas Younes, Catherine Thieblemont, +13 authors, Yasuhiro Oki.
Lancet Oncol, 2014 Jul 22; 15(9). PMID: 25042202
Highly Cited.
A review of rituximab, the first anti-CD20 monoclonal antibody used in the treatment of B non-Hodgkin's lymphomas.
Pierre Feugier.
Future Oncol, 2015 May 09; 11(9). PMID: 25952779
Modulation of immune complex-induced inflammation in vivo by the coordinate expression of activation and inhibitory Fc receptors.
R Clynes, J S Maizes, +3 authors, J V Ravetch.
J Exp Med, 1999 Jan 05; 189(1). PMID: 9874574    Free PMC article.
Highly Cited.
B-cell subpopulations in humans and their differential susceptibility to depletion with anti-CD20 monoclonal antibodies.
Maria J Leandro.
Arthritis Res Ther, 2013 Apr 10; 15 Suppl 1. PMID: 23566754    Free PMC article.
Levels of expression of CD19 and CD20 in chronic B cell leukaemias.
L Ginaldi, M De Martinis, +3 authors, D Catovsky.
J Clin Pathol, 1998 Aug 26; 51(5). PMID: 9708202    Free PMC article.
Glycoengineered CD20 antibody obinutuzumab activates neutrophils and mediates phagocytosis through CD16B more efficiently than rituximab.
Josée Golay, Fabio Da Roit, +5 authors, Martino Introna.
Blood, 2013 Oct 10; 122(20). PMID: 24106207
Highly Cited.
Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells.
Yohei Iwata, Takashi Matsushita, +10 authors, Thomas F Tedder.
Blood, 2010 Oct 22; 117(2). PMID: 20962324    Free PMC article.
Highly Cited.
Highly sensitive B cell analysis predicts response to rituximab therapy in rheumatoid arthritis.
Shouvik Dass, Andy C Rawstron, +3 authors, Paul Emery.
Arthritis Rheum, 2008 Sep 30; 58(10). PMID: 18821683
Clinical outcome of patients with follicular lymphoma receiving chemoimmunotherapy in the PRIMA study is not affected by FCGR3A and FCGR2A polymorphisms.
Hervé Ghesquières, Guillaume Cartron, +15 authors, Gilles Salles.
Blood, 2012 Aug 14; 120(13). PMID: 22885164
Brentuximab vedotin (SGN-35) for relapsed CD30-positive lymphomas.
Anas Younes, Nancy L Bartlett, +4 authors, Andres Forero-Torres.
N Engl J Med, 2010 Nov 05; 363(19). PMID: 21047225
Highly Cited.
Induction of cytosolic calcium flux by CD20 is dependent upon B Cell antigen receptor signaling.
Claire A Walshe, Stephen A Beers, +5 authors, Mark S Cragg.
J Biol Chem, 2008 Apr 23; 283(25). PMID: 18426802
Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2.
D J Slamon, B Leyland-Jones, +9 authors, L Norton.
N Engl J Med, 2001 Mar 15; 344(11). PMID: 11248153
Highly Cited.
A Novel Platform for the Potentiation of Therapeutic Antibodies Based on Antigen-Dependent Formation of IgG Hexamers at the Cell Surface.
Rob N de Jong, Frank J Beurskens, +10 authors, Paul W H I Parren.
PLoS Biol, 2016 Jan 07; 14(1). PMID: 26736041    Free PMC article.
Highly Cited.
Lymphocyte numbers and subsets in the human blood. Do they mirror the situation in all organs?
Katrin S Blum, Reinhard Pabst.
Immunol Lett, 2006 Nov 30; 108(1). PMID: 17129612
Metabolic properties of human IgA subclasses.
A Morell, F Skvaril, G Noseda, S Barandun.
Clin Exp Immunol, 1973 Apr 01; 13(4). PMID: 4717094    Free PMC article.
Lipid rafts and B cell signaling.
Neetu Gupta, Anthony L DeFranco.
Semin Cell Dev Biol, 2007 Aug 28; 18(5). PMID: 17719248    Free PMC article.
Lymphoma depletion during CD20 immunotherapy in mice is mediated by macrophage FcgammaRI, FcgammaRIII, and FcgammaRIV.
Veronique Minard-Colin, Yan Xiu, +5 authors, Thomas F Tedder.
Blood, 2008 May 23; 112(4). PMID: 18495955    Free PMC article.
Genetic and Epigenetic Modulation of CD20 Expression in B-Cell Malignancies: Molecular Mechanisms and Significance to Rituximab Resistance.
Akihiro Tomita.
J Clin Exp Hematop, 2016 Dec 17; 56(2). PMID: 27980307    Free PMC article.
Comparison of the effector functions of human immunoglobulins using a matched set of chimeric antibodies.
M Brüggemann, G T Williams, +5 authors, M S Neuberger.
J Exp Med, 1987 Nov 01; 166(5). PMID: 3500259    Free PMC article.
Highly Cited.
The Tumor Microenvironment Regulates CD19 and CD20 Immunotherapy for Lymphoma.
Jacquelyn M Lykken, Thomas F Tedder.
Cancer J, 2015 Jul 30; 21(4). PMID: 26222089
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Inmoo Rhee.
Arch Pharm Res, 2016 Aug 27; 39(11). PMID: 27562774
Highly Cited. Review.
Daratumumab monotherapy in patients with treatment-refractory multiple myeloma (SIRIUS): an open-label, randomised, phase 2 trial.
Sagar Lonial, Brendan M Weiss, +29 authors, Peter M Voorhees.
Lancet, 2016 Jan 19; 387(10027). PMID: 26778538
Highly Cited.
Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer.
Antonino Musolino, Nadia Naldi, +9 authors, Andrea Ardizzoni.
J Clin Oncol, 2008 Mar 19; 26(11). PMID: 18347005
Highly Cited.
Efficient complement-mediated lysis of cells containing the CAMPATH-1 (CDw52) antigen.
M Q Xia, G Hale, H Waldmann.
Mol Immunol, 1993 Aug 01; 30(12). PMID: 8366859
Expression of complement inhibitors CD46, CD55, and CD59 on tumor cells does not predict clinical outcome after rituximab treatment in follicular non-Hodgkin lymphoma.
W K Weng, R Levy.
Blood, 2001 Aug 25; 98(5). PMID: 11520782
Preclinical systemic lupus erythematosus.
Julie M Robertson, Judith A James.
Rheum Dis Clin North Am, 2014 Dec 02; 40(4). PMID: 25437281    Free PMC article.
Myeloid cells as effector cells for monoclonal antibody therapy of cancer.
Rens Braster, Tom O'Toole, Marjolein van Egmond.
Methods, 2013 Jul 03; 65(1). PMID: 23811299
Efficacy and safety of idelalisib in patients with relapsed, rituximab- and alkylating agent-refractory follicular lymphoma: a subgroup analysis of a phase 2 study.
Gilles Salles, Stephen J Schuster, +15 authors, Ajay K Gopal.
Haematologica, 2016 Dec 17; 102(4). PMID: 27979923    Free PMC article.
Idelalisib and rituximab in relapsed chronic lymphocytic leukemia.
Richard R Furman, Jeff P Sharman, +24 authors, Susan M O'Brien.
N Engl J Med, 2014 Jan 24; 370(11). PMID: 24450857    Free PMC article.
Highly Cited.
CAL-101, a p110delta selective phosphatidylinositol-3-kinase inhibitor for the treatment of B-cell malignancies, inhibits PI3K signaling and cellular viability.
Brian J Lannutti, Sarah A Meadows, +11 authors, Neill A Giese.
Blood, 2010 Oct 21; 117(2). PMID: 20959606    Free PMC article.
Highly Cited.
Immunotherapy with the trifunctional anti-CD20 x anti-CD3 antibody FBTA05 (Lymphomun) in paediatric high-risk patients with recurrent CD20-positive B cell malignancies.
Friedhelm R Schuster, Michael Stanglmaier, +8 authors, Raymund Buhmann.
Br J Haematol, 2014 Dec 17; 169(1). PMID: 25495919
Rapid redistribution of CD20 to a low density detergent-insoluble membrane compartment.
J P Deans, S M Robbins, M J Polyak, J A Savage.
J Biol Chem, 1998 Feb 07; 273(1). PMID: 9417086
CD20-induced lymphoma cell death is independent of both caspases and its redistribution into triton X-100 insoluble membrane rafts.
H T Claude Chan, David Hughes, +5 authors, Mark S Cragg.
Cancer Res, 2003 Sep 23; 63(17). PMID: 14500384
Enhancement of antibody-dependent cell-mediated cytotoxicity by endowing IgG with FcαRI (CD89) binding.
M Jack Borrok, Nadia M Luheshi, +5 authors, Ping Tsui.
MAbs, 2015 May 15; 7(4). PMID: 25970007    Free PMC article.
Homozygous A polymorphism of the complement C1qA276 correlates with prolonged overall survival in patients with diffuse large B cell lymphoma treated with R-CHOP.
Xuan Jin, Huirong Ding, +3 authors, Jun Zhu.
J Hematol Oncol, 2012 Aug 18; 5. PMID: 22897949    Free PMC article.
Mouse CD20 expression and function.
Junji Uchida, Youngkyun Lee, +8 authors, Thomas F Tedder.
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Fc gamma Rs modulate cytotoxicity of anti-Fas antibodies: implications for agonistic antibody-based therapeutics.
Yuanyuan Xu, Alexander J Szalai, +5 authors, Robert P Kimberly.
J Immunol, 2003 Jul 09; 171(2). PMID: 12847219
CD20: a regulator of cell-cycle progression of B lymphocytes.
T F Tedder, P Engel.
Immunol Today, 1994 Sep 01; 15(9). PMID: 7524522
Highly Cited. Review.
Fc Engineering for Developing Therapeutic Bispecific Antibodies and Novel Scaffolds.
Hongyan Liu, Abhishek Saxena, Sachdev S Sidhu, Donghui Wu.
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Panitumumab: a new anti-EGFR antibody for the treatment of advanced colorectal cancer.
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The PI3K pathway: clinical inhibition in chronic lymphocytic leukemia.
Jennifer R Brown.
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Idelalisib given front-line for treatment of chronic lymphocytic leukemia causes frequent immune-mediated hepatotoxicity.
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Highly Cited.
Dinutuximab: A Review in High-Risk Neuroblastoma.
Sheridan M Hoy.
Target Oncol, 2016 Feb 20; 11(2). PMID: 26891967
CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma.
Bertrand Coiffier, Eric Lepage, +10 authors, Christian Gisselbrecht.
N Engl J Med, 2002 Jan 25; 346(4). PMID: 11807147
Highly Cited.
The immunopathogenesis of seropositive rheumatoid arthritis: from triggering to targeting.
Vivianne Malmström, Anca I Catrina, Lars Klareskog.
Nat Rev Immunol, 2016 Dec 06; 17(1). PMID: 27916980
Highly Cited. Review.
Type I CD20 Antibodies Recruit the B Cell Receptor for Complement-Dependent Lysis of Malignant B Cells.
Patrick J Engelberts, Marleen Voorhorst, +10 authors, Frank J Beurskens.
J Immunol, 2016 Nov 04; 197(12). PMID: 27807190
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S E Degn, S Thiel.
Scand J Immunol, 2013 May 16; 78(2). PMID: 23672641
Safety and activity of lenalidomide and rituximab in untreated indolent lymphoma: an open-label, phase 2 trial.
Nathan H Fowler, R Eric Davis, +20 authors, Sattva S Neelapu.
Lancet Oncol, 2014 Dec 03; 15(12). PMID: 25439689    Free PMC article.
Highly Cited.
Differential sensitivity of CD4+ and CD8+ T lymphocytes to the killing efficacy of Fas (Apo-1/CD95) ligand+ tumor cells in B chronic lymphocytic leukemia.
I Tinhofer, I Marschitz, +4 authors, R Greil.
Blood, 1998 May 30; 91(11). PMID: 9596676
Simultaneous exposure to FcγR and FcαR on monocytes and macrophages enhances antitumor activity in vivo.
Bingyu Li, Lijun Xu, +10 authors, Jianmin Fang.
Oncotarget, 2017 Apr 30; 8(24). PMID: 28454118    Free PMC article.
Rituximab: a review of its use in chronic lymphocytic leukaemia, low-grade or follicular lymphoma and diffuse large B-cell lymphoma.
Gillian M Keating.
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Using the allergic immune system to target cancer: activity of IgE antibodies specific for human CD20 and MUC1.
Pearline Zhaoying Teo, Paul J Utz, Joseph A Mollick.
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Open-label phase III trial of panitumumab plus best supportive care compared with best supportive care alone in patients with chemotherapy-refractory metastatic colorectal cancer.
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Highly Cited.
Fc gamma receptor IIb on target B cells promotes rituximab internalization and reduces clinical efficacy.
Sean H Lim, Andrew T Vaughan, +13 authors, Martin J Glennie.
Blood, 2011 Jul 20; 118(9). PMID: 21768293
Results of a phase 1 study of AME-133v (LY2469298), an Fc-engineered humanized monoclonal anti-CD20 antibody, in FcγRIIIa-genotyped patients with previously treated follicular lymphoma.
Andres Forero-Torres, Sven de Vos, +11 authors, Kristen N Ganjoo.
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An IgG3 switch variant of rituximab mediates enhanced complement-dependent cytotoxicity against tumour cells with low CD20 expression levels.
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Ultra-Low Dosage Regimen of Rituximab in Autoimmune Blistering Skin Conditions.
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Front Immunol, 2018 May 04; 9. PMID: 29720979    Free PMC article.
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Reversing Autoimmunity Combination of Rituximab and Intravenous Immunoglobulin.
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Hematology Am Soc Hematol Educ Program, 2018 Dec 07; 2018(1). PMID: 30504336    Free PMC article.
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Spectral Photon-Counting Molecular Imaging for Quantification of Monoclonal Antibody-Conjugated Gold Nanoparticles Targeted to Lymphoma and Breast Cancer: An In Vitro Study.
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Immunosuppressive therapy with rituximab in common variable immunodeficiency.
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Clin Mol Allergy, 2019 May 14; 17. PMID: 31080365    Free PMC article.
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Overview of the Side-Effects of FDA- and/or EMA-Approved Targeted Therapies for the Treatment of Hematological Malignancies.
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The Role of Complement in the Mechanism of Action of Therapeutic Anti-Cancer mAbs.
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Monitoring of the Complement System Status in Patients With B-Cell Malignancies Treated With Rituximab.
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Front Immunol, 2020 Dec 18; 11. PMID: 33329558    Free PMC article.
Rituximab and obinutuzumab differentially hijack the B cell receptor and NOTCH1 signaling pathways.
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Glycoengineering of NK Cells with Glycan Ligands of CD22 and Selectins for B-Cell Lymphoma Therapy.
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Umbilical mesenchymal stem cell-derived extracellular vesicles as enzyme delivery vehicle to treat Morquio A fibroblasts.
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Addition of BTK inhibitor orelabrutinib to rituximab improved anti-tumor effects in B cell lymphoma.
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Blood Adv, 2021 Jul 30; 5(15). PMID: 34323957    Free PMC article.
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Methods Mol Biol, 2021 Sep 04; 2313. PMID: 34478129
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Multi-platform profiling characterizes molecular subgroups and resistance networks in chronic lymphocytic leukemia.
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Successful Pregnancies in a Patient with Childhood-onset Steroid-dependent Nephrotic Syndrome during Rituximab Maintenance Therapy.
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Molecular Aspects of Resistance to Immunotherapies-Advances in Understanding and Management of Diffuse Large B-Cell Lymphoma.
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