Review
. 2014 Jun; 86(5):485-91.
doi: 10.1124/mol.114.092684.

Analyses of CD20 monoclonal antibody-mediated tumor cell killing mechanisms: rational design of dosing strategies

Ronald P Taylor 1 Margaret A Lindorfer 2 
Affiliations
  • PMID: 24944188
  •     77 References
  •     19 citations

Abstract

Since approval of rituximab for treatment of B cell non-Hodgkin lymphoma, development of monoclonal antibodies (mAbs) for cancer treatment and elucidation of their cytotoxic mechanisms have been subject to intense investigations. Compelling evidence indicates that rituximab and another CD20 mAb, ofatumumab, must use the body's cellular and humoral immune effector functions to kill malignant cells. Other U.S. Food and Drug Administration-approved mAbs, including obinutuzumab, cetuximab, and trastuzumab, require, in part, these effector mechanisms to eliminate tumor cells. Although gram quantities of mAbs can be administered to patients, our investigations of CD20 mAb-based therapies for chronic lymphocytic leukemia (CLL), including correlative measurements in clinical trials and studies with primary cells and cell lines, indicate that effector mechanisms necessary for mAb activity can be saturated or exhausted if tumor burdens are high, thus substantially compromising the efficacy of high-dose mAb therapy. Under these conditions, another reaction (trogocytosis) predominates in which bound CD20 mAb and CD20 are removed from targeted cells by effector cells that express Fcγ receptors, thereby allowing malignant cells to escape unharmed and continue to promote disease pathology. To address this problem, we propose that a low-dose strategy, based on administering 30-50 mg of CD20 mAb three times per week, may be far more effective for CLL than standard dosing because it will minimize effector function saturation and reduce trogocytosis. This approach may have general applicability to other mAbs that use immune effector functions, and could be formulated into a subcutaneous treatment strategy that would be more accessible and possibly more efficacious for patients.

Complement-independent clearance of IgG-sensitized erythrocytes: inhibition by cortisone.
J P Atkinson, M M Frank.
Blood, 1974 Nov 01; 44(5). PMID: 4421780
Exhaustion of cytotoxic effector systems may limit monoclonal antibody-based immunotherapy in cancer patients.
Frank J Beurskens, Margaret A Lindorfer, +6 authors, Ronald P Taylor.
J Immunol, 2012 Mar 01; 188(7). PMID: 22368276    Free PMC article.
Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma.
Wen-Kai Weng, Ronald Levy.
J Clin Oncol, 2003 Sep 17; 21(21). PMID: 12975461
Highly Cited.
Monocytes mediate shaving of B-cell-bound anti-CD20 antibodies.
Anders E Pedersen, Mette B Jungersen, Charlotte D Pedersen.
Immunology, 2011 Mar 24; 133(2). PMID: 21426340    Free PMC article.
Chronic lymphocytic leukaemia CD20 expression is dependent on the genetic subtype: a study of quantitative flow cytometry and fluorescent in-situ hybridization in 510 patients.
Constantine S Tam, Joselle Otero-Palacios, +6 authors, Michael J Keating.
Br J Haematol, 2008 Mar 08; 141(1). PMID: 18324964
Both activating and inhibitory Fc gamma receptors mediate rituximab-induced trogocytosis of CD20 in mice.
Peter Boross, J H Marco Jansen, +2 authors, Jeanette H W Leusen.
Immunol Lett, 2012 Jan 31; 143(1). PMID: 22285696
Serial killing of tumor cells by human natural killer cells--enhancement by therapeutic antibodies.
Rauf Bhat, Carsten Watzl.
PLoS One, 2007 Mar 29; 2(3). PMID: 17389917    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.
Immune-modulating effects of the newest cetuximab-based chemoimmunotherapy regimen in advanced colorectal cancer patients.
Cirino Botta, Elena Bestoso, +9 authors, Pierpaolo Correale.
J Immunother, 2012 May 12; 35(5). PMID: 22576349
Systemic interleukin-2 and adoptive transfer of lymphokine-activated killer cells improves antibody-dependent cellular cytotoxicity in patients with relapsed B-cell lymphoma treated with rituximab.
Jesús G Berdeja, Allan Hess, +6 authors, Ian W Flinn.
Clin Cancer Res, 2007 Apr 18; 13(8). PMID: 17438098
FCGR2A and FCGR3A polymorphisms associated with clinical outcome of epidermal growth factor receptor expressing metastatic colorectal cancer patients treated with single-agent cetuximab.
Wu Zhang, Michael Gordon, +10 authors, Heinz-Josef Lenz.
J Clin Oncol, 2007 Aug 21; 25(24). PMID: 17704420
Highly Cited.
Targeted cancer immunotherapy.
Maya Zigler, Alexei Shir, Alexander Levitzki.
Curr Opin Pharmacol, 2013 May 08; 13(4). PMID: 23648271
Review.
Addition of rituximab to fludarabine and cyclophosphamide in patients with chronic lymphocytic leukaemia: a randomised, open-label, phase 3 trial.
M Hallek, K Fischer, +31 authors, German Chronic Lymphocytic Leukaemia Study Group.
Lancet, 2010 Oct 05; 376(9747). PMID: 20888994
Highly Cited.
Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets.
R A Clynes, T L Towers, L G Presta, J V Ravetch.
Nat Med, 2000 Mar 31; 6(4). PMID: 10742152
Highly Cited.
Role of antibody and complement in the immune clearance and destruction of erythrocytes. I. In vivo effects of IgG and IgM complement-fixing sites.
A D Schreiber, M M Frank.
J Clin Invest, 1972 Mar 01; 51(3). PMID: 4536807    Free PMC article.
Highly Cited.
Three new assays for rituximab based on its immunological activity or antigenic properties: analyses of sera and plasmas of RTX-treated patients with chronic lymphocytic leukemia and other B cell lymphomas.
Paul V Beum, Adam D Kennedy, Ronald P Taylor.
J Immunol Methods, 2004 Jul 15; 289(1-2). PMID: 15251416
Rituximab-CD20 complexes are shaved from Z138 mantle cell lymphoma cells in intravenous and subcutaneous SCID mouse models.
Yongli Li, Michael E Williams, +3 authors, Ronald P Taylor.
J Immunol, 2007 Sep 06; 179(6). PMID: 17785867
Lessons for the clinic from rituximab pharmacokinetics and pharmacodynamics.
Josée Golay, Gianpietro Semenzato, +8 authors, Mario Regazzi.
MAbs, 2013 Aug 13; 5(6). PMID: 23933992    Free PMC article.
Review.
Induced resistance to ofatumumab-mediated cell clearance mechanisms, including complement-dependent cytotoxicity, in chronic lymphocytic leukemia.
Nisar A Baig, Ronald P Taylor, +6 authors, Clive S Zent.
J Immunol, 2014 Jan 17; 192(4). PMID: 24431228    Free PMC article.
Rituximab anti-CD20 monoclonal antibody therapy in non-Hodgkin's lymphoma: safety and efficacy of re-treatment.
T A Davis, A J Grillo-López, +7 authors, R Levy.
J Clin Oncol, 2000 Aug 30; 18(17). PMID: 10963642
Highly Cited.
Mechanism of action of type II, glycoengineered, anti-CD20 monoclonal antibody GA101 in B-chronic lymphocytic leukemia whole blood assays in comparison with rituximab and alemtuzumab.
Luca Bologna, Elisa Gotti, +4 authors, Josée Golay.
J Immunol, 2011 Feb 08; 186(6). PMID: 21296976
Ofatumumab, a novel anti-CD20 monoclonal antibody for the treatment of B-cell malignancies.
Bruce D Cheson.
J Clin Oncol, 2010 May 12; 28(21). PMID: 20458041
Review.
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.
Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene.
Guillaume Cartron, Laurent Dacheux, +4 authors, Hervé Watier.
Blood, 2002 Jan 25; 99(3). PMID: 11806974
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.
Association of serum Rituximab (IDEC-C2B8) concentration and anti-tumor response in the treatment of recurrent low-grade or follicular non-Hodgkin's lymphoma.
N L Berinstein, A J Grillo-López, +7 authors, D Shen.
Ann Oncol, 1998 Nov 18; 9(9). PMID: 9818074
Highly Cited.
The role of complement in mAb-based therapies of cancer.
Ronald P Taylor, Margaret A Lindorfer.
Methods, 2013 Jul 28; 65(1). PMID: 23886909
Review.
FcgammaRIIIa polymorphisms and cetuximab induced cytotoxicity in squamous cell carcinoma of the head and neck.
Rodney J Taylor, Siaw-Lin Chan, +7 authors, Scott E Strome.
Cancer Immunol Immunother, 2008 Nov 04; 58(7). PMID: 18979096
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.
Alemtuzumab (CAMPATH 1H) does not kill chronic lymphocytic leukemia cells in serum free medium.
Clive S Zent, James B Chen, +3 authors, Steven A Schichman.
Leuk Res, 2004 Apr 08; 28(5). PMID: 15068903
Thrice-weekly low-dose rituximab decreases CD20 loss via shaving and promotes enhanced targeting in chronic lymphocytic leukemia.
Michael E Williams, John J Densmore, +6 authors, Ronald P Taylor.
J Immunol, 2006 Nov 04; 177(10). PMID: 17082663
Mechanisms of action of CD20 antibodies.
Peter Boross, Jeanette H W Leusen.
Am J Cancer Res, 2012 Dec 12; 2(6). PMID: 23226614    Free PMC article.
Binding of rituximab, trastuzumab, cetuximab, or mAb T101 to cancer cells promotes trogocytosis mediated by THP-1 cells and monocytes.
Paul V Beum, David A Mack, +2 authors, Ronald P Taylor.
J Immunol, 2008 Nov 20; 181(11). PMID: 19018005
Gnawing at Metchnikoff's paradigm.
Ronald P Taylor.
Blood, 2013 Oct 26; 122(17). PMID: 24159161
CD137 stimulation enhances the antilymphoma activity of anti-CD20 antibodies.
Holbrook E Kohrt, Roch Houot, +11 authors, Ronald Levy.
Blood, 2011 Jan 05; 117(8). PMID: 21193697    Free PMC article.
Highly Cited.
The direction of plasma membrane exchange between lymphocytes and accessory cells by trogocytosis is influenced by the nature of the accessory cell.
Sandrine Daubeuf, Margaret A Lindorfer, +2 authors, Denis Hudrisier.
J Immunol, 2010 Jan 22; 184(4). PMID: 20089699
Antibody therapeutics in cancer.
Mark X Sliwkowski, Ira Mellman.
Science, 2013 Sep 14; 341(6151). PMID: 24031011
Highly Cited. Review.
Pharmacokinetics and pharmacokinetic/pharmacodynamic associations of ofatumumab, a human monoclonal CD20 antibody, in patients with relapsed or refractory chronic lymphocytic leukaemia: a phase 1-2 study.
Bertrand Coiffier, Nedjad Losic, +12 authors, Jørgen Petersen.
Br J Haematol, 2010 Apr 23; 150(1). PMID: 20408846
Elements related to heterogeneity of antibody-dependent cell cytotoxicity in patients under trastuzumab therapy for primary operable breast cancer overexpressing Her2.
Stefania Varchetta, Nadia Gibelli, +9 authors, Francesco F Fagnoni.
Cancer Res, 2007 Dec 20; 67(24). PMID: 18089830
Chemoimmunotherapy for relapsed/refractory and progressive 17p13-deleted chronic lymphocytic leukemia (CLL) combining pentostatin, alemtuzumab, and low-dose rituximab is effective and tolerable and limits loss of CD20 expression by circulating CLL cells.
Clive S Zent, Ronald P Taylor, +14 authors, Thomas E Witzig.
Am J Hematol, 2014 Apr 12; 89(7). PMID: 24723493    Free PMC article.
Rituximab: mechanism of action.
George J Weiner.
Semin Hematol, 2010 Mar 31; 47(2). PMID: 20350658    Free PMC article.
Highly Cited. Review.
Mechanisms of killing by anti-CD20 monoclonal antibodies.
Martin J Glennie, Ruth R French, Mark S Cragg, Ronald P Taylor.
Mol Immunol, 2007 Sep 05; 44(16). PMID: 17768100
Highly Cited. Review.
Mechanism of action of therapeutic monoclonal antibodies: promises and pitfalls of in vitro and in vivo assays.
Josée Golay, Martino Introna.
Arch Biochem Biophys, 2012 Mar 06; 526(2). PMID: 22387378
Review.
Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin lymphomas.
Jessica L Teeling, Ruth R French, +10 authors, Martin J Glennie.
Blood, 2004 Jun 03; 104(6). PMID: 15172969
Highly Cited.
The in vivo mechanism of action of CD20 monoclonal antibodies depends on local tumor burden.
Peter Boross, J H Marco Jansen, +8 authors, Jeanette H W Leusen.
Haematologica, 2011 Sep 02; 96(12). PMID: 21880632    Free PMC article.
Immunohistochemical analysis as a means to predict responsiveness to rituximab treatment.
Y K Onno Teng, E W Nivine Levarht, +4 authors, Jacob M van Laar.
Arthritis Rheum, 2007 Dec 01; 56(12). PMID: 18050222
Monoclonal antibody therapy for B-cell non-Hodgkin's lymphoma.
Bruce D Cheson, John P Leonard.
N Engl J Med, 2008 Aug 09; 359(6). PMID: 18687642
Highly Cited. Review.
Loss of CD20 and bound CD20 antibody from opsonized B cells occurs more rapidly because of trogocytosis mediated by Fc receptor-expressing effector cells than direct internalization by the B cells.
Paul V Beum, Elizabeth M Peek, +5 authors, Ronald P Taylor.
J Immunol, 2011 Aug 16; 187(6). PMID: 21841127
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.
Trogocytosis of multiple B-cell surface markers by CD22 targeting with epratuzumab.
Edmund A Rossi, David M Goldenberg, +3 authors, Chien-Hsing Chang.
Blood, 2013 Jul 04; 122(17). PMID: 23821660
Mechanisms of heterogeneous distribution of monoclonal antibodies and other macromolecules in tumors: significance of elevated interstitial pressure.
R K Jain, L T Baxter.
Cancer Res, 1988 Dec 15; 48(24 Pt 1). PMID: 3191477
Highly Cited.
Possible implication of Fc γ receptor-mediated trogocytosis in susceptibility to systemic autoimmune disease.
Sakiko Masuda, Sari Iwasaki, +3 authors, Akihiro Ishizu.
Clin Dev Immunol, 2013 Oct 05; 2013. PMID: 24093044    Free PMC article.
Review.
Rituximab mediates loss of CD19 on B cells in the absence of cell death.
Jonathan D Jones, B JoNell Hamilton, William F C Rigby.
Arthritis Rheum, 2012 Jun 08; 64(10). PMID: 22674374    Free PMC article.
Stimulation of natural killer cells with a CD137-specific antibody enhances trastuzumab efficacy in xenotransplant models of breast cancer.
Holbrook E Kohrt, Roch Houot, +11 authors, Ronald Levy.
J Clin Invest, 2012 Feb 14; 122(3). PMID: 22326955    Free PMC article.
Highly Cited.
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.
What is trogocytosis and what is its purpose?
Etienne Joly, Denis Hudrisier.
Nat Immunol, 2003 Aug 28; 4(9). PMID: 12942076
Highly Cited.
Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
Tyler R Simpson, Fubin Li, +11 authors, Sergio A Quezada.
J Exp Med, 2013 Jul 31; 210(9). PMID: 23897981    Free PMC article.
Highly Cited.
Antibody therapy of cancer.
Andrew M Scott, Jedd D Wolchok, Lloyd J Old.
Nat Rev Cancer, 2012 Mar 23; 12(4). PMID: 22437872
Highly Cited. Review.
Molecular engineering to improve antibodies' anti-lymphoma activity.
Matthias Peipp, Jan G J van de Winkel, Thomas Valerius.
Best Pract Res Clin Haematol, 2011 Jun 11; 24(2). PMID: 21658620
Review.
The mechanism of anti-CD20-mediated B cell depletion revealed by intravital imaging.
Fabricio Montalvao, Zacarias Garcia, +4 authors, Philippe Bousso.
J Clin Invest, 2013 Nov 02; 123(12). PMID: 24177426    Free PMC article.
Rituximab infusion induces NK activation in lymphoma patients with the high-affinity CD16 polymorphism.
Suresh Veeramani, Siao-Yi Wang, +6 authors, George J Weiner.
Blood, 2011 Jul 20; 118(12). PMID: 21768303    Free PMC article.
Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lymphoma: half of patients respond to a four-dose treatment program.
P McLaughlin, A J Grillo-López, +13 authors, B K Dallaire.
J Clin Oncol, 1998 Aug 15; 16(8). PMID: 9704735
Highly Cited.
Characterization of bone marrow lymphoid infiltrates after immunochemotherapy for follicular lymphoma.
Camille Laurent, Geisilene Rusno de Paiva, +4 authors, Pierre Brousset.
Am J Clin Pathol, 2007 Nov 21; 128(6). PMID: 18024323
Novel type II anti-CD20 monoclonal antibody (GA101) evokes homotypic adhesion and actin-dependent, lysosome-mediated cell death in B-cell malignancies.
Waleed Alduaij, Andrei Ivanov, +10 authors, Tim M Illidge.
Blood, 2011 Mar 08; 117(17). PMID: 21378274    Free PMC article.
Highly Cited.
Monoclonal antibody (mAb)-based cancer therapy: Is it time to reevaluate dosing strategies?
Margaret A Lindorfer, Adrian Wiestner, Clive S Zent, Ronald P Taylor.
Oncoimmunology, 2012 Nov 20; 1(6). PMID: 23162771    Free PMC article.
Subcutaneous injections of low-dose veltuzumab (humanized anti-CD20 antibody) are safe and active in patients with indolent non-Hodgkin's lymphoma.
George O Negrea, Rebecca Elstrom, +7 authors, David M Goldenberg.
Haematologica, 2010 Dec 22; 96(4). PMID: 21173095    Free PMC article.
Humanized anti-CD20 antibody, veltuzumab, in refractory/recurrent non-Hodgkin's lymphoma: phase I/II results.
Franck Morschhauser, John P Leonard, +9 authors, David M Goldenberg.
J Clin Oncol, 2009 May 20; 27(20). PMID: 19451441
Fractionated subcutaneous rituximab is well-tolerated and preserves CD20 expression on tumor cells in patients with chronic lymphocytic leukemia.
Georg Aue, Margaret A Lindorfer, +5 authors, Adrian Wiestner.
Haematologica, 2009 Aug 15; 95(2). PMID: 19679883    Free PMC article.
The shaving reaction: rituximab/CD20 complexes are removed from mantle cell lymphoma and chronic lymphocytic leukemia cells by THP-1 monocytes.
Paul V Beum, Adam D Kennedy, +2 authors, Ronald P Taylor.
J Immunol, 2006 Feb 04; 176(4). PMID: 16456022
An Fcγ receptor-dependent mechanism drives antibody-mediated target-receptor signaling in cancer cells.
Nicholas S Wilson, Becky Yang, +17 authors, Avi Ashkenazi.
Cancer Cell, 2011 Jan 22; 19(1). PMID: 21251615
Highly Cited.
Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy.
Qian Gong, Qinglin Ou, +17 authors, Andrew C Chan.
J Immunol, 2005 Jan 07; 174(2). PMID: 15634903
Highly Cited.
Within peripheral blood mononuclear cells, antibody-dependent cellular cytotoxicity of rituximab-opsonized Daudi cells is promoted by NK cells and inhibited by monocytes due to shaving.
Paul V Beum, Margaret A Lindorfer, Ronald P Taylor.
J Immunol, 2008 Aug 08; 181(4). PMID: 18684983
Ofatumumab is more efficient than rituximab in lysing B chronic lymphocytic leukemia cells in whole blood and in combination with chemotherapy.
Luca Bologna, Elisa Gotti, +4 authors, Josée Golay.
J Immunol, 2012 Dec 12; 190(1). PMID: 23225880
The immune system and response to HER2-targeted treatment in breast cancer.
Giampaolo Bianchini, Luca Gianni.
Lancet Oncol, 2014 Feb 01; 15(2). PMID: 24480556
Highly Cited. Review.
Fcγ receptors enable anticancer action of proapoptotic and immune-modulatory antibodies.
Jeong M Kim, Avi Ashkenazi.
J Exp Med, 2013 Aug 28; 210(9). PMID: 23980122    Free PMC article.
Review.
CD16 polymorphisms and NK activation induced by monoclonal antibody-coated target cells.
Julie A Bowles, George J Weiner.
J Immunol Methods, 2005 Aug 20; 304(1-2). PMID: 16109421
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
Early treatment of high risk chronic lymphocytic leukemia with alemtuzumab, rituximab and poly-(1-6)-beta-glucotriosyl-(1-3)- beta-glucopyranose beta-glucan is well tolerated and achieves high complete remission rates.
Clive S Zent, Timothy G Call, +5 authors, George J Weiner.
Leuk Lymphoma, 2015 Feb 14; 56(8). PMID: 25676035    Free PMC article.
Classifying ten types of major cancers based on reverse phase protein array profiles.
Pei-Wei Zhang, Lei Chen, +3 authors, Yu-Dong Cai.
PLoS One, 2015 Mar 31; 10(3). PMID: 25822500    Free PMC article.
Anti-CD20 monoclonal antibody-dependent phagocytosis of chronic lymphocytic leukaemia cells by autologous macrophages.
A K Church, K R VanDerMeid, +4 authors, C S Zent.
Clin Exp Immunol, 2015 Aug 27; 183(1). PMID: 26307241    Free PMC article.
FCGR2A, FCGR3A polymorphisms and therapeutic efficacy of anti-EGFR monoclonal antibody in metastatic colorectal cancer.
Hou-Qun Ying, Feng Wang, +8 authors, Shu-Kui Wang.
Oncotarget, 2015 Sep 13; 6(29). PMID: 26363448    Free PMC article.
A phase II randomized trial comparing standard and low dose rituximab combined with alemtuzumab as initial treatment of progressive chronic lymphocytic leukemia in older patients: a trial of the ECOG-ACRIN cancer research group (E1908).
Clive S Zent, Xin Victoria Wang, +12 authors, Martin S Tallman.
Am J Hematol, 2015 Dec 15; 91(3). PMID: 26662208    Free PMC article.
Macrophage-Mediated Trogocytosis Leads to Death of Antibody-Opsonized Tumor Cells.
Ramraj Velmurugan, Dilip K Challa, +2 authors, E Sally Ward.
Mol Cancer Ther, 2016 May 27; 15(8). PMID: 27226489    Free PMC article.
Antibodies That Efficiently Form Hexamers upon Antigen Binding Can Induce Complement-Dependent Cytotoxicity under Complement-Limiting Conditions.
Erika M Cook, Margaret A Lindorfer, +7 authors, Ronald P Taylor.
J Immunol, 2016 Jul 31; 197(5). PMID: 27474078    Free PMC article.
Progress in tumor-associated macrophage (TAM)-targeted therapeutics.
Chayanon Ngambenjawong, Heather H Gustafson, Suzie H Pun.
Adv Drug Deliv Rev, 2017 Apr 30; 114. PMID: 28449873    Free PMC article.
Highly Cited. Review.
Therapeutic Antibodies to KIR3DL2 and Other Target Antigens on Cutaneous T-Cell Lymphomas.
Christian Schmitt, Anne Marie-Cardine, Armand Bensussan.
Front Immunol, 2017 Sep 16; 8. PMID: 28912774    Free PMC article.
Review.
Monocytes and Granulocytes Reduce CD38 Expression Levels on Myeloma Cells in Patients Treated with Daratumumab.
Jakub Krejcik, Kris A Frerichs, +15 authors, Niels W C J van de Donk.
Clin Cancer Res, 2017 Oct 14; 23(24). PMID: 29025767    Free PMC article.
Highly Cited.
Regulation of expression of MLAA-34 gene through transcriptional factors E2F1 and MZF-1.
Bo Lei, Aili He, +6 authors, Wanggang Zhang.
Int J Clin Exp Pathol, 2020 Jan 15; 12(6). PMID: 31934032    Free PMC article.
Mechanisms of Resistance to Anti-CD38 Daratumumab in Multiple Myeloma.
Ilaria Saltarella, Vanessa Desantis, +7 authors, Maria Antonia Frassanito.
Cells, 2020 Jan 16; 9(1). PMID: 31936617    Free PMC article.
Review.
CD20 and CD37 antibodies synergize to activate complement by Fc-mediated clustering.
Simone C Oostindie, Hilma J van der Horst, +14 authors, Ronald P Taylor.
Haematologica, 2019 Feb 23; 104(9). PMID: 30792198    Free PMC article.
Biting Off What Can Be Chewed: Trogocytosis in Health, Infection, and Disease.
Akhila Bettadapur, Hannah W Miller, Katherine S Ralston.
Infect Immun, 2020 May 06; 88(7). PMID: 32366574    Free PMC article.
Review.
Tumor-associated macrophages: Role in the pathological process of tumorigenesis and prospective therapeutic use (Review).
Olga V Zhukova, Tatiana F Kovaleva, +2 authors, Irina V Mukhina.
Biomed Rep, 2020 Sep 17; 13(5). PMID: 32934819    Free PMC article.
Review.
Mutations resulting in the formation of hyperactive complement convertases support cytocidal effect of anti-CD20 immunotherapeutics.
Anna Felberg, Aleksandra Urban, +5 authors, Marcin Okrój.
Cancer Immunol Immunother, 2019 Feb 07; 68(4). PMID: 30725204    Free PMC article.
Monitoring of the Complement System Status in Patients With B-Cell Malignancies Treated With Rituximab.
Anna Felberg, Michał Taszner, +7 authors, Marcin Okrój.
Front Immunol, 2020 Dec 18; 11. PMID: 33329558    Free PMC article.
Mechanisms of Therapeutic Antitumor Monoclonal Antibodies.
Li-Chung Tsao, Jeremy Force, Zachary C Hartman.
Cancer Res, 2021 Jun 20; 81(18). PMID: 34145037    Free PMC article.
Review.
The Multiple Roles of Trogocytosis in Immunity, the Nervous System, and Development.
Eileen Uribe-Querol, Carlos Rosales.
Biomed Res Int, 2021 Oct 05; 2021. PMID: 34604381    Free PMC article.
Review.