Journal Article
. 2004 Jun; 199(12):1659-69.
doi: 10.1084/jem.20040119.

The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy

Junji Uchida 1 Yasuhito Hamaguchi  Julie A Oliver  Jeffrey V Ravetch  Jonathan C Poe  Karen M Haas  Thomas F Tedder  
  • PMID: 15210744
  •     75 References
  •     210 citations


Anti-CD20 antibody immunotherapy effectively treats non-Hodgkin's lymphoma and autoimmune disease. However, the cellular and molecular pathways for B cell depletion remain undefined because human mechanistic studies are limited. Proposed mechanisms include antibody-, effector cell-, and complement-dependent cytotoxicity, the disruption of CD20 signaling pathways, and the induction of apoptosis. To identify the mechanisms for B cell depletion in vivo, a new mouse model for anti-CD20 immunotherapy was developed using a panel of twelve mouse anti-mouse CD20 monoclonal antibodies representing all four immunoglobulin G isotypes. Anti-CD20 antibodies rapidly depleted the vast majority of circulating and tissue B cells in an isotype-restricted manner that was completely dependent on effector cell Fc receptor expression. B cell depletion used both FcgammaRI- and FcgammaRIII-dependent pathways, whereas B cells were not eliminated in FcR common gamma chain-deficient mice. Monocytes were the dominant effector cells for B cell depletion, with no demonstrable role for T or natural killer cells. Although most anti-CD20 antibodies activated complement in vitro, B cell depletion was completely effective in mice with genetic deficiencies in C3, C4, or C1q complement components. That the innate monocyte network depletes B cells through FcgammaR-dependent pathways during anti-CD20 immunotherapy has important clinical implications for anti-CD20 and other antibody-based therapies.

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MAbs, 2010 Jan 13; 1(5). PMID: 20065652    Free PMC article.
Evolution of anti-CD20 monoclonal antibody therapeutics in oncology.
Ezogelin Oflazoglu, Laurent P Audoly.
MAbs, 2010 Jan 19; 2(1). PMID: 20081379    Free PMC article.
Engineered Fc variant antibodies with enhanced ability to recruit complement and mediate effector functions.
Gregory L Moore, Hsing Chen, Sher Karki, Greg A Lazar.
MAbs, 2010 Feb 13; 2(2). PMID: 20150767    Free PMC article.
B cells are required for optimal CD4+ and CD8+ T cell tumor immunity: therapeutic B cell depletion enhances B16 melanoma growth in mice.
David J DiLillo, Koichi Yanaba, Thomas F Tedder.
J Immunol, 2010 Mar 03; 184(7). PMID: 20194720    Free PMC article.
Highly Cited.
Fcgamma receptors modulate pulmonary inflammation by activating innate immune cells in murine hypersensitivity pneumonitis.
Hyo Jin Park, Hye Sung Kim, Doo Hyun Chung.
Immune Netw, 2010 Mar 17; 10(1). PMID: 20228933    Free PMC article.
Protective and pathogenic roles for B cells during systemic autoimmunity in NZB/W F1 mice.
Karen M Haas, Rei Watanabe, +5 authors, Thomas F Tedder.
J Immunol, 2010 Apr 07; 184(9). PMID: 20368280    Free PMC article.
FcgammaRIIB in autoimmunity and infection: evolutionary and therapeutic implications.
Kenneth G C Smith, Menna R Clatworthy.
Nat Rev Immunol, 2010 Apr 24; 10(5). PMID: 20414206    Free PMC article.
Highly Cited. Review.
Antibodies specific for a segment of human membrane IgE deplete IgE-producing B cells in humanized mice.
Hans D Brightbill, Surinder Jeet, +24 authors, Lawren C Wu.
J Clin Invest, 2010 May 12; 120(6). PMID: 20458139    Free PMC article.
Prolonged effects of short-term anti-CD20 B cell depletion therapy in murine systemic lupus erythematosus.
Kai W Bekar, Teresa Owen, +9 authors, Jennifer H Anolik.
Arthritis Rheum, 2010 May 28; 62(8). PMID: 20506300    Free PMC article.
B-cell homeostasis requires complementary CD22 and BLyS/BR3 survival signals.
Susan H Smith, Karen M Haas, +4 authors, Thomas F Tedder.
Int Immunol, 2010 Jun 02; 22(8). PMID: 20513733    Free PMC article.
B cell depletion reduces the development of atherosclerosis in mice.
Hafid Ait-Oufella, Olivier Herbin, +12 authors, Ziad Mallat.
J Exp Med, 2010 Jul 07; 207(8). PMID: 20603314    Free PMC article.
Highly Cited.
Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis.
Takashi Matsushita, Mayuka Horikawa, Yohei Iwata, Thomas F Tedder.
J Immunol, 2010 Jul 14; 185(4). PMID: 20624940    Free PMC article.
Highly Cited.
B-lymphocyte effector functions in health and disease.
David J DiLillo, Mayuka Horikawa, Thomas F Tedder.
Immunol Res, 2010 Dec 03; 49(1-3). PMID: 21125343
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.
B cell-targeted therapy with anti-CD20 monoclonal antibody in a mouse model of Graves' hyperthyroidism.
I Ueki, N Abiru, +4 authors, Y Nagayama.
Clin Exp Immunol, 2011 Jan 18; 163(3). PMID: 21235532    Free PMC article.
B lymphocytes differentially influence acute and chronic allograft rejection in mice.
David J DiLillo, Robert Griffiths, +4 authors, Thomas F Tedder.
J Immunol, 2011 Jan 21; 186(4). PMID: 21248259    Free PMC article.
B cell depletion in autoimmune diabetes: insights from murine models.
Jayne L Chamberlain, Kesley Attridge, +2 authors, Lucy Sk Walker.
Expert Opin Ther Targets, 2011 Mar 04; 15(6). PMID: 21366498    Free PMC article.
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.
Antitumour effects of single or combined monoclonal antibodies directed against membrane antigens expressed by human B cells leukaemia.
Séverine Loisel, Pierre-Alain André, +10 authors, Laurence Boumsell.
Mol Cancer, 2011 Apr 21; 10. PMID: 21504579    Free PMC article.
Rituximab resistance.
Andrew R Rezvani, David G Maloney.
Best Pract Res Clin Haematol, 2011 Jun 11; 24(2). PMID: 21658619    Free PMC article.
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.
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.
Regulatory B cell production of IL-10 inhibits lymphoma depletion during CD20 immunotherapy in mice.
Mayuka Horikawa, Veronique Minard-Colin, Takashi Matsushita, Thomas F Tedder.
J Clin Invest, 2011 Oct 25; 121(11). PMID: 22019587    Free PMC article.
Plitidepsin (Aplidin) is a potent inhibitor of diffuse large cell and Burkitt lymphoma and is synergistic with rituximab.
Nora M Barboza, Daniel J Medina, +4 authors, Debabrata Banerjee.
Cancer Biol Ther, 2012 Feb 18; 13(2). PMID: 22336911    Free PMC article.
Tumor-targeted T cells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning.
Hollie J Pegram, James C Lee, +4 authors, Renier J Brentjens.
Blood, 2012 Feb 23; 119(18). PMID: 22354001    Free PMC article.
Highly Cited.
Lymphocytes and the adventitial immune response in atherosclerosis.
Kirsti A Campbell, Michael J Lipinski, +3 authors, Coleen A McNamara.
Circ Res, 2012 Mar 20; 110(6). PMID: 22427326    Free PMC article.
Immunotherapy for B-cell lymphoma: current status and prospective advances.
Nurit Hollander.
Front Immunol, 2012 May 09; 3. PMID: 22566889    Free PMC article.
Combination strategies to enhance antitumor ADCC.
Holbrook E Kohrt, Roch Houot, +5 authors, Joshua Brody.
Immunotherapy, 2012 May 31; 4(5). PMID: 22642334    Free PMC article.
Transient B cell depletion or improved transgene expression by codon optimization promote tolerance to factor VIII in gene therapy.
Brandon K Sack, Sherin Merchant, +4 authors, Roland W Herzog.
PLoS One, 2012 Jun 02; 7(5). PMID: 22655063    Free PMC article.
Characterization of a mutated IgA2 antibody of the m(1) allotype against the epidermal growth factor receptor for the recruitment of monocytes and macrophages.
Stefan Lohse, Christina Brunke, +8 authors, Thomas Valerius.
J Biol Chem, 2012 Jun 09; 287(30). PMID: 22679018    Free PMC article.
Autoantigen-specific B-cell depletion overcomes failed immune tolerance in type 1 diabetes.
Rachel A Henry, Peggy L Kendall, James W Thomas.
Diabetes, 2012 Jun 16; 61(8). PMID: 22698916    Free PMC article.
Translating basic mechanisms of IgG effector activity into next generation cancer therapies.
Falk Nimmerjahn, Jeffrey V Ravetch.
Cancer Immun, 2012 Aug 17; 12. PMID: 22896758    Free PMC article.
Influence of FCGR3A genotype on the therapeutic response to rituximab in rheumatoid arthritis: an observational cohort study.
Alf Kastbom, Lars Cöster, +5 authors, Saedis Saevarsdottir.
BMJ Open, 2012 Sep 25; 2(5). PMID: 23002160    Free PMC article.
Clinical use of biologics in vasculitis syndromes.
Marino Paroli.
Biologics, 2012 Nov 03; 6. PMID: 23118526    Free PMC article.
Enhancement of the anti-melanoma response of Hu14.18K322A by αCD40 + CpG.
Kory L Alderson, Mitchell Luangrath, +4 authors, Paul M Sondel.
Cancer Immunol Immunother, 2012 Nov 16; 62(4). PMID: 23151945    Free PMC article.
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.
Regulatory B cell (B10 Cell) expansion during Listeria infection governs innate and cellular immune responses in mice.
Mayuka Horikawa, Eric T Weimer, +5 authors, Thomas F Tedder.
J Immunol, 2013 Jan 01; 190(3). PMID: 23275601    Free PMC article.
Aire's plant homeodomain(PHD)-2 is critical for induction of immunological tolerance.
Siyoung Yang, Kushagra Bansal, +2 authors, Diane Mathis.
Proc Natl Acad Sci U S A, 2013 Jan 16; 110(5). PMID: 23319629    Free PMC article.
Intravenous immunoglobulin therapy: how does IgG modulate the immune system?
Inessa Schwab, Falk Nimmerjahn.
Nat Rev Immunol, 2013 Feb 16; 13(3). PMID: 23411799
Highly Cited. Review.
Comparative assessment of clinically utilized CD20-directed antibodies in chronic lymphocytic leukemia cells reveals divergent NK cell, monocyte, and macrophage properties.
Sarwish Rafiq, Jonathan P Butchar, +7 authors, John C Byrd.
J Immunol, 2013 Feb 19; 190(6). PMID: 23418626    Free PMC article.
Toll-like receptor 2 ligands regulate monocyte Fcγ receptor expression and function.
Prexy Shah, Kavin Fatehchand, +6 authors, Jonathan P Butchar.
J Biol Chem, 2013 Mar 19; 288(17). PMID: 23504312    Free PMC article.
Interleukin-21 enhances rituximab activity in a cynomolgus monkey model of B cell depletion and in mouse B cell lymphoma models.
Cecile M Krejsa, Rick D Holly, +18 authors, Kim Waggie.
PLoS One, 2013 Jul 05; 8(6). PMID: 23825648    Free PMC article.
Glycovariant anti-CD37 monospecific protein therapeutic exhibits enhanced effector cell-mediated cytotoxicity against chronic and acute B cell malignancies.
Sarwish Rafiq, Anthony Siadak, +18 authors, Natarajan Muthusamy.
MAbs, 2013 Jul 26; 5(5). PMID: 23883821    Free PMC article.
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.
Ofatumumab-based chemoimmunotherapy is effective and well tolerated in patients with previously untreated chronic lymphocytic leukemia (CLL).
Tait Shanafelt, Mark C Lanasa, +9 authors, Clive S Zent.
Cancer, 2013 Aug 08; 119(21). PMID: 23922059    Free PMC article.
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.
Neutrophils mediate antibody-induced antitumor effects in mice.
Marcello Albanesi, David A Mancardi, +5 authors, Pierre Bruhns.
Blood, 2013 Aug 28; 122(18). PMID: 23980063    Free PMC article.
TIM-3 as a novel therapeutic target for eradicating acute myelogenous leukemia stem cells.
Yoshikane Kikushige, Toshihiro Miyamoto.
Int J Hematol, 2013 Sep 21; 98(6). PMID: 24046178
CD19 as a therapeutic target in a spontaneous autoimmune polyneuropathy.
P M Abraham, S H Quan, D Dukala, B Soliven.
Clin Exp Immunol, 2013 Oct 15; 175(2). PMID: 24116957    Free PMC article.
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.
Long-lived plasma cells in autoimmunity: lessons from B-cell depleting therapy.
Matthieu Mahévas, Marc Michel, Jean-Claude Weill, Claude-Agnès Reynaud.
Front Immunol, 2014 Jan 11; 4. PMID: 24409184    Free PMC article.
Anti-CD79 antibody induces B cell anergy that protects against autoimmunity.
Ian R Hardy, Nadia Anceriz, +17 authors, John C Cambier.
J Immunol, 2014 Jan 21; 192(4). PMID: 24442438    Free PMC article.
B cell depletion curtails CD4+ T cell memory and reduces protection against disseminating virus infection.
Ichiro Misumi, Jason K Whitmire.
J Immunol, 2014 Jan 24; 192(4). PMID: 24453250    Free PMC article.
Glycoengineering of therapeutic antibodies enhances monocyte/macrophage-mediated phagocytosis and cytotoxicity.
Sylvia Herter, Martina C Birk, +3 authors, Marina Bacac.
J Immunol, 2014 Feb 04; 192(5). PMID: 24489098    Free PMC article.
Increasing FcγRIIa affinity of an FcγRIII-optimized anti-EGFR antibody restores neutrophil-mediated cytotoxicity.
Stefanie Derer, Pia Glorius, +7 authors, Matthias Peipp.
MAbs, 2014 Feb 05; 6(2). PMID: 24492248    Free PMC article.
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.
Experience with rituximab in the treatment of antineutrophil cytoplasmic antibody associated vasculitis.
Jeremy M Clain, Rodrigo Cartin-Ceba, Fernando C Fervenza, Ulrich Specks.
Ther Adv Musculoskelet Dis, 2014 Apr 02; 6(2). PMID: 24688606    Free PMC article.
B cells and humoral immunity in atherosclerosis.
Dimitrios Tsiantoulas, Cody J Diehl, Joseph L Witztum, Christoph J Binder.
Circ Res, 2014 May 24; 114(11). PMID: 24855199    Free PMC article.
Highly Cited. Review.
Acute and chronic B cell depletion disrupts CD4+ and CD8+ T cell homeostasis and expansion during acute viral infection in mice.
Jacquelyn M Lykken, David J DiLillo, +5 authors, Thomas F Tedder.
J Immunol, 2014 Jun 15; 193(2). PMID: 24928986    Free PMC article.
Type I and type II Fc receptors regulate innate and adaptive immunity.
Andrew Pincetic, Stylianos Bournazos, +5 authors, Jeffrey V Ravetch.
Nat Immunol, 2014 Jul 22; 15(8). PMID: 25045879    Free PMC article.
Highly Cited. Review.
Three major uncertainties in the antibody therapy of cancer.
George T Stevenson.
Haematologica, 2014 Oct 02; 99(10). PMID: 25271313    Free PMC article.
Ibrutinib interferes with the cell-mediated anti-tumor activities of therapeutic CD20 antibodies: implications for combination therapy.
Fabio Da Roit, Patrick J Engelberts, +7 authors, Josée Golay.
Haematologica, 2014 Oct 26; 100(1). PMID: 25344523    Free PMC article.
The role of T and B cells in human atherosclerosis and atherothrombosis.
E Ammirati, F Moroni, M Magnoni, P G Camici.
Clin Exp Immunol, 2014 Oct 30; 179(2). PMID: 25352024    Free PMC article.
Prognostic influence of macrophages in patients with diffuse large B-cell lymphoma: a correlative study from a Nordic phase II trial.
Sari Riihijärvi, Idun Fiskvik, +8 authors, Sirpa Leppä.
Haematologica, 2014 Nov 09; 100(2). PMID: 25381134    Free PMC article.
Victory and defeat in the induction of a therapeutic response through vaccine therapy for human and canine brain tumors: a review of the state of the art.
Michael R Olin, G Elizabeth Pluhar, +3 authors, Christopher L Moertel.
Crit Rev Immunol, 2014 Nov 19; 34(5). PMID: 25404047    Free PMC article.
Conformation of the human immunoglobulin G2 hinge imparts superagonistic properties to immunostimulatory anticancer antibodies.
Ann L White, H T Claude Chan, +15 authors, Martin J Glennie.
Cancer Cell, 2014 Dec 17; 27(1). PMID: 25500122    Free PMC article.
Regulation of complement and modulation of its activity in monoclonal antibody therapy of cancer.
Saskia Meyer, Jeanette H W Leusen, Peter Boross.
MAbs, 2014 Dec 18; 6(5). PMID: 25517299    Free PMC article.
Ibrutinib impairs the phagocytosis of rituximab-coated leukemic cells from chronic lymphocytic leukemia patients by human macrophages.
Mercedes Borge, María Belén Almejún, +6 authors, Romina Gamberale.
Haematologica, 2015 Jan 27; 100(4). PMID: 25616578    Free PMC article.
Macrophages are critical effectors of antibody therapies for cancer.
Kipp Weiskopf, Irving L Weissman.
MAbs, 2015 Feb 11; 7(2). PMID: 25667985    Free PMC article.
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.
Clinical role of obinutuzumab in the treatment of naive patients with chronic lymphocytic leukemia.
Sonia Cerquozzi, Carolyn Owen.
Biologics, 2015 Mar 04; 9. PMID: 25733804    Free PMC article.
Antibody-mediated phagocytosis contributes to the anti-tumor activity of the therapeutic antibody daratumumab in lymphoma and multiple myeloma.
Marije B Overdijk, Sandra Verploegen, +8 authors, Paul W H I Parren.
MAbs, 2015 Mar 12; 7(2). PMID: 25760767    Free PMC article.
Highly Cited.
A bispecific antibody directly induces lymphoma cell death by simultaneously targeting CD20 and HLA-DR.
Jing Zeng, Ran Liu, Jinjing Wang, Yi Fang.
J Cancer Res Clin Oncol, 2015 Mar 17; 141(11). PMID: 25773122
Low Serum Vitamin D Levels Are Associated With Inferior Survival in Follicular Lymphoma: A Prospective Evaluation in SWOG and LYSA Studies.
Jennifer L Kelly, Gilles Salles, +12 authors, Jonathan W Friedberg.
J Clin Oncol, 2015 Apr 01; 33(13). PMID: 25823738    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.
Serum levels of anti-CCP antibodies, anti-MCV antibodies and RF IgA in the follow-up of patients with rheumatoid arthritis treated with rituximab.
Martina Fabris, Salvatore De Vita, +8 authors, Elio Tonutti.
Auto Immun Highlights, 2010 Nov 01; 1(2). PMID: 26000112    Free PMC article.
Role of B cells in tolerance induction.
James I Kim, David M Rothstein, James F Markmann.
Curr Opin Organ Transplant, 2015 Jun 25; 20(4). PMID: 26107970    Free PMC article.
Obinutuzumab for the treatment of patients with previously untreated chronic lymphocytic leukemia: overview and perspective.
Carolyn J Owen, Douglas A Stewart.
Ther Adv Hematol, 2015 Aug 20; 6(4). PMID: 26288711    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.
CD8⁺ T Cell-Independent Immune-Mediated Mechanisms of Anti-Tumor Activity.
G Elizabeth Pluhar, Christopher A Pennell, Michael R Olin.
Crit Rev Immunol, 2015 Sep 10; 35(2). PMID: 26351148    Free PMC article.
Sialylation of IgG Fc domain impairs complement-dependent cytotoxicity.
Isaak Quast, Christian W Keller, +7 authors, Jan D Lünemann.
J Clin Invest, 2015 Oct 06; 125(11). PMID: 26436649    Free PMC article.
Highly Cited.
Toll-like Receptor 4 Ligands Down-regulate Fcγ Receptor IIb (FcγRIIb) via MARCH3 Protein-mediated Ubiquitination.
Kavin Fatehchand, Li Ren, +7 authors, Jonathan P Butchar.
J Biol Chem, 2015 Dec 24; 291(8). PMID: 26694610    Free PMC article.
Influence of immunoglobulin isotype on therapeutic antibody function.
Stephen A Beers, Martin J Glennie, Ann L White.
Blood, 2016 Jan 15; 127(9). PMID: 26764357    Free PMC article.
Galectin-1 drives lymphoma CD20 immunotherapy resistance: validation of a preclinical system to identify resistance mechanisms.
Jacquelyn M Lykken, Mayuka Horikawa, +4 authors, Thomas F Tedder.
Blood, 2016 Feb 19; 127(15). PMID: 26888257    Free PMC article.
Protection from experimental autoimmune encephalomyelitis by polyclonal IgG requires adjuvant-induced inflammation.
Isaak Quast, Christian W Keller, +3 authors, Jan D Lünemann.
J Neuroinflammation, 2016 Feb 20; 13. PMID: 26893156    Free PMC article.
Tumor-associated macrophages and anti-tumor therapies: complex links.
Cristina Belgiovine, Maurizio D'Incalci, Paola Allavena, Roberta Frapolli.
Cell Mol Life Sci, 2016 Mar 10; 73(13). PMID: 26956893
Translating Inhibitory Fc Receptor Biology into Novel Therapeutic Approaches.
Falk Nimmerjahn.
J Clin Immunol, 2016 Mar 10; 36 Suppl 1. PMID: 26957094
Inflammation Causes Resistance to Anti-CD20-Mediated B Cell Depletion.
L H Laws, C E Parker, +7 authors, L V Riella.
Am J Transplant, 2016 Oct 28; 16(11). PMID: 27265023    Free PMC article.
The role of myeloid cells in cancer therapies.
Camilla Engblom, Christina Pfirschke, Mikael J Pittet.
Nat Rev Cancer, 2016 Jun 25; 16(7). PMID: 27339708
Highly Cited. Review.
CTLA-4 Limits Anti-CD20-Mediated Tumor Regression.
Zhenhua Ren, Jingya Guo, +7 authors, Yang-Xin Fu.
Clin Cancer Res, 2016 Jun 30; 23(1). PMID: 27354469    Free PMC article.
Integrating conventional and antibody-based targeted anticancer treatment into immunotherapy.
M Michelle Xu, Y Pu, R R Weichselbaum, Y-X Fu.
Oncogene, 2016 Jul 19; 36(5). PMID: 27425593    Free PMC article.
The PD-1/PD-L1 axis contributes to immune metabolic dysfunctions of monocytes in chronic lymphocytic leukemia.
M Qorraj, H Bruns, +5 authors, D Mougiakakos.
Leukemia, 2016 Aug 02; 31(2). PMID: 27479178
Near infrared photoimmunotherapy of B-cell lymphoma.
Tadanobu Nagaya, Yuko Nakamura, +3 authors, Hisataka Kobayashi.
Mol Oncol, 2016 Aug 12; 10(9). PMID: 27511870    Free PMC article.
CD16 is indispensable for antibody-dependent cellular cytotoxicity by human monocytes.
Wei Hseun Yeap, Kok Loon Wong, +7 authors, Siew Cheng Wong.
Sci Rep, 2016 Sep 28; 6. PMID: 27670158    Free PMC article.
Highly Cited.
Intravital imaging reveals improved Kupffer cell-mediated phagocytosis as a mode of action of glycoengineered anti-CD20 antibodies.
Capucine L Grandjean, Fabricio Montalvao, +7 authors, Philippe Bousso.
Sci Rep, 2016 Oct 05; 6. PMID: 27698437    Free PMC article.
Broadly Neutralizing Hemagglutinin Stalk-Specific Antibodies Induce Potent Phagocytosis of Immune Complexes by Neutrophils in an Fc-Dependent Manner.
Caitlin E Mullarkey, Mark J Bailey, +7 authors, Peter Palese.
mBio, 2016 Oct 06; 7(5). PMID: 27703076    Free PMC article.
Highly Cited.
A TLR7 agonist enhances the antitumor efficacy of obinutuzumab in murine lymphoma models via NK cells and CD4 T cells.
E J Cheadle, G Lipowska-Bhalla, +4 authors, T M Illidge.
Leukemia, 2016 Nov 29; 31(7). PMID: 27890931    Free PMC article.
Role of Fc-FcγR interactions in the antitumor activity of therapeutic antibodies.
Bryan C Barnhart, Michael Quigley.
Immunol Cell Biol, 2016 Dec 16; 95(4). PMID: 27974746
The Role and Function of Fcγ Receptors on Myeloid Cells.
Stylianos Bournazos, Taia T Wang, Jeffrey V Ravetch.
Microbiol Spectr, 2017 Jan 15; 4(6). PMID: 28087938    Free PMC article.
Successful cataract surgery in a patient with refractory Wegener's granulomatosis effectively treated with rituximab: A case report.
Abdullah M Alfawaz.
Saudi J Ophthalmol, 2017 Feb 18; 30(3). PMID: 28210182    Free PMC article.
Fcγ Receptor Heterogeneity in Leukocyte Functional Responses.
Carlos Rosales.
Front Immunol, 2017 Apr 05; 8. PMID: 28373871    Free PMC article.
Highly Cited. Review.
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.
Obinutuzumab-mediated high-affinity ligation of FcγRIIIA/CD16 primes NK cells for IFNγ production.
Cristina Capuano, Chiara Pighi, +7 authors, Ricciarda Galandrini.
Oncoimmunology, 2017 Apr 14; 6(3). PMID: 28405525    Free PMC article.
Signaling by Antibodies: Recent Progress.
Stylianos Bournazos, Taia T Wang, +2 authors, Jeffrey V Ravetch.
Annu Rev Immunol, 2017 Apr 28; 35. PMID: 28446061    Free PMC article.
Highly Cited. Review.
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.
Imaging B Cells in a Mouse Model of Multiple Sclerosis Using 64Cu-Rituximab PET.
Michelle L James, Aileen Hoehne, +12 authors, Sanjiv S Gambhir.
J Nucl Med, 2017 Jul 09; 58(11). PMID: 28687602    Free PMC article.
Insufficient Innate Immunity Contributes to the Susceptibility of the Castaneous Mouse to Orthopoxvirus Infection.
Patricia L Earl, Jeffrey L Americo, Bernard Moss.
J Virol, 2017 Jul 28; 91(19). PMID: 28747505    Free PMC article.
Vitamin D insufficiency is associated with an increased risk of early clinical failure in follicular lymphoma.
S I Tracy, M J Maurer, +14 authors, J R Cerhan.
Blood Cancer J, 2017 Aug 26; 7(8). PMID: 28841207    Free PMC article.
Impact of Depleting Therapeutic Monoclonal Antibodies on the Host Adaptive Immunity: A Bonus or a Malus?
Claire Deligne, Benoît Milcent, +2 authors, Sophie Sibéril.
Front Immunol, 2017 Sep 01; 8. PMID: 28855903    Free PMC article.
Therapeutic Potential of Shark Anti-ICOSL VNAR Domains is Exemplified in a Murine Model of Autoimmune Non-Infectious Uveitis.
Marina Kovaleva, Katherine Johnson, +2 authors, Andrew Porter.
Front Immunol, 2017 Oct 11; 8. PMID: 28993766    Free PMC article.
Therapeutic Antibodies: What Have We Learnt from Targeting CD20 and Where Are We Going?
Michael J E Marshall, Richard J Stopforth, Mark S Cragg.
Front Immunol, 2017 Oct 20; 8. PMID: 29046676    Free PMC article.
Modulating Cytotoxic Effector Functions by Fc Engineering to Improve Cancer Therapy.
Christian Kellner, Anna Otte, +2 authors, Matthias Peipp.
Transfus Med Hemother, 2017 Oct 27; 44(5). PMID: 29070978    Free PMC article.
Antibody Tumor Targeting Is Enhanced by CD27 Agonists through Myeloid Recruitment.
Anna H Turaj, Khiyam Hussain, +19 authors, Sean H Lim.
Cancer Cell, 2017 Dec 05; 32(6). PMID: 29198913    Free PMC article.
PD-1 blockade enhances elotuzumab efficacy in mouse tumor models.
Natalie A Bezman, Amy Jhatakia, +9 authors, Robert F Graziano.
Blood Adv, 2018 Jan 04; 1(12). PMID: 29296719    Free PMC article.
Autologous T-cell activation fosters ABT-199 resistance in chronic lymphocytic leukemia: rationale for a combined therapy with SYK inhibitors and anti-CD20 monoclonal antibodies.
Esteban Enrique Elías, María Belén Almejún, +14 authors, Romina Gamberale.
Haematologica, 2018 May 12; 103(10). PMID: 29748439    Free PMC article.
Monoclonal antibody-mediated killing of tumour cells by neutrophils.
Niels Heemskerk, Marjolein van Egmond.
Eur J Clin Invest, 2018 Jun 02; 48 Suppl 2. PMID: 29855035    Free PMC article.
Epitopes of MUC1 Tandem Repeats in Cancer as Revealed by Antibody Crystallography: Toward Glycopeptide Signature-Guided Therapy.
Dapeng Zhou, Lan Xu, Wei Huang, Torsten Tonn.
Molecules, 2018 Jun 03; 23(6). PMID: 29857542    Free PMC article.
Past, Present, and Future of Rituximab-The World's First Oncology Monoclonal Antibody Therapy.
Timothy M Pierpont, Candice B Limper, Kristy L Richards.
Front Oncol, 2018 Jun 20; 8. PMID: 29915719    Free PMC article.
Highly Cited. Review.
Shaving Is an Epiphenomenon of Type I and II Anti-CD20-Mediated Phagocytosis, whereas Antigenic Modulation Limits Type I Monoclonal Antibody Efficacy.
Lekh N Dahal, Chie-Yin Huang, +10 authors, Stephen A Beers.
J Immunol, 2018 Jul 13; 201(4). PMID: 29997125    Free PMC article.
Peripheral Blood B Cell Depletion after Rituximab and Complete Response in Lupus Nephritis.
Liliana Michelle Gomez Mendez, Matthew D Cascino, +7 authors, Paul Brunetta.
Clin J Am Soc Nephrol, 2018 Aug 10; 13(10). PMID: 30089664    Free PMC article.
IL-15 enhanced antibody-dependent cellular cytotoxicity mediated by NK cells and macrophages.
Meili Zhang, Bernard Wen, +8 authors, Thomas A Waldmann.
Proc Natl Acad Sci U S A, 2018 Oct 31; 115(46). PMID: 30373815    Free PMC article.
Anti-ICOSL New Antigen Receptor Domains Inhibit T Cell Proliferation and Reduce the Development of Inflammation in the Collagen-Induced Mouse Model of Rheumatoid Arthritis.
Ronan O'Dwyer, Marina Kovaleva, +8 authors, Caroline J Barelle.
J Immunol Res, 2018 Nov 13; 2018. PMID: 30417018    Free PMC article.
Versatile cell ablation tools and their applications to study loss of cell functions.
Fengming Liu, Shen Dai, +15 authors, Xuebin Qin.
Cell Mol Life Sci, 2019 Jul 31; 76(23). PMID: 31359086    Free PMC article.
Mechanisms of Resistance to Monoclonal Antibodies (mAbs) in Lymphoid Malignancies.
Pallawi Torka, Mathew Barth, Robert Ferdman, Francisco J Hernandez-Ilizaliturri.
Curr Hematol Malig Rep, 2019 Sep 29; 14(5). PMID: 31559580
Systemic and Intra-Nodal Activation of NK Cells After Rituximab Monotherapy for Follicular Lymphoma.
Monika Enqvist, Benedikt Jacobs, +5 authors, Karl-Johan Malmberg.
Front Immunol, 2019 Oct 02; 10. PMID: 31572357    Free PMC article.
The Essential Role Played by B Cells in Supporting Protective Immunity Against Trichuris muris Infection Is by Controlling the Th1/Th2 Balance in the Mesenteric Lymph Nodes and Depends on Host Genetic Background.
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Front Immunol, 2020 Jan 11; 10. PMID: 31921120    Free PMC article.
Flow cytometry-based assessment of direct-targeting anti-cancer antibody immune effector functions.
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Methods Enzymol, 2020 Feb 01; 632. PMID: 32000909    Free PMC article.
Site-specific N-glycan Analysis of Antibody-binding Fc γ Receptors from Primary Human Monocytes.
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Mol Cell Proteomics, 2020 Jan 01; 19(2). PMID: 31888963    Free PMC article.
Current Strategies to Target Tumor-Associated-Macrophages to Improve Anti-Tumor Immune Responses.
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Cells, 2019 Dec 28; 9(1). PMID: 31878087    Free PMC article.
There Is (Scientific) Strength in Numbers: A Comprehensive Quantitation of Fc Gamma Receptor Numbers on Human and Murine Peripheral Blood Leukocytes.
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Front Immunol, 2020 Mar 03; 11. PMID: 32117269    Free PMC article.
Sex differences in vaccine-induced humoral immunity.
Stephanie Fischinger, Carolyn M Boudreau, +2 authors, Galit Alter.
Semin Immunopathol, 2018 Dec 14; 41(2). PMID: 30547182    Free PMC article.
PD-L1 and tumor-associated macrophages in de novo DLBCL.
Ronald McCord, Christopher R Bolen, +5 authors, Jeffrey M Venstrom.
Blood Adv, 2019 Feb 17; 3(4). PMID: 30770362    Free PMC article.
Functional diversification of hybridoma-produced antibodies by CRISPR/HDR genomic engineering.
Johan M S van der Schoot, Felix L Fennemann, +18 authors, Ferenc A Scheeren.
Sci Adv, 2019 Sep 07; 5(8). PMID: 31489367    Free PMC article.
High-resolution quantification of discrete phagocytic events by live cell time-lapse high-content microscopy imaging.
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J Cell Sci, 2020 Feb 02; 133(5). PMID: 32005699    Free PMC article.
Targeting the Antibody Checkpoints to Enhance Cancer Immunotherapy-Focus on FcγRIIB.
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Front Immunol, 2019 Apr 02; 10. PMID: 30930905    Free PMC article.
A transcriptional signature accurately identifies Aspergillus Infection across healthy and immunosuppressed states.
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Transl Res, 2020 Mar 14; 219. PMID: 32165060    Free PMC article.
Disrupting LILRB4/APOE Interaction by an Efficacious Humanized Antibody Reverses T-cell Suppression and Blocks AML Development.
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Cancer Immunol Res, 2019 Jun 20; 7(8). PMID: 31213474    Free PMC article.
Harnessing the immune system via FcγR function in immune therapy: a pathway to next-gen mAbs.
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Immunol Cell Biol, 2020 Mar 12; 98(4). PMID: 32157732    Free PMC article.
Specialization of mucosal immunoglobulins in pathogen control and microbiota homeostasis occurred early in vertebrate evolution.
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Innate Immune Defense Mechanisms by Myeloid Cells That Hamper Cancer Immunotherapy.
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Front Immunol, 2020 Aug 01; 11. PMID: 32733461    Free PMC article.
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Contributions of natural killer cells to the immune response against Plasmodium.
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Malar J, 2019 Sep 20; 18(1). PMID: 31533835    Free PMC article.
The Role of Complement in the Mechanism of Action of Therapeutic Anti-Cancer mAbs.
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Antibodies (Basel), 2020 Nov 01; 9(4). PMID: 33126570    Free PMC article.
Complement Activation in the Treatment of B-Cell Malignancies.
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Antibodies (Basel), 2020 Dec 05; 9(4). PMID: 33271825    Free PMC article.
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.
Harnessing innate immunity in cancer therapy.
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Tumor-associated myeloid cells: diversity and therapeutic targeting.
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Cell Mol Immunol, 2021 Jan 22; 18(3). PMID: 33473192    Free PMC article.
Complement-Dependent Activity of CD20-Specific IgG Correlates With Bivalent Antigen Binding and C1q Binding Strength.
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Front Immunol, 2021 Jan 29; 11. PMID: 33505398    Free PMC article.
Imaging the mechanisms of anti-CD20 therapy in vivo uncovers spatiotemporal bottlenecks in antibody-dependent phagocytosis.
Capucine L Grandjean, Zacarias Garcia, +2 authors, Philippe Bousso.
Sci Adv, 2021 Feb 21; 7(8). PMID: 33608271    Free PMC article.
Autoantibodies Targeting Intracellular and Extracellular Proteins in Autoimmunity.
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Front Immunol, 2021 Mar 26; 12. PMID: 33763057    Free PMC article.
Harnessing and Enhancing Macrophage Phagocytosis for Cancer Therapy.
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Front Immunol, 2021 Apr 02; 12. PMID: 33790906    Free PMC article.
The Type II Anti-CD20 Antibody Obinutuzumab (GA101) Is More Effective Than Rituximab at Depleting B Cells and Treating Disease in a Murine Lupus Model.
Anthony D Marinov, Haowei Wang, +7 authors, Mark J Shlomchik.
Arthritis Rheumatol, 2020 Dec 06; 73(5). PMID: 33277983    Free PMC article.
Murlentamab, a Low Fucosylated Anti-Müllerian Hormone Type II Receptor (AMHRII) Antibody, Exhibits Anti-Tumor Activity through Tumor-Associated Macrophage Reprogrammation and T Cell Activation.
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Cancers (Basel), 2021 May 01; 13(8). PMID: 33924378    Free PMC article.
Afucosylated IgG Targets FcγRIV for Enhanced Tumor Therapy in Mice.
Rens Braster, Marijn Bögels, +8 authors, Gestur Vidarsson.
Cancers (Basel), 2021 Jun 03; 13(10). PMID: 34069226    Free PMC article.
Tight nanoscale clustering of Fcγ receptors using DNA origami promotes phagocytosis.
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Elife, 2021 Jun 04; 10. PMID: 34080973    Free PMC article.
Development of a Macrophage-Based ADCC Assay.
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Vaccines (Basel), 2021 Jul 03; 9(6). PMID: 34204268    Free PMC article.
Prognostic significance of FCGR2B expression for the response of DLBCL patients to rituximab or obinutuzumab treatment.
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Blood Adv, 2021 Jul 30; 5(15). PMID: 34323958    Free PMC article.
Novel oncolytic adenovirus expressing enhanced cross-hybrid IgGA Fc PD-L1 inhibitor activates multiple immune effector populations leading to enhanced tumor killing in vitro, in vivo and with patient-derived tumor organoids.
Firas Hamdan, Erkko Ylösmäki, +18 authors, Vincenzo Cerullo.
J Immunother Cancer, 2021 Aug 08; 9(8). PMID: 34362830    Free PMC article.
Testicular Diffuse Large B-Cell Lymphoma-Clinical, Molecular, and Immunological Features.
Marjukka Pollari, Suvi-Katri Leivonen, Sirpa Leppä.
Cancers (Basel), 2021 Aug 28; 13(16). PMID: 34439203    Free PMC article.
Targeting B cells in the pre-phase of systemic autoimmunity globally interferes with autoimmune pathology.
Anja Werner, Simon Schäfer, +7 authors, Falk Nimmerjahn.
iScience, 2021 Sep 30; 24(9). PMID: 34585117    Free PMC article.
Remodeling the Tumor Myeloid Landscape to Enhance Antitumor Antibody Immunotherapies.
Khiyam Hussain, Mark S Cragg, Stephen A Beers.
Cancers (Basel), 2021 Oct 14; 13(19). PMID: 34638388    Free PMC article.
The selection of variable regions affects effector mechanisms of IgA antibodies against CD20.
Mitchell Evers, Thies Rösner, +12 authors, Thomas Valerius.
Blood Adv, 2021 Sep 16; 5(19). PMID: 34525171    Free PMC article.
Humoral immunity in hepatitis B virus infection: Rehabilitating the B in HBV.
Thomas Vanwolleghem, Tom Adomati, Stijn Van Hees, Harry L A Janssen.
JHEP Rep, 2022 Jan 22; 4(2). PMID: 35059620    Free PMC article.
Fc-null anti-PD-1 monoclonal antibodies deliver optimal checkpoint blockade in diverse immune environments.
Julia Moreno-Vicente, Jane E Willoughby, +11 authors, Stephen A Beers.
J Immunother Cancer, 2022 Jan 13; 10(1). PMID: 35017153    Free PMC article.
Tumor-Associated Macrophages: Reasons to Be Cheerful, Reasons to Be Fearful.
Izabela Szulc-Kielbik, Michal Kielbik.
Exp Suppl, 2022 Feb 16; 113. PMID: 35165862
Rituximab in patients with acute ST-elevation myocardial infarction: an experimental medicine safety study.
Tian X Zhao, Muhammad Aetesam-Ur-Rahman, +9 authors, Ziad Mallat.
Cardiovasc Res, 2021 Mar 31; 118(3). PMID: 33783498    Free PMC article.
Macrophage-Based Combination Therapies as a New Strategy for Cancer Immunotherapy.
Lin Tian, Anhua Lei, +4 authors, Jin Zhang.
Kidney Dis (Basel), 2022 Mar 01; 8(1). PMID: 35224005    Free PMC article.
Promoting antibody-dependent cellular phagocytosis for effective macrophage-based cancer immunotherapy.
Xu Cao, Jing Chen, +9 authors, Mingye Feng.
Sci Adv, 2022 Mar 19; 8(11). PMID: 35302839    Free PMC article.
Immunomodulatory Treatment Strategies Targeting B Cells for Heart Failure.
Xinxin Zhang, Yuxi Sun, +3 authors, Ying Liu.
Front Pharmacol, 2022 Mar 31; 13. PMID: 35350762    Free PMC article.
HIF activation enhances FcγRIIb expression on mononuclear phagocytes impeding tumor targeting antibody immunotherapy.
Khiyam Hussain, Rena Liu, +28 authors, Mark S Cragg.
J Exp Clin Cancer Res, 2022 Apr 09; 41(1). PMID: 35392965    Free PMC article.
The Role of Myeloid Cells in Hepatotoxicity Related to Cancer Immunotherapy.
Cathrin L C Gudd, Lucia A Possamai.
Cancers (Basel), 2022 Apr 24; 14(8). PMID: 35454819    Free PMC article.