Anti-CD20 monoclonal antibody-dependent phagocytosis of chronic lymphocytic leukaemia cells by autologous macrophages

Clinical and Experimental Immunology

Volumn 183, Issue 1, 2016, Pages 90-101

  Church, A K ^a   Vandermeid, K R ^b   Baig, N A ^a   Baran, A M ^b   Witzig, T E ^a   Nowakowski, G S ^a   Zent, C S ^b  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Alemtuzumab; Anti CD20 monoclonal antibodies; Antibody dependent phagocytosis; Chronic lymphocytic leukaemia; CLL; Macrophage; Obinotuzumab; Ocaratuzumab; Ofatumumab; Rituximab; Ublituximab

Indexed keywords

ALEMTUZUMAB; CD20 ANTIGEN; CD52 ANTIGEN; OBINUTUZUMAB; OCARATUZUMAB; OFATUMUMAB; RITUXIMAB; UBLITUXIMAB; MONOCLONAL ANTIBODY;

ANTIBODY DEPENDENT PHAGOCYTOSIS; ANTIGEN EXPRESSION; ARTICLE; CHRONIC LYMPHATIC LEUKEMIA; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG EFFICACY; EFFECTOR CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA CELL; MACROPHAGE; MONOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; CELL CULTURE; CELL DIFFERENTIATION; COMBINATION DRUG THERAPY; COMPARATIVE STUDY; DRUG EFFECTS; IMMUNOLOGY; IMMUNOTHERAPY; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; PROCEDURES;

ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; CELL DIFFERENTIATION; CELLS, CULTURED; DRUG THERAPY, COMBINATION; HUMANS; IMMUNOTHERAPY; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MACROPHAGES; PHAGOCYTOSIS; RITUXIMAB;

EID: 84955385349     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12697     Document Type: Article

References (38)

1. Hallek M, Fischer K, Fingerle-Rowson G et al. Addition of rituximab to fludarabine and cyclophosphamide in patients with chronic lymphocytic leukaemia: a randomised, open-label, phase 3 trial. Lancet 2010; 376:1164-74.
2. Taylor RP, Lindorfer MA. Analyses of CD20 monoclonal antibody-mediated tumor cell killing mechanisms: rational design of dosing strategies. Mol Pharmacol 2014; 86:485-91.
3. Uchida J, Hamaguchi Y, Oliver JA et al. The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med 2004; 199:1659-69.
4. Lefebvre ML, Krause SW, Salcedo M, Nardin A. Ex vivo-activated human macrophages kill chronic lymphocytic leukemia cells in the presence of rituximab: mechanism of antibody-dependent cellular cytotoxicity and impact of human serum. J Immunother 2006; 29:388-97.
5. Montalvao F, Garcia Z, Celli S et al. The mechanism of anti-CD20-mediated B cell depletion revealed by intravital imaging. J Clin Invest 2013; 123:5098-103.
6. Gul N, Babes L, Siegmund K et al. Macrophages eliminate circulating tumor cells after monoclonal antibody therapy. J Clin Invest 2014; 124:812-23.
7. Golay J, Introna M. Mechanism of action of therapeutic monoclonal antibodies: promises and pitfalls of in vitro and in vivo assays. Arch Biochem Biophys 2012; 526:146-53.
8. Weiskopf K, Weissman IL. Macrophages are critical effectors of antibody therapies for cancer. MAbs 2015; 7:303-10.
9. Pallasch CP, Leskov I, Braun CJ et al. Sensitizing protective tumor microenvironments to antibody-mediated therapy. Cell 2014; 156:590-602.
10. Hallek M, Cheson BD, Catovsky D et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia (IWCLL) updating the National Cancer Institute-Working Group (NCI-WG) 1996 guidelines. Blood 2008; 111:5446-56.
11. Baig NA, Taylor RP, Lindorfer MA et al. Induced resistance to ofatumumab-mediated cell clearance mechanisms, including complement-dependent cytotoxicity, in chronic lymphocytic leukemia. J Immunol 2014; 192:1620-9.
12. Baig NA, Taylor RP, Lindorfer MA et al. Complement dependent cytotoxicity (CDC) in chronic lymphocytic leukemia (CLL): Ofatumumab enhances alemtuzumab CDC and reveals cells resistant to activated complement. Leuk Lymphoma 2012; 53(11):2218-2227.
13. Leidi M, Gotti E, Bologna L et al. M2 macrophages phagocytose rituximab-opsonized leukemic targets more efficiently than m1 cells in vitro. J Immunol 2009; 182:4415-22.
14. Beurskens FJ, Lindorfer MA, Farooqui M et al. Exhaustion of cytotoxic effector systems may limit monoclonal antibody-based immunotherapy in cancer patients. J Immunol 2012; 188:3532-41.
15. Yeo JC, Wall AA, Stow JL, Hamilton NA. High-throughput quantification of early stages of phagocytosis. BioTechniques 2013; 55:115-24.
16. Flannagan RS, Jaumouille V, Grinstein S. The cell biology of phagocytosis. Annu Rev Pathol 2012; 7:61-98.
17. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull 1979; 86:420-8.
18. Kellner C, Derer S, Valerius T, Peipp M. Boosting ADCC and CDC activity by Fc engineering and evaluation of antibody effector functions. Methods 2014; 65:105-13.
19. Gustafson MP, Abraham RS, Lin Y et al. Association of an increased frequency of CD14(+) HLA-DR(lo/neg) monocytes with decreased time to progression in chronic lymphocytic leukaemia (CLL). Br J Haematol 2012; 156:674-6.
20. Maffei R, Bulgarelli J, Fiorcari S et al. The monocytic population in chronic lymphocytic leukemia shows altered composition and deregulation of genes involved in phagocytosis and inflammation. Haematologica 2013; 98:1115-23.
21. Boissard F, Fournie JJ, Laurent C, Poupot M, Ysebaert L. Nurse like cells: chronic lymphocytic leukemia associated macrophages. Leuk Lymphoma 2015; 56:1570-1572.
22. Teeling JL, French RR, Cragg MS et al. Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin lymphomas. Blood 2004; 104:1793-800.
23. Teeling JL, Mackus WJ, Wiegman LJ et al. The biological activity of human CD20 monoclonal antibodies is linked to unique epitopes on CD20. J Immunol 2006; 177:362-71.
24. Griffin FM Jr, Griffin JA, Leider JE, Silverstein SC. Studies on the mechanism of phagocytosis. I. Requirements for circumferential attachment of particle-bound ligands to specific receptors on the macrophage plasma membrane. J Exp Med 1975; 142:1263-82.
25. de Romeuf C, Dutertre CA, Le Garff-Tavernier M et al. Chronic lymphocytic leukaemia cells are efficiently killed by an anti-CD20 monoclonal antibody selected for improved engagement of FcgammaRIIIA/CD16. Br J Haematol 2008; 140:635-43.
26. Mossner E, Brunker P, Moser S et al. 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. Blood 2010; 115:4393-402.
27. Forero-Torres A, de Vos S, Pohlman BL et al. Results of a phase 1 study of AME-133v (LY2469298), an Fc-engineered humanized monoclonal anti-CD20 antibody, in FcgammaRIIIa-genotyped patients with previously treated follicular lymphoma. Clin Cancer Res 2012; 18:1395-403.
28. Schreiber AD, Frank MM. Role of antibody and complement in the immune clearance and destruction of erythrocytes. II. Molecular nature of IgG and IgM complement-fixing sites and effects of their interaction with serum. J Clin Invest 1972; 51:583-9.
29. Ehlenberger AG, Nussenzweig V. The role of membrane receptors for C3b and C3d in phagocytosis. J Exp Med 1977; 145:357-71.
30. Kabbash L, Esdaile J, Shenker S et al. Reticuloendothelial system Fc receptor function in systemic lupus erythematosus: effect of decreased sensitization on clearance of autologous erythrocytes. J Rheumatol 1987; 14:487-9.
31. Lindorfer MA, Kohl J, Taylor RP. Interactions between the complement system and Fcg receptors. In: Ackerman ME, Nimmerhahn F, eds. Antibody Fc: linking adaptive and innate immunity. Philadelphia: Elsevier Press, 2014:49-74.
32. Bleeker WK, Munk ME, Mackus WJ et al. Estimation of dose requirements for sustained in vivo activity of a therapeutic human anti-CD20 antibody. Br J Haematol 2008; 140:303-12.
33. Taylor RP, Lindorfer MA. Fcgamma-receptor-mediated trogocytosis impacts mAb-based therapies: historical precedence and recent developments. Blood 2015; 125:762-6.
34. Zent CS, Taylor RP, Lindorfer MA et al. 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. Am J Hematol 2014; 89:757-65.
35. Da Roit F, Engelberts PJ, Taylor RP et al. Ibrutinib interferes with the cell-mediated anti-tumor activities of therapeutic CD20 antibodies: implications for combination therapy. Haematologica 2015; 100:77-86.
36. Borge M, Almejun MB, Podaza E et al. Ibrutinib impairs the phagocytosis of rituximab-coated leukemic cells from chronic lymphocytic leukemia patients by human macrophages. Haematologica 2015; 100:e140-142.
37. Duong MN, Matera EL, Mathe D et al. Effect of kinase inhibitors on the therapeutic properties of monoclonal antibodies. MAbs 2015; 7:192-8.
38. Hepburn AL, Mason JC, Wang S et al. Both Fcgamma and complement receptors mediate transfer of immune complexes from erythrocytes to human macrophages under physiological flow conditions in vitro. Clin Exp Immunol 2006; 146:133-45.