Activation of complement by monoclonal antibodies that target cell-associated β2-microglobulin: Implications for cancer immunotherapy

Molecular Immunology

Volumn 56, Issue 4, 2013, Pages 549-560

  Pokrass, Michael J ^a   Liu, Monica F ^a   Lindorfer, Margaret A ^a   Taylor, Ronald P ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Antibodies; Beta 2 microglobulin; Cancer immunotherapy; Complement; Human

Indexed keywords

BETA 2 MICROGLOBULIN; COMPLEMENT COMPONENT C3B; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; IMMUNOGLOBULIN G2B; MONOCLONAL ANTIBODY; IMMUNOGLOBULIN G; PROTEIN BINDING;

ARTICLE; CANCER IMMUNOTHERAPY; COMPLEMENT ACTIVATION; COMPLEMENT DEPENDENT CYTOTOXICITY; CYTOLYSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; HLA SYSTEM; HUMAN; HUMAN CELL; HUMAN TISSUE; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STOICHIOMETRY; TARGET CELL; TUMOR CELL LINE; ANIMAL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; CELL CULTURE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; IMMUNOLOGY; IMMUNOTHERAPY; JURKAT CELL LINE; METABOLISM; NEOPLASMS; NEUTROPHIL; PATHOLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; BETA 2-MICROGLOBULIN; CELL LINE, TUMOR; CELLS, CULTURED; COMPLEMENT ACTIVATION; COMPLEMENT C3B; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; IMMUNOGLOBULIN G; IMMUNOTHERAPY; JURKAT CELLS; LEUKOCYTES, MONONUCLEAR; MICE; MICROSCOPY, FLUORESCENCE; NEOPLASMS; NEUTROPHILS; PROTEIN BINDING;

EID: 84881096011     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.05.242     Document Type: Article

References (66)

1. Barnstable C.J., Bodmer W.F., Brown G., Galfre G., Milstein C., Williams A.F., Ziegler A. Production of monoclonal antibodies to Group A erythrocytes, HLA and other human cell surface antigens-new tools for genetic analysis. Cell 1978, 14:9-20.
2. Beum P.V., Kennedy A.D., Taylor R.P. 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. Journal of Immunological Methods 2004, 289:97-109.
3. Beum P.V., Kennedy A.D., Williams M.E., Lindorfer M.A., Taylor R.P. The shaving reaction: Rituximab/CD20 complexes are removed from mantle cell lymphoma and chronic lymphocytic leukemia cells by THP-1 monocytes. Journal of Immunology 2006, 176:2600-2609.
4. Beum P.V., Lindorfer M.A., Beurskens F., Stukenberg P.T., Lokhorst H.M., Pawluczkowycz A.W., Parren P.W., van de Winkel J.G., Taylor R.P. Complement activation on B lymphocytes opsonized with rituximab or ofatumumab produces substantial changes in membrane structure preceding cell lysis. Journal of Immunology 2008, 181:822-832.
5. Beum P.V., Lindorfer M.A., Peek E.M., Stukenberg P.T., de Weers M., Beurskens F.J., Parren P.W.H.I., van de Winkel J.G.J., Taylor R.P. Penetration of antibody-opsonized cells by the membrane attack complex of complement promotes Ca2+ influx and induces streamers. European Journal of Immunology 2011, 41:2436-2446.
6. Beum P.V., Lindorfer M.A., Taylor R.P. 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. Journal of Immunology 2008, 181:2916-2924.
7. Beum P.V., Mack D.A., Pawluczkowycz A.W., Lindorfer M.A., Taylor R.P. Binding of rituximab, trastuzumab, cetuximab, or mAb T101 to cancer cells promotes trogocytosis mediated by THP-1 cells and monocytes. Journal of Immunology 2008, 181:8120-8132.
8. Blok V.T., Daha M.R., Tijsma O., Harris C.L., Morgan B.P., Gleuren G.J., Gorter A. A bispecific monoclonal antibody directed against both the membrane-bound complement regulator CD55 and the renal tumor-associated antigen G250 enhances C3 deposition and tumor cell lysis by complement. Journal of Immunology 1998, 160:3437-3443.
9. Bowles J.A., Wang S.-Y., Link B.K., Beuerlein G., Campbell M.-A., Marquis D., Ondek B., Wooldridge J.E., Smith B.J., Breitmeyer J.B., Weiner G.J. Anti-CD20 monoclonal antibody with enhanced affinity for CD16 activates NK cells at lower concentrations and more effectively than rituximab. Blood 2006, 108:2648-2654.
10. Brodsky F.M., Bodmer W.F., Parham P. Characterization of a monoclonal anti-beta2-microglobulin antibody and its use in the genetic and biochemical analysis of major histocompatibility antigens. European Journal of Immunology 1979, 9:536-545.
11. Cao Y., Lan Y., Qian J., Zheng Y., Hong S., Li H., Wang M., Kwak L.W., Lin D., Yang J., Yi Q. Targeting cell surface β2-microglobulin by pentameric IgM antibodies. British Journal of Haematology 2011, 154:111-121.
12. Carter P.J. Potent antibody therapeutics by design. Nature Reviews Immunology 2006, 6:343-357.
13. Chang J.H., Sutherland W.M., Parsons S.J. Monoclonal antibodies to oncoproteins. Methods in Enzymology 1995, 254:430-445.
14. Clayton A., Harris C.L., Court J., Mason M.D., Morgan B.P. Antigen-presenting cell exosomes are protected from complement-mediated lysis by expression of CD55 and CD59. European Journal of Immunology 2003, 33:522-531.
15. Craig M.L., Bankovich A.J., Taylor R.P. Visualization of the transfer reaction: tracking immune complexes from erythrocyte complement receptor 1 to macrophages. Clinical Immunology 2002, 105:36-47.
16. da Silveira S.A., Kikuchi S., Fossati-Jimack L., Moll T., Saito T., Verbeek J.S., Botto M., Walport M.J., Carroll M., Izui S. Complement activation selectively potentiates the pathogenicity of the IgG2b and IgG3 isotypes of a high affinity anti-erythrocyte autoantibody. Journal of Experimental Medicine 2002, 195:665-672.
17. Dangl J.L., Wensel T.G., Morrison S.L., Stryer L., Herzenberg L.A., Oi V.T. Segmental flexibility and complement fixation of genetically engineered chimeric human, rabbit and mouse antibodies. EMBO Journal 1988, 7:1989-1994.
18. Datema G., Stein S., Eijsink C., Mulder A., Claas F.H.J., Doxiadis I.I.N. HLA-C expression on platelets: studies with an HLA-Cw1-specific human monoclonal antibody. Vox Sanguinis 2000, 79:108-111.
19. del Conde I., Cruz M.A., Zhang H., Lopez J.A., Afshar-Kharghan V. Platelet activation leads to activation and propagation of the complement system. Journal of Experimental Medicine 2005, 201:871-879.
20. Estrov Z., Talpaz M., Ku S., Harris D., Van Q., Beran M., Hirsch-Ginsberg C., Huh Y., Yee G., Kurzrock R. Z-138: a new mature B-cell acute lymphoblastic leukemia cell line from a patient with transformed chronic lymphocytic leukemia. Leukemia Research 1998, 22:341-353.
21. Golay J., Introna M. Mechanism of action of therapeutic monoclonal antibodies. Promises and pitfalls of in vitro and in vivo assays. Archives of Biochemistry and Biophysics 2012, 526:146-153.
22. Hahn C.S., French O.G., Foley P., Martin E.N., Taylor R.P. Bispecific monoclonal antibodies mediate binding of dengue virus to erythrocytes in a monkey model of passive viremia. Journal of Immunology 2001, 166:1057-1065.
23. Hamad O.A., Nilsson P.H., Wouters D., Lambris J.D., Ekdahl K.N., Nilsson B. Complement component C3 binds to activated normal platelets without preceding proteolytic activation and promotes binding to complement receptor I. Journal of Immunology 2010, 184:2686-2692.
24. Harris C.L., Lublin D.M., Morgan B.P. Efficient generation of monoclonal antibodies for specific protein domains using recombinant immunoglobulin fusion proteins: pitfalls and solutions. Journal of Immunological Methods 2002, 268:245-258.
25. Hartley P.S., Savill J., Brown S.B. The death of human platelets during incubation in citrated plasma involves shedding of CD42b and aggregation of dead platelets. Thrombosis and Haemostasis 2005, 95:100-106.
26. Hartley P.S., Savill J.S., Brown S.B. Hypoglycaemia predisposes platelets to death by affecting calcium homeostasis and mitochondrial integrity. Platelets 2007, 18:103-112.
27. Hillmen P., Young N.S., Schubert J., Brodsky R.A., Socie G., Muus P., Roth A., Szer J., Elbute M.E., Nakamura R., Browne P., Risitano A.M., Hill A., Schrezenmeier H., Fu C.L., Maciejewski J., Rollins S.A., Mojcik C.F., Rother R.P., Luzzatto L. The complement inhibitor eculizumab in paroxysmal nocturnal hemoglobinuria. New England Journal of Medicine 2006, 355:1233-1243.
28. Huang W.C., Zhau H.E., Chung L.W.K. Androgen receptor survival signaling is blocked by anti-β2-microglobulin monoclonal antibody via a MAPK/lipogenic pathway in human prostrate cancer cells. Journal of Biological Chemistry 2010, 285:7947-7956.
29. Johnson L.N., Winter K.M., Reid S., Hartkopf-Theis T., Marks D.C. Cryopreservation of buffy-coat derived platelet concentrations in dimethyl sulfoxide and platelet additive solution. Cryobiology 2011, 62:100-106.
30. Josson S., Nomura T., Lin J.T., Huang W.C., Wu D., Zhau H.E., Zayzafoon M., Weizmann M.N., Gururagan M., Chung L.W.K. β2-Microglobulin induces epithelial to mesenchymal transition and confers cancer lethality and bone metastasis in human cancer cells. Cancer Research 2011, 71:2600-2610.
31. Kao K.J., Cook D.J., Scornik J.C. Quantitative analysis of platelet surface HLA by W6/32 anti-HLA monoclonal antibody. Blood 1968, 68:627-632.
32. Kennedy A.D., Beum P.V., Solga M.D., DiLillo D.J., Lindorfer M.A., Hess C.E., Densmore J.J., Williams M.E., Taylor R.P. Rituximab infusion promotes rapid complement depletion and acute CD20 loss in chronic lymphocytic leukemia. Journal of Immunology 2004, 172:3280-3288.
33. Kennedy A.D., Solga M.D., Schuman T.A., Chi A.W., Lindorfer M.A., Sutherland W.M., Foley P.L., Taylor R.P. An anti-C3b(i) mAb enhances complement activation, C3b(i) deposition, and killing of CD20+ cells by Rituximab. Blood 2003, 101:1071-1079.
34. Klaus G.G.B., Pepys M.B., Kitajima K., Askonas B.A. Activation of mouse complement by different classes of mouse antibody. Immunology 1979, 38:687-695.
35. Lindorfer M.A., Jinivizian H.B., Foley P.L., Kennedy A.D., Solga M.D., Taylor R.P. The B cell complement receptor 2 transfer reaction. Journal of Immunology 2003, 170:3671-3678.
36. Lindorfer M.A., Wiestner A., Zent C.S., Taylor R.P. Monoclonal antibody (mAb)-based cancer therapy: Is it time to reevaluate dosing strategies?. Oncoimmunology 2012, 1:959-961.
37. McKenzie S.E. The yin and yang of Fcγ receptors in ITP. Blood 2008, 111:971-972.
38. Meli A., Carter T., McCormack A., Hannah M.J., Rose M.L. Antibody alone is not a stimulator of exocytosis of Weibel-Palade bodies from human endothelial cells. Transplantation 2012, 94:794-801.
39. Minard-Colin V., Xiu Y., Poe J.C., Horikawa M., Magro C.M., Hamaguchi Y., Haas K.M., Tedder T.F. Lymphoma depletion during CD20 immunotherapy in mice is mediated by macrophage FcγRI, FcγRIII and FcγRIV. Blood 2008, 112:1205-1213.
40. Najaoui A., Bakchoul T., Stoy J., Bein G., Rummel M.J., Santoso S., Sachs U.J. Autoantibody-mediated complement activation on platelets is a common finding in patients with immune thrombocytopenic purpura (ITP). European Journal of Haematology 2012, 88:167-174.
41. Natarajan K., Li H., Mariuzza R.A., Margulies D.H. MHC class I molecules, structure and function. Reviews in Immunogenetics 1999, 1:32-46.
42. Neuberger M.S., Rajewsky K. Activation of mouse complement by monoclonal mouse antibodies. European Journal of Immunology 1981, 11:1012-1016.
43. Nimmerjahn F., Ravetch J.V. Antibodies, Fc receptors and cancer. Current Opinion in Immunology 2007, 19:239-245.
44. Oi V.T., Vuong T.M., Hardy R., Reidler J., Dangl J., Herzenberg L.A., Stryer L. Correlation between segmental flexibility and effector function of antibodies. Nature 1984, 307:136-140.
45. Overdijk M.B., Verploegen S., Buijsse A.O., Vink T., Leusen J.H.W., Bleeker W.K., Parren P.W.H.I. Crosstalk between human IgG isotypes and murine effector cells. Journal of Immunology 2012, 189:3430-3438.
46. Peerschke E.I., Yin W., Ghebrehiwet B. Complement activation on platelets. Implication for vascular inflammation and thrombosis. Molecular Immunology 2010, 47:2170-2175.
47. Peerschke E.I., Yin W., Grigg S.E., Ghebrehiwet B. Blood platelets activate the classical pathway of human complement. Journal of Thrombosis and Haemostasis 2006, 4:2035-2042.
48. Peerschkle E.I., Reid K.B.M., Ghebrehiwet B. Platelet activation by C1q results in the induction of αIIb/β3 Integrins (GPIIb-IIIa) and the expression of P-selectin and procoagulant activity. Journal of Experimental Medicine 1993, 178:579-587.
49. Rother R.R., Rollins S.A., Mojcik C.F., Brodsky R.A., Bell L. Discovery and development of the complement inhibitor eculizumab for the treatment of paroxysmal nocturnal hemoglobinuria. Nature Biotechnology 2007, 25:1256-1264.
50. Ruuls S.R., Lammerts van Beueren J.J., van de Winkel J.G.J., Parren W.H.I. Novel human antibody therapeutics: the age of the Umabs. Biotechnology Journal 2008, 3:1157-1171.
51. Sartz L., Olin A.I., Kristoffersson A.C., Stahl A., Johansson M.E., Westman K., Fremeaux-Bacchi V., Nilsson-Ekdahl K., Karpman D. A novel C3 mutation causing increased formation of the C3 convertase in familial atypical hemolytic uremic syndrome. Journal of Immunology 2012, 188:2030-2037.
52. Song S., Crow A.R., Siragam V., Freedman J., Lazarus A.H. Monoclonal antibodies that mimic the action of anti-D in the amelioration of murine ITP act by a mechanism distinct from that of IVIg. Blood 2005, 105:1546-1548.
53. Stahl A., Vaziri-Sani F., Heinen S., Kristoffersson A.-C., Gydell K.-H., Raafat R., Gutierrez A., Beringer O., Zipfel P.F., Karpman D. Factor H dysfunction in patients with atypical hemolytic uremic syndrome contributes to complement deposition on platelets and their activation. Blood 2008, 111:5307-5315.
54. Taylor R.P., Lindorfer M.A. Drug Insight: the mechanism of action of rituximab in autoimmune disease-the immune complex decoy hypothesis. Nature Clinical Practice Rheumatology 2007, 3:86-95.
55. Taylor R.P., Lindorfer M.A. Immunotherapeutic mechanisms of anti-CD20 monoclonal antibodies. Current Opinion in Immunology 2008, 20:444-449.
56. Taylor R.P., Martin E.N., Reinagel M.L., Nardin A., Craig M., Choice Q., Schlimgen R., Greenbaum S., Incardona N.L., Ochs H.D. Bispecific monoclonal antibody complexes facilitate erythrocyte binding and liver clearance of a prototype particulate pathogen in a monkey model. Journal of Immunology 1997, 159:4035-4044.
57. Teeling J.L., French R.R., Cragg M.S., van den Brakel J., Pluyter M., Huang H., Chan C., Parren P.W., Hack C.E., Dechant M., Valerius T., van de Winkel J.G., Glennie M.J. Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin's lymphomas. Blood 2004, 104:1793-1800.
58. Vikentiou M., Psarra K., Kapsimali V., Liapis K., Michael M., Tsionos K., Lianidou E., Papasteriades C. Distinct neutrophil subpopulations phenotype by flow cytometry in myelodysplastic syndromes. Leukemia & Lymphoma 2009, 50:401-409.
59. Weiner G.J. Rituximab: mechanism of action. Seminars in Hematology 2010, 47:115-123.
60. Whipple E.C., Ditto A.H., Shanahan R.S., Gatesman J.R., Little S.F., Taylor R.P., Lindorfer M.A. Low doses of antigen coupled to anti-CR2 mAbs induce rapid and enduring IgG immune responses in mice and in cynomolgus monkeys. Molecular Immunology 2007, 44:377-388.
61. Williams M.E., Densmore J.J., Pawluczkowycz A.W., Beum P.V., Kennedy A.D., Lindorfer M.A., Hamil S.H., Eggleton J.C., Taylor R.P. Thrice-weekly low-dose rituximab decreases CD20 loss via shaving and promotes enhanced targeting in chronic lymphocytic leukemia. Journal of Immunology 2006, 177:7435-7443.
62. Yang J., Cao Y., Hong S., Li H., Qian J., Kwak L.W., Yi Q. Human-like mouse models for testing the efficacy and safety of anti-β2-microglobulin monoclonal antibodies to treat myeloma. Clinical Cancer Research 2009, 15:951-959.
63. Yang J., Qian J., Wezeman M., Wang S., Lin P., Wang M., Yaccoby S., Kwak L.W., Barlogie B., Yi Q. Targeting β2-microglobulin for induction of tumor apoptosis in human hematological malignancies. Cancer Cell 2006, 10:296-307.
64. Yang J., Yi Q. Killing tumor cells through their surface β2-microglobulin or major histocompatibility complex class I molecules. Cancer 2010, 116:1638-1645.
65. Yang J., Zhang X., Wang J., Qian J., Zhang L., Wang M., Kwak L.W., Yi Q. Anti-β2-microglobulin monoclonal antibodies induce apoptosis in myeloma cells by recruiting MHC class I to and excluding growth and survival cytokine receptors from lipid rafts. Blood 2007, 110:3028-3035.
66. Zent C.S., Chen J.B., Kurten R.C., Kaushal G.P., Lacy H.M., Schichman S.A. Alemtuzumab (CAMPATH 1H) does not kill chronic lymphocytic leukemia cells in serum free medium. Leukemia Research 2004, 28:495-507.