Binding of rituximab, trastuzumab, cetuximab, or mAb T101 to cancer cells promotes trogocytosis mediated by THP-1 cells and monocytes

Journal of Immunology

Volumn 181, Issue 11, 2009, Pages 8120-8132

  Beum, Paul V ^a   Mack, David A ^a   Pawluczkowycz, Andrew W ^a   Lindorfer, Margaret A ^a   Taylor, Ronald P ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CETUXIMAB; FC RECEPTOR; LYMPHOCYTE ANTIGEN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY T101; RITUXIMAB; TRASTUZUMAB; UNCLASSIFIED DRUG;

ANTIGENIC MODULATION; ANTIGENICITY; ARTICLE; CANCER CELL; CANCER IMMUNOTHERAPY; CELL INTERACTION; CELL ISOLATION; CONTROLLED STUDY; DRUG APPROVAL; DRUG BINDING; DRUG RECEPTOR BINDING; FOOD AND DRUG ADMINISTRATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; MONOCYTE; PRIORITY JOURNAL; TARGET CELL; TROGOCYTOSIS; TUMOR CELL; UNITED STATES;

EID: 71849101849     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.11.8120     Document Type: Article

References (58)

1. Hudrisier, D., J. Riond, H. Mazarguil, J. E. Gairin, and E. Joly. 2001. CTLs rapidly capture membrane fragments from target cells in a TCR signaling-dependent manner. J. Immunol. 166: 3645-3649. (Pubitemid 32224883)
2. Joly, E., and D. Hudrisier. 2003. What is trogocytosis and what is its purpose? Nat. Immunol. 4: 815. (Pubitemid 37098646)
3. Hudrisier, D., J. Riond, L. Garidou, C. Duthoit, and E. Joly. 2005. T cell activation correlates with an increased proportion of antigen among the materials acquired from target cells. Eur. J. Immunol. 35: 2284-2294. (Pubitemid 41179749)
4. Hudrisier, D., A. Aucher, A. L. Puaux, C. Bordier, and E. Joly. 2007. Capture of target cell membrane components via trogocytosis is triggered by a selected set of surface molecules on T or B cells. J. Immunol. 178: 3637-3647. (Pubitemid 46417631)
5. Beum, P. V., A. D. Kennedy, M. E. Williams, M. A. Lindorfer, and R. P. Taylor. 2006. The shaving reaction: rituximab/CD20 complexes are removed from mantle cell lymphoma and chronic lymphocytic leukemia cells by THP-1 monocytes. J. Immunol. 176: 2600-2609.
6. Kennedy, A. D., P. V. Beum, M. D. Solga, D. J. DiLillo, M. A. Lindorfer, C. E. Hess, J. J. Densmore, M. E. Williams, and R. P. Taylor. 2004. Rituximab infusion promotes rapid complement depletion and acute CD20 loss in chronic lymphocytic leukemia. J. Immunol. 172: 3280-3288.
7. Williams, M. E., J. J. Densmore, A. W. Pawluczkowycz, P. V. Beum, A. D. Kennedy, M. A. Lindorfer, S. H. Hamil, J. C. Eggleton, and R. P. Taylor. 2006. Thrice-weekly low-dose rituximab decreases CD20 loss via shaving and promotes enhanced targeting in chronic lymphocytic leukemia. J. Immunol. 177: 7435-7443.
8. Beum, P. V., M. A. Lindorfer, and R. P. Taylor. 2008. 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. J. Immunol. 181: 2916-2924.
9. Ritz, J., J. M. Pesando, S. E. Sallan, L. A. Clavell, J. Notis-McConarty, P. Rosenthal, and S. F. Scholossman. 1981. Serotherapy of acute lymphoblastic leukemia with monoclonal antibody. Blood 58: 141-152. (Pubitemid 11064471)
10. Miller, R. A., D. G. Maloney, J. McKillop, and R. Levy. 1981. In vitro effects of murine hybridoma monoclonal antibody in a patient with T-cell leukemia. Blood 58: 78-86.
11. Chatenoud, L., M. F. Baudrihaye, H. Kreis, G. Goldstein, J. Schindler, and J. F. Bach. 1982. Human in vivo antigenic modulation induced by the anti-T cell OKT3 monoclonal antibody. Eur. J. Immunol. 12: 979-982. (Pubitemid 13203591)
12. Rinnooy Kan, E. A., E. Platzer, K. Welte, and C. Y. Wang. 1984. Modulation induction of the T3 antigen by OKT3 antibody is monocyte dependent. J. Immunol. 133: 2979-2985.
13. Pesando, J. M., P. Hoffman, and M. Abed. 1986. Antibody-induced antigenic modulation is antigen dependent: characterization of 22 proteins on a malignant human B cell line. J. Immunol. 137: 3689-3695.
14. Bertram, J. H., P. S. Gill, A. M. Levine, D. Boquiren, F. M. Hoffman, P. Meyer, and M. S. Mitchell. 1986. Monoclonal antibody T101 in T cell malignancies: a clinical, pharmacokinetic, and immunologic correlation. Blood 68: 752-761.
15. Musolino, A., N. Naldi, B. Bortesi, D. Pezzuolo, M. Capelletti, G. Missale, D. Laccabue, A. Zerbini, R. Camisa, G. Bisagni, et al. 2008. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J. Clin. Oncol. 26: 1789-1796.
16. Hudis, C. A. 2007. Trastuzumab: mechanism of action and use in clinical practice. N. Engl. J. Med. 357: 39-51. (Pubitemid 47026733)
17. Kurai, J., H. Chikumi, K. Hashimoto, K. Yamaguchi, A. Yamasaki, T. Sako, H. Touge, H. Makino, M. Takata, M. Miyata, et al. 2007. Antibody-dependent cellular cytotoxicity mediated by cetuximab against lung cancer cell lines. Clin. Cancer Res. 13: 1552-1561. (Pubitemid 46450447)
18. Galizia, G., D. Lieto, F. De Vita, M. Orditura, P. Castellano, T. Troiani, V. Imperatore, and F. Ciardiello. 2007. Cetuximab, a chimeric human mouse anti-epidermal growth factor receptor monoclonal antibody, in the treatment of human colorectal cancer. Oncogene 26: 3654-3660. (Pubitemid 46842715)
19. + cells by rituximab. Blood 101: 1071-1079.
20. Craig, M. L., A. J. Bankovich, and R. P. Taylor. 2002. Visualization of the transfer reaction: tracking immune complexes from erythrocyte complement receptor 1 to macrophages. Clin. Immunol. 105: 36-47.
21. Gyimesi, E., A. J. Bankovich, T. A. Schuman, J. B. Goldberg, M. A. Lindorfer, and R. P. Taylor. 2004. Staphylococcus aureus bound to complement receptor 1 on human erythocytes by bispecific monoclonal antibodies is phagocytosed by acceptor macrophages. Immunol. Lett. 95: 185-192. (Pubitemid 39237664)
22. Edberg, J. C., L. Tosic, E. L. Wright, W. M. Sutherland, and R. P. Taylor. 1988. Quantitative analyses of the relationship between C3 consumption, C3b capture, and immune adherence of complement-fixing antibody/DNA immune complexes. J. Immunol. 141: 4258-4265.
23. Wiener, E., R. A. Dellow, F. Mawas, and C. H. Rodeck. 1996. Role of FcγRIIa (CD32) in IgG anti-RhD-mediated red cell phagocytosis in vitro. Transfus. Med. 6: 235-241. (Pubitemid 27101007)
24. Flesch, B. K., G. Achtert, and J. Neppert. 1997. Inhibition of monocyte and polymorphonuclear granulocyte immune phagocytosis by monoclonal antibodies specific for Fcγ RI, II, and III. Ann. Hematol. 74: 15-22.
25. Tebo, A. E., P. G. Kremsner, and A. J. F. Luty. 2002. Fcγ receptor-mediated phagocytosis of Plasmodium falciparum-infected erythrocytes in vitro. Clin. Exp. Immunol. 130: 300-306. (Pubitemid 35286218)
26. Kou, Z., M. Quinn, H. Chen, W. W. Rodrigo, R. C. Rose, J. J. Schlesinger, and X. Jin. 2008. Monocytes, but not T or B cells, are the principal target cells for dengue virus (DV) infection among human peripheral blood mononuclear cells. J. Med. Virol. 80: 134-146. (Pubitemid 350220099)
27. Guyre, P. M., R. F. Graziano, B. A. Vance, P. M. Morganelli, and M. W. Fanger. 1989. Monoclonal antibodies that bind to distinct epitopes on FcγRI are able to trigger receptor function. J. Immunol. 143: 1650-1655.
28. George, T. C., D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey. 2004. Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer. Cytometry 59A: 237-245.
29. Beum, P. V., M. A. Lindorfer, B. E. Hall, T. C. George, K. Frost, P. J. Morrissey, and R. P. Taylor. 2006. Quantitative analysis of protein co-localization on B cells opsonized with rituximab and complement using the ImageStream multispectral imaging flow cytometer. J. Immunol. Methods 317: 90-99.
30. Beekman, J. M., C. E. van der Poel, J. A. Van Der Linden, D. L. van den Berg, P. V. van den Berghe, J. G. van de Winkel, and J. H. Leusen. 2008. Filamin A stabilizes FcγRI surface expression and prevents its lysosomal routing. J. Immunol. 180: 3938-3945.
31. Daubeuf, S., A.-L. Puaux, E. Joly, and D. Hudrisier. 2007. A simple trogocytosis-based method to detect, quantify, characterize and purify antigen-specific live lymphocytes by flow cytometry, via their capture of membrane fragments from antigen-presenting cells. Nat. Protoc. 1: 2536-2542.
32. Teeling, J. L., T. Jansen-Hendriks, T. W. Kuijpers, M. de Haas, J. G. J. van de Winkel, C. E. Hack, and W. K. Bleeker. 2001. Therapeutic efficacy of intravenous immunoglobulin preparations depends on the immunoglobulin G dimers: studies in experimental immune thrombocytopenia. Blood 98: 1095-1099.
33. Teeling, J., R. R. French, M. S. Cragg, J. van den Brakel, M. Pluyter, H. Huang, C. Chan, P. W. Parren, C. E. Hack, M. Dechant, et al. 2004. Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin's lymphomas. Blood 104: 1793-1800. (Pubitemid 39202289)
34. Janssen, E., K. Tabeta, M. J. Barnes, S. Rutschmann, S. McBride, K. S. Bahjat, S. P. Schoenberger, A. N. Theofilopoulos, B. Beutler, and K. Hoebe. 2006. Efficient T cell activation via a Toll-interleukin 1 receptor-independent pathway. Immunity 24: 787-799. (Pubitemid 43867366)
35. Griffin, F. M., J. A. Griffin, J. E. Leider, and S. C. Silverstein. 1975. 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. 142: 1263-1282.
36. Griffin, F. M., J. A. Griffin, and S. C. Silverstein. 1976. Studies on the mechanism of phagocytosis: II. The interaction of macrophages with anti-immunoglobulin IgG-coated bone marrow-derived lymphocytes. J. Exp. Med. 144: 788-809.
37. Swanson, J. A., and C. Watts. 1995. Macropinocytosis. Trends Cell Biol. 5: 424-427.
38. Davis, W., P. T. Harrison, M. J. Hutchinson, and J. M. Allen. 1995. Two distinct regions of FcγRI initiate separate signalling pathways involved in endocytosis and phagocytosis. EMBO J. 14: 432-441.
39. Koval, M., K. Preiter, C. Adles, P. D. Stahl, and T. H. Steinberg. 1998. Size of IgG-opsonized particles determines macrophage response during internalization. Exp. Cell Res. 242: 265-273. (Pubitemid 28366542)
40. Lovdal, T., E. Andersen, and A. B. T. Brech. 2000. Fc receptor mediated endocytosis of small soluble immunoglobulin G immune complexes in Kupffer and endothelial cells from rat liver. J. Cell Sci. 113: 3255-3266. (Pubitemid 30793932)
41. Guyre, C., T. Keler, S. Swink, L. Vitale, R. Graziano, and M. Fanger. 2001. Receptor modulation by FcγRI-specific fusion proteins is dependent on receptor number and modified by IgG. J. Immunol. 167: 6303-6311. (Pubitemid 33081561)
42. Swanson, J. A., and A. D. Hoppe. 2004. The coordination of signaling during Fc receptor-mediated phagocytosis. J. Leukocyte Biol. 76: 1093-1103.
43. Li, Y., M. E. Williams, J. B. Cousar, A. W. Pawluczkowycz, M. A. Lindorfer, and R. P. Taylor. 2007. Rituximab/CD20 complexes are shaved from Z138 mantle cell lymphoma cells in intravenous and subcutaneous SCID mouse models. J. Immunol. 179: 4263-4271.
44. Schroff, R. W., R. A. Klein, M. M. Farrell, and H. C. Stevenson. 1984. Enhancing effects of monocytes on modulation of a lymphocyte membrane antigen. J. Immunol. 133: 2270-2277. (Pubitemid 14033065)
45. Ioan-Facsinay, A., S. J. de Kimpe, S. M. M. Hellwig, P. L. van Lent, F. M. A. Hofhuis, H. H. van Ojik, C. Sedlik, S. A. de Silveira, J. Gerber, Y. F. de Jong, et al. 2002. FcγRI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity 16: 391-402. (Pubitemid 34260917)
46. Bevaart, L., M. J. H. Jansen, M. J. van Vugt, J. S. Verbeek, J. G. J. van de Winkel, and J. H. W. Leusen. 2006. The high-affinity IgG receptor, Fc-γRI, plays a central role in antibody therapy of experimental melanoma. Cancer Res. 66: 1261-1264. (Pubitemid 43259901)
47. Baudino, L., F. Nimmerjahn, S. A. da Silveira, E. Martinez-Soria, T. Saito, M. Carroll, J. V. Ravetch, J. S. Verbeek, and S. Izui. 2008. Differential contribution of three activating IgG Fc receptors (FcγRI, FcγRIII, and FcγRIV) to IgG2a- and IgG2b-induced autoimmune hemolytic anemia in mice. J. Immunol. 180: 1948-1953.
48. Schreiber, A. D., and M. M. Frank. 1972. Role of antibody and complement in the immune clearance and destruction of erythrocytes: in vivo effects of IgG and IgM complement fixing sites. J. Clin. Invest. 51: 575-582.
49. Frank, M. M. 1989. The role of macrophages in blood stream clearance. In Human Monocytes. M. Zembala and G. L. Asherson, eds. Academic Press, New York, pp. 337-344.
50. Kimberly, R. P., J. E. Salmon, J. C. Edberg, and A. Gibofsky. 1989. The role of Fcγ receptors in mononuclear phagocyte system function. Clin. Exp. Rheumatol. 7: 103-108.
51. Gong, Q., Q. Ou, S. Ye, W. P. Lee, J. Cornelius, L. Diehl, W. Y. Lin, Z. Hu, Y. Lu, Y. Chen, et al. 2005. Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J. Immunol. 174: 817-826. (Pubitemid 40094277)
52. Kavai, M., and G. Szegedi. 2007. Immune complex clearance by monocytes and macrophages in systemic lupus erythematosus. Autoimmun. Rev. 6: 497-502. (Pubitemid 47069975)
53. Wallace, P. K., P. Kaufman, L. Lewis, T. Keler, A. Givan, J. Fisher, M. Waugh, A. Wahner, P. Guyre, M. Fanger, and M. Ernstoff. 2001. Bispecific antibody-targeted phagocytosis of HER-2/neu expressing tumor cells by myeloid cells activated in vivo. J. Immunol. Methods 248: 167-182.
54. Golay, J., M. Manganini, V. Facchinetti, R. Gramigna, R. Broady, G. Borleri, A. Rambaldi, and M. Introna. 2003. Rituximab-mediated antibody-dependent cellular cytotoxicity against neoplastic B cells is stimulated strongly by interleukin-2. Haematologica 88: 1002-1012. (Pubitemid 37151151)
55. Dall'Ozzo, S., S. Tartas, G. Paintaud, G. Cartron, P. Colombat, P. Bardos, H. Watier, and G. Thibault. 2004. Rituximab-dependent cytotoxicity by natural killer cells: influence of FCGR3A polymorphism on the concentration-effect relationship. Cancer Res. 64: 4664-4669. (Pubitemid 38856941)
56. Bowles, J. A., and G. J. Weiner. 2005. CD16 polymorphisms and NK activation induced by monoclonal antibody-coated target cells. J. Immunol. Methods 304: 88-99.
57. Berdeja, J. G., A. Hess, D. M. Lucas, P. O'Donnell, R. F. Ambinder, L. F. Diehl, D. Carter-Brookins, S. Newton, and I. W. Flinn. 2007. 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. Clin. Cancer Res. 13: 2392-2399.
58. Laurent, C., G. R. de Paiva, L. Ysebaert, G. Laurent, M. March, G. Delsol, and P. Brousset. 2007. Characterization of bone marrow lymphoid infiltrates after immunochemotherapy for follicular lymphoma. Am. J. Pathol. 128: 974-980.