Afucosylated Antibodies increase activation of Fcg RIIIa-dependent signaling components to intensify processes promoting ADCC

Cancer Immunology Research

Volumn 3, Issue 2, 2015, Pages 173-183

  Liu, Scot D ^a   Chalouni, Cecile ^a   Young, Judy C ^a   Junttila, Teemu T ^a   Sliwkowski, Mark X ^a   Lowe, John B ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FC GAMMA RECEPTOR IIIA; IMMUNOGLOBULIN RECEPTOR; OBINUTUZUMAB; RITUXIMAB; TRASTUZUMAB; UNCLASSIFIED DRUG; ACTIN; FC RECEPTOR; FCGR3A PROTEIN, HUMAN; FUCOSE; MONOCLONAL ANTIBODY;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CELL COUNT; CELL STIMULATION; CONFOCAL MICROSCOPE; CONTROLLED STUDY; CYTOTOXICITY ASSAY; DEGRANULATION; FUCOSYLATION; HUMAN; HUMAN CELL; LYMPHOCYTE SUBPOPULATION; NATURAL KILLER CELL; SIGNAL TRANSDUCTION; ANTIBODY AFFINITY; CELL CULTURE; CHEMISTRY; CYTOSKELETON; IMMUNOLOGY; METABOLISM;

ACTINS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODY AFFINITY; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CELL DEGRANULATION; CELLS, CULTURED; CYTOSKELETON; FUCOSE; HUMANS; KILLER CELLS, NATURAL; RECEPTORS, IGG; SIGNAL TRANSDUCTION; TRASTUZUMAB;

EID: 84940450182     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-14-0125     Document Type: Article

References (50)

1. Habermann TM, Weller EA, Morrison V.A., Gascoyne RD, Cassileth PA, Cohn JB, et al Rituximab-CHOP versus CHOP alone or with maintenance rituximab in older patients with diffuse large B-cell lymphoma. J Clin Oncol 2006;24:3121-7.
2. Baselga J, Carbonell X, Castaneda-Soto NJ, Clemens M., Green M, Harvey V, et al Phase IIstudy ofefficacy, safety, and pharmacokinetics of trastuzumab monotherapy administered on a 3-weekly schedule. J Clin Oncol 2005; 23:2162-71.
3. Hudis CA. Trastuzumab mechanism of action and use in clinical practice. N Engl J Med 2007;357:39-51.
4. Weiner GJ. Rituximab: mechanism of action. Semin Hematol 2010;47: 115-23.
5. Lanier LL. Natural killer cell receptor signaling. Curr Opin Immunol 2003;15:308-14.
6. Orange JS. Formation and function of the lytic NK-cell immunological synapse. Nat Rev Immunol 2008;8:713-25.
7. Clynes RA, Towers TL, Presta L.G., Ravetch JV. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med 2000;6: 443-6.
8. Cartron G, Dacheux L, Salles G., Solal-Celigny P, Bardos P, Colombat P., et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 2002;99:754-8.
9. Weng WK, Levy R. Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J Clin Oncol 2003;21:3940-7.
10. Mellor JD, Brown MP, Irving H.R., Zalcberg JR, Dobrovic A. A critical review of the role of Fc gamma receptor polymorphisms in the response to monoclonal antibodies in cancer. J Hematol Oncol 2013;6:1.
11. Musolino A, Naldi N, Bortesi B., Pezzuolo D, Capelletti M, Missale G., et al. 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 2008;26:1789-96.
12. Hurvitz SA, Betting DJ, Stern H.M., Quinaux E., Stinson J, Seshagiri S, et al Analysis of Fcgamma receptor IIIa and IIa polymorphisms: lack of correlation with outcome in trastuzumab-treated breast cancer patients. Clin Cancer Res 2012;18:3478-86.
13. Tamura K, Shimizu C, Hojo T., Akashi-Tanaka S, Kinoshita T, Yonemori K., et al. FcgammaR2A and 3A polymorphisms predict clinical outcome of trastuzumab in both neoadjuvant and metastatic settings in patients with HER2-positive breast cancer. Ann Oncol 2011;22:1302-7.
14. Mossner E, Brunker P, Moser S., Puntener U, Schmidt C, Herter 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.
15. Shields RL, Lai J, Keck R., O'Connell LY, Hong K, Meng Y.G., et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 2002;277:26733-40.
16. Shinkawa T, Nakamura K, Yamane N., Shoji-Hosaka E, Kanda Y, Sakurada M., et al. The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J Biol Chem 2003;278:3466-73.
17. Junttila TT, Parsons K, Olsson C., Lu Y, Xin Y, Theriault J., et al. Superior in vivo efficacy of afucosylated trastuzumab in the treatment of HER2-amplified breast cancer. Cancer Res 2010;70:4481-9.
18. Goede V, Fischer K, Busch R., Engelke A, Eichhorst B, Wendtner C.M., et al. Head-to-head comparison of obinutuzumab (GA101) plus chlorambucil (Clb) versus rituximab plus Clb in patients with chronic lymphocytic leukemia (CLL) and co-existing medical conditions (comorbidities): final stage 2 results of the CLL11 trial [abstract]. In: Proceedings of the 2013 ASH Annual Meeting and Exposition; 2013 Dec 6-10; New Orleans, LA: ASH; 2013. Abstract nr. 6.
19. Salcedo TW, Kurosaki T, Kanakaraj P., Ravetch JV, Perussia B. Physical and functional association of p56lck with Fc gamma RIIIA (CD16) in natural killer cells. J Exp Med 1993;177:1475-80.
20. O'Shea J.J., Weissman AM, Kennedy I.C., Ortaldo JR. Engagement of the natural killer cell IgG Fc receptor results in tyrosine phosphorylation of the zeta chain. Proc Natl Acad Sci U S A 1991;88:350-4.
21. Vivier E, Morin P, O'Brien C, Druker B, Schlossman S.F., Anderson P. Tyrosine phosphorylation of the Fc gamma RIII(CD16): zeta complex in human natural killer cells. Induction by antibody-dependent cytotoxicity but not by natural killing. J Immunol 1991;146:206-10.
22. Vivier E, da Silva AJ, Ackerly M, Levine H, Rudd C.E., Anderson P. Association of a 70-kDa tyrosine phosphoprotein with the CD16: zeta: gamma complex expressed in human natural killer cells. Eur J Immunol 1993;23: 1872-6.
23. Einspahr KJ, Abraham RT, Binstadt B.A., Uehara Y., Leibson PJ. Tyrosine phosphorylation provides an early and requisite signal for the activation of natural killer cell cytotoxic function. Proc Natl Acad Sci U S A 1991; 88:79-83.
24. Bonnema JD, Karnitz LM, Schoon R.A., Abraham RT, Leibson PJ. Fc receptor stimulation of phosphatidylinositol 3-kinase in natural killer cells is associated with protein kinase C-independent granule release and cellmediated cytotoxicity. J Exp Med 1994;180:1427-35.
25. Kanakaraj P, Duckworth B, Azzoni L., Kamoun M, Cantley LC, Perussia B. Phosphatidylinositol-3 kinase activation induced upon Fc gamma RIIIA ligand interaction. J Exp Med 1994;179:551-8.
26. Jiang K, Zhong B, Gilvary D.L., Corliss BC, Hong-Geller E, Wei S, et al. Pivotal role of phosphoinositide-3 kinase in regulation of cytotoxicity in natural killer cells. Nat Immunol 2000;1:419-25.
27. Galandrini R, Palmieri G, Piccoli M., Frati L, Santoni A. Role for the Rac1 exchange factor Vav in the signaling pathways leading to NK cell cytotoxicity. J Immunol 1999;162:3148-52.
28. Riteau B, Barber DF, Long EO Vav1 phosphorylation is induced by beta2 integrin engagement on natural killer cells upstream of actin cytoskeleton and lipid raft reorganization. J Exp Med 2003;198:469-74.
29. Xu X, Chong AS Vav in natural killer cells is tyrosine phosphorylated upon cross-linking of Fc gamma RIIIA and is constitutively associated with a serine/threonine kinase. Biochem J 1996;318:527-32.
30. Orange JS, Harris KE, Andzelm M.M., Valter MM, Geha RS, Strominger JL. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc Natl Acad Sci U S A 2003;100:14151-6.
31. Bhat R, Watzl C. Serial killing of tumor cells by human natural killer cells-enhancement by therapeutic antibodies. PLoS ONE 2007;2: e326.
32. Vivier E, Nunes JA, Vely F. Natural killer cell signaling pathways. Science 2004;306:1517-9.
33. Camus M, Tosolini M, Mlecnik B., Pages F, Kirilovsky A, Berger A., et al. Coordination of intratumoral immune reaction and human colorectal cancer recurrence. Cancer Res 2009;69:2685-93.
34. Erdag G, Schaefer JT, Smolkin M.E., Deacon DH, Shea SM, Dengel LT, et al Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res 2012;72:1070-80.
35. Gasdaska JR, Sherwood S, Regan J.T., Dickey LF. An afucosylated anti-CD20 monoclonal antibody with greater antibody-dependent cellular cytotoxicity and B-cell depletion and lower complement-dependent cytotoxicity than rituximab. Mol Immunol 2012;50:134-41.
36. Beck A, Reichert JM Marketing approval of mogamulizumab: a triumph for glyco-engineering. MAbs 2012;4:419-25.
37. Rexer BN, Arteaga CL Optimal targeting of HER2-PI3K signaling in breast cancer: mechanistic insights and clinical implications. Cancer Res 2013;73: 3817-20.
38. Markasz L, Stuber G, Vanherberghen B., Flaberg E, Olah E, Carbone E., et al. Effect of frequently used chemotherapeutic drugs on the cytotoxic activity of human natural killer cells. Mol Cancer Ther 2007;6:644-54.
39. Ravetch JV, Kinet JP Fc receptors. Ann Rev Immunol 1991;9:457-92.
40. Braster R, O'Toole T, van Egmond M. Myeloid cells as effector cells for monoclonal antibody therapy of cancer. Methods 2014;65:28-37.
41. Herter S, Birk MC, Klein C, Gerdes C., Umana P, Bacac M. Glycoengineering of therapeutic antibodies enhances monocyte/macrophage-mediated phagocytosis and cytotoxicity. J Immunol 2014;192:2252-60.
42. Garcia-Garcia E., Rosales C. Signal transduction during Fc receptor-mediated phagocytosis. J Leukoc Biol 2002;72:1092-108.
43. Nordstrom JL, Gorlatov S, Zhang W., Yang Y, Huang L, Burke S., et al. Antitumor activity and toxicokinetics analysis of MGAH22, an anti-HER2 monoclonal antibody with enhanced Fcgamma receptor binding properties. Breast Cancer Res 2011;13:R123.
44. Merlin JL, Barberi-Heyob M, Bachmann N. In vitro comparative evaluation of trastuzumab (Herceptin) combined with paclitaxel (Taxol) or docetaxel (Taxotere) in HER2-expressing human breast cancer cell lines. Ann Oncol 2002;13:1743-8.
45. Diefenbach A, Jamieson AM, Liu S.D., Shastri N., Raulet DH. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 2000;1:119-26.
46. Spear P, Wu MR, Sentman M.L., Sentman CL. NKG2D ligands as therapeutic targets. Cancer Immunity 2013;13:8.
47. Melis M, Spatafora M, Melodia A., Pace E, Gjomarkaj M, Merendino A.M., et al. ICAM-1 expression by lung cancer cell lines: effects of upregulation by cytokines on the interaction with LAK cells. Eur Respir J 1996;9:1831-8.
48. Iida S, Kuni-Kamochi R, Mori K., Misaka H, Inoue M, Okazaki A., et al. Two mechanisms of the enhanced antibody-dependent cellular cytotoxicity (ADCC) efficacy of non-fucosylated therapeutic antibodies in human blood. BMC Cancer 2009;9:58.
49. Velders MP, van Rhijn CM, Oskam E, Fleuren GJ, Warnaar S.O., Litvinov SV. The impact of antigen density and antibody affinity on antibody-dependent cellular cytotoxicity: relevance for immunotherapy of carcinomas. Br J Cancer 1998;78:78-83.
50. Nimmerjahn F, Ravetch JV Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 2008;8:34-47.