Humanised IgG1 antibody variants targeting membrane-bound carcinoembryonic antigen by antibody-dependent cellular cytotoxicity and phagocytosis

British Journal of Cancer

Volumn 101, Issue 10, 2009, Pages 1758-1768

  Ashraf, S Q ^a,b   Umana, P ^c   Mossner E ^c   Ntouroupi, T ^a   Brunker P ^c   Schmidt, C ^c   Wilding, J L ^a   Mortensen, N J ^b   Bodmer, W F ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^c GlycArt Biotechnology AG   (Switzerland)

Author keywords

ADCC; ADCP; CEA; Colorectal cancer; Glycoengineering; Monocyte derived macrophages; NK cells; PR1A3

Indexed keywords

BETA 1,4 N ACETYLGLUCOSAMINYLTRANSFERASE III; CARCINOEMBRYONIC ANTIGEN; CD16 ANTIGEN; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G1 ANTIBODY; TRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN BINDING; ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; EFFECTOR CELL; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; GENETIC VARIABILITY; GLYCOSYLATION; GRANULOCYTE; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; PRIORITY JOURNAL;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CARCINOEMBRYONIC ANTIGEN; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; FLOW CYTOMETRY; HUMANS; IMMUNOGLOBULIN G; KILLER CELLS, NATURAL; MICE; MICE, SCID; PHAGOCYTOSIS; PROTEIN ENGINEERING; RECEPTORS, IGG; TRANSFECTION;

EID: 70449427821     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605355     Document Type: Article

References (51)

1. Adams GP, Weiner LM (2005) Monoclonal antibody therapy of cancer. Nat Biotechnol 23: 1147-1157
2. Akewanlop C, Watanabe M, Singh B, Walker M, Kufe DW, Hayes DF (2001) Phagocytosis of breast cancer cells mediated by anti-MUC-1 monoclonal antibody, DF3, and its bispecific antibody. Cancer Res 61: 4061-4065
3. Benitez-Ribas D, Adema GJ, Winkels G, Klasen IS, Punt CJ, Figdor CG, de Vries IJ (2006) Plasmacytoid dendritic cells of melanoma patients present exogenous proteins to CD4+ T cells after Fc gamma RII-mediated uptake. J Exp Med 203: 1629-1635
4. Blomberg K, Hautala R, Lovgren J, Mukkala VM, Lindqvist C, Akerman K (1996) Time-resolved fluorometric assay for natural killer activity using target cells labelled with a fluorescence enhancing ligand. J Immunol Methods 193: 199-206
5. Blumenthal RD, Hansen HJ, Goldenberg DM (2008) In vitro and in vivo anticancer efficacy of unconjugated humanized anti-CEA monoclonal antibodies. Br J Cancer 99: 837-838; author reply 839-840
6. Brodsky FM, Parham P, Barnstable CJ, Crumpton MJ, Bodmer WF (1979) Monoclonal antibodies for analysis of the HLA system. Immunol Rev 47: 3-61
7. Carter PJ (2006) Potent antibody therapeutics by design. Nat Rev Immunol 6: 343-357
8. Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P, Watier H (2002) Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 99: 754-758
9. Clynes R (2006) Antitumor antibodies in the treatment of cancer: Fc receptors link opsonic antibody with cellular immunity. Hematol Oncol Clin North Am 20: 585-612
10. Clynes RA, Towers TL, Presta LG, Ravetch JV (2000) Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med 6: 443-446
11. Conaghan PJ, Ashraf SQ, Tytherleigh MG, Wilding JL, Tchilian E, Bicknell D, Mortensen NJ, Bodmer WF (2008) Targeted killing of colorectal cancer cell lines by a humanised IgG1 monoclonal antibody that binds to membrane-bound carcinoembryonic antigen. Br J Cancer 98: 1217-1225
12. Cunningham D, Humblet Y, Siena S, Khayat D, Bleiberg H, Santoro A, Bets D, Mueser M, Harstrick A, Verslype C, Chau I, Van Cutsem E (2004) Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. N Engl J Med 351: 337-345 (Pubitemid 38944402)
13. Dhodapkar KM, Kaufman JL, Ehlers M, Banerjee DK, Bonvini E, Koenig S, Steinman RM, Ravetch JV, Dhodapkar MV (2005) Selective blockade of inhibitory Fcgamma receptor enables human dendritic cell maturation with IL-12p70 production and immunity to antibody-coated tumor cells. Proc Natl Acad Sci USA 102: 2910-2915
14. Durbin H, Bodmer WF (1987) A sensitive micro-immunoassay using beta-galactosidase/anti-beta-galactosidase complexes. J Immunol Methods 97: 19-27
15. Durbin H, Young S, Stewart LM, Wrba F, Rowan AJ, Snary D, Bodmer WF (1994) An epitope on carcinoembryonic antigen defined by the clinically relevant antibody PR1A3. Proc Natl Acad Sci USA 91: 4313-4317
16. Ferrara C, Stuart F, Sondermann P, Brunker P, Umana P (2006) The carbohydrate at FcgammaRIIIa Asn-162. An element required for high affinity binding to non-fucosylated IgG glycoforms. J Biol Chem 281: 5032-5036
17. Goldberg RM (2005) Cetuximab. Nat Rev Drug Discov (Suppl): S10-S11
18. Goldenberg DM (2002) Targeted therapy of cancer with radiolabeled antibodies. J Nucl Med 43: 693-713
19. Graff CP, Chester K, Begent R, Wittrup KD (2004) Directed evolution of an anti-carcinoembryonic antigen scFv with a 4-day monovalent dissociation half-time at 37 degrees C. Protein Eng Des Sel 17: 293-304
20. Granowska M (1993) Radioimmunoscintigraphy with technetium-99m labelled monoclonal antibody, 1A3, in colorectal cancer. Eur J Nucl Med 20: 1128
21. Granowska M, Jass JR, Britton KE, Northover JM (1989) A prospective study of the use of 111In-labelled monoclonal antibody against carcino-embryonic antigen in colorectal cancer and of some biological factors affecting its uptake. Int J Colorectal Dis 4: 97-108
22. Huls G, Heijnen IA, Cuomo E, van der Linden J, Boel E, van de Winkel JG, Logtenberg T (1999) Antitumor immune effector mechanisms recruited by phage display-derived fully human IgG1 and IgA1 monoclonal antibodies. Cancer Res 59: 5778-5784
23. Jones PT, Dear PH, Foote J, Neuberger MS, Winter G (1986) Replacing the complementarity-determining regions in a human antibody with those from a mouse. Nature 321: 522-525
24. Kalergis AM, Ravetch JV (2002) Inducing tumor immunity through the selective engagement of activating Fcgamma receptors on dendritic cells. J Exp Med 195: 1653-1659
25. Karagiannis SN, Bracher MG, Hunt J, McCloskey N, Beavil RL, Beavil AJ, Fear DJ, Thompson RG, East N, Burke F, Moore RJ, Dombrowicz DD, Balkwill FR, Gould HJ (2007) IgE-antibody-dependent immunotherapy of solid tumors: cytotoxic and phagocytic mechanisms of eradication of ovarian cancer cells. J Immunol 179: 2832-2843
26. Lazar GA, Dang W, Karki S, Vafa O, Peng JS, Hyun L, Chan C, Chung HS, Eivazi A, Yoder SC, Vielmetter J, Carmichael DF, Hayes RJ, Dahiyat BI (2006) Engineered antibody Fc variants with enhanced effector function. Proc Natl Acad Sci USA 103: 4005-4010
27. Liersch T, Meller J, Kulle B, Behr TM, Markus P, Langer C, Ghadimi BM, Wegener WA, Kovacs J, Horak ID, Becker H, Goldenberg DM (2005) Phase II trial of carcinoembryonic antigen radioimmunotherapy with 131I-labetuzumab after salvage resection of colorectal metastases in the liver: five-year safety and efficacy results. J Clin Oncol 23: 6763-6770
28. McEarchern JA, Oflazoglu E, Francisco L, McDonagh CF, Gordon KA, Stone I, Klussman K, Turcott E, van Rooijen N, Carter P, Grewal IS, Wahl AF, Law CL (2007) Engineered anti-CD70 antibody with multiple effector functions exhibits in vitro and in vivo antitumor activities. Blood 109: 1185-1192
29. McLaughlin P, Grillo-Lopez AJ, Link BK, Levy R, Czuczman MS, Williams ME, Heyman MR, Bence-Bruckler I, White CA, Cabanillas F, Jain V, Ho AD, Lister J, Wey K, Shen D, Dallaire BK (1998) Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lympho-ma: half of patients respond to a four-dose treatment program. J Clin Oncol 16: 2825-2833
30. Melief CJ (2008) Cancer immunotherapy by dendritic cells. Immunity 29: 372-383
31. Metes D, Ernst LK, Chambers WH, Sulica A, Herberman RB, Morel PA (1998) Expression of functional CD32 molecules on human NK cells is determined by an allelic polymorphism of the FcgammaRIIC gene. Blood 91: 2369-2380
32. Munn DH, McBride M, Cheung NK (1991) Role of low-affinity Fc receptors in antibody-dependent tumor cell phagocytosis by human monocyte-derived macrophages. Cancer Res 51: 1117-1123
33. Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G, Laccabue D, Zerbini A, Camisa R, Bisagni G, Neri TM, Ardizzoni A (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
34. Niwa R, Hatanaka S, Shoji-Hosaka E, Sakurada M, Kobayashi Y, Uehara A, Yokoi H, Nakamura K, Shitara K (2004a) Enhancement of the antibody-dependent cellular cytotoxicity of low-fucose IgG1 Is independent of FcgammaRIIIa functional polymorphism. Clin Cancer Res 10: 6248-6255
35. Niwa R, Shoji-Hosaka E, Sakurada M, Shinkawa T, Uchida K, Nakamura K, Matsushima K, Ueda R, Hanai N, Shitara K (2004b) Defucosylated chimeric anti-CC chemokine receptor 4 IgG1 with enhanced antibody-dependent cellular cytotoxicity shows potent therapeutic activity to T-cell leukemia and lymphoma. Cancer Res 64: 2127-2133
36. Ntouroupi TG, Ashraf SQ, McGregor SB, Turney BW, Seppo A, Kim Y, Wang X, Kilpatrick MW, Tsipouras P, Tafas T, Bodmer WF (2008) Detection of circulating tumour cells in peripheral blood with an automated scanning fluorescence microscope. Br J Cancer 99: 789-795
37. Olszewski AJ, Grossbard ML (2004) Empowering targeted therapy: lessons from rituximab. Sci STKE 2004: pe30
38. Reichert JM, Valge-Archer VE (2007) Development trends for monoclonal antibody cancer therapeutics. Nat Rev Drug Discov 6: 349-356
39. Richards JO, Karki S, Lazar GA, Chen H, Dang W, Desjarlais JR (2008) Optimization of antibody binding to FcgammaRIIa enhances macro-phage phagocytosis of tumor cells. Mol Cancer Ther 7: 2517-2527
40. Richman PI, Bodmer WF (1987) Monoclonal antibodies to human colorectal epithelium: markers for differentiation and tumour characterization. Int J Cancer 39: 317-328
41. Roda JM, Parihar R, Lehman A, Mani A, Tridandapani S, Carson III WE (2006) Interleukin-21 enhances NK cell activation in response to antibody-coated targets. J Immunol 177: 120-129
42. Saltz L, Easley C, Kirkpatrick P (2006) Panitumumab. Nat Rev Drug Discov 5: 987-988
43. Schmitz M, Zhao S, Schakel K, Bornhauser M, Ockert D, Rieber EP (2002) Native human blood dendritic cells as potent effectors in antibody-dependent cellular cytotoxicity. Blood 100: 1502-1504
44. Schuster M, Umana P, Ferrara C, Brunker P, Gerdes C, Waxenecker G, Wiederkum S, Schwager C, Loibner H, Himmler G, Mudde GC (2005) Improved effector functions of a therapeutic monoclonal Lewis Y-specific antibody by glycoform engineering. Cancer Res 65: 7934-7941
45. Sharkey RM, Goldenberg DM (2005) Perspectives on cancer therapy with radiolabeled monoclonal antibodies. J Nucl Med 46(Suppl 1): 115S-127S
46. Stewart LM, Young S, Watson G, Mather SJ, Bates PA, Band HA, Wilkinson RW, Ross EL, Snary D (1999) Humanisation and characterisation of PR1A3, a monoclonal antibody specific for cell-bound carcinoembryonic antigen. Cancer Immunol Immunother 47: 299-306
47. Umana P, Jean-Mairet J, Moudry R, Amstutz H, Bailey JE (1999) Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat Biotechnol 17: 176-180
48. Watanabe M, Wallace PK, Keler T, Deo YM, Akewanlop C, Hayes DF (1999) Antibody dependent cellular phagocytosis (ADCP) and antibody dependent cellular cytotoxicity (ADCC) of breast cancer cells mediated by bispecific antibody, MDX-210. Breast Cancer Res Treat 53: 199-207
49. Weng WK, Levy R (2003) Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J Clin Oncol 21: 3940-3947
50. Wong JY, Chu DZ, Williams LE, Yamauchi DM, Ikle DN, Kwok CS, Liu A, Wilczynski S, Colcher D, Yazaki PJ, Shively JE, Wu AM, Raubitschek AA (2004) Pilot trial evaluating an 123I-labeled 80-kilodalton engineered anticarcinoembryonic antigen antibody fragment (cT84.66 minibody) in patients with colorectal cancer. Clin Cancer Res 10: 5014-5021
51. Zhang W, Gordon M, Schultheis AM, Yang DY, Nagashima F, Azuma M, Chang HM, Borucka E, Lurje G, Sherrod AE, Iqbal S, Groshen S, Lenz HJ (2007) FCGR2A and FCGR3A polymorphisms associated with clinical outcome of epidermal growth factor receptor expressing metastatic colorectal cancer patients treated with single-agent cetuximab. J Clin Oncol 25: 3712-3718