Glyco-engineered anti-EGFR mAb elicits ADCC by NK cells from colorectal cancer patients irrespective of chemotherapy

British Journal of Cancer

Volumn 110, Issue 5, 2014, Pages 1221-1227

  Oppenheim, D E ^a   Spreafico, R ^a   Etuk, A ^a   Malone, D ^a   Amofah, E ^a   Pena Murillo C ^a   Murray, T ^a   McLaughlin, L ^a   Choi, B S ^a   Allan, S ^b   Belousov, A ^c   Passioukov, A ^d   Gerdes, C ^d   Umana P ^d   Farzaneh, F ^a   Ross, P ^a,b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

^c ROCHE DIAGNOSTICS GMBH   (Germany)

^d Roche Glycart AG   (Switzerland)

Author keywords

ADCC; Colorectal cancer; GA201; Glyco engineering; Monoclonal antibody

Indexed keywords

IMGATUZUMAB; IRINOTECAN; OXALIPLATIN; CAPECITABINE; CD16 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; FLUOROURACIL; FOLINIC ACID; MONOCLONAL ANTIBODY; PANITUMUMAB;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CANCER CHEMOTHERAPY; CANCER PATIENT; COLORECTAL CANCER; COLORECTAL CARCINOMA; CONTROLLED STUDY; DEGRANULATION ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; LEUKOCYTE; NATURAL KILLER CELL; PRIORITY JOURNAL; TREATMENT RESPONSE; CANCER IMMUNOTHERAPY; CYTOTOXICITY ASSAY; DRUG EFFECT; DRUG POTENCY; K562 CELL LINE; LEUKOCYTE COUNT;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CASE-CONTROL STUDIES; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; GLYCOPROTEINS; GPI-LINKED PROTEINS; HUMANS; IMMUNOGLOBULIN G; K562 CELLS; KILLER CELLS, NATURAL; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, IGG;

EID: 84895835829     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2014.35     Document Type: Article

References (46)

1. Alter G, Malenfant JM, Altfeld M (2004) CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods 294(1-2): 15-22. (Pubitemid 39626587)
2. Amado RG, Wolf M, Peeters M, Van Cutsem E, Siena S, Freeman DJ, Juan T, Sikorski R, Suggs S, Radinsky R, Patterson SD, Chang DD (2008) Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J Clin Oncol 26(10): 1626-1634.
3. American Cancer Society (2013) What are the key statistics about colorectal cancer? Available at: http://www.cancer.org/cancer/ colonandrectumcancer/detailedguide/colorectal-cancer-key-statistics. American Cancer Society: Atlanta, GA.
4. Azria D, Bibeau F, Barbier N, Zouhair A, Lemanski C, Rouanet P, Ychou M, Senesse P, Ozsahin M, Pelegrin A, Dubois JB, Thezenas S (2005) Prognostic impact of epidermal growth factor receptor (EGFR) expression on loco-regional recurrence after preoperative radiotherapy in rectal cancer. BMC Cancer 5: 62.
5. Bokemeyer C, Bondarenko I, Makhson A, Hartmann JT, Aparicio J, de Braud F, Donea S, Ludwig H, Schuch G, Stroh C, Loos AH, Zubel A, Koralewski P (2009) Fluorouracil, leucovorin, and oxaliplatin with and without cetuximab in the first-line treatment of metastatic colorectal cancer. J Clin Oncol 27(5): 663-671.
6. Burnet M (1957) Cancer; a biological approach. I. The processes of control. Br Med J 1(5022): 779-786.
7. 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(3): 754-758. (Pubitemid 34525533)
8. Chen X, Trivedi PP, Ge B, Krzewski K, Strominger JL (2007) Many NK cell receptors activate ERK2 and JNK1 to trigger microtubule organizing center and granule polarization and cytotoxicity. Proc Natl Acad Sci USA 104(15): 6329-6334. (Pubitemid 47186094)
9. Ciardiello F, Tortora G (2008) EGFR antagonists in cancer treatment. N Engl J Med 358(11): 1160-1174.
10. Coca S, Perez-Piqueras J, Martinez D, Colmenarejo A, Saez M, Vallejo C, Martos J, Moreno M (1997) The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer 79: 2320-2328. (Pubitemid 27251014)
11. de Gramont A, Figer A, Seymour M, Homerin M, Hmissi A, Cassidy J, Boni C, Cortes-Funes H, Cervantes A, Freyer G, Papamichael D, Le Bail N, Louvet C, Hendler D, de Braud F, Wilson C, Morvan F, Bonetti A (2000) Leucovorin and fluorouracil with or without oxaliplatin as first-line treatment in advanced colorectal cancer. J Clin Oncol 18(16): 2938-2947. (Pubitemid 30644117)
12. Douillard JY (2000) Irinotecan and high-dose fluorouracil/leucovorin for metastatic colorectal cancer. Oncology (Williston Park) 14(12 Suppl 14): 51-55.
13. Ferrara C, Grau S, Jager C, Sondermann P, Brunker P, Waldhauer I, Hennig M, Ruf A, Rufer AC, Stihle M, Umana P, Benz J (2011) Unique carbohydrate- carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Natl Acad Sci USA 108(31): 12669-12674.
14. 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(8): 5032-5036. (Pubitemid 43847767)
15. Gerdes CA, Nicolini VG, Herter S, van Puijenbroek E, Lang S, Roemmele M, Moessner E, Freytag O, Friess T, Ries CH, Bossenmaier B, Mueller HJ, Umana P (2013) GA201 (RG7160): a novel, humanized, glycoengineered anti-EGFR antibody with enhanced ADCC and superior in vivo efficacy compared with cetuximab. Clin Cancer Res 19(5): 1126-1138.
16. Giacchetti S, Itzhaki M, Gruia G, Adam R, Zidani R, Kunstlinger F, Brienza S, Alafaci E, Bertheault-Cvitkovic F, Jasmin C, Reynes M, Bismuth H, Misset JL, Levi F (1999) Long-term survival of patients with unresectable colorectal cancer liver metastases following infusional chemotherapy with 5-fluorouracil, leucovorin, oxaliplatin and surgery. Ann Oncol 10(6): 663-669. (Pubitemid 29342371)
17. Giacomelli L, Gianni W, Belfiore C, Gandini O, Repetto L, Filippini A, Frati L, Agliano AM, Gazzaniga P (2003) Persistence of epidermal growth factor receptor and interleukin 10 in blood of colorectal cancer patients after surgery identifies patients with high risk to relapse. Clin Cancer Res 9(7): 2678-2682. (Pubitemid 36842113)
18. Goldberg RM, Sargent DJ, Morton RF, Fuchs CS, Ramanathan RK, Williamson SK, Findlay BP, Pitot HC, Alberts SR (2004) A randomized controlled trial of fluorouracil plus leucovorin, irinotecan, and oxaliplatin combinations in patients with previously untreated metastatic colorectal cancer. J Clin Oncol 22(1): 23-30. (Pubitemid 41095110)
19. Grothey A, Goetz MP (2004) Oxaliplatin plus oral fluoropyrimidines in colorectal cancer. Clin Colorectal Cancer 4(Suppl 1): S37-S42. (Pubitemid 38854688)
20. Ishigami S, Natsugoe S, Tokuda K, Nakajo A, Che X, Iwashige H, Aridome K, Hokita S, Aikou T (2000) Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 88: 577-583. (Pubitemid 30056932)
21. Karapetis CS, Khambata-Ford S, Jonker DJ, O'Callaghan CJ, Tu D, Tebbutt NC, Simes RJ, Chalchal H, Shapiro JD, Robitaille S, Price TJ, Shepherd L, Au HJ, Langer C, Moore MJ, Zalcberg JR (2008) K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med 359(17): 1757-1765.
22. Kohne CH, van Cutsem E, Wils J, Bokemeyer C, El-Serafi M, Lutz MP, Lorenz M, Reichardt P, Ruckle-Lanz H, Frickhofen N, Fuchs R, Mergenthaler HG, Langenbuch T, Vanhoefer U, Rougier P, Voigtmann R, Muller L, Genicot B, Anak O, Nordlinger B (2005) Phase III study of weekly high-dose infusional fluorouracil plus folinic acid with or without irinotecan in patients with metastatic colorectal cancer: European Organisation for Research and Treatment of Cancer Gastrointestinal Group Study 40986. J Clin Oncol 23(22): 4856-4865. (Pubitemid 46223990)
23. Laurent-Puig P, Lievre A, Blons H (2009) Mutations and response to epidermal growth factor receptor inhibitors. Clin Cancer Res 15(4): 1133-1139.
24. Levy EM, Roberti MP, Mordoh J (2011) Natural killer cells in human cancer: from biological functions to clinical applications. J Biomed Biotechnol 2011: 676198.
25. Lievre A, Bachet JB, Le Corre D, Boige V, Landi B, Emile JF, Cote JF, Tomasic G, Penna C, Ducreux M, Rougier P, Penault-Llorca F, Laurent-Puig P (2006) KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res 66(8): 3992-3995.
26. Markman B, Javier Ramos F, Capdevila J, Tabernero J (2010) EGFR and KRAS in colorectal cancer. Adv Clin Chem 51: 71-119.
27. Maughan TS, Adams RA, Smith CG, Meade AM, Seymour MT, Wilson RH, Idziaszczyk S, Harris R, Fisher D, Kenny SL, Kay E, Mitchell JK, Madi A, Jasani B, James MD, Bridgewater J, Kennedy MJ, Claes B, Lambrechts D, Kaplan R, Cheadle JP (2011) Addition of cetuximab to oxaliplatin-based first-line combination chemotherapy for treatment of advanced colorectal cancer: results of the randomised phase 3 MRC COIN trial. Lancet 377(9783): 2103-2114.
28. Menon A, Janssen-van Rhijn C, Morreau H, Putter H, Tollenaar R, van de Velde C, Leuren G, Kuppen P (2004) Immune system and prognosis in colorectal cancer: a detailed immunohistochemical analysis. Lab Invest 84: 493-501. (Pubitemid 41656477)
29. Mossner E, Brunker P, Moser S, Puntener U, Schmidt C, Herter S, Grau R, Gerdes C, Nopora A, van Puijenbroek E, Ferrara C, Sondermann P, Jager C, Strein P, Fertig G, Friess T, Schull C, Bauer S, Dal Porto J, Del Nagro C, Dabbagh K, Dyer MJ, Poppema S, Klein C, Umana P (2010) 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 115(22): 4393-4402.
30. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4(2): 133-142.
31. Nicholson RI, Gee JM, Harper ME (2001) EGFR and cancer prognosis. Eur J Cancer 37(Suppl 4): S9-15.
32. Nimmerjahn F, Ravetch JV (2005) Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310(5753): 1510-1512. (Pubitemid 41746349)
33. Raulet DH (2006) Missing self recognition and self tolerance of natural killer (NK) cells. Semin Immunol 18(3): 145-150. (Pubitemid 43817563)
34. Roche (2013) Obinutuzumab (GA101) significantly improved progressionfree survival in people with chronic lymphocytic leukemia (CLL). Available at: http://www.roche.com/media/media-releases/med-cor-2013-01-31.htm. Roche: Basel, Switzerland.
35. Saltz L (2000) Irinotecan-based combinations for the adjuvant treatment of stage III colon cancer. Oncology (Williston Park) 14(12 Suppl 14): 47-50.
36. Sandel MH, Speetjens FM, Menon AG, Albertsson PA, Basse PH, Hokland M, Nagelkerke JF, Tollenaar RA, van de Velde CJ, Kuppen PJ (2005) Natural killer cells infiltrating colorectal cancer and MHC class I expression. Mol Immunol 42(4): 541-546. (Pubitemid 39655966)
37. Schneider-Merck T, Lammerts van Bueren JJ, Berger S, Rossen K, van Berkel PH, Derer S, Beyer T, Lohse S, Bleeker WK, Peipp M, Parren PW, van de Winkel JG, Valerius T, Dechant M (2010) Human IgG2 antibodies against epidermal growth factor receptor effectively trigger antibody-dependent cellular cytotoxicity but, in contrast to IgG1, only by cells of myeloid lineage. J Immunol 184(1): 512-520.
38. Spano JP, Lagorce C, Atlan D, Milano G, Domont J, Benamouzig R, Attar A, Benichou J, Martin A, Morere JF, Raphael M, Penault-Llorca F, Breau JL, Fagard R, Khayat D, Wind P (2005) Impact of EGFR expression on colorectal cancer patient prognosis and survival. Ann Oncol 16(1): 102-108. (Pubitemid 40124486)
39. Taylor RJ, Chan SL, Wood A, Voskens CJ, Wolf JS, Lin W, Chapoval A, Schulze DH, Tian G, Strome SE (2009) FcgammaRIIIa polymorphisms and cetuximab induced cytotoxicity in squamous cell carcinoma of the head and neck. Cancer Immunol Immunother 58(7): 997-1006.
40. Tournigand C, Andre T, Achille E, Lledo G, Flesh M, Mery-Mignard D, Quinaux E, Couteau C, Buyse M, Ganem G, Landi B, Colin P, Louvet C, de Gramont A (2004) FOLFIRI followed by FOLFOX6 or the reverse sequence in advanced colorectal cancer: a randomized GERCOR study. J Clin Oncol 22(2): 229-237. (Pubitemid 41095086)
41. Umana P, Jean-Mairet J, Moudry R, Amstutz H, Bailey JE (1999) Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibodydependent cellular cytotoxic activity. Nat Biotechnol 17(2): 176-180. (Pubitemid 29072543)
42. Van Cutsem E, Kohne CH, Hitre E, Zaluski J, Chang Chien CR, Makhson A, D'Haens G, Pinter T, Lim R, Bodoky G, Roh JK, Folprecht G, Ruff P, Stroh C, Tejpar S, Schlichting M, Nippgen J, Rougier P (2009) Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med 360(14): 1408-1417.
43. Villegas F, Coca S, Villarrubia V, Jiminez R, Chillon M, Jareno J, Zuil M, Callol L (2002) Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer 35: 23-28. (Pubitemid 34028087)
44. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S (2008) Functions of natural killer cells. Nat Immunol 9(5): 503-510. (Pubitemid 351560519)
45. Wu J, Edberg JC, Redecha PB, Bansal V, Guyre PM, Coleman K, Salmon JE, Kimberly RP (1997) A novel polymorphism of FcgammaRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J Clin Invest 100(5): 1059-1070. (Pubitemid 27386289)
46. 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(24): 3712-3718. (Pubitemid 47372612)