A novel anti-CD19 monoclonal antibody (GBR 401) with high killing activity against B cell malignancies

Journal of Hematology and Oncology

Volumn 7, Issue 1, 2014, Pages

  Breton, Caroline S ^a   Nahimana, Aimable ^a   Aubry, Dominique ^a   Macoin, Julie ^b   Moretti, Pierre ^b   Bertschinger, Martin ^b   Hou, Samuel ^b   Duchosal, Michel A ^a   Back, Jonathan ^b  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b Glenmark Pharmaceuticals SA   (Switzerland)

Author keywords

ADCC; Anti CD19 monoclonal antibody; B cell malignancies; GBR 401; Therapeutic antibody

Indexed keywords

CD19 ANTIBODY; CD20 ANTIBODY; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY GBR 401; RITUXIMAB; UNCLASSIFIED DRUG; CD19 ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; BURKITT LYMPHOMA; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CELL DEATH; CELL KILLING; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFICACY; DRUG MECHANISM; HUMAN; HUMAN CELL; HUMORAL IMMUNE DEFICIENCY; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; RAJI CELL; SCID MOUSE; SINGLE DRUG DOSE; XENOGRAFT; ANIMAL; DRUG SCREENING; IMMUNOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD19; BURKITT LYMPHOMA; CELL LINE, TUMOR; HUMANS; MICE; MICE, SCID; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84899473907     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/1756-8722-7-33     Document Type: Article

References (49)

1. Treatment with monoclonal antibodies in acute lymphoblastic leukemia: current knowledge and future prospects. Gokbuget N, Hoelzer D, Ann Hematol 2004 83 201 205 10.1007/s00277-003-0752-8 14648023
2. Modern therapy of acute lymphoblastic leukemia. Bassan R, Hoelzer D, J Clin Oncol 2011 29 532 543 10.1200/JCO.2010.30.1382 21220592
3. Monoclonal antibodies in the treatment of non-Hodgkin's lymphoma. Fanale MA, Younes A, Drugs 2007 67 333 350 10.2165/00003495-200767030-00002 17335294
4. Anti-CD20 antibody therapy for B-cell lymphomas. Maloney DG, N Engl J Med 2012 366 2008 2016 10.1056/NEJMct1114348 22621628
5. Novel antibody-based therapies for acute lymphoblastic leukemia. Hoelzer D, Hematology Am Soc Hematol Educ Program 2011 2011 243 249 10.1182/ asheducation-2011.1.243 22160041
6. Fcgamma receptor-dependent effector mechanisms regulate CD19 and CD20 antibody immunotherapies for B lymphocyte malignancies and autoimmunity. Tedder TF, Baras A, Xiu Y, Springer Semin Immunopathol 2006 28 351 364 10.1007/s00281-006-0057-9 17091246
7. The in vivo mechanism of action of CD20 monoclonal antibodies depends on local tumor burden. Boross P, Jansen JH, De Haij S, Beurskens FJ, van der Poel CE, Bevaart L, Nederend M, Golay J, van de Winkel JG, Parren PW, Leusen JH, Haematologica 2011 96 1822 1830 10.3324/haematol.2011.047159 21880632
8. The predictive significance of CD20 expression in B-cell lymphomas. Prevodnik VK, Lavrencak J, Horvat M, Novakovic BJ, Diagn Pathol 2011 6 33 10.1186/1746-1596-6-33 21486448
9. Therapy of B-cell lymphoma with anti-CD20 antibodies can result in the loss of CD20 antigen expression. Davis TA, Czerwinski DK, Levy R, Clin Cancer Res 1999 5 611 615 10100713
10. Thrice-weekly low-dose rituximab decreases CD20 loss via shaving and promotes enhanced targeting in chronic lymphocytic leukemia. Williams ME, Densmore JJ, Pawluczkowycz AW, Beum PV, Kennedy AD, Lindorfer MA, Hamil SH, Eggleton JC, Taylor RP, J Immunol 2006 177 7435 7443 17082663
11. Identification of an alternative CD20 transcript variant in B-cell malignancies coding for a novel protein associated to rituximab resistance. Henry C, Deschamps M, Rohrlich PS, Pallandre JR, Remy-Martin JP, Callanan M, Traverse-Glehen A, GrandClement C, Garnache-Ottou F, Gressin R, Deconinck E, Salles G, Robinet E, Tiberghien P, Borg C, Ferrand C, Blood 2010 115 2420 2429 10.1182/blood-2009-06-229112 20089966
12. Rituximab infusion promotes rapid complement depletion and acute CD20 loss in chronic lymphocytic leukemia. Kennedy AD, Beum PV, Solga MD, DiLillo DJ, Lindorfer MA, Hess CE, Densmore JJ, Williams ME, Taylor RP, J Immunol 2004 172 3280 3288 14978136
13. B cell-directed therapies for autoimmune disease and correlates of disease response and relapse. Levesque MC, St Clair EW, J Allergy Clin Immunol 2008 121 13 21 quiz 22-13 10.1016/j.jaci.2007.11.030 18206502
14. CD19 antigen in leukemia and lymphoma diagnosis and immunotherapy. Scheuermann RH, Racila E, Leuk Lymphoma 1995 18 385 397 10.3109/ 10428199509059636 8528044
15. Expression of human B cell-associated antigens on leukemias and lymphomas: a model of human B cell differentiation. Anderson KC, Bates MP, Slaughenhoupt BL, Pinkus GS, Schlossman SF, Nadler LM, Blood 1984 63 1424 1433 6609729
16. A glycoengineered anti-CD19 antibody with potent antibody-dependent cellular cytotoxicity activity in vitro and lymphoma growth inhibition in vivo. Ward E, Mittereder N, Kuta E, Sims GP, Bowen MA, Dall'Acqua W, Tedder T, Kiener P, Coyle AJ, Wu H, Jallal B, Herbst R, Br J Haematol 2011 155 426 437 10.1111/j.1365-2141.2011.08857.x 21902688
17. A nonfucosylated human antibody to CD19 with potent B-cell depletive activity for therapy of B-cell malignancies. Cardarelli PM, Rao-Naik C, Chen S, Huang H, Pham A, Moldovan-Loomis MC, Pan C, Preston B, Passmore D, Liu J, Kuhne MR, Witte A, Blanset D, King DJ, Cancer Immunol Immunother 2010 59 257 265 10.1007/s00262-009-0746-z 19657637
18. Anti-CD19 and anti-CD22 monoclonal antibodies increase the effectiveness of chemotherapy in Pre-B acute lymphoblastic leukemia cell lines. Stanciu-Herrera C, Morgan C, Herrera L, Leuk Res 2008 32 625 632 10.1016/j.leukres.2007.07.002 17706771
19. Immunotherapy using unconjugated CD19 monoclonal antibodies in animal models for B lymphocyte malignancies and autoimmune disease. Yazawa N, Hamaguchi Y, Poe JC, Tedder TF, Proc Natl Acad Sci U S A 2005 102 15178 15183 10.1073/pnas.0505539102 16217038
20. Structural basis for improved efficacy of therapeutic antibodies on defucosylation of their Fc glycans. Mizushima T, Yagi H, Takemoto E, Shibata-Koyama M, Isoda Y, Iida S, Masuda K, Satoh M, Kato K, Genes Cells 2011 16 1071 1080 10.1111/j.1365-2443.2011.01552.x 22023369
21. Fucose depletion from human IgG1 oligosaccharide enhances binding enthalpy and association rate between IgG1 and FcgammaRIIIa. Okazaki A, Shoji-Hosaka E, Nakamura K, Wakitani M, Uchida K, Kakita S, Tsumoto K, Kumagai I, Shitara K, J Mol Biol 2004 336 1239 1249 10.1016/j.jmb.2004.01.007 15037082
22. Macrophage and NK-mediated killing of precursor-B acute lymphoblastic leukemia cells targeted with a-fucosylated anti-CD19 humanized antibodies. Matlawska-Wasowska K, Ward E, Stevens S, Wang Y, Herbst R, Winter SS, Wilson BS, Leukemia 2013 27 1263 1274 10.1038/leu.2013.5 23307031
23. GA101 induces NK-cell activation and antibody-dependent cellular cytotoxicity more effectively than rituximab when complement is present. Kern DJ, James BR, Blackwell S, Gassner C, Klein C, Weiner GJ, Leuk Lymphoma 2013 54 2500 2505 10.3109/10428194.2013.781169 23452151
24. An afucosylated anti-CD20 monoclonal antibody with greater antibody-dependent cellular cytotoxicity and B-cell depletion and lower complement-dependent cytotoxicity than rituximab. Gasdaska JR, Sherwood S, Regan JT, Dickey LF, Mol Immunol 2012 50 134 141 10.1016/j.molimm.2012.01.001 22305040
25. Levels of expression of CD19 and CD20 in chronic B cell leukaemias. Ginaldi L, De Martinis M, Matutes E, Farahat N, Morilla R, Catovsky D, J Clin Pathol 1998 51 364 369 10.1136/jcp.51.5.364 9708202
26. Rituximab: converging mechanisms of action in non-Hodgkin's lymphoma? Eisenbeis CF, Caligiuri MA, Byrd JC, Clin Cancer Res 2003 9 5810 5812 14676100
27. Rituximab (monoclonal anti-CD20 antibody): mechanisms of action and resistance. Smith MR, Oncogene 2003 22 7359 7368 10.1038/sj.onc.1206939 14576843
28. B-cell depletion in vitro and in vivo with an afucosylated anti-CD19 antibody. Herbst R, Wang Y, Gallagher S, Mittereder N, Kuta E, Damschroder M, Woods R, Rowe DC, Cheng L, Cook K, Evans K, Sims GP, Pfarr DS, Bowen MA, Dall'Acqua W, Shlomchik M, Tedder TF, Kiener P, Jallal B, Wu H, Coyle AJ, J Pharmacol Exp Ther 2010 335 213 222 10.1124/jpet.110.168062 20605905
29. Potent in vitro and in vivo activity of an Fc-engineered anti-CD19 monoclonal antibody against lymphoma and leukemia. Horton HM, Bernett MJ, Pong E, Peipp M, Karki S, Chu SY, Richards JO, Vostiar I, Joyce PF, Repp R, Desjarlais JR, Zhukovsky EA, Cancer Res 2008 68 8049 8057 10.1158/0008-5472.CAN- 08-2268 18829563
30. The impact of Fc engineering on an anti-CD19 antibody: increased Fcgamma receptor affinity enhances B-cell clearing in nonhuman primates. Zalevsky J, Leung IW, Karki S, Chu SY, Zhukovsky EA, Desjarlais JR, Carmichael DF, Lawrence CE, Blood 2009 113 3735 3743 10.1182/blood-2008-10-182048 19109559
31. B cell antigen receptor-mediated apoptosis. Importance of accessory molecules CD19 and CD22, and of surface IgM cross-linking. Chaouchi N, Vazquez A, Galanaud P, Leprince C, J Immunol 1995 154 3096 3104 7534787
32. Caspase-independent killing of Burkitt lymphoma cell lines by rituximab. Daniels I, Abulayha AM, Thomson BJ, Haynes AP, Apoptosis 2006 11 1013 1023 10.1007/s10495-006-6314-5 16544097
33. CD20-induced lymphoma cell death is independent of both caspases and its redistribution into triton X-100 insoluble membrane rafts. Chan HT, Hughes D, French RR, Tutt AL, Walshe CA, Teeling JL, Glennie MJ, Cragg MS, Cancer Res 2003 63 5480 5489 14500384
34. Monoclonal antibodies directed to CD20 and HLA-DR can elicit homotypic adhesion followed by lysosome-mediated cell death in human lymphoma and leukemia cells. Ivanov A, Beers SA, Walshe CA, Honeychurch J, Alduaij W, Cox KL, Potter KN, Murray S, Chan CH, Klymenko T, Erenpreisa J, Glennie MJ, Illidge TM, Cragg MS, J Clin Invest 2009 119 2143 2159 19620786
35. Autophagy: from phenomenology to molecular understanding in less than a decade. Klionsky DJ, Nat Rev Mol Cell Biol 2007 8 931 937 10.1038/nrm2245 17712358
36. Antibody-induced nonapoptotic cell death in human lymphoma and leukemia cells is mediated through a novel reactive oxygen species-dependent pathway. Honeychurch J, Alduaij W, Azizyan M, Cheadle EJ, Pelicano H, Ivanov A, Huang P, Cragg MS, Illidge TM, Blood 2012 119 3523 3533 10.1182/blood-2011-12-395541 22354003
37. Combination anti-CD74 (milatuzumab) and anti-CD20 (rituximab) monoclonal antibody therapy has in vitro and in vivo activity in mantle cell lymphoma. Alinari L, Yu B, Christian BA, Yan F, Shin J, Lapalombella R, Hertlein E, Lustberg ME, Quinion C, Zhang X, Lozanski G, Muthusamy N, Prætorius-Ibba M, O'Connor OA, Goldenberg DM, Byrd JC, Blum KA, Baiocchi RA, Blood 2011 117 4530 4541 10.1182/blood-2010-08-303354 21228331
38. Molecular mechanisms of CD99-induced caspase-independent cell death and cell-cell adhesion in Ewing's sarcoma cells: actin and zyxin as key intracellular mediators. Cerisano V, Aalto Y, Perdichizzi S, Bernard G, Manara MC, Benini S, Cenacchi G, Preda P, Lattanzi G, Nagy B, Knuutila S, Colombo MP, Bernard A, Picci P, Scotlandi K, Oncogene 2004 23 5664 5674 10.1038/sj.onc. 1207741 15184883
39. CD40 stimulation sensitizes CLL cells to lysosomal cell death induction by type II anti-CD20 mAb GA101. Jak M, Van Bochove GG, Reits EA, Kallemeijn WW, Tromp JM, Umana P, Klein C, Van Lier RA, Van Oers MH, Eldering E, Blood 2011 118 5178 5188 10.1182/blood-2011-01-331702 21948297
40. Novel type II anti-CD20 monoclonal antibody (GA101) evokes homotypic adhesion and actin-dependent, lysosome-mediated cell death in B-cell malignancies. Alduaij W, Ivanov A, Honeychurch J, Cheadle EJ, Potluri S, Lim SH, Shimada K, Chan CH, Tutt A, Beers SA, Glennie MJ, Cragg MS, Illidge TM, Blood 2011 117 4519 4529 10.1182/blood-2010-07-296913 21378274
41. Monoclonal antibody therapy for B-cell malignancies. Cheson BD, Semin Oncol 2006 33 2 14
42. Monoclonal antibodies for B-cell lymphomas: rituximab and beyond. Bello C, Sotomayor EM, Hematology Am Soc Hematol Educ Program 2007 2007 233 242 10.1182/asheducation-2007.1.233
43. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Ferrara C, Grau S, Jager C, Sondermann P, Brunker P, Waldhauer I, Hennig M, Ruf A, Rufer AC, Stihle M, Umaña P, Benz J, Proc Natl Acad Sci U S A 2011 108 12669 12674 10.1073/pnas.1108455108 21768335
44. Quantitative evaluation of fucose reducing effects in a humanized antibody on Fcgamma receptor binding and antibody-dependent cell-mediated cytotoxicity activities. Chung S, Quarmby V, Gao X, Ying Y, Lin L, Reed C, Fong C, Lau W, Qiu ZJ, Shen A, Vanderlaan M, Song A, MAbs 2012 4 326 340 10.4161/mabs.19941 22531441
45. Two mechanisms of the enhanced antibody-dependent cellular cytotoxicity (ADCC) efficacy of non-fucosylated therapeutic antibodies in human blood. Iida S, Kuni-Kamochi R, Mori K, Misaka H, Inoue M, Okazaki A, Shitara K, Satoh M, BMC Cancer 2009 9 58 10.1186/1471-2407-9-58 19226457
46. Improving effector functions of antibodies for cancer treatment: Enhancing ADCC and CDC. Natsume A, Niwa R, Satoh M, Drug Des Devel Ther 2009 3 7 16 19920917
47. Enhanced ADCC activity of affinity maturated and Fc-engineered mini-antibodies directed against the AML stem cell antigen CD96. Mohseni Nodehi S, Repp R, Kellner C, Brautigam J, Staudinger M, Schub N, Peipp M, Gramatzki M, Humpe A, PLoS ONE 2012 7 42426 10.1371/journal.pone.0042426 22879978
48. Antigenic modulation limits the efficacy of anti-CD20 antibodies: implications for antibody selection. Beers SA, French RR, Chan HT, Lim SH, Jarrett TC, Vidal RM, Wijayaweera SS, Dixon SV, Kim H, Cox KL, Kerr JP, Johnston DA, Johnson PW, Verbeek JS, Glennie MJ, Cragg MS, Blood 2010 115 5191 5201 10.1182/blood-2010-01-263533 20223920
49. Caspase-independent type III programmed cell death in chronic lymphocytic leukemia: the key role of the F-actin cytoskeleton. Barbier S, Chatre L, Bras M, Sancho P, Roue G, Virely C, Yuste VJ, Baudet S, Rubio M, Esquerda JE, Sarfati M, Merle-Béral H, Susin SA, Haematologica 2009 94 507 517 10.3324/haematol.13690 19278964