Anti-CD22/CD20 bispecific antibody with enhanced trogocytosis for treatment of lupus

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Rossi, Edmund A ^a,b   Chang, Chien Hsing ^a,b   Goldenberg, David M ^a,b,c  

^a IMMUNOMEDICS INC   (United States)

^b IBC Pharmaceuticals Inc   (United States)

^c CENTER FOR MOLECULAR MEDICINE AND IMMUNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD19 ANTIGEN; CD20 ANTIGEN; CD22 ANTIGEN; CD79 ANTIGEN; CD79B ANTIGEN; CELL ADHESION MOLECULE; CELL SURFACE PROTEIN; COMPLEMENT COMPONENT C3D RECEPTOR; EPRATUZUMAB; HERMES ANTIGEN; IMMUNOGLOBULIN FC FRAGMENT; L SELECTIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD20; MONOCLONAL ANTIBODY CD22; RITUXIMAB; UNCLASSIFIED DRUG; VELTUZUMAB; BISPECIFIC ANTIBODY; LYMPHOCYTE ANTIGEN RECEPTOR;

ANTIBODY SPECIFICITY; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CELL COMMUNICATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOCOMPROMISED PATIENT; IMMUNOFLUORESCENCE MICROSCOPY; LYMPHOCYTE DEPLETION; SYSTEMIC LUPUS ERYTHEMATOSUS; TROGOCYTOSIS; COMPARATIVE STUDY; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; IMMUNOLOGICAL SYNAPSE; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, SYSTEMIC; METABOLISM;

ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; B-LYMPHOCYTES; FLOW CYTOMETRY; HUMANS; IMMUNOLOGICAL SYNAPSES; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICROSCOPY, FLUORESCENCE; RECEPTORS, ANTIGEN, B-CELL;

EID: 84901311724     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098315     Document Type: Article

References (50)

1. Goldenberg DM (2006) Epratuzumab in the therapy of oncological and immunological diseases. Expert Rev Anticancer Ther 6: 1341-1353.
2. Looney RJ (2010) B cell-targeted therapies for systemic lupus erythematosus: an update on clinical trial data. Drugs 70: 529-540.
3. Mok MY (2010) The immunological basis of B-cell therapy in systemic lupus erythematosus. Int J Rheum. Dis 13: 3-11.
4. Navarra SV, Guzman RM, Gallacher AE, Hall S, Levy RA, et al. (2011) Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet 377: 721-731.
5. Carnahan J, Wang P, Kendall R, Chen C, Hu S, et al. (2003) Epratuzumab, a humanized monoclonal antibody targeting CD22: characterization of in vitro properties. Clin Cancer Res 9: 3982S-3990S. (Pubitemid 37169205)
6. Carnahan J, Stein R, Qu Z, Hess K, Cesano A, et al. (2007) Epratuzumab, a CD22-targeting recombinant humanized antibody with a different mode of action from rituximab. Mol Immunol 44: 1331-1341. (Pubitemid 44415959)
7. Haas KM, Sen S, Sanford IG, Miller AS, Poe JC, et al. (2006) CD22 ligand binding regulates normal and malignant B lymphocyte survival in vivo. J Immunol 177: 3063-3073. (Pubitemid 44277823)
8. John B, Herrin BR, Raman C, Wang YN, Bobbitt KR, et al. (2003) The B cell coreceptor CD22 associates with AP50, a clathrin-coated pit adapter protein, via tyrosine-dependent interaction. J Immunol 170: 3534-3543. (Pubitemid 36359220)
9. Kelm S, Gerlach J, Brossmer R, Danzer CP, Nitschke L (2002) The ligand-binding domain of CD22 is needed for inhibition of the B cell receptor signal, as demonstrated by a novel human CD22-specific inhibitor compound. J Exp Med 195: 1207-1213. (Pubitemid 34517147)
10. Lajaunias F, Nitschke L, Moll T, Martinez-Soria E, Semac I, et al. (2002) Differentially regulated expression and function of CD22 in activated B-1 and B-2 lymphocytes. J Immunol 168: 6078-6083. (Pubitemid 34620023)
11. Mills DM, Stolpa JC, Cambier JC (2004) Cognate B cell signaling via MHC class II: differential regulation of B cell antigen receptor and MHC class II/Ig-alpha beta signaling by CD22. J Immunol 172: 195-201. (Pubitemid 38020472)
12. Nitschke L (2009) CD22 and Siglec-G: B-cell inhibitory receptors with distinct functions. Immunol Rev 230: 128-143.
13. Onodera T, Poe JC, Tedder TF, Tsubata T (2008) CD22 regulates time course of both B cell division and antibody response. J Immunol 180: 907-913.
14. Richards S, Watanabe C, Santos L, Craxton A, Clark EA (2008) Regulation of B-cell entry into the cell cycle. Immunol Rev 224: 183-200.
15. Samardzic T, Gerlach J, Muller K, Marinkovic D, Hess J, et al. (2002) CD22 regulates early B cell development in BOB.1/OBF.1-deficient mice. Eur J Immunol 32: 2481-2489.
16. Szczepanik M, kahira-Azuma M, Bryniarski K, Tsuji RF, Kawikova I, et al. (2003) B-1 B cells mediate required early T cell recruitment to elicit protein-induced delayed-type hypersensitivity. J Immunol 171: 6225-6235.
17. Walker JA, Smith KG (2008) CD22: an inhibitory enigma. Immunology 123: 314-325. (Pubitemid 351192818)
18. Leung SO, Shevitz J, Pellegrini MC, Dion AS, Shih LB, et al. (1994) Chimerization of LL2, a rapidly internalizing antibody specific for B cell lymphoma. Hybridoma 13: 469-476.
19. Losman MJ, Hansen HJ, Dworak H, Krishnan IS, Qu Z, et al. (1997) Generation of a high-producing clone of a humanized anti-B-cell lymphoma monoclonal antibody (hLL2). Cancer 80: 2660-2666. (Pubitemid 28009524)
20. Goldenberg DM, Stein R, Leonard JP, Steinfeld SD, Dorner T, et al. (2006) B cell therapy with the anti-CD22 monoclonal antibody epratuzumab: comment on the editorial by St. Clair and Tedder. Arthritis Rheum. 54: 2344-2345.
21. Leonard JP, Coleman M, Ketas JC, Chadburn A, Ely S, et al. (2003) Phase I/II trial of epratuzumab (humanized anti-CD22 antibody) in indolent non-Hodgkin's lymphoma. J Clin Oncol 21: 3051-3059. (Pubitemid 46606284)
22. Leonard JP, Coleman M, Ketas JC, Chadburn A, Furman R, et al. (2004) Epratuzumab, a humanized anti-CD22 antibody, in aggressive non-Hodgkin's lymphoma: phase I/II clinical trial results. Clin Cancer Res 10: 5327-5334. (Pubitemid 39100467)
23. Leonard JP, Coleman M, Ketas J, Ashe M, Fiore JM, et al. (2005) Combination antibody therapy with epratuzumab and rituximab in relapsed or refractory non-Hodgkin's lymphoma. J Clin Oncol 23: 5044-5051. (Pubitemid 46224011)
24. Leonard JP, Goldenberg DM (2007) Preclinical and clinical evaluation of epratuzumab (anti-CD22 IgG) in B-cell malignancies. Oncogene 26: 3704-3713. (Pubitemid 46842705)
25. Leonard JP, Schuster SJ, Emmanouilides C, Couture F, Teoh N, et al. (2008) Durable complete responses from therapy with combined epratuzumab and rituximab: final results from an international multicenter, phase 2 study in recurrent, indolent, non-Hodgkin lymphoma. Cancer 113: 2714-2723.
26. Raetz EA, Cairo MS, Borowitz MJ, Blaney SM, Krailo MD, et al. (2008) Chemoimmunotherapy reinduction with epratuzumab in children with acute lymphoblastic leukemia in marrow relapse: a Children's Oncology Group Pilot Study. J Clin Oncol 26: 3756-3762.
27. Steinfeld SD, Tant L, Burmester GR, Teoh NK, Wegener WA, et al. (2006) Epratuzumab (humanised anti-CD22 antibody) in primary Sjogren's syndrome: an open-label phase I/II study. Arthritis Res Ther 8: R129.
28. Dorner T, Kaufmann J, Wegener WA, Teoh N, Goldenberg DM, et al. (2006) Initial clinical trial of epratuzumab (humanized anti-CD22 antibody) for immunotherapy of systemic lupus erythematosus. Arthritis Res Ther 8: R74.
29. Wallace DJ, Gordon C, Strand V, Hobbs K, Petri M, et al. (2013) Efficacy and safety of epratuzumab in patients with moderate/severe flaring systemic lupus erythematosus: results from two randomized, double-blind, placebo-controlled, multicentre studies (ALLEVIATE) and follow-up. Rheumatology. (Oxford) 52: 1313-1322.
30. Wallace DJ, Kalunian K, Petri MA, Strand V, Houssiau FA, et al. (2013) Efficacy and safety of epratuzumab in patients with moderate/severe active systemic lupus erythematosus: results from EMBLEM, a phase IIb, randomised, double-blind, placebo-controlled, multicentre study. Ann Rheum Dis.
31. Wallace D, Kalunian K, Petri M, Strand V, Kilgallen B, et al. (2010) Epratuzumab demonstrates clinically meaningful improvements in patients with moderate to severe systemic lupus erythematosus (SLE): Results from EMBLEM™, a phase IIb study. Ann Rheum Dis (suppl 3): 558.
32. Rossi EA, Goldenberg DM, Michel R, Rossi DL, Wallace DJ, et al. (2013) Trogocytosis of multiple B-cell surface markers by CD22 targeting with epratuzumab. Blood 122: 3020-3029.
33. Joly E, Hudrisier D (2003) What is trogocytosis and what is its purpose? Nat Immunol 4: 815. (Pubitemid 37098646)
34. Beum PV, Kennedy AD, Williams ME, Lindorfer MA, Taylor RP (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. (Pubitemid 43201712)
35. Ahmed KA, Xiang J (2011) Mechanisms of cellular communication through intercellular protein transfer. J Cell Mol Med 15: 1458-1473.
36. Davis DM (2007) Intercellular transfer of cell-surface proteins is common and can affect many stages of an immune response. Nat Rev Immunol 7: 238-243.
37. Rechavi O, Goldstein I, Kloog Y (2009) Intercellular exchange of proteins: the immune cell habit of sharing. FEBS Lett 583: 1792-1799.
38. Sprent J (2005) Swapping molecules during cell-cell interactions. Sci STKE. 2005: e8.
39. Ahmed KA, Munegowda MA, Xie Y, Xiang J (2008) Intercellular trogocytosis plays an important role in modulation of immune responses. Cell Mol Immunol 5: 261-269.
40. Caumartin J, Lemaoult J, Carosella ED (2006) Intercellular exchanges of membrane patches (trogocytosis) highlight the next level of immune plasticity. Transpl. Immunol 17: 20-22. (Pubitemid 44828805)
41. Lemaoult J, Caumartin J, Daouya M, Favier B, Le RS, et al. (2007) Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells. Blood 109: 2040-2048. (Pubitemid 46348204)
42. Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, et al. (2006) Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: Results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 54: 2793-2806. (Pubitemid 44497758)
43. Gunnarsson I, Jonsdottir T (2013) Rituximab treatment in lupus nephritis-where do we stand? Lupus 22: 381-389.
44. Mysler EF, Spindler AJ, Guzman R, Bijl M, Jayne D, et al. (2013) Efficacy and safety of ocrelizumab in active proliferative lupus nephritis: results from the randomized, double-blind phase III BELONG study. Arthritis Rheum.
45. Rossi EA, Chang CH, Cardillo TM, Goldenberg DM (2013) Optimization of multivalent bispecific antibodies and immunocytokines with improved in vivo properties. Bioconjug. Chem 24: 63-71.
46. Goldenberg DM, Morschhauser F, Wegener WA (2010) Veltuzumab (humanized anti-CD20 monoclonal antibody): characterization, current clinical results, and future prospects. Leuk Lymphoma 51: 747-755.
47. Sharkey RM, Juweid M, Shevitz J, Behr T, Dunn R, et al. (1995) Evaluation of a complementarity-determining region-grafted (humanized) anti-carcinoembryonic antigen monoclonal antibody in preclinical and clinical studies. Cancer Res 55: 5935s-5945s.
48. Rossi DL, Rossi EA, Goldenberg DM, Chang CH (2011) A new mammalian host cell with enhanced survival enables completely serum-free development of high-level protein production cell lines. Biotechnol. Prog. 27: 766-775.
49. Rossi EA, Goldenberg DM, Cardillo TM, Stein R, Chang CH (2009) Hexavalent bispecific antibodies represent a new class of anticancer therapeutics: 1. Properties of anti-CD20/CD22 antibodies in lymphoma. Blood 113: 6161-6171.
50. Gupta P, Goldenberg DM, Rossi EA, Chang CH (2010) Multiple signaling pathways induced by hexavalent, monospecific, anti-CD20 and hexavalent, bispecific, anti-CD20/CD22 humanized antibodies correlate with enhanced toxicity to B-cell lymphomas and leukemias. Blood 116: 3258-3267.