Inhibitory FcγRIIb (CD32b) becomes activated by therapeutic mAb in both cis and trans and drives internalization according to antibody specificity

Blood

Volumn 123, Issue 5, 2014, Pages 669-677

  Vaughan, Andrew T ^a   Iriyama, Chisako ^a,b   Beers, Stephen A ^a   Chan, Claude H T ^a   Lim, Sean H ^a   Williams, Emily L ^a   Shah, Vallari ^a   Roghanian, Ali ^a   Frendéus, Bjorn ^c   Glennie, Martin J ^a   Cragg, Mark S ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c BioInvent International AB   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 ANTIGEN; CD19 MONOCLONAL ANTIBODY; CD20 MONOCLONAL ANTIBODY; CD22 MONOCLONAL ANTIBODY; CD32 MONOCLONAL ANTIBODY; CD38 ANTIGEN; CD38 MONOCLONAL ANTIBODY; CD40 LIGAND MONOCLONAL ANTIBODY; FC RECEPTOR IIB; IMMUNOGLOBULIN M ANTIBODY; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1 MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY; OBINUTUZUMAB; RITUXIMAB; TOSITUMOMAB; UNCLASSIFIED DRUG; CD20 ANTIGEN; FC RECEPTOR; ISOPROTEIN;

ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; CELL DENSITY; CELL SURFACE; CHRONIC LYMPHATIC LEUKEMIA; CIS ISOMER; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG RECEPTOR BINDING; HUMAN; HUMAN CELL; INTERNALIZATION; LEUKEMIA CELL LINE; PRIMARY CELL LINE; PRIORITY JOURNAL; TRANS ISOMER; TRANSCRIPTION INITIATION; IMMUNOLOGY; METABOLISM; PROTEIN TRANSPORT;

ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; ANTIGENS, CD20; B-LYMPHOCYTES; HUMANS; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RECEPTORS, IGG;

EID: 84894078151     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-04-490821     Document Type: Article

References (45)

1. Glennie MJ, French RR, Cragg MS, Taylor RP. Mechanisms of killing by anti-CD20 monoclonal antibodies. Mol Immunol. 2007;44(16):3823-3837. (Pubitemid 47332625)
2. Beers SA, French RR, Chan HT, et al. Antigenic modulation limits the efficacy of anti-CD20 antibodies: implications for antibody selection. Blood. 2010;115(25):5191-5201.
3. Lim SH, Vaughan AT, Ashton-Key M, et al. Fc gamma receptor IIb on target B cells promotes rituximab internalization and reduces clinical efficacy. Blood. 2011;118(9):2530-2540.
4. Benichou G, Voisin GA. Antibody bipolar bridging: isotype-dependent signals given to guinea pig alveolar macrophages by anti-MHC alloantibodies. Cell Immunol. 1987;106(2):304-317. (Pubitemid 17106564)
5. Molina A. A decade of rituximab: improving survival outcomes in non-Hodgkin's lymphoma. Annu Rev Med. 2008;59:237-250. (Pubitemid 351291630)
6. Lenz G, Dreyling M, Hoster E, et al. Immunochemotherapy with rituximab and cyclophosphamide, doxorubicin, vincristine, and prednisone significantly improves response and time to treatment failure, but not long-term outcome in patients with previously untreated mantle cell lymphoma: results of a prospective randomized trial of the German Low Grade Lymphoma Study Group (GLSG). J Clin Oncol. 2005;23(9):1984-1992. (Pubitemid 46211378)
7. Hallek M, Fischer K, Fingerle-Rowson G, et al International Group of Investigators; German Chronic Lymphocytic Leukaemia Study Group. Addition of rituximab to fludarabine and cyclophosphamide in patients with chronic lymphocytic leukaemia: a randomised, open-label, phase 3 trial. Lancet. 2010;376(9747):1164-1174.
8. O'Brien SM, Kantarjian H, Thomas DA, et al. Rituximab dose-escalation trial in chronic lymphocytic leukemia. J Clin Oncol. 2001;19(8):2165-2170. (Pubitemid 32366970)
9. Lee L, Crump M, Khor S, et al. Impact of rituximab on treatment outcomes of patients with diffuse large b-cell lymphoma: a population-based analysis. Br J Haematol. 2012;158(4):481-488.
10. Beers SA, Chan CH, James S, et al. Type II (tositumomab) anti-CD20 monoclonal antibody out performs type I (rituximab-like) reagents in B-cell depletion regardless of complement activation. Blood. 2008;112(10):4170-4177.
11. Beers SA, Chan CH, French RR, Cragg MS, Glennie MJ. CD20 as a target for therapeutic type I and II monoclonal antibodies. Semin Hematol. 2010;47(2):107-114.
12. Chan CH, Wang J, French RR, Glennie MJ. Internalization of the lymphocytic surface protein CD22 is controlled by a novel membrane proximal cytoplasmic motif. J Biol Chem. 1998;273(43):27809-27815. (Pubitemid 28496067)
13. Press OW, Farr AG, Borroz KI, Anderson SK, Martin PJ. Endocytosis and degradation of monoclonal antibodies targeting human B-cell malignancies. Cancer Res. 1989;49(17):4906-4912. (Pubitemid 19213646)
14. Ellis JH, Barber KA, Tutt A, et al. Engineered anti-CD38 monoclonal antibodies for immunotherapy of multiple myeloma. J Immunol. 1995;155(2):925-937.
15. Bonardi MA, French RR, Amlot P, Gromo G, Modena D, Glennie MJ. Delivery of saporin to human B-cell lymphoma using bispecific antibody: targeting via CD22 but not CD19, CD37, or immunoglobulin results in efficient killing. Cancer Res. 1993;53(13):3015-3021. (Pubitemid 23210305)
16. Elsässer D, Valerius T, Repp R, et al. HLA class II as potential target antigen on malignant B cells for therapy with bispecific antibodies in combination with granulocyte colony-stimulating factor. Blood. 1996;87(9):3803-3812. (Pubitemid 26129608)
17. Greenman J, Tutt AL, George AJ, Pulford KA, Stevenson GT, Glennie MJ. Characterization of a new monoclonal anti-Fc gamma RII antibody, AT10, and its incorporation into a bispecific F(ab′) 2 derivative for recruitment of cytotoxic effectors. Mol Immunol. 1991;28(11):1243-1254.
18. Press OW, Eary JF, Badger CC, et al. Treatment of refractory non-Hodgkin's lymphoma with radiolabeled MB-1 (anti-CD37) antibody. J Clin Oncol. 1989;7(8):1027-1038. (Pubitemid 19196525)
19. Mason DY, Stein H, Gerdes J, et al. Value of monoclonal anti-CD22 (p135) antibodies for the detection of normal and neoplastic B lymphoid cells. Blood. 1987;69(3):836-840. (Pubitemid 17057465)
20. Walshe CA, Beers SA, French RR, et al. Induction of cytosolic calcium flux by CD20 is dependent upon B Cell antigen receptor signaling. J Biol Chem. 2008;283(25):16971-16984.
21. Budde P, Bewarder N, Weinrich V, Schulzeck O, Frey J. Tyrosine-containing sequence motifs of the human immunoglobulin G receptors FcRIIb1 and FcRIIb2 essential for endocytosis and regulation of calcium flux in B cells. J Biol Chem. 1994;269(48):30636-30644. (Pubitemid 24376551)
22. Miettinen HM, Rose JK, Mellman I. Fc receptor isoforms exhibit distinct abilities for coated pit localization as a result of cytoplasmic domain heterogeneity. Cell. 1989;58(2):317-327. (Pubitemid 19191414)
23. Nimmerjahn F, Ravetch JV. Antibodies, Fc receptors and cancer. Curr Opin Immunol. 2007;19(2):239-245. (Pubitemid 46356962)
24. Luqman M, Klabunde S, Lin K, et al. The antileukemia activity of a human anti-CD40 antagonist antibody, HCD122, on human chronic lymphocytic leukemia cells. Blood. 2008;112(3):711-720.
25. Johnson PW, Steven NM, Chowdhury F, Tutt AL, Glennie M. A Cancer Research UK phase I study evaluating safety, tolerability, and biological effects of chimeric anti-CD40 monoclonal antibody (MAb), Chi Lob 7/4 [abstract]. J Clin Oncol. 2010;28:Abstract 2507.
26. Chan HT, Hughes D, French RR, et al. CD20-induced lymphoma cell death is independent of both caspases and its redistribution into triton X-100 insoluble membrane rafts. Cancer Res. 2003;63(17):5480-5489. (Pubitemid 37139867)
27. Niederfellner G, Lammens A, Mundigl O, et al. Epitope characterization and crystal structure of GA101 provide insights into the molecular basis for type I/II distinction of CD20 antibodies. Blood. 2011;118(2):358-367.
28. Lubinski JM, Lazear HM, Awasthi S, Wang F, Friedman HM. The herpes simplex virus 1 IgG fc receptor blocks antibody-mediated complement activation and antibody-dependent cellular cytotoxicity in vivo. J Virol. 2011;85(7):3239-3249.
29. Van Vliet KE, De Graaf-Miltenburg LA, Verhoef J, Van Strijp JA. Direct evidence for antibody bipolar bridging on herpes simplex virus-infected cells. Immunology. 1992;77(1):109-115.
30. Wang SY, Racila E, Taylor RP, Weiner GJ. NK-cell activation and antibody-dependent cellular cytotoxicity induced by rituximab-coated target cells is inhibited by the C3b component of complement. Blood. 2008;111(3):1456-1463. (Pubitemid 351213433)
31. Wang SY, Veeramani S, Racila E, et al. Depletion of the C3 component of complement enhances the ability of rituximab-coated target cells to activate human NK cells and improves the efficacy of monoclonal antibody therapy in an in vivo model. Blood. 2009;114(26):5322-5330.
32. Cragg MS, Glennie MJ. Antibody specificity controls in vivo effector mechanisms of anti-CD20 reagents. Blood. 2004;103(7):2738-2743. (Pubitemid 38393032)
33. Beum PV, Kennedy AD, Williams ME, Lindorfer MA, Taylor RP. The shaving reaction: rituximab/CD20 complexes are removed from mantle cell lymphoma and chronic lymphocytic leukemia cells by THP-1 monocytes. J Immunol. 2006;176(4):2600-2609. (Pubitemid 43201712)
34. Muta T, Kurosaki T, Misulovin Z, Sanchez M, Nussenzweig MC, Ravetch JV. A 13-amino-acid motif in the cytoplasmic domain of Fc gamma RIIB modulates B-cell receptor signalling. Nature. 1994;369(6478):340. (Pubitemid 24159548)
35. Malbec O, Fridman WH, Daëron M. Negative regulation of hematopoietic cell activation and proliferation by Fc gamma RIIB. Curr Top Microbiol Immunol. 1999;244:13-27. (Pubitemid 29304667)
36. Williams EL, Tutt AL, French RR, et al. Development and characterisation of monoclonal antibodies specific for the murine inhibitory FcgRIIB (CD32B). Eur J Immunol. 2012;42(8):2109-2120.
37. Tzeng SJ, Bolland S, Inabe K, Kurosaki T, Pierce SK. The B cell inhibitory Fc receptor triggers apoptosis by a novel c-Abl family kinase-dependent pathway. J Biol Chem. 2005;280(42):35247-35254. (Pubitemid 41532712)
38. Clark MR, Massenburg D, Siemasko K, Hou P, Zhang M. B-cell antigen receptor signaling requirements for targeting antigen to the MHC class II presentation pathway. Curr Opin Immunol. 2004;16(3):382-387. (Pubitemid 38595378)
39. Abès R, Gélizé E, Fridman WH, Teillaud JL. Long-lasting antitumor protection by anti-CD20 antibody through cellular immune response. Blood. 2010;116(6):926-934.
40. Gergely J, Sármay G. Fc gamma RII-mediated regulation of human B cells. Scand J Immunol. 1996;44(1):1-10. (Pubitemid 26227449)
41. Wagle NM, Faassen AE, Kim JH, Pierce SK. Regulation of B cell receptor-mediated MHC class II antigen processing by FcgammaRIIB1. J Immunol. 1999;162(5):2732-2740. (Pubitemid 29309296)
42. Rankin CT, Veri MC, Gorlatov S, et al. CD32B, the human inhibitory Fc-gamma receptor IIB, as a target for monoclonal antibody therapy of B-cell lymphoma. Blood. 2006;108(7):2384-2391. (Pubitemid 44497523)
43. Hu CY, Rodriguez-Pinto D, DuW, et al. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J Clin Invest. 2007;117(12):3857-3867.
44. Su K, Yang H, Li X, et al. Expression profile of FcgammaRIIb on leukocytes and its dysregulation in systemic lupus erythematosus. J Immunol. 2007;178(5):3272-3280. (Pubitemid 46333211)
45. Qian L, Qian C, Chen Y, et al. Regulatory dendritic cells program B cells to differentiate into CD19hiFcγIIbhi regulatory B cells through IFN-β and CD40L. Blood. 2012;120(3):581-591.