Molecular engineering to improve antibodies' anti-lymphoma activity

Best Practice and Research: Clinical Haematology

Volumn 24, Issue 2, 2011, Pages 217-229

  Peipp, Matthias ^a   Van De Winkel, Jan G J ^b,c   Valerius, Thomas ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c GENMAB   (Netherlands)

Author keywords

ADCC; antibody engineering; CDC; immunotherapy; pharmacokinetics

Indexed keywords

ALANINE; ANTINEOPLASTIC AGENT; CASPASE; CD16 ANTIGEN; CD20 ANTIBODY; CD20 ANTIGEN; DACLIZUMAB; ECULIZUMAB; EPITOPE; FC RECEPTOR IIA; FC RECEPTOR IIB; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4; LFB R 603; MONOCLONAL ANTIBODY; RITUXIMAB; UNCLASSIFIED DRUG;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY ENGINEERING; ANTIBODY ISOLATION; ANTIGEN ANTIBODY REACTION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; BLOOD; BONE MARROW; CELL PROLIFERATION; CHRONIC LYMPHATIC LEUKEMIA; COMPLEMENT ACTIVATION; COMPLEMENT DEPENDENT CYTOTOXICITY; CRYSTAL STRUCTURE; DOWN REGULATION; EXPERIMENTAL MODEL; EXPERIMENTAL MOUSE; GRANULOCYTE; IMMUNE RESPONSE; IMMUNOGENICITY; IN VITRO STUDY; LYMPH NODE; LYMPHOMA; MACROPHAGE; MITOSIS INHIBITION; MONOCYTE; NONHUMAN; PLASMA HALF LIFE; PRIMATE; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN GLYCOSYLATION; PROTEIN POLYMORPHISM;

EID: 79958262207     PISSN: 15216926     EISSN: 15321924     Source Type: Journal    
DOI: 10.1016/j.beha.2011.03.004     Document Type: Review

References (91)

1. G. Köhler, and C. Milstein Continuous cultures of fused cells secreting antibody of predefined specificity Nature 256 1975 495 497
2. K.A. Foon, and R.F. Todd Immunologic classification of leukemia and lymphoma Blood 68 1986 1 31 (Pubitemid 16041710)
3. O.W. Press, F. Appelbaum, and J.A. Ledbetter Monoclonal antibody 1F5 (anti-CD20) serotherapy of human B-cell lymphomas Blood 694 1987 584 591 (Pubitemid 17022032)
4. P. Ehrlich On immunity with special reference to cell life Proc Royal Soc London 66 1900 424 448
5. M.S. Neuberger, G.T. Williams, and E.B. Mitchell A hapten-specific chimaeric IgE antibody with human physiological effector function Nature 314 6008 1985 268 270 (Pubitemid 15076516)
6. L. Riechmann, M. Clark, and H. Waldmann Reshaping human antibodies for therapy Nature 332 1988 323 327 (Pubitemid 18091075)
7. V. Ghetie, and E.S. Ward Multiple roles for the major histocompatibility complex class I- related receptor FcRn Annu Rev Immunol 18 2000 739 766 (Pubitemid 30365396)
8. D.G. Maloney, A.J. Grillo-Lopez, and C.A. White IDEC-C2B8 (Rituximab) anti-CD20 monoclonal antibody therapy in patients with relapsed low-grade non-Hodgkin's lymphoma Blood 90 6 1997 2188 2195 (Pubitemid 27392702)
9. B.D. Cheson, and J.P. Leonhard Monoclonal antibody therapy for B- cell non-Hodgkin's lymphoma N Engl J Med 359 2008 613 626
10. P.J. Carter Potent antibody therapeutics by design Nat Rev Immunol 6 2006 343 357
11. R.A. Miller, D.G. Malony, and R. Warnke Treatment of B-cell lymphoma with monoclonal ant-idiotype antibody N Engl J Med 306 1982 517
12. R. Houot, and R. Levy Vaccines for lymphomas: idiotype vaccines and beyond Blood Rev 23 3 2009 137 142
13. M.S. Cragg, C.A. Walshe, and A.O. Ivanov The biology of CD20 and its potential as a target for mAb therapy Curr Dir Autoimmun 8 2005 140 174
14. M.J. Glennie, R.R. French, and M.S. Cragg Mechanisms of killing by anti-CD20 monoclonal antibodies Mol Immunol 44 16 2007 3823 3837 (Pubitemid 47332625)
15. E. Mössner, P. Brünker, and S. Moser 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 2010 4393 4402
16. R.L. Stanfield, A. Zemia, and I.A. Wilson Antibody elbow angles are influenced by their light chain class J Mol Biol 357 2006 1566 1574
17. J.C. Byrd, S. Kitada, and I.W. Flinn The mechanism of tumor cell clearance by rituximab in vivo in patients with B-cell chronic lymphocytic leukemia: evidence of caspase activation and apoptosis induction Blood 99 3 2002 1038 1043 (Pubitemid 34525569)
18. N. Di Gaetano, E. Cittera, and R. Nota Complement activation determines the therapeutic activity of rituximab in vivo J Immunol 171 3 2003 1581 1587 (Pubitemid 36900094)
19. F. Nimmerjahn, and J.V. Ravetch Divergent immunoglobulin g subclass activity through selective Fc receptor binding Science (New York, N.Y) 310 5753 2005 1510 1512 (Pubitemid 41746349)
20. R.A. Clynes, T.L. Towers, and L.G. Presta Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets Nat Med 6 4 2000 443 446 (Pubitemid 30208162)
21. J. Uchida, Y. Hamaguchi, and J.A. Oliver The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy J Exp Med 199 12 2004 1659 1669 (Pubitemid 38821999)
22. Q. Gong, Q. Ou, and S. Ye Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy J Immunol 174 2 2005 817 826 (Pubitemid 40094277)
23. S. de Haij, J.H. Jansen, and P. Boross In vivo cytotoxicity of Type I CD20 antibodies critically depends on Fc receptor ITAM signaling Cancer Res 70 8 2010 3209 3217
24. G. Cartron, L. Dacheux, and G. Salles Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene Blood 99 3 2002 754 758 (Pubitemid 34525533)
25. W.K. Weng, and R. Levy Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma J Clin Oncol 21 21 2003 3940 3947 (Pubitemid 46606207)
26. J.M. Reichert, and V.E. Valge-Archer Development trends for monoclonal antibody cancer therapeutics Nat Rev Drug Discov 6 5 2007 349 356 (Pubitemid 46696550)
27. D.R. Burton Immunoglobulin G: functional sites Mol Immunol 22 3 1985 161 206 (Pubitemid 15076803)
28. T.A. Waldmann, and W. Strober Metabolism of immunoglobulins Prog Allergy 13 1969 1 110
29. P. Bruhns, B. Iannascoli, and P. England Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses Blood 113 16 2009 3716 3725
30. M. Dechant, G. Vidarsson, and B. Stockmeyer Chimeric IgA antibodies against HLA class II effectively trigger lymphoma cell killing Blood 100 13 2002 4574 4580 (Pubitemid 35429700)
31. J.G. van de Winkel, and P.J. Capel Human IgG Fc receptor heterogeneity: molecular aspects and clinical implications Immunol Today 14 5 1993 215 221 (Pubitemid 23124515)
32. H.R. Koene, M. Kleijer, and J. Algra Fc gammaRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell Fc gammaRIIIa, independently of the Fc gammaRIIIa-48L/R/H phenotype Blood 90 3 1997 1109 1114 (Pubitemid 27314146)
33. Y.M. Lucisano Valim, and P.J. Lachmann The effect of antibody isotype and antigenic epitope density on the complement-fixing activity of immune complexes: a systematic study using chimaeric anti-NIP antibodies with human Fc regions Clin Exp Immunol 84 1 1991 1 8
34. P.J. Carter, and P.D. Senter Antibody-drug conjugates for cancer therapy Cancer J 14 3 2008 154 169
35. S.I. Park, and O.W. Press Radioimmunotherapy for treatment of B-cell lymphomas and other hematologic malignancies Curr Opin Hematol 14 6 2007 632 638 (Pubitemid 47494079)
36. N. Lonberg Human antibodies from transgenic animals Nat Biotechnol 23 9 2005 1117 1125 (Pubitemid 41486393)
37. A.M. Geurts, G.J. Cost, and Y. Freyvert Knockout rats via embryo microinjection of zinc-finger nucleases Science 325 5939 2009 433
38. T. Clackson, H.R. Hoogenboom, and A.D. Griffiths Making antibody fragments using phage display libraries Nature 352 6336 1991 624 628 (Pubitemid 21912394)
39. A. Lanzavecchia, D. Corti, and F. Sallusto Human monoclonal antibodies by immortalization of memory B cells Curr Opin Biotechnol 18 6 2007 523 528
40. M.J. Bernett, S. Karki, and G.L. Moore Engineering fully human monoclonal antibodies from murine variable regions J Mol Biol 396 5 2010 1474 1490
41. P.T. Jones, P.H. Dear, and J. Foote Replacing the complementarity- determining regions in a human antibody with those from a mouse Nature 321 6069 1986 522 525 (Pubitemid 16052256)
42. Y. Tang, J. Lou, and R.K. Alpaugh Regulation of antibody-dependent cellular cytotoxicity by IgG intrinsic and apparent affinity for target antigen J Immunol 179 5 2007 2815 2823
43. B. Li, L. Zhao, and H. Guo Characterization of a rituximab variant with potent antitumor activity against rituximab-resistant B-cell lymphoma Blood 114 24 2009 5007 5015
44. R. Jefferis, and J. Lund Interaction sites on human IgG-Fc for FcgammaR: current models Immunol Lett 82 1-2 2002 57 65 (Pubitemid 34468035)
45. P. Sondermann, R. Huber, and V. Oosthuizen The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gammaRIII complex Nature 406 6793 2000 267 273 (Pubitemid 30604397)
46. A. Wright, and S.L. Morrison Effect of glycosylation on antibody function: implications for genetic engineering Trends Biotechnol 15 1 1997 26 32 (Pubitemid 27067150)
47. R. Jefferis Glycosylation as a strategy to improve antibody-based therapeutics Nat Rev Drug Discov 8 3 2009 226 234
48. T. Shinkawa, K. Nakamura, and N. Yamane The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity J Biol Chem 278 5 2003 3466 3473 (Pubitemid 36801263)
49. P.H. van Berkel, J. Gerritsen, and E. van Voskuilen Rapid production of recombinant human IgG With improved ADCC effector function in a transient expression system Biotechnol Bioeng 105 2 2010 350 357
50. P. Umana, J. Jean-Mairet, and R. Moudry Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity Nat Biotechnol 17 2 1999 176 180 (Pubitemid 29072543)
51. J. Davies, L. Jiang, and L.Z. Pan Expression of GnTIII in a recombinant anti-CD20 CHO production cell line: expression of antibodies with altered glycoforms leads to an increase in ADCC through higher affinity for FC gamma RIII Biotechnol Bioeng 74 4 2001 288 294 (Pubitemid 32678662)
52. N. Yamane-Ohnuki, S. Kinoshita, and M. Inoue-Urakubo Establishment of FUT8 knockout Chinese hamster ovary cells: an ideal host cell line for producing completely defucosylated antibodies with enhanced antibody-dependent cellular cytotoxicity Biotechnol Bioeng 87 5 2004 614 622 (Pubitemid 39295406)
53. R.L. Shields, J. Lai, and R. Keck Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity J Biol Chem 277 30 2002 26733 26740 (Pubitemid 34951677)
54. C. Ferrara, F. Stuart, and P. Sondermann The carbohydrate at Fcgamma RIIIa ASN162: an element required for high affinity binding to non-fucosylated lgG glycoforms J Biol Chem 281 8 2005 5032 5036 (Pubitemid 43847767)
55. R. Niwa, S. Hatanaka, and E. Shoji-Hosaka Enhancement of the antibody-dependent cellular cytotoxicity of low-fucose IgG1 Is independent of FcgammaRIIIa functional polymorphism Clin Cancer Res 10 18 Pt 1 2004 6248 6255 (Pubitemid 39287533)
56. M. Shibata-Koyama, S. Iida, and H. Misaka Nonfucosylated rituximab potentiates human neutrophil phagocytosis through its high binding for FcgammaRIIIb and MHC class II expression on the phagocytotic neutrophils Exp Hematol 37 3 2009 309 321
57. M. Peipp, J.J. Lammerts van Bueren, and T. Schneider-Merck Antibody fucosylation differentially impacts cytotoxicity mediated by NK and PMN effector cells Blood 112 6 2008 2390 2399
58. R.L. Shields, A.K. Namenuk, and K. Hong High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R J Biol Chem 276 9 2001 6591 6604
59. G.A. Lazar, W. Dang, and S. Karki Engineered antibody Fc variants with enhanced effector function Proc Natl Acad Sci U S A 103 11 2006 4005 4010
60. J.B. Stavenhagen, S. Gorlatov, and N. Tuaillon Fc optimization of therapeutic antibodies enhances their ability to kill tumor cells in vitro and controls tumor expansion in vivo via low-affinity activating Fcgamma receptors Cancer Res 67 18 2007 8882 8890 (Pubitemid 47437465)
61. H.M. Horton, M.J. Bernett, and E. Pong Potent in vitro and in vivo activity of an Fc-engineered anti-CD19 monoclonal antibody against lymphoma and leukemia Cancer Res 68 19 2008 8049 8057
62. J. Zalevsky, I.W. Leung, and S. Karki The impact of Fc engineering on an anti-CD19 antibody: increased Fcgamma receptor affinity enhances B-cell clearing in nonhuman primates Blood 113 16 2009 3735 3743
63. S.Y. Wang, S. Veeramani, and E. Racila 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 114 26 2009 5322 5330
64. E.E. Idusogie, L.G. Presta, and H. Gazzano-Santoro Mapping of the C1q binding site on rituxan, a chimeric antibody with a human IgG1 Fc J Immunol 164 8 2000 4178 4184 (Pubitemid 30215076)
65. E.E. Idusogie, P.Y. Wong, and L.G. Presta Engineered antibodies with increased activity to recruit complement J Immunol 166 4 2001 2571 2575 (Pubitemid 32173494)
66. G.L. Moore, H. Chen, and S. Karki Engineered Fc variant antibodies with enhanced ability to recruit complement and mediate effector functions MAbs 2 2 2010
67. N.L. Berinstein, A.J. Grillo-Lopez, and C.A. White Association of serum Rituximab (IDEC-C2B8) concentration and anti-tumor response in the treatment of recurrent low-grade or follicular non-Hodgkin's lymphoma Ann Oncol 9 9 1998 995 1001 (Pubitemid 28496709)
68. J.J. Lammerts van Bueren, W.K. Bleeker, and H.O. Bøgh The impact of target dynamics on the dose-effect relationship of a therapeutic antibody against epidermal growth factor receptor Cancer Res 66 15 2006 7630 7638 (Pubitemid 44289220)
69. L.B. Shih, H.H. Lu, and H. Xuan Internalization and intracellular processing of an anti-B-cell lymphoma monoclonal antibody, LL2 Int J Cancer 56 4 1994 538 545 (Pubitemid 24094405)
70. W.P. Burmeister, A.H. Huber, and P.J. Bjorkman Crystal structure of the complex of rat neonatal Fc receptor with Fc Nature 372 6504 1994 379 383 (Pubitemid 24363442)
71. V. Oganesyan, M.M. Damschroder, and R.M. Woods Structural characterization of a human Fc fragment engineered for extended serum half-life Mol Immunol 46 8-9 2009 1750 1755
72. J. Zalevsky, A.K. Chamberlain, and H.M. Horton Enhanced antibody half-life improves in vivo activity Nat Biotechnol 28 2 2010 157 159
73. A.F. Gerritsen, M. Bosch, and M. de Weers High throughput screening for antibody induced complement-dependent cytotoxicity in early antibody discovery using homogeneous macroconfocal fluorescence imaging J Immunol Methods 352 1-2 2010 140 146
74. J.L. Teeling, R.R. French, and M.S. Cragg Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin lymphomas Blood 104 6 2004 1793 1800 (Pubitemid 39202289)
75. M. Peipp, T. Schneider-Merck, and M. Dechant Tumor cell killing mechanisms of epidermal growth factor receptor (EGFR) antibodies are not affected by lung cancer-associated EGFR kinase mutations J Immunol 180 6 2008 4338 4345
76. F. Nimmerjahn, and J.V. Ravetch Fcgamma receptors: old friends and new family members Immunity 24 1 2006 19 28 (Pubitemid 43077197)
77. B. Schraven, and U. Kalinke CD28 superagonists: what makes the difference in humans? Immunity 28 5 2008 591 595 (Pubitemid 351636245)
78. A. Quintas-Cardama, W. Wierda, and S. O'Brien Investigational immunotherapeutics for B-cell malignancies J Clin Oncol 28 5 2010 884 892
79. C. de Romeuf, C.A. Dutertre, and M. Le Garff-Tavernier Chronic lymphocytic leukaemia cells are efficiently killed by an anti-CD20 monoclonal antibody selected for improved engagement of FcgammaRIIIA/CD16 Br J Haematol 140 6 2008 635 643 (Pubitemid 351300917)
80. L.G. Presta Molecular engineering and design of therapeutic antibodies Curr Opin Immunol 20 4 2008 460 470
81. M.R. Clark IgG effector mechanisms Chem Immunol 65 1997 88 110 (Pubitemid 27029828)
82. J.A. Bowles, S.Y. Wang, and B.K. Link Anti-CD20 monoclonal antibody with enhanced affinity for CD16 activates NK cells at lower concentrations and more effectively than rituximab Blood 108 8 2006 2648 2654
83. A. Natsume, M. In, and H. Takamura Engineered antibodies of IgG1/IgG3 mixed isotype with enhanced cytotoxic activities Cancer Res 68 10 2008 3863 3872
84. W.F. Dall'Acqua, P.A. Kiener, and H. Wu Properties of human IgG1s engineered for enhanced binding to the neonatal Fc receptor (FcRn) J Biol Chem 281 33 2006 23514 23524 (Pubitemid 44274126)
85. W.F. Dall'Acqua, R.M. Woods, and E.S. Ward Increasing the affinity of a human IgG1 for the neonatal Fc receptor: biological consequences J Immunol 169 9 2002 5171 5180 (Pubitemid 35217187)
86. A. Datta-Mannan, D.R. Witcher, and Y. Tang Humanized IgG1 variants with differential binding properties to the neonatal Fc receptor: relationship to pharmacokinetics in mice and primates Drug Metab Dispos 35 1 2007 86 94 (Pubitemid 46036480)
87. A. Datta-Mannan, D.R. Witcher, and Y. Tang Monoclonal antibody clearance. Impact of modulating the interaction of IgG with the neonatal Fc receptor J Biol Chem 282 3 2007 1709 1717 (Pubitemid 47076691)
88. P.R. Hinton, J.M. Xiong, and M.G. Johlfs An engineered human IgG1 antibody with longer serum half-life J Immunol 176 1 2006 346 356 (Pubitemid 43023280)
89. Y.A. Yeung, M.K. Leabman, and J.S. Marvin Engineering human IgG1 affinity to human neonatal Fc receptor: impact of affinity improvement on pharmacokinetics in primates J Immunol 182 12 2009 7663 7671
90. Y.A. Yeung, X. Wu, and A.E. Reyes 2nd A therapeutic anti-VEGF antibody with increased potency independent of pharmacokinetic half-life Cancer Res 70 8 2010 3269 3277
91. S.B. Petkova, S. Akilesh, and T.J. Sproule Enhanced half-life of genetically engineered human IgG1 antibodies in a humanized FcRn mouse model: potential application in humorally mediated autoimmune disease Int Immunol 18 12 2006 1759 1769 (Pubitemid 44884038)