Influence of immunoglobulin isotype on therapeutic antibody function

Blood

Volumn 127, Issue 9, 2016, Pages 1097-1101

  Beers, Stephen A ^a   Glennie, Martin J ^a   White, Ann L ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; FC RECEPTOR; FC RECEPTOR IIB; IMMUNOGLOBULIN CLASS; MONOCLONAL ANTIBODY; IMMUNOLOGIC FACTOR; VACCINE;

ANTIBODY STRUCTURE; CANCER THERAPY; DRUG ACTIVITY; DRUG EFFECT; DRUG MECHANISM; DRUG RECEPTOR BINDING; DRUG TARGETING; HUMAN; IMMUNOMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; BIOLOGICAL MODEL; IMMUNOLOGY; METABOLISM;

ANTIBODIES, MONOCLONAL; HUMANS; IMMUNOGLOBULIN ISOTYPES; IMMUNOLOGIC FACTORS; MODELS, BIOLOGICAL; RECEPTORS, IGG; VACCINES;

EID: 84960414647     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-09-625343     Document Type: Review

References (76)

1. Sliwkowski MX, Mellman I. Antibody therapeutics in cancer. Science. 2013;341(6151):1192-1198.
2. Postow MA, Callahan MK, Wolchok JD. Immune Checkpoint Blockade in Cancer Therapy. J Clin Oncol. 2015;33(17):1974-1982.
3. Herlyn D, Koprowski H. IgG2a monoclonal antibodies inhibit human tumor growth through interaction with effector cells. Proc Natl Acad Sci USA. 1982;79(15):4761-4765.
4. Isaacs JD, Greenwood J, Waldmann H. Therapy with monoclonal antibodies. II. The contribution of Fc gamma receptor binding and the influence of C (H) 1 and C (H) 3 domains on in vivo effector function. J Immunol. 1998;161(8):3862-3869.
5. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med. 2000;6(4):443-446.
6. Nimmerjahn F, Bruhns P, Horiuchi K, Ravetch JV. FcgammaRIV: a novel FcR with distinct IgG subclass specificity. Immunity. 2005;23(1):41-51.
7. Uchida J, Hamaguchi Y, Oliver JA, et al. The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med. 2004;199(12):1659-1669.
8. Nimmerjahn F, Ravetch JV. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science. 2005;310(5753):1510-1512.
9. Minard-Colin V, Xiu Y, Poe JC, et al. Lymphoma depletion during CD20 immunotherapy in mice is mediated by macrophage FcgammaRI, FcgammaRIII, and FcgammaRIV. Blood. 2008;112(4):1205-1213.
10. 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.
11. Butchar JP, Mehta P, Justiniano SE, et al. Reciprocal regulation of activating and inhibitory Fcgamma receptors by TLR7/8 activation: implications for tumor immunotherapy. Clin Cancer Res. 2010;16(7):2065-2075.
12. Shi Y, Fan X, Deng H, et al. Trastuzumab triggers phagocytic killing of high HER2 cancer cells in vitro and in vivo by interaction with Fcg receptors on macrophages. J Immunol. 2015;194(9):4379-4386.
13. Biburger M, Aschermann S, Schwab I, et al. Monocyte subsets responsible for immunoglobulin G-dependent effector functions in vivo. Immunity. 2011;35(6):932-944.
14. Schwab I, Lux A, Nimmerjahn F. Pathways Responsible for Human Autoantibody and Therapeutic Intravenous IgG Activity in Humanized Mice. Cell Reports. 2015;13(3):610-620.
15. Gong Q, Ou Q, Ye S, et al. Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J Immunol. 2005;174(2):817-826.
16. Montalvao F, Garcia Z, Celli S, et al. The mechanism of anti-CD20-mediated B cell depletion revealed by intravital imaging. J Clin Invest. 2013;123(12):5098-5103.
17. Gül N, Babes L, Siegmund K, et al. Macrophages eliminate circulating tumor cells after monoclonal antibody therapy. J Clin Invest. 2014;124(2):812-823.
18. Tipton TR, Roghanian A, Oldham RJ, et al. Antigenic modulation limits the effector cell mechanisms employed by type I anti-CD20 monoclonal antibodies. Blood. 2015;125(12):1901-1909.
19. Kohrt HE, Houot R, Goldstein MJ, et al. CD137 stimulation enhances the antilymphoma activity of anti-CD20 antibodies. Blood. 2011;117(8):2423-2432.
20. Albanesi M, Mancardi DA, Jönsson F, et al. Neutrophils mediate antibody-induced antitumor effects in mice. Blood. 2013;122(18):3160-3164.
21. Hernandez-Ilizaliturri FJ, Jupudy V, Ostberg J, et al. Neutrophils contribute to the biological antitumor activity of rituximab in a non-Hodgkin's lymphoma severe combined immunodeficiency mouse model. Clin Cancer Res. 2003;9(16 Pt 1):5866-5873.
22. Golay J, Manganini M, Facchinetti V, et al. Rituximab-mediated antibody-dependent cellular cytotoxicity against neoplastic B cells is stimulated strongly by interleukin-2. Haematologica. 2003;88(9):1002-1012.
23. Cartron G, Dacheux L, Salles G, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood. 2002;99(3):754-758.
24. Dahal LN, Roghanian A, Beers SA, Cragg MS. FcgR requirements leading to successful immunotherapy. Immunol Rev. 2015;268(1):104-122.
25. Hargreaves CE, Rose-Zerilli MJJ, Machado LR, et al. Fcg receptors: genetic variation, function, and disease. Immunol Rev. 2015;268(1):6-24.
26. Redman JM, Hill EM, AlDeghaither D, Weiner LM. Mechanisms of action of therapeutic antibodies for cancer. Mol Immunol. 2015;67(2 Pt A):28-45.
27. Umana P, Moessner E, Bruenker P, et al. Novel 3rd generation humanized type II CD20 antibody with glycoengineered Fc and modified elbow hinge for enhanced ADCC and superior apoptosis induction. ASH Annu Mtg Abstr. 2006;108(11):229.
28. Herter S, Birk MC, Klein C, Gerdes C, Umana P, Bacac M. Glycoengineering of therapeutic antibodies enhances monocyte/macrophagemediated phagocytosis and cytotoxicity. J Immunol. 2014;192(5):2252-2260.
29. Mössner E, Brünker P, Moser S, et al. Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cellmediated B-cell cytotoxicity. Blood. 2010;115(22):4393-4402.
30. Goede V, Fischer K, Engelke A, et al. Obinutuzumab as frontline treatment of chronic lymphocytic leukemia: updated results of the CLL11 study. Leukemia. 2015;29(7):1602-1604.
31. Presta LG, Shields RL, Namenuk AK, Hong K, Meng YG. Engineering therapeutic antibodies for improved function. Biochem Soc Trans. 2002;30(4):487-490.
32. Shields RL, Lai J, Keck R, et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibodydependent cellular toxicity. J Biol Chem. 2002;277(30):26733-26740.
33. Shields RL, Namenuk AK, Hong K, et al. 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. 2001;276(9):6591-6604.
34. 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.
35. Kinder M, Greenplate AR, Strohl WR, Jordan RE, Brezski RJ. An Fc engineering approach that modulates antibody-dependent cytokine release without altering cell-killing functions. MAbs. 2015;7(3):494-504.
36. Boross P, Lohse S, Nederend M, et al. IgA EGFR antibodies mediate tumour killing in vivo. EMBO Mol Med. 2013;5(8):1213-1226.
37. Josephs DH, Spicer JF, Karagiannis P, Gould HJ, Karagiannis SN. IgE immunotherapy: a novel concept with promise for the treatment of cancer. MAbs. 2014;6(1):54-72.
38. Bulliard Y, Jolicoeur R, Windman M, et al. Activating Fc g receptors contribute to the antitumor activities of immunoregulatory receptortargeting antibodies. J Exp Med. 2013;210(9):1685-1693.
39. Bulliard Y, Jolicoeur R, Zhang J, Dranoff G, Wilson NS, Brogdon JL. OX40 engagement depletes intratumoral Tregs via activating FcgRs, leading to antitumor efficacy. Immunol Cell Biol. 2014;92(6):475-480.
40. Selby MJ, Engelhardt JJ, Quigley M, et al. Anti-CTLA-4 antibodies of IgG2a isotype enhance antitumor activity through reduction of intratumoral regulatory T cells. Cancer Immunol Res. 2013;1(1):32-42.
41. Simpson TR, Li F, Montalvo-Ortiz W, et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J Exp Med. 2013;210(9):1695-1710.
42. Dahan R, Sega E, Engelhardt J, Selby M, Korman AJ, Ravetch JV. FcgRs Modulate the Anti-tumor Activity of Antibodies Targeting the PD-1/PD-L1 Axis. Cancer Cell. 2015;28(3):285-295.
43. Romano E, Kusio-Kobialka M, Foukas PG, et al. Ipilimumab-dependent cell-mediated cytotoxicity of regulatory T cells ex vivo by nonclassical monocytes in melanoma patients. Proc Natl Acad Sci USA. 2015;112(19):6140-6145.
44. Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N Engl J Med. 2015;373(1):23-34.
45. Bruhns P, Iannascoli B, England P, et al. Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood. 2009;113(16):3716-3725.
46. Lux A, Yu X, Scanlan CN, Nimmerjahn F. Impact of immune complex size and glycosylation on IgG binding to human FcgRs. J Immunol. 2013;190(8):4315-4323.
47. Hussain K, Hargreaves CE, Roghanian A, et al. Upregulation of FcgRIIb on monocytes is necessary to promote the superagonist activity of TGN1412. Blood. 2015;125(1):102-110.
48. Michaud HA, Gomard T, Gros L, et al. A crucial role for infected-cell/antibody immune complexes in the enhancement of endogenous antiviral immunity by short passive immunotherapy. PLoS Pathog. 2010;6(6):e1000948.
49. Abès R, Gélizé E, Fridman WH, Teillaud JL. Longlasting antitumor protection by anti-CD20 antibody through cellular immune response. Blood. 2010;116(6):926-934.
50. DiLillo DJ, Ravetch JV. Differential Fc-Receptor Engagement Drives an Anti-tumor Vaccinal Effect. Cell. 2015;161(5):1035-1045.
51. 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.
52. Roghanian A, Teige I, Mårtensson L, et al. Antagonistic human FcgRIIB (CD32B) antibodies have anti-tumor activity and overcome resistance to antibody therapy in vivo. Cancer Cell. 2015;27(4):473-488.
53. Vaughan AT, Iriyama C, Beers SA, et al. Inhibitory FcgRIIb (CD32b) becomes activated by therapeutic mAb in both cis and trans and drives internalization according to antibody specificity. Blood. 2014;123(5):669-677.
54. Croft M, Benedict CA, Ware CF. Clinical targeting of the TNF and TNFR superfamilies. Nat Rev Drug Discov. 2013;12(2):147-168.
55. Li F, Ravetch JV. Inhibitory Fcg receptor engagement drives adjuvant and anti-tumor activities of agonistic CD40 antibodies. Science. 2011;333(6045):1030-1034.
56. White AL, Beers SA, Cragg MS. FcgRIIB as a key determinant of agonistic antibody efficacy. Curr Top Microbiol Immunol. 2014;382:355-372.
57. White AL, Chan HT, Roghanian A, et al. Interaction with FcgRIIB is critical for the agonistic activity of anti-CD40 monoclonal antibody. J Immunol. 2011;187(4):1754-1763.
58. Wilson NS, Yang B, Yang A, et al. An Fcg receptor-dependent mechanism drives antibodymediated target-receptor signaling in cancer cells. Cancer Cell. 2011;19(1):101-113.
59. Xu Y, Szalai AJ, Zhou T, et al. Fc gamma Rs modulate cytotoxicity of anti-Fas antibodies: implications for agonistic antibody-based therapeutics. J Immunol. 2003;171(2):562-568.
60. White AL, Chan HT, French RR, et al. Conformation of the human immunoglobulin G2 hinge imparts superagonistic properties to immunostimulatory anticancer antibodies. Cancer Cell. 2015;27(1):138-148.
61. Li F, Ravetch JV. Antitumor activities of agonistic anti-TNFR antibodies require differential FcgRIIB coengagement in vivo. Proc Natl Acad Sci USA. 2013;110(48):19501-19506.
62. White AL, Chan HT, French RR, et al. FcγR||B controls the potency of agonistic anti-TNFR mAbs. Cancer Immunol Immunother. 2013;62(5):941-948.
63. White AL, Dou L, Chan HT, et al. Fcg receptor dependency of agonistic CD40 antibody in lymphoma therapy can be overcome through antibody multimerization. J Immunol. 2014;193(4):1828-1835.
64. Li F, Ravetch JV. Apoptotic and antitumor activity of death receptor antibodies require inhibitory Fcg receptor engagement. Proc Natl Acad Sci USA. 2012;109(27):10966-10971.
65. Smith P, DiLillo DJ, Bournazos S, Li F, Ravetch JV. Mouse model recapitulating human Fcg receptor structural and functional diversity. Proc Natl Acad Sci USA. 2012;109(16):6181-6186.
66. Johnson P, Challis R, Chowdhury F, et al. Clinical and biological effects of an agonist anti-CD40 antibody: a Cancer Research UK phase I study. Clin Cancer Res. 2015;21(6):1321-1328.
67. Richman LP, Vonderheide RH. Role of crosslinking for agonistic CD40 monoclonal antibodies as immune therapy of cancer. Cancer Immunol Res. 2014;2(1):19-26.
68. Dillon TM, Ricci MS, Vezina C, et al. Structural and functional characterization of disulfide isoforms of the human IgG2 subclass. J Biol Chem. 2008;283(23):16206-16215.
69. Martinez T, Guo A, Allen MJ, et al. Disulfide connectivity of human immunoglobulin G2 structural isoforms. Biochemistry. 2008;47(28):7496-7508.
70. Wypych J, Li M, Guo A, et al. Human IgG2 antibodies display disulfide-mediated structural isoforms. J Biol Chem. 2008;283(23):16194-16205.
71. Allen MJ, Guo A, Martinez T, et al. Interchain disulfide bonding in human IgG2 antibodies probed by site-directed mutagenesis. Biochemistry. 2009;48(17):3755-3766.
72. Chan FK, Chun HJ, Zheng L, Siegel RM, Bui KL, Lenardo MJ. A domain in TNF receptors that mediates ligand-independent receptor assembly and signaling. Science. 2000;288(5475):2351-2354.
73. Smulski CR, Beyrath J, Decossas M, et al. Cysteine-rich domain 1 of CD40 mediates receptor self-assembly. J Biol Chem. 2013;288(15):10914-10922.
74. Remer M, White A, Glennie M, Al-Shamkhani A, Johnson P. The use of anti-CD40 mAb in cancer [published online ahead of print February 5, 2015]. Curr Top Microbiol Immunol. doi:10.1007/83-2014-427.
75. Pedersen IM, Buhl AM, Klausen P, Geisler CH, Jurlander J. The chimeric anti-CD20 antibody rituximab induces apoptosis in B-cell chronic lymphocytic leukemia cells through a p38 mitogen activated protein-kinase-dependent mechanism. Blood. 2002;99(4):1314-1319.
76. Yakes FM, Chinratanalab W, Ritter CA, King W, Seelig S, Arteaga CL. Herceptin-induced inhibition of phosphatidylinositol-3 kinase and Akt Is required for antibody-mediated effects on p27, cyclin D1, and antitumor action. Cancer Res. 2002;62(14):4132-4141.