Role of Fc-FcγR interactions in the antitumor activity of therapeutic antibodies

Immunology and Cell Biology

Volumn 95, Issue 4, 2017, Pages 340-346

  Barnhart, Bryan C ^a   Quigley, Michael ^b  

^a Bristol Myers Squibb   (United States)

^b BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER ANTIBODY; CD20 ANTIBODY; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; FC RECEPTOR; GILVETMAB; IMMUNOGLOBULIN G2A; IPILIMUMAB; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OCARATUZUMAB; PROGRAMMED DEATH 1 LIGAND 1; RITUXIMAB; TRASTUZUMAB; MONOCLONAL ANTIBODY; PROTEIN BINDING;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY STRUCTURE; ANTIGEN BINDING; ANTIGEN PRESENTATION; ANTINEOPLASTIC ACTIVITY; CELL MATURATION; HUMAN; IMMUNORECEPTOR TYROSINE BASED INHIBITION MOTIF; MACROPHAGE; MONOCYTE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW; ANIMAL; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; NEOPLASM; PROCEDURES; PROTEIN ENGINEERING; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL; HUMANS; IMMUNOTHERAPY; NEOPLASMS; PROTEIN BINDING; PROTEIN ENGINEERING; RECEPTORS, FC; RECEPTORS, IGG; SIGNAL TRANSDUCTION;

EID: 85008331099     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2016.121     Document Type: Review

References (56)

1. Weiner GJ. Building better monoclonal antibody-based therapeutics. Nat Rev Cancer 2015; 15: 361-370.
2. Pincetic A, Bournazos S, DiLillo DJ, Maamary J, Wang TT, Dahan R, et al. Type I and type II Fc receptors regulate innate and adaptive immunity. Nat Immunol 2014; 15: 707-716.
3. DiLillo DJ, Ravetch JV. Fc-receptor interactions regulate both cytotoxic and immunomodulatory therapeutic antibody effector functions. Cancer Immunol Res 2015; 3: 704-713.
4. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med 2000; 6: 443-446.
5. Boruchov AM, Heller G, Veri MC, Bonvini E, Ravetch JV, Young JW. Activating and inhibitory IgG Fc receptors on human DCs mediate opposing functions. J Clin Invest 2005; 115: 2914-2923.
6. Bruhns P, Jonsson F. Mouse and human Fc?R effector functions. Immunol Rev 2015; 268: 25-51.
7. Lux A, Yu X, Scanlan CN, Nimmerjahn F. Impact of immune complex size and glycosylation on IgG binding to human FcgammaRs. J Immunol 2013; 190: 4315-4323.
8. DiLillo DJ, Tan GS, Palese P, Ravetch JV. Broadly neutralizing hemagglutinin stalkspecific antibodies require FcgammaR interactions for protection against influenza virus in vivo. Nat Med 2014; 20: 143-151.
9. Bournazos S, DiLillo DJ, Ravetch JV. humanized mice to study FcgammaR function. Curr Top Microbiol Immunol 2014; 382: 237-248.
10. Clynes R, Takechi Y, Moroi Y, Houghton A, Ravetch JV. Fc receptors are required in passive and active immunity to melanoma. Proc Natl Acad Sci USA 1998; 95: 652-656.
11. Lopez-Albaitero A, Lee SC, Morgan S, Grandis JR, Gooding WE, Ferrone S, et al. Role of polymorphic Fc gamma receptor IIIa and EGFR expression level in cetuximab mediated, NK cell dependent in vitro cytotoxicity of head and neck squamous cell carcinoma cells. Cancer Immunol Immunother 2009; 58: 1853-1864.
12. Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 2002; 99: 754-758.
13. Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G, et al. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J Clin Oncol 2008; 26: 1789-1796.
14. Bibeau F, Lopez-Crapez E, Di Fiore F, Thezenas S, Ychou M, Blanchard F, et al. Impact of Fc{gamma}RIIa-Fc{gamma}RIIIa polymorphisms and KRAS mutations on the clinical outcome of patients with metastatic colorectal cancer treated with cetuximab plus irinotecan. J Clin Oncol 2009; 27: 1122-1129.
15. Forero-Torres A, de Vos S, Pohlman BL, Pashkevich M, Cronier DM, Dang NH, et al. Results of a phase 1 study of AME-133v (LY2469298), an Fc-engineered humanized monoclonal anti-CD20 antibody, in FcgammaRIIIa-genotyped patients with previously treated follicular lymphoma. Clin Cancer Res 2012; 18: 1395-1403.
16. Klein C, Lammens A, Schafer W, Georges G, Schwaiger M, Mossner E, et al. Epitope interactions of monoclonal antibodies targeting CD20 and their relationship to functional properties. MAbs 2013; 5: 22-33.
17. Cheney CM, Stephens DM, Mo X, Rafiq S, Butchar J, Flynn JM, et al. Ocaratuzumab, an Fc-engineered antibody demonstrates enhanced antibody-dependent cell-mediated cytotoxicity in chronic lymphocytic leukemia. MAbs 2014; 6: 749-755.
18. Tobinai K, Ogura M, Kobayashi Y, Uchida T, Watanabe T, Oyama T, et al. Phase I study of LY2469298, an Fc-engineered humanized anti-CD20 antibody, in patients with relapsed or refractory follicular lymphoma. Cancer Sci 2011; 102: 432-438.
19. Yamane-Ohnuki N, Satoh M. Production of therapeutic antibodies with controlled fucosylation. MAbs 2009; 1: 230-236.
20. Goede V, Fischer K, Busch R, Engelke A, Eichhorst B, Wendtner CM, et al. Obinutuzumab plus chlorambucil in patients with CLL and coexisting conditions. N Engl J Med 2014; 370: 1101-1110.
21. Salles G, Morschhauser F, Lamy T, Milpied N, Thieblemont C, Tilly H, et al. Phase 1 study results of the type II glycoengineered humanized anti-CD20 monoclonal antibody obinutuzumab (GA101) in B-cell lymphoma patients. Blood 2012; 119: 5126-5132.
22. DiLillo DJ, Ravetch JV. Differential Fc-receptor engagement drives an anti-Tumor vaccinal effect. Cell 2015; 161: 1035-1045.
23. Uchida J, Hamaguchi Y, Oliver JA, Ravetch JV, Poe JC, Haas KM, et al. The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptordependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med 2004; 199: 1659-1669.
24. Schneider-Merck T, Lammerts van Bueren JJ, Berger S, Rossen K, van Berkel PH, Derer S, et al. Human IgG2 antibodies against epidermal growth factor receptor effectively trigger antibody-dependent cellular cytotoxicity but, in contrast to IgG1, only by cells of myeloid lineage. J Immunol 2010; 184: 512-520.
25. Banerjee D, Matthews P, Matayeva E, Kaufman JL, Steinman RM, Dhodapkar KM. Enhanced T-cell responses to glioma cells coated with the anti-EGF receptor antibody and targeted to activating FcgammaRs on human dendritic cells. J Immunother 2008; 31: 113-120.
26. Dhodapkar KM, Krasovsky J, Williamson B, Dhodapkar MV. Antitumor monoclonal antibodies enhance cross-presentation of cellular antigens and the generation of myeloma-specific killer T cells by dendritic cells. J Exp Med 2002; 195: 125-133.
27. Machy P, Serre K, Leserman L. Class I-restricted presentation of exogenous antigen acquired by Fcgamma receptor-mediated endocytosis is regulated in dendritic cells. Eur J Immunol 2000; 30: 848-857.
28. Rafiq K, Bergtold A, Clynes R. Immune complex-mediated antigen presentation induces tumor immunity. J Clin Invest 2002; 110: 71-79.
29. Regnault A, Lankar D, Lacabanne V, Rodriguez A, Thery C, Rescigno M, et al. Fcgamma receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J Exp Med 1999; 189: 371-380.
30. Dhodapkar KM, Kaufman JL, Ehlers M, Banerjee DK, Bonvini E, Koenig S, et al. Selective blockade of inhibitory Fcgamma receptor enables human dendritic cell maturation with IL-12p70 production and immunity to antibody-coated tumor cells. Proc Natl Acad Sci USA 2005; 102: 2910-2915.
31. Melero I, Berman DM, Aznar MA, Korman AJ, Perez Gracia JL, Haanen J. Evolving synergistic combinations of targeted immunotherapies to combat cancer. Nat Rev Cancer 2015; 15: 457-472.
32. McDermott DF, Sosman JA, Sznol M, Massard C, Gordon MS, Hamid O, et al. Atezolizumab, an anti-programmed death-ligand 1 antibody, in metastatic renal cell carcinoma: long-Term safety, clinical activity, and immune correlates from a phase IA study. J Clin Oncol 2016; 34: 833-842.
33. Dahan R, Sega E, Engelhardt J, Selby M, Korman AJ, Ravetch JV. FcgammaRs modulate the anti-Tumor activity of antibodies targeting the PD-1/PD-L1 axis. Cancer Cell 2015; 28: 285-295.
34. Scognamiglio G, De Chiara A, Di Bonito M, Tatangelo F, Losito NS, Anniciello A, et al. Variability in immunohistochemical detection of programmed death ligand 1 (PD-L1) in cancer tissue types. Int J Mol Sci 2016; 17: 5.
35. Taube JM, Klein A, Brahmer JR, Xu H, Pan X, Kim JH, et al. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res 2014; 20: 5064-5074.
36. Kaufman HL, Russell J, Hamid O, Bhatia S, Terheyden P, D'Angelo SP, et al. Avelumab in patients with chemotherapy-refractory metastatic Merkel cell carcinoma: a multicentre, single-group, open-label, phase 2 trial. Lancet Oncol 2016; 17: 1374-1385.
37. Walker LS, Sansom DM. The emerging role of CTLA4 as a cell-extrinsic regulator of T cell responses. Nat Rev Immunol 2011; 11: 852-863.
38. Bulliard Y, Jolicoeur R, Windman M, Rue SM, Ettenberg S, Knee DA, et al. Activating Fc gamma receptors contribute to the antitumor activities of immunoregulatory receptortargeting antibodies. J Exp Med 2013; 210: 1685-1693.
39. Selby MJ, Engelhardt JJ, Quigley M, Henning KA, Chen T, Srinivasan 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: 32-42.
40. Simpson TR, Li F, Montalvo-Ortiz W, Sepulveda MA, Bergerhoff K, Arce F, 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: 1695-1710.
41. Bulliard Y, Jolicoeur R, Zhang J, Dranoff G, Wilson NS, Brogdon JL. OX40 engagement depletes intratumoral Tregs via activating FcgammaRs, leading to antitumor efficacy. Immunol Cell Biol 2014; 92: 475-480.
42. Mahoney KM, Rennert PD, Freeman GJ. Combination cancer immunotherapy and new immunomodulatory targets. Nat Rev Drug Discov 2015; 14: 561-584.
43. Li F, Ravetch JV. Inhibitory Fcgamma receptor engagement drives adjuvant and anti-Tumor activities of agonistic CD40 antibodies. Science 2011; 333: 1030-1034.
44. White AL, Chan HT, Roghanian A, French RR, Mockridge CI, Tutt AL, et al. Interaction with FcgammaRIIB is critical for the agonistic activity of anti-CD40 monoclonal antibody. J Immunol 2011; 187: 1754-1763.
45. Li F, Ravetch JV. Antitumor activities of agonistic anti-TNFR antibodies require differential FcgammaRIIB coengagement in vivo. Proc Natl Acad Sci USA 2013; 110: 19501-19506.
46. Xu Y, Szalai AJ, Zhou T, Zinn KR, Chaudhuri TR, Li X, et al. Fc gamma Rs modulate cytotoxicity of anti-Fas antibodies: implications for agonistic antibody-based therapeutics. J Immunol 2003; 171: 562-568.
47. Chuntharapai A, Dodge K, Grimmer K, Schroeder K, Marsters SA, Koeppen H, et al. Isotype-dependent inhibition of tumor growth in vivo by monoclonal antibodies to death receptor 4. J Immunol 2001; 166: 4891-4898.
48. Chu SY, Vostiar I, Karki S, Moore GL, Lazar GA, Pong E, et al. Inhibition of B cell receptor-mediated activation of primary human B cells by coengagement of CD19 and FcgammaRIIb with Fc-engineered antibodies. Mol Immunol 2008; 45: 3926-3933.
49. Li F, Ravetch JV. Apoptotic and antitumor activity of death receptor antibodies require inhibitory Fcgamma receptor engagement. Proc Natl Acad Sci USA 2012; 109: 10966-10971.
50. Mimoto F, Katada H, Kadono S, Igawa T, Kuramochi T, Muraoka M, et al. Engineered antibody Fc variant with selectively enhanced FcgammaRIIb binding over both FcgammaRIIa(R131) and FcgammaRIIa(H131). Protein Eng Des Sel 2013; 26: 589-598.
51. Wilson NS, Yang B, Yang A, Loeser S, Marsters S, Lawrence D, et al. An Fcgamma receptor-dependent mechanism drives antibody-mediated target-receptor signaling in cancer cells. Cancer Cell 2011; 19: 101-113.
52. Dahan R, Barnhart BC, Li F, Yamniuk AP, Korman AJ, Ravetch JV. Therapeutic activity of agonistic, human anti-CD40 monoclonal antibodies requires selective FcgammaR engagement. Cancer Cell 2016; 29: 820-831.
53. Bruhns P, Teillaud JL. Inhibitory IgG receptor-expressing cells: the must-have accessory for anti-CD40 immunomodulatory mAb efficacy. Cancer Cell 2016; 29: 771-773.
54. Young A, Ngiow SF, Barkauskas DS, Sult E, Hay C, Blake SJ, et al. Co-inhibition of CD73 and A2AR adenosine signaling improves anti-Tumor immune responses. Cancer Cell 2016; 30: 391-403.
55. Smith P, DiLillo DJ, Bournazos S, Li F, Ravetch JV. Mouse model recapitulating human Fcgamma receptor structural and functional diversity. Proc Natl Acad Sci USA 2012; 109: 6181-6186.
56. Guilliams M, Bruhns P, Saeys Y, Hammad H, Lambrecht BN. The function of Fc [gamma] receptors in dendritic cells and macrophages. Nat Rev Immunol 2014; 14: 94-108.