Antibodies, Fc receptors and cancer

Current Opinion in Immunology

Volumn 19, Issue 2, 2007, Pages 239-245

  Nimmerjahn, Falk ^a,b   Ravetch, Jeffrey V ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; MONOCLONAL ANTIBODY;

ANTIBODY AFFINITY; B CELL LYMPHOMA; CANCER IMMUNOTHERAPY; INNATE IMMUNITY; REVIEW; TUMOR IMMUNITY;

ANIMALS; ANTIBODIES; HUMANS; IMMUNOGLOBULIN ISOTYPES; MICE; NEOPLASMS; RECEPTORS, FC;

EID: 33847652822     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2007.01.005     Document Type: Review

References (60)

1. Waldmann T.A. Immunotherapy: past, present and future. Nat Med 9 (2003) 269-277
2. Lonberg N. Human antibodies from transgenic animals. Nat Biotechnol 23 (2005) 1117-1125
3. Carter P.J. Potent antibody therapeutics by design. Nat Rev Immunol 6 (2006) 343-357
4. von Mehren M., Adams G.P., and Weiner L.M. Monoclonal antibody therapy for cancer. Annu Rev Med 54 (2003) 343-369
5. Adams G.P., and Weiner L.M. Monoclonal antibody therapy of cancer. Nat Biotechnol 23 (2005) 1147-1157
6. Egen J.G., Kuhns M.S., and Allison J.P. CTLA-4: new insights into its biological function and use in tumor immunotherapy. Nat Immunol 3 (2002) 611-618
7. Sanderson K., Scotland R., Lee P., Liu D., Groshen S., Snively J., Sian S., Nichol G., Davis T., Keler T., et al. Autoimmunity in a phase I trial of a fully human anti-cytotoxic T-lymphocyte antigen-4 monoclonal antibody with multiple melanoma peptides and Montanide ISA 51 for patients with resected stages III and IV melanoma. J Clin Oncol 23 (2005) 741-750
8. Li S., Schmitz K.R., Jeffrey P.D., Wiltzius J.J., Kussie P., and Ferguson K.M. Structural basis for inhibition of the epidermal growth factor receptor by cetuximab. Cancer Cell 7 (2005) 301-311
9. Sunada H., Magun B.E., Mendelsohn J., and MacLeod C.L. Monoclonal antibody against epidermal growth factor receptor is internalized without stimulating receptor phosphorylation. Proc Natl Acad Sci USA 83 (1986) 3825-3829
10. Zhang M., Yao Z., Zhang Z., Garmestani K., Goldman C.K., Ravetch J.V., Janik J., Brechbiel M.W., and Waldmann T.A. Effective therapy for a murine model of human anaplastic large-cell lymphoma with the anti-CD30 monoclonal antibody, HeFi-1, does not require activating Fc receptors. Blood 108 (2006) 705-710
11. Ravetch J.V. Fc receptors. In: Paul W.E. (Ed). Fundamental Immunology. edn5 (2003), Lippincott-Raven 685-700
12. Vitetta E.S., and Ghetie V.F. Immunology. Considering therapeutic antibodies. Science 313 (2006) 308-309
13. Ravetch J.V., and Lanier L.L. Immune inhibitory receptors. Science 290 (2000) 84-89
14. Nimmerjahn F., and Ravetch J.V. Fcγ receptors: old friends and new family members. Immunity 24 (2006) 19-28
15. Kalergis A.M., and Ravetch J.V. Inducing tumor immunity through the selective engagement of activating Fcγ receptors on dendritic cells. J Exp Med 195 (2002) 1653-1659
16. Zhang M., Zhang Z., Garmestani K., Goldman C.K., Ravetch J.V., Brechbiel M.W., Carrasquillo J.A., and Waldmann T.A. Activating Fc receptors are required for antitumor efficacy of the antibodies directed toward CD25 in a murine model of adult T-cell leukemia. Cancer Res 64 (2004) 5825-5829
17. Uchida J., Hamaguchi Y., Oliver J.A., Ravetch J.V., Poe J.C., Haas K.M., and Tedder T.F. The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med 199 (2004) 1659-1669
18. ••] shows that the cytotoxic activity of different antibody isotypes is dependent on specific activating FcRs. By contrast, complement-dependent cytotoxicity did not play an important role in tumor-cell killing.
19. Nimmerjahn F., and Ravetch J.V. Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science 310 (2005) 1510-1512. This study demonstrates that the basis for differential antibody isotype activity in vivo is the engagement of specific activating and inhibitory FcR pairs. By assigning an A/I ratio based on the affinities of antibody isotypes to these FcR pairs, antibody activity could be predicted in vivo.
20. Clynes R.A., Towers T.L., Presta L.G., and Ravetch J.V. Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med 6 (2000) 443-446
21. Bevaart L., Jansen M.J., van Vugt M.J., Verbeek J.S., van de Winkel J.G., and Leusen J.H. The high-affinity IgG receptor, FcγRI, plays a central role in antibody therapy of experimental melanoma. Cancer Res 66 (2006) 1261-1264
22. Barnes N., Gavin A.L., Tan P.S., Mottram P., Koentgen F., and Hogarth P.M. FcγRI-deficient mice show multiple alterations to inflammatory and immune responses. Immunity 16 (2002) 379-389
23. Ioan-Facsinay A., de Kimpe S.J., Hellwig S.M., van Lent P.L., Hofhuis F.M., van Ojik H.H., Sedlik C., da Silveira S.A., Gerber J., de Jong Y.F., et al. FcγRI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity 16 (2002) 391-402
24. Weng W.K., Czerwinski D., Timmerman J., Hsu F.J., and Levy R. Clinical outcome of lymphoma patients after idiotype vaccination is correlated with humoral immune response and immunoglobulin G Fc receptor genotype. J Clin Oncol 22 (2004) 4717-4724
25. Weng W.K., and Levy R. Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J Clin Oncol 21 (2003) 3940-3947
26. Cartron G., Dacheux L., Salles G., Solal-Celigny P., Bardos P., Colombat P., and Watier H. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcγRIIIa gene. Blood 99 (2002) 754-758
27. Bergtold A., Desai D.D., Gavhane A., and Clynes R. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 23 (2005) 503-514. These authors show that the inhibitory FcγRIIB is important for prolonged presentation of immune complexes on DCs, thus allowing the priming of B cells. In contrast to this recycling by FcγRIIB, ICs taken up via FcγRIII are degraded in acidic vesicles resulting in peptide presentation on MHC molecules for priming of T cells.
28. Regnault A., Lankar D., Lacabanne V., Rodriguez A., Thery C., Rescigno M., Saito T., Verbeek S., Bonnerot C., Ricciardi-Castagnoli P., et al. Fcγ receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J Exp Med 189 (1999) 371-380
29. Groh V., Li Y.Q., Cioca D., Hunder N.N., Wang W., Riddell S.R., Yee C., and Spies T. Efficient cross-priming of tumor antigen-specific T cells by dendritic cells sensitized with diverse anti-MICA opsonized tumor cells. Proc Natl Acad Sci USA 102 (2005) 6461-6466
30. •] provides convincing evidence that the inhibitory FcR is an important regulator of DC activation and thus might contribute to the maintenance of peripheral tolerance in the cellular immune system.
31. Dhodapkar K.M., Krasovsky J., Williamson B., and Dhodapkar M.V. Antitumor monoclonal antibodies enhance cross-presentation of cellular antigens and the generation of myeloma-specific killer T cells by dendritic cells. J Exp Med 195 (2002) 125-133
32. •].
33. Schuurhuis D.H., van Montfoort N., Ioan-Facsinay A., Jiawan R., Camps M., Nouta J., Melief C.J., Verbeek J.S., and Ossendorp F. Immune complex-loaded dendritic cells are superior to soluble immune complexes as antitumor vaccine. J Immunol 176 (2006) 4573-4580
34. Coutelier J.P., van der Logt J.T., Heessen F.W., Warnier G., and Van Snick J. IgG2a restriction of murine antibodies elicited by viral infections. J Exp Med 165 (1987) 64-69
35. Fossati-Jimack L., Ioan-Facsinay A., Reininger L., Chicheportiche Y., Watanabe N., Saito T., Hofhuis F.M., Gessner J.E., Schiller C., Schmidt R.E., et al. Markedly different pathogenicity of four immunoglobulin G isotype-switch variants of an antierythrocyte autoantibody is based on their capacity to interact in vivo with the low-affinity Fcγ receptor III. J Exp Med 191 (2000) 1293-1302
36. Kaminski M.S., Kitamura K., Maloney D.G., Campbell M.J., and Levy R. Importance of antibody isotype in monoclonal anti-idiotype therapy of a murine B cell lymphoma. A study of hybridoma class switch variants. J Immunol 136 (1986) 1123-1130
37. Kipps T.J., Parham P., Punt J., and Herzenberg L.A. Importance of immunoglobulin isotype in human antibody-dependent, cell-mediated cytotoxicity directed by murine monoclonal antibodies. J Exp Med 161 (1985) 1-17
38. Markine-Goriaynoff D., and Coutelier J.P. Increased efficacy of the immunoglobulin G2a subclass in antibody-mediated protection against lactate dehydrogenase-elevating virus-induced polioencephalomyelitis revealed with switch mutants. J Virol 76 (2002) 432-435
39. 2b antibody effector functions in vivo.
40. Schlageter A.M., and Kozel T.R. Opsonization of Cryptococcus neoformans by a family of isotype-switch variant antibodies specific for the capsular polysaccharide. Infect Immun 58 (1990) 1914-1918
41. Taborda C.P., Rivera J., Zaragoza O., and Casadevall A. More is not necessarily better: prozone-like effects in passive immunization with IgG. J Immunol 170 (2003) 3621-3630
42. Lambert S.L., Okada C.Y., and Levy R. TCR vaccines against a murine T cell lymphoma: a primary role for antibodies of the IgG2c class in tumor protection. J Immunol 172 (2004) 929-936
43. Clynes R., Takechi Y., Moroi Y., Houghton A., and Ravetch J.V. Fc receptors are required in passive and active immunity to melanoma. Proc Natl Acad Sci USA 95 (1998) 652-656
44. Clynes R., and Ravetch J.V. Cytotoxic antibodies trigger inflammation through Fc receptors. Immunity 3 (1995) 21-26
45. Sylvestre D., Clynes R., Ma M., Warren H., Carroll M.C., and Ravetch J.V. Immunoglobulin G-mediated inflammatory responses develop normally in complement-deficient mice. J Exp Med 184 (1996) 2385-2392
46. Ravetch J.V., and Clynes R.A. Divergent roles for Fc receptors and complement in vivo. Annu Rev Immunol 16 (1998) 421-432
47. Yazawa N., Hamaguchi Y., Poe J.C., and Tedder T.F. Immunotherapy using unconjugated CD19 monoclonal antibodies in animal models for B lymphocyte malignancies and autoimmune disease. Proc Natl Acad Sci USA 102 (2005) 15178-15183
48. Zhang Z., Zhang M., Ravetch J.V., Goldman C., and Waldmann T.A. Effective therapy for a murine model of adult T-cell leukemia with the humanized anti-CD2 monoclonal antibody, MEDI-507. Blood 102 (2003) 284-288
49. Zhang Z., Zhang M., Goldman C.K., Ravetch J.V., and Waldmann T.A. Effective therapy for a murine model of adult T-cell leukemia with the humanized anti-CD52 monoclonal antibody, Campath-1H. Cancer Res 63 (2003) 6453-6457
50. Rankin C.T., Veri M.C., Gorlatov S., Tuaillon N., Burke S., Huang L., Inzunza D., Li H., Thomas S., Johnson S., et al. CD32B, the human inhibitory Fc-γ receptor IIB, as a target for monoclonal antibody therapy of B-cell lymphoma. Blood 108 (2006) 2384-2391
51. Dijstelbloem H.M., van de Winkel J.G., and Kallenberg C.G. Inflammation in autoimmunity: receptors for IgG revisited. Trends Immunol 22 (2001) 510-516
52. Shields R.L., Namenuk A.K., Hong K., Meng Y.G., Rae J., Briggs J., Xie D., Lai J., Stadlen A., Li B., et al. High resolution mapping of the binding site on human IgG1 for FcγRI, FcγRII, FcγRIII, and FcRn and design of IgG1 variants with improved binding to the FcγR. J Biol Chem 276 (2001) 6591-6604
53. Lazar G.A., Dang W., Karki S., Vafa O., Peng J.S., Hyun L., Chan C., Chung H.S., Eivazi A., Yoder S.C., et al. Engineered antibody Fc variants with enhanced effector function. Proc Natl Acad Sci USA 103 (2006) 4005-4010. This study together with [52] shows that engineering of the antibody protein backbone allows generation of antibody variants with enhanced binding to activating FcRs, which show enhanced cytotoxic activity in vitro and in vivo.
54. Niwa R., Natsume A., Uehara A., Wakitani M., Iida S., Uchida K., Satoh M., and Shitara K. IgG subclass-independent improvement of antibody-dependent cellular cytotoxicity by fucose removal from Asn297-linked oligosaccharides. J Immunol Methods 306 (2005) 151-160
55. Niwa R., Shoji-Hosaka E., Sakurada M., Shinkawa T., Uchida K., Nakamura K., Matsushima K., Ueda R., Hanai N., and Shitara K. Defucosylated chimeric anti-CC chemokine receptor 4 IgG1 with enhanced antibody-dependent cellular cytotoxicity shows potent therapeutic activity to T-cell leukemia and lymphoma. Cancer Res 64 (2004) 2127-2133
56. Shields R.L., Lai J., Keck R., O'Connell L.Y., Hong K., Meng Y.G., Weikert S.H., Presta L.G., Namenuk A.K., Rae J., et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human FcγRIII and antibody-dependent cellular toxicity. J Biol Chem 277 (2002) 26733-26740
57. Shinkawa T., Nakamura K., Yamane N., Shoji-Hosaka E., Kanda Y., Sakurada M., Uchida K., Anazawa H., Satoh M., Yamasaki M., et al. 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 (2003) 3466-3473
58. Ferrara C., Stuart F., Sondermann P., Brunker P., and Umana P. The carbohydrate at FcγRIIIa Asn-162. An element required for high affinity binding to non-fucosylated IgG glycoforms. J Biol Chem 281 (2006) 5032-5036. This study shows the importance of the carbohydrate moiety on human FcγRIIIA for the differential binding to antibodies that have high or low fucose content. This might explain why these antibody glycovariants show a differential binding only to FcγRIIIA and not to the other low-affinity receptors.
59. Kaneko Y., Nimmerjahn F., and Ravetch J.V. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313 (2006) 670-673. This study demonstrates that sialic acid in the sugar moiety of the IgG Fc-portion is an important determinant of antibody activity. Antibodies with high levels of sialic acid that are present in the steady state show reduced binding to FcRs, whereas antibodies with low sialic acid content are generated during an immune response. Moreover, this study identifies the sialic acid rich IgG fraction in the anti-inflammatory therapeutic intravenous immunoglobulin G as its active component.
60. Rademacher T.W., Williams P., and Dwek R.A. Agalactosyl glycoforms of IgG autoantibodies are pathogenic. Proc Natl Acad Sci USA 91 (1994) 6123-6127