IgG4 subclass antibodies impair antitumor immunity in melanoma

Journal of Clinical Investigation

Volumn 123, Issue 4, 2013, Pages 1457-1474

  Karagiannis, Panagiotis ^a   Gilbert, Amy E ^a   Josephs, Debra H ^a   Ali, Niwa ^a   Dodev, Tihomir ^b   Saul, Louise ^a   Correa, Isabel ^a   Roberts, Luke ^c   Beddowes, Emma ^c   Koers, Alexander ^d   Hobbs, Carl ^b   Ferreira, Silvia ^c   Geh, Jenny L C ^d   Healy, Ciaran ^d   Harries, Mark ^e   Acland, Katharine M ^c   Blower, Philip J ^d   Mitchell, Tracey ^c   Fear, David J ^b   Spicer, James F ^b   Lacy, Katie E ^a   Nestle, Frank O ^a   Karagiannis, Sophia N ^a   more..

^a Queen Mary University of London and Barts NIHR BRC NHS Trust National Institute for Health and Care Research   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c GUY S HOSPITAL   (United Kingdom)

^d ST THOMAS HOSPITAL   (United Kingdom)

^e GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD22 ANTIGEN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G4; IMMUNOGLOBULIN G4 ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 4; UNCLASSIFIED DRUG; VASCULOTROPIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD; CANCER PATIENT; CELL FUNCTION; CELL INFILTRATION; CELL POLARITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOTOXICITY; DRUG POTENCY; EFFECTOR CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LYMPH NODE; MAJOR CLINICAL STUDY; MALE; MELANOMA; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SERUM; SURVIVAL RATE; TH2 CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; TUMOR VOLUME; TUMOR XENOGRAFT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTINEOPLASTIC AGENTS; B-LYMPHOCYTES; CELL POLARITY; COCULTURE TECHNIQUES; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOGLOBULIN G; INTERLEUKIN-10; INTERLEUKIN-4; KAPLAN-MEIER ESTIMATE; LYMPHATIC METASTASIS; MALE; MELANOMA; MICE; MIDDLE AGED; RECEPTORS, IGG; SIALIC ACID BINDING IG-LIKE LECTIN 2; SKIN NEOPLASMS; TH2 CELLS; TUMOR CELLS, CULTURED; TUMOR ESCAPE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84875855215     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI65579     Document Type: Article

References (76)

1. Weide B, et al. Functional T cells targeting NY-ESO-1 or Melan-A are predictive for survival of patients with distant melanoma metastasis. J Clin Oncol. 2012;30(15):1835-1841.
2. Watson DB, Burns GF, Mackay IR. In vitro growth of B lymphocytes infiltrating human melanoma tissue by transformation with EBV: Evidence for secretion of anti-melanoma antibodies by some transformed cells. J Immunol. 1983;130(5):2442-2447.
3. Kirkwood JM, Robinson JE. Human IgG and IgM monoclonal antibodies against autologous melanoma produced by Epstein-Barr-virus-transformed B lymphocytes. Cancer Immunol Immunother. 1990; 32(4):228-234.
4. Erdag G, et al. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res. 2012;72(5):1070-1080.
5. Andreu P, et al. FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell. 2010;17(2):121-134.
6. Schioppa T, et al. B regulatory cells and the tumorpromoting actions of TNF-alpha during squamous carcinogenesis. Proc Natl Acad Sci U S A. 2011; 108(26):10662-10667.
7. Jefferis R. Isotype and glycoform selection for antibody therapeutics. Arch Biochem Biophys. 2012; 526(2):159-166.
8. Papadea C, Check IJ. Human immunoglobulin G and immunoglobulin G subclasses: Biochemical, genetic, and clinical aspects. Crit Rev Clin Lab Sci. 1989;27(1):27-58.
9. Steplewski Z, Sun LK, Shearman CW, Ghrayeb J, Daddona P, Koprowski H. Biological activity of human-mouse IgG1, IgG2, IgG3, and IgG4 chimeric monoclonal antibodies with antitumor specificity. Proc Natl Acad Sci U S A. 1988;85(13):4852-4856.
10. Aalberse RC, Schuurman J. IgG4 breaking the rules. Immunology. 2002;105(1):9-19.
11. Aalberse RC, Stapel SO, Schuurman J, Rispens T. Immunoglobulin G4: An odd antibody. Clin Exp Allergy. 2009;39(4):469-477.
12. French M. Serum IgG subclasses in normal adults. Monogr Allergy. 1986;19:100-107.
13. Neild GH, Rodriguez-Justo M, Wall C, Connolly JO. Hyper-IgG4 disease: Report and characterisation of a new disease. BMC Med. 2006;4:23.
14. Stone JH, Zen Y, Deshpande V. IgG4-related disease. N Engl J Med. 2012;366(6):539-551.
15. Eifan AO, Shamji MH, Durham SR. Long-term clinical and immunological effects of allergen immunotherapy. Curr Opin Allergy Clin Immunol. 2011; 11(6):586-593.
16. Frew AJ. Allergen immunotherapy. J Allergy Clin Immunol. 2010;125(2 suppl 2):S306-S313.
17. Garcia BE, Sanz ML, Gato JJ, Fernandez J, Oehling A. IgG4 blocking effect on the release of antigen-specific histamine. J Investig Allergol Clin Immunol. 1993;3(1):26-33.
18. Shamji MH, et al. Functional rather than immunoreactive levels of IgG4 correlate closely with clinical response to grass pollen immunotherapy. Allergy. 2012;67(2):217-226.
19. Harada K, et al. Significance of IgG4-positive cells in extrahepatic cholangiocarcinoma: Molecular mechanism of IgG4 reaction in cancer tissue. Hepatology. 2012;56(1):157-164.
20. Cipponi A, et al. Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res. 2012;72(16):3997-4007.
21. Daveau M, et al. IgG4 subclass in malignant melanoma. J Natl Cancer Inst. 1977;58(2):189-192.
22. Ellyard JI, Simson L, Parish CR. Th2-mediated anti-tumour immunity: Friend or foe? Tissue Antigens. 2007;70(1):1-11.
23. Platts-Mills TA, Woodfolk JA, Erwin EA, Aalberse R. Mechanisms of tolerance to inhalant allergens: The relevance of a modified Th2 response to aller-gens from domestic animals. Springer Semin Immunopathol. 2004;25(3-4):271-279.
24. Satoguina JS, Weyand E, Larbi J, Hoerauf A. T regulatory-1 cells induce IgG4 production by B cells: Role of IL-10. J Immunol. 2005;174(8):4718-4726.
25. Francis JN, et al. Grass pollen immunotherapy: IL-10 induction and suppression of late responses precedes IgG4 inhibitory antibody activity. J Allergy Clin Immunol. 2008;121(5):1120-1125.
26. Robinson DS, Larche M, Durham SR. Tregs and allergic disease. J Clin Invest. 2004;114(10):1389-1397.
27. Jeannin P, Lecoanet S, Delneste Y, Gauchat JF, Bonnefoy JY. IgE versus IgG4 production can be differentially regulated by IL-10. J Immunol. 1998; 160(7):3555-3561.
28. Gilbert AE, et al. Monitoring the systemic human memory B cell compartment of melanoma patients for anti-tumor IgG antibodies. PLoS One. 2011; 6(4):e19330.
29. Punnonen J, de Waal Malefyt R, van Vlasselaer P, Gauchat JF, de Vries JE. IL-10 and viral IL-10 prevent IL-4-induced IgE synthesis by inhibiting the accessory cell function of monocytes. J Immunol. 1993;151(3):1280-1289.
30. Zaidi MR, et al. Interferon-gamma links ultraviolet radiation to melanomagenesis in mice. Nature. 2011;469(7331):548-553.
31. James LK, et al. Allergen specificity of IgG(4)-expressing B cells in patients with grass pollen allergy undergoing immunotherapy. J Allergy Clin Immunol. 2012;130(3):663-670.
32. Nakamura K, Malykhin A, Coggeshall KM. The Src homology 2 domain-containing inositol 5-phosphatase negatively regulates Fcgamma receptor-mediated phagocytosis through immunoreceptor tyrosine-based activation motif-bearing phagocytic receptors. Blood. 2002;100(9):3374-3382.
33. van der Poel CE, Spaapen RM, van de Winkel JG, Leusen JH. Functional characteristics of the high affinity IgG receptor, FcgammaRI. J Immunol. 2011;186(5):2699-2704.
34. Chu CC, et al. Resident CD141 (BDCA3)+ dendritic cells in human skin produce IL-10 and induce regulatory T cells that suppress skin inflammation. J Exp Med. 2012;209(5):935-945.
35. French MA, Harrison G. Serum IgG subclass concentrations in healthy adults: A study using monoclonal antisera. Clin Exp Immunol. 1984;56(2):473-475.
36. Anderson KS, et al. Serum antibodies to the HPV16 proteome as biomarkers for head and neck cancer. Br J Cancer. 2011;104(12):1896-1905.
37. Hussein MR, Elsers DA, Fadel SA, Omar AE. Immunohistological characterisation of tumour infiltrating lymphocytes in melanocytic skin lesions. J Clin Pathol. 2006;59(3):316-324.
38. Yeilding NM, Gerstner C, Kirkwood JM. Analysis of two human monoclonal antibodies against melanoma. Int J Cancer. 1992;52(6):967-973.
39. Yamaguchi H, et al. Cell-surface antigens of melanoma recognized by human monoclonal antibodies. Proc Natl Acad Sci U S A. 1987;84(8):2416-2420.
40. Schmidt P, Kopecky C, Hombach A, Zigrino P, Mauch C, Abken H. Eradication of melanomas by targeted elimination of a minor subset of tumor cells. Proc Natl Acad Sci U S A. 2011;108(6):2474-2479.
41. Zabierowski SE, Herlyn M. Melanoma stem cells: The dark seed of melanoma. J Clin Oncol. 2008; 26(17):2890-2894.
42. Ladanyi A, et al. Prognostic impact of B-cell density in cutaneous melanoma. Cancer Immunol Immunother. 2011;60(12):1729-1738.
43. Zapata JM, Llobet D, Krajewska M, Lefebvre S, Kress CL, Reed JC. Lymphocyte-specific TRAF3 transgenic mice have enhanced humoral responses and develop plasmacytosis, autoimmunity, inflammation, and cancer. Blood. 2009;113(19):4595-4603.
44. Coker HA, Durham SR, Gould HJ. Local somatic hypermutation and class switch recombination in the nasal mucosa of allergic rhinitis patients. J Immunol. 2003;171(10):5602-5610.
45. Whiteside TL. Immune suppression in cancer: Effects on immune cells, mechanisms and future therapeutic intervention. Semin Cancer Biol. 2006; 16(1):3-15.
46. Gerlini G, Tun-Kyi A, Dudli C, Burg G, Pimpinelli N, Nestle FO. Metastatic melanoma secreted IL-10 down-regulates CD1 molecules on dendritic cells in metastatic tumor lesions. Am J Pathol. 2004; 165(6):1853-1863.
47. Platts-Mills T, Vaughan J, Squillace S, Woodfolk J, Sporik R. Sensitisation, asthma, and a modified Th2 response in children exposed to cat allergen: A population-based cross-sectional study. Lancet. 2001;357(9258):752- 756.
48. Nakashima H, et al. An amplification of IL-10 and TGF-beta in patients with IgG4-related tubulointerstitial nephritis. Clin Nephrol. 2010;73(5):385-391.
49. Zen Y, Nakanuma Y. Pathogenesis of IgG4-related disease. Curr Opin Rheumatol. 2011;23(1):114-118.
50. Krop EJ, Stapel SO, De Vrieze H, Van der Zee JS. Immunoglobulin E and G4 antibody responses in occupational airway exposure to bovine and porcine plasma proteins. Int Arch Allergy Immunol. 2006; 139(3):237-244.
51. Matsui EC, et al. Mouse allergen-specific immunoglobulin G and immunoglobulin G4 and allergic symptoms in immunoglobulin E-sensitized laboratory animal workers. Clin Exp Allergy. 2005; 35(10):1347-1353.
52. Strid J, Sobolev O, Zafirova B, Polic B, Hayday A. The intraepithelial T cell response to NKG2D-ligands links lymphoid stress surveillance to atopy. Science. 2011;334(6060):1293-1297.
53. Nevala WK, Vachon CM, Leontovich AA, Scott CG, Thompson MA, Markovic SN. Evidence of systemic Th2-driven chronic inflammation in patients with metastatic melanoma. Clin Cancer Res. 2009;15(6):1931-1939.
54. Deng W, et al. Down-modulation of TNFSF15 in ovarian cancer by VEGF and MCP-1 is a pre-requisite for tumor neovascularization. Angiogenesis. 2012; 15(1):71-85.
55. Maeda K, Mehta H, Drevets DA, Coggeshall KM. IL-6 increases B-cell IgG production in a feed-forward proinflammatory mechanism to skew hematopoiesis and elevate myeloid production. Blood. 2010;115(23):4699-4706.
56. Hirano H, et al. TLR4, IL-6, IL-18, MyD88 and HMGB1 are highly expressed in intracranial inflammatory lesions and the IgG4/IgG ratio correlates with TLR4 and IL-6. Neuropathology. 2012;32(6):628-637.
57. Labrijn AF, Aalberse RC, Schuurman J. When binding is enough: Nonactivating antibody formats. Curr Opin Immunol. 2008;20(4):479-485.
58. Bruhns P, et al. Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood. 2009; 113(16):3716-3725.
59. Rispens T, Ooievaar-De Heer P, Vermeulen E, Schuurman J, van der Neut Kolfschoten M, Aalberse RC. Human IgG4 binds to IgG4 and conformationally altered IgG1 via Fc-Fc interactions. J Immunol. 2009;182(7):4275-4281.
60. Leyendeckers H, et al. Correlation analysis between frequencies of circulating antigen-specific IgG-bearing memory B cells and serum titers of antigen-specific IgG. Eur J Immunol. 1999;29(4):1406-1417.
61. van Schouwenburg PA, et al. IgG4 production against adalimumab during long term treatment of RA patients. J Clin Immunol. 2012;32(5):1000-1006.
62. Svenson M, Geborek P, Saxne T, Bendtzen K. Monitoring patients treated with anti-TNF-alpha biopharmaceuticals: Assessing serum infliximab and anti-infliximab antibodies. Rheumatology (Oxford). 2007;46(12):1828-1834.
63. Bruggemann M, et al. Comparison of the effector functions of human immunoglobulins using a matched set of chimeric antibodies. J Exp Med. 1987;166(5):1351-1361.
64. Balch CM, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol. 2009;27(36):6199-6206.
65. Lapointe R, Bellemare-Pelletier A, Housseau F, Thibodeau J, Hwu P. CD40-stimulated B lymphocytes pulsed with tumor antigens are effective antigen-presenting cells that can generate specific T cells. Cancer Res. 2003;63(11):2836-2843.
66. Karagiannis SN, et al. IgE-antibody-dependent immunotherapy of solid tumors: Cytotoxic and phagocytic mechanisms of eradication of ovarian cancer cells. J Immunol. 2007;179(5):2832-2843.
67. Schauer U, et al. IgG subclass concentrations in certified reference material 470 and reference values for children and adults determined with the binding site reagents. Clin Chem. 2003;49(11):1924-1929.
68. Campoli M, Ferrone S, Wang X. Functional and clinical relevance of chondroitin sulfate proteoglycan 4. Adv Cancer Res. 2010;109:73-121.
69. Price MA, et al. CSPG4, a potential therapeutic target, facilitates malignant progression of melanoma. Pigment Cell Melanoma Res. 2011;24(6):1148-1157.
70. Neri D, et al. Recombinant anti-human melanoma antibodies are versatile molecules. J Invest Dermatol. 1996;107(2):164-170.
71. Karagiannis P, et al. Characterisation of an engineered trastuzumab IgE antibody and effector cell mechanisms targeting HER2/neu-positive tumour cells. Cancer Immunol Immunother. 2009;58(6):915-930.
72. Bracher M, Gould HJ, Sutton BJ, Dombrowicz D, Karagiannis SN. Three-colour flow cytometric method to measure antibody-dependent tumour cell killing by cytotoxicity and phagocytosis. J Immunol Methods. 2007;323(2):160-171.
73. Bunk S, et al. Internalization and coreceptor expression are critical for TLR2-mediated recognition of lipoteichoic acid in human peripheral blood. J Immunol. 2010;185(6):3708-3717.
74. Tamm A, Schmidt RE. The binding epitopes of human CD16 (Fc gamma RIII) monoclonal antibodies. Implications for ligand binding. J Immunol. 1996;157(4):1576-1581.
75. Hober D, et al. Circulating and cell-bound antibodies increase coxsackievirus B4-induced production of IFN-alpha by peripheral blood mononuclear cells from patients with type 1 diabetes. J Gen Virol. 2002;83(pt 9):2169-2176.
76. Karagiannis SN, et al. Role of IgE receptors in IgE antibody-dependent cytotoxicity and phagocytosis of ovarian tumor cells by human monocytic cells. Cancer Immunol Immunother. 2008;57(2):247-263.