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01.02.2008 | Original Article

Role of IgE receptors in IgE antibody-dependent cytotoxicity and phagocytosis of ovarian tumor cells by human monocytic cells

verfasst von: Sophia N. Karagiannis, Marguerite G. Bracher, Rebecca L. Beavil, Andrew J. Beavil, James Hunt, Natalie McCloskey, Richard G. Thompson, Nicholas East, Frances Burke, Brian J. Sutton, David Dombrowicz, Frances R. Balkwill, Hannah J. Gould

Erschienen in: Cancer Immunology, Immunotherapy | Ausgabe 2/2008

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Abstract

Antibodies directed against tumor-associated antigens are emerging as effective treatments for a number of cancers, although the mechanism(s) of action for some are unclear and still under investigation. We have previously examined a chimeric IgE antibody (MOv18 IgE), against the ovarian tumor-specific antigen, folate binding protein (FBP), and showed that it can direct human PBMC to kill ovarian cancer cells. We have developed a three-color flow cytometric assay to investigate the mechanism by which IgE receptors on U937 monocytes target and kill ovarian tumor cells. U937 monocytes express three IgE receptors, the high-affinity receptor, FcεRI, the low-affinity receptor, CD23, and galectin-3, and mediate tumor cell killing in vitro by two mechanisms, cytotoxicity, and phagocytosis. Our results suggest that CD23 mediates phagocytosis, which is enhanced by upregulation of CD23 on U937 cells with IL-4, whereas FcεRI mediates cytotoxicity. We show that effector : tumor cell bridging is associated with both activities. Galectin-3 does not appear to be involved in tumor cell killing. U937 cells and IgE exerted ovarian tumor cell killing in vivo in our xenograft model in nude mice. Harnessing IgE receptors to target tumor cells suggests the potential of tumor-specific IgE antibodies to activate effector cells in immunotherapy of ovarian cancer.

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Glennie MJ, van de Winkel JG (2003) Renaissance of cancer therapeutic antibodies. Drug Discov Today 8:503–510PubMedCrossRef

Carter PJ (2006) Potent antibody therapeutics by design. Nat Rev Immunol 6:343–357PubMedCrossRef

Brüggeman M, Caskey HM, Teale C, Waldmann H, Williams G, Surani NA, Neuberger MS (1987) Comparison of the effector functions of human immunoglobulins using a matched set of chimeric antibodies. J Exp Med 166:1351–1361CrossRef

Dyer MJS, Hale G, Hayhoe FGJ, Waldmann H (1989) Effects in vivo in patients with lymphoid malignancies; influence of antibody isotype. Blood 73:1431–1439PubMed

Clynes RA, Towers TL, Presta LG, Ravetch JV (2000) Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med 6:443–446PubMedCrossRef

Reali E, Greiner JW, Corti A, Gould HJ, Bottazzoli F, Paganelli G, Schlom J, Siccardi AG (2001) IgEs targeted on tumor cells: therapeutic activity and potential in the design of tumour vaccines. Cancer Res 61:5517–5522PubMed

Gould HJ, Sutton BJ, Beavil AJ, Beavil RL, McCloskey N, Coker HA, Fear D, Smurthwaite L (2003) The biology of IgE and the basis of allergic disease. Annu Rev Immunol 21:579–628PubMedCrossRef

Gould HJ, Mackay GA, Karagiannis SN, O’Toole CM, Marsh PJ, Daniel BE, Coney LR Zurawski VR Jr, Joseph M, Capron M, Gilbert M, Murphy GF, Korngold R (1999) Comparison of IgE and IgG antibody-dependent cytotoxicity in vitro and in a SCID mouse xenograft model of ovarian carcinoma. Eur J Immunol 29:3527–3537PubMedCrossRef

Karagiannis SN, Wang Q, East N, Burke F, Riffard S, Bracher MG, Thompson RG, Durham SR, Schwartz LB, Balkwill FR, Gould HJ (2003) Activity of human monocytes in IgE antibody-dependent surveillance and killing of ovarian tumor cells. Eur J Immunol 33:1030–1040PubMedCrossRef

10.

Campbell IG, Jones TA, Foulkes WD, Trowsdale J (1991) Folate binding protein is a marker for ovarian cancer. Cancer Res 51:5329–5338PubMed

11.

Coney LR, Tomassetti A, Carayannopoulos L, Frasca V, Kamen BA, Colnaghi MI, Zurawski VR Jr (1991) Cloning of a tumor-associated antigen: MOv18 and MOv19 antibodies recognize a folate-binding protein. Cancer Res 51:6125–6132PubMed

12.

Toffoli G, Cernigoi C, Russo A, Gallo A, Bagnoli M, Boiocchi M (1997) Overexpression of folate binding protein in ovarian cancers. Int J Cancer 74:193–198PubMedCrossRef

13.

Williams J, Johnson S, Mascali JJ, Smith H, Rosenwasser LJ, Borish L (1992) Regulation of low affinity IgE receptor (CD23) expression on mononuclear phagocytes in normal and asthmatic subjects. J Immunol 149:2823–2829PubMed

14.

Wong HL, Lotze MT, Wahl LM, Wahl SM (1992) Administration of recombinant IL-4 to humans regulates gene expression, phenotype, and function in circulating monocytes. J Immunol 148:2118–2125PubMed

15.

Boltz-Nitulescu G, Willheim M, Spittler A, Leutmezer F, Tempfer C, Winkler S (1995) Modulation of IgA, IgE, and IgG Fc receptor expression on human mononuclear phagocytes by 1 alpha,25-dihydroxyvitamin D3 and cytokines. J Leukoc Biol 58:256–262PubMed

16.

Maurer D, Fiebiger E, Reininger B, Wolff-Winiski B, Jouvin MH, Kilgus O, Kinet JP, Stingl G (1994) Expression of functional high affinity immunoglobulin E receptors (Fc epsilon RI) on monocytes of atopic individuals. J Exp Med 179:745–750PubMedCrossRef

17.

Reischl IG, Corvaia N, Effenberger F, Wolff-Winiski B, Kromer E, Mudde GC (1996) Function and regulation of Fc epsilon RI expression on monocytes from non-atopic donors. Clin Exp Allergy 26:630–641PubMedCrossRef

18.

Frigeri LG, Liu FT (1992) Surface expression of functional IgE binding protein, an endogenous lectin, on mast cells and macrophages. J Immunol 148:861–867PubMed

19.

Liu FT, Hsu DK, Zuberi RI, Kuwabara I, Chi EY, Henderson WR Jr (1995) Expression and function of galectin-3, a beta-galactoside-binding lectin, in human monocytes and macrophages. Am J Pathol 147:1016–1028PubMed

20.

Liu FT, Hsu DK, Zuberi RI, Shenhav A, Hill PN, Kuwabara I, Chen SS (1996) Modulation of functional properties of galectin-3 by monoclonal antibodies binding to the non-lectin domain. Biochemistry 35:6073–6079PubMedCrossRef

21.

Yokota A, Kikutani H, Tanaka T, Sato R, Barsumian EL, Suemura M, Kishimoto T (1988) Two species of human Fcε receptor II (FcεRII/CD23): tissue-specific and IL-4-specific regulation of gene expression. Cell 55:611–618PubMedCrossRef

22.

Yokota A, Yukawa K, Yamamoto A, Sugiyama K, Suemura M, Tashiro Y, Kishimoto T, Kikutani H (1992) Two forms of the low-affinity Fc receptor for IgE differentially mediate endocytosis and phagocytosis: identification of the critical cytoplasmic domains. Proc Natl Acad Sci USA 89:5030–5034PubMedCrossRef

23.

Mossalayi MD, Paul-Eugene N, Ouaaz F, Arock M, Kolb JP, Kilchherr E, Debre P, Dugas B (1994) Involvement of Fc epsilon RII/CD23 and L-arginine-dependent pathway in IgE-mediated stimulation of human monocyte functions. Int Immunol 6:931–938PubMedCrossRef

24.

Paul-Eugene N, Mossalayi D, Sarfati M, Yamaoka K, Aubry JP, Bonnefoy JY, Dugas B, Kolb JP (1995) Evidence for a role of Fc epsilon RII/CD23 in the IL-4-induced nitric oxide production by normal human mononuclear phagocytes. Cell Immunol 163:314–318PubMedCrossRef

25.

Vouldoukis I, Riveros-Moreno V, Dugas B, Ouaaz F, Becherel P, Debre P, Moncada S, Mossalayi MD (1995) The killing of Leishmania major by human macrophages is mediated by nitric oxide induced after ligation of the Fc epsilon RII/CD23 surface antigen. Proc Natl Acad Sci USA 92:7804–7808PubMedCrossRef

26.

Ravetch JV, Kinet JP (1991) Fc receptors. Annu Rev Immunol 9:457–492PubMed

27.

Dyall R, Vasovic LV, Clynes RA, Nikolic-Zugic J (1999) Cellular requirements for the monoclonal antibody-mediated eradication of an established solid tumor. Eur J Immunol 29:30–37PubMedCrossRef

28.

Liu FT (2005) Regulatory roles of galectins in the immune response. Int Arch Allergy Immunol 136:385–400PubMedCrossRef

29.

Sundström G, Nilsson K (1976) Establishment and characterization of a human histiocytic cell-line (U937). Int J Cancer 17:565–577PubMedCrossRef

30.

Benard J, Da Silva J, De Blois MC, Boyer P, Duvillard P, Chiric E, Riou G (1985) Characterization of a human ovarian adenocarcinoma line, IGROV1, in tissue culture and in nude mice. Cancer Res 45:4970–4979PubMed

31.

Balkwill FR, Lee A, Aldam G, Moodie E, Thomas JA, Tavernier J, Fiers W (1986) Human tumor xenografts treated with recombinant human tumor necrosis factor alone or in combination with interferons. Cancer Res 46:3990–3993PubMed

32.

Bracher M, Gould HJ, Sutton BJ, Dombrowicz D, Karagiannis SN (2007) Three-colour flow cytometric method to measure antibody-dependent tumour cell killing by cytotoxicity and phagocytosis. J Immunol Methods 323:160–171PubMedCrossRef

33.

Neuberger MS, Williams GT, Mitchell EB, Jouhal SS, Flanagan JG, Rabbitts TH (1985) A hapten-specific chimaeric IgE antibody with human physiological effector function. Nature 314:268–270PubMedCrossRef

34.

Cook JP, Henry AJ, McDonnell JM, Owens RJ, Sutton BJ, Gould HJ (1997) Identification of contact residues in the IgE binding site of human FcεRIα. Biochemistry 36:15579–15588PubMedCrossRef

35.

Wakai M, Pasley P, Sthoeger ZM, Posnett DN, Brooks R, Hashimoto S, Chiorazzi N (1993) Anti-CD23 monoclonal antibodies: comparisons of epitope specificities and modulating capacities for IgE binding and production. Hybridoma 12:25–43PubMedCrossRef

36.

Mavromatis BH, Cheson BD (2004) Novel therapies for chronic lymphocytic leukemia. Blood Rev 18:137–148PubMedCrossRef

37.

Riske F, Hakimi J, Mallamaci M, Griffin M, Pilson B, Tobkes N, Lin P, Danho W, Kochan J, Chizzonite R (1991) High affinity human IgE receptor (Fc epsilon RI). Analysis of functional domains of the alpha-subunit with monoclonal antibodies. J Biol Chem 266:11245–11251PubMed

38.

Wang B, Rieger A, Kilgus O, Ochiai K, Maurer D, Fodinger D, Kinet JP, Stingl G (1992) Epidermal Langerhans cells from normal human skin bind monomeric IgE via Fc epsilon RI. J Exp Med 175:1353–1365PubMedCrossRef

39.

Lin S, Cicala C, Scharenberg AM, Kinet JP (1996) The FcεRI β subunit functions as an amplifier of FcεRI γ-mediated cell activation signals. Cell 85:985–995PubMedCrossRef

40.

Tomassetti A, Coney LR, Canevari S, Miotti S, Facheris P, Zurawski VR Jr, Colnaghi MI (1993) Isolation and biochemical characterization of the soluble and membrane forms of folate binding protein expressed in the ovarian carcinoma cell line IGROV1. FEBS Lett 317:143–146PubMedCrossRef

41.

Vercelli D, Helm B, Marsh P, Padlan E, Geha RS, Gould H (1989) The B-cell binding site on human immunoglobulin E. Nature 338:649–651PubMedCrossRef

42.

Keegan AD, Fratazzi C, Shopes B, Baird B, Conrad DH (1991) Characterization of new rat anti-mouse IgE monoclonals and their use along with chimeric IgE to further define the site that interacts with FcεRII and FcεRI. Mol Immunol 28:1149–1154PubMedCrossRef

43.

Kayaba H, Dombrowicz D, Woerly G, Papin JP, Loiseau S, Capron M (2001) Human eosinophils and human high affinity IgE receptor transgenic mouse eosinophils express low levels of high affinity IgE receptor, but release IL-10 upon receptor activation. J Immunol 167:995–1003PubMed

44.

Oliver JM, Kepley CL, Ortega E, Wilson BS (2000) Immunologically mediated signaling in basophils and mast cells: finding therapeutic targets for allergic diseases in the human FcepsilonR1 signalling pathway. Immunopharmacology 48:269–281PubMedCrossRef

45.

Gounni AS, Lamkhioued B, Ochiai K, Tanaka Y, Delaporte E, Capron A, Kinet JP, Capron M (1994) High-affinity IgE receptor on eosinophils is involved in defence against parasites. Nature 367:183–186PubMedCrossRef

46.

Cormier SA, Taranova AG, Bedient C, Nguyen T, Protheroe C, Pero R, Dimina D, Ochkur SI, O’Neill K, Colbert D, Lombari TR, Constant S, McGarry MP, Lee JJ, Lee NA (2006) Pivotal advance: eosinophil infiltration of solid tumors is an early and persistent inflammatory host response. J Leukoc Biol 79:1131–1139PubMedCrossRef

47.

Munitz A, Levi-Schaffer F (2004) Eosinophils: ‘new’ roles for ‘old’ cells. Allergy 59:268–275PubMedCrossRef

48.

MacGlashan DW Jr (1993) Releasability of human basophils: cellular sensitivity and maximal histamine release are independent variables. J Allergy Clin Immunol 91:605–615PubMedCrossRef

49.

Coney LR, Mezzanzanica D, Sanborn D, Casalini P, Colnaghi MI, Zurawski VR Jr (1994) Chimeric murine-human antibodies directed against folate binding receptor are efficient mediators of ovarian carcinoma cell killing. Cancer Res 54:2448–2455PubMed

50.

Molthoff CF, Prinssen HM, Kenemans P, van Hof AC, den Hollander W, Verheijen RH (1997) Escalating protein doses of chimeric monoclonal antibody MOv18 immunoglobulin G in ovarian carcinoma patients: a phase I study. Cancer 80:2712–2720PubMedCrossRef

51.

Buijs WC, Tibben JG, Boerman OC, Molthoff CF, Massuger LF, Koenders EB, Schijf CP, Siegel JA, Corstens FH (1998) Dosimetric analysis of chimeric monoclonal antibody cMOv18 IgG in ovarian carcinoma patients after intraperitoneal and intravenous administration. Eur J Nucl Med 25:1552–1561PubMedCrossRef

Titel: Role of IgE receptors in IgE antibody-dependent cytotoxicity and phagocytosis of ovarian tumor cells by human monocytic cells
verfasst von: Sophia N. Karagiannis
Marguerite G. Bracher
Rebecca L. Beavil
Andrew J. Beavil
James Hunt
Natalie McCloskey
Richard G. Thompson
Nicholas East
Frances Burke
Brian J. Sutton
David Dombrowicz
Frances R. Balkwill
Hannah J. Gould
Publikationsdatum: 01.02.2008
Verlag: Springer-Verlag
Erschienen in: Cancer Immunology, Immunotherapy / Ausgabe 2/2008
Print ISSN: 0340-7004
Elektronische ISSN: 1432-0851
DOI: https://doi.org/10.1007/s00262-007-0371-7

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Role of IgE receptors in IgE antibody-dependent cytotoxicity and phagocytosis of ovarian tumor cells by human monocytic cells

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