Comparative reactivity of human IgE to cynomolgus monkey and human effector cells and effects on IgE effector cell potency

mAbs

Volumn 6, Issue 2, 2014, Pages 509-522

  Saul, Louise ^a,b   Josephs, Debra H ^a,b   Cutler, Keith ^c   Bradwell, Andrew ^c   Karagiannis, Panagiotis ^a   Selkirk, Chris ^d   Gould, Hannah J ^e   Jones, Paul ^d   Spicer, James F ^b   Karagiannis, Sophia N ^a  

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

^b GUY S HOSPITAL   (United Kingdom)

^c PUBLIC HEALTH ENGLAND   (United Kingdom)

^d IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^e KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Allergooncology; Allergy; Antibody effector functions; Cancer; Cross species reactivity; Cynomolgus monkey; IgE; IgE Fc receptors; Non human primate

Indexed keywords

CYTOKINE; FC RECEPTOR; FC RECEPTOR IA; GAMMA INTERFERON; HISTAMINE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN E ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL CELL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CONTROLLED STUDY; CROSS REACTION; CYTOKINE RELEASE; EFFECTOR CELL; EX VIVO STUDY; HISTAMINE RELEASE; HUMAN; HUMAN CELL; IMMUNOGLOBULIN BLOOD LEVEL; MACACA FASCICULARIS; MONOCYTE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PROTEIN BINDING;

ALLERGOONCOLOGY; ALLERGY; ANTIBODY EFFECTOR FUNCTIONS; CANCER; CROSS-SPECIES REACTIVITY; CYNOMOLGUS MONKEY; IGE; IGE FC RECEPTORS; NON-HUMAN PRIMATE;

ANIMALS; ANTIBODY AFFINITY; CELLS, CULTURED; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNOGLOBULIN E; IMMUNOTHERAPY; LECTINS, C-TYPE; LEUKOCYTES, MONONUCLEAR; MACACA FASCICULARIS; MODELS, ANIMAL; PROTEIN BINDING; RECEPTORS, IGE; SPECIES SPECIFICITY;

EID: 84896539805     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.4161/mabs.27828     Document Type: Article

References (47)

1. Gould HJ, Sutton BJ. IgE in allergy and asthma today. Nat Rev Immunol 2008; 8:205-17; PMID:18301424; http://dx.doi.org/10.1038/nri2273
2. Yoshimoto T, Yasuda K, Tanaka H, Nakahira M, Imai Y, Fujimori Y, Nakanishi K. Basophils contribute to T(H)2-IgE responses in vivo via IL-4 production and presentation of peptide-MHC class II complexes to CD4+ T cells. Nat Immunol 2009; 10:706-12; PMID:19465908; http://dx.doi.org/10.1038/ni.1737
3. Holgate ST, Djukanovic R, Casale T, Bousquet J. Anti-immunoglobulin E treatment with omalizumab in allergic diseases: an update on anti-inflammatory activity and clinical efficacy. Clin Exp Allergy 2005; 35:408-16; PMID:15836747; http://dx.doi.org/10.1111/j.1365-2222.2005.02191.x
4. Weiszer I, Patterson R, Pruzansky JJ. Ascaris hypersensitivity in the rhesus monkey. I. A model for the study of immediate type thypersensitity in the primate. J Allergy 1968; 41:14-22; PMID:4169344; http://dx.doi.org/10.1016/ 0021-8707(68)90004-X
5. Ferreira FD, Mayer P, Sperr WR, Valent P, Seiberler S, Ebner C, Liehl E, Scheiner O, Kraft D, Valenta R. Induction of IgE antibodies with predefined specificity in rhesus monkeys with recombinant birch pollen allergens, Bet v 1 and Bet v 2. J Allergy Clin Immunol 1996; 97:95-103; PMID:8568143; http://dx.doi.org/10.1016/S0091-6749(96)70287-7
6. Iwashita K, Kawasaki H, Sawada M, In M, Mataki Y, Kuwabara T. Shortening of the induction period of allergic asthma in cynomolgus monkeys by Ascaris suum and house dust mite. J Pharmacol Sci 2008; 106:92-9; PMID:18187925; http://dx.doi.org/10.1254/jphs.FP0071523
7. Van Scott MR, Hooker JL, Ehrmann D, Shibata Y, Kukoly C, Salleng K, Westergaard G, Sandrasagra A, Nyce J. Dust mite-induced asthma in cynomolgus monkeys. J Appl Physiol (1985) 2004; 96:1433-44; PMID:14672959; http://dx.doi.org/10.1152/japplphysiol.01128.2003
8. Bree A, Schlerman FJ, Wadanoli M, Tchistiakova L, Marquette K, Tan X-Y, Jacobson BA, Widom A, Cook TA, Wood N, et al. IL-13 blockade reduces lung inflammation after Ascaris suum challenge in cynomolgus monkeys. J Allergy Clin Immunol 2007; 119:1251-7; PMID:17379289; http://dx.doi.org/10.1016/j.jaci.2007. 02.009
9. Coffman RL, Hessel EM. Nonhuman primate models of asthma. J Exp Med 2005; 201:1875-9; PMID:15967818; http://dx.doi.org/10.1084/jem.20050901
10. rd, Kreutner W, Egan RW, Chapman RW. Effects of an antibody to interleukin-5 in a monkey model of asthma. Am J Respir Crit Care Med 1995; 152:467-72; PMID:7633694; http://dx.doi.org/10.1164/ajrccm.152.2.7633694
11. Beck A, Reichert JM. Therapeutic Fc-fusion proteins and peptides as successful alternatives to antibodies. MAbs 2011; 3:415-6; PMID:21785279; http://dx.doi.org/10.4161/mabs.3.5.17334
12. Ishizaka T, Ishizaka K, Orange RP, Austen KF. The capacity of human immunoglobulin E to mediate the release of histamine and slow reacting substance of anaphylaxis (SRS-A) from monkey lung. J Immunol 1970; 104:335-43; PMID:4189671
13. Garman SC, Wurzburg BA, Tarchevskaya SS, Kinet JP, Jardetzky TS. Structure of the Fc fragment of human IgE bound to its high-affinity receptor Fc epsilonRI alpha. Nature 2000; 406:259-66; PMID:10917520; http://dx.doi.org/10. 1038/35018500
14. Karagiannis SN, Wang Q, East N, Burke F, Riffard S, Bracher MG, Thompson RG, Durham SR, Schwartz LB, Balkwill FR, et al. Activity of human monocytes in IgE antibody-dependent surveillance and killing of ovarian tumor cells. Eur J Immunol 2003; 33:1030-40; PMID:12672069; http://dx.doi.org/10.1002/eji.200323185
15. Carter DL, Shieh TM, Blosser RL, Chadwick KR, Margolick JB, Hildreth JE, Clements JE, Zink MC. CD56 identifies monocytes and not natural killer cells in rhesus macaques. Cytometry 1999; 37:41-50; PMID:10451505; http://dx.doi.org/10. 1002/(SICI) 1097-0320 (19990901)37:1〈41: :AIDCYTO5〉3.0.CO;2-4
16. Karagiannis SN, Bracher MG, Beavil RL, Beavil AJ, Hunt J, McCloskey N, Thompson RG, East N, Burke F, Sutton BJ, 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; 57:247-63; PMID:17657488; http://dx.doi.org/10.1007/s00262-007-0371-7
17. Rudman SM, Josephs DH, Cambrook H, Karagiannis P, Gilbert AE, Dodev T, Hunt J, Koers A, Montes A, Taams L, et al. Harnessing engineered antibodies of the IgE class to combat malignancy: initial assessment of FcεRI-mediated basophil activation by a tumour-specific IgE antibody to evaluate the risk of type I hypersensitivity. Clin Exp Allergy 2011; 41:1400-13; PMID:21569129; http://dx.doi.org/10.1111/j.1365-2222.2011.03770.x
18. Platzer B, Fiebiger E. The signal peptide of the IgE receptor alpha-chain prevents surface expression of an immunoreceptor tyrosine-based activation motiffree receptor pool. J Biol Chem 2010; 285:15314-23; PMID:20304923; http://dx.doi.org/10.1074/jbc.M110.104281
19. Krejsa CM, Neradilek MB, Polissar NL, Cox N, Clark D, Cowan L, Bussiere J, Lebrec H. An inter-laboratory retrospective analysis of immunotoxicological endpoints in non-human primates: flow cytometry immunophenotyping. J Immunotoxicol 2013; 10:361-72; PMID:23384295; http://dx.doi.org/10.3109/ 1547691X.2012.755237
20. Hudson SA, Herrmann H, Du J, Cox P, Haddad B, Butler B, Crocker PR, Ackerman SJ, Valent P, Bochner BS. Developmental, malignancy-related, and cross-species analysis of eosinophil, mast cell, and basophil siglec-8 expression. J Clin Immunol 2011; 31:1045-53; PMID:21938510; http://dx.doi.org/ 10.1007/s10875-011-9589-4
21. Gould HJ, Sutton BJ, Beavil AJ, Beavil RL, McCloskey N, Coker HA, Fear D, Smurthwaite L. The biology of IGE and the basis of allergic disease. Annu Rev Immunol 2003; 21:579-628; PMID:12500981; http://dx.doi.org/10.1146/annurev. immunol.21.120601.141103
22. Hsu AP, Sowerwine KJ, Lawrence MG, Davis J, Henderson CJ, Zarember KA, Garofalo M, Gallin JI, Kuhns DB, Heller T, et al. Intermediate phenotypes in patients with autosomal dominant hyper-IgE syndrome caused by somatic mosaicism. J Allergy Clin Immunol 2013; 131:1586-93; PMID:23623265; http://dx.doi.org/10. 1016/j.jaci.2013.02.038
23. Potaczek DP, Michel S, Sharma V, Zeilinger S, Vogelberg C, von Berg A, Bufe A, Heinzmann A, Laub O, Rietschel E, et al. Different FCER1A polymorphisms influence IgE levels in asthmatics and non-asthmatics. Pediatr Allergy Immunol 2013; 24:441-9; PMID:23725541; http://dx.doi.org/10.1111/pai.12083
24. Kanthaswamy S, Ng J, Satkoski Trask J, George DA, Kou AJ, Hoffman LN, Doherty TB, Houghton P, Smith DG. The genetic composition of populations of cynomolgus macaques (Macaca fascicularis) used in biomedical research. J Med Primatol 2013; 42:120-31; PMID:23480663; http://dx.doi.org/10.1111/jmp.12043
25. Dehlink E, Baker AH, Yen E, Nurko S, Fiebiger E. Relationships between levels of serum IgE, cell-bound IgE, and IgE-receptors on peripheral blood cells in a pediatric population. PLoS One 2010; 5:e12204; PMID:20808937; http://dx.doi.org/10.1371/journal.pone.0012204
26. Peters MC, Mekonnen ZK, Yuan S, Bhakta NR, Woodruff PG, Fahy JV. Measures of gene expression in sputum cells can identify TH2-high and TH2-low subtypes of asthma. J Allergy Clin Immunol 2013; 24:01209-8; PMID:24075231
27. Palermo MS, Vermeulen ME, Giordano MN. Human antibody-dependent cellular cytotoxicity mediated by interferon gamma-activated neutrophils is impaired by vasoactive intestinal peptide. J Neuroimmunol 1996; 69:123-8; PMID:8823383; http://dx.doi.org/10.1016/0165-5728(96)00078-1
28. Pullyblank AM, Guillou PJ, Monson JR. Interleukin 1 and tumour necrosis factor alpha may be responsible for the lytic mechanism during anti-tumour antibody-dependent cell-mediated cytotoxicity. Br J Cancer 1995; 72:601-6; PMID:7669568; http://dx.doi.org/10.1038/bjc.1995.380
29. Xiong M, Elson G, Legarda D, Leibovich SJ. Production of vascular endothelial growth factor by murine macrophages: regulation by hypoxia, lactate, and the inducible nitric oxide synthase pathway. Am J Pathol 1998; 153:587-98; PMID:9708818; http://dx.doi.org/10.1016/S0002-9440(10)65601-5
30. Kozyrev IL, Miura T, Haga T, Kuwata T, Hayami M. Construction of SIV/HIV-1 chimeric viruses having the IL-5 gene and determination of their ability to replicate and produce IL-5. Arch Virol 2001; 146:1051-62; PMID:11504415; http://dx.doi.org/10.1007/s007050170105
31. Jeong AR, Nakamura S, Mitsunaga F. Gene expression profile of Th1 and Th2 cytokines and their receptors in human and nonhuman primates. J Med Primatol 2008; 37:290-6; PMID:18466281
32. Jensen-Jarolim E, Achatz G, Turner MC, Karagiannis S, Legrand F, Capron M, Penichet ML, Rodríguez JA, Siccardi AG, Vangelista L, et al. AllergoOncology: the role of IgE-mediated allergy in cancer. Allergy 2008; 63:1255-66; PMID:18671772; http://dx.doi.org/10.1111/j.1398-9995.2008.01768.x
33. Gould HJ, Mackay GA, Karagiannis SN, O'Toole CM, Marsh PJ, Daniel BE, Coney LR, Zurawski VR Jr., Joseph M, Capron M, et al. Comparison of IgE and IgG antibody-dependent cytotoxicity in vitro and in a SCID mouse xenograft model of ovarian carcinoma. Eur J Immunol 1999; 29:3527-37; PMID:10556807; http://dx.doi.org/10.1002/(SICI) 1521- 4141(199911)29 :11〈3527: :AIDIMMU3527〉3.0.CO;2-5
34. Karagiannis SN, Josephs DH, Karagiannis P, Gilbert AE, Saul L, Rudman SM, Dodev T, Koers A, Blower PJ, Corrigan C, et al. Recombinant IgE antibodies for passive immunotherapy of solid tumours: from concept towards clinical application. Cancer Immunol Immunother 2012; 61:1547-64; PMID:22139135; http://dx.doi.org/10.1007/s00262-011-1162-8
35. Josephs DH, Spicer JF, Corrigan CJ, Gould HJ, Karagiannis SN. Epidemiological associations of allergy, IgE and cancer. Clin Exp Allergy 2013; 43:1110-23; PMID:24074329
36. Josephs DH, Spicer JF, Karagiannis P, Gould HJ, Karagiannis SN. IgE immunotherapy: A novel concept with promise for the treatment of cancer. MAbs 2014; 6:1034-52; http://dx.doi.org/10.4161/mabs.27029
37. Eastwood D, Findlay L, Poole S, Bird C, Wadhwa M, Moore M, Burns C, Thorpe R, Stebbings R. Monoclonal antibody TGN1412 trial failure explained by species differences in CD28 expression on CD4+ effector memory T-cells. Br J Pharmacol 2010; 161:512-26; PMID:20880392; http://dx.doi.org/10.1111/j.1476- 5381.2010.00922.x
38. Lowe PJ, Tannenbaum S, Wu K, Lloyd P, Sims J. On setting the first dose in man: quantitating biotherapeutic drug-target binding through pharmacokinetic and pharmacodynamic models. Basic Clin Pharmacol Toxicol 2010; 106:195-209; PMID:20050847; http://dx.doi.org/10.1111/j.1742-7843.2009.00513.x
39. Pallardy M, Hünig T. Primate testing of TGN1412: right target, wrong cell. Br J Pharmacol 2010; 161:509-11; PMID:20880391; http://dx.doi.org/10. 1111/j.1476-5381.2010.00925.x
40. Karagiannis SN, Bracher MG, Hunt J, McCloskey N, Beavil RL, Beavil AJ, Fear DJ, Thompson RG, East N, Burke F, et al. IgE-antibody-dependent immunotherapy of solid tumors: cytotoxic and phagocytic mechanisms of eradication of ovarian cancer cells. J Immunol 2007; 179:2832-43; PMID:17709497
41. Neuberger MS, Williams GT, Mitchell EB, Jouhal SS, Flanagan JG, Rabbitts TH. A hapten-specific chimaeric IgE antibody with human physiological effector function. Nature 1985; 314:268-70; PMID:2580239; http://dx.doi.org/10.1038/ 314268a0
42. Cook JP, Henry AJ, McDonnell JM, Owens RJ, Sutton BJ, Gould HJ. Identification of contact residues in the IgE binding site of human FcepsilonRIalpha. Biochemistry 1997; 36:15579-88; PMID:9398286; http://dx.doi.org/10.1021/bi9713005
43. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947-8; PMID:17846036; http://dx.doi.org/ 10.1093/bioinformatics/btm404
44. Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006; 22:195-201; PMID:16301204; http://dx.doi.org/10.1093/bioinformatics/bti770
45. Meng YG, Singh N, Wong WL. Binding of cynomolgus monkey IgE to a humanized anti-human IgE antibody and human high affinity IgE receptor. Mol Immunol 1996; 33:635-42; PMID:8760275; http://dx.doi.org/10.1016/0161-5890(96) 00024-7
46. Karagiannis P, Singer J, Hunt J, Gan SK, Rudman SM, Mechtcheriakova D, Knittelfelder R, Daniels TR, Hobson PS, Beavil AJ, et al. Characterisation of an engineered trastuzumab IgE antibody and effector cell mechanisms targeting HER2/neu-positive tumour cells. Cancer Immunol Immunother 2009; 58:915-30; PMID:18941743; http://dx.doi.org/10.1007/s00262-008-0607-1
47. 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; 323:160-71; PMID:17531261; http://dx.doi.org/10.1016/j.jim.2007.04.009