An anti-EGFR IgA that displays improved pharmacokinetics and myeloid effector cell engagement in vivo

Cancer Research

Volumn 76, Issue 2, 2016, Pages 403-417

  Lohse, Stefan ^a   Meyer, Saskia ^b   Meulenbroek, Laura A P M ^b   Jansen, J H Marco ^b   Nederend, Maaike ^b   Kretschmer, Anna ^a   Klausz, Katja ^a   Möginger, Uwe ^c,d   Derer, Stefanie ^a   Rösner, Thies ^a   Kellner, Christian ^a   Schewe, Denis ^a   Sondermann, Peter ^e   Tiwari, Sanjay ^a   Kolarich, Daniel ^c   Peipp, Matthias ^a   Leusen, Jeanette H W ^b   Valerius, Thomas ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e SuppreMol GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; EPIDERMAL GROWTH FACTOR RECEPTOR; FC RECEPTOR; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN A2; IMMUNOGLOBULIN A2 ANTIBODY; UNCLASSIFIED DRUG; ANTI-IGA; ANTIIDIOTYPIC ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY ENGINEERING; ANTIBODY PRODUCTION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW CELL; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG ELIMINATION; DRUG HALF LIFE; EFFECTOR CELL; FEMALE; GLYCOSYLATION; HUMAN; HUMAN CELL; IN VIVO STUDY; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; ANIMAL; BAGG ALBINO MOUSE; CELL DIFFERENTIATION; GENETIC TRANSFECTION; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; PROCEDURES; SCID MOUSE; TRANSGENIC MOUSE;

ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; CELL DIFFERENTIATION; HUMANS; IMMUNOTHERAPY; MICE; MICE, INBRED BALB C; MICE, SCID; MICE, TRANSGENIC; MYELOID CELLS; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSFECTION;

EID: 84959018760     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-1232     Document Type: Article

References (50)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;145:646-74.
2. Mendelsohn J, Baselga J. Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. J Clin Oncol 2003;21:2787-99.
3. Pao W, Miller VA. Epidermal growth factor receptor mutations, smallmolecule kinase inhibitors, and non-small-cell lung cancer: current knowledge and future directions. J Clin Oncol 2005;2:e73.
4. Baselga J. Targeting tyrosine kinases in cancer: the second wave. Science 2006;312:1175-8.
5. Schmitz KR, Ferguson KM. Interaction of antibodies with ErbB receptor extracellular regions. Exp Cell Res 2009;315:659-70.
6. 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: 512-20.
7. Price TJ, Peeters M, Kim TW, Cascinu S, Ruff P, Suresh AS, et al. Panitumumab versus cetuximab in patients with chemotherapy-refractory wildtype KRAS exon 2 metastatic colorectal cancer (ASPECCT): a randomised, multicentre, open-label, non-inferiority phase 3 study. Lancet Oncol 2014;15:569-79.
8. Uchida J, Hamaguchi Y, Oliver JA, Ravetch JV, Poe JC, Haas KM, et al. The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med 2004;199:1659-69.
9. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014;41:49-61.
10. Albanesi M, Mancardi DA, Jönsson F, Iannascoli B, Fiette L, Di Santo JP, et al. Neutrophils mediate antibody-induced antitumor effects in mice. Blood 2013;122:3160-4.
11. Dechant M, Beyer T, Schneider-Merck T, Weisner W, Peipp M, van de Winkel JGJ, et al. Effector mechanisms of recombinant IgA antibodies against EGFR. J Immunol 2007;179:2936-43.
12. Huls G, Heijnen IA, Cuomo E, van der Linden J, Boel E, van de Winkel JG, et al. Antitumor immune effectormechanisms recruited by phage displayderived fully human IgG1 and IgA1 monoclonal antibodies. Cancer Res 1999;59:5778-84.
13. Lohse S, Brunke C, Derer S, Peipp M, Boross P, Kellner C, et al. Characterization of a mutated IgA2 antibody of the m(1) allotype against the epidermal growth factor receptor as novel cytotoxic trigger molecule for the recruitment of monocytes and macrophages. J Biol Chem 2012;287: 25139-50.
14. Woof JM, RussellMW.Structure and function relationships in IgA. Mucosal Immunol 2011;4:590-7.
15. Monteiro RC, van de Winkel JG. IgA Fc receptors. Annu Rev Immunol 2003;21:177-204.
16. Woof JM, Burton DR. Human antibody-Fc receptor interactions illuminated by crystal structures. Nat Rev Immunol 2004;4:89-99.
17. Mattu TS, Pleass RJ, Willis AC, Kilian M, Wormald MR, Lellouch AC, et al. The glycosylation and structure of human serum IgA1, Fab, and Fc regions and the role of N-glycosylation on Fca receptor interactions. J Biol Chem 1998;273:2260-72.
18. Gomes MM, Wall SB, Takahashi K, Novak J, Renfrow MB, Herr AB. Analysis of IgA1 N-glycosylation and its contribution to FcaRI binding. Biochemistry 2008;47:11285-99.
19. Xue J, Zhao Q, Zhu L, Zhang W. Deglycosylation of FcaR at N58 increases it's binding to IgA. Glycobiology 2010;20:905-15.
20. Ferrara C, Stuart F, Sondermann P, Brünker P, Umaña P. The carbohydrate at FcgRIIIa Asn-162. An element required for high affinity binding to nonfucosylated IgG glycoforms. J Biol Chem 2006;281:5032-6.
21. Kawamura S, Saitou N, Ueda S. Concerted evolution of the primate immunoglobulin alpha-gene through gene conversion. J Biol Chem 1992;267:7359-67.
22. Chintalacharuvu KR, Raines M, Morrison SL. Divergence of human alphachain constant region sequences. A novel recombinant alpha 2 gene. J Immunol 1994;152:5299-304.
23. Wurm FM. Production of recombinant protein therapeutics in cultivated mammalian cells. Nat Biotechnol 2004;22:1393-8.
24. Kiryluk K, Novak J. The genetics and immunobiology of IgA nephropathy. J Clin Invest 2014;124:2325-32.
25. Furtado PB, Whitty PW, Robertson A, Eaton JT, Almogren A, Kerr MA, et al. Solution structure determination of monomeric human IgA2 by X-ray and neutron scattering, analytical ultracentrifugation and constrained modeling: a comparison with monomeric human IgA1. J Mol Biol 2004;338: 921-41.
26. Chintalacharuvu KR, Yu LJ, Bhola N, Kobayashi K, Fernandez CZ, Morrison SL. Cysteine residues required for the attachment of the light chain in human IgA2. J Immunol 2002;169:5072-7.
27. Tsuzukida Y, Wang CC, Putnam FW. Structure of the A2m(1) allotype of human IgA - a recombinant molecule. Proc Natl Acad Sci U S A 1979; 76:1104-8.
28. Johansen FE, Braathen R, Brandtzaeg P. The J chain is essential for polymeric Ig receptor-mediated epithelial transport of IgA. J Immunol 2001;167:5185-92.
29. Deshpande N, Jensen PH, Packer NH, Kolarich D. GlycoSpectrumScan: fishing glycopeptides from MS spectra of protease digests of human colostrum sIgA. J Proteome Res 2010;9:1063-75.
30. Boross P, Lohse S,NederendM, Jansen JH, van TeteringG, Dechant M, et al. IgA EGFR antibodies mediate tumor killing in vivo. EMBO Mol Med 2013;5:1213-26.
31. Rifai A, Fadden K, Morrison SL, Chintalacharuvu KR. The N-glycans determine the differential blood clearance and hepatic uptake of human immunoglobulin IgA1 and IgA2 isotypes. J Exp Med 2000;191: 2171-82.
32. Ghetie V, Ward ES. Multiple roles for the major histocompatibility complex class I-related receptor FcRn. Annu Rev Immunol 2000; 18:739-66.
33. Seested T, Nielsen HM, Christensen EI, Appa RS. The unsialylated subpopulation of recombinant activated factor VII binds to the asialo-glyvoprotein receptor (ASGPR) on primary rat hepatocytes. Thromb Haemost 2010;104:1166-73.
34. Ko SY, Pegu A, Rudicell RS, Yang ZY, Joyce MG, Chen X, et al. Enhanced neonatal Fc receptor function improves protection against primate SHIV infection. Nature 2014;514:642-5.
35. Brunke C, Lohse S, Derer S, Peipp M, Boross P, Kellner C, et al. Impact of a tail piece cysteine deletion on biochemical and functional properties of an epidermal growth factor receptor-directed IgA2m(1) antibody. mAbs 2013;5:936-45.
36. Kolarich D, Rapp E, Struwe WB, Haslam SM, Zaja J, McBride R, et al. The minimum information required for a glycomics experiment (MIRAGE) project: improving the standards for reporting mass-spectrometry-based glycoanalytic data. Mol Cell Proteomics 2013;12:991-5.
37. Jensen PH, Karlsson NG, Kolarich D, Packer NH. Structural analysis of N-and O-glycans released from glycoproteins. Nat Protoc 2012;7: 1299-310.
38. Kellner C, Bleeker WK, Lammerts van Bueren JJ, Staudinger M, Klausz K, Derer S, et al. Human kappa light chain targeted Pseudomonas exotoxin A identifying human antibodies and Fab fragments with favorable characteristics of antibody-drug conjugate development. J Immunol Methods 2011;371:122-33.
39. Roy A, Kucukural A, Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 2010;5: 725-38.
40. Filipe V, Que I, Carpenter JF, Löwik C, Jiskoot W. In vivo imaging of aggregates after subcutaneous and intravenous injection in mice. Pharm Res 2014;31:216-27.
41. Reichert JM. Antibodies to watch in 2014. MAbs 2014;6:5-14.
42. Bruggemann M, Williams GT, Bindon CI, Clark MR, Walker MR, Jefferis R, et al. Comparison of the effector functions of human immunoglobulins using a matched set of chimeric antibodies. J Exp Med 1987; 166:1351-61.
43. Liu HF, Ma J, Winter C, Bayer R. Recovery and purification process development for monoclonal antibody. mAbs 2010;2:480-99.
44. Pascal V, Laffleur B, Debin A, Cuvillier A, van Egmond M, Drocourt D, et al. Anti-CD20 IgA can protect mice against lymphoma development: evaluation of the direct impact of IgA and cytotoxic effector recruitment onCD20 target cells. Haematologica 2012;97:1686-94.
45. Marouka T, Nagata T, Kasahara M. Identification of the rat IgA Fc receptor encoded in the leukocyte receptor complex. Immunogenetics 2004; 55:712-6.
46. KeltonW,Mehta N, Charab W, Lee J, Lee CH, Kojima T, et al. IgGA: a "crossisotype" engineered human Fc antibody domain that displays both IgGlike and IgA-like effector functions. Chem Biol 2014;21:1603-9.
47. Sand KM, Dalhus B, Christianson GJ, Bern M, Foss S, Cameron J, et al. Dissection of the neonatal Fc receptor (FcRn)-albumin interface using mutagenesis and anti-FcRn albumin-blocking antibodies. J Biol Chem 2014;289:17228-39.
48. Dumitru CA, Lang S, Brandau S. Modulation of neutrophil granulocytes in the tumor microenvironment: mechanisms and consequences for tumor progression. Semin Cancer Biol 2013;23:141-8.
49. Zhang QW, Liu L, Gong CY, Shi HS, Zeng YH, Wang XZ, et al. Prognostic significance of tumor-associated macrophages in solid tumor: a metaanalysis of the literature. PLoS One 2012;7:e50946.
50. Bleeker WK, Lammerts van Bueren JJ, vanOjik HH, Gerristen AF, Pluyter M, Houtkamp M, et al. Dual mode of action of a human anti-epidermal growth factor receptor monoclonal antibody for cancer therapy. J Immunol 2004;173:4699-707.