Highly parallel characterization of IgG Fc binding interactions

mAbs

Volumn 6, Issue 4, 2014, Pages 915-927

  Boesch, Austin W ^a   Brown, Eric P ^a   Cheng, Hao D ^b   Ofori, Maame Ofua ^a   Normandin, Erica ^a   Nigrovic, Peter A ^c   Alter, Galit ^d   Ackerman, Margaret E ^a,b,e  

^a DARTMOUTH COLLEGE   (United States)

^b DARTMOUTH COLLEGE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Antibody; Fc domain; Fc receptor; Glycosylation; IgG; Lectin; Luminex; Multiplex

Indexed keywords

DECTIN 2; FC RECEPTOR; GLYCAN; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4; LECTIN; MICROSPHERE; IMMUNOGLOBULIN CONSTANT REGION; MONOCLONAL ANTIBODY; PROTEIN BINDING; TRASTUZUMAB;

ANTIBODY RESPONSE; ARTICLE; DEGLYCOSYLATION; GLYCOSYLATION; PROTEIN BINDING; CHEMISTRY; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOGLOBULIN CONSTANT REGION; POINT MUTATION;

ANTIBODIES, MONOCLONAL, HUMANIZED; HEK293 CELLS; HUMANS; IMMUNOGLOBULIN CONSTANT REGIONS; IMMUNOGLOBULIN G; MICROSPHERES; POINT MUTATION; PROTEIN BINDING; RECEPTORS, IGG;

EID: 84903776700     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.4161/mabs.28808     Document Type: Article

References (56)

1. Jefferis R, Pound J, Lund J, Goodall M. Effector mechanisms activated by human IgG subclass antibodies: clinical and molecular aspects. Review article. Ann Biol Clin (Paris) 1994; 52:57-65; PMID:8210076
2. Jefferis R, Lund J, Pound JD. IgG-Fc-mediated effector functions: molecular definition of interaction sites for effector ligands and the role of glycosylation. Immunol Rev 1998; 163:59-76; PMID:9700502; http://dx.doi.org/10. 1111/j.1600-065X.1998.tb01188.x
3. Bazin R, Lemieux R, Tremblay T, St-Amour I. Tetramolecular immune complexes are more efficient than IVIg to prevent antibody-dependent in vitro and in vivo phagocytosis of blood cells. Br J Haematol 2004; 127:90-6; PMID:15384982; http://dx.doi.org/10.1111/j.1365-2141.2004.05105.x
4. Lux A, Yu X, Scanlan CN, Nimmerjahn F. Impact of immune complex size and glycosylation on IgG binding to human FcγRs. J Immunol 2013; 190:4315-23; PMID:23509345; http://dx.doi.org/10.4049/jimmunol.1200501
5. Teeling JL, Jansen-Hendriks T, Kuijpers TW, de Haas M, van de Winkel JG, Hack CE, Bleeker WK. Therapeutic efficacy of intravenous immunoglobulin preparations depends on the immunoglobulin G dimers: studies in experimental immune thrombocytopenia. Blood 2001; 98:1095-9; PMID:11493456; http://dx.doi.org/10.1182/blood.V98.4.1095
6. Liu H, May K. Disulfide bond structures of IgG molecules: structural variations, chemical modifications and possible impacts to stability and biological function. MAbs 2012; 4:17-23; PMID:22327427; http://dx.doi.org/10. 4161/mabs.4.1.18347
7. Lazar GA, Dang W, Karki S, Vafa O, Peng JS, Hyun L, Chan C, Chung HS, Eivazi A, Yoder SC, et al. Engineered antibody Fc variants with enhanced effector function. Proc Natl Acad Sci U S A 2006; 103:4005-10; PMID:16537476; http://dx.doi.org/10.1073/pnas.0508123103
8. de Lange GG. Polymorphisms of human immunoglobulins: Gm, Am, Em and Km allotypes. Exp Clin Immunogenet 1989; 6:7-17; PMID:2698222
9. Kumpel BM, Wiener E, Urbaniak SJ, Bradley BA. Human monoclonal anti-D antibodies. II. The relationship between IgG subclass, Gm allotype and Fc mediated function. Br J Haematol 1989; 71:415-20; PMID:2539182; http://dx.doi.org/10.1111/j.1365-2141.1989.tb04300.x
10. Nimmerjahn F, Ravetch JV. Translating basic mechanisms of IgG effector activity into next generation cancer therapies. Cancer Immun 2012; 12:13; PMID:22896758
11. Jefferis R. Isotype and glycoform selection for antibody therapeutics. Arch Biochem Biophys 2012; 526:159-66; PMID:22465822; http://dx.doi.org/10.1016/ j.abb.2012.03.021
12. Ackerman ME, Crispin M, Yu X, Baruah K, Boesch AW, Harvey DJ, Dugast AS, Heizen EL, Ercan A, Choi I, et al. Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity. J Clin Invest 2013; 123:2183-92; PMID:23563315; http://dx.doi.org/10.1172/JCI65708
13. Hess C, Winkler A, Lorenz AK, Holecska V, Blanchard V, Eiglmeier S, Schoen AL, Bitterling J, Stoehr AD, Petzold D, et al. T cell-independent B cell activation induces immunosuppressive sialylated IgG antibodies. J Clin Invest 2013; 123:3788-96; PMID:23979161; http://dx.doi.org/10.1172/JCI65938
14. Rombouts Y, Ewing E, van de Stadt LA, Selman MH, Trouw LA, Deelder AM, Huizinga TW, Wuhrer M, van Schaardenburg D, Toes RE, et al. Anti-citrullinated protein antibodies acquire a proinflammatory Fc glycosylation phenotype prior to the onset of rheumatoid arthritis. Ann Rheum Dis 2013; (Forthcoming); PMID:24106048; http://dx.doi.org/10.1136/annrheumdis-2013-203565
15. Bondt A, Selman MH, Deelder AM, Hazes JM, Willemsen SP, Wuhrer M, Dolhain RJ. Association between galactosylation of immunoglobulin G and improvement of rheumatoid arthritis during pregnancy is independent of sialylation. J Proteome Res 2013; 12:4522-31; PMID:24016253; http://dx.doi.org/10.1021/pr400589m
16. Ackerman ME, Alter G. Opportunities to exploit non-neutralizing HIV-specific antibody activity. Curr HIV Res 2013; 11:365-77; PMID:24191934; http://dx.doi.org/10.2174/1570162X113116660058
17. Raghavan M, Chen MY, Gastinel LN, Bjorkman PJ. Investigation of the interaction between the class I MHC-related Fc receptor and its immunoglobulin G ligand. Immunity 1994; 1:303-15; PMID:7889418; http://dx.doi.org/10.1016/1074- 7613(94)90082-5
18. Anthony RM, Wermeling F, Karlsson MC, Ravetch JV. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci U S A 2008; 105:19571-8; PMID:19036920; http://dx.doi.org/10.1073/pnas. 0810163105
19. Wilson TJ, Fuchs A, Colonna M. Cutting edge: human FcRL4 and FcRL5 are receptors for IgA and IgG. J Immunol 2012; 188:4741-5; PMID:22491254; http://dx.doi.org/10.4049/jimmunol.1102651
20. Wilson TJ, Gilfillan S, Colonna M. Fc receptor-like A associates with intracellular IgG and IgM but is dispensable for antigen-specific immune responses. J Immunol 2010; 185:2960-7; PMID:20668221; http://dx.doi.org/10.4049/ jimmunol.1001428
21. Arnold JN, Dwek RA, Rudd PM, Sim RB. Mannan binding lectin and its interaction with immunoglobulins in health and in disease. Immunol Lett 2006; 106:103-10; PMID:16814399; http://dx.doi.org/10.1016/j.imlet.2006.05.007
22. Keeble AH, Khan Z, Forster A, James LC. TRIM21 is an IgG receptor that is structurally, thermodynamically, and kinetically conserved. Proc Natl Acad Sci U S A 2008; 105:6045-50; PMID:18420815; http://dx.doi.org/10.1073/pnas. 0800159105
23. Dong X, Storkus WJ, Salter RD. Binding and uptake of agalactosyl IgG by mannose receptor on macrophages and dendritic cells. J Immunol 1999; 163:5427-34; PMID:10553068
24. Karsten CM, Pandey MK, Figge J, Kilchenstein R, Taylor PR, Rosas M, McDonald JU, Orr SJ, Berger M, Petzold D, et al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcγRIIB and dectin-1. Nat Med 2012; 18:1401-6; PMID:22922409; http://dx.doi.org/10.1038/nm. 2862
25. Lu J, Marjon KD, Mold C, Du Clos TW, Sun PD. Pentraxins and Fc receptors. Immunol Rev 2012; 250:230-8; PMID:23046133; http://dx.doi.org/10.1111/j.1600- 065X.2012.01162.x
26. Stemerding AM, Köhl J, Pandey MK, Kuipers A, Leusen JH, Boross P, Nederend M, Vidarsson G, Weersink AY, van de Winkel JG, et al. Staphylococcus aureus formyl peptide receptor-like 1 inhibitor (FLIPr) and its homologue FLIPr-like are potent FcγR antagonists that inhibit IgG-mediated effector functions. J Immunol 2013; 191:353-62; PMID:23740955; http://dx.doi.org/10.4049/ jimmunol.1203243
27. Bruhns P, Iannascoli B, England P, Mancardi DA, Fernandez N, Jorieux S, Daëron M. Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood 2009; 113:3716-25; PMID:19018092; http://dx.doi.org/10.1182/blood-2008-09-179754
28. Warncke M, Calzascia T, Coulot M, Balke N, Touil R, Kolbinger F, Heusser C. Different adaptations of IgG effector function in human and nonhuman primates and implications for therapeutic antibody treatment. J Immunol 2012; 188:4405-11; PMID:22461693; http://dx.doi.org/10.4049/jimmunol.1200090
29. Brüggemann M, Williams GT, Bindon CI, Clark MR, Walker MR, Jefferis R, Waldmann H, Neuberger MS. Comparison of the effector functions of human immunoglobulins using a matched set of chimeric antibodies. J Exp Med 1987; 166:1351-61; PMID:3500259; http://dx.doi.org/10.1084/jem.166.5.1351
30. Wasyl Z, Luchter E, Bielanski W Jr. Determination of the effective radius of protein molecules by thin-layer gel filtration. Biochim Biophys Acta 1971; 243:11-8; PMID:4107733; http://dx.doi.org/10.1016/0005-2795(71)90031-6
31. Moore GL, Chen H, Karki S, Lazar GA. Engineered Fc variant antibodies with enhanced ability to recruit complement and mediate effector functions. MAbs 2010; 2:181-9; PMID:20150767; http://dx.doi.org/10.4161/mabs.2.2.11158
32. Richards JO, Karki S, Lazar GA, Chen H, Dang W, Desjarlais JR. Optimization of antibody binding to FcgammaRIIa enhances macrophage phagocytosis of tumor cells. Mol Cancer Ther 2008; 7:2517-27; PMID:18723496; http://dx.doi.org/10.1158/1535-7163.MCT-08-0201
33. Tao MH, Morrison SL. Studies of aglycosylated chimeric mouse-human IgG. Role of carbohydrate in the structure and effector functions mediated by the human IgG constant region. J Immunol 1989; 143:2595-601; PMID:2507634
34. Pound JD, Lund J, Jefferis R. Aglycosylated chimaeric human IgG3 can trigger the human phagocyte respiratory burst. Mol Immunol 1993; 30:233-41; PMID:8381917; http://dx.doi.org/10.1016/0161-5890(93)90052-D
35. Nesspor TC, Raju TS, Chin CN, Vafa O, Brezski RJ. Avidity confers FcγR binding and immune effector function to aglycosylated immunoglobulin G1. J Mol Recognit 2012; 25:147-54; PMID:22407978; http://dx.doi.org/10.1002/ jmr.2155
36. Li Y, Tao SC, Bova GS, Liu AY, Chan DW, Zhu H, Zhang H. Detection and verification of glycosylation patterns of glycoproteins from clinical specimens using lectin microarrays and lectin-based immunosorbent assays. Anal Chem 2011; 83:8509-16; PMID:21975078; http://dx.doi.org/10.1021/ac201452f
37. Baruah K, Bowden TA, Krishna BA, Dwek RA, Crispin M, Scanlan CN. Selective deactivation of serum IgG: a general strategy for the enhancement of monoclonal antibody receptor interactions. J Mol Biol 2012; 420:1-7; PMID:22484364; http://dx.doi.org/10.1016/j.jmb.2012.04.002
38. Bowden TA, Baruah K, Coles CH, Harvey DJ, Yu X, Song BD, Stuart DI, Aricescu AR, Scanlan CN, Jones EY, et al. Chemical and structural analysis of an antibody folding intermediate trapped during glycan biosynthesis. J Am Chem Soc 2012; 134:17554-63; PMID:23025485; http://dx.doi.org/10.1021/ja306068g
39. Shibata-Koyama M, Iida S, Misaka H, Mori K, Yano K, Shitara K, Satoh M. Nonfucosylated rituximab potentiates human neutrophil phagocytosis through its high binding for FcgammaRIIIb and MHC class II expression on the phagocytotic neutrophils. Exp Hematol 2009; 37:309-21; PMID:19218011; http://dx.doi.org/10. 1016/j.exphem.2008.11.006
40. Zhou Q, Shankara S, Roy A, Qiu H, Estes S, McVie-Wylie A, Culm-Merdek K, Park A, Pan C, Edmunds T. Development of a simple and rapid method for producing non-fucosylated oligomannose containing antibodies with increased effector function. Biotechnol Bioeng 2008; 99:652-65; PMID:17680659; http://dx.doi.org/ 10.1002/bit.21598
41. McGreal EP, Rosas M, Brown GD, Zamze S, Wong SY, Gordon S, Martinez-Pomares L, Taylor PR. The carbohydrate-recognition domain of Dectin-2 is a C-type lectin with specificity for high mannose. Glycobiology 2006; 16:422-30; PMID:16423983; http://dx.doi.org/10.1093/glycob/cwj077
42. Kogelberg H, Tolner B, Sharma SK, Lowdell MW, Qureshi U, Robson M, Hillyer T, Pedley RB, Vervecken W, Contreras R, et al. Clearance mechanism of a mannosylated antibody-enzyme fusion protein used in experimental cancer therapy. Glycobiology 2007; 17:36-45; PMID:17000699; http://dx.doi.org/10.1093/glycob/ cwl053
43. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000; 100:587-97; PMID:10721995; http://dx.doi.org/10.1016/ S0092-8674(00)80694-7
44. Van Patten SM, Hughes H, Huff MR, Piepenhagen PA, Waire J, Qiu H, Ganesa C, Reczek D, Ward PV, Kutzko JP, et al. Effect of mannose chain length on targeting of glucocerebrosidase for enzyme replacement therapy of Gaucher disease. Glycobiology 2007; 17:467-78; PMID:17251309; http://dx.doi.org/10.1093/ glycob/cwm008
45. Franco A, Damdinsuren B, Ise T, Dement-Brown J, Li H, Nagata S, Tolnay M. Human Fc receptor-like 5 binds intact IgG via mechanisms distinct from those of Fc receptors. J Immunol 2013; 190:5739-46; PMID:23616577; http://dx.doi.org/10. 4049/jimmunol.1202860
46. Yu X, Vasiljevic S, Mitchell DA, Crispin M, Scanlan CN. Dissecting the molecular mechanism of IVIg therapy: the interaction between serum IgG and DC-SIGN is independent of antibody glycoform or Fc domain. J Mol Biol 2013; 425:1253-8; PMID:23416198; http://dx.doi.org/10.1016/j.jmb.2013.02.006
47. Käsermann F, Boerema DJ, Rüegsegger M, Hofmann A, Wymann S, Zuercher AW, Miescher S. Analysis and functional consequences of increased Fabsialylation of intravenous immunoglobulin (IVIG) after lectin fractionation. PLoS One 2012; 7:e37243; PMID:22675478; http://dx.doi.org/10.1371/journal.pone. 0037243
48. Bayry J, Bansal K, Kazatchkine MD, Kaveri SV. DC-SIGN and alpha2,6-sialylated IgG Fc interaction is dispensable for the anti-inflammatory activity of IVIg on human dendritic cells. Proc Natl Acad Sci U S A 2009; 106:E24, author reply E25; PMID:19237553; http://dx.doi.org/10.1073/pnas. 0900016106
49. Crispin M, Yu X, Bowden TA. Crystal structure of sialylated IgG Fc: implications for the mechanism of intravenous immunoglobulin therapy. Proc Natl Acad Sci U S A 2013; 110:E3544-6; PMID:23929778; http://dx.doi.org/10.1073/pnas. 1310657110
50. Sondermann P, Pincetic A, Maamary J, Lammens K, Ravetch JV. General mechanism for modulating immunoglobulin effector function. Proc Natl Acad Sci U S A 2013; 110:9868-72; PMID:23697368; http://dx.doi.org/10.1073/pnas.1307864110
51. Nimmerjahn F, Ravetch JV. Analyzing antibody-Fc-receptor interactions. Methods Mol Biol 2008; 415:151-62; PMID:18370153
52. Barouch DH, Yang ZY, Kong WP, Korioth-Schmitz B, Sumida SM, Truitt DM, Kishko MG, Arthur JC, Miura A, Mascola JR, et al. A human T-cell leukemia virus type 1 regulatory element enhances the immunogenicity of human immunodeficiency virus type 1 DNA vaccines in mice and nonhuman primates. J Virol 2005; 79:8828-34; PMID:15994776; http://dx.doi.org/10.1128/JVI.79.14.8828-8834.2005
53. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 2010; 329:856-61; PMID:20616233; http://dx.doi.org/10.1126/science.1187659
54. Orcutt KD, Ackerman ME, Cieslewicz M, Quiroz E, Slusarczyk AL, Frangioni JV, Wittrup KD. A modular IgG-scFv bispecific antibody topology. Protein Eng Des Sel 2010; 23:221-8; PMID:20019028; http://dx.doi.org/10.1093/protein/gzp077
55. Feng Y, Gong R, Dimitrov DS. Design, expression and characterization of a soluble single-chain functional human neonatal Fc receptor. Protein Expr Purif 2011; 79:66-71; PMID:21453773; http://dx.doi.org/10.1016/j.pep.2011.03.012
56. Brown EP, Licht AF, Dugast AS, Choi I, Bailey-Kellogg C, Alter G, Ackerman ME. High-throughput, multiplexed IgG subclassing of antigen-specific antibodies from clinical samples. J Immunol Methods 2012; 386:117-23; PMID:23023091; http://dx.doi.org/10.1016/j.jim.2012.09.007