Antibody therapeutics: Isotype and glycoform selection

Expert Opinion on Biological Therapy

Volumn 7, Issue 9, 2007, Pages 1401-1413

  Jefferis, Roy ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

ADCC; Aglycosylated antibody; Bisecting N acetylglucosamine; CDC; Effector functior; Fucosylation; Galactosylation; Human IgG subclass (1,2,3,4); IgG fab glycosylation; IgG Fc glycosylation; IgG Fc receptor; Pharmacokinetic; Therapeutic antibody

Indexed keywords

ADALIMUMAB; ALEMTUZUMAB; BASILIXIMAB; BETA INTERFERON; BEVACIZUMAB; CD3 ANTIBODY; CETUXIMAB; CYTOTOXIC AGENT; DACLIZUMAB; EFALIZUMAB; ETANERCEPT; FC RECEPTOR; GEMTUZUMAB OZOGAMICIN; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4; INFLIXIMAB; MONOCLONAL ANTIBODY; NATALIZUMAB; OMALIZUMAB; PALIVIZUMAB; PANITUMUMAB; RITUXIMAB; TGN 1421; TRASTUZUMAB; UNCLASSIFIED DRUG; VECTIBIX; ZENOPAX;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN ANTIBODY COMPLEX; APOPTOSIS; B LYMPHOCYTE; BINDING AFFINITY; BIOLOGICAL ACTIVITY; CANCER CELL CULTURE; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL EFFECTIVENESS; CLINICAL TRIAL; COMBINATION CHEMOTHERAPY; COMPLEMENT DEPENDENT CYTOTOXICITY; CROHN DISEASE; CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; GLYCOSYLATION; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; KIDNEY GRAFT REJECTION; MOLECULAR INTERACTION; MONOTHERAPY; MULTIPLE SCLEROSIS; NEUROLOGICAL COMPLICATION; NONHODGKIN LYMPHOMA; NONHUMAN; PROTEIN ENGINEERING; PROTEIN FUNCTION; REVIEW; RHEUMATOID ARTHRITIS; TREATMENT RESPONSE; TUBERCULOSIS; UNSPECIFIED SIDE EFFECT; X RAY CRYSTALLOGRAPHY;

ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; FUCOSE; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN ISOTYPES; NEOPLASMS; RECEPTORS, IGG;

EID: 34748865088     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.7.9.1401     Document Type: Review

References (95)

1. REICHERT JM, ROSENDWEIG CJ, FADEN LB et al.: Monoclonal antibody successes in the clinic. Nat. Biotechnol. (2005) 23:1073-1078.
2. CARTER PJ: Potent antibody therapeutics by design. Nat. Rev. (2006) 6:343-357.
3. SATOH M, IIDA S, SHITARA K: Non-fucosylated therapeutic antibodies as next-generation therapeutic antibodies. Expert Opin. Biol. Ther. (2006) 6:1161-1173.
4. BAKER M: Upping the ante on antibodies. Nat. Biotechnol. (2005) 23:1065-1072.
5. GLENNIE MJ, VAN DE WINKEL JG: Renaissance of cancer therapeutic antibodies. Drug Discov. Today (2003) 8:503-510.
6. MIRIK GR, BRADT BM, DENARDO SJ, DENARDO GL: A review of human anti-globulin antibody (HAGA, HAMA, HACA, HAHA) responses to monoclonal antibodies. Not four letter words. Q. J. Nucl. Med. Mol. Imaging (2004) 48:251-257.
7. KLITGAARD JL, COLJEE VJ, ANDERSEN PS et al.: Reduced susceptibility of recombinant polyclonal antibodies to inhibitory anti-variable domain antibody responses. J. Immunol. (2006) 177:3782-3790.
8. DEISENHOFER J: Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9- and 2.8-Å resolution. Biochemistry (1981) 20:2361-2370.
9. WOOF JM, BURTON DR: Human antibody-Fc receptor interactions illuminated by crystal structures. Nat. Rev. Immunol. (2004) 4:89-99.
10. NEZLIN R, GHETIE V: Interactions of immunoglobulins outside the antigen-combining site. Adv. Immunol. (2004) 82:155-215.
11. VAN SORGE NM, VAN DER POL WL, VAN DE WINKEL JG: FcγR polymorphisms: implications for function, disease susceptibility and immunotherapy. Tissue Antigens (2003) 61:189-202.
12. NIMMERJAHN F, RAVETCH JV: Fcγ receptors: old friends and new family members. Immunity (2006) 24:19-28.
13. JEFFERIS R: Glycosylation of recombinant antibody therapeutics. Biotechnol. Progress (2005) 21:11-16.
14. SINCLAIR AM, ELLIOTT S: Glycoengineering: the effect of glycosylation on the properties of therapeutic proteins. J. Pharm. Sci. (2005) 94:1626-1635.
15. SHIELDS RL, LAI J, KECK, R et al.: Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human FcγRIII and antibody-dependent cellular toxicity. J. Biol. Chem. (2002) 277:26733-26740.
16. SHINKAWA T, NAKAMURA K, YAMANE N et al.: The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J. Biol. Chem. (2003) 278:3466-3473.
17. NIWA R, NATSUME A, UEHARA A et al.: IgG subclass-independent improvement of antibody-dependent cellular cytotoxicity by fucose removal from Asn297-linked oligosaccharides. J. Immunol. Methods (2005) 306:151-160.
18. FERRARA C, BRUNKER P, MOSER S et al.: Modulation of therapeutic antibody effector functions by glycosylation engineering: influence of Golgi enzyme localization domain and co-expression of heterologous β1, 4-N-acetylglucosaminyltransferase III and Golgi α-mannosidase II. Biotechnol. Bioeng. (2006) 93:851-861.
19. MIMURA Y, SONDERMANN P, GHIRLANDO R et al.: The role of oligosaccharide residues of IgG1-Fc in Fcγllb binding. J. Biol. Chem. (2001) 276:45539-45547.
20. KRAPP S, MIMURA Y, JEFFERIS R et al.: Structural analysis of human IgG glycoforms reveals a correlation between oligosaccharide content, structural integrity and Fcγ-receptor affinity. J. Mol. Biol. (2003) 325:979-989.
21. JONES AJ, PAPAC DI, CHIN EH et al.: Selective clearance of glycoforms of a complex glycoprotein pharmaceutical caused by terminal N-acetylglucosamine is similar in humans and cynomolgus monkeys. Glycobiology (2007) 17:529-540.
22. ALETE DE, RACHER AJ, BIRCH JR et al.: Proteomic analysis of enriched microsomal fractions from GS-NS0 murine myeloma cells with varying secreted recombinant monoclonal antibody productivities. Proteomics (2005) 18:4689-4704.
23. QIAN J, LIU T, YANG L et al.: Structural characterization of N-linked oligosaccharides on monoclonal antibody cetuximab by the combination of orthogonal matrix-assisted laser desorption/ionization hybrid quadrupole-quadrupole time-of-flight tandem mass spectrometry and sequential enzymatic digestion. Anal. Biochem. (2007) 364:8-18.
24. GARRED P, MICHAELSEN TE, AASE A: The IgG subclass pattern of complement activation depends on epitope density and antibody and complement concentration. Scand. J. Immunol. (1989) 30:379-382.
25. MICHAELSEN TE, GARRED P, AASE A: Human IgG subclass pattern of inducing complement-mediated cytolysis depends on antigen concentration and to a lesser extent on epitope patchiness, antibody affinity and complement concentration. Eur. J. Immunol. (1991) 21:11-16.
26. LUCISANO VALIM YM, LACHMANN PJ: The effect of antibody isotype and antigenic epitope density on the complement-fixing activity of immune complexes: a systematic study using chimaeric anti-NIP antibodies with human Fc regions. Clin. Exp. Immunol. (1991) 84:1-8.
27. VOICE JK, LACHMANN PJ: Neutrophil Fc γ and complement receptors involved in binding soluble IgG immune complexes and in specific granule release induced by soluble IgG immune complexes. Eur. J. Immunol. (1997) 27:2514-2523.
28. WATIER H: Variability factors in the clinical response to recombinant antibodies and IgG Fc-containing fusion proteins. Expert Opin. Biol. Ther. (2005) 5(Suppl. 1):S1-S8.
29. MARCUS R, HAGENBEEK A: The therapeutic use of rituximab in non-Hodgkin's lymphoma. Eur. J. Haematol. Suppl. (2007) 67:5-14.
30. LIFELY MR, HALE G, BOYSE S: Glycosylation and biological activity of CAMPATH-1H expressed in different cell lines and grown under different culture conditions. Glycobiology (1995) 5:813-822.
31. UMANA P, JEAN-MAIRET J, MOUDRY R et al.: Engineered glycoforms of an anti-neuroblastoma. IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat. Biotechnol. (1999) 17:176-180.
32. DAVIES J, JIANG L, LABARRE MJ et al.: Expression of GTIII in a recombinant anti-CD20 CHO production cell line: expression of antibodies of altered glycoforms leads to an increase in ADCC thro' higher affinity for FcRIII. Biotech. Bioeng. (2001) 74:288-294.
33. YMANE-OHUKI N, KINOSHITA S, INOUE-URAKUBO M et al.: Establishment of FUT8 knockout Chinese hamster ovary cells: an ideal host cell line for producing completely defucosylated antibodies with enhanced antibody-dependent cellular cytotoxicity. Biotechnol. Bioeng. (2004) 87:614-622.
34. PREITHNER S, ELM S, LEPPOLD S et al.: High concentrations of therapeutic IgG1 antibodies are needed to compensate for the inhibition of ADCC by excess endogenous immunoglobulin G. Mol. Immunol. (2006) 43:1183-1193.
35. NECHANSKY A, SCHUSTER M, JOST W et al.: Compensation of endogenous IgG mediated inhibition of antibody-dependent cellular cytotoxicity by glyco-engineering of therapeutic antibodies. Mol. Immunol. (2007) 44:1815-1817.
36. IIDA S, MISAKA H, INOUE M et al.: Non-fucosylated therapeutic IgG antibody can evade the inhibitory effect of serum IgG on antibody-dependent cellular cytotoxicity through its binding to FcγRIIIa. Clin. Cancer Res. (2006) 12:2879-2887.
37. SUZUKI E, NIWA R, SAJI SA et al.: Nonfucosylated anti-HER2 antibody augments antibody-dependent cellular cytotoxicity in breast cancer patients. Clin. Cancer Res. (2007) 13:1875-1882.
38. ANDERSON CL: Human IgG Fc receptors. Clin. Immunol. Immunopathol. (1989) 53:S63-S71.
39. KOENE HR, KLEIJER M, ALGRA J et al.: FcγRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell FcγRIIIa, independently of the FcγRIIIa-48L/R/H phenotype. Blood (1997) 90:1109-1114.
40. CARTRON G, DACHEUX L, SALLES G et al.: Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcγRIIIa gene. Blood (2002) 99:754-758.
41. ANOLIK JH, CAMPBELL D, FELGAR RE et al.: The relationship of FcγRIIIa genotype to degree of B cell depletion by Rituximab in the treatment of systemic lupus erythematosus. Arthritis Rheum. (2003) 48:455-459.
42. LOUIS E, EL GHOUL Z, VERMEIRE S et al.: Association between polymorphism in IgG FcγIIIa coding gene and biological response to Infliximab in Crohn's disease. Aliment. Pharmacol. Ther. (2004) 19:511-519.
43. MIESCHER S, SPYCHER MO, AMSTUTZ H et al.: A single recombinant anti-RhD IgG prevents RhD immunization: association of RhD-positive red blood cell clearance rate with polymorphisms in the FcγRIIA and FcγIIIA genes. Blood (2004) 103:4028-4035.
44. LIN TS, FLINN IW, MODALI R et al.: FCGR3A and FCGR2A polymorphisms may not correlate with response to Alemtuzumab in chronic lymphocytic leukemia. Blood (2005) 105:289-291.
45. TEELING JL, FRENCH RR, CRAGG MS et al.: Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin lymphomas. Blood (2004) 104:1793-1800.
46. CRAGGS MS, WALSHE CA, IVANOVAO et al.: The biology of CD20 and its potential as a target for mAb therapy. Curr. Dir. Autoimmun. (2005) 8:140-174.
47. TEELING JL, MACKUS WJ, WIEGMAN LJ et al.: The biological activity of human CD20 monoclonal antibodies is linked to unique epitopes on CD20. J. Immunol. (2006) 177:362-371.
48. CARDELLI PM, QUIN M, BUCKMAN D et al.: Binding to CD20 by anti-B1 antibody or F(ab')(2) is sufficient for induction of apoptosis in B-cell lines. Cancer Immunol. Immunother. (2002) 51:15-24
49. LIU Y, ZHENG M, LAI Z et al.: Inhibition of human B-cell lymphoma by an anti-CD20 antibody and its chimeric F(ab')2 fragment via induction of apoptosis. Cancer Lett. (2004) 205:143-153
50. LUND J, TAKAHASHI N, POUND J et al.: Multiple interactions of IgG with its core oligosaccharide can modulate recognition by complement and human FcyRI and influence the synthesis of its oligosaccharide chains. J. Immunol. (1996) 157:4963-4969.
51. SHIELDS RL, NAMENUK AK, HONG K et al.: High resolution mapping of the binding site on human IgG1 for FcγRI, FcγRII, FcγRIII, and FcRn and design of IgG1 variants with improved binding to the FcγR. J. Biol. Chem. (2001) 276:6591-6604.
52. LAZAR GA, DANG W, KARKI S et al.: Engineered antibody Fc variants with enhanced effector function. Proc. Natl. Acad. Sci. USA (2006) 103:4005.
53. DALL'ACQUA WF, COOK KE, DAMSCHRODER MM: Modulation of the effector functions of a human IgG1 through engineering of its hinge region. J. Immunol. (2006) 177:1129-1138.
54. VERI MC, GORLATOV S, LI H et al.: Monoclonal antibodies capable of discriminating the human inhibitory Fcγ-receptor IIB (CD32B) from the activating Fcγ-receptor IIA (CD32A): biochemical, biological and functional characterization. Immunology (2007).
55. SARVAS H, RAUTONEN H, KAYHTY M et al.: Effect of Gm allotypes on IgG2 antibody responses and IgG2 concentrations in children and adults. Int. Immunol. (1990) 2:317-322.
56. PAN Q, HAMMARSTROM L: Molecular basis of IgG subclass deficiency. Immunol. Rev. (2000) 178:99-110.
57. JONSSON G, OXELIUS VA, TRUEDSSON L et al.: Homozygosity for the IgG2 subclass allotype G2M(n) protects against severe infection in hereditary C2 deficiency. J. Immunol. (2006) 77:722-728.
58. SALTZ L, EASTLEY C, KIRKPATRICK P: Panitumumab. Nat. Rev. Drug Discov. (2006) 5:987-988.
59. PARREN PW, WARMERDAM PA, BOEIJE LC et al.: On the interaction of IgG subclasses with the low affinity FcγRIIa (CD32) on human monocytes, neutrophils, and platelets. Analysis of a functional polymorphism to human IgG2. J. Clin. Invest. (1992) 90:1537-1546.
60. RODRIGUEZ ME, VAN DER POL W-L, SANDERS LAM: Crucial role of FcγRIIa (CD32) in assessment of functional anti-Streptococcus pneumoniae antibody activity in human sera. J. Infect. Dis. (1999) 179:423-433.
61. LAI Z, KIMMEL R, PETERSEN S et al.: Multi-vaient human monoclonal antibody preparation against Pseudomonas aeruginosa derived from transgenic mice containing human immunoglobulin loci is protective against fatal pseudomonas sepsis caused by multiple serotypes. Vaccine (2005) 23:3264-3271.
62. PENICHETT ML, DELA CRUZ JS, SHIN SU, MORRISON SL: A recombinant IgG3-(IL-2) fusion protein for the treatment of human HER2/neu expressing tumors. Hum. Antibodies (2001) 10:43-49.
63. HELQUERA G, RODRIGUEZ JA, PENICHET ML: Cytokines fused to antibodies and their combinations as therapeutic agents against different peritoneal HER2/neu expressing tumors. Mol. Cancer Ther. (2006) 5:1029-1040.
64. MICHAESEN TE, BREKKE OH, AASE A et al.: One disulfide bond in front of the second heavy chain constant region is necessary and sufficient for effector functions of human IgG3 without a genetic hinge. Proc. Natl. Acad. Sci. USA (1994) 91:9243-9247.
65. BREKKE OH, MICHAELSEN TE, SANDLIE I: The structural requirements for complement activation by IgG: does it hinge on the hinge? Immunol. Today (1995) 16:85-90.
66. JEFFERIS R: Immunoglobulins: Allotypes. In: Encyclopaedia of Immunology. 2nd Edition, Roitt IM, Delves PJ (Eds), Saunders, Florida, USA (1998).
67. AALBERSE RC, SHCUUMANN J: IgG4 breaking the rules. Immunology (2002) 105:9-19.
68. SMALLING R, FOOT M, MOLINEUX G et al.: Drug-induced and antibody-mediated pure red cell aplasia: a review of literature and current knowledge. Biotechnol. Annu. Rev. (2004) 10:237-250.
69. AMICO D, BARBUI AM, ERBA E et al.: Differential response of human acute myeloid leukemia cells to Gemtuzumab ozogamicin in vitro: role of Chk1 and Chk2 phosphorylation and caspase 3. Blood (2003) 101:4589-4597.
70. 4-integrin antagonism in the treatment of multiple sclerosis. Expert Opin. Biol. Ther. (2007) 7:123-136.
71. BRUGGEMANN M, WILLIAMS GT, BINDON CL et al.: Comparison of the effector function of human immunoglobulins using a matched set of chimeric antibodies. J. Exp. Med. (1987) 166:1351-1361.
72. HOLLAND M, HEWINS P, GOODALL M et al.: Anti-neutrophil cytoplasmic antibody IgG subclasses in Wegener's granulomatosis: a possible pathogenic role for the IgG4 subclass. Clin. Exp. Immunol. (2004) 138:183-192.
73. EHLERS S: Tumor necrosis factor and its blockade in granulomatous infections: differential modes of action of infliximab and etanercept? Clin. Infect. Dis. (2005) 41 (Suppl. 3):S199-S203.
74. DUBCENCO E, OTTAWAY CA, CHEN DL, BAKER JP: Neurological symptoms suggestive of demyelisation in Crohn's disease after infliximab therapy. Eur. J. Gastroenterol. Hepatol. (2006) 18:565-566.
75. COLE MS, ANASETTI C, TSO JY: Human IgG2 variants of chimeric anti-CD3 are non-mitogenic to T cells. J. Immunol. (1997) 159:3613-3621.
76. SONDERMANN P, HUBER R, OOSTHUIZEN V, JACOB U: The 3.2-A crystal structure of the human IgG1 Fc -FcγRIII complex. Nature (2000) 406:267-273.
77. RADAEV S, MOTYKA S, FRIDMAN WH et al.: The structure of human type FcγIII receptor in complex with Fc. J. Biol. Chem. (2001) 276:16469-16477.
78. MARTIN WL, WEST AP, GAN L, BJORKMAN PJ: Crystal structure at 2.8 A of an FcRn/heterodimeric Fc complex: mechanism of pH-dependent binding. Mol. Cell (2001) 7:867-877.
79. HINTON PR, XIONG JM, JOHLFS MG et al.: An engineered human IgG1 antibody with longer serum half-life. J. Immunol. (2006) 176:346-356.
80. VACCARO C, ZHOU J, OBER RJ, WARD ES: Engineering the Fc region of immunoglobulin G to modulate in vivo antibody levels. Nat. Biotechnol. (2005) 23:1283-1288.
81. BITONTI AJ, DUMONT JA: Pulmonary administration of therapeutic proteins using an immunoglobulin transport pathway. Adv. Drug Deliv. Rev. (2006) 58:1106-1118.
82. YOUINGS A, CHANG SC, DWEK RA et al.: Site-specific glycosylation of human immunoglobulin G is altered in four rheumatoid arthritis patients. Biochem. J. (1996) 314:621-630.
83. HOLLAND M, YAGI H, TAKAHASHI N et al.: Differential glycosylation of polyclonal IgG, IgG-Fc and IgG-Fab isolated from the sera of patients with ANCA associated systemic vasculitis. Biochim Biophys. Acta (2006) 1760:669-677.
84. HUANG L, BIOLOSI S, BALES KR, KUCHIBHOTLA U: Impact of variable domain glycosylation on antibody clearance: an LC/MS characterization. Anal Biochem. (2006) 349:197-207.
85. ANDERSEN DC, REILLY DE: Production technologies for monoclonal antibodies and their fragments. Curr. Opin. Biotechnol. (2000) 15:456-462.
86. GOMORD V, CHABERLAIN P, JEFFERIS R, FAYE L: Biopharmaceutical production in plants: problems, solutions and opportunities. Trends Biotechnol. (2005) 23:559-565.
87. FITCHETTE AC, DINH OT, FAYE L, BARDOR M: Plant proteomics and glycosylation. Methods Mol. Biol. (2007) 355:317-342.
88. COX KM, STERLING JD, REGAN JT et al.: Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor. Nat. Biotechnol. (2006) 24:1591-1597.
89. KAPRIVOVA A, STEMMER C, ALTMANN F et al.: Targeted knockouts of Physcomitrella lacking plant-specific immunogenic N-glycans. Plant. Biotechnol. J. (2004) 2:517-523.
90. STRASSER R, ALTMANN F, MACH L et al.: Generation of Arabidopsis thaliana plants with complex N-glycans lacking β1,2-linked xylose and core αl,3-linked fucose. FEBS Lett. (2004) 561:132-136.
91. HILL DR, AIMILLER JJ, SHIX, JARVIS DL: Isolation and analysis of a baculovirus vector that supports recombinant glycoprotein sialylation by SfSWT- cells cultured in serum-free medium. Biotechnol. Bioeng. (2006) 95:37-47.
92. HAMILTON SR, DAVIDSON RC, SETHURAMAN N et al.: Humanization of yeast to produce complex terminally sialylated glycoproteins. Science (2006) 313:1441-1443.
93. GEORGIOU G, SEGATORI L: Preparative expression of secreted proteins in bacteria: status report and future prospects. Curr. Opin. Biotechnol. (2005) 16:538-545.
94. WACKER M, FELDMAN MF, CALLWAERT N et al.: Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems. Proc. Natl. Acad. Sci. USA (2006) 103:7088-7093.
95. WONG JB, SINGH G, KAVANAUGH A: Estimating the cost-effectiveness of 54 weeks of infliximab for rheumatoid arthritis. Am. J. Med. (2002) 113:400-408.