Processing of complex N-glycans in IgG Fc-region is affected by core fucosylation

mAbs

Volumn 7, Issue 5, 2015, Pages 863-870

  Castilho, Alexandra ^a   Gruber, Clemens ^a   Thader, Andreas ^a   Oostenbrink, Chris ^a   Pechlaner, Maria ^a   Steinkellner, Herta ^a   Altmann, Friedrich ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

Bisected glycans; Cetuximab; Core fucosylation; Glycan modelling; IgG; Nicotiana benthamiana; Sialylation

Indexed keywords

ALPHA 1 3 FUCOSE; ALPHA 1,3 FUCOSYLTRANSFERASE; ALPHA 2,6 SIALYLTRANSFERASE; CETUXIMAB; FC RECEPTOR; FUCOSE; GLYCAN DERIVATIVE; GLYCOPEPTIDE; GLYCOPROTEIN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1; N GLYCAN; OLIGOSACCHARIDE; SIALYLTRANSFERASE; UNCLASSIFIED DRUG; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G; POLYSACCHARIDE;

ARTICLE; ELECTROSPRAY MASS SPECTROMETRY; FUCOSYLATION; GLYCOSYLATION; HEPG2 CELL LINE; HUMAN; INFORMATION PROCESSING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR BIOLOGY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SIALYLATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; MOUSE; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; CETUXIMAB; CRYSTALLOGRAPHY, X-RAY; FUCOSE; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; PROTEIN CONFORMATION;

EID: 84954312231     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.1080/19420862.2015.1053683     Document Type: Article

References (48)

1. Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA. The impact of glycosylation on the biological function and structure of human immunoglobulins. Ann Rev Immunol 2007; 25:21-50; PMID:17029568; http://dx. doi. org/10. 1146/annurev. immunol. 25. 022106. 141702
2. Zauner G, Selman MH, Bondt A, Rombouts Y, Blank D, Deelder AM, Wuhrer M. Glycoproteomic analysis of antibodies. Mol Cell Prot MCP 2013; 12:856-65; PMID:23325769; http://dx. doi. org/10. 1074/mcp. R112. 026005
3. 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
4. Nimmerjahn F, Ravetch JV. Anti-inflammatory actions of intravenous immunoglobulin. Ann Rev Immunol 2008; 26:513-33; PMID:18370923; http://dx. doi. org/ 10. 1146/annurev. immunol. 26. 021607. 090232
5. Shields RL, Lai J, Keck R, O'Connell LY, Hong K, Meng YG, Weikert SH, Presta LG. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. The J Biol Chem 2002; 277:26733-40; PMID:11986321; http://dx. doi. org/10. 1074/jbc. M202069200
6. Ferrara C, Grau S, Jager C, Sondermann P, Brunker P, Waldhauer I, Hennig M, Ruf A, Rufer AC, Stihle M, et al. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Nat Acad Sci U S A 2011; 108:12669-74; PMID:21768335; http://dx. doi. org/10. 1073/ pnas. 1108455108
7. Cartron G, de Guibert S, Dilhuydy MS, Morschhauser F, Leblond V, Dupuis J, Mahe B, Bouabdallah R, Lei G, Wenger M, et al. Obinutuzumab (GA101) in relapsed/refractory chronic lymphocytic leukemia: final data from the phase 1/2 GAUGUIN study. Blood 2014; 124:2196-202; PMID:25143487; http://dx. doi. org/10. 1182/blood-2014-07-586610
8. Qiu X, Wong G, Audet J, Bello A, Fernando L, Alimonti JB, Fausther-Bovendo H, Wei H, Aviles J, Hiatt E, Johnson A, et al. Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 2014; 514:47-53; PMID:25171469
9. Anumula KR. Quantitative glycan profiling of normal human plasma derived immunoglobulin and its fragments Fab and Fc. J Immunol Meth 2012; 382:167-76; PMID:22683540; http://dx. doi. org/10. 1016/j. jim. 2012. 05. 022
10. Stadlmann J, Pabst M, Altmann F. Analytical and functional aspects of antibody sialylation. J Clin Immunol 2010; 30:15-9; PMID:20390325; http://dx. doi. org/ 10. 1007/s10875-010-9409-2
11. Gutierrez G, Malan Borel I, Margni RA. The placental regulatory factor involved in the asymmetric IgG antibody synthesis responds to IL-6 features. J Reprod Immunol 2001; 49:21-32; PMID:11137110; http://dx. doi. org/10. 1016/S0165-0378(00)00074-7
12. Canellada A, Blois S, Gentile T, Margni Idehu RA. In vitro modulation of protective antibody responses by estrogen, progesterone and interleukin-6. Am J Reprod Immunol 2002; 48:334-43; PMID:12516657; http:// dx. doi. org/10. 1034/j. 1600-0897. 2002. 01141. x
13. Huang L, Biolsi S, Bales KR, Kuchibhotla U. Impact of variable domain glycosylation on antibody clearance: an LC/MS characterization. Anal Biochem 2006; 349:197-207; PMID:16360109; http://dx. doi. org/10. 1016/j. ab. 2005. 11. 012
14. Loos A, Steinkellner H. IgG-Fc glycoengineering in non-mammalian expression hosts. Arch Biochem Biophys 2012; 526:167-73; PMID:22634260; http://dx. doi. org/10. 1016/j. abb. 2012. 05. 011
15. Strasser R. Biological significance of complex N-glycans in plants and their impact on plant physiology. Front Plant Sci 2014; 5:363; PMID:25101107; http://dx. doi. org/10. 3389/fpls. 2014. 00363
16. Stadlmann J, Pabst M, Kolarich D, Kunert R, Altmann F. Analysis of immunoglobulin glycosylation by LCESI-MS of glycopeptides and oligosaccharides. Proteomics 2008; 8:2858-71; PMID:18655055; http://dx. doi. org/10. 1002/pmic. 200700968
17. Ayoub D, Jabs W, Resemann A, Evers W, Evans C, Main L, Baessmann C, Wagner-Rousset E, Suckau D, Beck A. Correct primary structure assessment and extensive glyco-profiling of cetuximab by a combination of intact, middle-up, middle-down and bottom-up ESI and MALDI mass spectrometry techniques. MAbs 2013; 5:699-710; PMID:23924801; http://dx. doi. org/ 10. 4161/mabs. 25423
18. Stoger E, Fischer R, Moloney M, Ma JK. Plant molecular pharming for the treatment of chronic and infectious diseases. Ann Rev Plant Biol 2014; 65:743-68; PMID:24579993; http://dx. doi. org/10. 1146/annurevarplant-050213-035850
19. Strasser R, Stadlmann J, Schähs M, Stiegler G, Quendler H, Mach L, Glössl J, Weterings K, Pabst M, et al. Generation of glyco-engineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure. Plant Biotechnol J 2008; 6:392-402; PMID:18346095; http://dx. doi. org/10. 1111/j. 1467-7652. 2008. 00330. x
20. Castilho A, Strasser R, Stadlmann J, Grass J, Jez J, Gattinger P, Kunert R, Quendler H, Pabst M, Leonard R, et al. In planta protein sialylation through overexpression of the respective mammalian pathway. J Biol Chem 2010; 285:15923-30; PMID:20305285; http://dx. doi. org/10. 1074/jbc. M109. 088401
21. Narasimhan S, Freed JC, Schachter H. The effect of a "bisecting" N-acetylglucosaminyl group on the binding of biantennary, complex oligosaccharides to concanavalin A, Phaseolus vulgaris erythroagglutinin (E-PHA), and Ricinus communis agglutinin (RCA-120) immobilized on agarose. Carb Res 1986; 149:65-83; PMID:3731182; http://dx. doi. org/10. 1016/S0008-6215(00)90370-7
22. Umana P, Jean-Mairet J, Moudry R, Amstutz H, Bailey JE. Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nature Biotechnol 1999; 17:176-80; PMID:10052355; http://dx. doi. org/10. 1038/6179
23. Crispin M, Yu X, Bowden TA. Crystal structure of sialylated IgG Fc: implications for the mechanism of intravenous immunoglobulin therapy. Proc Nat Acad Sci U S A 2013; 110:E3544-6; PMID:23929778; http://dx. doi. org/10. 1073/pnas. 1310657110
24. Sturm A, Van Kuik JA, Vliegenthart JF, Chrispeels MJ. Structure, position, and biosynthesis of the high mannose and the complex oligosaccharide side chains of the bean storage protein phaseolin. J Biol Chem 1987; 262:13392-403; PMID:3654619
25. Go EP, Chang Q, Liao HX, Sutherland LL, Alam SM, Haynes BF, Desaire H. Glycosylation site-specific analysis of clade C HIV-1 envelope proteins. J Prot Res 2009; 8:4231-42; PMID:19610667; http://dx. doi. org/ 10. 1021/pr9002728
26. Pabst M, Chang M, Stadlmann J, Altmann F. Glycan profiles of the 27 N-glycosylation sites of the HIV envelope protein CN54gp140. Biol Chem 2012; 393:719-30; PMID:22944675; http://dx. doi. org/10. 1515/hsz-2012-0148
27. Jefferis R, Lund J, Mizutani H, Nakagawa H, Kawazoe Y, Arata Y, Takahashi, N. A comparative study of the N-linked oligosaccharide structures of human IgG subclass proteins. Biol Chem 1990; 268:529-37; PMID:2363690
28. Masuda K, Yamaguchi Y, Kato K, Takahashi N, Shimada I, Arata Y. Pairing of oligosaccharides in the Fc region of immunoglobulin G. FEBS lett 2000; 473:349-57; PMID:10818239; http://dx. doi. org/ 10. 1016/S0014-5793(00)01557-X
29. 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
30. Krapp S, Mimura Y, Jefferis R, Huber R, Sondermann P. Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J Mol Biol 2003; 325:979-89; PMID:12527303; http://dx. doi. org/10. 1016/S0022-2836(02)01250-0
31. Radaev S, Sun PD. Recognition of IgG by Fcgamma receptor. The role of Fc glycosylation and the binding of peptide inhibitors. J Biol Chem 2001; 276:16478-83; PMID:11297533; http://dx. doi. org/10. 1074/jbc. M100351200
32. Lu J, Chu J, Zou Z, Hamacher NB, Rixon MW, Sun PD. Structure of FcgammaRI in complex with Fc reveals the importance of glycan recognition for highaffinity IgG binding. Proc Nat Acad Sci U S A 2015; 112:833-8; PMID:25561553; http://dx. doi. org/ 10. 1073/pnas. 1418812112
33. Sondermann P, Pincetic A, Maamary J, Lammens K, Ravetch JV. General mechanism for modulating immunoglobulin effector function. Proc Nat Acad Sci U S A 2013; 110:9868-72; PMID:23697368; http://dx. doi. org/10. 1073/pnas. 1307864110
34. Ferrara C, Brunker P, Suter T, Moser S, Puntener U, Umana P. Modulation of therapeutic antibody effector functions by glycosylation engineering: influence of Golgi enzyme localization domain and co-expression of heterologous beta1, 4-N-acetylglucosaminyltransferase III and Golgi alpha-mannosidase II. Biotechnol and Bioeng 2006; 93:851-61; PMID:16435400; http://dx. doi. org/10. 1002/bit. 20777
35. Brockhausen I, Schachter H. Glycosyltransferases involved in N-and O-glycan biosynthesis. In: Glycosciences: status and perspectives, eds. H.-J. Gabius aSG, London-Weinheim: Chapman & Hall; 1997:79-113.
36. Frank M, Walker RC, Lanzilotta WN, Prestegard JH, Barb AW. Immunoglobulin G1 Fc domain motions: implications for Fc engineering. J Mol Biol 2014; 426:1799-811; PMID:24522230; http://dx. doi. org/ 10. 1016/j. jmb. 2014. 01. 011
37. Ahmed AA, Giddens J, Pincetic A, Lomino JV, Ravetch JV, Wang LX, Bjorkman PJ. Structural characterization of anti-inflammatory immunoglobulin G Fc proteins. J Mol Biol 2014; 426:3166-79; PMID:25036289; http:// dx. doi. org/10. 1016/j. jmb. 2014. 07. 006
38. Lai B, Hasenhindl C, Obinger C, Oostenbrink C. Molecular dynamics simulation of the crystallizable fragment of IgG1-insights for the design of Fcabs. Intern J Mol Sci 2014; 15:438-55; PMID:24451126; http://dx. doi. org/10. 3390/ijms15010438
39. Pastores GM, Petakov M, Giraldo P, Rosenbaum H, Szer J, Deegan PB, Amato DJ, Mengel E, Tan ES, Chertkoff R, et al. A Phase 3, multicenter, open-label, switchover trial to assess the safety and efficacy of taliglucerase alfa, a plant cell-expressed recombinant human glucocerebrosidase, in adult and pediatric patients with Gaucher disease previously treated with imiglucerase. Blood Cells Mol Dis 2014; 53:253-260; PMID:24950666; http://dx. doi. org/10. 1016/j. bcmd. 2014. 05. 004
40. Marillonnet S, Thoeringer C, Kandzia R, Klimyuk V, Gleba Y. Systemic Agrobacterium tumefaciens-mediated transfection of viral replicons for efficient transient expression in plants. Nature Biotechnol 2005; 23:718-23; PMID:15883585; http://dx. doi. org/10. 1038/ nbt1094
41. Bondili JS, Castilho A, Mach L, Glossl J, Steinkellner H, Altmann F, Strasser R. Molecular cloning and heterologous expression of beta1, 2-xylosyltransferase and core alpha1, 3-fucosyltransferase from maize. Phytochemistry 2006; 67:2215-24; PMID:16920165; http:// dx. doi. org/10. 1016/j. phytochem. 2006. 07. 007
42. Castilho A, Gattinger P, Grass J, Jez J, Pabst M, Altmann F, Gorfer M, Strasser R, Steinkellner H. Nglycosylation engineering of plants for the biosynthesis of glycoproteins with bisected and branched complex N-glycans. Glycobiology 2011; 21:813-23; PMID:21317243; http://dx. doi. org/10. 1093/glycob/ cwr009
43. Strasser R, Castilho A, Stadlmann J, Kunert R, Quendler H, Gattinger P, Jez J, Rademacher T, Altmann F, Mach L, et al. Improved virus neutralization by plantproduced anti-HIV antibodies with a homogeneous beta1, 4-galactosylated N-glycan profile. J Biol Chem 2009; 284:20479-85; PMID:19478090; http://dx. doi. org/10. 1074/jbc. M109. 014126
44. Castilho A, Pabst M, Leonard R, Veit C, Altmann F, Mach L, Glossl J, Strasser R, Steinkellner H. Construction of a functional CMP-sialic acid biosynthesis pathway in Arabidopsis. Plant Physiol 2008; 147:331-9; PMID:18326787; http://dx. doi. org/10. 1104/ pp. 108. 117572
45. Castilho A, Bohorova N, Grass J, Bohorov O, Zeitlin L, Whaley K, Altmann F, Steinkellner Hl. Rapid high yield production of different glycoforms of Ebola virus monoclonal antibody. PloS one 2011; 6:e26040; PMID:22039433; http://dx. doi. org/10. 1371/journal. pone. 0026040
46. Leiter H, Mucha J, Staudacher E, Grimm R, Glossl J, Altmann F. Purification, cDNA cloning, and expression of GDP-L-Fuc:Asn-linked GlcNAc alpha1, 3-fucosyltransferase from mung beans. J Biol Chem 1999; 274:21830-9; PMID:10419500; http://dx. doi. org/ 10. 1074/jbc. 274. 31. 21830
47. Fabini G, Freilinger A, Altmann F, Wilson IB. Identification of core alpha 1, 3-fucosylated glycans and cloning of the requisite fucosyltransferase cDNA from Drosophila melanogaster. Potential basis of the neural anti-horseadish peroxidase epitope. J Biol Chem 2001; 276:28058-67; PMID:11382750; http://dx. doi. org/ 10. 1074/jbc. M100573200
48. Wang JM, Cieplak P, Kollman PA. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J Comput Chem 2000; 21:1049-74; http://dx. doi. org/10. 1002/1096-987X(200009) 21:12%3c1049::AID-JCC3%3e3. 0. CO;2-F