Differences in N-glycan structures found on recombinant IgA1 and IgA2 produced in murine myeloma and CHO cell lines

mAbs

Volumn 2, Issue 3, 2010, Pages 320-334

  Yoo, Esther M ^a   Yu, Li J ^a   Wims, Letitia A ^a   Goldberg, David ^b   Morrison, Sherie L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PALO ALTO RESEARCH CENTER   (United States)

Author keywords

Expression system; Glycosylation; IgA; Mass spectrometry; Recombinant antibody

Indexed keywords

GLYCAN; IMMUNOGLOBULIN A1; IMMUNOGLOBULIN A2; RECOMBINANT ANTIBODY;

ANIMAL CELL; ARTICLE; GLYCOSYLATION; IMMUNOGENICITY; MOUSE; MYELOMA; NONHUMAN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SIALYLATION;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL LINE, TUMOR; CHO CELLS; CRICETINAE; CRICETULUS; IMMUNOGLOBULIN A; MICE; POLYSACCHARIDES; PROTEIN ENGINEERING; RECOMBINANT PROTEINS;

EID: 77953666582     PISSN: 19420862     EISSN: None     Source Type: Journal    
DOI: 10.4161/mabs.2.3.11802     Document Type: Article

References (58)

1. Stubbe H, Berdoz J, Kraehenbuhl JP, Corthesy B. Polymeric IgA is superior to monomeric IgA and IgG carrying the same variable domain in preventing Clostridium difficile toxin A damaging of T84 monolayers. J Immunol 2000; 164:1952-1960
2. Ma JK, Hikmat BY, Wycoff K, Vine ND, Chargelegue D, Yu L, et al. Characterization of a recombinant plant monoclonal secretory antibody and preventive immunotherapy in humans. Nat Med 1998; 4:601-606 (Pubitemid 28237360)
3. Vidarsson G, van Der Pol WL, van Den Elsen JM, Vile H, Jansen M, Duijs J, et al. Activity of human IgG and IgA subclasses in immune defense against Neisseria meningitidis serogroup B. J Immunol 2001; 166:6250-6256
4. Stockmeyer B, Dechant M, van Egmond M, Tutt AL, Sundarapandiyan K, Graziano RF, et al. Triggering Fcalpha-receptor I (CD89) recruits neutrophils as effector cells for CD20-directed antibody therapy. J Immunol 2000; 165:5954-5961
5. van Egmond M, van Spriel AB, Vermeulen H, Huls G, van Garderen E, van de Winkel JG. Enhancement of polymorphonuclear cell-mediated tumor cell killing on simultaneous engagement of FcgammaRI (CD64) and FcalphaRI (CD89). Cancer Res 2001; 61:4055-4060 (Pubitemid 32720970)
6. Otten MA, Rudolph E, Dechant M, Tuk CW, Reijmers RM, Beelen RH, et al. Immature neutrophils mediate tumor cell killing via IgA but not IgG Fc receptors. J Immunol 2005; 174:5472-5480 (Pubitemid 40593187)
7. Dechant M, Vidarsson G, Stockmeyer B, Repp R, Glennie MJ, Gramatzki M, et al. Chimeric IgA antibodies against HLA class II effectively trigger lymphoma cell killing. Blood 2002; 100:4574-4580 (Pubitemid 35429700)
8. Torano A, Tsuzukida Y, Liu YS, Putnam FW. Location and structural significance of the oligosaccharides in human Ig-A1 and IgA2 immunoglobulins. Proc Natl Acad Sci USA 1977; 74:2301-2305 (Pubitemid 8110699)
9. Chintalacharuvu KR, Raines M, Morrison SL. Divergence of human alpha-chain constant region gene sequences. A novel recombinant alpha2 gene. J Immunol 1994; 152:5299-5304 (Pubitemid 2101927)
10. 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 Fcalpha receptor interactions. J Biol Chem 1998; 273:2260-2272 (Pubitemid 28069279)
11. Baenziger J, Kornfeld S. Structure of the carbohydrate units of IgA1 immunoglobulin. J Biol Chem 1974; 249:7260-7269
12. Endo T, Mestecky J, Kulhavy R, Kobata A. Carbohydrate heterogeneity of human myeloma proteins of the IgA1 and IgA2 subclasses. Mol Immunol 1994; 31:1415-1422 (Pubitemid 24381798)
13. Field MC, Amatayakul-Chantler S, Rademacher TW, Rudd PM, Dwek RA. Structural analysis of the N-glycans from human immunoglobulin A1: comparison of normal human serum immunoglobulin A1 with that isolated from patients with rheumatoid arthritis. Biochem J 1994; 299:261-275 (Pubitemid 24106318)
14. Oortwijn BD, Roos A, Royle L, van Gijlswijk-Janssen DJ, Faber-Krol MC, Eijgenraam JW, et al. Differential glycosylation of polymeric and monomeric IgA: a possible role in glomerular inflammation in IgA nephropathy. J Am Soc Nephrol 2006; 17:3529-3539 (Pubitemid 44865296)
15. Gomes MM, Wall SB, Takahashi K, Novak J, Renfrow MB, Herr AB. Analysis of IgA1 N-glycosylation and its contribution to FcalphaRI binding. Biochemistry 2008; 47:11285-11299
16. Tanaka A, Iwase H, Hiki Y, Kokubo T, Ishii-Karakasa I, Toma K, et al. Evidence for a site-specific fucosylation of N-linked oligosaccharide of immunoglobulin A1 from normal human serum. Glycoconj J 1998; 15:995-1000. (Pubitemid 29129200)
17. Royle L, Roos A, Harvey DJ, Wormald MR, van Gijlswijk-Janssen D, Redwan el RM, et al. Secretory IgA N- and O-glycans provide a link between the innate and adaptive immune systems. J Biol Chem 2003; 278:20140-20153 (Pubitemid 36799209)
18. Chintalacharuvu SR, Emancipator SN. The glycosylation of IgA produced by murine B cells is altered by Th2 cytokines. J Immunol 1997; 159:2327-2333
19. Chintalacharuvu SR, Nagy NU, Sigmund N, Nedrud JG, Amm ME, Emancipator SN. T cell cytokines determine the severity of experimental IgA nephropathy by regulating IgA glycosylation. Clin Exp Immunol 2001; 126:326-333 (Pubitemid 32995149)
20. Rifai A, Fadden K, Morrison SL, Chintalacharuvu KR. The N-glycans determine the differential blood clearance and hepatic uptake of human immunoglobulin (Ig)A1 and IgA2 isotypes. J Exp Med 2000; 191:2171-2182 (Pubitemid 30416363)
21. Goldberg D, Sutton-Smith M, Paulson J, Dell A. Automatic annotation of matrix-assisted laser desorption/ionization N-glycan spectra. Proteomics 2005; 5:865-875 (Pubitemid 40469017)
22. Campbell C, Stanley P. A dominant mutation to ricin resistance in Chinese hamster ovary cells induces UDP-GlcNAc:glycopeptide beta-4-N- acetylglucosaminyltransferase III activity. J Biol Chem 1984; 259:13370-13378 (Pubitemid 15223868)
23. Deutscher SL, Nuwayhid N, Stanley P, Briles EIB, Hirschberg CB. Translocation across golgi vesicle membranes: A CHO glycosylation mutant deficient in CMP-sialic acid transport. Cell 1984; 39:295-299 (Pubitemid 15191212)
24. Oelmann S, Stanley P, Gerardy-Schahn R. Point mutations identified in Lec8 Chinese hamster ovary glycosylation mutants that inactivate both the UDP-galactose and CMP-sialic acid transporters. J Biol Chem 2001; 276:26291-26300 (Pubitemid 37412845)
25. Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 2006; 313:670-673 (Pubitemid 44201145)
26. Anthony RM, Nimmerjahn F, Ashline DJ, Reinhold VN, Paulson JC, Ravetch JV. Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 2008; 320:373-376 (Pubitemid 351555659)
27. Shields RL, Lai J, Keck R, O'Connell LY, Hong K, Meng YG, et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 2002; 277:26733-26740 (Pubitemid 34951677)
28. Peipp M, Lammerts van Bueren JJ, Schneider-Merck T, Bleeker WW, Dechant M, Beyer T, et al. Antibody fucosylation differentially impacts cytotoxicity mediated by NK and PMN effector cells. Blood 2008; 112:2390-2399
29. Jefferis R, Lund J. Interaction sites on human IgG-Fc for FcgammaR: current models. Immunol Lett 2002; 82:57-65. (Pubitemid 34468035)
30. Tomana M, Novak J, Julian BA, Matousovic K, Konecny K, Mestecky J. Circulating immune complexes in IgA nephropathy consist of IgA1 with galactose-deficient hinge region and antiglycan antibodies. J Clin Invest 1999; 104:73-81. (Pubitemid 29534347)
31. Hiki Y, Odani H, Takahashi M, Yasuda Y, Nishimoto A, Iwase H, et al. Mass spectrometry proves under-Oglycosylation of glomerular IgA1 in IgA nephropathy. Kidney Int 2001; 59:1077-1085 (Pubitemid 32206870)
32. Allen AC, Bailey EM, Brenchley PE, Buck KS, Barratt J, Feehally J. Mesangial IgA1 in IgA nephropathy exhibits aberrant O-glycosylation: observations in three patients. Kidney Int 2001; 60:969-973 (Pubitemid 34205796)
33. Odani H, Hiki Y, Takahashi M, Nishimoto A, Yasuda Y, Iwase H, et al. Direct evidence for decreased sialylation and galactosylation of human serum IgA1 Fc O-glycosylated hinge peptides in IgA nephropathy by mass spectrometry. Biochem Biophys Res Commun 2000; 271:268-274 (Pubitemid 30444888)
34. Iwanami N, Iwase H, Takahashi N, Kato K, Itoh A, Takatani T, et al. Similarities between N-glycan glycoform of tonsillar IgA1 and that of aberrant IgA1 abundant in IgA nephropathy patient serum. J Nephrol 2008; 21:118-126 (Pubitemid 351780581)
35. Taylor AK, Wall R. Selective removal of alpha heavychain glycosylation sites causes immunoglobulin A degradation and reduced secretion. Mol Cell Biol 1988; 8:4197-4203
36. Atkin JD, Pleass RJ, Owens RJ, Woof JM. Mutagenesis of the human IgA1 heavy chain tailpiece that prevents dimer assembly. J Immunol 1996; 157:156-159
37. Phalipon A, Cardona A, Kraehenbuhl JP, Edelman L, Sansonetti PJ, Corthesy B. Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo. Immunity 2002; 17:107-115 (Pubitemid 34874623)
38. Herr AB, Ballister ER, Bjorkman PJ. Insights into IgA-mediated immune responses from the crystal structures of human FcalphaRI and its complex with IgA1-Fc. Nature 2003; 423:614-620
39. Oortwijn BD, Roos A, van der Boog PJ, Klar-Mohamad N, van Remoortere A, Deelder AM, et al. Monomeric and polymeric IgA show a similar association with the myeloid FcalphaRI/CD89. Mol Immunol 2007; 44:966-973 (Pubitemid 44429976)
40. Carayannopoulos L, Max EE, Capra JD. Recombinant human IgA expressed in insect cells. Proc Natl Acad Sci USA 1994; 91:8348-8352 (Pubitemid 24273661)
41. Basset C, Devauchelle V, Durand V, Jamin C, Pennec YL, Youinou P, et al. Glycosylation of immunoglobulin A influences its receptor binding. Scand J Immunol 1999; 50:572-579
42. Moura IC, Arcos-Fajardo M, Sadaka C, Leroy V, Benhamou M, Novak J, et al. Glycosylation and size of IgA1 are essential for interaction with mesangial transferrin receptor in IgA nephropathy. J Am Soc Nephrol 2004; 15:622-634 (Pubitemid 38294792)
43. Chuang PD, Morrison SL. Elimination of N-linked glycosylation sites from the human IgA1 constant region: effects on structure and function. J Immunol 1997; 158:724-732
44. Shibuya A, Sakamoto N, Shimizu Y, Shibuya K, Osawa M, Hiroyama T, et al. Fc alpha/mu receptor mediates endocytosis of IgM-coated microbes. Nat Immunol 2000; 1:441-446
45. Ramsland PA, Willoughby N, Trist HM, Farrugia W, Hogarth PM, Fraser JD, et al. Structural basis for evasion of IgA immunity by Staphylococcus aureus revealed in the complex of SSL7 with Fc of human IgA1. Proc Natl Acad Sci USA 2007; 104:15051-15056
46. 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 modelling: a comparison with monomeric human IgA1. J Mol Biol 2004; 338:921-941 (Pubitemid 38542823)
47. Chou HH, Takematsu H, Diaz S, Iber J, Nickerson E, Wright KL, et al. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc Natl Acad Sci USA 1998; 95:11751-11756 (Pubitemid 28460486)
48. Irie A, Koyama S, Kozutsumi Y, Kawasaki T, Suzuki A. The molecular basis for the absence of N-glycolylneuraminic acid in humans. J Biol Chem 1998; 273:15866-15871 (Pubitemid 28298210)
49. Zhu A, Hurst R. Anti-N-glycolylneuraminic acid antibodies identified in healthy human serum. Xenotransplantation 2002; 9:376-381 (Pubitemid 36358933)
50. Tangvoranuntakul P, Gagneux P, Diaz S, Bardor M, Varki N, Varki A, et al. Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc Natl Acad Sci USA 2003; 100:12045-12050 (Pubitemid 37271512)
51. Galili U. Abnormal expression of alpha-galactosyl epitopes in man. A trigger for autoimmune processes? Lancet 1989; 2:358-361
52. Qian J, Liu T, Yang L, Daus A, Crowley R, Zhou Q. 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. (Pubitemid 46497948)
53. Chung CH, Mirakhur B, Chan E, Le QT, Berlin J, Morse M, et al. Cetuximab-induced anaphylaxis and IgE specific for galactose-alpha-1,3- galactose. N Engl J Med 2008; 358:1109-1117 (Pubitemid 351398485)
54. Noguchi A, Mukuria CJ, Suzuki E, Naiki M. Immunogenicity of N-glycolylneuraminic acid-containing carbohydrate chains of recombinant human erythropoietin expressed in Chinese hamster ovary cells. J Biochem 1995; 117:59-62.
55. Chintalacharuvu KR, Morrison SL. Residues critical for H-L disulfide bond formation in human IgA1 and IgA2. J Immunol 1996; 157:3443-3449
56. Chintalacharuvu KR, Gurbaxani B, Morrison SL. Incomplete assembly of IgA2m(2) in Chinese hamster ovary cells. Mol Immunol 2007; 44:3445-3452
57. 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; 143:2595-2601
58. Papac DI, Briggs JB, Chin ET, Jones AJ. A highthroughput microscale method to release N-linked oligosaccharides from glycoproteins for matrix-assisted laser desorption/ionization time-of-flight mass spectrometric analysis. Glycobiology 1998; 8:445-454