Glycoengineered monoclonal antibodies with homogeneous glycan (M3, G0, G2, and A2) using a chemoenzymatic approach have different affinities for FcγRIIIa and variable antibody-dependent cellular cytotoxicity activities

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Kurogochi, Masaki ^a   Mori, Masako ^a   Osumi, Kenji ^a   Tojino, Mami ^a   Sugawara, Shu Ichi ^a   Takashima, Shou ^a   Hirose, Yuriko ^a   Tsukimura, Wataru ^a   Mizuno, Mamoru ^a   Amano, Junko ^a   Matsuda, Akio ^a   Tomita, Masahiro ^b   Takayanagi, Atsushi ^c   Shoda, Shin Ichiro ^d   Shirai, Takashi ^a  

^a NOGUCHI INSTITUTE   (Japan)

^b Immuno Biological Laboratories Co Ltd   (Japan)

^c KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOD PROTEIN; ENDOH PROTEIN; ENDOLL PROTEIN; ENDOM PROTEIN; ENDOS PROTEIN; FC GAMMA RECEPTOR IIIA; FC RECEPTOR; GLYCAN A2; GLYCAN DERIVATIVE; GLYCAN G0; GLYCAN G2; GLYCAN M3; MONOCLONAL ANTIBODY; N ACETYL BETA GLUCOSAMINIDASE; UNCLASSIFIED DRUG; ACETYLGLUCOSAMINIDASE; IMMUNOGLOBULIN FC FRAGMENT; POLYSACCHARIDE; TRASTUZUMAB;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY PRODUCTION; ARTICLE; BINDING AFFINITY; CATION EXCHANGE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; FUCOSYLATION; GLYCOSYLATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LACTOCOCCUS LACTIS; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROMOTER REGION; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTON NUCLEAR MAGNETIC RESONANCE; ULTRAFILTRATION; CHEMISTRY; HUMAN; METABOLISM;

ACETYLGLUCOSAMINIDASE; ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; POLYSACCHARIDES; TRASTUZUMAB;

EID: 84941309144     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132848     Document Type: Article

References (72)

1. Green MC, Murray JL, Hortobagyi GN. (2000) Monoclonal antibody therapy for solid tumors. Cancer Treat Rev. 26: 269-286. PMID: 10913382.
2. Adams GP, Weiner LM. (2005) Monoclonal antibody therapy of cancer. Nat Biotechnol. 23: 1147- 1157. PMID: 16151408.
3. Jefferis R. (2007) Antibody therapeutics: isotype and glycoform selection. Expert Opin Biol Ther. 7: 1401-1413. PMID: 17727329.
4. Jefferis R. (2005) Glycosylation of recombinant antibody therapeutics. Biotechnol Prog. 21: 11-16. PMID: 15903235.
5. Nimmerjahn F, Ravetch JV. (2008) Fcγ receptors as regulators of immune responses. Nat Rev Immunol. 8: 34-47. PMID: 18064051.
6. Deisenhofer J. (1981) 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. 20: 2361-2370. PMID: 7236608.
7. Krapp S, Mimura Y, Jefferis R, Huber R, Sondermann P. (2003) Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J Mol Biol. 325: 979- 989. PMID: 12527303.
8. Wormald MR, Rudd PM, Harvey DJ, Chang SC, Scragg IG, Dwek RA. (1997) Variations in oligosaccharide- protein interactions in immunoglobulin G determine the site-specific glycosylation profiles and modulate the dynamic motion of the Fc oligosaccharides. Biochemistry. 36: 1370-1380. PMID: 9063885.
9. Yamaguchi Y, Nishimura M, Nagano M, Yagi H, Sasakawa H, Uchida K, et al. (2006) Glycoform-dependent conformational alteration of the Fc region of human immunoglobulin G1 as revealed by NMR spectroscopy. Biochim Biophys Acta. 1760: 693-700. PMID: 16343775.
10. Barb AW, Prestegard JH. (2011) NMR analysis demonstrates immunoglobulin G N-glycans are accessible and dynamic. Nat Chem Biol. 7: 147-153. doi:10.1038/nchembio.511PMID: 21258329.
11. Sondermann P, Huber R, Oosthuizen V, Jacob U. (2000) The 3.2-Å crystal structure of the human IgG1 Fc fragment-FcγRIII complex. Nature. 406: 267-273. PMID: 10917521.
12. Crispin M, Bowden TA, Coles CH, Harlos K, Aricescu AR, Harvey DJ, et al. (2009) Carbohydrate and domain architecture of an immature antibody glycoform exhibiting enhanced effector functions. J Mol Biol. 387: 1061-1066. PMID: 19236877.
13. Martin WL, West AP Jr, Gan L, Bjorkman PJ. (2001) Crystal structure at 2.8 Å of an FcRn/heterodimeric Fc complex: mechanism of pH-dependent binding. Mol Cell. 7: 867-877. PMID: 11336709.
14. Umaña P, Jean-Mairet J, Moudry R, Amstutz H, Bailey JE. (1999) Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat Biotechnol. 117: 176-180.
15. Shields RL, Lai J, Keck R, O'Connell LY, Hong K, Meng YG, et al. (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human FcγRIII and antibody-dependent cellular toxicity. J Biol Chem. 277: 26733-26740. PMID: 11986321.
16. Kanda Y, Yamada T, Mori K, Okazaki A, Inoue M, Kitajima-Miyama K, et al. (2007) Comparison of biological activity among nonfucosylated therapeutic IgG1 antibodies with three different N-linked Fc oligosaccharides: The high-mannose, hybrid, and complex types. Glycobiology. 17: 104-118. PMID: 17012310.
17. Hodoniczky J, Zheng YZ, James DC. (2005) Control of recombinant monoclonal antibody effector functions by Fc N-glycan remodeling in vitro. Biotechnol Prog. 21: 1644-1652. PMID: 16321047.
18. Li H, Sethuraman N, Stadheim TA, Zha D, Prinz B, Ballew N, et al. (2006) Optimization of humanized IgGs in glycoengineered Pichia pastoris. Nat Biotechnol. 24: 210-5. PMID: 16429149.
19. Schähs M, Strasser R, Stadlmann J, Kunert R, Rademacher T, Steinkellner H. (2007) Production of a monoclonal antibody in plants with a humanized N-glycosylation pattern. Plant Biotechnol J. 5:657- 663. PMID: 17678502.
20. Loos A, Steinkellner H. (2012) IgG-Fc glycoengineering in non-mammalian expression hosts. Arch Biochem Biophys. 526: 167-73. PMID: 22634260.
21. Yamane-Ohnuki N, Kinoshita S, Inoue-Urakubo M, Kusunoki M, Iida S, Nakano R, et al. (2004) 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. 87: 614-622. PMID: 15352059.
22. Huang W, Giddens J, Fan SQ, Toonstra C, Wang LX. (2012) Chemoenzymatic glycoengineering of intact IgG antibodies for gain of functions. J Am Chem Soc. 134: 12308-12318. doi:10.1021/ja3051266PMID: 22747414.
23. Goodfellow JJ, Baruah K, Yamamoto K, Bonomelli C, Krishna B, Harvey DJ, et al. (2012) An endoglycosidase with alternative glycan specificity allows broadened glycoprotein remodelling. J Am Chem Soc. 134: 8030-8033doi:10.1021/ja301334b PMID: 22551167.
24. Collin M, Olsén A. (2001) EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J. 20: 3046-3055. PMID: 11406581.
25. Iizuka M, Ogawa S, Takeuchi A, Nakakita S, Kubo Y, Miyawaki Y, et al. (2009) Production of a recombinant mouse monoclonal antibody in transgenic silkworm cocoons. FEBS J. 276: 5806-5820. doi:10.1111/j.1742-4658.2009.07262.x PMID: 19740109.
26. Baruah K, Bowden TA, Krishna BA, Dwek RA, Crispin M, Scanlan CN. (2012) Selective deactivation of serum IgG: A general strategy for the enhancement of monoclonal antibody receptor interactions. J Mol Biol. 420: 1-7. doi:10.1016/j.jmb.2012.04.002 PMID: 22484364.
27. Huang W, Li C, Li B, Umekawa M, Yamamoto K, Zhang X, et al. (2009) Glycosynthases enable a highly efficient chemoenzymatic synthesis of N-glycoproteins carrying intact natural N-glycans. J Am Chem Soc 131: 2214-2223. doi:10.1021/ja8074677 PMID: 19199609.
28. Sun B, Bao W, Tian X, Li M, Liu H, Dong J, et al. (2014) A simplified procedure for gram-scale production of sialylglycopeptide (SGP) from egg yolk and subsequent semi-synthesis of Man3GlcNAc oxazoline. Carbohydr Res 396: 62-69. PMID: 25124522.
29. Smith EL, Giddens JP, Iavarone AT, Godula K, Wang LX, Bertozzi CR. (2014) Chemoenzymatic Fc glycosylation via engineered aldehyde tags. Bioconjug Chem. 25: 788-795. doi:10.1021/bc500061s PMID: 24702330.
30. Noguchi M, Tanaka T, Gyakushi H, Kobayashi A, Shoda S. (2009) Efficient synthesis of sugar oxazolines from unprotected N-acetyl-2-amino sugars by using chloroformamidinium reagent in water. J Org Chem. 74: 2210-2212. doi:10.1021/jo8024708PMID: 19203234.
31. Prang N, Preithner S, Brischwein K, Göster P, Wöppel A, Müller J, et al. (2005) Cellular and complement- dependent cytotoxicity of Ep-CAM-specific monoclonal antibody MT201 against breast cancer cell lines. Br J Cancer. 92: 342-349. PMID: 15655555.
32. Parekh BS, Berger E, Sibley S, Cahya S, Xiao L, LaCerte MA, et al. (2012) Development and validation of an antibody-dependent cell-mediated cytotoxicity-reporter gene assay. MAbs. 4: 310-318doi:10.4161/mabs.19873 PMID: 22531445.
33. Iizuka M, Tomita M, Shimizu K, Kikuchi Y, Yoshizato K. (2008) Translational enhancement of recombinant protein synthesis in transgenic silkworms by a 5'-untranslated region of polyhedrin gene of Bombyx mori Nucleopolyhedrovirus. J Biosci Bioeng. 105: 595-603. PMID: 18640598.
34. Harris RJ, Kabakoff B, Macchi FD, Shen FJ, Kwong M, Andya JD, et al. (2001) Identification of multiple sources of charge heterogeneity in a recombinant antibody. J Chromatogr B Biomed Sci Appl. 752: 233-245. PMID: 11270864.
35. Tamura T, Thibert C, Royer C, Kanda T, Abraham E, Kamba M, et al. (2000) Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon-derived vector. Nat Biotechnol. 18: 81- 84. PMID: 10625397.
36. Tomita M, Munetsuna H, Sato T, Adachi T, Hino R, Hayashi M, et al. (2003) Transgenic silkworms produce recombinant human type III procollagen in cocoons. Nat Biotechnol. 21: 52-56. PMID: 12483223.
37. Adachi T, Wang X, Murata T, Obara M, Akutsu H, Machida M, et al. (2010) Production of a non-triple helical collagen a chain in transgenic silkworms and its evaluation as a gelatin substitute for cell culture. Biotechnol Bioeng. 106: 860-870. doi:10.1002/bit.22752PMID: 20589667.
38. Kurogochi M, Amano J. (2014) Relative quantitation of glycopeptides based on stable isotope labeling using MALDI-TOF MS. Molecules. 19: 9944-9961. doi:10.3390/molecules19079944PMID: 25010467.
39. Wang S, Ionescu R, Peekhaus N, Leung JY, Ha S, Vlasak J. (2010) Separation of post-translational modifications in monoclonal antibodies by exploiting subtle conformational changes under mildly acidic conditions. J Chromatogr A. 1217: 6496-6502. PMID: 20828701.
40. Ha S, Ou Y, Vlasak J, Li Y, Wang S, Vo K, et al. (2011) Isolation and characterization of IgG1 with asymmetrical Fc glycosylation. Glycobiology. 21: 1087-1096doi:10.1093/glycob/cwr047 PMID: 21470983.
41. Shigeta M, Shibukawa Y, Ihara H, Miyoshi E, Taniguchi N, Gu J (2006) β1, 4-N-Acetylglucosaminyltransferase III potentiates β1integrin-mediated neuritogenesis induced by serum deprivation in Neuro2a cells. Glycobiology 16: 564-571. PMID: 16531477.
42. Zou G, Ochiai H, Huang W, Yang Q, Li C, Wang LX. (2011) Chemoenzymatic synthesis and Fcγ receptor binding of homogeneous glycoforms of antibody Fc domain. Presence of a bisecting sugar moiety enhances the affinity of Fc to FcγIIIa receptor. J Am Chem Soc. 133: 18975-18991. doi:10.1021/ja208390n PMID: 22004528.
43. Shields RL, Namenuk AK, Hong K, Meng YG, Rae J, Briggs J, et al. (2001) High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R. J Biol Chem. 276: 6591-6560 PMID: 11096108.
44. Tarentino AL, Plummer TH Jr. (1994) Enzymatic deglycosylation of asparagine-linked glycans: purification, properties, and specificity of oligosaccharide-cleaving enzymes from Flavobacterium meningosepticum. Methods Enzymol. 230: 44-57 PMID: 8139511.
45. Kato T, Fujita K, Takeuchi M, Kobayashi K, Natsuka S, Ikura K, et al. (2002) Identification of an endo-β- N-acetylglucosaminidase gene in Caenorhabditis elegans and its expression in Escherichia coli. Glycobiology. 12: 581-587. PMID: 12244070.
46. Suzuki T, Yano K, Sugimoto S, Kitajima K, Lennarz WJ, Inoue S, et al. (2002) Endo-β-N-acetylglucosaminidase, an enzyme involved in processing of free oligosaccharides in the cytosol. Proc Natl Acad Sci U S A. 99: 9691-9696. PMID: 12114544.
47. Tarentino AL, Plummer TH Jr, Maley F. (1974) The release of intact oligosaccharides from specific glycoproteins by endo-β-N-acetylglucosaminidase H. J Biol Chem. 249: 818-824. PMID: 4204553.
48. Tai T, Yamashita K, Ogata-Arakawa M, Koide N, Muramatsu T, Iwashita S, et al. (1975) Structural studies of two ovalbumin glycopeptides in relation to the endo-β-N-acetylglucosaminidase specificity. J Biol Chem. 250: 8569-8575. PMID: 389.
49. Kadowaki S, Yamamoto K, Fujisaki M, Izumi K, Tochikura T, Yokoyama T. (1990) Purification and characterization of a novel fungal endo-β-N-acetylglucosaminidase acting on complex oligosaccharides of glycoproteins. Agric Biol Chem. 54: 97-106. PMID: 1368528.
50. Strecker G, Herlant-Peers MC, Fournet B, Montreuil J (1977) Structure of seven oligosaccharides excreted in the urine of a patient with sandhoff's disease (GM2 gangliosidosis-variant O). Eur J Biochem 81: 165-171. PMID: 412673.
51. Huang W, Yang Q, Umekawa M, Yamamoto K, Wang LX (2010) Arthrobacter endo-β-N-acetylglucosaminidase shows transglycosylation activity on complex-type N-glycan oxazolines: one-pot conversion of ribonuclease B to sialylated ribonuclease C. ChemBioChem 11: 1350-1355doi:10.1002/cbic.201000242PMID: 20486148.
52. Paulsen H, Peters T, Sinnwell V, Lebuhn R, Meyer B. (1984) Bestimmung der Konformationen von Triund Tetrasaccharid-Sequenzen der Core-Struktur von N-Glycoproteinen. Problem der (1→6) glycosidischen Bindung. Liebigs Ann. Chem., 951-976.
53. Fan SQ, Huang W, Wang LX. (2012) Remarkable transglycosylation activity of glycosynthase mutants of endo-D, an endo-β-N-acetylglucosaminidase from Streptococcus pneumoniae. J Biol Chem. 287: 11272-11281doi:10.1074/jbc.M112.340497 PMID: 22318728.
54. Wei Y, Li C, Huang W, Li B, Strome S, Wang LX. (2008) Glycoengineering of human IgG1-Fc through combined yeast expression and in vitro chemoenzymatic glycosylation. Biochemistry. 47:10294- 10304. doi: 10.1021/bi800874y PMID: 18771295.
55. Iannello A, Ahmad A. (2005) Role of antibody-dependent cell-mediated cytotoxicity in the efficacy of therapeutic anti-cancer monoclonal antibodies. Cancer Metastasis Rev. 24: 487-499. PMID: 16408158.
56. Shinkawa T, Nakamura K, Yamane N, Shoji-Hosaka E, Kanda Y, Sakurada M, et al. (2003) 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. 278: 3466-3473. PMID: 12427744.
57. Ferrara C, Grau S, Jäger C, Sondermann P, Brünker P, Waldhauer I, et al. (2011) Unique carbohydrate- carbohydrate interactions are required for high affinity binding between FcγRIII and antibodies lacking core fucose. Proc Natl Acad Sci U S A. 108: 12669-12674. doi:10.1073/pnas.1108455108 PMID: 21768335.
58. Mizushima T, Yagi H, Takemoto E, Shibata-Koyama M, Isoda Y, Iida S, et al. (2011) Structural basis for improved efficacy of therapeutic antibodies on defucosylation of their Fc glycans. Genes Cells. 16:1071-1080. doi:10.1111/j.1365-2443.2011.01552.xPMID: 22023369.
59. Junttila TT, Parsons K, Olsson C, Lu Y, Xin Y, Theriault J, et al. (2010) Superior in vivo efficacy of afucosylated trastuzumab in the treatment of HER2-amplified breast cancer. Cancer Res. 70: 4481-4489. doi:10.1158/0008-5472.CAN-09-3704 PMID: 20484044.
60. Kaneko Y, Nimmerjahn F, Ravetch JV. (2006) Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science. 313: 670-673. PMID: 16888140.
61. Forthal DN, Gach JS, Landucci G, Jez J, Strasser R, Kunert R, et al. (2010) Fc-glycosylation influences Fcγ receptor binding and cell-mediated anti-HIV activity of monoclonal antibody 2G12. J Immunol. 185: 6876-6882. doi:10.4049/jimmunol.1002600 PMID: 21041724.
62. Tada M, Ishii-Watabe A, Suzuki T, Kawasaki N. (2014) Development of a cell-based assay measuring the activation of FcγRIIa for the characterization of therapeutic monoclonal antibodies. PLoS One. 9: e95787. doi:10.1371/journal.pone.0095787 PMID: 24752341.
63. Zhang N, Liu L, Dumitru CD, Cummings NR, Cukan M, Jiang Y, et al. (2011) Glycoengineered Pichia produced anti-HER2 is comparable to trastuzumab in preclinical study. MAbs. 3: 289-298. PMID: 21487242.
64. Malhotra R, Wormald MR, Rudd PM, Fischer PB, Dwek RA, Sim RB. (1995) Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat Med. 1: 237-243. PMID: 7585040.
65. Zhou Q, Shankara S, Roy A, Qiu H, Estes S, McVie-Wylie A, et al. (2008) Development of a simple and rapid method for producing non-fucosylated oligomannose containing antibodies with increased effector function. Biotechnol Bioeng. 99: 652-665. PMID: 17680659.
66. Chung CH, Mirakhur B, Chan E, Le QT, Berlin J, Morse M, et al. (2008) Cetuximab-induced anaphylaxis and IgE specific for galactose-α-1, 3-galactose. N Engl J Med. 358: 1109-1117doi:10.1056/NEJMoa074943PMID: 18337601.
67. Sarma VR, Silverton EW, Davies DR, Terry WD. (1971) The three-dimensional structure at 6 Å resolution of a human gamma Gl immunoglobulin molecule. J Biol Chem. 246: 3753-3759. PMID: 5578919.
68. Ahmed AA, Giddens J, Pincetic A, Lomino JV, Ravetch JV, Wang LX, et al. (2014) Structural characterization of anti-inflammatory immunoglobulin G Fc proteins. J Mol Biol. 426: 3166-3179. PMID: 25036289.
69. Wright A, Sato Y, Okada T, Chang K, Endo T, Morrison S. (2000) In vivo trafficking and catabolism of IgG1 antibodies with Fc associated carbohydrates of differing structure. Glycobiology. 10: 1347-1355. PMID: 11159927.
70. Wu AM, Senter PD. (2005) Arming antibodies: prospects and challenges for immunoconjugates. Nat Biotechnol. 23: 1137-1146. PMID: 16151407.
71. Ricart AD, Tolcher AW. (2007) Technology insight: cytotoxic drug immunoconjugates for cancer therapy. Nat Clin Pract Oncol. 4: 245-255. PMID: 17392715.
72. Yoshikawa M, Mukai Y, Okada Y, Tsumori Y, Tsunoda S, Tsutsumi Y, et al. (2013) Robo4 is an effective tumor endothelial marker for antibody-drug conjugates based on the rapid isolation of the anti- Robo4 cell-internalizing antibody. Blood. 121: 2804-2813. doi:10.1182/blood-2012-12-468363 PMID: 23365463.