EndoS and EndoS2 hydrolyze Fc-glycans on therapeutic antibodies with different glycoform selectivity and can be used for rapid quantification of high-mannose glycans

Glycobiology

Volumn 25, Issue 10, 2015, Pages 1053-1063

  Sjögren, Jonathan ^a,c   Cosgrave, Eoin F J ^b,d   Allhorn, Maria ^a   Nordgren, Maria ^c   Björk, Stephan ^c   Olsson, Fredrik ^c   Fredriksson, Sarah ^c   Collin, Mattias ^a  

^a LUND UNIVERSITY   (Sweden)

^b WATERS CORPORATION   (United States)

^c Genovis AB   (Sweden)

^d SEATTLE GENETICS INC   (United States)

Author keywords

endoglycosidase; EndoS; glycosylation; IgG; Streptococcus pyogenes

Indexed keywords

ADALIMUMAB; CETUXIMAB; DENOSUMAB; ENDOS; ENDOS2; GLYCAN; GLYCOSIDASE; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G; MANNOSE; MANNOSE OLIGOSACCHARIDE; MONOCLONAL ANTIBODY; PANITUMUMAB; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; MANNAN; NDOS PROTEIN, STREPTOCOCCUS PYOGENES; POLYSACCHARIDE;

ANTIGEN BINDING; ARTICLE; COMPARATIVE STUDY; ENZYME ACTIVITY; GLYCOSYLATION; HYDROLYSIS; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ENGINEERING; STREPTOCOCCUS PYOGENES; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; CHEMISTRY; ENZYME SPECIFICITY;

ADALIMUMAB; ANTIBODIES, MONOCLONAL; BACTERIAL PROTEINS; CETUXIMAB; DENOSUMAB; GLYCOSIDE HYDROLASES; HYDROLYSIS; IMMUNOGLOBULIN FC FRAGMENTS; MANNANS; POLYSACCHARIDES; SUBSTRATE SPECIFICITY;

EID: 84943594555     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwv047     Document Type: Article

References (45)

1. Allhorn M, Briceno JG, Baudino L, Lood C, Olsson ML, Izui S, Collin M. 2010. The IgG-specific endoglycosidase EndoS inhibits both cellular and complement-mediated autoimmune hemolysis. Blood. 115:5080-5088.
2. Allhorn M, Olin AI, Nimmerjahn F, Collin M. 2008. Human IgG/Fc gamma R interactions are modulated by streptococcal IgG glycan hydrolysis. PLoS ONE. 3:e1413.
3. An Z. 2011. Therapeutic Monoclonal Antibodies: From Bench to Clinic. New Jersey, NJ: John Wiley & Sons.
4. Anthony RM, Ravetch JV. 2010. A novel role for the IgG Fc glycan: the antiinflammatory activity of sialylated IgG Fcs. J Clin Immunol. 30(Suppl 1): S9-14.
5. Anthony RM, Wermeling F, Karlsson MCI, Ravetch JV. 2008. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci USA. 105:19571-19578.
6. Ayoub D, Jabs W, Resemann A, Evers W, Evans C, Main L, Baessmann C, Wagner-Rousset E, Suckau D, Beck A. 2013. 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. 5:699-710.
7. Beck A, Reichert JM. 2012. Marketing approval of mogamulizumab: a triumph for glyco-engineering. mAbs. 4:419-425.
8. Beck A, Wurch T, Bailly C, Corvaia N. 2010. Strategies and challenges for the next generation of therapeutic antibodies. Nat Rev Immunol. 10:345-352.
9. Bournazos S, Chow S-K, Abboud N, Casadevall A, Ravetch JV. 2014. Human IgG Fc domain engineering enhances antitoxin neutralizing antibody activity. J Clin Invest. 124:725-729.
10. Chan AC, Carter PJ. 2010. Therapeutic antibodies for autoimmunity and inflammation. Nat Rev Immunol. 10:301-316.
11. Collin M. 2012. EndoS, a "drug from a bug" as a novel treatment for autoimmunity of the blood. ISBT Sci Ser. 7:142-145.
12. Collin M, Olsé n A. 2001. EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J. 20:3046-3055.
13. Collin M, Shannon O, Björck L. 2008. IgG glycan hydrolysis by a bacterial enzyme as a therapy against autoimmune conditions. Proc Natl Acad Sci USA. 105:4265-4270.
14. Collin M, Svensson MD, Sjöholm AG, Jensenius JC, Sjöbring U, Olsé n A. 2002.
15. Endo S and SpeB from Streptococcus pyogenes inhibit immunoglobulinmediated opsonophagocytosis. Infect Immun. 70:6646-6651.
16. Dalziel M, Crispin M, Scanlan CN, Zitzmann N, Dwek RA. 2014. Emerging principles for the therapeutic exploitation of glycosylation. Science. 343:1235681-1235681.
17. Dixon EV, Claridge JK, Harvey DJ, Baruah K, Yu X, Vesiljevic S, Mattick S, Pritchard LK, Krishna B, Scanlan CN, et al. 2014. Fragments of bacterial endoglycosidase S and immunoglobulin G reveal subdomains of each that contribute to deglycosylation. J Biol Chem. 289:13876-13889.
18. Garbe J, Collin M. 2012. Bacterial hydrolysis of host glycoproteins - powerful protein modification and efficient nutrient acquisition. J Innate Immun. 4:121-131.
19. Goetze AM, Liu YD, Zhang Z, Shah B, Lee E, Bondarenko PV, Flynn GC. 2011. High-mannose glycans on the Fc region of therapeutic IgG antibodies increase serum clearance in humans. Glycobiol. 21:949-959.
20. Gorovits B, Krinos-Fiorotti C. 2013. Proposed mechanism of off-target toxicity for antibody-drug conjugates driven by mannose receptor uptake. Cancer Immunol Immunother. 62:217-223.
21. Harvey DJ, Merry AH, Royle L, Campbell MP, Dwek RA, Rudd PM. 2009. Proposal for a standard system for drawing structural diagrams of N- and O-linked carbohydrates and related compounds. Proteomics. 9:3796-3801.
22. Hills AE, Patel A, Boyd P, James DC. 2001. Metabolic control of recombinant monoclonal antibody N-glycosylation in GS-NS0 cells. Biotechnol Bioeng. 75:239-251.
23. Hirose M, Vafia K, Kalies K, Groth S, Westermann J, Zillikens D, Ludwig RJ, Collin M, Schmidt E. 2012. Enzymatic autoantibody glycan hydrolysis alleviates autoimmunity against typeVII collagen. J. Autoimmun. 39:304-314.
24. Huang W, Giddens J, Fan S-Q, Toonstra C, Wang L-X. 2012. Chemoenzymatic glycoengineering of intact IgG antibodies for gain of functions. J Am Chem Soc. 134:12308-12318.
25. Iida S, Misaka H, Inoue M, Shibata M, Nakano R, Yamane-Ohnuki N, Wakitani M, Yano K, Shitara K, Satoh M. 2006. Nonfucosylated therapeutic IgG1 antibody can evade the inhibitory effect of serum immunoglobulin G on antibody-dependent cellular cytotoxicity through its high binding to FcgammaRIIIa. Clin Cancer Res. 12:2879-2887.
26. Jabs W, Resemann A, Evers W, Evans C, Main L, Baessmann C, Suckau D, Wagner-Rousset E, Ayoub D, Beck A. 2012. Fast and extensive mass spectrometry characterization of therapeutic mAbs: the panitumumab case study. Poster CASSS Mass Spec 2012: P-125.
27. Janin-Bussat M-C, Tonini L, Huillet C, Colas O, Klinguer-Hamour C, Corvaïa N, Beck A. 2013. Cetuximab Fab and Fc N-glycan fast characterization using IdeS digestion and liquid chromatography coupled to electrospray ionization mass spectrometry. Methods Mol Biol. 988:93-113.
28. Jefferis R. 2005. Glycosylation of recombinant antibody therapeutics. Biotechnol Progr. 21:11-16.
29. Jefferis R. 2009a. Glycosylation as a strategy to improve antibody-based therapeutics. Nat Rev Drug Discov. 8:226-234.
30. Jefferis R. 2009b. Recombinant antibody therapeutics: the impact of glycosylation on mechanisms of action. Trends Pharmacol Sci. 30:356-362.
31. 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.
32. Monnet C, Jorieux S, Souyris N, Zaki O, Jacquet A, Fournier N, Crozet F, de Romeuf C, Bouayadi K, Urbain R, et al. 2014. Combined glyco- and protein-Fc engineering simultaneously enhance cytotoxicity and half-life of a therapeutic antibody. mAbs. 6:422-436.
33. Pincetic A, Bournazos S, DiLillo DJ, Maamary J, Wang TT, Dahan R, Fiebiger B-M, Ravetch JV. 2014. Type I and type II Fc receptors regulate innate and adaptive immunity. Nat Immunol. 15:707-716.
34. Puɥić M, Knezević A, Vidic J, Adamczyk B, Novokmet M, Pola͉ek O, Gornik O, Supraha-Goreta S, WormaldMR, Qian J, Liu T, Yang L, Daus A, Crowley R, Zhou Q. 2007. 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. 364:8-18.
35. Quast I, Lünemann JD. 2014. Fc glycan-modulated immunoglobulin G effector functions. J Clin Immunol. 34:S51-S55.
36. Redzić I, et al. 2011. High throughput isolation and glycosylation analysis of IgG-variability and heritability of the IgG glycome in three isolated human populations. Mol Cell Proteomics. 10:M111. 010090-M111. 010090.
37. Robblee J, Collins BE, Kaundinya G, Bosques CJ. 2013. Methods related to denosumab. Google Patents.
38. Ruhaak LR, Zauner G, Huhn C, Bruggink C, Deelder AM, Wuhrer M. 2010. Glycan labeling strategies and their use in identification and quantification. Anal Bioanal Chem. 397:3457-3481.
39. Sjögren J, Collin M. 2014. Bacterial glycosidases in pathogenesis and glycoengineering. Future Microbiol. 9:1039-1051.
40. Sjögren J, Okumura CYM, Collin M, Nizet V, Hollands A. 2011. Study of the IgG endoglycosidase EndoS in group A streptococcal phagocyte resistance and virulence. BMC Microbiol. 11:120.
41. Sjögren J, Struwe WB, Cosgrave EFJ, Rudd PM, Stervander M, Allhorn M, Hollands A, Nizet V, Collin M. 2013. EndoS2 is a unique and conserved enzyme of serotype M49 group A Streptococcus that hydrolyses N-linked glycans on IgG and α1-acid glycoprotein. Biochem J. 455:107-118.
42. Sondermann P, Pincetic A, Maamary J, Lammens K, Ravetch JV. 2013. General mechanism for modulating immunoglobulin effector function. Proc Natl Acad Sci USA. 110:9868-9872.
43. van Timmeren MM, van der Veen BS, Stegeman CA, Petersen AH, Hellmark T, Collin M, Heeringa P. 2010. IgG glycan hydrolysis attenuates ANCAmediated glomerulonephritis. J Am Soc Nephrol. 21:1103-1114.
44. von Pawel-Rammingen U, Johansson BP, Björck L. 2002. IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G. EMBO J. 21:1607-1615.
45. Woof JM, Burton DR. 2004. Human antibody-Fc receptor interactions illuminated by crystal structures. Nat Rev Immunol. 4:89-99.