Pro-inflammatory pattern of IgG1 Fc glycosylation in multiple sclerosis cerebrospinal fluid

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Wuhrer, Manfred ^a,b,c   Selman, Maurice H J ^a   McDonnell, Liam A ^a   Kümpfel, Tania ^d   Derfuss, Tobias ^e   Khademi, Mohsen ^f   Olsson, Tomas ^f   Hohlfeld, Reinhard ^d,g   Meinl, Edgar ^d   Krumbholz, Markus ^d,h  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^e UNIVERSITY HOSPITAL BASEL   (Switzerland)

^f KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^g Munich Cluster of Systems Neurology ^*  (Germany)

^h UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Cerebrospinal fluid; Glycosylation; Immunoglobulin G; Multiple sclerosis

Indexed keywords

GLYCOPEPTIDE; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G1; METHOTREXATE; N ACETYLGLUCOSAMINE; PEPTIDE DERIVATIVE; AUTACOID; BIOLOGICAL MARKER; IMMUNOGLOBULIN G;

ADULT; ARTICLE; BLOOD SAMPLING; CELL COUNT; CEREBROSPINAL FLUID CYTOLOGY; CLINICAL ARTICLE; CONTROLLED STUDY; DEMYELINATION; FEMALE; FUCOSYLATION; HUMAN; IMMUNOGLOBULIN PRODUCTION; INFLAMMATORY DISEASE; MALE; MASS SPECTROMETRY; MULTIPLE SCLEROSIS; PROTEIN AFUCOSYLATION; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN FUNCTION; PROTEIN GALACTOSYLATION; PROTEIN GLYCOSYLATION; RELAPSE; SIALYLATION; BLOOD; CEREBROSPINAL FLUID; GLYCOSYLATION; MIDDLE AGED;

ADULT; BIOMARKERS; FEMALE; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN G; INFLAMMATION MEDIATORS; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS;

EID: 84949955706     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0450-1     Document Type: Article

References (55)

1. Stangel M, Fredrikson S, Meinl E, Petzold A, Stuve O, Tumani H. The utility of cerebrospinal fluid analysis in patients with multiple sclerosis. Nat Rev Neurol. 2013;9(5):267-76. doi: 10.1038/nrneurol.2013.41.
2. von Büdingen HC, Bar-Or A, Zamvil SS. B cells in multiple sclerosis: connecting the dots. Curr Opin Immunol. 2011;23(6):713-20. http://dx.doi.org/10.1016/j.coi.2011.09.003.
3. Antel J, Bar-Or A. Roles of immunoglobulins and B cells in multiple sclerosis: from pathogenesis to treatment. J Neuroimmunol. 2006;180(1-2):3-8.
4. Elliott C, Lindner M, Arthur A, Brennan K, Jarius S, Hussey J, et al. Functional identification of pathogenic autoantibody responses in patients with multiple sclerosis. Brain. 2012;135(Pt 6):1819-33. doi: 10.1093/brain/aws105.
5. Storch MK, Piddlesden S, Haltia M, Iivanainen M, Morgan P, Lassmann H. Multiple sclerosis: in situ evidence for antibody- and complement-mediated demyelination. Ann Neurol. 1998;43(4):465-71.
6. Lucchinetti C, Bruck W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann Neurol. 2000;47(6):707-17.
7. Krumbholz M, Derfuss T, Hohlfeld R, Meinl E. B cells and antibodies in multiple sclerosis pathogenesis and therapy. Nat Rev Neurol. 2012;8(11):613-23.
8. Lux A, Nimmerjahn F. Impact of differential glycosylation on IgG activity crossroads between innate and adaptive immunity III. In: Pulendran B, Katsikis PD, Schoenberger SP, editors. Advances in Experimental Medicine and Biology. New York: Springer; 2012. p. 113-24.
9. Huhn C, Selman MHJ, Ruhaak LR, Deelder AM, Wuhrer M. IgG glycosylation analysis. Proteomics. 2009;9(4):882-913. doi: 10.1002/pmic.200800715.
10. Rademacher TW, Williams P, Dwek RA. Agalactosyl glycoforms of IgG autoantibodies are pathogenic. Proc Natl Acad Sci. 1994;91(13):6123-7.
11. Karsten CM, Pandey MK, Figge J, Kilchenstein R, Taylor PR, Rosas M, et al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcgammaRIIB and dectin-1. Nat Med. 2012;18(9):1401-6. doi: 10.1038/nm.2862.
12. Schwab I, Nimmerjahn F. Intravenous immunoglobulin therapy: how does IgG modulate the immune system? Nat Rev Immunol. 2013;13(3):176-89.
13. Nandakumar KS, Collin M, Olsen A, Nimmerjahn F, Blom AM, Ravetch JV, et al. Endoglycosidase treatment abrogates IgG arthritogenicity: importance of IgG glycosylation in arthritis. Eur J Immunol. 2007;37(10):2973-82.
14. Albert H, Collin M, Dudziak D, Ravetch JV, Nimmerjahn F. In vivo enzymatic modulation of IgG glycosylation inhibits autoimmune disease in an IgG subclass-dependent manner. Proc Natl Acad Sci. 2008;105(39):15005-9.
15. Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science. 2006;313(5787):670-3.
16. 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(5874):373-6.
17. von Gunten S, Shoenfeld Y, Blank M, Branch DR, Vassilev T, Kasermann F, et al. IVIG pluripotency and the concept of Fc-sialylation: challenges to the scientist. Nat Rev Immunol. 2014;14(5):349. doi: 10.1038/nri3401-c1.
18. Schwab I, Lux A, Nimmerjahn F. Reply to [mdash] IVIG pluripotency and the concept of Fc-sialylation: challenges to the scientist. Nat Rev Immunol. 2014;14(5):349. doi: 10.1038/nri3401-c2.
19. Ito K, Furukawa J-i, Yamada K, Tran NL, Shinohara Y, Izui S. Lack of galactosylation enhances the pathogenic activity of IgG1 but not IgG2a anti-erythrocyte autoantibodies. J Immunol. 2014;192(2):581-8. doi: 10.4049/jimmunol.1302488.
20. Lifely MR, Hale C, Boyce S, Keen MJ, Phillips J. Glycosylation and biological activity of CAMPATH-1H expressed in different cell lines and grown under different culture conditions. Glycobiology. 1995;5(8):813-22.
21. Umana P, Jean-Mairet J, Moudry R, Amstutz H, Bailey JE. Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat Biotech. 1999;17(2):176-80.
22. Gasdaska JR, Sherwood S, Regan JT, Dickey LF. An afucosylated anti-CD20 monoclonal antibody with greater antibody-dependent cellular cytotoxicity and B-cell depletion and lower complement-dependent cytotoxicity than rituximab. Mol Immunol. 2012;50(3):134-41.
23. Parekh RB, Dwek RA, Sutton BJ, Fernandes DL, Leung A, Stanworth D, et al. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature. 1985;316(6027):452-7.
24. Selman MH, Niks EH, Titulaer MJ, Verschuuren JJ, Wuhrer M, Deelder AM. IgG fc N-glycosylation changes in Lambert-Eaton myasthenic syndrome and myasthenia gravis. J Proteome Res. 2011;10(1):143-52. doi: 10.1021/pr1004373.
25. Fokkink W-JR, Selman MHJ, Dortland JR, Durmuş B, Kuitwaard K, Huizinga R, et al. IgG Fc N-Glycosylation in Guillain-Barré syndrome treated with immunoglobulins. J Proteome Res. 2014;13(3):1722-30. doi: 10.1021/pr401213z.
26. Albrecht S, Unwin L, Muniyappa M, Rudd PM. Glycosylation as a marker for inflammatory arthritis. Cancer Biomark. 2014;14(1):17-28. doi: 10.3233/cbm-130373.
27. Ercan A, Barnes MG, Hazen M, Tory H, Henderson L, Dedeoglu F, et al. Multiple juvenile idiopathic arthritis subtypes demonstrate proinflammatory IgG glycosylation. Arthritis Rheum. 2012;64(9):3025-33. doi: 10.1002/art.34507.
28. Rombouts Y, Ewing E, van de Stadt LA, Selman MHJ, Trouw LA, Deelder AM, et al. Anti-citrullinated protein antibodies acquire a pro-inflammatory Fc glycosylation phenotype prior to the onset of rheumatoid arthritis. Ann Rheum Dis. 2013. doi: 10.1136/annrheumdis-2013-203565.
29. Bradl M, Misu T, Takahashi T, Watanabe M, Mader S, Reindl M, et al. Neuromyelitis optica: pathogenicity of patient immunoglobulin in vivo. Ann Neurol. 2009;66(5):630-43.
30. Bennett JL, Lam C, Kalluri SR, Saikali P, Bautista K, Dupree C, et al. Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann Neurol. 2009;66(5):617-29.
31. Tradtrantip L, Ratelade J, Zhang H, Verkman AS. Enzymatic deglycosylation converts pathogenic neuromyelitis optica anti-aquaporin-4 immunoglobulin G into therapeutic antibody. Ann Neurol. 2013;73(1):77-85. doi: 10.1002/ana.23741.
32. Collin M, Olsen A. Effect of SpeB and EndoS from streptococcus pyogenes on human immunoglobulins. Infect Immun. 2001;69(11):7187-9.
33. Benkhoucha M, Molnarfi N, Santiago-Raber ML, Weber MS, Merkler D, Collin M, et al. IgG glycan hydrolysis by EndoS inhibits experimental autoimmune encephalomyelitis. J Neuroinflammation. 2012;9:209. doi: 10.1186/1742-2094-9-209.
34. van Timmeren MM, van der Veen BS, Stegeman CA, Petersen AH, Hellmark T, Collin M, et al. IgG glycan hydrolysis attenuates ANCA-mediated glomerulonephritis. J Am Soc Nephrol. 2010;21(7):1103-14.
35. Yang R, Otten MA, Hellmark T, Collin M, Björck L, Zhao MH, et al. Successful treatment of experimental glomerulonephritis with IdeS and EndoS, IgG-degrading streptococcal enzymes. Nephrol Dial Transplant. 2010;25(8):2479-86.
36. Song T, Ozcan S, Becker A, Lebrilla CB. In-depth method for the characterization of glycosylation in manufactured recombinant monoclonal antibody drugs. Anal Chem. 2014;86(12):5661-6. doi: 10.1021/ac501102t.
37. Jefferis R. Glycosylation as a strategy to improve antibody-based therapeutics. Nat Rev Drug Discov. 2009;8(3):226-34.
38. Reiber H, Peter JB. Cerebrospinal fluid analysis: disease-related data patterns and evaluation programs. J Neurol Sci. 2001;184(2):101-22.
39. Shikata K, Yasuda T, Takeuchi F, Konishi T, Nakata M, Mizuochi T. Structural changes in the oligosaccharide moiety of human IgG with aging. Glycoconj J. 1998;15(7):683-9.
40. Pucic M, Knezevic A, Vidic J, Adamczyk B, Novokmet M, Polasek O, et al. High throughput isolation and glycosylation analysis of IgG - variability and heritability of the IgG glycome in three isolated human populations. Mol Cell Proteomics. 2011;10(10):M111.010090.
41. Selman MHJ, McDonnell LA, Palmblad M, Ruhaak LR, Deelder AM, Wuhrer M. Immunoglobulin G glycopeptide profiling by matrix-assisted laser desorption ionization fourier transform ion cyclotron resonance mass spectrometry. Anal Chem. 2010;82(3):1073-81. doi: 10.1021/ac9024413.
42. R Core Team. R: A language and environment for statistical computing. 301st ed. Vienna, Austria: R Foundation for Statistical Computing; 2013.
43. Benjamini Y, Hochberg Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995;57(1):289-300.
44. Cleveland WS. Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc. 1979;74(368):829-36.
45. Lux A, Yu X, Scanlan CN, Nimmerjahn F. Impact of immune complex size and glycosylation on IgG binding to human FcγRs. J Immunol. 2013;190(8):4315-23. doi: 10.4049/jimmunol.1200501.
46. Scherer HU, van der Woude D, Ioan-Facsinay A, el Bannoudi H, Trouw LA, Wang J, et al. Glycan profiling of anti-citrullinated protein antibodies isolated from human serum and synovial fluid. Arthritis Rheum. 2010;62(6):1620-9.
47. Collin M, Ehlers M. The carbohydrate switch between pathogenic and immunosuppressive antigen-specific antibodies. Exp Dermatol. 2013;22(8):511-4. doi: 10.1111/exd.12171.
48. Urich E, Gutcher I, Prinz M, Becher B. Autoantibody-mediated demyelination depends on complement activation but not activatory Fc-receptors. Proc Natl Acad Sci. 2006;103(49):18697-702. doi: 10.1073/pnas.0607283103.
49. Torkildsen O, Vedeler CA, Nyland HI, Myhr KM. FcgammaR and multiple sclerosis: an overview. Acta Neurol Scand Suppl. 2006;183:61-3.
50. Eickhoff K, Kaschka W, Skvaril F, Theilkaes L, Heipertz R. Determination of IgG subgroups in cerebrospinal fluid of multiple sclerosis patients and others. Acta Neurol Scand. 1979;60(5):277-82.
51. Losy J, Michalowska-Wender G, Wender M. IgG1-IgG4 subclasses in the cerebrospinal fluid and blood serum and their synthesis in the central nervous system in multiple sclerosis. Neurol Neurochir Pol. 1992;26(3):297-303.
52. Wang J, Balog CIA, Stavenhagen K, Koeleman CAM, Scherer HU, Selman MHJ, et al. Fc-glycosylation of IgG1 is modulated by B-cell stimuli. Mol Cell Proteomics. 2011;10(5):M110.004655.
53. Müthing J, Kemminer SE, Conradt HS, Sagi D, Nimtz M, Kärst U, et al. Effects of buffering conditions and culture pH on production rates and glycosylation of clinical phase I anti-melanoma mouse IgG3 monoclonal antibody R24. Biotechnol Bioeng. 2003;83(3):321-34.
54. García-Vallejo JJ, Ilarregui JM, Kalay H, Chamorro S, Koning N, Unger WW, et al. CNS myelin induces regulatory functions of DC-SIGN-expressing, antigen-presenting cells via cognate interaction with MOG. J Exp Med. 2014;211(7):1465-83. doi: 10.1084/jem.20122192.
55. Functional glycomics gateway. Symbol and text nomenclature for representation of glycan structure. http://www.functionalglycomics.org/static/consortium/Nomenclature.shtml. Accessed 05/28/2014.