ACS Publications. Most Trusted. Most Cited. Most Read

OR SEARCH CITATIONS

My Activity
Publications
CONTENT TYPES

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Proteome Res. 2014, 13, 3, 1722-1730
RETURN TO ISSUEPREVArticleNEXT

IgG Fc N-Glycosylation in Guillain–Barré Syndrome Treated with Immunoglobulins

View Author Information
† ‡ †Department of Immunology, ‡Department of Neurology, and §Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Dr. Molewaterplein 50, 3000 CA Rotterdam, The Netherlands
∥ Center for Proteomics and Metabolomics, Leiden University Medical Center, 2300 RC Leiden, The Netherlands
*Phone: +31 10 704 3999. Fax +31 01 704 4727. E-mail: [email protected]
Cite this: J. Proteome Res. 2014, 13, 3, 1722–1730
Publication Date (Web):February 17, 2014
https://doi.org/10.1021/pr401213z
Copyright © 2014 American Chemical Society
Request reuse permissions

    Article Views

    1115

    Altmetric

    -

    Citations

    43
    LEARN ABOUT THESE METRICS
    Other access options
    Get e-Alerts
    SUBJECTS:

    Abstract

    Abstract Image

    Intravenous immunoglobulin (IVIg) is the treatment of choice for Guillain–Barré syndrome (GBS), an immune-mediated peripheral neuropathy causing rapidly progressive limb weakness and respiratory failure. The working mechanism of IVIg in autoimmune diseases has not been elucidated, but previous studies indicate that some anti-inflammatory effects may be mediated by the N-glycosylation of the Fc-portion of IgG. GBS is a model disease to investigate these effects because GBS is an acute and monophasic disorder usually affecting healthy persons, which is treated with a standard course of IVIg, although the clinical response is highly variable. In the current study, the N-glycosylation of the Fc-portion of serum IgG was investigated in patients with GBS before and after treatment with IVIg in relation to clinical course and outcome. Glycoforms of serum IgG1 and IgG2 were determined separately by liquid chromatography mass spectrometry. These IgG subclasses were purified from the serum of 174 GBS patients before and in 150 patients 2 weeks after standard IVIg treatment regimen. Treatment-naive GBS patients compared with age- and sex-matched controls had lower levels of galactosylation of IgG1 and IgG2. IVIg preparations contained relatively high levels of galactosylated and sialylated IgG Fc glycoforms compared with serum IgG in patients. Treatment with IVIg resulted in an increase in serum of the Fc-galactosylation and -sialylation of both IgG1 and IgG2. The extent of normalization in serum IgG Fc glycosylation varied between patients. Multiple logistic regression analysis showed that patients with persistent low IgG galactosylation and sialylation despite IVIg treatment had the most severe forms of GBS and needed ventilator support more often. Kaplan–Meier analysis showed that these patients also needed more time to be able to walk again compared with patients with a normalized IgG Fc glycosylation profile. In conclusion, our results suggest that serum IgG Fc glycosylation in GBS is related to disease severity and clinical recovery after IVIg and may help to develop new measures to monitor the efficacy of treatment.

    KEYWORDS:

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    Cited By

    This article is cited by 43 publications.

    1. Irena Trbojević-Akmačić, Guinevere S. M. Lageveen-Kammeijer, Bram Heijs, Tea Petrović, Helena Deriš, Manfred Wuhrer, Gordan Lauc. High-Throughput Glycomic Methods. Chemical Reviews 2022, 122 (20) , 15865-15913. https://doi.org/10.1021/acs.chemrev.1c01031
    2. Yannick Kronimus, Alexandra Albus, Mike Hasenberg, Bernd Walkenfort, Marc Seifert, Bettina Budeus, Janine Gronewold, Dirk M. Hermann, J. Alexander Ross, Günter Lochnit, Sebastian P. Galuska, Katrin Marcus, Barbara Sitek, Jens Klotsche, David Mengel, Sascha Neumann, Richard Dodel. Fc N‐glycosylation of autoreactive Aβ antibodies as a blood‐based biomarker for Alzheimer's disease. Alzheimer's & Dementia 2023, 19 (12) , 5563-5572. https://doi.org/10.1002/alz.13124
    3. Ana Turčić, Barbara Radovani, Željka Vogrinc, Mario Habek, Dunja Rogić, Tereza Gabelić, Ljiljana Zaninović, Gordan Lauc, Ivan Gudelj. Higher MRI lesion load in multiple sclerosis is related to the N-glycosylation changes of cerebrospinal fluid immunoglobulin G. Multiple Sclerosis and Related Disorders 2023, 79 , 104921. https://doi.org/10.1016/j.msard.2023.104921
    4. Renato Mastrangeli, Abhijeet Satwekar, Horst Bierau. Innovative Metrics for Reporting and Comparing the Glycan Structural Profile in Biotherapeutics. Molecules 2023, 28 (8) , 3304. https://doi.org/10.3390/molecules28083304
    5. Alessandro Allegra, Nicola Cicero, Giuseppe Mirabile, Concetto Mario Giorgianni, Sebastiano Gangemi. Novel Biomarkers for Diagnosis and Monitoring of Immune Thrombocytopenia. International Journal of Molecular Sciences 2023, 24 (5) , 4438. https://doi.org/10.3390/ijms24054438
    6. Benjamin S. Haslund-Gourley, Brian Wigdahl, Mary Ann Comunale. IgG N-glycan Signatures as Potential Diagnostic and Prognostic Biomarkers. Diagnostics 2023, 13 (6) , 1016. https://doi.org/10.3390/diagnostics13061016
    7. Jana Sophia Buhre, Mareike Becker, Marc Ehlers. IgG subclass and Fc glycosylation shifts are linked to the transition from pre- to inflammatory autoimmune conditions. Frontiers in Immunology 2022, 13 https://doi.org/10.3389/fimmu.2022.1006939
    8. Wei Wang, Xuewen Xu, Chenjun Huang, Chunfang Gao. N‐glycan profiling alterations of serum and immunoglobulin G in immune thrombocytopenia. Journal of Clinical Laboratory Analysis 2022, 36 (2) https://doi.org/10.1002/jcla.24201
    9. Yusuke Mimura, Yuka Mimura-Kimura, Radka Saldova, Pauline M. Rudd, Roy Jefferis. Enhanced Immunomodulatory Effect of Intravenous Immunoglobulin by Fc Galactosylation and Nonfucosylation. Frontiers in Immunology 2022, 13 https://doi.org/10.3389/fimmu.2022.818382
    10. Iwona Wojcik, David E. Schmidt, Lisa A. de Neef, Minke A. E. Rab, Bob Meek, Okke de Weerdt, Manfred Wuhrer, C. Ellen van der Schoot, Jaap J. Zwaginga, Masja de Haas, David Falck, Gestur Vidarsson. A functional spleen contributes to afucosylated IgG in humans. Scientific Reports 2021, 11 (1) https://doi.org/10.1038/s41598-021-03196-w
    11. Marija Pezer. Immunoglobulin G Glycosylation in Diseases. 2021, 395-431. https://doi.org/10.1007/978-3-030-76912-3_13
    12. Richard J. Pleass. The therapeutic potential of sialylated Fc domains of human IgG. mAbs 2021, 13 (1) https://doi.org/10.1080/19420862.2021.1953220
    13. Fabio Dall’Olio, Nadia Malagolini. Immunoglobulin G Glycosylation Changes in Aging and Other Inflammatory Conditions. 2021, 303-340. https://doi.org/10.1007/978-3-030-76912-3_10
    14. David E. Schmidt, Noortje de Haan, Myrthe E. Sonneveld, Leendert Porcelijn, C. Ellen van der Schoot, Masja de Haas, Jaap-Jan Zwaginga, Manfred Wuhrer, Gestur Vidarsson. IgG-Fc glycosylation before and after rituximab treatment in immune thrombocytopenia. Scientific Reports 2020, 10 (1) https://doi.org/10.1038/s41598-020-59651-7
    15. Yuliya V. Markina, Elena V. Gerasimova, Alexander M. Markin, Victor Y. Glanz, Wei-Kai Wu, Igor A. Sobenin, Alexander N. Orekhov. Sialylated Immunoglobulins for the Treatment of Immuno-Inflammatory Diseases. International Journal of Molecular Sciences 2020, 21 (15) , 5472. https://doi.org/10.3390/ijms21155472
    16. Yu. V. Markina, A. M. Markin, I. A. Sobenin, A. N. Orekhov. Prospects for the use of sialylated immunoglobulins in the treatment of different diseases. Fundamental and Clinical Medicine 2020, 5 (2) , 112-118. https://doi.org/10.23946/2500-0764-2020-5-2-112-118
    17. Taia T. Wang, Jeffrey V. Ravetch. Functional diversification of IgGs through Fc glycosylation. Journal of Clinical Investigation 2019, 129 (9) , 3492-3498. https://doi.org/10.1172/JCI130029
    18. Mami Matsuda-Lennikov, Matthew Biancalana, Juan Zou, Juan C. Ravell, Lixin Zheng, Chrysi Kanellopoulou, Ping Jiang, Giulia Notarangelo, Huie Jing, Evan Masutani, Andrew J. Oler, Lisa Renee Olano, Benjamin L. Schulz, Michael J. Lenardo. Magnesium transporter 1 (MAGT1) deficiency causes selective defects in N-linked glycosylation and expression of immune-response genes. Journal of Biological Chemistry 2019, 294 (37) , 13638-13656. https://doi.org/10.1074/jbc.RA119.008903
    19. Lee-Fong Yau, Ju Liu, Min Jiang, Gang Bai, Jing-Rong Wang, Zhi-Hong Jiang. An integrated approach for comprehensive profiling and quantitation of IgG-Fc glycopeptides with application to rheumatoid arthritis. Journal of Chromatography B 2019, 1122-1123 , 64-72. https://doi.org/10.1016/j.jchromb.2019.05.027
    20. Mario Montoya Jaramillo, Felipe Herrera Ruiz, Edgar Eliud Castillo, Alexander Pabón Moreno, Neylor Chalabe Jimenez, Víctor Leal Martínez, Jeison Torrens Soto, Leonardo Fontecha Gomez. Síndrome de Guillain-Barré asociado al uso de Adalimumab en un paciente con colitis ulcerosa. A propósito de un caso. Acta Colombiana de Cuidado Intensivo 2019, 19 (2) , 117-121. https://doi.org/10.1016/j.acci.2018.09.001
    21. Christopher Beneduce, Elma Kurtagic, Carlos J. Bosques. Anti-inflammatory Activity of IgG-Fc. 2019, 35-62. https://doi.org/10.1007/82_2019_148
    22. Taia T. Wang. IgG Fc Glycosylation in Human Immunity. 2019, 63-75. https://doi.org/10.1007/82_2019_152
    23. Yannick Kronimus, Richard Dodel, Sebastian P. Galuska, Sascha Neumann. IgG Fc N-glycosylation: Alterations in neurologic diseases and potential therapeutic target?. Journal of Autoimmunity 2019, 96 , 14-23. https://doi.org/10.1016/j.jaut.2018.10.006
    24. Ivan Gudelj, Gordan Lauc, Marija Pezer. Immunoglobulin G glycosylation in aging and diseases. Cellular Immunology 2018, 333 , 65-79. https://doi.org/10.1016/j.cellimm.2018.07.009
    25. Galit Alter, Tom H.M. Ottenhoff, Simone A. Joosten. Antibody glycosylation in inflammation, disease and vaccination. Seminars in Immunology 2018, 39 , 102-110. https://doi.org/10.1016/j.smim.2018.05.003
    26. Kyle T. Amber, Jessica Shiu, Katherine Ferris, Sergei A. Grando. Role of Intravenous Immunoglobulin in Dermatologic Disorders. 2018, 401-423. https://doi.org/10.1007/978-3-319-66884-0_39
    27. Michaela Seeling, Christin Brückner, Falk Nimmerjahn. Differential antibody glycosylation in autoimmunity: sweet biomarker or modulator of disease activity?. Nature Reviews Rheumatology 2017, 13 (10) , 621-630. https://doi.org/10.1038/nrrheum.2017.146
    28. Rogier van Gent, Herold J. Metselaar, Jaap Kwekkeboom. Immunomodulation by hyperimmunoglobulins after solid organ transplantation: Beyond prevention of viral infection. Transplantation Reviews 2017, 31 (2) , 78-86. https://doi.org/10.1016/j.trre.2017.01.001
    29. Myrthe E. Sonneveld, Joke Koelewijn, Masja de Haas, Jon Admiraal, Rosina Plomp, Carolien A. M. Koeleman, Agnes L. Hipgrave Ederveen, Peter Ligthart, Manfred Wuhrer, C. Ellen van der Schoot, Gestur Vidarsson. Antigen specificity determines anti‐red blood cell IgG‐Fc alloantibody glycosylation and thereby severity of haemolytic disease of the fetus and newborn. British Journal of Haematology 2017, 176 (4) , 651-660. https://doi.org/10.1111/bjh.14438
    30. S. Könemann, M. Dörr, S.B. Felix. Cardiac Immunomodulation. 2017, 681-714. https://doi.org/10.1016/B978-0-12-803267-1.00028-4
    31. Dan Zhang, Bingchao Chen, Yanmin Wang, Peng Xia, Chengyan He, Yujie Liu, Ruiqing Zhang, Mo Zhang, Zhili Li. Disease-specific IgG Fc N-glycosylation as personalized biomarkers to differentiate gastric cancer from benign gastric diseases. Scientific Reports 2016, 6 (1) https://doi.org/10.1038/srep25957
    32. Anna Hiu Yi Wong, Yuki Fukami, Makoto Sudo, Norito Kokubun, Shinsuke Hamada, Nobuhiro Yuki. Sialylated IgG-Fc: a novel biomarker of chronic inflammatory demyelinating polyneuropathy. Journal of Neurology, Neurosurgery & Psychiatry 2016, 87 (3) , 275-279. https://doi.org/10.1136/jnnp-2014-309964
    33. Manfred Wuhrer, Maurice H. J. Selman, Liam A. McDonnell, Tania Kümpfel, Tobias Derfuss, Mohsen Khademi, Tomas Olsson, Reinhard Hohlfeld, Edgar Meinl, Markus Krumbholz. Pro-inflammatory pattern of IgG1 Fc glycosylation in multiple sclerosis cerebrospinal fluid. Journal of Neuroinflammation 2015, 12 (1) https://doi.org/10.1186/s12974-015-0450-1
    34. Willem Jan R. Fokkink, David Falck, Tom C. M. Santbergen, Ruth Huizinga, Manfred Wuhrer, Bart C. Jacobs, . Comparison of Fc N-Glycosylation of Pharmaceutical Products of Intravenous Immunoglobulin G. PLOS ONE 2015, 10 (10) , e0139828. https://doi.org/10.1371/journal.pone.0139828
    35. Isaak Quast, Christian W. Keller, Michael A. Maurer, John P. Giddens, Björn Tackenberg, Lai-Xi Wang, Christian Münz, Falk Nimmerjahn, Marinos C. Dalakas, Jan D. Lünemann. Sialylation of IgG Fc domain impairs complement-dependent cytotoxicity. Journal of Clinical Investigation 2015, 125 (11) , 4160-4170. https://doi.org/10.1172/JCI82695
    36. Nathaniel Washburn, Inessa Schwab, Daniel Ortiz, Naveen Bhatnagar, Jonathan C. Lansing, Amy Medeiros, Steven Tyler, Divya Mekala, Edward Cochran, Hetal Sarvaiya, Kevin Garofalo, Robin Meccariello, James W. Meador, Laura Rutitzky, Birgit C. Schultes, Leona Ling, William Avery, Falk Nimmerjahn, Anthony M. Manning, Ganesh V. Kaundinya, Carlos J. Bosques. Controlled tetra-Fc sialylation of IVIg results in a drug candidate with consistent enhanced anti-inflammatory activity. Proceedings of the National Academy of Sciences 2015, 112 (11) https://doi.org/10.1073/pnas.1422481112
    37. Jan D. Lünemann, Falk Nimmerjahn, Marinos C. Dalakas. Intravenous immunoglobulin in neurology—mode of action and clinical efficacy. Nature Reviews Neurology 2015, 11 (2) , 80-89. https://doi.org/10.1038/nrneurol.2014.253
    38. Jacqueline Kerr, Isabella Quinti, Martha Eibl, Helen Chapel, Peter J. Späth, W. A. Carrock Sewell, Abdulgabar Salama, Ivo N. van Schaik, Taco W. Kuijpers, Hans-Hartmut Peter. Is Dosing of Therapeutic Immunoglobulins Optimal? A Review of a Three-Decade Long Debate in Europe. Frontiers in Immunology 2014, 5 https://doi.org/10.3389/fimmu.2014.00629
    39. M. Basta, D. R. Branch. 7 th International Immunoglobulin Conference: Mechanisms of Action. Clinical & Experimental Immunology 2014, 178 , 87-88. https://doi.org/10.1111/cei.12523
    40. W.-J. R. Fokkink, M. H. C. Selman, M. Wuhrer, B. C. Jacobs. Immunoglobulin G Fc N-glycosylation in Guillain-Barré syndrome treated with intravenous immunoglobulin. Clinical & Experimental Immunology 2014, 178 , 105-107. https://doi.org/10.1111/cei.12530
    41. S. Jolles, S. C. Jordan, J. S. Orange, I. N. van Schaik. Immunoglobulins: current understanding and future directions. Clinical & Experimental Immunology 2014, 178 , 163-168. https://doi.org/10.1111/cei.12555
    42. Bianca van den Berg, Christa Walgaard, Judith Drenthen, Christiaan Fokke, Bart C. Jacobs, Pieter A. van Doorn. Guillain–Barré syndrome: pathogenesis, diagnosis, treatment and prognosis. Nature Reviews Neurology 2014, 10 (8) , 469-482. https://doi.org/10.1038/nrneurol.2014.121
    43. W. A. Carrock Sewell, Jacqueline Kerr, Marie‐Emmanuelle Behr‐Gross, Hans‐Hartmut Peter, . European consensus proposal for immunoglobulin therapies. European Journal of Immunology 2014, 44 (8) , 2207-2214. https://doi.org/10.1002/eji.201444700
    Download PDF

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect