流感和COVID-19患者之间免疫球蛋白 G 糖基化的差异

Marina Kljaković-Gašpić Batinjan, Tea Petrović, Frano Vučković, Irzal Hadžibegović, Barbara Radovani, Ivana Jurin, Lovorka Đerek, Eva Huljev, Alemka Markotić, Ivica Lukšić, Irena Trbojević-Akmačić, Gordan Lauc, Ivan Gudelj, Rok Čivljak

工程(英文) ›› 2023, Vol. 26 ›› Issue (7) : 54-62.

PDF(1378 KB)
PDF(1378 KB)
工程(英文) ›› 2023, Vol. 26 ›› Issue (7) : 54-62. DOI: 10.1016/j.eng.2022.08.007
研究论文
Article

流感和COVID-19患者之间免疫球蛋白 G 糖基化的差异

作者信息 +

Differences in Immunoglobulin G Glycosylation Between Influenza and COVID-19 Patients

Author information +
History +

摘要

如果不了解与可结晶片段(Fc)结构域天冬酰胺297 相连的N-聚糖发生的变化,就无法充分认识免疫球蛋白G(IgG)在免疫系统调节和对抗传染病中的重要作用。这些聚糖影响抗体稳定性、半衰期、分泌、免疫原性和效应子功能。因此,本研究分析并比较了64 名流感患者、77 名新冠病毒肺炎(COVID-19)患者和56 名健康对照者的总IgG 糖组——在单个聚糖结构和衍生糖基化特征[唾液酸化、半乳糖基化、岩藻糖基化和平分型N-乙酰氨基葡萄糖(GlcNAc)]的水平上。本研究显示,已故的COVID-19 患者中IgG 半乳糖基化、唾液酸化和平分型GlcNAc 显著减少(其中平分型GlcNAc 显示出最显著的减少),而IgG 岩藻糖基化则增加。另外,流感患者和COVID-19 幸存者中IgG 半乳糖基化保持稳定。流感患者的IgG 糖基化更具时间依赖性:在疾病的前7 天,唾液酸化增加,岩藻糖基化和平分型GlcNAc减少;在接下来的21 天内,唾液酸化减少,岩藻糖化增加(而平分型GlcNAc保持稳定)。COVID-19 幸存者和流感患者IgG糖基化变化的相似性可能是对包膜病毒产生充分免疫反应的结果,而在已故COVID-19 患者中观察到的变化可能表明其偏差。

Abstract

The essential role of immunoglobulin G (IgG) in immune system regulation and combatting infectious diseases cannot be fully recognized without an understanding of the changes in its N-glycans attached to the asparagine 297 of the Fc domain that occur under such circumstances. These glycans impact the antibody stability, half-life, secretion, immunogenicity, and effector functions. Therefore, in this study, we analyzed and compared the total IgG glycome—at the level of individual glycan structures and derived glycosylation traits (sialylation, galactosylation, fucosylation, and bisecting N-acetylglucosamine (GlcNAc))—of 64 patients with influenza, 77 patients with coronavirus disease 2019 (COVID-19), and 56 healthy controls. Our study revealed a significant decrease in IgG galactosylation, sialylation, and bisecting GlcNAc (where the latter shows the most significant decrease) in deceased COVID-19 patients, whereas IgG fucosylation was increased. On the other hand, IgG galactosylation remained stable in influenza patients and COVID-19 survivors. IgG glycosylation in influenza patients was more time-dependent: In the first seven days of the disease, sialylation increased and fucosylation and bisecting GlcNAc decreased; in the next 21 days, sialylation decreased and fucosylation increased (while bisecting GlcNAc remained stable). The similarity of IgG glycosylation changes in COVID-19 survivors and influenza patients may be the consequence of an adequate immune response to enveloped viruses, while the observed changes in deceased COVID-19 patients may indicate its deviation.

关键词

流感 / 新冠病毒肺炎 / 病毒感染 / 糖基化 / 免疫球蛋白G / 肺炎

Keywords

Influenza / COVID-19 / Viral infection / Glycosylation / Immunoglobulin G / Pneumonia

引用本文

导出引用
Marina Kljaković-Gašpić Batinjan, Tea Petrović, Frano Vučković. 流感和COVID-19患者之间免疫球蛋白 G 糖基化的差异. Engineering. 2023, 26(7): 54-62 https://doi.org/10.1016/j.eng.2022.08.007

参考文献

[1]
Szucs T. The socio-economic burden of influenza. J Antimicrob Chemother 1999;44(Suppl B):11–5.
[2]
Suthar S, Das S, Nagpure A, Madhurantakam C, Tiwari SB, Gahlot P, et al. Epidemiology and diagnosis, environmental resources quality and socioeconomic perspectives for COVID-19 pandemic. J Environ Manage 2021;280:111700.
[3]
Piroth L, Cottenet J, Mariet AS, Bonniaud P, Blot M, Tubert-Bitter P, et al. Comparison of the characteristics, morbidity, and mortality of COVID-19 and seasonal influenza: a nationwide, population-based retrospective cohort study. Lancet Respir Med 2021;9(3):251–9.
[4]
Petersen E, Koopmans M, Go U, Hamer DH, Petrosillo N, Castelli F, et al. Comparing SARS-CoV-2 with SARS-CoV and influenza pandemics. Lancet Infect Dis 2020;20(9):e238–44.
[5]
Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia. JAMA 2020;323(11):1061–9.
[6]
Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus. Lancet 2020;395(10223):497–506.
[7]
Thevarajan I, Nguyen THO, Koutsakos M, Druce J, Caly L, van de Sandt CE, et al. Breadth of concomitant immune responses prior to patient recovery: a case report of non-severe COVID-19. Nat Med 2020;26(4):453–5.
[8]
Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, Morrissey M, et al. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 2011;208 (1):181–93.
[9]
Chiu C, Ellebedy AH, Wrammert J, Ahmed R. B cell responses to influenza infection and vaccination. Curr Top Microbiol Immunol 2015;386:381–98.
[10]
Plebani A, Ugazio AG, Avanzini MA, Massimi P, Zonta L, Monafo V, et al. Serum IgG subclass concentrations in healthy subjects at different age: age normal percentile charts. Eur J Pediatr 1989;149(3):164–7.
[11]
Gornik O, Pavic´ T, Lauc G. Alternative glycosylation modulates function of IgG and other proteins—implications on evolution and disease. Biochim Biophys Acta 2012;1820(9):1318–26.
[12]
Vidarsson G, Dekkers G, Rispens T. IgG subclasses and allotypes: from structure to effector functions. Front Immunol 2014;5:520.
[13]
Kobata A. The N-linked sugar chains of human immunoglobulin G: their unique pattern, and their functional roles. Biochim Biophys Acta 2008;1780 (3):472–8.
[14]
Gudelj I, Lauc G, Pezer M. Immunoglobulin G glycosylation in aging and diseases. Cell Immunol 2018;333:65–79.
[15]
Lux A, Yu X, Scanlan CN, Nimmerjahn F. Impact of immune complex size and glycosylation on IgG binding to human FccRs. J Immunol 2013;190(8):4315–23.
[16]
Czajkowsky DM, Andersen JT, Fuchs A, Wilson TJ, Mekhaiel D, Colonna M, et al. Developing the IVIG biomimetic, hexa-Fc, for drug and vaccine applications. Sci Rep 2015;5(1):9256.
[17]
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 FccRIII and antibody-dependent cellular toxicity. J Biol Chem 2002;277(30):26733–40.
[18]
Forthal DN, Gach JS, Landucci G, Jez J, Strasser R, Kunert R, et al. Fcglycosylation influences Fcc receptor binding and cell-mediated anti-HIV activity of monoclonal antibody 2G12. J Immunol 2010;185(11):6876–82.
[19]
Larsen MD, de Graaf EL, Sonneveld ME, Plomp HR, Nouta J, Hoepel W, et al. Afucosylated IgG characterizes enveloped viral responses and correlates with COVID-19 severity. Science 2021;371(6532):eabc8378.
[20]
Hoepel W, Chen HJ, Geyer CE, Allahverdiyeva S, Manz XD, de Taeye SW, et al. High titers and low fucosylation of early human anti-SARS-CoV-2 IgG promote inflammation by alveolar macrophages. Sci Transl Med 2021;13(596): eabf8654.
[21]
Ackerman ME, Crispin M, Yu X, Baruah K, Boesch AW, Harvey DJ, et al. Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity. J Clin Invest 2013;123(5):2183–92.
[22]
Wang TT, Sewatanon J, Memoli MJ, Wrammert J, Bournazos S, Bhaumik SK, et al. IgG antibodies to dengue enhanced for FccRIIIA binding determine disease severity. Science 2017;355(6323):395–8.
[23]
Larsen MD, de Graaf EL, Sonneveld ME, Plomp HR, Nouta J, Hoepel W, et al. Afucosylated IgG characterizes enveloped viral responses and correlates with COVID-19 severity. Science 2021;371(6532):eabc8378.
[24]
Pucic´ M, Knezevic´ A, Vidicˇ J, Adamczyk B, Novokmet M, Polašek 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):010090.
[25]
Deriš H, Cindric´ A, Lauber M, Petrovic´ T, Bielik A, Taron CH, et al. Robustness and repeatability of GlycoWorks RapiFluor-MS IgG N-glycan profiling in a long-term high-throughput glycomic study. Glycobiology 2021;31(9): 1062–7.
[26]
Keser T, Pavic´ T, Lauc G, Gornik O. Comparison of 2-aminobenzamide, procainamide and RapiFluor-MS as derivatizing agents for high-throughput HILIC-UPLC-FLR-MS N-glycan analysis. Front Chem 2018;6:324.
[27]
Petrovic´ T, Alves I, Bugada D, Pascual J, Vucˇkovic´ F, Skelin A, et al. Composition of the immunoglobulin G glycome associates with the severity of COVID-19. Glycobiology 2021;31(4):372–7.
[28]
Bournazos S, Vo HTM, Duong V, Auerswald H, Ly S, Sakuntabhai A, et al. Antibody fucosylation predicts disease severity in secondary dengue infection. Science 2021;372(6546):1102–5.
[29]
Olbei M, Hautefort I, Modos D, Treveil A, Poletti M, Gul L, et al. SARS-CoV-2 causes a different cytokine response compared to other cytokine stormcausing respiratory viruses in severely Ill patients. Front Immunol 2021;12:629193.
[30]
Liu Q, Zhou YH, Yang ZQ. The cytokine storm of severe influenza and development of immunomodulatory therapy. Cell Mol Immunol 2016;13 (1):3–10.
[31]
Giron LB, Colomb F, Papasavvas E, Azzoni L, Yin X, Fair M, et al. Interferon-a alters host glycosylation machinery during treated HIV infection. EBioMedicine 2020;59:102945.
[32]
Kurimoto A, Kitazume S, Kizuka Y, Nakajima K, Oka R, Fujinawa R, et al. The absence of core fucose up-regulates GnT-III and Wnt target genes: a possible mechanism for an adaptive response in terms of glycan function. J Biol Chem 2014;289(17):11704–14.
[33]
Wang T, Maamary J, Tan G, Bournazos S, Davis C, Krammer F, et al. Anti-HA glycoforms drive B cell affinity selection and determine influenza vaccine efficacy. Cell 2015;162(1):160–9.
[34]
Irvine EB, Alter G. Understanding the role of antibody glycosylation through the lens of severe viral and bacterial diseases. Glycobiology 2020;30 (4):241–53.
[35]
Huang T, Chen X, Zhao C, Liu X, Zhang Z, Li T, et al. Sialylated immunoglobulin G can neutralize influenza virus infection through receptor mimicry. Oncotarget 2016;7(13):15606–17.
PDF(1378 KB)

Accesses

Citation

Detail

段落导航
相关文章

/