Control of lupus activity during pregnancy via the engagement of IgG sialylation: novel crosstalk between IgG sialylation and pDC functions

doi:10.1007/s11684-022-0965-7

Front. Med.

2023, Vol. 17

Issue (3) : 549-561 https://doi.org/10.1007/s11684-022-0965-7

RESEARCH ARTICLE

Control of lupus activity during pregnancy via the engagement of IgG sialylation: novel crosstalk between IgG sialylation and pDC functions

You Wang^1,^2,³, Sihan Lin^1,^2,³, Jiayue Wu^1,^2,³, Meng Jiang^1,^2,³, Jianhua Lin^1,^2,³, Yu Zhang^1,^2,³, Huihua Ding⁴, Haibo Zhou⁴(

), Nan Shen^4,^5,⁶(

), Wen Di^1,^2,³(

)

¹. Department of Obstetrics and Gynaecology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai 200127, China
². Shanghai Key Laboratory of Gynaecologic Oncology, Shanghai 200127, China
³. State Key Laboratory of Oncogenes and Related Genes, Shanghai Cancer Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai 200127, China
⁴. Shanghai Institute of Rheumatology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai 200001, China
⁵. Center for Autoimmune Genomics and Etiology (CAGE), Cincinnati Children’s Hospital Medical Center, Cincinnati Ohio 45229, USA
⁶. Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati Ohio 45267, USA

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Abstract

Immunoglobulin (IgG) glycosylation affects the effector functions of IgG in a myriad of biological processes and has been closely associated with numerous autoimmune diseases, including systemic lupus erythematosus (SLE), thus underlining the pathogenic role of glycosylation aberration in autoimmunity. This study aims to explore the relationship between IgG sialylation patterns and lupus pregnancy. Relative to that in serum samples from the control cohort, IgG sialylation level was aberrantly downregulated in serum samples from the SLE cohort at four stages (from preconception to the third trimester of pregnancy) and was significantly associated with lupus activity and fetal loss during lupus pregnancy. The type I interferon signature of pregnant patients with SLE was negatively correlated with the level of IgG sialylation. The lack of sialylation dampened the ability of IgG to suppress the functions of plasmacytoid dendritic cells (pDCs). RNA-seq analysis further revealed that the expression of genes associated with the spleen tyrosine kinase (SYK) signaling pathway significantly differed between IgG- and deSia-IgG-treated pDCs. This finding was confirmed by the attenuation of the ability to phosphorylate SYK and BLNK in deSia-IgG. Finally, the coculture of pDCs isolated from pregnant patients with SLE with IgG/deSia-IgG demonstrated the sialylation-dependent anti-inflammatory function of IgG. Our findings suggested that IgG influences lupus activity through regulating pDCs function via the modulation of the SYK pathway in a sialic acid-dependent manner.

Keywords pregnancy IgG glycome type I interferon systemic lupus erythematosus

Corresponding Author(s): Haibo Zhou,Nan Shen,Wen Di

Just Accepted Date: 22 February 2023 Online First Date: 07 April 2023 Issue Date: 28 July 2023

Cite this article:

You Wang,Sihan Lin,Jiayue Wu, et al. Control of lupus activity during pregnancy via the engagement of IgG sialylation: novel crosstalk between IgG sialylation and pDC functions[J]. Front. Med., 2023, 17(3): 549-561.

URL:

https://academic.hep.com.cn/fmd/EN/10.1007/s11684-022-0965-7
https://academic.hep.com.cn/fmd/EN/Y2023/V17/I3/549

Fig.1 Flow chart for identifying SLE and control cohorts.

Fig.2 IgG sialylation is associated with disease activity and fetal loss in pregnant females with SLE. (A) Representative chromatogram of a sample from a pregnant patient with SLE. The composition of total IgG N-glycans separated into 24 chromatographic glycan peaks (GP1–GP24, with GP8 consisting of GP8a and GP8b, GP16 formed by GP16a and GP16b, and GP18 comprising GP18a and GP18b). Each glycan peak corresponded to a specific glycan structure that was named in accordance with the naming system presented in Table S2. (B) Comparison of IgG sialylation levels between two cohorts (SLE and control). Abbreviations: pre, preconception; trim, trimester; S total, proportion of sialylated structures in total IgG glycans; S1 total, proportion of monosialylated structures in total IgG glycans. Results of two groups were compared by using unpaired t-test if normally distributed and by Mann–Whitney U test if distributed otherwise. * P < 0.05, ** P < 0.01. (C) Pearson’s correlation analysis of clinical parameters with sialylated IgG glycans. (D) ROC curves illustrating the discriminative power of IgG-derived traits (S total and S1 total) (solid line) for fetal survival in patients with SLE during the second trimester. Results of two groups were compared through unpaired t-test if normally distributed and by Mann–Whitney U test if distributed otherwise. ** P < 0.01. (E) Pearson’s correlation analysis of ISGs of PBMCs from 13 pregnant patients with SLE with sialylated-derived glycan traits.

Fig.3 Lack of sialylation dampens the ability of IgG to suppress the function of activated pDCs. Primary human pDCs purified from the PBMCs of 10 healthy female donors were preincubated with IgG or deSia-IgG then stimulated with ODN2216 and R848 overnight. (A) Levels of the costimulatory molecules CD40 and HLADR assessed by flow cytometry. The same control group without any stimulation was used for both R848 and CpG groups. (B) Production of IFN-I and (C) other cytokines (IL-6 and TNF-α) measured in the cell supernatant by using ELISA and CBA, respectively. MFI, mean fluorescence intensity. Results of two groups were compared by using unpaired t-test. * P < 0.05, ** P < 0.01, *** P < 0.001, **** P < 0.0001. ns, not significant.

Fig.4 IgG transduces signals via the SYK pathway. Primary human pDCs purified from the PBMCs of 10 healthy female donors were preincubated with IgG or deSia-IgG then stimulated with CpG overnight. (A) Kyoto Encyclopedia of Genes and Genomes enrichment bubble chart showing the enrichment of differentially expressed genes between IgG and deSia-IgG. (B) GSEA determining the concordant differences in TLR-related gene sets between different groups. (C) Heatmap representing changed genes enriched in the TLR and IFN-I pathways among the three groups. (D) Kinase enrichment analysis showing that differentially expressed genes (CpG + IgG vs. CpG + deSia-IgG) were enriched in the SYK pathway. (E) Changed genes activated or inhibited by SYK. Red, upregulated by IgG; Green, downregulated by IgG.

Fig.5 Sialylation is necessary for IgG to enhance SYK pathway activation. Human pDCs (from 10 healthy female donors) were fixed with prewarmed buffer, permeabilized at room temperature, then stained with pY348 and pY84. (A) Phosphorylation of SYK and BLNK measured through flow cytometry. (B) Intracellular levels of phosphorylated IRF-7 in pDCs analyzed through flow cytometry. Abbreviations: MFI, mean fluorescence intensity. Results of two groups were compared by using unpaired t-test. * P < 0.05, ** P < 0.01, *** P < 0.001, **** P < 0.0001. ns, not significant.

Fig.6 IgG inhibits the activation of pDCs from pregnant patients with SLE in a sialylation-dependent manner. Purified pDCs pooled from seven pregnant patients with SLE were pretreated with IgG and deSia-IgG at the concentration of 10 mg/mL then stimulated with CpG (0.5 μmol/L). Results of two groups were compared by using unpaired t-test. * P < 0.05, ** P < 0.01, *** P < 0.001, **** P < 0.0001. ns, not significant.

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