N-glycosylation profiling of serum immunoglobulin in opisthorchiasis patients

Sudarat Onsurathum; Muchena J Kailemia; Kitti Intuyod; Ornuma Haonon; Chawalit Pairojkul; Raynoo Thanan; Porntip Pinlaor; Carlito B Lebrilla; Somchai Pinlaor

doi:10.1016/j.jprot.2020.103980

N-glycosylation profiling of serum immunoglobulin in opisthorchiasis patients

J Proteomics. 2021 Jan 6:230:103980. doi: 10.1016/j.jprot.2020.103980. Epub 2020 Sep 11.

Authors

Sudarat Onsurathum¹, Muchena J Kailemia², Kitti Intuyod³, Ornuma Haonon³, Chawalit Pairojkul⁴, Raynoo Thanan⁵, Porntip Pinlaor⁶, Carlito B Lebrilla⁷, Somchai Pinlaor⁸

Affiliations

¹ Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand; Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen 40002, Thailand; Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok 65000, Thailand.
² Department of Chemistry, University of California, Davis, CA 95616, United States.
³ Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand; Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen 40002, Thailand.
⁴ Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen 40002, Thailand; Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand.
⁵ Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen 40002, Thailand; Department of Biochemistry, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand.
⁶ Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen 40002, Thailand; Centre for Research and Development of Medical Diagnostic Laboratories, Faculty of Associated Medical Sciences, Khon Kaen University, Khon Kaen 40002, Thailand.
⁷ Department of Chemistry, University of California, Davis, CA 95616, United States. Electronic address: cblebrilla@ucdavis.edu.
⁸ Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand; Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen 40002, Thailand. Electronic address: psomec@kku.ac.th.

PMID: 32927111
DOI: 10.1016/j.jprot.2020.103980

Abstract

Alteration of immunoglobulin glycosylation correlates with inflammatory diseases and infectious diseases including parasitic infections. Immunoglobulin glycosylation patterns may be implicated in disease development and have also been proposed as diagnostic tools for several diseases. Previous studies have reported the immunoglobulin profiles in experimental animals and in patients infected with the carcinogenic human liver fluke, Opisthorchis viverrini. However, the N-glycosylation profiles of immunoglobulins and their subclass-specific glycoforms in opisthorchiasis patients have never been elucidated. Here, N-glycosylation patterns of immunoglobulins and their subclass-specific glycoforms in sera of O. viverrini-infected patients were investigated using triple quadrupole mass spectrometry coupled with multiple reaction monitoring. Peptide fragmentation was utilized to quantify the immunoglobulin glycoforms normalized to the unique peptide of each subclass. Overall, serum levels of IgG and IgA in O. viverrini patients were significantly increased compared to uninfected controls. Twenty-seven glycoforms were detected based on analysis of detached glycans in all immunoglobulin subclasses. The abundance of immunoglobulin glycopeptides in serum of opisthorchiasis patients deviated significantly from controls. Immunoglobulin glycosylation patterns were associated with both pro- and anti-inflammatory properties. In conclusion, O. viverrini infection alters the serum immunoglobulin glycosylation profile and these changes could distinguish between O. viverrini-infected individuals and healthy controls. SIGNIFICANCE: We demonstrated that both quantities and glycoforms of serum immunoglobulin subclasses were altered in Opisthorchis viverrini-infected individuals as investigated by the QqQ-MS-MRM method. Patterns of immunoglobulin with a specific glycoform might contribute to immune responses to O. viverrini infection.

Keywords: Glycosylation; Immunoglobulin; Multiple reaction monitoring; Opisthorchis viverrini; Serum; Triple quadrupole mass spectrometry.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Glycosylation
Humans
Immunoglobulins
Mass Spectrometry
Opisthorchiasis*
Opisthorchis*

Substances

Immunoglobulins

Grants and funding

R01 GM049077/GM/NIGMS NIH HHS/United States