Altered O-linked glycosylation in benign and malignant meningiomas
Background Changes in protein glycosylation have been reported in various diseases, including cancer; however, the consequences of altered glycosylation in meningiomas remains undefined. We established two benign meningioma cell lines—SUT-MG12 and SUT-MG14, WHO grade I—and demonstrated the glycan an...
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PeerJ Inc.
2024-01-01
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| author | Chutima Talabnin Thanawat Trasaktaweesakul Pitchanun Jaturutthaweechot Pundit Asavaritikrai Dusit Kongnawakun Atit Silsirivanit Norie Araki Krajang Talabnin |
| author_facet | Chutima Talabnin Thanawat Trasaktaweesakul Pitchanun Jaturutthaweechot Pundit Asavaritikrai Dusit Kongnawakun Atit Silsirivanit Norie Araki Krajang Talabnin |
| author_sort | Chutima Talabnin |
| collection | DOAJ |
| description | Background Changes in protein glycosylation have been reported in various diseases, including cancer; however, the consequences of altered glycosylation in meningiomas remains undefined. We established two benign meningioma cell lines—SUT-MG12 and SUT-MG14, WHO grade I—and demonstrated the glycan and glycosyltransferase profiles of the mucin-type O-linked glycosylation in the primary benign meningioma cells compared with two malignant meningioma cell lines—HKBMM and IOMM-Lee, WHO grade III. Changes in O-linked glycosylation profiles in malignant meningiomas were proposed. Methods Primary culture technique, morphological analysis, and immunocytochemistry were used to establish and characterize two benign meningioma cell lines. The glycan profiles of the primary benign and malignant meningiomas cell lines were then analyzed using lectin cytochemistry. The gene expression of O-linked glycosyltransferases, mucins, sialyltransferases, and fucosyltransferases were analyzed in benign and malignant meningioma using the GEO database (GEO series GSE16581) and quantitative-PCR (qPCR). Results Lectin cytochemistry revealed that the terminal galactose (Gal) and N-acetyl galactosamine (GalNAc) were highly expressed in primary benign meningioma cells (WHO grade I) compared to malignant meningioma cell lines (WHO grade III). The expression profile of mucin types O-glycosyltransferases in meningiomas were observed through the GEO database and gene expression experiment in meningioma cell lines. In the GEO database, C1GALT1-specific chaperone (COSMC) and mucin 1 (MUC1) were significantly increased in malignant meningiomas (Grade II and III) compared with benign meningiomas (Grade I). Meanwhile, in the cell lines, Core 2 β1,6-N-acetylglucosaminyltransferase-2 (C2GNT2) was highly expressed in malignant meningiomas. We then investigated the complex mucin-type O-glycans structures by determination of sialyltransferases and fucosyltransferases. We found ST3 β-galactoside α-2,3-sialyltransferase 4 (ST3GAL4) was significantly decreased in the GEO database, while ST3GAL1, ST3GAL3, α1,3 fucosyltransferases 1 and 8 (FUT1 and FUT8) were highly expressed in malignant meningioma cell lines—(HKBMM)—compared to primary benign meningioma cells—(SUT-MG12 and SUT-MG14). Conclusion Our findings are the first to demonstrate the potential glycosylation changes in the O-linked glycans of malignant meningiomas compared with benign meningiomas, which may play an essential role in the progression, tumorigenesis, and malignancy of meningiomas. |
| first_indexed | 2024-03-08T11:48:02Z |
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| spelling | doaj.art-04c3782afa0e479da4bd90f7264dc89e2024-01-24T15:05:32ZengPeerJ Inc.PeerJ2167-83592024-01-0112e1678510.7717/peerj.16785Altered O-linked glycosylation in benign and malignant meningiomasChutima Talabnin0Thanawat Trasaktaweesakul1Pitchanun Jaturutthaweechot2Pundit Asavaritikrai3Dusit Kongnawakun4Atit Silsirivanit5Norie Araki6Krajang Talabnin7School of Chemistry, Institute of Science, Suranaree University of Technology, Nakhon Ratchasima, ThailandSchool of Translational Medicine, Institute of Medicine, Suranaree University of Technology, Nakhon Ratchasima, ThailandSchool of Chemistry, Institute of Science, Suranaree University of Technology, Nakhon Ratchasima, ThailandSchool of Surgery, Institute of Medicine, Suranaree University of Technology, Nakhon Ratchasima, ThailandSchool of Pathology, Institute of Medicine, Suranaree University of Technology, Nakhon Ratchasima, ThailandDepartment of Biochemistry, Faculty of Medicine, Khon Kaen University, Khon Kaen, ThailandDepartment of Tumor Genetics and Biology, Graduate School of Medical Sciences, Faculty of Life Sciences, Kumamoto University, Kumamoto, JapanSchool of Pathology, Institute of Medicine, Suranaree University of Technology, Nakhon Ratchasima, ThailandBackground Changes in protein glycosylation have been reported in various diseases, including cancer; however, the consequences of altered glycosylation in meningiomas remains undefined. We established two benign meningioma cell lines—SUT-MG12 and SUT-MG14, WHO grade I—and demonstrated the glycan and glycosyltransferase profiles of the mucin-type O-linked glycosylation in the primary benign meningioma cells compared with two malignant meningioma cell lines—HKBMM and IOMM-Lee, WHO grade III. Changes in O-linked glycosylation profiles in malignant meningiomas were proposed. Methods Primary culture technique, morphological analysis, and immunocytochemistry were used to establish and characterize two benign meningioma cell lines. The glycan profiles of the primary benign and malignant meningiomas cell lines were then analyzed using lectin cytochemistry. The gene expression of O-linked glycosyltransferases, mucins, sialyltransferases, and fucosyltransferases were analyzed in benign and malignant meningioma using the GEO database (GEO series GSE16581) and quantitative-PCR (qPCR). Results Lectin cytochemistry revealed that the terminal galactose (Gal) and N-acetyl galactosamine (GalNAc) were highly expressed in primary benign meningioma cells (WHO grade I) compared to malignant meningioma cell lines (WHO grade III). The expression profile of mucin types O-glycosyltransferases in meningiomas were observed through the GEO database and gene expression experiment in meningioma cell lines. In the GEO database, C1GALT1-specific chaperone (COSMC) and mucin 1 (MUC1) were significantly increased in malignant meningiomas (Grade II and III) compared with benign meningiomas (Grade I). Meanwhile, in the cell lines, Core 2 β1,6-N-acetylglucosaminyltransferase-2 (C2GNT2) was highly expressed in malignant meningiomas. We then investigated the complex mucin-type O-glycans structures by determination of sialyltransferases and fucosyltransferases. We found ST3 β-galactoside α-2,3-sialyltransferase 4 (ST3GAL4) was significantly decreased in the GEO database, while ST3GAL1, ST3GAL3, α1,3 fucosyltransferases 1 and 8 (FUT1 and FUT8) were highly expressed in malignant meningioma cell lines—(HKBMM)—compared to primary benign meningioma cells—(SUT-MG12 and SUT-MG14). Conclusion Our findings are the first to demonstrate the potential glycosylation changes in the O-linked glycans of malignant meningiomas compared with benign meningiomas, which may play an essential role in the progression, tumorigenesis, and malignancy of meningiomas.https://peerj.com/articles/16785.pdfMeningiomasO-linked glycosylationSialyltransferasesFucosyltransferasesGlycosyltransferasesMucin |
| spellingShingle | Chutima Talabnin Thanawat Trasaktaweesakul Pitchanun Jaturutthaweechot Pundit Asavaritikrai Dusit Kongnawakun Atit Silsirivanit Norie Araki Krajang Talabnin Altered O-linked glycosylation in benign and malignant meningiomas PeerJ Meningiomas O-linked glycosylation Sialyltransferases Fucosyltransferases Glycosyltransferases Mucin |
| title | Altered O-linked glycosylation in benign and malignant meningiomas |
| title_full | Altered O-linked glycosylation in benign and malignant meningiomas |
| title_fullStr | Altered O-linked glycosylation in benign and malignant meningiomas |
| title_full_unstemmed | Altered O-linked glycosylation in benign and malignant meningiomas |
| title_short | Altered O-linked glycosylation in benign and malignant meningiomas |
| title_sort | altered o linked glycosylation in benign and malignant meningiomas |
| topic | Meningiomas O-linked glycosylation Sialyltransferases Fucosyltransferases Glycosyltransferases Mucin |
| url | https://peerj.com/articles/16785.pdf |
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