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FUT8-mediated aberrant N-glycosylation of SEMA7A promotes head and neck squamous cell carcinoma progression
- Zhonglong Liu1, Xiaoyan Meng1, Yuxin Zhang2, Jingjing Sun3, Xiao Tang1, Zhiyuan Zhang1, Liu Liu1, Yue He1
Author information
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1. Department of Oral Maxillofacial & Head and Neck Oncology, Shanghai Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, National Clinical Research Center for Oral Disease, Shanghai, China;
2. Department of Oral Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases, Shanghai, China;
3. Department of Oral Pathology, Shanghai Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, National Clinical Research Center for Oral Disease Shanghai, Shanghai, China
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History
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Received |
Revised |
Published |
31 Oct 2023 |
23 Feb 2024 |
01 Jan 2024 |
Issue Date |
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10 Jul 2024 |
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References
1. Siegel R. L., Miller K. D., Fuchs H. E.& Jemal, A. Cancer statistics, 2022.CA Cancer J. Clin. 72, 7-33 (2022).
2. Magalhaes, A., Duarte, H. O.& Reis, C. A. Aberrant glycosylation in cancer: a novel molecular mechanism controlling metastasis.Cancer Cell 31, 733-735 (2017).
3. RodrÍguez, E., Schetters, S. T.T. & van Kooyk, Y. The tumour glyco-code as a novel immune checkpoint for immunotherapy.Nat. Rev. Immunol. 18, 204-211 (2018).
4. Oliveira-Ferrer, L., Legler, K. & Milde-Langosch, K. Role of protein glycosylation in cancer metastasis.Semin. Cancer Biol. 44, 141-152 (2017).
5. Marsico G., Russo L., Quondamatteo F.& Pandit, A. Glycosylation and integrin regulation in cancer.Trends Cancer 4, 537-552 (2018).
6. Chakraborty A.& Dimitroff, C. J. Cancer immunotherapy needs to learn how to stick to its guns.J. Clin. Invest. 129, 5089-5091 (2019).
7. Gomes J., Stefan M., Ana M.& Celso, A. R. Early GalNAc O-glycosylation: pushing the tumor boundaries.Cancer Cell 32, 544-545 (2017).
8. Li, C. W.et al.Glycosylation and stabilization of programmed death ligand-1 suppresses T-cell activity.Nat. Commun. 7, 12632(2016).
9. Sasawatari S., Okamoto Y., Kumanogoh A.& Toyofuku, T. Blockade of N-glycosylation promotes antitumor immune response of T cells.J. Immunol. 204, 1373-1385 (2020).
10. Shao, B.et al.Deglycosylation of PD-L1 by 2-deoxyglucose reverses PARP inhibitor-induced immunosuppression in triple-negative breast cancer.Am. J. Cancer. Res. 8, 1837-1846 (2018).
11. Li, C. W.et al. Eradication of triple-negative breast cancer cells by targeting glycosylated PD-L1. Cancer Cell 33, 187-201.e10 (2018).
12. Lee, H. H.et al. Removal of N-linked glycosylation enhances PD-L1 detection and predicts Anti-PD-1/PD-L1 therapeutic efficacy. Cancer Cell 36, 168-178.e4 (2019).
13. Sun, L.et al.Targeting Glycosylated PD-1 induces potent antitumor immunity.Cancer Res. 80, 2298-2310 (2020).
14. Chen, J. T.et al.Glycoprotein B7-H3 overexpression and aberrant glycosylation in oral cancer and immune response.Proc. Natl Acad. Sci. USA 112, 13057-13062 (2015).
15. Huang, Y.et al.FUT8-mediated aberrant N-glycosylation of B7H3 suppresses the immune response in triple-negative breast cancer.Nat. Commun. 12, 2672(2021).
16. Xu, Y.et al.PD-L2 glycosylation promotes immune evasion and predicts anti-EGFR efficacy.J. Immunother. Cancer 9, e002699(2021).
17. Lin M. C., Huang M. J., Liu C. H., Yang T. L.& Huang, M. C. GALNT2 enhances migration and invasion of oral squamous cell carcinoma by regulating EGFR glycosylation and activity.Oral Oncol. 50, 478-484 (2014).
18. Song, X.et al.Pharmacologic suppression of B7-H4 glycosylation restores antitumor immunity in immune-cold breast cancers.Cancer Discov. 10, 1872-1893 (2020).
19. Jongbloets, B. C.et al.Stage-specific functions of Semaphorin7A during adult hippocampal neurogenesis rely on distinct receptors.Nat. Commun. 8, 14666(2017).
20. van Rijn, A.et al. Semaphorin 7A promotes chemokine-driven dendritic cell migration.J. Immunol. 196, 459-468 (2016).
21. Yamada, A.et al.Molecular cloning of a glycosylphosphatidylinositol-anchored molecule CD108w.J. Immunol. 162, 4094-4100 (1999).
22. Liu, H.et al.Structural basis of semaphorin-plexin recognition and viral mimicry from SEMA7A and A39R complexes with PlexinC1.Cell 142, 749-761 (2010).
23. Suzuki, K.et al.Semaphorin 7A initiates T-cell-mediated inflammatory responses through alpha1beta1 integrin.Nature 446, 680-684 (2007).
24. Suzuki, K., Kumanogoh, A.& Kikutani, H. Semaphorins and their receptors in immune cell interactions.Nat. Immunol. 9, 17-23 (2008).
25. Elder, A. M.et al.Semaphorin 7A promotes macrophage-mediated lymphatic remodeling during postpartum mammary gland involution and in breast cancer.Cancer Res. 78, 6473-6485 (2018).
26. Garcia-Areas, R. et al. Suppression of tumor-derived Semaphorin 7A and genetic ablation of host-derived Semaphorin 7A impairs tumor progression in a murine model of advanced breast carcinoma.Int. J. Oncol. 51, 1395-1404 (2017).
27. Garcia-Areas, R. et al. Semaphorin7A promotes tumor growth and exerts a pro-angiogenic effect in macrophages of mammary tumor-bearing mice.Front. Physiol. 5, 17(2014).
28. Tarullo, S. E.et al.Postpartum breast cancer progression is driven by semaphorin 7a-mediated invasion and survival.Oncogene 39, 2772-2785 (2020).
29. Kinehara, Y.et al.Semaphorin 7A promotes EGFR-TKI resistance in EGFR mutant lung adenocarcinoma cells.JCI Insight 3, e123093(2018).
30. Inoue N., Nishizumi H., Naritsuka H., Kiyonari H.& Sakano, H. SEMA7A/PlxnCl signaling triggers activity-dependent olfactory synapse formation.Nat. Commun. 9, 1842(2018).
31. Janssen, B. J.et al.Structural basis of semaphorin-plexin signalling.Nature 467, 1118-1122 (2010).
32. Grigaravicius P., von Deimling, A. & Frappart, P. O. RINT1 functions as a multitasking protein at the crossroads between genomic stability, ER homeostasis, and autophagy.Autophagy 12, 1413-1415 (2016).
33. Ng, B. G.et al.Expanding the molecular and clinical phenotypes of FUT8-CDG.J. Inherit. Metab. Dis. 43, 871-879 (2020).
34. Järvå, M. A.et al.Structural basis of substrate recognition and catalysis by fucosyltransferase 8.J. Biol. Chem. 295, 6677-6688 (2020).
35. Lin J. C.& Tarn, W. Y. RBM4 down-regulates PTB and antagonizes its activity in muscle cell-specific alternative splicing.J. Cell Biol. 193, 509-520 (2011).
36. D, D., Hung, K. Y. & Tarn, W. Y. RBM4 modulates radial migration via alternative splicing of Dab1 during cortex development.Mol. Cell Biol. 38, e00007-e00018 (2018).
37. Markus, M. A., Yang, Y. H.& Morris, B. J. Transcriptome-wide targets of alternative splicing by RBM4 and possible role in cancer.Genomics 107, 138-144 (2016).
38. Mahoney, K. M.et al.A secreted PD-L1 splice variant that covalently dimerizes and mediates immunosuppression.Cancer Immunol. Immunother. 68, 421-432 (2019).
39. Hassounah, N. B.et al.Identification and characterization of an alternative cancer-derived PD-L1 splice variant.Cancer Immunol. Immunother. 68, 407-420 (2019).
40. Wang, C.et al.Distinct roles of programmed death ligand 1 alternative splicing isoforms in colorectal cancer.Cancer Sci. 112, 178-193 (2021).
41. Cagnoni A. J.,Pérez Sáez, J. M., Rabinovich, G. A. & Mariño, K. V. Turning-off signaling by siglecs, selectins, and galectins: chemical inhibition of glycan-dependent interactions in cancer.Front Oncol 6, 109(2016).
42. Chen, C. Y.et al.Fucosyltransferase 8 as a functional regulator of nonsmall cell lung cancer.Proc. Natl Acad. Sci. USA 110, 630-635 (2013).
43. Agrawal, P.et al. A systems biology approach identifies FUT8 as a driver of melanoma metastasis. Cancer Cell 31, 804-819.e7 (2017).
44. Chiang, W. F.et al.Carcinoembryonic antigen-related cell adhesion molecule 6 (CEACAM6) promotes EGF receptor signaling of oral squamous cell carcinoma metastasis via the complex N-glycosylation.Oncogene 37, 116-127 (2018).