Acknowledgement
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (No. 2021R1C1C1012076 to J.Y.) and by the ChungAng University Research Grants in 2020 (to Y.L.).
References
- Aebi, M. (2013). N-linked protein glycosylation in the ER. Biochim. Biophys. Acta 1833, 2430-2437. https://doi.org/10.1016/j.bbamcr.2013.04.001
- Al-Dabbagh, B., Henry, X., El Ghachi, M., Auger, G., Blanot, D., Parquet, C., Mengin-Lecreulx, D., and Bouhss, A. (2008). Active site mapping of MraY, a member of the polyprenyl-phosphate N-acetylhexosamine 1-phosphate transferase superfamily, catalyzing the first membrane step of peptidoglycan biosynthesis. Biochemistry 47, 8919-8928. https://doi.org/10.1021/bi8006274
- Belaya, K., Finlayson, S., Slater, C.R., Cossins, J., Liu, W.W., Maxwell, S., McGowan, S.J., Maslau, S., Twigg, S.R., Walls, T.J., et al. (2012). Mutations in DPAGT1 cause a limb-girdle congenital myasthenic syndrome with tubular aggregates. Am. J. Hum. Genet. 91, 193-201. https://doi.org/10.1016/j.ajhg.2012.05.022
- Blom, N., Sicheritz-Ponten, T., Gupta, R., Gammeltoft, S., and Brunak, S. (2004). Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4, 1633-1649. https://doi.org/10.1002/pmic.200300771
- Bouhss, A., Trunkfield, A.E., Bugg, T.D., and Mengin-Lecreulx, D. (2008). The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol. Rev. 32, 208-233. https://doi.org/10.1111/j.1574-6976.2007.00089.x
- Chung, B.C., Mashalidis, E.H., Tanino, T., Kim, M., Matsuda, A., Hong, J., Ichikawa, S., and Lee, S.Y. (2016). Structural insights into inhibition of lipid I production in bacterial cell wall synthesis. Nature 533, 557-560. https://doi.org/10.1038/nature17636
- Chung, B.C., Zhao, J., Gillespie, R.A., Kwon, D.Y., Guan, Z., Hong, J., Zhou, P., and Lee, S.Y. (2013). Crystal structure of MraY, an essential membrane enzyme for bacterial cell wall synthesis. Science 341, 1012-1016. https://doi.org/10.1126/science.1236501
- Dan, N. and Lehrman, M.A. (1997). Oligomerization of hamster UDP-GlcNAc:dolichol-P GlcNAc-1-P transferase, an enzyme with multiple transmembrane spans. J. Biol. Chem. 272, 14214-14219. https://doi.org/10.1074/jbc.272.22.14214
- Dong, Y.Y., Wang, H., Pike, A.C.W., Cochrane, S.A., Hamedzadeh, S., Wyszynski, F.J., Bushell, S.R., Royer, S.F., Widdick, D.A., Sajid, A., et al. (2018). Structures of DPAGT1 explain glycosylation disease mechanisms and advance TB antibiotic design. Cell 175, 1045-1058.e16. https://doi.org/10.1016/j.cell.2018.10.037
- Goulabchand, R., Vincent, T., Batteux, F., Eliaou, J.F., and Guilpain, P. (2014). Impact of autoantibody glycosylation in autoimmune diseases. Autoimmun. Rev. 13, 742-750. https://doi.org/10.1016/j.autrev.2014.02.005
- Hakulinen, J.K., Hering, J., Branden, G., Chen, H., Snijder, A., Ek, M., and Johansson, P. (2017). MraY-antibiotic complex reveals details of tunicamycin mode of action. Nat. Chem. Biol. 13, 265-267. https://doi.org/10.1038/nchembio.2270
- Haltiwanger, R.S. and Lowe, J.B. (2004). Role of glycosylation in development. Annu. Rev. Biochem. 73, 491-537. https://doi.org/10.1146/annurev.biochem.73.011303.074043
- Huang, K.Y., Lee, T.Y., Kao, H.J., Ma, C.T., Lee, C.C., Lin, T.H., Chang, W.C., and Huang, H.D. (2019). dbPTM in 2019: exploring disease association and cross-talk of post-translational modifications. Nucleic Acids Res. 47(D1), D298-D308. https://doi.org/10.1093/nar/gky1074
- Izumi, M., Yuasa, H., and Hashimoto, H. (2009). Bisubstrate analogues as glycosyltransferase inhibitors. Curr. Top. Med. Chem. 9, 87-105. https://doi.org/10.2174/156802609787354351
- Karve, T.M. and Cheema, A.K. (2011). Small changes huge impact: the role of protein posttranslational modifications in cellular homeostasis and disease. J. Amino Acids 2011, 207691.
- Kaushal, G.P. and Elbein, A.D. (1985). Purification and properties of UDP-GlcNAc:dolichyl-phosphate GlcNAc-1-phosphate transferase. Activation and inhibition of the enzyme. J. Biol. Chem. 260, 16303-16309. https://doi.org/10.1016/S0021-9258(17)36236-1
- Keller, R.K., Boon, D.Y., and Crum, F.C. (1979). N-Acetylglucosamine- 1-phosphate transferase from hen oviduct: solubilization, characterization, and inhibition by tunicamycin. Biochemistry 18, 3946-3952. https://doi.org/10.1021/bi00585a016
- Lauc, G., Huffman, J.E., Pucic, M., Zgaga, L., Adamczyk, B., Muzinic, A., Novokmet, M., Polasek, O., Gornik, O., Kristic, J., et al. (2013). Loci associated with N-glycosylation of human immunoglobulin G show pleiotropy with autoimmune diseases and haematological cancers. PLoS Genet. 9, e1003225.
- Lehle, L. and Tanner, W. (1976). The specific site of tunicamycin inhibition in the formation of dolichol-bound N-acetylglucosamine derivatives. FEBS Lett. 72, 167-170. https://doi.org/10.1016/0014-5793(76)80922-2
- Lehrman, M.A. (1991). Biosynthesis of N-acetylglucosamine-P-P-dolichol, the committed step of asparagine-linked oligosaccharide assembly. Glycobiology 1, 553-562. https://doi.org/10.1093/glycob/1.6.553
- Mashalidis, E.H., Kaeser, B., Terasawa, Y., Katsuyama, A., Kwon, D.Y., Lee, K., Hong, J., Ichikawa, S., and Lee, S.Y. (2019). Chemical logic of MraY inhibition by antibacterial nucleoside natural products. Nat. Commun. 10, 2917.
- Mashalidis, E.H. and Lee, S.Y. (2020). Structures of bacterial MraY and human GPT provide insights into rational antibiotic design. J. Mol. Biol. 432, 4946-4963. https://doi.org/10.1016/j.jmb.2020.03.017
- Nakaya, T., Yabe, M., Mashalidis, E.H., Sato, T., Yamamoto, K., Hikiji, Y., Katsuyama, A., Shinohara, M., Minato, Y., Takahashi, S., et al. (2022). Synthesis of macrocyclic nucleoside antibacterials and their interactions with MraY. Nat. Commun. 13, 7575.
- Ohtsubo, K. and Marth, J.D. (2006). Glycosylation in cellular mechanisms of health and disease. Cell 126, 855-867. https://doi.org/10.1016/j.cell.2006.08.019
- Plouhar, P.L. and Bretthauer, R.K. (1982). A phospholipid requirement for dolichol pyrophosphate N-acetylglucosamine synthesis in phospholipase A2-treated rat lung microsomes. J. Biol. Chem. 257, 8907-8911. https://doi.org/10.1016/S0021-9258(18)34218-2
- Plouhar, P.L. and Bretthauer, R.K. (1983). Restoration by phospholipids of dolichol pyrophosphate N-acetylglucosamine synthesis in delipidated rat lung microsomes. J. Biol. Chem. 258, 12988-12993. https://doi.org/10.1016/S0021-9258(17)44069-5
- Price, N.P. and Momany, F.A. (2005). Modeling bacterial UDP-HexNAc: polyprenol-P HexNAc-1-P transferases. Glycobiology 15, 29R-42R. https://doi.org/10.1093/glycob/cwi065
- Ramazi, S., Allahverdi, A., and Zahiri, J. (2020). Evaluation of post-translational modifications in histone proteins: a review on histone modification defects in developmental and neurological disorders. J. Biosci. 45, 135.
- Takatsuki, A., Arima, K., and Tamura, G. (1971). Tunicamycin, a new antibiotic. I. Isolation and characterization of tunicamycin. J. Antibiot. (Tokyo) 24, 215-223. https://doi.org/10.7164/antibiotics.24.215
- Tkacz, J.S. and Lampen, O. (1975). Tunicamycin inhibition of polyisoprenyl N-acetylglucosaminyl pyrophosphate formation in calf-liver microsomes. Biochem. Biophys. Res. Commun. 65, 248-257. https://doi.org/10.1016/S0006-291X(75)80086-6
- Wang, R., Steensma, D.H., Takaoka, Y., Yun, J.W., Kajimoto, T., and Wong, C.H. (1997). A search for pyrophosphate mimics for the development of substrates and inhibitors of glycosyltransferases. Bioorg. Med. Chem. 5, 661-672. https://doi.org/10.1016/S0968-0896(97)00005-9
- Wang, Y., Zhang, L., He, Z., Deng, J., Zhang, Z., Liu, L., Ye, W., and Liu, S. (2020). Tunicamycin induces ER stress and inhibits tumorigenesis of head and neck cancer cells by inhibiting N-glycosylation. Am. J. Transl. Res. 12, 541-550.
- Wu, J., Chen, S., Liu, H., Zhang, Z., Ni, Z., Chen, J., Yang, Z., Nie, Y., and Fan, D. (2018). Tunicamycin specifically aggravates ER stress and overcomes chemoresistance in multidrug-resistant gastric cancer cells by inhibiting N-glycosylation. J. Exp. Clin. Cancer Res. 37, 272.
- Wu, X., Rush, J.S., Karaoglu, D., Krasnewich, D., Lubinsky, M.S., Waechter, C.J., Gilmore, R., and Freeze, H.H. (2003). Deficiency of UDP-GlcNAc:Dolichol Phosphate N-Acetylglucosamine-1 Phosphate Transferase (DPAGT1) causes a novel congenital disorder of Glycosylation Type Ij. Hum. Mutat. 22, 144-150. https://doi.org/10.1002/humu.10239
- Wurde, A.E., Reunert, J., Rust, S., Hertzberg, C., Haverkamper, S., Nurnberg, G., Nurnberg, P., Lehle, L., Rossi, R., and Marquardt, T. (2012). Congenital disorder of glycosylation type Ij (CDG-Ij, DPAGT1-CDG): extending the clinical and molecular spectrum of a rare disease. Mol. Genet. Metab. 105, 634-641. https://doi.org/10.1016/j.ymgme.2012.01.001
- Xu, L., Appell, M., Kennedy, S., Momany, F.A., and Price, N.P. (2004). Conformational analysis of chirally deuterated tunicamycin as an active site probe of UDP-N-acetylhexosamine:polyprenol-P N-acetylhexosamine-1-P translocases. Biochemistry 43, 13248-13255. https://doi.org/10.1021/bi048327q
- Yoo, J., Mashalidis, E.H., Kuk, A.C.Y., Yamamoto, K., Kaeser, B., Ichikawa, S., and Lee, S.Y. (2018). GlcNAc-1-P-transferase-tunicamycin complex structure reveals basis for inhibition of N-glycosylation. Nat. Struct. Mol. Biol. 25, 217-224. https://doi.org/10.1038/s41594-018-0031-y
- Zhao, G., Kang, J., Xu, G., Wei, J., Wang, X., Jing, X., Zhang, L., Yang, A., Wang, K., Wang, J., et al. (2020). Tunicamycin promotes metastasis through upregulating endoplasmic reticulum stress induced GRP78 expression in thyroid carcinoma. Cell Biosci. 10, 115.