The sphingomyelin synthase family: proteins, diseases, and inhibitors

References

Bickert, A., Ginkel, C., Kol, M., vom Dorp, K., Jastrow, H., Degen, J., Jacobs, R.L., Vance, D.E., Winterhager, E., Jiang, X.C., et al. (2015). Functional characterization of enzymes catalyzing ceramide phosphoethanolamine biosynthesis in mice. J. Lipid. Res. 56, 821–835.10.1194/jlr.M055269Search in Google Scholar PubMed PubMed Central

Cabukusta, B., Kol, M., Kneller, L., Hilderink, A., Bickert, A., Mina, J.G., Korneev, S., and Holthuis, J.C. (2017). ER residency of the ceramide phosphoethanolamine synthase SMSr relies on homotypic oligomerization mediated by its SAM domain. Sci. Rep. 7, 41290.10.1038/srep41290Search in Google Scholar PubMed PubMed Central

Deng, X., Lin, F., Zhang, Y., Li, Y., Zhou, L., Lou, B., Li, Y., Dong, J., Ding, T., Jiang, X., et al. (2014). Identification of small molecule sphingomyelin synthase inhibitors. Eur. J. Med. Chem. 73, 1–7.10.1016/j.ejmech.2013.12.002Search in Google Scholar PubMed

Ding, T., Kabir, I., Li, Y., Lou, C., Yazdanyar, A., Xu, J., Dong, J., Zhou, H., Park, T., Boutjdir, M., et al. (2015). All members in the sphingomyelin synthase gene family have ceramide phosphoethanolamine synthase activity. J. Lipid. Res. 56, 537–545.10.1194/jlr.M054627Search in Google Scholar PubMed PubMed Central

Hayashi, Y., Nemoto-Sasaki, Y., Tanikawa, T., Oka, S., Tsuchiya, K., Zama, K., Mitsutake, S., Sugiura, T., and Yamashita, A. (2014). Sphingomyelin synthase 2, but not sphingomyelin synthase 1, is involved in HIV-1 envelope-mediated membrane fusion. J. Biol. Chem. 289, 30842–30856.10.1074/jbc.M114.574285Search in Google Scholar PubMed PubMed Central

Hla, T. and Dannenberg, A.J. (2012). Sphingolipid signaling in metabolic disorders. Cell Metab. 16, 420–434.10.1016/j.cmet.2012.06.017Search in Google Scholar PubMed PubMed Central

Huitema, K., van den Dikkenberg, J., Brouwers, J.F., and Holthuis, J.C. (2004). Identification of a family of animal sphingomyelin synthases. EMBO J. 23, 33–44.10.1038/sj.emboj.7600034Search in Google Scholar PubMed PubMed Central

Kiss, Z. and Tomono, M. (1995). Compound D609 inhibits phorbol ester-stimulated phospholipase D activity and phospholipase C-mediated phosphatidylethanolamine hydrolysis. Biochim. Biophys. Acta. 1259, 105–108.10.1016/0005-2760(95)00148-6Search in Google Scholar PubMed

Kol, M., Panatala, R., Nordmann, M., Swart, L., van Suijlekom, L., Cabukusta, B., Hilderink, A., Grabietz, T., Mina, J.G., Somerharju, P., et al. (2016). Switching head group selectivity in mammalian sphingolipid biosynthesis by active-site engineering of sphingomyelin synthases. J. Lipid. Res. 57, 1273–1285.10.1194/jlr.M068692Search in Google Scholar PubMed PubMed Central

Li, Z., Fan, Y., Liu, J., Li, Y., Huan, C., Bui, H.H., Kuo, M.S., Park, T.S., Cao, G., and Jiang, X.C. (2012). Impact of sphingomyelin synthase 1 deficiency on sphingolipid metabolism and atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 32, 1577–1584.10.1161/ATVBAHA.112.251538Search in Google Scholar PubMed PubMed Central

Li, Y., Dong, J.B., Ding, T.B., Kuo, M.S., Cao, G.Q., Jiang, X.C., and Li, Z.Q. (2013). Sphingomyelin synthase 2 activity and liver steatosis: an effect of ceramide-mediated peroxisome proliferator-activated receptor γ 2 suppression. Arterioscler. Thromb. Vasc. Biol. 33, 1513–1520.10.1161/ATVBAHA.113.301498Search in Google Scholar PubMed PubMed Central

Li, Y.L., Qi, X.Y., Jiang, H., Deng, X.D., Dong, Y.P., Ding, T.B., Zhou, L., Men, P., Chu, Y., Wang, R.X., et al. (2015). Discovery, synthesis and biological evaluation of 2-(4-(N-phenethylsulfamoyl)phenoxy)acetamides (SAPAs) as novel sphingomyelin synthase 1 inhibitors. Bioorg. Med. Chem. 23, 6173–6184.10.1016/j.bmc.2015.07.060Search in Google Scholar PubMed

Liu, J., Huan, C., Chakraborty, M., Zhang, H., Lu, D., Kuo, M.S., Cao, G., and Jiang, X.C. (2009). Macrophage sphingomyelin synthase 2 deficiency decreases atherosclerosis in mice. Circ. Res. 105, 295–303.10.1161/CIRCRESAHA.109.194613Search in Google Scholar PubMed PubMed Central

Lou, B., Dong, J., Li, Y., Ding, T., Bi, T., Li, Y., Deng, X., Ye, D., and Jiang, X.C. (2014). Pharmacologic inhibition of sphingomyelin synthase (SMS) activity reduces apolipoprotein-B secretion from hepatocytes and attenuates endotoxin-mediated macrophage inflammation. PLoS One 9, e102641.10.1371/journal.pone.0102641Search in Google Scholar PubMed PubMed Central

Luberto, C. and Hannun, Y.A. (1998). Sphingomyelin synthase, a potential regulator of intracellular levels of ceramide and diacylglycerol during SV40 transformation. Does sphingomyelin synthase account for the putative phosphatidylcholine-specific phospholipase C? J. Biol. Chem. 273, 14550–14559.10.1074/jbc.273.23.14550Search in Google Scholar PubMed

Mitsutake, S., Zama, K., Yokota, H., Yoshida, T., Tanaka, M., Mitsui, M., Ikawa, M., Okabe, M., Tanaka, Y., Yamashita, T., et al. (2011). Dynamic modification of sphingomyelin in lipid microdomains controls development of obesity, fatty liver, and type 2 diabetes. J. Biol. Chem. 286, 28544–28555.10.1074/jbc.M111.255646Search in Google Scholar PubMed PubMed Central

Moore, K.J. and Tabas, I. (2011). Macrophages in the pathogenesis of atherosclerosis. Cell 145, 341–355.10.1016/j.cell.2011.04.005Search in Google Scholar PubMed PubMed Central

Qiao, F. and Bowie, J.U. (2005). The many faces of SAM. Sci. STKE. 2005, re7.10.1126/stke.2862005re7Search in Google Scholar PubMed

Sakamoto, H., Yoshida, T., Sanaki, T., Shigaki, S., Morita, H., Oyama, M., Mitsui, M., Tanaka, Y., Nakano, T., Mitsutake, S., et al. (2017). Possible roles of long-chain sphingomyelines and sphingomyelin synthase 2 in mouse macrophage inflammatory response. Biochem. Biophys. Res. Commun. 482, 202–207.10.1016/j.bbrc.2016.11.041Search in Google Scholar PubMed

Tafesse, F.G., Vacaru, A.M., Bosma, E.F., Hermansson, M., Jain, A., Hilderink, A., Somerharju, P., and Holthuis, J.C. (2014). Sphingomyelin synthase-related protein SMSr is a suppressor of ceramide-induced mitochondrial apoptosis. J. Cell Sci. 127, 445–454.10.1242/jcs.138933Search in Google Scholar PubMed

Tani, M. and Kuge, O. (2009). Sphingomyelin synthase 2 is palmitoylated at the COOH-terminal tail, which is involved in its localization in plasma membranes. Biochem. Biophys. Res. Commun. 381, 328–332.10.1016/j.bbrc.2009.02.063Search in Google Scholar PubMed

Taniguchi, M. and Okazaki, T. (2014). The role of sphingomyelin and sphingomyelin synthases in cell death, proliferation and migration-from cell and animal models to human disorders. Biochim. Biophys. Acta. 1841, 692–703.10.1016/j.bbalip.2013.12.003Search in Google Scholar PubMed

Taniguchi, M., Tasaki, T., Ninomiya, H., Ueda, Y., Kuremoto, K.I., Mitsutake, S., Igarashi, Y., Okazaki, T., and Takegami, T. (2016). Sphingomyelin generated by sphingomyelin synthase 1 is involved in attachment and infection with Japanese encephalitis virus. Sci. Rep. 6, 37829.10.1038/srep37829Search in Google Scholar PubMed PubMed Central

Ternes, P., Brouwers, J.F., van den Dikkenberg, J., and Holthuis, J.C. (2009). Sphingomyelin synthase SMS2 displays dual activity as ceramide phosphoethanolamine synthase. J. Lipid. Res. 50, 2270–2277.10.1194/jlr.M900230-JLR200Search in Google Scholar PubMed PubMed Central

Ullman, M.D. and Radin, N.S. (1974). Enzymatic formation of sphingomyelin from ceramide and lecithin in mouse liver. J. Biol. Chem. 249, 1506–1512.10.1016/S0021-9258(19)42911-6Search in Google Scholar

Vacaru, A.M., Tafesse, F.G., Ternes, P., Kondylis, V., Hermansson, M., Brouwers, J.F., Somerharju, P., Rabouille, C., and Holthuis, J.C. (2009). Sphingomyelin synthase-related protein SMSr controls ceramide homeostasis in the ER. J. Cell Biol. 185, 1013–1027.10.1083/jcb.200903152Search in Google Scholar PubMed PubMed Central

Virreira Winter, S., Zychlinsky, A., and Bardoel, B.W. (2016). Genome-wide CRISPR screen reveals novel host factors required for Staphylococcus aureus α-hemolysin-mediated toxicity. Sci. Rep. 6, 24242.10.1038/srep24242Search in Google Scholar PubMed PubMed Central

Yano, M., Watanabe, K., Yamamoto, T., Ikeda, K., Senokuchi, T., Lu, M., Kadomatsu, T., Tsukano, H., Ikawa, M., Okabe, M., et al. (2011). Mitochondrial dysfunction and increased reactive oxygen species impair insulin secretion in sphingomyelin synthase 1-null mice. J. Biol. Chem. 286, 3992–4002.10.1074/jbc.M110.179176Search in Google Scholar PubMed PubMed Central

Yano, M., Yamamoto, T., Nishimura, N., Gotoh, T., Watanabe, K., Ikeda, K., Garan, Y., Taguchi, R., Node, K., Okazaki, T., et al. (2013). Increased oxidative stress impairs adipose tissue function in sphingomyelin synthase 1 null mice. PLoS One 8, e61380.10.1371/journal.pone.0061380Search in Google Scholar PubMed PubMed Central

Yeang, C., Varshney, S., Wang, R., Zhang, Y., Ye, D., and Jiang, X.C. (2008). The domain responsible for sphingomyelin synthase (SMS) activity. Biochim. Biophys. Acta. 1781, 610–617.10.1016/j.bbalip.2008.07.002Search in Google Scholar PubMed PubMed Central