An Arabidopsis neutral ceramidase mutant ncer1 accumulates hydroxyceramides and is sensitive to oxidative stress

Frontiers in Plant Science

Volumn 6, Issue JUNE, 2015, Pages 1-8

  Li, Jian ^a   Bi, Fang Cheng ^a,b   Yin, Jian ^a   Wu, Jian Xin ^a   Rong, Chan ^a   Wu, Jia Li ^a   Yao, Nan ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b INSTITUTE OF ANIMAL SCIENCE   (China)

Author keywords

Arabidopsis neutral ceramidases; Ceramides; Hydroxyceramides; Oxidative stress; Sphingolipids

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 84935032571     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00460     Document Type: Article

References (39)

1. Bi, F.-C., Liu, Z., Wu, J.-X., Liang, H., Xi, X.-L., Fang, C., et al. (2014). Loss of ceramide kinase in Arabidopsis impairs defenses and promotes ceramide accumulation and mitochondrial H2O2 bursts. Plant Cell 26, 3449–3467. doi: 10.1105/tpc.114.127050
2. Chen, M., Cahoon, E. B., Saucedo-García, M., Plasencia, J., and Gavilanes-Ruíz, M. (2009). “Plant sphingolipids: structure, synthesis and function,” in: Lipids in Photosynthesis: Essential and Regulatory Functions, eds H. Wada and N. Murata (Dordrecht: Springer), 77–115. doi: 10.1007/978-90-481-2 863-1_5
3. Chen, M., Markham, J. E., Dietrich, C. R., Jaworski, J. G., and Cahoon, E. B. (2008). Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis. Plant Cell 20, 1862–1878. doi: 10.1105/tpc.107.057851
4. Dickson, R. C., and Lester, R. L. (2002). Sphingolipid functions in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1583, 13–25. doi: 10.1016/S1388-1981(02)00210-X
5. El Bawab, S., Bielawska, A., and Hannun, Y. A. (1999). Purification and characterization of a membrane-bound nonlysosomal ceramidase from rat brain. J. Biol. Chem. 274, 27948–27955. doi: 10.1074/jbc.274.39.27948
6. Futerman, A. H., and Hannun, Y. A. (2004). The complex life of simple sphingolipids. EMBO Rep. 5, 777–782. doi: 10.1038/sj.embor.7400208
7. Hannun, Y. A., and Obeid, L. M. (2002). The Ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind. J. Biol. Chem. 277, 25847–25850. doi: 10.1074/jbc.R200008200
8. Koch, J., Gaertner, S., Li, C. M., Quintern, L. E., Bernardo, K., Levran, O., et al. (1996). Molecular cloning and characterization of a full-length complementary DNA encoding human acid ceramidase. Identification of the first molecular lesion causing Farber disease. J. Biol. Chem. 271, 33110-33115. doi: 10.1074/jbc.271.51.33110
9. Kogot-Levin, A., and Saada, A. (2014).Ceramide and the mitochondrial respiratory chain. Biochimie 100, 88-94. doi: 10.1016/j.biochi.2013.07.027
10. Konig, S., Feussner, K., Schwarz, M., Kaever, A., Iven, T., Landesfeind, M., et al. (2012). Arabidopsis mutants of sphingolipid fatty acid alpha-hydroxylases accumulate ceramides and salicylates. New Phytol 196, 1086-1097. doi: 10.1111/j.1469-8137.2012.04351.x
11. Kono, M., Dreier, J. L., Ellis, J. M., Allende, M., Kalkofen, D. N., Sanders, K. M., et al. (2006). Neutral ceramidase encoded by the Asah2 gene is essential for the intestinal degradation of sphingolipids.J. Biol Chem. 281, 7324-7331. doi: 10.1074/jbc.M508382200
12. Kota, V., and Hama, H. (2014). 2’-Hydroxy ceramide in membrane homeostasis and cell signaling. Adv. Biol Regul 54,223-230. doi: 10.1016/j.jbior.2013.09.012
13. Kyogashima, M., Tadano-Aritomi, K., Aoyama, T., Yusa, A., Goto, Y., Tamiya- Koizumi, K., et al. (2008). Chemical and apoptotic properties of hydroxy- ceramides containing long-chain bases with unusual alkyl chain lengths. J. Biochem. 144, 95-106. doi: 10.1093/jb/mvn050
14. Li, C. M., Hong, S.B., Kopal, G., He, X., Linke, T., Hou, W. S., et al. (1998). Cloning and characterization of the full-length cDNA and genomic sequences encoding murine acid ceramidase. Genomics 50, 267-274. doi: 10.1006/geno.1998.5334
15. Liang, H., Yao, N., Song, J. T., Luo, S., Lu, H., and Greenberg, J. T. (2003). Ceramides modulate programmed cell death in plants. Genes Dev. 17, 2636-2641. doi: 10.1101/gad.1140503
16. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2 method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
17. Mao, C, and Obeid, L. M. (2002). “Ceramidases: regulators of turnover of ceramide and ceramide-mediated responses,” in: Ceramide Signaling, ed. A. H. Futerman (Austin, TX: Landes Bioscience), 29-40. doi: 10.1007/978-1-4419-9272-7_4
18. Mao, C, Xu, R., Bielawska, A., and Obeid, L. M. (2000). Cloning of an alkaline ceramidase from Saccharomyces cerevisiae. J. Biol Chem. 275, 6876-6884. doi: 10.1074/jbc.275.10.6876
19. Mao, C, Xu, R., Szulc, Z. M., Bielawska, A., Galadari, S. H., and Obeid, L. M. (2001). Cloning and characterization of a novel human alkaline ceramidase: a mammalian enzyme that hydrolyzes phytoceramide. J. Biol Chem. 276, 26577-26588. doi: 10.1074/jbc.M102818200
20. Mitsutake, S., Tani, M., Okino, N., Mori, K., Ichinose, S., Omori, A., et al. (2001). Purification, characterization, molecular cloning, and subcellular distribution of neutral ceramidase of rat kidney. J. Biol. Chem. 276, 26249-26259. doi: 10.1074/jbc.M102233200
21. Monjusho, H., Okino, N., Tani, M., Maeda, M., Yoshida, M., and Ito, M. (2003). A neutral ceramidase homologue from Dictyostelium discoideum exhibits an acidic pH optimum. Biochem. J. 376, 473-479. doi: 10.1042/BJ20030652
22. Ohlsson, L., Palmberg, C, Duan, R. D., Olsson, M., Bergman, T., and Nilsson, A. (2007). Purification and characterization of human intestinal neutral ceramidase. Biochimie 89, 950-960. doi: 10.1016/j.biochi.2007.03.009
23. Olsson, M., Duan, R.-D., Ohlsson, L., and Nilsson, A. (2004). Rat intestinal ceramidase: purification, properties, and physiological relevance. Am. J. Physiol. Gastrointest. Liver Physiol. 287, 929-937. doi: 10.1152/ajpgi.00155.2004
24. Pata, M. O., Wu, B. X., Bielawski, J., Xiong, T. C, Hannun, Y. A., and Ng, C. K. (2008). Molecular cloning and characterization of OsCDase, a ceramidase enzyme from rice. Plant J. 55, 1000-1009. doi: 10.1111/j.1365-313X.2008.03569.
25. Pyne, N. J., Long, J. S., Lee, S. C., Loveridge, C., Gillies, L., and Pyne, S. (2009). New aspects of sphingosine 1-phosphate signaling in mammalian cells. Adv. Enzyme Regul. 49, 214–221. doi: 10.1016/j.advenzreg.2009.01.011
26. Schmelz, E. M., Roberts, P. C., Kustin, E. M., Lemonnier, L. A., Sullards, M. C., and Dillehay, D. L. et al. (2001). Modulation of intracellular β-Catenin localization and intestinal tumor genesis in vivo and in vitro by sphingolipids. Cancer Res. 61, 6723–6729.
27. Shi, L., Bielawski, J., Mu, J., Dong, H., Teng, C., Zhang, J., et al. (2007). Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis. Cell Res. 17, 1030–11040. doi: 10.1038/cr.2007.100
28. Spiegel, S., and Milstien, S. (2003). Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 4, 397–407. doi: 10.1038/nrm1103
29. Sun, W., Hu, W., Xu, R., Jin, J., Szulc, Z. M., Zhang, G., et al. (2009). Alkaline ceramidase 2 regulates beta1 integrin maturation and cell adhesion. FASEB J. 23, 656–666. doi: 10.1096/fj.08-115634
30. Sun, W., Xu, R., Hu, W., Jin, J., Crellin, H. A., Bielawski, J., et al. (2007). Up-regulation of the human alkaline ceramidase 1 and acidceramidase mediates calcium-induced differentiation of epidermal keratinocytes. J. Invest. Dermatol. 128, 389–397. doi: 10.1038/sj.jid.5701025
31. Symolon, H., Schmelz, E. M., Dillehay, D. L., and Merrill, A. H.. (2004). Dietary soy sphingolipids suppress tumorigenesis and gene expression in 1,2-dimethylhydrazine-treated CF1 mice and ApcMin/+Mice. J. Nutr. 134, 1157–1161.
32. Tani, M., Okino, N., Mori, K., Tanigara, T., Izu, H., and Ito, M. (2000). Molecular cloning of the full-length cDNA encoding mouse neutral ceramidase. J. Biol. Chem. 275, 11229–11234. doi: 10.1074/jbc.275.15.11229
33. Ternes, P., Feussner, K., Werner, S., Lerche, J., Iven, T., Heilmann, I., et al. (2011). Disruption of the ceramide synthase LOH1 causes spontaneous cell death in Arabidopsis thaliana. New Phytol. 192, 841–854. doi: 10.1111/j.1469-8137.2011.03852.x
34. Wang, W., Yang, X., Tangchaiburana, S., Ndeh, R., Markham, J. E., Tsegaye, Y., et al. (2008). An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 20, 3163–3179. doi: 10.1105/tpc.108.060053
35. Wu, J.-X, Li, J., Liu, Z., Yin, J., Chang, Z.-Y., Rong, C., et al. (2015). The Arabidopsis ceramidase AtACER functions in disease resistance and salt tolerance. Plant J. 81, 767–780. doi: 10.1111/tpj.12769
36. Xu, R., Jin, J., Hu, W., Sun, W., Bielawski, J., Szulc, Z., et al. (2006). Golgi alkaline ceramidase regulates cell proliferation and survival by controlling levels of sphingosine and S1P. FASEB J. 20, 1813–1825. doi: 10.1096/fj.05-5689com
37. Yoshimura, Y., Okino, N., Tani, M., and Ito, M. (2002). Molecular clonng and characterization of a secretory neutral ceramidase of Drosophila melanogaster. J. Biochem. 132, 229–236. doi: 10.1093/oxfordjournals.jbchem.a003215
38. Yoshimura, Y., Tani, M., Okino, N., Iida, H., and Ito, M. (2004). Molecular cloning and functional analysis of zebrafish neutral ceramidase. J. Biol. Chem. 279, 44012–44022. doi: 10.1074/jbc.M405598200
39. Yu, X., Wang, X., Huang, X., Buchenauer, H., Han, Q., Guo, J., et al. (2011). Cloning and characterization of a wheat neutral ceramidase gene Ta-CDase. Mol. Biol. Rep. 38, 3447–3454. doi: 10.1007/s11033-010-0454-y