Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter June 1, 2005

Ceramides induce programmed cell death in Arabidopsis cells in a calcium-dependent manner

  • Helen E. Townley , Kerrie McDonald , Gareth I. Jenkins , Marc R. Knight and Christopher J. Leaver
From the journal Biological Chemistry

Abstract

While the role of C2-ceramide in the induction of programmed cell death (PCD) in animal systems has been well documented, little is known of its role in plant cells. Here we show that C2-ceramide induces PCD in Arabidopsis suspension cultures, which is preceded by the generation of a calcium transient and an increase in reactive oxygen species (ROS). Inhibition of the calcium transient prevented cell death, whereas inhibition of ROS had no effect on cell survival. These observations suggest that calcium signalling plays a role in ceramide-induced PCD but is independent of the generation of ROS.

:

These authors contributed equally to this work; Corresponding author

References

Ariga, T., Jarvis, W.D., and Yu, R.K. (1998). Role of sphingolipid-mediated cell death in neurodegenerative diseases. J. Lipid Res.39, 1–16.10.1016/S0022-2275(20)34198-5Search in Google Scholar

Balasubramanian, B., Pogozelski, W., and Tullius, T. (1998). DNA strand breaking by the hydroxyl radical is governed by the accessible surface areas of the hydrogen atoms of the DNA backbone. Proc. Natl. Acad. Sci. USA95, 9738–9743.10.1073/pnas.95.17.9738Search in Google Scholar PubMed PubMed Central

Bieberich, E., Freischutz, B., Suzuki, M., and Yu, R.K. (1999). Differential effects of glycolipid biosynthesis inhibitors on ceramide-induced cell death in neuroblastoma cells. J. Neurochem.72, 1040–1049.10.1046/j.1471-4159.1999.0721040.xSearch in Google Scholar PubMed

Bielawska, A., Crane, H.M., Liotta, D., Obeid, L.M., and Hannun, Y.A. (1993). Selectivity of ceramide-mediated biology. Lack of activity of erythro-dihydroceramide. J. Biol. Chem.268, 26226–26232.Search in Google Scholar

Brodersen, P., Peterson, M., Olszak, B., Skov, S., Odum, N., Jorgensen, L.B., Brown, R.E., and Mundy, J. (2002). Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev.16, 490–502.10.1101/gad.218202Search in Google Scholar PubMed PubMed Central

Cuvillier, O., Pirianov, G., Kleuser, B., Vanek, P.G., Coso, O.A., Gutkind, S., and Spiegel, S. (1996). Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature381, 800–803.10.1038/381800a0Search in Google Scholar PubMed

Darios, F., Lambeng, N., Troadec, J., Michel, P., and Ruberg, M. (2003). Ceramide increases mitochondrial free calcium levels via caspase 8 and Bid: role in initiation of cell death. J. Neurochem.84, 643–654.10.1046/j.1471-4159.2003.01590.xSearch in Google Scholar PubMed

Fukuda, H. (2000). Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol. Biol.44, 245–253.10.1023/A:1026532223173Search in Google Scholar

Garcia-Ruiz, C., Colell, A., Mari, M., Morales, A., and Fernandez-Checa, J.C. (1997). Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species: role of mitochondrial glutathione. J. Biol. Chem.272, 11369–11377.10.1074/jbc.272.17.11369Search in Google Scholar PubMed

Gudz, T., Tserng, K., and Hoppel, C. (1997). Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide. J. Biol. Chem.272, 24154–24158.10.1074/jbc.272.39.24154Search in Google Scholar PubMed

Hengartner, M. (2000). The biochemistry of apoptosis. Nature407, 770–776.10.1038/35037710Search in Google Scholar PubMed

Jones, A. (2000). Does the plant mitochondrion integrate cellular stress and regulate programmed cell death?Trends Plant Sci.5, 225–230.Search in Google Scholar

Kerr, J.F., Wyllie, A.H., and Currie, A.R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer26, 239–257.10.1038/bjc.1972.33Search in Google Scholar

Knight, H., and Knight, M.R. (1995). Recombinant aequorin methods for intracellular calcium measurement in plants. Methods Cell Biol.4, 201–216.10.1016/S0091-679X(08)61455-7Search in Google Scholar

Knight, M.R., Campbell, A.K., Smith, S.M., and Trewavas, A.J. (1991). Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature352, 524–526.10.1038/352524a0Search in Google Scholar

Knight, H., Trewavas, A.J., and Knight, M.R. (1996). Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell8, 489–503.Search in Google Scholar

Kolesnick, R.N., and Kronke, M. (1998). Regulation of ceramide production and apoptosis. Annu. Rev. Physiol.60, 643–665.10.1146/annurev.physiol.60.1.643Search in Google Scholar

Levine, A., Pennell, R.L., Alvarez, M.E., Palmer. R., and Lamb, C. (1996). Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol.6, 427–437.10.1016/S0960-9822(02)00510-9Search in Google Scholar

Lincoln, J.E., Richael, C., Overduin, B., Smith, K., Bostock, R., and Gilchrist, D.G. (2002). Expression of the antiapoptotic baculovirus p35 gene in tomato blocks programmed cell death and provides broad-spectrum resistance to disease. Proc. Natl. Acad. Sci. USA99, 15217–15221.10.1073/pnas.232579799Search in Google Scholar

May, M.J., and Leaver, C.J. (1993). Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. Plant Physiol.103, 621–627.10.1104/pp.103.2.621Search in Google Scholar

Mihai, R., Wong, N.A., Luckett, M., Sheffield, E., and Farndon, J.R. (1998). No correlation between phaeochromocytoma catecholamine secretion and granule ultrastructure. Br. J. Surg.85, 1681–1685.Search in Google Scholar

Mihai, R., Lai, T., Schofield, G., and Farndon, J.R. (2000). C2-Ceramide increases cytoplasmic calcium concentrations in human parathyroid cells. Biochem. Biophys. Res. Commun.268, 636–641.10.1006/bbrc.2000.2159Search in Google Scholar

Mittler, R., and Lam, E. (1995). Inhibition of programmed cell death in tobacco plants during a pathogen- induced hypersensitive response at low oxygen pressure. Plant Cell8, 1991–2001.Search in Google Scholar

Mittler, R., del Pozo, O., Meisel, L., and Lam, E. (1997). Pathogen-induced programmed cell death in plants, a possible defense mechanism. Dev. Genet.21, 279–289.10.1002/(SICI)1520-6408(1997)21:4<279::AID-DVG5>3.0.CO;2-4Search in Google Scholar

Nagata, S. (2000). Apoptotic DNA fragmentation. Exp. Cell Res.256, 12–18.10.1006/excr.2000.4834Search in Google Scholar

Quillet-Mary, A., Jaffrezou, J., Mansat, V., Bordier, C., Naval, J., and Laurent, G. (1997). Implication of mitochondrial hydrogen peroxide generation in ceramide-induced apoptosis. J. Biol. Chem.272, 21388–1395.10.1074/jbc.272.34.21388Search in Google Scholar

Rippo, M.R., Malisan, F., Ravagnan, L., Tomassini, B., Condo, I., Costantini, P., Susin, S.A., Rufini, A., Todaro, M., Kroemer, G., and Testi, R. (2000). GD3 ganglioside as an intracellular mediator of apoptosis. Eur. Cytokine Netw.11, 487–488.Search in Google Scholar

Rubinstein, B. (2000). Regulation of cell death in flower petals. Plant Mol. Biol.44, 303–318.10.1023/A:1026540524990Search in Google Scholar

Ryerson, D.E., and Heath, M.C. (1996). Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell8, 393–402.Search in Google Scholar

See, V., Koch, B., and Loeffer, J.P. (2001). C2-ceramide and reactive oxygen species inhibit pituitary adenylate cyclase activating polypeptide (PACAP)-induced cyclic-AMP-dependent signalling pathway. J. Neurochem.76, 778–788.Search in Google Scholar

Siskind, L., and Colombini, M. (2000). The lipids C2- and C16-ceramide form large stable channels: implications for apoptosis. J. Biol. Chem.275, 38640–38644.10.1074/jbc.C000587200Search in Google Scholar

Siskind, L.J., Davoody, A., Lewin, N., Marshall, S., and Colombini, M. (2003). Enlargement and contracture of C2-ceramide channels. Biophys. J.85, 1560–1575.10.1016/S0006-3495(03)74588-3Search in Google Scholar

Spassieva, S.D., Markham, J.E., and Hille, J. (2002). The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J.32, 561–572.10.1046/j.1365-313X.2002.01444.xSearch in Google Scholar

Swidzinski, J.A., Sweetlove, L., and Leaver, C.J. (2002). A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J.30, 431–446.10.1046/j.1365-313X.2002.01301.xSearch in Google Scholar

Tada, M., and Concha, M.L. (2001). Vertebrate gastrulation: calcium waves orchestrate cell movements. Current Biol.11, R470-R472.10.1016/S0960-9822(01)00284-6Search in Google Scholar

Umemura, K., Ogawa, N., Yamauchi, T., Iwata, M., Shimura, M., and Koga, J. (2000). Cerebroside elicitors found in diverse phytopathogens activate defense responses in rice plants. Plant Cell Physiol.41, 676–683.10.1093/pcp/41.6.676Search in Google Scholar PubMed

Wang, H., Jones, C., Ciacci-Zanella, J., Holt, T., Gilchrist, D.G., and Dickman, M.B. (1996). Fumonisins and Alternaria alternata lycopersici toxins: sphinganine analog mycotoxins induce apoptosis in monkey kidney cells. Proc. Natl. Acad. Sci. USA93, 3461–3465.10.1073/pnas.93.8.3461Search in Google Scholar PubMed PubMed Central

Wong, K., Li, X.-B., and Hunchuk, N. (1995). N-Acetylsphingosine (C2-ceramide) inhibited neutrophil superoxide formation and calcium influx. J. Biol. Chem.270, 3056–3062.10.1074/jbc.270.7.3056Search in Google Scholar PubMed

Published Online: 2005-06-01
Published in Print: 2005-02-01

©2005 by Walter de Gruyter Berlin New York

Downloaded on 29.3.2024 from https://www.degruyter.com/document/doi/10.1515/BC.2005.020/html
Scroll to top button