Abstract
Ion fluxes across the plasma membrane activated by 1 mM Ce4+, cell apoptosis and taxol biosynthesis in suspension cultures ofTaxus cuspidata were studied. The extracellular pH sharply decreased upon the addition of 1 mM Ce4+, then increased gradually and exceeded the initial pH value over a time period of 12 h. The extracellular Ca2+ concentration decreased within the first 3 h after the addition of Ce4+, then gradually decreased to one third of initial value in control at about 72 h and remained unchanged afterwards. Experiments with an ion channel blocker and a Ca2+-channel blocker indicated that the dynamic changes in extracellular pH and the Ca2+ concentration resulted from the Ce4+-induced activation of H+ uptake and Ca2+ influx across the plasma membranevia ion channels. A pretreatment of the ion channel blocker initiated Ce4+-treated cells to undergo necrosis, and the prior addition of the Ca2+-channel blocker inhibited Ce4+-induced taxol biosynthesis and apoptosis. It is thus inferred that H+ uptake is necessary for cells to survive a Ce4+-caused acidic environment and is one of the mechanisms of Ce4-induced apoptosis. Furthermore, the Ca2+ influx across the plasma membrane mediated both the Ce4+-induced apoptosis and taxol biosynthesis.
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Hirasuna, T. J., L. J. Pestchanker, and V. Srinivasan (1996) Taxol production on suspension cultures ofTaxus baccata.Plant Cell Tiss. Org. Cult. 44: 95–106.
Ketchum, R. E. B., D. M. Gibson, R. B. Croteau, and M. L. Shuler (1999) The kinetics of taxoid accumulation in cell suspension cultures ofTaxus following elicitation with methyl jasmonate.Biotechnol. Bioeng. 62: 97–105.
Yukimune, Y., H. Tabata, Y. Higashi, and Y. Hara (1996) Methyl jasmonic-induced overproduction of paclitaxel and baccatin III inTaxus cell suspension cultures-addition of methyl jasmonic acid as elicitor toTaxus baccata andTaxus medis suspension cell culture.Natural Biotech. 14: 1129–1132.
Yuan, Y. J., Z. Y. Ma, Z. Q. Ge, Z. Q. Miao, and A. P. Zeng (2000) Apoptosis and taxol production in suspension cultures ofTaxus spp. cells.J. Chem. Ind. Eng. 51 (Suppl.): 43–46.
Yuan, Y. J., G. W. Hu, and C. G. Wang (1998) Effect of La, Ce onTaxus cuspidata cell growth, biosynthesis and release of taxol.J. Rare Earth 16: 300–306.
Li, J. C., Z. H. Ma, Y. J. Yuan, A. C. Sun, and C. X. Hu (2001) Dynamic effects of cerium on syntheses of soluble protein and taxol in suspension culture ofTaxus Chinensis var.mairei cells.Rare Earth 19: 233–238.
Yuan, Y. J., J. C. Li, Z. Q. Ge, and J. C. Wu (2002) Superoxide anion burst and taxol production induced by Ce4+ in suspension cultures ofTaxus cuspidata.J. Mol. Catalysis B: Enzymatic 18: 551–560.
Serrano, R. (1989) Structure and function of plasma membrane ATPase.Annu. Rev. Plant Physiol Plant Mol. Biol. 40: 61–94.
Yuan, Y. J., Z. Q. Ge, J. C. Li, J. C. Wu, and Z. D. Hu (2002) Differentiation of apoptotic and necrotic cells in suspension cultures ofTaxus cuspidata by the combined use of fluorescent dying and histochemical staining methods.Biotechnol. Lett. 24: 71–76.
Jabs, T., M. Tschöpe, C. Colling, K. Hahlbrock, and D. Scheel (1997) Elicitor-stimulated ion fluxes and O −2 from the oxidative burst are essential components in triggering defense gene activation and phytoalexins synthesis in parsley.Proc. Natl. Acad. Sci. USA 94: 4800–4805.
Segal, J. (1986) Lunthanum increases the rat thymocytes cytoplasmic free calcium concentration by enhancing calcium influx.Biochim. Biophys. Acta 886: 267–271.
Powis, D. A., C. L. Clark, and K. J. O’brien (1994) Lanthanum can be transported by the sodium-calcium exchange pathway and directly triggers cathcholamine release from bovine chromaffin cells.Cell Calcium 16: 377–390.
Gelli, A., V. J. Higgins, and E. Blumwald (1997) Activation of plasma membrane Ca2+-permeable channels by race-specific fungal elicitors.Plant Physiol. 113: 269–279.
Xu, H. and M. C. Health (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of theCompea rust fungus.Plant Cell 10: 585–598.
Ormerod, M. G., X. M. Sun, R. T. Snowden, and R. Davies (1993) Increased membrane permeability of apoptotic thymocytes: A flow cytometric study.Cytometry 14: 595–602.
Wu, Z. L., Y. J. Yuan, Z. H. Ma, and Z. D. Hu (2000) Kinetics of two-liquid-phase Taxus cuspidata cell culture for production of Taxol.Biochem. Eng. J. 5: 137–142.
Sze, H., X. Li, and M. G. Palmgren (1999) Energization of plant cell membranes by H+-pumping ATPases: Regulation and biosynthesis.Plant Cell 11: 677–689.
Blein, J. P., M. L. Milat, and P. Ricci (1991) Responses of cultured tobacco cells to cryptogein, a proteinaceous elicitor formPhytophthora cryptogea.Plant Physiol. 95: 486–491.
Hu, G. W., J. C. Li, and Y. J. Yuan (2000) Effect of rare earth onTaxus cuspidata intracellular calcium concentration.J. Tianjin Univ. (Sci. Technol.) 33: 19–20.
Atkinson, M. M., L. D. Keppler, and E. W. Orlandi (1990) Involvement of plasma membrane calcium influx in bacterial induction of the K+/H+ and hypersensitive responses in tobacco.Plant Physiol. 92: 215–221.
Baker, C. J., M. M. Atkinson, and A. Collmer (1987) Concurrent loss in Tn5 mutants ofPseudomonas syringae pv.Syringae of the ability to induce the hypersensitive response and host plasma membrane K+/H+ exchange in tobacco.Phytopathology 77: 1268–1272.
Lichtenthaler, H. K. (1998) The stress concept in plants: An introduction.Ann. N. Y. Acad. Sci. 351: 187–198.
Barry, M. A., J. E. Roynolds, and A. Eastman (1993) Etopside-induced apoptosis in human HL-60 cells is associated with intracellular acidification.Cancer Res 53: 2349–2357.
Chen, Q., R. S. P. Benson, A. D. Whetton, S. R. Brant, M. Donowitz, M. H. Montrose, C. Dive, and A. J. M. Watson (1997) Role of acid/base homeostasis in the suppression of apoptosis in haemopoietic cells by v-Abl protein tyrosine kinase.J. Cell Sci. 110: 379–387.
Li, J. and A. Eastman (1995) Apoptosis in a interleukin-2-dependent cytotoxic T lymphocyte cell line is associated with intracellular acidification.J. Biol. Chem. 270: 3203–3211.
Rajotte, D., P. Haddad, A. Human, E. J. J. Cragoe, and T. Hoang (1992) Role of protein kinase C and the Na+/H+ antiport in suppression of apoptosis by granulocyte macrophage colony-stimulating factor in interleukin-3.J. Biol. Chem. 267: 9980–9987.
Nürnberger, T., D. Nennstiel, T. Jabs, W. R. Sacks, K. Hahlbrock, and D. Scheel (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses.Cell 78: 449–460.
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Li, JC., Ge, ZQ. & Yuan, YJ. Ce4+-stimulated ion fluxes are responsible for apoptosis and taxol biosynthesis in suspension cultures of Taxus cells. Biotechnol. Bioprocess Eng. 10, 109–114 (2005). https://doi.org/10.1007/BF02932579
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DOI: https://doi.org/10.1007/BF02932579