Abstract
The signal events of 1 mM Ce4+ (Ce(NH4)2(NO3)6)-induced apoptosis of cultured Taxus cuspidata cells were investigated. The percentage of apoptotic cells increased from 0.82% to 51.32% within 6 days. Caspase-3-like protease activity became notable during the second day of Ce4+-treatment, and the maximum activity was 5-fold higher than that of control cells at the fourth day. When the experiment system was pretreated with acetyl-Asp-Glu-Val-Asp-aldehyde (Ac-DEVD-CHO) at 100 μM, caspase-3-like activity resulted in distinct inhibition by 70% and 77.3% after 3 and 4 days of induction. Furthermore, 100 μM Ac-DEVD-CHO partially reduced the apoptotic cells by 58.6% and 60.8% at day 4 and 5 respectively. Ce4+ induced superoxide anions (O2·−) transient burst, and the first peak appeared at around 3.7–4 h, the second appeared at about 7 h. Both O2·− burst and cell apoptosis were effectively suppressed by application of diphenyl iodonium (NADPH oxidase inhibitor). Inhibition of O2·− production attenuated caspase-3-like activation by 49% and 53.6% during day 3 and 4 respectively. In addition, a total of 15 protein spots changed in response to caspase-3-like protease activation were identified by two-dimensional gel electrophoresis. These results suggest that Ce4+ of 1 mM induces apoptosis in suspension cultures of T. cuspidata through O2·− burst as well as caspase-3-like protease activation. The burst of O2·− exerts its activity as an upstream of caspase-3-like activation. Our results also implicate that other signal pathways independent of an O2·− burst possibly participate in mediating caspase-3-like protease activation.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- Ac-DEVD-AMC:
-
acetyl-Asp-Glu-Val-Asp-aminomethylcoumarin
- Ac-DEVD-CHO:
-
acetyl-Asp-Glu-Val-Asp-aldehyde
- DPI:
-
diphenylene iodonium
- PBS:
-
phosphate buffered saline
- PI:
-
propidium iodide
- REEs:
-
rare earth elements
- ROS:
-
reactive oxygen species.
References
J Balk SK Chew CJ Leaver PF. Mccabe (2003) ArticleTitleThe intermembrance space of plant mitochondria contains a Dnase activity that may be involved in programmed cell death Plant J 34 573–583 Occurrence Handle10.1046/j.1365-313X.2003.01748.x Occurrence Handle1:CAS:528:DC%2BD3sXlsFelsrs%3D Occurrence Handle12787240
EP. Beers (1997) ArticleTitleProgrammed cell death during plant growth and development Cell Death Differ 4 649–661 Occurrence Handle10.1038/sj.cdd.4400297
B Buckner GS Johal D. Janick-Buckner (2000) ArticleTitleCell death in maize Physiol Plant 108 231–239 Occurrence Handle10.1034/j.1399-3054.2000.108003231.x Occurrence Handle1:CAS:528:DC%2BD3cXislSntLg%3D
HM Chen J Zhou YR. Dai (2000) ArticleTitleCleave of lamin-like proteins in in vivo and in vitro apoptosis of tobacco protoplasts induced by heat shock FEBS Lett. 480 165–168 Occurrence Handle10.1016/S0014-5793(00)01912-8 Occurrence Handle1:CAS:528:DC%2BD3cXmt1Sju7s%3D Occurrence Handle11034321
NV Chichkova SH Kim ES Titova et al. (2004) ArticleTitleA plant caspase-like protease activated during the hypersensitive response Plant Cell 16 157–171 Occurrence Handle10.1105/tpc.017889 Occurrence Handle1:CAS:528:DC%2BD2cXosVeltA%3D%3D Occurrence Handle14660804
YM Chung YS Bae SY. Lee (2003) ArticleTitleMolecular ordering of ROS production, mitochondrial changes, and caspase activtion during sodium saliculate-induced apoptosis Free Radical Biol Med 34 434–442 Occurrence Handle10.1016/S0891-5849(02)01301-1 Occurrence Handle1:CAS:528:DC%2BD3sXptFGiug%3D%3D
A Clarke D Radhika RD Hurst JT Hancock SJ. Neill (2000) ArticleTitleNO way back: Nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures Plant J 24 667–677 Occurrence Handle10.1046/j.1365-313x.2000.00911.x Occurrence Handle1:CAS:528:DC%2BD3MXltFOksA%3D%3D Occurrence Handle11123805
J Dat S Vandenabeele E Vranaová M Montagu ParticleVan D Inzé F. Van Breusegem ParticleVan (2000) ArticleTitleDual action of the active oxygen species during plant stress responses Cell Mol life Sci 57 779–795 Occurrence Handle10.1007/s000180050041 Occurrence Handle1:CAS:528:DC%2BD3cXksFyisrk%3D Occurrence Handle10892343
AJ Jong ParticleDe FA Hoeberichts ET Yakimova E Maximova EJ. Woltering (2000) ArticleTitleChemical-induced apoptotic cell death in tomato cells: Involvement of caspase-like proteases Planta 211 656–662 Occurrence Handle10.1007/s004250000341 Occurrence Handle11089678
AJ Dong ParticleDe ET Yakimova VM Kapchina EJ. Woltering (2002) ArticleTitleA critical role for ethtlene in hydrogen perxide release during programmed cell death in tomato suspension cells Planta 214 537–545 Occurrence Handle10.1007/s004250100654 Occurrence Handle11925037
SL Dellaporta J Wood JB. Hicks (1983) ArticleTitleA plant DNA minipreparation: Version II Plant Mol Biol Rep 1 19–23 Occurrence Handle1:CAS:528:DyaL2cXksFWhtrk%3D
O Del Pozo E. Lam (1998) ArticleTitleCaspases and programmed cell death in the hypersensitive response of plants to pathogens Curr Biol 8 1129–1132 Occurrence Handle10.1016/S0960-9822(98)70469-5 Occurrence Handle1:CAS:528:DyaK1cXmslagsLs%3D Occurrence Handle9778530
M Elbaz A Avni M. Weil (2002) ArticleTitleConstitutive caspase-like machinery executes programmed cell death in plant cells Cell Death Differ 9 726–733 Occurrence Handle10.1038/sj.cdd.4401030 Occurrence Handle1:STN:280:DC%2BD38zhsFCjsw%3D%3D Occurrence Handle12058273
RE Ellis JY Yuan HR. Horvitz (1991) ArticleTitleMechanism and functions of cell death Annu Rev Cell Biol 7 663–698 Occurrence Handle10.1146/annurev.cb.07.110191.003311 Occurrence Handle1:CAS:528:DyaK38Xitlyj Occurrence Handle1809356
ZQ Ge YJ Yuan YD Wang ZY Ma ZD. Hu (2002) ArticleTitleCe4+-induced apoptosis of Taxus cuspidata cells in suspensions culture J Rare Earths 20 139–144
RB Han YJ. Yuan (2004) ArticleTitleOxidative burst in suspension culture of Taxus cuspidata induced by a Laminar shear stress in short-term Biotechnol Prog 20 507–513 Occurrence Handle10.1021/bp034242p Occurrence Handle1:CAS:528:DC%2BD3sXpsFygsro%3D Occurrence Handle15058996
X He AR. Kermode (2003) ArticleTitleProteases associated with programmed cell death of megagametophyte cells after germination of white spruce (Picea glauca) seeds Plant Mol Biol 52 729–744 Occurrence Handle10.1023/A:1025008117046 Occurrence Handle1:CAS:528:DC%2BD3sXmtVentLc%3D Occurrence Handle13677463
YW He CS. Loh (2000) ArticleTitleCerium and lanthanum promote floral initiation and reproductive growth of Arabidopsis thaliana Plant Sci 159 117–124 Occurrence Handle10.1016/S0168-9452(00)00338-1 Occurrence Handle1:CAS:528:DC%2BD3cXmslOqu7k%3D Occurrence Handle11011099
T Jabs M TschÖpe C Colling K Hahlbrock D. Scheel (1997) ArticleTitleElicitor-stimulated ion fluxes and O2·− from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley Proc Natl Acad Sci 94 4800–4805 Occurrence Handle10.1073/pnas.94.9.4800 Occurrence Handle1:CAS:528:DyaK2sXjtVykur0%3D Occurrence Handle9114072
BF Jin K He HX Wang et al. (2003) ArticleTitleProteomic analysis of ubiquitin-proteasome effects: insight into the function of eukaryotic initiation factor 5A Oncogene 22 4819–4830 Occurrence Handle10.1038/sj.onc.1206738 Occurrence Handle1:CAS:528:DC%2BD3sXlvVKnsrg%3D Occurrence Handle12894223
T Kaji S Hachimura W Ise S. Kaminogawa (2003) ArticleTitleProteome analysis reveals caspase activation in hyporesponsive CD4 T lymphocytes induced in vivo by the oral administration of antigen J Biol Chem 278 27836–27843 Occurrence Handle10.1074/jbc.M212820200 Occurrence Handle1:CAS:528:DC%2BD3sXlsFKktbc%3D Occurrence Handle12736267
HAAJ Korthout G Berecki W Bruin BV Duijn M. Wang (2000) ArticleTitleThe presence and subcellular localization of caspase 3-like proteinases in plant cells FEBS Lett 475 139–144 Occurrence Handle10.1016/S0014-5793(00)01643-4 Occurrence Handle1:CAS:528:DC%2BD3cXktVSnurw%3D Occurrence Handle10858505
A Levine R Tenhaken RA Dixon CJ. Lamb (1994) ArticleTitleH2O2 from the oxidative burst orchestrates the pant hypersensitive disease resistance response as a local trigger of programmed cell death and a diffusible inducer of cellular protectant genes Cell 79 583–593 Occurrence Handle10.1016/0092-8674(94)90544-4 Occurrence Handle1:CAS:528:DyaK2MXit1Glu7Y%3D Occurrence Handle7954825
C Li YJ Yuan ZH Ma ZD Hu AC Sun CX. Hu (2002) ArticleTitleCell apoptosis induced by oligosaccharide in suspension cultures of Taxus chinensis Acta Botanica Sinica 44 598–602 Occurrence Handle1:CAS:528:DC%2BD3sXlt1amur4%3D
P Mlejnek S. Procházka (2002) ArticleTitleActivation of caspase-like proteases and induction of apoptosis by isopentenyladenosine in tobacco BY-2 cells Planta 215 158–166 Occurrence Handle10.1007/s00425-002-0733-5 Occurrence Handle1:CAS:528:DC%2BD38Xjt1GitLo%3D Occurrence Handle12012253
K Overmyer H Tuominen R Kettunen et al. (2000) ArticleTitleOzone-sensitive Arabidopsisrcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death Plant Cell 12 1849–1862 Occurrence Handle10.1105/tpc.12.10.1849 Occurrence Handle1:CAS:528:DC%2BD3cXotFaisL8%3D Occurrence Handle11041881
JJ Qiao YJ Yuan H Zhao JC Wu AP. Zeng (2002) ArticleTitleApoptotic cell death in suspension cultures of Taxus cuspidata co-treated with salicylic acid and hydrogen peroxide Biotechnol Lett 25 387–390 Occurrence Handle10.1023/A:1022494213446
PH Ryerson MC. Heath (1996) ArticleTitleCleavage of nuclear DNA into oligonucleosomal framents during cell death induced by fungal infection or abiotic treatments Plant Cell 8 393–402 Occurrence Handle10.1105/tpc.8.3.393 Occurrence Handle1:CAS:528:DyaK28XitVKmtLo%3D Occurrence Handle12239388
S Simizu M Takada K Umezawa M. Imoto (1998) ArticleTitleRequirements of caspase-3-(-like) protease-mediated Hydrogen Peroxide production for apoptosis induced by various anticancer drugs J Biol Chem 273 26900–26907 Occurrence Handle10.1074/jbc.273.41.26900 Occurrence Handle1:CAS:528:DyaK1cXmslais70%3D Occurrence Handle9756937
M Solomon B Belenghi M Delledone E Menachem A. Levine (1999) ArticleTitleThe involvement of cysteine proteases and protease inhibitors genes in the regulation of programmed cell death in plants Plant Cell 11 431–443 Occurrence Handle10.1105/tpc.11.3.431 Occurrence Handle1:CAS:528:DyaK1MXitlehs7c%3D Occurrence Handle10072402
SJ Stohs D. Bagchi (1995) ArticleTitleOxidative mechanism in the toxicity of metal ions Free Rad Biol Med 18 321–336 Occurrence Handle10.1016/0891-5849(94)00159-H Occurrence Handle1:CAS:528:DyaK2MXjsFOrsLg%3D Occurrence Handle7744317
Y Sun DL Liu ZQ Yu Q Zhang J Bai DY. Sun (2003) ArticleTitleAn apoplastic mechanism for short-term effects of rare earth elements at lower concentrations Plant Cell Environ 26 887–896 Occurrence Handle10.1046/j.1365-3040.2003.01021.x Occurrence Handle1:CAS:528:DC%2BD3sXls1Gnt7g%3D Occurrence Handle12803616
B Thiede F Siejak C Dimmler T. Rudel (2002) ArticleTitlePrediction of translocation and cleavage of heterogeneous ribonuclear proteins and Rho guanine nucleotide dissociation inhibitor 2 during apoptosis by subcellular proteome analysis Proteomics 2 996–1006 Occurrence Handle10.1002/1615-9861(200208)2:8<996::AID-PROT996>3.0.CO;2-3 Occurrence Handle1:CAS:528:DC%2BD38Xmslyhs70%3D Occurrence Handle12203895
RH Tian GY Zhang CH Yan YR. Dai (2000) ArticleTitleInvolvement of poly(ADP-ribose)polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells FEBS Lett 474 11–15 Occurrence Handle10.1016/S0014-5793(00)01561-1 Occurrence Handle1:CAS:528:DC%2BD3cXjs1ChsL4%3D Occurrence Handle10828442
W Wätjen D. Beyersmann (2004) ArticleTitleCadmium-induced apoptosis in C6 glioma cells: Influence of oxidative stress Biometals 17 65–78 Occurrence Handle10.1023/A:1024405119018 Occurrence Handle14977363
W Wätjen M Cox M Biagioli D. Beyersmann (2002) ArticleTitleCadmium-induced apoptosis in C6 glioma cells: Mediation by caspase 9-activation Biometals 15 15–25 Occurrence Handle10.1023/A:1013141926228 Occurrence Handle11860019
C Yu M Rahmani P Dent S. Grant (2004) ArticleTitleThe hierarchical relationship between MAPK signaling and ROS generation in human leukemia cells undergoing apoptosis in response to the proteasome inhibitor bortezomib Exp Cell Res 295 555–566 Occurrence Handle10.1016/j.yexcr.2004.02.001 Occurrence Handle1:CAS:528:DC%2BD2cXjt1alsbw%3D Occurrence Handle15093752
YJ Yuan ZQ Ge JC Li JC Wu ZD. Hu (2002a) ArticleTitleDifferentiation of apoptotic and necrotic cells in suspension cultures of Taxus cuspidataby the combined use of fluorescent dying and histochemical staining methods Biotechnol Lett 24 71–76 Occurrence Handle10.1023/A:1013819228190 Occurrence Handle1:CAS:528:DC%2BD38XhtlKmsb4%3D
YJ Yuan GW Hu CG Wang Y Jing YQ Zhou PW. Shen (1998) ArticleTitleEffect of rare earth compounds on the growths, Taxol biosynthesis and release of Taxus Cuspidata cell culture J Rare Earths 16 56–60 Occurrence Handle1:CAS:528:DyaK1cXntFent74%3D
YJ Yuan JC Li ZQ Ge JC. Wu (2002b) ArticleTitleSuperoxide anion burst and taxol production induced by Ce4+ in suspension cultures of Taxus cuspidata J Mol Catal B: Enzym 18 251–260 Occurrence Handle10.1016/S1381-1177(02)00103-0 Occurrence Handle1:CAS:528:DC%2BD38XnsVaitLs%3D
A Zuppini B Baldan R Millioni F Favaron L Navazio P. Mariani (2003) ArticleTitleChitosan induces Ca2+-mediated programmed cell death in soybean cells New Phytol 161 557–568 Occurrence Handle10.1046/j.1469-8137.2003.00969.x
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ge, ZQ., Yang, S., Cheng, JS. et al. Signal role for activation of caspase-3-like protease and burst of superoxide anions during Ce4+-induced apoptosis of cultured Taxus cuspidata cells. Biometals 18, 221–232 (2005). https://doi.org/10.1007/s10534-005-0582-3
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10534-005-0582-3