Online citations, reference lists, and bibliographies.
← Back to Search

Cytochrome C Is Released In A Reactive Oxygen Species-Dependent Manner And Is Degraded Via Caspase-Like Proteases In Tobacco Bright-Yellow 2 Cells En Route To Heat Shock-Induced Cell Death1

R. A. Vacca, D. Valenti, A. Bobba, R. Merafina, S. Passarella, E. Marra
Published 2006 · Medicine, Biology

Cite This
Download PDF
Analyze on Scholarcy
To gain some insight into the mechanism of plant programmed cell death, certain features of cytochrome c (cyt c) release were investigated in heat-shocked tobacco (Nicotiana tabacum) Bright-Yellow 2 cells in the 2- to 6-h time range. We found that 2 h after heat shock, cyt c is released from intact mitochondria into the cytoplasm as a functionally active protein. Such a release did not occur in the presence of superoxide anion dismutase and catalase, thus showing that it depends on reactive oxygen species (ROS). Interestingly, ROS production due to xanthine plus xanthine oxidase results in cyt c release in sister control cultures. Maximal cyt c release was found 2 h after heat shock; later, activation of caspase-3-like protease was found to increase with time. Activation of this protease did not occur in the presence of ROS scavenger enzymes. The released cyt c was found to be progressively degraded in a manner prevented by either the broad-range caspase inhibitor (zVAD-fmk) or the specific inhibitor of caspase-3 (AC-DEVD-CHO), which have no effect on cyt c release. In the presence of these inhibitors, a significant increase in survival of the cells undergoing programmed cell death was found. We conclude that ROS can trigger release of cyt c, but do not cause cell death, which requires caspase-like activation.
This paper references
Reactive Oxygen Species Influence Nerve Growth Factor Synthesis in Primary Rat Astrocytes
P. Naveilhan (1994)
Rapid isolation of high molecular weight plant DNA.
M. G. Murray (1980)
Mitochondrial involvement in tracheary element programmed cell death
X-H Yu (2002)
Activation of caspase-like proteases and induction of apoptosis by isopentenyladenosine in tobacco BY-2 cells
P. Mlejnek (2002)
Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat‐induced programmed cell death in cucumber plants
J. Balk (1999)
Chloride Channel Inhibition Prevents ROSdependentApoptosis Induced by Ischemia-Reperfusion in Mouse Cardiomyocytes
X. Wang (2005)
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
M. M. Bradford (1976)
Production of Reactive Oxygen Species, Alteration of Cytosolic Ascorbate Peroxidase, and Impairment of Mitochondrial Metabolism Are Early Events in Heat Shock-Induced Programmed Cell Death in Tobacco Bright-Yellow 2 Cells1
R. A. Vacca (2004)
Cytochrome c release and caspase activation during menadione‐induced apoptosis in plants
Y. Sun (1999)
Membrane potential, adenylate levels and Mg2+ are interconnected via adenylate kinase equilibrium in plant cells.
A. Igamberdiev (2003)
Fas-induced Activation of the Cell Death-related Protease CPP32 Is Inhibited by Bcl-2 and by ICE Family Protease Inhibitors*
R. Armstrong (1996)
Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria
G. Petrosillo (2003)
A plant caspaselike protease activated during the hypersensitive response
N V Chichkova (2004)
Cytochrome c, released from cerebellar granule cells undergoing apoptosis or excytotoxic death, can generate protonmotive force and drive ATP synthesis in isolated mitochondria
A. Atlante (2003)
Oxidative Stress Increased Respiration and Generation of Reactive Oxygen Species, Resulting in ATP Depletion, Opening of Mitochondrial Permeability Transition, and Programmed Cell Death1
B. Tiwari (2002)
Apoptosis and cytochrome c release in cerebellar granule cells.
A. Bobba (2004)
Measuring programmed cell death in plants.
L. Rizhsky (2004)
Substrate Specificities of Caspase Family Proteases*
R. Talanian (1997)
[Mitochondrial control of apoptosis].
G. Kroemer (2001)
Tobacco BY-2 Cell Line as the “HeLa” Cell in the Cell Biology of Higher Plants
T. Nagata (1992)
Production of Reactive Oxygen Species and Release of l‐Glutamate During Superoxide Anion‐Induced Cell Death of Cerebellar Granule Neurons
Toru Satoh (1998)
Blocking Cytochrome c Activity within Intact Neurons Inhibits Apoptosis
S. Neame (1998)
An APAF-1·Cytochrome c Multimeric Complex Is a Functional Apoptosome That Activates Procaspase-9*
H. Zou (1999)
Bypasses of the antimycin a block of mitochondrial electron transport in relation to ubisemiquinone function.
A. Alexandre (1984)
Enzymes of the ascorbate biosynthesis and ascorbate-glutathione cycle in cultured cells of tobacco Bright Yellow 2
M. C. Pinto (2000)
The mitochondrion--an organelle commonly involved in programmed cell death in Arabidopsis thaliana.
N. Yao (2004)
Involvement of poly(ADP‐ribose) polymerase and activation of caspase‐3‐like protease in heat shock‐induced apoptosis in tobacco suspension cells
R. H. Tian (2000)
Porin and cytochrome oxidase containing contact sites involved in the oxidation of cytosolic NADH.
G. La Piana (2005)
Electron spin resonance study on the permeability of superoxide radicals in lipid bilayers and biological membranes
G. Mao (1992)
Cytochrome c Is Released from Mitochondria in a Reactive Oxygen Species (ROS)-dependent Fashion and Can Operate as a ROS Scavenger and as a Respiratory Substrate in Cerebellar Neurons Undergoing Excitotoxic Death*
A. Atlante (2000)
Mannose induces an endonuclease responsible for DNA laddering in plant cells.
J. C. Stein (1999)
Bax directly induces release of cytochrome c from isolated mitochondria.
J. Jürgensmeier (1998)
Changes in the Antioxidant Systems as Part of the Signaling Pathway Responsible for the Programmed Cell Death Activated by Nitric Oxide and Reactive Oxygen Species in Tobacco Bright-Yellow 2 Cells1
M. D. de Pinto (2002)
Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD‐specific caspase activation and independently of mitochondrial transmembrane depolarization
E. Bossy-Wetzel (1998)
A Plant Caspase-Like Protease Activated during the Hypersensitive Response Article, publication date, and citation information can be found at
N. Chichkova (2004)
Riboflavin Uptake and FAD Synthesis in Saccharomyces cerevisiae Mitochondria
V. Bafunno (2004)
Harpin inactivates mitochondria in Arabidopsis suspension cells.
Maren Krause (2004)
The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells
M. C. Pinto (2005)
Extracellular H(2)O(2) induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants.
D. Bellincampi (2000)
Many ways to exit? Cell death categories in plants.
W. G. van Doorn (2005)
Electron Transfer between Cytochrome c and p66Shc Generates Reactive Oxygen Species that Trigger Mitochondrial Apoptosis
M. Giorgio (2005)
Programmed cell death in cell cultures
P. McCabe (2004)
Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves.
M. Jiang (2002)
Enzymatic assay of fumarase
H U Bergmeyer (1974)
Bcl-xL Regulates the Membrane Potential and Volume Homeostasis of Mitochondria
M. V. Heiden (1997)
Cytochrome c and dATP-Dependent Formation of Apaf-1/Caspase-9 Complex Initiates an Apoptotic Protease Cascade
Peng Li (1997)
Do Plant Caspases Exist?
E. Woltering (2002)
The PET1-CMS Mitochondrial Mutation in Sunflower Is Associated with Premature Programmed Cell Death and Cytochrome c Release
J. Balk (2001)
The biochemistry of apoptosis
M. Hengartner (2000)
Programmed cell death during pollination-induced petal senescence in petunia.
Y. Xu (2000)
Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism responsible for anti‐apoptotic effects of melatonin
S. A. Andrabi (2004)
dATP causes specific release of cytochrome C from mitochondria.
J. Yang (1998)
Acrolein-induced cell death in PC12 cells: Role of mitochondria-mediated oxidative stress
J. Luo (2005)
Cascade of Caspase Activation in Potassium-Deprived Cerebellar Granule Neurons: Targets for Treatment with Peptide and Protein Inhibitors of Apoptosis
E. Gerhardt (2001)
Constitutive caspase-like machinery executes programmed cell death in plant cells
M. Elbaz (2002)
Early release and subsequent caspase‐mediated degradation of cytochrome c in apoptotic cerebellar granule cells
A. Bobba (1999)
The redox state of the ascorbatedehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells
M C De Pinto (1999)
Caspase-like protease involvement in the control of plant cell death
Eric Lam (2004)
Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response
M. Delledonne (2001)
The superoxide synthases of rose cells . Comparison Of assays
Murphy (1998)
The apoptosis/necrosis transition in cerebellar granule cells depends on the mutual relationship of the antioxidant and the proteolytic systems which regulate ROS production and cytochrome c release en route to death
A. Atlante (2003)

This paper is referenced by
An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica.
Jian Sun (2012)
Chapter 2 Mitochondrion and Chloroplast Regulation of Plant Programmed Cell Death
Theresa J. Reape (2018)
Molecular mechanisms governing plant responses to high temperatures.
B. Li (2018)
Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death.
Lingrui Zhang (2008)
Exploring the developmental plasticity of plant cells: somatic embryogenesis in root explants
D. J. Hunt (2015)
ERK-like MAPK signaling and cytochrome c response to oleic acid in two-liquid-phase suspension cultures of Taxus cuspidata
Jing-sheng Cheng (2008)
Preservation of mitochondrial functional integrity in mitochondria isolated from small cryopreserved mouse brain areas.
Daniela Valenti (2014)
OsVPE3 Mediates GA-induced Programmed Cell Death in Rice Aleurone Layers via Interacting with Actin Microfilaments
Heting Zhang (2020)
Nuclear calcium controls the apoptotic-like cell death induced by d-erythro-sphinganine in tobacco cells.
C. Lachaud (2010)
The role of the mitochondrion in plant responses to biotic stress
S. Amirsadeghi (2007)
Spatial and temporal nature of reactive oxygen species production and programmed cell death in elm (Ulmus pumila L.) seeds during controlled deterioration.
Die Hu (2012)
Reassessing apoptosis in plants
M. Dickman (2017)
Nitric oxide suppresses aluminum-induced programmed cell death in peanut (Arachis hypoganea L.) root tips by improving mitochondrial physiological properties.
H. He (2018)
Knock‐out of metacaspase and/or cytochrome c results in the activation of a ROS‐independent acetic acid‐induced programmed cell death pathway in yeast
N. Guaragnella (2010)
Different involvement of the mitochondrial, plastidial and cytosolic ascorbate-glutathione redox enzymes in heat shock responses.
Vittoria Locato (2009)
Sanguinarine-induced oxidative stress and apoptosis-like programmed cell death(AL-PCD) in root meristem cells of Allium cepa.
A. Żabka (2017)
Mechanism and Interaction of Nanoparticle-Induced Programmed Cell Death in Plants
Fatma Yanik (2018)
Unveiling Interactions among Mitochondria, Caspase-Like Proteases, and the Actin Cytoskeleton during Plant Programmed Cell Death (PCD)
Christina E. N. Lord (2013)
N-acetylcysteine reduces the renal oxidative stress and apoptosis induced by hemorrhagic shock.
M. Moreira (2016)
Metabolic Reprogramming in Chloroplasts under Heat Stress in Plants
Qing-Long Wang (2018)
Cr-induced disturbance on expression of six COX genes in rice seedlings
Xiao-Zhang Yu (2018)
Overexpression of Ferredoxin, PETF, Enhances Tolerance to Heat Stress in Chlamydomonas reinhardtii
Yi-Hsien Lin (2013)
Chloroplastic NADPH oxidase-like activity-mediated perpetual hydrogen peroxide generation in the chloroplast induces apoptotic-like death of Brassica napus leaf protoplasts
Rajesh Kumar Tewari (2011)
Chloroplasts of Arabidopsis Are the Source and a Primary Target of a Plant-Specific Programmed Cell Death Signaling Pathway[W]
C. Kim (2012)
The VvBAP1 gene is identified as a potential inhibitor of cell death in grape berries.
Shifeng Cao (2019)
Stress signalling dynamics of the mitochondrial electron transport chain and oxidative phosphorylation system in higher plants.
Corentin Dourmap (2019)
Programmed cell death of tobacco BY‐2 cells induced by still culture conditions is affected by the age of the culture under agitation
Asahi Hiraga (2010)
Crible de mutants de la mort cellulaire programmée chez Arabidopsis thaliana
Abdelmajid Djoumad (2010)
Genetic and Molecular Mechanisms Controlling Reactive Oxygen Species and Hormonal Signalling of Cell Death in Response to Environmental Stresses in Arabidopsis thaliana
Per Mühlenbock (2006)
Erratum to: Environmentally induced programmed cell death in leaf protoplasts of Aponogeton madagascariensis
Christina E. N. Lord (2010)
Nitric oxide promotes MPK6-mediated caspase-3-like activation in cadmium-induced Arabidopsis thaliana programmed cell death.
Y. Ye (2013)
Cell response to imaging contrast agents suggested for atherosclerotic plaque imaging
Amit Laskar (2013)
See more
Semantic Scholar Logo Some data provided by SemanticScholar