Singlet Oxygen Induces Oxidation of Cellular DNA

Ravanat, Jean‐Luc; Mascio, Paolo Di; Martinez, Gláucia Regina; Medeiros, Marisa H. G.; Cadet, Jean

doi:10.1074/jbc.m006681200

Cited by 300 publications

(192 citation statements)

References 36 publications

(42 reference statements)

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“…Therefore, our results show that the most relevant ROS, which is produced in the chlorophyll-containing lipid membranes of leaf tissue exposed to light, is 1 O 2 both under basal and stress conditions. 1 O 2 oxidizes cellular components, such as nucleic bases (Ravanat et al, 2000), proteins (Davies, 2003), and membranes and this characteristic is exploited in photodynamic therapies to kill cancer cells (Girotti and Kriska, 2004), bacteria (Maisch et al, 2007), and also to conceive herbicides (Fufezan et al, 2002;Tripathy et al, 2007). We have observed that 1 O 2 -mediated LPO precedes cell death in our 1 O 2 -overproducing mutants vte1 npq1 and ch1.…”

Section: Discussionmentioning

confidence: 64%

Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants

Triantaphylidès¹,

Krischke²,

Hoeberichts³

et al. 2008

Plant Physiology

499

358

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Reactive oxygen species act as signaling molecules but can also directly provoke cellular damage by rapidly oxidizing cellular components, including lipids. We developed a high-performance liquid chromatography-electrospray ionization-tandem mass spectrometry-based quantitative method that allowed us to discriminate between free radical (type I)-and singlet oxygen ( 1 O 2 ; type II)-mediated lipid peroxidation (LPO) signatures by using hydroxy fatty acids as specific reporters. Using this method, we observed that in nonphotosynthesizing Arabidopsis (Arabidopsis thaliana) tissues, nonenzymatic LPO was almost exclusively catalyzed by free radicals both under normal and oxidative stress conditions. However, in leaf tissues under optimal growth conditions, 1 O 2 was responsible for more than 80% of the nonenzymatic LPO. In Arabidopsis mutants favoring 1 O 2 production, photooxidative stress led to a dramatic increase of 1 O 2 (type II) LPO that preceded cell death. Furthermore, under all conditions and in mutants that favor the production of superoxide and hydrogen peroxide (two sources for type I LPO reactions), plant cell death was nevertheless always preceded by an increase in 1 O 2 -dependent (type II) LPO. Thus, besides triggering a genetic cell death program, as demonstrated previously with the Arabidopsis fluorescent mutant, 1 O 2 plays a major destructive role during the execution of reactive oxygen species-induced cell death in leaf tissues.Plant leaves capture sun-derived light energy to drive CO 2 fixation during photosynthesis. During this process, leaves need to cope with photooxidative stress when the balance between energy absorption and consumption is disturbed. Excess excitation energy in the photosystems (PSI and PSII) leads to the inhibition of photosynthesis via the production of various reactive oxygen species (ROS) at different spatial levels of the cell (Apel and Hirt, 2004;Asada, 2006;Van Breusegem and Dat, 2006). Both exposure to high light intensities and decreased CO 2 availability direct linear electron transfer toward the reduction of molecular oxygen, generating superoxide radicals (O 2 2. ) at PSI (the Mehler reaction). Superoxide dismutation generates hydrogen peroxide (H 2 O 2 ), which is detoxified in the chloroplast by ascorbate peroxidases. As such, this so-called water-water cycle participates in the dissipation of excess energy (Asada, 2006). Decreased CO 2 availability affects the first step in CO 2 fixation by shifting the carboxylation of Rubisco by the Rubisco carboxylase-oxygenase enzyme toward oxygenation, a process called photorespiration. This leads, through the action of glycolate oxidase, to peroxisomal H 2 O 2 production that is counteracted by catalases. Finally, when the intersystem electron carriers are overreduced, triplet excited P680 in the PSII reaction center as well as triplet chlorophylls in the light-harvesting antennae are produced, with the production of singlet oxygen ( 1 O 2 ) as a consequence (Krieger-Liszkay, 2005). In photosynthetic membranes, 1 O 2 ...

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Section: Discussionmentioning

confidence: 64%

Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants

Triantaphylidès¹,

Krischke²,

Hoeberichts³

et al. 2008

Plant Physiology

499

358

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“…Our experimental observations, therefore, appear to support that 1 O 2 is not the major active species involved in the formation of Cu(II)/H 2 O 2 /ascorbate-dependent DNA damages. Moreover, the presence of significant amount of thymidine oxidation products, 5-FodU and 5-HmdU, also supported that 1 O 2 was not the main effective ROS because 1 O 2 specifically induces the formation of 8-oxodG, but not 5-FodU and 5-HmdU (55).…”

Section: Mechanistic Considerationsmentioning

confidence: 69%

Identification and Quantification of a Guanine−Thymine Intrastrand Cross-Link Lesion Induced by Cu(II)/H₂O₂/Ascorbate

Hong

Cao

Wang

et al. 2006

Chem. Res. Toxicol.

136

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Reactive oxygen species (ROS) can be induced by both endogenous and exogenous processes and they can damage biological molecules including nucleic acids. It was shown that X-or γ-ray irradiation of aqueous solutions of DNA, during which · OH is one of the major ROS, can lead to the formation of intrastrand crosslink lesions where the neighboring nucleobases in the same DNA strand are covalently bonded. Previous 32 P-postlabeling studies suggested that the intrastrand crosslink lesions may arise from Fenton reaction, which also induces the formation of · OH; the structures of the proposed intrastrand crosslink lesions, however, have not been determined. Here we showed for the first time that the treatment of calf thymus DNA with Cu(II)/H 2 O 2 /ascorbate could lead to the formation of an intrastrand crosslink lesion, i.e., G^T, where the C8 of guanine is covalently bonded to the neighboring 3′ thymine through its methyl carbon. LC-MS/MS quantification results showed dose-responsive formation of G^T. In addition, the yield of the intrastrand crosslink was approximately three orders of magnitude lower than those of commonly observed single-base lesions, that is, 8-oxo-7,8-dihydro-2′-deoxyguanosine, 5-(hydroxymethyl)-2′-deoxyuridine and 5-formyl-2′-deoxyuridine. The induction of intrastrand crosslink lesion in calf thymus DNA by Fenton reagents in vitro suggests that this type of lesion might be formed endogenously in mammalian cells.

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“…These results suggest the involvement of 1 O 2 , but not H 2 O 2 , in Cu(II)-mediated DNA damage at higher concentrations of homocysteine. Recently, it is reported that 1 O 2 is able to oxidize cellular DNA directly (Ravanat et al, 2000).…”

Section: Discussionmentioning

confidence: 99%

Oxidative damage to cellular and isolated DNA by homocysteine: implications for carcinogenesis

2003

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Homocysteine is considered to be an important risk factor for cancer as well as cardiovascular diseases. To clarify whether homocysteine has potential carcinogenicity, we investigated formation of 8-oxo-7,8-dihydro-2 0 -deoxyguanosine (8-oxodG), which is known to be correlated with the incidence of cancer, induced by homocysteine in human cultured cell lines. Homocysteine increased the amount of 8-oxodG in human leukemia cell line HL-60, whereas the amount of 8-oxodG in its hydrogen peroxide (H 2 O 2 )-resistant clone HP100 was not increased. We investigated the mechanism for oxidative DNA damage by homocysteine using 32 P-labeled DNA fragments obtained from human tumor suppressor genes and a protooncogene. There were two mechanisms by which homocysteine caused DNA damage in the presence of Cu(II). A low concentration of homocysteine (20 lm) frequently induced piperidine-labile sites at thymine residues, whereas a high concentration of homocysteine (100 lm) resulted in damage principally to guanine residues. Catalase inhibited DNA damage by 20 lm homocysteine, indicating the participation of H 2 O 2 , but was ineffective in preventing DNA damage by 100 lm homocysteine. Experiments using a singlet oxygen probe showed that 100 lm homocysteine enhanced chemiluminescence intensity in deuterium oxide more than that in H 2 O. These results indicated that the metal-dependent DNA damage through H 2 O 2 is likely to be a more relevant mechanism for homocysteine carcinogenicity.

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Singlet Oxygen Induces Oxidation of Cellular DNA

Cited by 300 publications

References 36 publications

Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants

Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants

Identification and Quantification of a Guanine−Thymine Intrastrand Cross-Link Lesion Induced by Cu(II)/H₂O₂/Ascorbate

Oxidative damage to cellular and isolated DNA by homocysteine: implications for carcinogenesis

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Singlet Oxygen Induces Oxidation of Cellular DNA

Cited by 300 publications

References 36 publications

Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants

Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants

Identification and Quantification of a Guanine−Thymine Intrastrand Cross-Link Lesion Induced by Cu(II)/H2O2/Ascorbate

Oxidative damage to cellular and isolated DNA by homocysteine: implications for carcinogenesis

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Identification and Quantification of a Guanine−Thymine Intrastrand Cross-Link Lesion Induced by Cu(II)/H₂O₂/Ascorbate