Skip Navigation


Mutagenesis Advance Access originally published online on November 13, 2007
Mutagenesis 2008 23(1):19-26; doi:10.1093/mutage/gem028
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
23/1/19    most recent
gem028v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Shi, Y.
Right arrow Articles by Zheng, R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shi, Y.
Right arrow Articles by Zheng, R.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?


© The Author 2007. Published by Oxford University Press on behalf of the UK Environmental Mutagen Society. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org.

Fast repair of oxidative DNA damage by phenylpropanoid glycosides and their analogues

Yimin Shi1, Wengfeng Wang3, Chungyang Huang1, Zhongjian Jia2, Side Yao3 and Rongliang Zheng1,4,*

1School of Life Sciences 2College of Chemistry and Chemical Engineering, Lanzhou University, Lanzhou 730000, P.R. China 3Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai 201800, P.R. China 4E-Institutes of Shanghai Municipal Education Commission, Shanghai 200000, P.R. China

The repair activities and reaction mechanisms of phenylpropanoid glycosides (PPGs) and their analogues, isolated from Chinese folk medicinal herbs, towards oxidative DNA damage were studied with pulse radiolytic technique. On pulse irradiation of nitrogen-saturated 4 mM poly C aqueous solution containing one of the tested polyphenols, 40 mM K2S2O8 and 200 mM t-BuOH, the transient absorption spectrum of the oxidative radical of poly C decays with the concurrent formation of the phenoxyl radical of the tested polyphenols within several tens of microseconds after the electron pulse irradiation. The result indicated that there was a repair reaction between oxidative radical of poly C and the tested polyphenols. The repair activities also were observed for the tested polyphenols towards the radical cations of single-stranded DNA (ssDNA) and double-stranded DNA (dsDNA). The rate constants were determined to be 3.7–6.4 x 109, 4.8–5.5 x 108 and 8.8–10.3 x 108 M–1·sec–1 for the repair reactions of oxidative radical of poly C and radical cations of ssDNA and dsDNA, respectively. The result of this study together with those of our previous studies demonstrates that PPGs and their analogues can fast repair not only the damage of deoxynucleoside and deoxynucleotide but also the damage of integral DNA, with the latter being closer to a cellular condition.


   Introduction
Top
 Introduction
Materials and methods
 Results
 Discussion
 Funding
 References
 
Many pathological processes including cancer and ageing are related to DNA damage. These can be caused by environmental agents, such as ionizing radiation, UV light and a variety of chemical agents, as well as normal cellular metabolism in which reactive oxygen species (ROS) are formed as by-products. The results of electron paramagnetic resonance studies demonstrated that base radicals including radical cations and anions, resulting from ionizing radiation or oxidation by oxidizing intermediates of chemical carcinogens, are able to induce strand breaks (1Go,2Go) and form stable base lesions (3Go,4Go). Although evolution grants cells an effective enzymatic repair system to repair damaged DNA (5Go), enzymatic repair is not perfect, and there always is some DNA damage slipping through the enzymatic repair system. Moreover, cell's repair capacity of DNA damage decreases as cell ages, while in the process of ageing, more deleterious oxygen species are formed, resulting in accumulation of DNA damage and increase of the mutation frequencies. Therefore, DNA damage may be regarded as an inevitable product of living, which always exists prior to DNA replication, and hence, the possibility of mutation leading to degenerative diseases can never be expelled. Thus, it is imperative that effort be made to look for approaches by which either ROS can be scavenged prior to damaging DNA or cell's inadequate repair capacity can be supplemented.

With this in mind, much attention has been focused on the scavenging activity of antioxidants in preventing DNA from the attack of ROS. In the case of ionization, however, because ionization occurs within the DNA itself, the DNA damage caused thereby cannot be prevented by antioxidants. With regard to indirect effect, because of very high reactivity of hydroxyl radical being the primary product of ionization (6Go) and the much higher concentration of biomolecules than antioxidants in cells, the reactions of hydroxyl radical with biomolecules are very difficult to be prevented even by the most reactive hydroxyl radical scavengers in vivo. In light of these, non-enzymatic repair of DNA damage, that is, the elimination or neutralization of DNA radicals either resulting from ionization or generated secondarily by the hydroxyl radical attack, can be explored as a feasible strategy for the reduction of damage such as mutation induced by hydroxyl radical or ionization (7Go).

With regard to non-enzymatic repair of DNA damage, O'Neill reported that there was a fast repair process by endogenous antioxidants, such as thiols and ascorbate, towards oxidizing hydroxyl radical adducts of dGMP and dG with high rate constants (3.6 x 107 to 8.4 x 108 M–1·sec–1) (8Go). Jiang's study showed that hydroxycinnamic acid derivatives could fast repair hydroxyl radical adduct of dGMP (9Go). The fast repair activities of phenylpropanoid glycosides (PPGs) and their analogues towards hydroxyl radical adducts of dGMP, dAMP (10Go–13Go), thymine radical anions (14Go,15Go), TMP radical anions (16Go) and radical cations of dAMP, dGMP and dCMP (17Go) have been investigated in our laboratory. However, so far there is no report indicating that the oxidative damage of integral DNA rather than only DNA constituent can be fast repaired by endogenous reductants or by natural antioxidants. Furthermore, previous evidences were not sufficient to support the universality of fast repair of DNA damage by chemicals. Our present study focuses on the non-enzymatic repair of oxidative damage in integral DNA, rather than constituents of DNA, by PPGs and their analogues.

PPGs, a class of polyphenols, exist in Pedicularis species and other plants and have been proved to be potent antioxidants. Pedicularis is a Chinese folk medicinal herb used as a tonic (18Go). Some PPGs extracted from other plants have been reported to have antioxidative (19Go,20Go), antitumor (21Go,22Go), antiviral (23Go) and antiplatelet activities (24Go), and to inhibit leukotriene B4 formation (25Go). Our previous studies found that PPGs were able to inhibit the lipid peroxidation of mouse liver microsomes (26Go,27Go) and linoleic acid in micelles (27Go), inhibit haemolysis of erythrocyte induced by radicals (28Go), chelate ferrous ions (29Go), inhibit the growth of tumor cells (30Go) and enable tumor cells to redifferentiate (31Go), scavenge ·OH (32Go,33Go) as well as fast repair DNA damage induced by oxidative stress (10Go–17Go). The pharmacological activities and mechanisms of natural PPGs were reviewed by us (34Go). 6-O-(E)-Feruloyl-glucose (FG) and 6-O-(E)-p-hydroxy-cinnamoyl-glucose (HCG), analogues of PPG, were isolated and purified from Aristolochia manshuriensis Kom. Aristolochia L. genus is a folk medicinal herb being used as emmenagogue, lactogogue, diuretics and painkiller, and to treat stomatitis, glossitis, absence of mind, oedema, leakorrhea, amenorrhoea, arthritis, poisoning and pruritus. High doses of Aristolochia L. genus can induce acute kidney function exhaustion (35Go–37Go).

In the present study, the repair effect of natural polyphenols on oxidative damage of DNA was investigated by pulse radiolytic technique.


   Materials and methods
Top
 Introduction
 Materials and methods
Results
 Discussion
 Funding
 References
 
Materials
Pedicularioside A (PED A) and cistanoside C (CIS C) were isolated and purified from Pedicularis. FG and HCG, were isolated and purified from A. manshuriensis Kom. Their structures are shown in Figure 1. Poly C and DNA were purchased from Sigma (St. Louis, MO). Single-stranded DNA (ssDNA) was obtained by boiling 4 mM double-stranded DNA (dsDNA) for 10 min followed by immediate cooling with an ice bath for 20 min. All other chemicals were purchased from Shanghai Biochemical Corporation (Shanghai, China) and were of reagent grade.


Figure 1
View larger version (15K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Fig. 1. Structures of tested phenylpropanoid glycosides and their analogues.

 
Pulse radiolysis
Pulse radiolysis experiment was conducted using a linear accelerator providing 8 MeV electron pulse with the duration of 8 nsec. The dosimetery of the electron pulse was determined by a thiocyanate dosimeter containing 10 mM KSCN solution saturated with nitrous oxide, by taking {epsilon}(SCN)– = 7600 dm3.mol–1.cm–1480 nm at 480 nm. The detailed description of the pulse radiolysis equipment and experimental conditions had been given elsewhere (38Go). In the present work, the average pulse dose was 14 Gy.

Generation of radical cations of DNA
On pulse radiolysis of 4 mM DNA aqueous solution containing 40 mM K2S2O8 and 200 mM t-BuOH and saturated with N2, hydrated electrons (eFormula), OH· and hydrogen atoms (H·) were produced with G's (µmol/J) of 0.29, 0.29 and 0.06, respectively (39Go). OH· was scavenged by t-BuOH to form the t-BuOH(–H)·, while H· and eFormula reacted with S2OFormula to produce SOFormula:

Formula (1)

Formula (2)

Formula (3)

Formula (4)
SOFormula reacted with DNA to form DNA radical cations:

Formula (5)


   Results
Top
 Introduction
 Materials and methods
 Results
Discussion
 Funding
 References
 
Transient absorption spectra of oxidative radical of poly C and radical cations of ssDNA and dsDNA
On pulse irradiation of 4 mM poly C aqueous solution containing 40 mM K2S2O8 and 200 mM t-BuOH and saturated with nitrogen at pH 7.0, a transient absorption spectrum was observed and was characterized by an optical absorption maximum at 440 nm (Figure 2A). In this reaction system, because of the much higher concentration of K2S2O8 than that of poly C, the primary products of pulse irradiation, H· and eFormula, reacted predominately with K2S2O8, producing secondary oxidative free radical SOFormula (Equations 3 and 4). SOFormula then reacted with poly C to produce C(5)-yl and C(6)-yl sulphate radical adducts of poly C (oxidative radical of poly C) (4). The absorption spectrum observed, therefore, should be assigned to the oxidative radical of poly C. The transient spectra of ssDNA and dsDNA radical cations were also observed under the same condition (Figure 2B and C).


Figure 2
View larger version (11K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Fig. 2. Transient absorption spectra of DNA radical cations obtained by pulse radiolysis of their nitrogen-saturated 4 mM aqueous solution containing 40 mM K2S2O8 and 200 mM t-BuOH at pH 7.0. (A) Poly C·+ at 2 µsec; (B) ssDNA·+ at 15 µsec; (C) dsDNA·+ at 20 µsec.

 
Transient absorption spectra of phenoxyl radicals of tested polyphenols
On pulse radiolysis of 0.1 mM PED A aqueous solution containing 20 mM K2S2O8 ans 200 mM t-BuOH and saturated with nitrogen, a transient absorption spectrum appeared and was characterized by a maximum absorption within 390–400 nm (Figure 3A). The optical absorption reached a maximum after 10 µsec (Figure 3A, inset). In the above reaction system, because of the much higher concentration of K2S2O8 than that of PED A, the primary products of pulse irradiation, H· and eFormula, reacted predominately with K2S2O8, producing secondary oxidative free radical SOFormula (Equations 3 and 4). SOFormula then reacted with PED A to produce phenoxyl radical of PED A formed by Equation (6). The absorption spectrum observed, therefore, should be assigned to phenoxyl radical of PED A.


Figure 3
View larger version (18K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Fig. 3. Transient absorption spectra upon pulse radiolysis of 0.1 mM tested polyphenols aqueous solution containing 20 mM K2S2O8 and 200 mM t-BuOH and saturated with nitrogen at pH 7.0. (A) PED A at 16 µsec; (B) CIS C at 10 µsec; (C) FG at 10 µsec; and (D) HCG at 10 µsec. Inset: trace showing the build-up of optical absorption at (A) 400 nm, (B) 340 nm, (C) 360 nm and (D) 340 nm.

 

Formula (6)

The same results were observed in pulse radiolysis of 0.1 mM CIS C, FG or HCG aqueous solution containing 20 mM K2S2O8 and 200 mM t-BuOH and saturated with nitrogen, with {lambda}max = 360, 360 and 340 nm, respectively (Figure 3B–D).

Repair reactions of oxidative DNA damage by tested polyphenols
At 1 µsec after pulse radiolysis of 4 mM poly C aqueous solution containing 0.04 mM PED A, 40 mM K2S2O8 and 200 mM t-BuOH and saturated with nitrogen at pH 7.0, a transient absorption spectrum was observed (Figure 4A-a). This spectrum was the same as that of the oxidative radical of poly C and, therefore, was assigned to the oxidative radical of poly C. At 20 µsec after the pulse irradiation, the transient absorption spectrum of phenoxyl radical of PED A grew in concomitance with the disappearance of that of the oxidative radical of poly C (Figure 4A-b). This change of transient absorption spectrum indicated that an electron transfer reaction took place between the oxidative radical of poly C and PED A.


Figure 4
View larger version (22K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Fig. 4. Transient absorption spectra upon pulse radiolysis of nitrogen-saturated 4 mM poly C aqueous solution containing 40 mM K2S2O8, 200 mM t-BuOH and tested polyphenols—(A) 0.06 mM PED A: a 0.8 µsec, b 20 µsec; (B) 0.06 mM CIS C: a 0.7 µsec, b 15 µsec; (C) 0.04 mM FG: a 1 µsec, b 15 µsec; (D) 0.08 mM HCG: a 1 µsec, b 15 µsec. Inset: trace showing the build-up of optical absorption at (A) 370 nm, (B) 360 nm, (C) 360 nm and (D) 340 nm.

 
The repair activities of other phenols, CIS C, FG or HCG towards the oxidative radical of poly C, FG or HCG towards ssDNA radical cations as well as CIS C or FG towards dsDNA radical cations also were observed (Figures 4–6).


Figure 5
View larger version (12K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Fig. 5. Transient absorption spectra upon pulse radiolysis of nitrogen-saturated 4 mM ssDNA aqueous solution containing 40 mM K2S2O8, 200 mM t-BuOH and tested polyphenols—(A) 0.06 mM FG: a 2 µsec, b 75 µsec; (B) 0.04 mM HCG: a 0.08 µsec, b 10 µsec. Inset: trace showing the build-up of optical absorption at (A) 360 nm and (B) 340 nm.

 


Figure 6
View larger version (13K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Fig. 6. Transient absorption spectra upon pulse radiolysis of nitrogen-saturated 4 mM dsDNA aqueous solution containing 40 mM K2S2O8, 200 mM t-BuOH and tested polyphenols—(A) 0.04 mM FG: a 0.09 µsec, b 9 µsec; (B) 0.04 mM HCG: a 1 µsec, b 10 µsec. Inset: trace showing the build-up of optical absorption at (A) 360 nm and (B) 340 nm.

 

   Discussion
Top
 Introduction
 Materials and methods
 Results
 Discussion
Funding
 References
 
Both DNA and tested polyphenols can react with SOFormula at high rate constants; hence, there are two parallel reactions in the above repair system in principle. Taking poly C and PED A as examples:

Formula (7)

Formula (8)

However, according to the competitive reaction principle, SOFormula reacts predominately with DNA to form DNA radical cations because of the much higher concentration of DNA than that of PED A.

The reaction of dCMP with SOFormula primarily produces dCMP radical cation (dCMP·+). Being an oxidizing radical itself, dCMP·+ undergoes deprotonation to generate a neutral radical, dCMP(–H)· (40Go). In contrast to the much greater yield of reducing radicals formed in the interaction of dCMP with hydroxyl radicals followed by the process of dehydration, the yield of reducing products formed on interaction of dCMP with SOFormula, is <10%. The situation of poly C and DNA could be assumed to be similar. Therefore, acting as antioxidants, PPGs and their analogues can react with poly C(–H)·

Formula (9)

This is the case in the present study.

It is well known that purine can be oxidized more easily than pyrimidine by oxidants including SOFormula. Therefore, in DNA, SOFormula oxidizes more purine than pyrimidine; hence, the radical cations of DNA are mainly purine-type radical cations and are oxidative. These oxidative radicals may react with reductants, and consequently be repaired as such. Our experimental results consist with this assumption.

The curve of inset in Figure 4A represents the change of absorption of PED A-PhO· at 370 nm with time after the pulse irradiation. The growth of absorbance follows first-order kinetics. The value of the slope is the apparent rate constant (kapp) of generation of PED A-PhO· through reaction of PED A with poly C(–H)·. Varying the concentration of PED A (0.02–0.1 mM), a series of kapp are obtained. The dependence of kapp on [PED A] is a straight line. The slope yields the rate constant (k) for electron transfer from PED A to poly C(–H)· (Figure 7). The rate constants of reaction between tested polyphenols and oxidative radical of poly C, ssDNA and dsDNA radical cation were deduced and are shown in Table I. Jiang's study showed that simpler phenols, hydroxycinnamic acid derivatives, are able to fast repair oxidative OH radical adduct of dGMP with high rate constants (2–3 x 109 dm3/mol·sec) (9Go). Therefore, the repair rate constants towards oxidative DNA damage by tested polyphenols are comparable with that of simpler phenols towards oxidative DNA damage (9Go).


View this table:
[in this window]
[in a new window]

  		Table I. The rate constants for repair reactions of DNA radical cations by PPGs and their analogues

 


Figure 7
View larger version (16K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Fig. 7. The dependencies of the apparent rate constants for the growth of optical absorbance on the concentrations of tested polyphenols upon pulse irradiation of nitrogen-saturated aqueous solution containing 4 mM poly C, ssDNA or dsDNA, 40 mM K2S2O8 and 200 mM t-BuOH.

 
The result of this study in addition to that of our previous studies demonstrates that PPGs and their analogues can fast repair not only oxidative damage of deoxynucleoside and deoxynucleotide but also damage of integral DNA, with the latter being closer to a cellular condition.

There are three principal interaction modes between polyphenol and DNA: (i) intercalation of the drug between two pairs of neighbouring bases, (ii) formation of covalent bonds with bases and (iii) association in the minor groove of DNA double helix. Taking the fast repair being an electron transfer reaction and the geometry of PPGs and their analogues into consideration, the most probable hypothesis corresponding to our case is an association of PPGs and their analogues in the minor groove of DNA double helix. In order to test this hypothesis, we performed the docking calculation using a JUMNA software. The result shows that PPGs and their analogue molecules can dock into the minor groove of DNA and form complexes with a configuration that is suitable for the electron transfers between base radicals of DNA and ligands (PPGs). Such complexes can be formed without major distortion of DNA structure and stabilized further by their interactions with the rhamonsyl side-groups (41Go–43Go).

Phenolic antioxidants can protect DNA from damage by ROS either by scavenging ROS prior to their attacking DNA or by fast repair of damaged DNA caused by free radicals as demonstrated in this work. These two ways complement each other. Our study shows that PPGs and their analogues are also effective hydroxyl radical scavengers, thus can protect DNA from the attack of OH· (32Go,33Go). The result of our present work indicates that PPGs and their analogues, being electron donors, can fast repair radical cations of DNA by electron transfer reaction. However, since the hydroxyl radical is very reactive, its lifespan in a biological system is very short, and it will react at the site close to where it is generated, the protective effect exerted by scavenging hydroxyl radical can only be feasible at places where the concentration of antioxidant is quite high. Therefore, we believe that the protection mode of the tested polyphenols on DNA radicals is preferably a fast repair effect, not a hydroxyl radical-scavenging effect.

Although damaged DNA can be repaired by enzymatic systems, yet the enzymatic repair of DNA damage takes a timescale of hours (44Go). In our present study, the fast repair reaction is initiated and finished in a timescale of microseconds, preventing these transient products from reacting with other biological macromolecules, such as proteins, enzymes and so on. This non-enzymatic repair reaction is very fast, around nine orders faster than enzymatic repair.

A number of endogenous reductants, such as ascorbate and thiols, can react with both dGMP-OH· and dGMP·+ at a high rate (8Go), implicating that a potential or effective repair process exists in the cells. In light of this, one may assume that non-enzymatic fast repair also occurs in cells even though our observation of fast repair reaction was only in chemical systems so far. Based on this assumption, the non-enzymatic fast repair may be restricted to the primary damage, that is DNA radicals, induced by ROS, while the enzymatic repair system may repair steady-state lesions of DNA resulting from DNA radicals. These two repair systems complement each other. A deeper understanding of both repair systems undoubtedly helps researchers find new methods to prevent and/or intervene disease caused by DNA damage.


   Funding
Top
 Introduction
 Materials and methods
 Results
 Discussion
 Funding
References
 
National Natural Science Foundation of China (Project Number: 39270193); E-Institutes of Shanghai Municipal Education Commission (Project Number: E-04010).


   Notes
 
* To whom correspondence should be addressed. Tel: +86 0931 8912563; Email: zhengrl{at}lzu.edu.cn


   References
Top
 Introduction
 Materials and methods
 Results
 Discussion
 Funding
 References
 

    1. Boon PJ, Cullis PM, Symons MCR, Wren BW. Effects of ionizing radiation on deoxyribonucleic acid and related systems. Part 1. The role of oxygen. J. Chem. Soc. Perkin Trans. (1984) 2:1393–1399.

    2. Boon PJ, Cullis PM, Symons MCR, Wren BW. Effects of ionizing radiation on deoxyribonucleic acid and related systems. Part 2. The influence of nitroimidazole drugs on the course of radiation damage to aqueous deoxyribonucleic acid. J. Chem. Soc. Perkin Trans. (1985) 2:1057–1061.

    3. Teoule R. Effects of Ionizing Radiation on DNA—Huttermann J, Kohnlein W, Teoule R, eds. (1978) Berlin: Springer Verlagh. 153, 166, 187.

    4. Wolf P, Jones GDD, Candeias LP, Oneill P. Induction of strand breaks in polyribonucleotides and DNA by the sulphate radical anion—role of electron loss centers as precursors of strand breakage. Int. J. Radiat. Biol. (1993) 64:7–18.[Web of Science][Medline]

    5. Wallance SS. Oxidative damage to DNA and its repair. In: Oxidative Stress and the Molecular Biology of Antioxidant Defenses—Scandalios JG, ed. (1997) Woodbury, NY: Cold Spring Harbor Laboratory Press. 49–90.

    6. Steenken S. Purine bases, nucleosides and nucleotides: aqueous solution redox chemistry and transformation reaction of their radical cations and e– and OH adducts. Chem. Rev. (1989) 89:503–520.[CrossRef][Web of Science]

    7. Simic MG, Bergtold DS, Karam LR. Generation of oxy radicals in biosystems. Mutat. Res. (1989) 214:3–12.[Web of Science][Medline]

    8. O'Neill P. Pulse radiolytic study of the interaction of thiols and ascorbate with OH adducts of dGMP and dG: implications for DNA repair process. Radiat. Res. (1983) 96:198–210.[Web of Science][Medline]

    9. Jiang Y, Yao SD, Lin NY. Fast repair of oxidizing OH radical adduct of dGMP by hydroxycinnamic acid derivatives: a pulse radiolytic study. Radiat. Phys. Chem. (1997) 49:447–450.[CrossRef]

    10. Li WY, Zheng RL, Su BN, Jia ZJ, Li HC, Jiang Y, Yao SD, Lin NY. Repair of dGMP hydroxyl radical adducts by verbascoside via electron transfer: a pulse radiolytic study. Int. J. Radiat. Biol. (1996) 69:481–486.[CrossRef][Web of Science][Medline]

    11. Li WY, Zou ZH, Zheng RL, Jia ZJ, Yao SD, Lin NY. Fast repair of thymine-hydroxyl radical adduct by phenylpropanoid glycosides. Radiat. Phys. Chem. (1997) 49:429–432.[CrossRef]

    12. Shi YM, Wang WF, Shi YP, Jia ZJ, Yao SD, Lin WZ, Han ZH, Zheng RL. Fast repair of dAMP hydroxyl adducts by verbasicoside via electron transfer. Sci. China C (1999) 42:621–627.

    13. Shi YM, Wang WF, Shi YP, Zheng RL, Jia ZJ. Fast repair of dAMP and dGMP hydroxyl adducts by phenylpropanoid glycosides and their analogs. Biochim. Biophys. Acta (1999) 1472:115–127.[Medline]

    14. Li WY, Zheng RL, Jia ZJ, Zou ZH, Lin NY. Repair effect of phenylpropanoid glycosides on thymine radical anion induced by pulse radiolysis. Biophys. Chem. (1997) 67:281–286.[CrossRef][Web of Science][Medline]

    15. Li WY, Zheng RL, Zhao SL, Jiang Y, Lin NY. Repair effect of thymine radical anion by echinocoside using pulse radiolysis. Sci. China C (1996) 39:544–550.

    16. Shi YM, Lin WZ, Kang JH, Zheng RL, Jia ZJ. Fast repair of TMP radical anion by phenylpropanoid glycosides and their analogs. Radiat. Phys. Chem. (2000) 58:131–138.[CrossRef]

    17. Shi YM, Kang JH, Lin WZ, Fan PT, Jia ZJ, Yao SD, Wang WF, Zheng RL. Fast repair of deoxynucleotide radical cations by phenylpropanoid glycosides and their analogs. Biochim. Biophys. Acta (1999) 1472:279–289.[Medline]

    18. Jiangsu New Medical College. The Chinese Medicine Dictionary (1977) Shanghai: Shanghai People's Publishing House. 276, 286, 487, 2674.

    19. Miyase T, Ishion M, Akahori C, Ueno A, Ohkawa Y, Tanizawa H. Phenylethanoid glycosides from Plantago asiatica. Phytochemistry (1991) 30:2015–2018.[CrossRef][Web of Science]

    20. Pan N, Hori H. Antioxidant action of acteoside and its analogs on lipid peroxidation. Redox Rep. (1996) 2:149–154.[Medline]

    21. Pettit GR, Numata A, Takemura T, Ode RH, Narula AS, Schmidt JM, Gragg GM, Pase CP. Antineoplastic agents 107. Isolation of acteoside and isoacteoside from Gastilleja linariaefolia. J. Nat. Prod. (1990) 53:456–458.[CrossRef][Medline]

    22. Mahato SB, Sahu NP, Roy SK, Sharma OP. Potential antitumor agents from Lantana camara: structures of flavonoid-, and phenylpropanoid glycosides. Tetrahedron (1994) 50:9439–9446.[CrossRef][Web of Science]

    23. Kong B, Dustmann JH. The caffeoylics as a new family of natural antiviral compounds. Naturwissensschaften (1991) 72:659–661.

    24. Cano E, Veiga M, Jimenez C, Riguera R. Pharmacological effects of three phenylpropanoid glycosides from Mussatia. Planta Med. (1990) 56:24–26.[CrossRef][Web of Science][Medline]

    25. Jimenez C, Villaverde MC, Riguera R, Castedo L, Stermuz F. Triterpene glycosides from Mussatia species. Phytochemistry (1989) 28:2773–2776.[CrossRef][Web of Science]

    26. Li J, Zheng RL, Liu ZM, Jia ZJ. Scavenging effects of phenylpropanoid glycosides on superoxide and its antioxidation effect. Acta Pharmacol. Sin. (1992) 13:427–430.[Web of Science]

    27. Wang PF, Zheng RL. Inhibition of autooxidation of linoleic acid by phenylpropanoid glycosides from Pedicularis in micelles. Chem. Phys. Lipids (1992) 63:37–40.[CrossRef][Web of Science][Medline]

    28. Li J, Wang PF, Zheng RL, Lui ZM, Jia ZJ. Protection of phenylpropanoid glycosides from Pedicularis against oxidative hemolysis in vitro. Planta Med. (1993) 59:315–317.[CrossRef][Web of Science][Medline]

    29. Li J, Ge RC, Zheng RL, Liu ZM, Jia ZJ. Antioxidative and chelating activities of phenylpropanoid glycosides from Pedicularis striata. Acta Pharmacol. Sin. (1997) 18:77–80.[Web of Science]

    30. Li J, Zheng Y, Zheng RL, Liu ZM, Jia ZJ. Antitumor effects of phenylpropanoid glycosides. Chin. Pharm. J. (1995) 30:269–271.

    31. Li J, Zheng Y, Zhou H, Su BN, Zheng RL. Differentiation of human gastric adenocarcinoma cell line MGc 80-3 induced by verbascoside. Planta Med. (1997) 63:499–502.[CrossRef][Web of Science][Medline]

    32. Wang PF, Zheng RL, Gao JJ, Jia ZJ, Wang WF, Yao SD, Zhang JS, Lin NY. Reaction of hydroxyl radical with phenylpropanoid glycosides from Pedicularis species: a pulse radiolysis study. Sci. China C (1996) 39:154–158.

    33. Shi YM, Wang WF, Kang JH, et al. Reaction of hydroxyl radical with phenylpropanoid glycoside and its derivatives by pulse radiolysis. Sci. China C (1999) 42:420–426.

    34. Pan J, Yuan CS, Lin CJ, Zheng RL. Pharmacological activities and mechanism of natural phenylpropanoid glycosides. Pharmazie (2003) 52:767–777.

    35. Pharmacopoia of P. R. China (1995) Beijing: People's Health Publishing House. 124.

    36. Horacio AP. Minor aristolochic acids from Aristolochia argentina and mass spectral analysis of aristolochic acids. Phytochemistry (1987) 26:519–529.[Web of Science]

    37. Li H, Sakagami Y, Marumo S, Chen XM. Eleven aristolochic acids derivatives from Aristolochia cinnabarina. Phytochemistry (1994) 37:237–239.[CrossRef][Web of Science][Medline]

    38. Yao SD, Sheng SG, Cai JH, Zhang JS. Nanosecond pulse radiolysis studies in China. Radiat. Phys. Chem. (1995) 46:105–113.[CrossRef]

    39. Asmus KD. Sulfur-centered free radicals. In: Radioprotectors and Anticarcinogens—Nygaard OF, Simic MG, eds. (1983) New York: Academic Press. 23–42.

    40. Hazra DK, Steenken S. Pattern of OH radical addition to cytosine and 1-, 3-, 5- and 6-subsitituted cytosine. Electron transfer and dehydration reactions of the OH adducts. J. Am. Chem. Soc. (1983) 105:4380–4386.[CrossRef][Web of Science]

    41. Delalande O, Gao K, Fan BT, Zakrzewska K, El Fassia N, Jia ZJ, Zheng RL, Panaye A, Doucet JP. Docking study of cistanoside C to telomeric DNA fragment. SAR QSAR Environ. Res. (2002) 13:675–688.[CrossRef][Web of Science][Medline]

    42. Sperandio O, Fan BT, Zakrzewska K, Jia ZJ, Zheng RL, Panaye A, Doucet JP, El Fassi N. Theoretical study of fast repair of DNA damage by cistanoside C and analogs: mechanism and docking. SAR QSAR Environ. Res. (2002) 13:243–260.[CrossRef][Web of Science][Medline]

    43. Gao K, Fan BT, El Fassi N, Zakrzewska K, Jia ZJ, Zheng RL, Panaye A, Couesnon T, Doucet JP. Comparative study of activities between verbascoside and rutin by Docking Method. QSAR and Comb. Sci. (2003) 22:18–28.[CrossRef]

    44. Yakes FM, Van Houte B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc. Natl Acad. Sci. USA (1997) 94:514–519.[Abstract/Free Full Text]

Received on April 4, 2007; revised on June 22, 2007; accepted on June 24, 2007.


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?



This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
23/1/19    most recent
gem028v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Shi, Y.
Right arrow Articles by Zheng, R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shi, Y.
Right arrow Articles by Zheng, R.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?