Abstract

Some semi-synthetic flavonoids, particularly derivatives of rutin, are used as therapeutic agents in the treatment of diseases involving free radicals. Here, for the first time, a complete study has been made of the relationship between the structure of such molecules and their superoxide, hydroxyl and peroxyl radical scavenging activity. The molecules chosen for this study were rutin, its aglycone (quercetin), and their methyl ethyl and hydroxyl-ethyl derivatives. Our results are consistent with the general agreement on the structural requirements for free radical scavenging activity. Moreover, we have shown that alkylation of the hydroxyl in position 7 enhanced the scavenging, and also that in a Fenton reaction system, some quercetin derivatives with free catechol moiety or free hydroxyl in position 3 (or both) were pro-oxidant, through superoxide radical and hydrogen peroxide production. Although the structural features needed for pro-oxidant activity are not entirely clear, it appears that to avoid pro-oxidant behaviour, the hydroxyl group in position 3 should be blocked to prevent its auto-oxidation. Thus, flavonoids cannot only be considered purely as antioxidants, since under certain reaction conditions they can also display pro-oxidant activity. This unexpected behaviour could explain, in part, the observed toxicity of some flavonoids in-vivo.

References

Awad
,
H. M.
,
Boersma
,
M. G.
,
Vervoort
,
J.
,
Rietjens
,
I. M. C. M.
(
2000
)
Peroxidase-catalyzed formation of quercetin quinone methide-glutathioneadducts
.
Arch. Biochem. Biophys.
 
378
:
224
233
.

Awad
,
H. M.
,
Boersma
,
M. G.
,
Boeren
,
S.
,
van Bladeren
,
P. J.
,
Vervoort
,
J.
,
Rietjens
,
I. M. C. M.
(
2001
)
Structure-activity study on the quinone/quinone methide chemistry of flavonoids
.
Chem. Res. Toxicol.
 
14
:
398
408
.

Boersma
,
M. G.
,
Vervoort
,
J.
,
Szymusiak
,
H.
,
Lemanska
,
K.
,
Tyrakowska
,
B.
,
Cenas
,
N.
,
Segura-Aguilar
,
J.
,
Rietjens
,
I.
(
2000
)
Regioselectivity and reversibility of glutathione conjugation of quercetin quinone methide
.
Chem. Res. Toxicol.
 
13
:
185
191
.

Bors
,
W.
,
Heller
,
W.
,
Michel
,
C.
,
Saran
,
M.
(
1990
)
Flavonoids as antioxidants: determination of radical-scavenging efficiencies
. In:
Packer
,
L.
,
Glazer
,
A. N.
(eds)
Methods in enzymology.
 
Academic Press
,
San Diego
, pp
343
355
.

Bradford
,
M.
(
1976
)
A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding
.
Anal. Biochem.
 
72
:
248
254
.

Brown
,
S. B.
,
Rajananda
,
V.
,
Holroyd
,
J. A.
,
Evans
,
E. G. V.
(
1982
)
A study of the mechanismof quercetin oxygenationby 18O labelling
.
Biochem. J.
 
205
:
239
244
.

Buxton
,
G. V.
,
Greenstock
,
C. L.
,
Helman
,
W. P.
,
Ross
,
A. B.
(
1988
)
Critical review of rate constants for reactions of hydrated electrons hydrogen atoms and hydroxy1 radicals in aqueous solution
.
J. Phys. Chem. Ref. Data
 
17
:
513
904
.

Canada
,
A. T.
,
Giannella
,
E.
,
Nguyen
,
T. D.
,
Mason
,
R. P.
(
1990
)
The production of reactive oxygen species by dietary flavonols
.
Free Radic. Biol. Med.
 
9
:
441
449
.

Cao
,
G.
,
Sofic
,
E.
,
Prior
,
R.
(
1997
)
Antioxidant and prooxidant behavior of flavonoids: structure-activity relationships
.
Free Radic. Biol. Med.
 
22
:
749
760
.

Chang
,
W.
,
Lee
,
Y.
,
Lu
,
F.
,
Chieng
,
H.
(
1993
)
Inhibitory effects of flavonoids on xanthine oxydase
.
Anticancer Res.
 
13
:
2165
2170
.

Cos
,
P.
,
Ying
,
L.
,
Calomme
,
M.
,
Hu
,
J. P.
,
Cimanga
,
K.
,
van Poel
,
B.
,
Pieters
,
L.
,
Vlietinck
,
A. J.
,
Vanden Berghe
,
D.
(
1998
)
Structure-activity relationship and classification of flavonoids as inhibitors of xanthine oxidase and superoxide scavengers
.
J. Nat. Prod.
 
61
:
71
76
.

Costantino
,
L.
,
Rastelli
,
G.
,
Albasini
,
A.
(
1992
)
Inhibitory activity of flavonols towards the xanthine oxidase enzyme
.
Int. J. Pharmaceutics
 
86
:
17
23
.

Cotelle
,
N.
,
Bernier
,
J. L.
,
Catteau
,
J. P.
,
Pommery
,
J.
,
Wallet
,
J. C.
,
Gaydou
,
E. M.
(
1996
)
Antioxidant properties of hydroxy-flavones
.
Free Radic. Biol. Med.
 
20
:
35
43
.

Courbat
,
P.
,
Albert
,
A.
(
1975
)
Patent: DE 2515084 C2
.

Courbat
,
P.
,
Valenza
,
A.
(
1973
)
Contribution à l'étude de dérivés O-β-hydroxyéthylés de la quercétine
.
Helv. Chim. Acta
 
56
:
1604
1614
.

El-Sukkary
,
M. M. A.
,
Speier
,
G.
(
1981
)
Oxygenation of 3-hydroxy-flavones by superoxide anion
.
J.C.S. Chem. Comm.
:
745
.

Goldstein
,
S.
,
Czapski
,
G.
(
1984
)
Mannitol as an hydroxyl radical scavenger in aqueous solution and biological systems
.
Int. J. Radiat. Biol.
 
46
:
725
729
.

Haenen
,
G. R. M. M.
,
Jansen
,
F. P.
,
Bast
,
A.
(
1993
)
The antioxidant properties of five O-(β-hydroxyethyl)-rutosides of the flavonoid mixture Venoruton
.
Phlebology
 
S1
:
10
17
.

Halliwell
,
B.
,
Gutteridge
,
J. M. C.
(
1999a
)
Reactive species as useful biomolecules
. In:
Free radicals in biology and medicine.
 Third edn,
Oxford University Press Inc.
,
Oxford
, pp
430
484
.

Halliwell
,
B.
,
Gutteridge
,
J. M. C.
(
1999b
)
Freeradicals, other reactive species and disease
. In:
Free radicals in biology andmedicine.
 Third edition,
Oxford University Press Inc.
,
Oxford
, pp
617
783
.

Hanasaki
,
Y.
,
Ogawa
,
S.
,
Fukui
,
S.
(
1994
)
The correlation between active oxygens scavenging and antioxidative effects of flavonoids
.
Free Radic. Biol. Med.
 
16
:
845
850
.

Heitzer
,
T.
,
Schlinzig
,
T.
,
Krohn
,
K.
,
Meinertz
,
T.
,
Münzel
,
T.
(
2001
)
Endothelial dysfunction, oxidative stress, and risk of cardiovascular events in patients with coronary artery disease
.
Circulation
 
104
:
2638
2640
.

Hodnick
,
W. F.
,
Kalyanaraman
,
B.
,
Pritsos
,
C. A.
,
Pardini
,
R. S.
(
1988
)
The production of hydroxyl and semiquinone free radicals during the autoxidation of redox active flavonoids
.
Basic Life Sci.
 
49
:
149
152
.

Hu
,
J. P.
,
Calomme
,
M.
,
La Sure
,
A.
,
De Bruyne
,
T.
,
Pieters
,
L.
,
Vlietinck
,
A.
,
Van den Berghe
,
D. A.
(
1995
)
Structure-activity relationship of flavonoids with superoxide scavenging activity
.
Biol. Trace Elem. Res.
 
47
:
327
331
.

Janssens
,
D.
,
Michiels
,
C.
,
Arnould
,
T.
,
Remacle
,
J.
(
1996
)
Effects of hydroxyethylrutosides on hypoxia-induced activation of human endothelial cells in vitro
.
Br. J. Pharmacol.
 
118
:
599
604
.

Jovanovic
,
S. V.
,
Steenken
,
S.
,
Simic
,
M. G.
,
Hara
,
Y.
(
1998
)
Antioxidant properties of flavonoids: reduction potentials and electron transfer reactions of flavonoid radicals
. In:
Rice-Evans
,
C. A.
,
Packer
,
L.
(eds)
Flavonoids in health and disease.
 
Marcel Dekker
,
New York
, pp
137
163
.

Kachur
,
A. V.
,
Turtle
,
S. W.
,
Biaglow
,
J. E.
(
1998
)
Autoxidation of ferrous ion complexes: a method for the generation of hydroxyl radicals
.
Radiat. Res.
 
150
:
475
482
.

Laughton
,
M. J.
,
Halliwell
,
B.
,
Evans
,
P. J.
,
Hoult
,
J. R. S.
(
1989
)
Antioxidant and pro-oxidant actions of the plant phenolics quercetin gossypol and myricetin
.
Biochem. Pharmacol.
 
38
:
2859
2865
.

Michel
,
C. C.
,
Kendall
,
S.
(
1993
)
β-Hydroxyethyl rutosides reverse the increased permeability induced in frog microvessels by protein-free perfusions
.
Phlebology
(
Suppl. 1
):
18
21
.

Michiels
,
C.
,
Arnould
,
T.
,
Remacle
,
J.
(
1994
)
Rôle clé de l'hypoxie et des cellules endothéliales dans le développement des veines variqueuses
.
Medecine et Science
 
10
:
845
853
.

Miura
,
Y. H.
,
Tomita
,
I.
,
Watanabe
,
T.
,
Hirayama
,
T.
,
Fukui
,
S.
(
1998
)
Active oxygens generation by flavonoids
.
Biol. Pharm. Bull.
 
21
:
93
96
.

Mora
,
A.
,
Payá
,
M.
,
Rios
,
J. L.
,
Alcaraz
,
M. J.
(
1990
)
Structure-activity relationships of polymethoxy flavones and other flavonoids as inhibitors of non-enzymic lipid peroxidation
.
Biochem. Pharmacol.
 
40
:
793
797
.

Picq
,
M.
,
Prigent
,
A. F.
,
Némoz
,
G.
,
André
,
A. C.
,
Pacheco
,
H.
(
1982
)
Penta-substituted quercetin analogues as selective inhibitors of particulate 3′-5′ cyclic AMP phosphodiesterase from rat brain
.
J. Med. Chem.
 
25
:
1192
1198
.

Puppo
,
A.
(
1992
)
Effect of flavonoids on hydroxyl radical formation by Fenton-type reactions; influence of the iron chelator
.
Phytochemistry
 
31
:
85
88
.

Rekka
,
E.
,
Kourounakis
,
P. N.
(
1991
)
Effect of hydroxyethyl rutosides and related compounds on lipid peroxidation and free radical scavenging activity. Some structural aspects
.
J. Pharm. Pharmacol.
 
43
:
486
491
.

Rice-Evans
,
C. A.
,
Miller
,
N. J.
,
Paganga
,
G.
(
1996
)
Structure-antioxidant activity relationships of flavonoids and phenolic acids
.
Free Radic. Biol. Med.
 
20
:
933
956
.

Robak
,
J.
,
Gryglewsky
,
R. J.
(
1988
)
Flavonoids are scavengers of superoxide anions
.
Biochem. Pharmacol.
 
37
:
837
841
.

Saran
,
M.
,
Michel
,
C.
,
Stettmaier
,
K.
,
Bors
,
W.
(
2000
)
Arguments against the significance of the Fenton reaction contributing to signalpathway sunder in vivo conditions
.
Free Rad. Res.
 
33
:
567
579
.

Scheline
,
R. R.
(
1966
)
A rapid synthesis of 3O methylgallic acid
.
Acta Chem. Scand.
 
20
:
1182
.

Sichel
,
G.
,
Corsaro
,
C.
,
Scalia
,
M.
,
Di Bilio
,
A. J.
,
Bonomo
,
R. P.
(
1991
)
In vitro scavenger activity of some flavonoids and melanins against O2
.
Free Radic. Biol. Med.
 
11
:
1
8
.

Takahama
,
U.
(
1987
)
Oxidation products of kaempferol anion radical
.
Plant Cell Physiol.
 
28
:
953
957
.

Tang
,
J.
,
Yuan
,
P.
(
1996
)
Preparation and structure elucidation of Troxerutin
.
Zhongguo Yiyao Gongye Zazhi.
 
27
:
291
292
.

Ubeaud
,
G.
,
Schmitt
,
C.
,
Jaeck
,
D.
,
Lave
,
T.
,
Coassolo
,
P.
(
1995
)
Bosentan a new endothelin receptor antagonist: prediction of systemic plasma clearance in man from combined in vivo and in vitro data
.
Xenobiotica
 
25
:
1381
1390
.

van Acker
,
S. A. B. E.
,
Van den Berg
,
D.
,
Tromp
,
M. N. J. L.
,
Griffioen
,
D. H.
,
van Bennekom
,
W. P.
,
van der Vijgh
,
W. J. F.
,
Bast
,
A.
(
1996
)
Structural aspects of antioxidant activity of flavonoids
.
Free Radic. Biol. Med.
 
20
:
331
342
.

van Acker
,
S. A. B. E.
,
Plemper van Balen
,
G.
,
van der Berg
,
D.
,
Bast
,
A.
,
van der Vijgh
,
W. J. F.
(
1998
)
Influence of iron chelation on the antioxidant activity of flavonoids
.
Biochem. Pharmacol.
 
56
:
935
943
.

van Acker
,
F. A. A.
,
Hageman
,
J. A.
,
Haenen
,
G. R. M. M.
,
van der Vijgh
,
W. J. F.
,
Bast
,
A.
,
Menge
,
W. M. P. B.
(
2000
)
Synthesis of novel 3,7-substituted-2-(3′,4′-dihydroxyphenyl)flavones with improved antioxidant activity
.
J. Med. Chem.
 
43
:
3752
3760
.

Van den Berg
,
R.
,
Haenen
,
G. R. M. M.
,
Van den Berg
,
H.
,
van der Vijgh
,
W.
,
Bast
,
A.
(
2000
)
The predictive value of the antioxidant capacity of structurally related flavonoids using the Trolox equivalent antioxidant capacity (TEAC) assay
.
Food Chem.
 
70
:
391
395
.

Yuting
,
C.
,
Rongliang
,
Z.
,
Zhongjian
,
J.
,
Yong
,
J.
(
1990
)
Flavonoids as superoxide scavengers and antioxidants
.
Free Radic. Biol. Med.
 
9
:
19
21
.

Zhao
,
M. J.
,
Jung
,
L.
(
1995
)
Kinetics of the competitive degradation of deoxyribose and other molecules by hydroxyl radicals produced by the Fenton reaction in the presence of ascorbic acid
.
Free Rad. Res.
 
23
:
229
243
.

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