6 Antioxidant Properties of Singlet Oxygen Suppressors
6.7 Flavonoids as Singlet Oxygen Suppressors
Flavonoids are another family of naturally occurring substances that should be consid-ered in terms of antioxidant and singlet oxy-gen suppression activities. They are important secondary metabolites that protect plants against bacteria and fungi as well as from UV–VIS photo-induced oxidation reac-tions, and continue to be the main target of
research in plant bio-prospection (Veitch and Grayer, 2008; Pedriali et al., 2010). In the past decade, scientists started to become aware of the fact that 1O2 suppression is an important aspect of flavonoid activity. The values of
1O2 rate constants (KQ), physicochemical properties, and molecular structure of flavo-noid, carotenoid and catechin molecules, Trolox (a vitamin-E derivative), ATP, glu-cose, histidine, ascorbic acid and diphenyl-benzofuran (DPBF), are presented in Table 6.2.
β-carotene-5,8-endoperoxide
5,8-dihydroxy-β,β-carotene
β-apo-8-carotenal
β-apo-10-carotenal
β-apo-14-carotenal
β-ionone O
OHHO
O
O O
O O
Fig. 6.16. Structures of some of the 1O2 oxidation products of b-carotenoids.
Antioxidant Properties of Singlet Oxygen Suppressors 81
Table 6.2. Singlet oxygen total quenching rate constants (KQ), HOMO energies and LogP for a series of flavonoids and other antioxidants.
Antioxidant EHOMO (eV)
10−8 KQ (mol.l−1.s−1)
LogP Experimental (theoretical)
b-Carotene 100 (15.5)
Lycopene 200 (15.5)
a-Tocopherol
O
HO 2.0 (11.9)
l-Histidine 0.9 (−1.3)
DPBF O 200 (6.5)
Trolox
O HO
CH3 CH3 CH3
H3C
O OH
−8.90 1.2 2.4 (3.0)
Gallic acid O OH
OH HO OH
−9.32 0.05 (0.9)
Ascorbic acid 11.20 2.0 (−2.4)
Kaempferol
O OH
HO O
OH
OH
−9.04 0.005 2.72 (2.1)
Rutin
O O
OH HO
OH
OH
ORutinoside −9.06 1.2 −2.7 (1.8)
Quercetin
O O
OH HO
OH
OH
OH −9.05 4.6 2.26 (2.1)
Myricetin
O O
OH HO
OH
OH OH
OH
−9.06 5.1 (−0.5)
Fisetin
HO O O
OH
OH OH
−8.99 0.01 2.20 (2.1)
Apigenin
O O
OH HO
OH −9.16 0.28 2.62 (2.1)
Continued
Chlorogenic acid
OH OH OH HO O
OH OH O
O
−9.23 0.022 (−0.4)
Flavone
O
O −9.29 <0.003
Flavonol
O O
OH −8.97 0.053 (1.5)
NaN3 3.0
ATP
O N HO
O P O O–
N N N
NH2
O O– O P O O– O–
O P
0.0004
Glucose
O OH H OH H HO
OH
H H
H
OH 0.0001
Melanin 1.0
Tannic acid 0.22
Catechin
O
OH OH HO
OH
OH 0.11
EGCG
O O OH HO
OH OH
O OH OH OH
OH
1.5
Malvidin
O+
OH HO
OH OH
O
O 5.6
EGCG, epigallocatechin gallate.
Table 6.2. Continued.
Antioxidant EHOMO (eV)
10−8 KQ (mol.l−1.s−1)
LogP Experimental (theoretical)
Antioxidant Properties of Singlet Oxygen Suppressors 83
By using these data, it is possible to draw important conclusions about structure–
activity relationships and the mechanisms of
1O2 (Mukai et al., 2005; Nagai et al., 2005;
Yamaguchi et al., 2005). A quick glance at Table 6.2 shows that carotenoids are clearly the most efficient singlet oxygen suppressors, the efficiency of which is similar to that of DPBF, which is an efficient singlet oxygen probe. All other molecules have non-bonding electron pairs like those found in the azide ion, polyphenols, DNA bases and proteins.
Polyphenols are also good 1O2 suppres-sors. By comparing the value of kQ of myri-cetin (kQ = 5.1 × 108 mol.l−1.s−1) with that of
It seems to be necessary for these molecules to have aryllic O–R groups that carry non-bonding electron pairs that favour com-plexation with singlet oxygen by forming a charge-transfer complex. It therefore seems that the suppression mechanism of flavo-noids is basically due to the process of the reversible electron transfer reaction; how-ever, before reaching that conclusion, one should analyse further the data shown in Table 6.2. We have thus presented data as two figures, in which kQ is plotted as a func-tion of the number of O–R groups (Fig. 6.17) and HOMO energies (Fig. 6.18).
Note that there is a clear relationship between the number of O–R available groups and the value of kQ (Fig. 6.17). However, it is not only the number of O–R groups that mat-ters because sugars have lots of OH groups, but are poor singlet oxygen suppressors (Table 6.2). In fact, one can notice that the energy of the HOMO orbitals is also impor-tant (Fig. 6.18), in agreement with the mech-anism of the electron transfer reaction.
Therefore, a higher HOMO energy allows the formation of a charge transfer complex and reversible electron transfer reaction.
Tannins are an exception to this rule, once they have a large number of O–R groups, and we could expect more efficient singlet oxygen suppression than is observed. We suspect that this low value of kQ of tannins is
due to the formation of aggregates and low availability of the O–H groups that could deactivate singlet oxygen. However, it is important to mention that, besides their low
1O2 suppression constant measured in vitro, tannins have shown expressive protection against singlet oxygen induced damage in DNA, indicating that other factors besides kQ
should be considered in understanding pro-tection against specific oxidative damages.
Another factor that should be consid-ered in terms of the efficiency of singlet oxygen suppression is the partition in the aqueous and organic phases. Rutin and myricetin are good suppressors of singlet oxygen, but present a logP lower than zero (Table 6.2). It means that they should work well in solution but in compartmentalized systems and membranes their protection efficiency should be small. On the other hand, quercetin is an efficient singlet oxy-gen suppressor and has a logP value of 2.26, indicating that it will partition well in mem-branes and therefore have a better potential to protect them from oxidative damage.
Although physical quenching is clearly the most efficient mechanism of interaction between 1O2 and flavonoids, chemical prod-ucts have also been detected indicating that chemical quenching also takes place. 1O2
cannot react by Diels–Alder with benzo-furan; however, it can attack the 2–3 double
9.0 Fig. 6.17. Number of oxygens with a non-bonding electron pair in linear relationship with Log KQ. (Adapted from Mukai et al., 2005 and Nagai et al., 2005.) O–R are chemical groups in which O is bound to an H or alkyl group.
bond of the hydroxyflavanone quercetin (Fig. 6.19a) to afford a depside. This type of reaction may proceed through a hydroper-oxide intermediate, which cyclizes and decomposes with the loss of carbon monox-ide or carbon dioxmonox-ide.
The oxidation of quercetin to the cor-responding depside also occurs in biologi-cal systems. However, the precursors of flavonoids, chalcones, conjugated with car-bonylic groups favour the Diels–Alder reac-tion with this species of oxygen (Fig. 6.19b).
A somewhat related reaction is the oxida-tion of chalcones, which are the biogenetic precursor of aurones. Sensitized photooxy-genation of a chalcone proceeds through dioxetane to yield aurone.
Vitamine E (a-tocopherol and similar compounds) is also a relatively efficient singlet oxygen suppressor (Table 6.2) and is widely used as an antioxidant agent (Huang et al., 2005; Molyneux, 2007;
Nenadis et al., 2007). Trolox, which is a water-soluble derivative of vitamin E, is also used
O O
Fig. 6.19. Mechanism of attack of 1O2 in the flavonoids (a) quercetin and (b) chalcon.
Gallic acid
–9.35 –9.30 –9.25 –9.20 –9.15 –9.10 –9.05–9.00 –8.95 –8.90 6
Fig. 6.18. KQ versus HOMO energy for a series of flavones, flavonols and similar structures.
Antioxidant Properties of Singlet Oxygen Suppressors 85
as an antioxidant and efficiently quenches singlet oxygen. The chemical structure of these molecules as well as the range of their kQ values (1–2 × 108 mol.l−1.s−1) sug-gest that the mechanism of singlet oxygen suppression of this class of molecules is similar to that observed for flavonoids, i.e.
due to a reversible electron transfer reac-tion. Both a-tocopherol and b-carotene are hydrophobic molecules with a high ten-dency to localize in membranes. b-Carotene is, however, a much more efficient 1O2
suppressor, suggesting that it should be more efficient in protecting membranes from damage initiated by 1O2. In fact, Stratton and Liebler have shown that, in concentration conditions similar to those found physiologically, b-carotene was highly effective in protecting against for-mation of oxidation products of membranes and a-tocopherol was ineffective (Stratton and Liebler, 1997).
Several other groups of molecules are also known to suppress 1O2 with high effi-ciency so that they could be considered as antioxidant owing to their 1O2 suppression abilities. Examples can include ascorbic acid, histidine and catechins (Table 6.2).
Betanidines, found in high concentration in beetroot, also seem to hold promising prop-erties to protect against damage resulting from 1O2 (Bonacin et al., 2009).
Carotenoids, which suppress 1O2
through triplet–triplet energy transfer, present kQ values that are around two orders of magnitude larger than those observed for the other groups of molecules cited in Table 6.2. However, it does not mean that one should disregard the 1O2
suppressor abilities of flavonoid deriva-tives and catechins, because these mol-ecules may be present in different concentrations and they certainly have dif-ferent cellular and extracellular localiza-tion domains. In fact, aqueous extracts of plants, namely Andrographis paniculata and Swertia chirata, significantly protect against oxidative damage induced by vari-ous oxidants including 1O2 (Tripathi et al., 2007). The difference in polarities among these groups of molecules suggests possi-ble synergistic roles of carotenoids and
flavonoids. Carotenoids are extremely lipophilic (logP >15) and should either work inside the structure of a membrane protein or inside the membrane itself, whereas most of the flavonoids are hydrophilic and should work in aqueous interfaces or in aqueous solutions.
6.8 Conclusions
Singlet oxygen plays important roles in photo-induced damage in animals and plants, causing damage to human skin and decreasing crop yields. 1O2 is particularly generated by the absorption of UVA–VIS photons by naturally occurring photosen-sitizers, whose triplets react with molecu-lar oxygen. The reactivity of 1O2 with electron-rich double bonds allows it to react with several biomolecules, changing their chemical structure and altering their functions. In terms of the effects in mem-branes, formation of lipid hydroperoxide is the first step in lipid peroxidation that can progress to chain break and loss of mem-brane integrity. Nature has developed a series of chemicals that protect biomol-ecules from the damage caused by 1O2. The main quenchers found in nature suppress
1O2 by physical mechanisms. The fact that all these molecules are well known anti-oxidant agents and that they have high effi-ciency in quenching 1O2 indicates that an important part of their antioxidant activity is due to the suppression of 1O2. Carotenoids are the most efficient 1O2 suppressors and the mechanism of suppression is by triplet–triplet energy transfer. Their main site of localization is hydrophobic envi-ronments, contrary to flavonoids and catechins, which are also efficient 1O2 sup-pressors, whose main quenching mecha-nism is due to reversible electron transfer reactions. The different environments and suppressor mechanisms of these molecules suggest a possible synergistic action of carotenoids, flavonoids and catechins in suppressing 1O2 and helping cells to keep homeostasis under conditions of redox misbalance.
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