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Carotenoids are pigments which play a major role in the protection of plants against photooxidative processes. They are efficient antioxidants scavenging singlet molecular oxygen and peroxyl radicals. In the human organism, carotenoids are part of the antioxidant defense system. They interact synergistically with other antioxidants; mixtures of carotenoids are more effective than single compounds. According to their structure most carotenoids exhibit absorption maxima at around 450 nm. Filtering of blue light has been proposed as a mechanism protecting the macula lutea against photooxidative damage. There is increasing evidence from human studies that carotenoids protect the skin against photooxidative damage.
Antioxidant activity of carotenoids
Wilhelm Stahl
, Helmut Sies
Institut f
uur Biochemie und Molekularbiologie I, Heinrich-Heine-Universit
uusseldorf, P.O. Box 101007,
D-40001 Duusseldorf, Germany
Carotenoids are pigments which play a major role in the protection of plants against
photooxidative processes. They are efficient antioxidants scavenging singlet molecular oxygen
and peroxyl radicals. In the human organism, carotenoids are part of the antioxidant defense
system. They interact synergistically with other antioxidants; mixtures of carotenoids are more
effective than single compounds. According to their structure most carotenoids exhibit ab-
sorption maxima at around 450 nm. Filtering of blue light has been proposed as a mechanism
protecting the macula lutea against photooxidative damage. There is increasing evidence from
human studies that carotenoids protect the skin against photooxidative damage.
Ó2003 Elsevier Ltd. All rights reserved.
1. Introduction
Carotenoids are among the most common natural pigments, and more than 600
different compounds have been characterized until now, with b-carotene as the most
prominent (Olson and Krinsky, 1995). Carotenoids are responsible for many of the
red, orange, and yellow hues of plant leaves, fruits, and flowers, as well as the colors
of some birds, insects, fish, and crustaceans. Only plants, bacteria, fungi, and algae
can synthesize carotenoids, but many animals incorporate them from their diet.
Carotenoids serve as antioxidants in animals, and the socalled provitamin A car-
otenoids are used as a source for vitamin A. Carotenoids attracted attention, because
a number of epidemiological studies have revealed that an increased consumption
of a diet rich in carotenoids is correlated with a diminished risk for several degen-
erative disorders, including various types of cancer, cardiovascular or ophthalmo-
logical diseases (Mayne, 1996). The preventive effects have been associated with their
antioxidant activity, protecting cells and tissues from oxidative damage (Sies and
Corresponding author. Tel.: +49-211-811-2711; fax: +49-211-811-3029.
E-mail address: (W. Stahl).
0098-2997/$ - see front matter Ó2003 Elsevier Ltd. All rights reserved.
Molecular Aspects of Medicine 24 (2003) 345–351
Stahl, 1995). Carotenoids also influence cellular signaling and may trigger redox-
sensitive regulatory pathways (Stahl et al., 2002).
2. Structures of carotenoids
The unique structure of carotenoids determines their potential biological func-
tions and actions (Britton, 1995). Most carotenoids can be derived from a 40-carbon
basal structure, which includes a system of conjugated double bonds. The central
chain may carry cyclic end-groups which can be substituted with oxygen-containing
functional groups. Based on their composition, carotenoids are divided in two
classes, carotenes containing only carbon and hydrogen atoms, and oxocarotenoids
(xanthophylls) which carry at least one oxygen atom.
The pattern of conjugated double bonds in the polyene backbone of carotenoids
determines their light absorbing properties and influences the antioxidant activity
of carotenoids. According to the number of double bonds, several cis/trans (E/Z)
configurations are possible for a given molecule. Carotenoids tend to isomerize and
form a mixture of mono- and poly-cis-isomers in addition to the all-trans form.
Generally, the all-trans form is predominant in nature.
Carotenoids are lipophilic molecules which tend to accumulate in lipophilic
compartments like membranes or lipoproteins. The lipophilicity of these compounds
also influences their absorption, transport and excretion in the organism (Stahl et al.,
3. Antioxidant activity––singlet oxygen quenching, peroxyl radical scavenging
As an attribute to aerobic life the human organism is exposed to a variety of
different prooxidants capable to damage biologically relevant molecules, such as
DNA, proteins, carbohydrates, and lipids (Sies, 1986; Halliwell, 1996). Among the
various defense strategies, carotenoids are most likely involved in the scavenging of
two of the reactive oxygen species, singlet molecular oxygen (1O2), and peroxyl
radicals. Further, they are effective deactivators of electronically excited sensitizer
molecules which are involved in the generation of radicals and singlet oxygen
(Truscott, 1990; Young and Lowe, 2001).
The interaction of carotenoids with 1O2depends largely on physical quenching
which involves direct energy transfer between both molecules. The energy of singlet
molecular oxygen is transferred to the carotenoid molecule to yield ground state
oxygen and a triplet excited carotene. Instead of further chemical reactions, the
carotenoid returns to ground state dissipating its energy by interaction with the
surrounding solvent. In contrast to physical quenching, chemical reactions between
the excited oxygen and carotenoids is of minor importance, contributing less than
0.05% to the total quenching rate. Since the carotenoids remain intact during
physical quenching of 1O2or excited sensitizers, they can be reused several fold
in such quenching cycles. Among the various carotenoids, xanthophylls as well as
346 W. Stahl, H. Sies / Molecular Aspects of Medicine 24 (2003) 345–351
carotenes proved to be efficient quenchers of singlet oxygen interacting with reaction
rates that approach diffusion control (Foote and Denny, 1968; Baltschun et al., 1997;
Conn et al., 1991; Di Mascio et al., 1989).
The efficacy of carotenoids for physical quenching is related to the number of
conjugated double bonds present in the molecule which determines their lowest
triplet energy level. b-Carotene and structurally related carotenoids have triplet
energy levels close to that of 1O2enabling energy transfer. In addition to b-carotene,
also zeaxanthin, cryptoxanthin, and a-carotene, all of which are detected in human
serum and tissues, belong to the group of highly active quenchers of 1O2. The most
efficient carotenoid is the open ring carotenoid lycopene, which contributes up to
30% to total carotenoids in humans (Di Mascio et al., 1989).
For clinical use, b-carotene is applied to ameliorate the secondary effects of the
hereditary photosensitivity disorder erythropoietic protoporphyria (Mathews-Roth,
1993). It is suggested that the carotenoid intercepts the reaction sequence that leads
to the formation of singlet oxygen; the latter is thought to be the damaging agent
responsible for the skin lesions observed in this disease.
Among the various radicals which are formed under oxidative conditions in the
organism, carotenoids most efficiently react with peroxyl radicals. They are gener-
ated in the process of lipid peroxidation, and scavenging of this species interrupts the
reaction sequence which finally leads to damage in lipophilic compartments. Due to
their lipophilicity and specific property to scavenge peroxyl radicals, carotenoids are
thought to play an important role in the protection of cellular membranes and
lipoproteins against oxidative damage (Sies and Stahl, 1995). The antioxidant ac-
tivity of carotenoids regarding the deactivation of peroxyl radicals likely depends on
the formation of radical adducts forming a resonance stabilized carbon-centered
A variety of products have been detected subsequent to oxidation of carotenoids,
including carotenoid epoxides and apo-carotenoids of different chain length (Ken-
nedy and Liebler, 1991). It should be noted that these compounds might possess
biological activities and interfere with signaling pathways when present in unphys-
iologically high amounts (Wang and Russell, 1999).
The antioxidant activity of carotenoids depends on the oxygen tension present in
the system (Burton and Ingold, 1984; Palozza, 1998). At low partial pressures of
oxygen such as those found in most tissues under physiological conditions, b-caro-
tene was found to inhibit the oxidation. In contrast, the initial antioxidant activity of
b-carotene is followed by a prooxidant action at high oxygen tension. It has been
suggested that prooxidant effects of b-carotene may be related to adverse effects
observed under the supplementation of high doses of b-carotene.
4. Cooperative effects of carotenoids with other antioxidants
The antioxidant defense system of the organism is a complex network and com-
prises several enzymatic and non-enzymatic antioxidants (Sies, 1993). It has been
suggested that interactions between structurally different compounds with variable
W. Stahl, H. Sies / Molecular Aspects of Medicine 24 (2003) 345–351 347
antioxidant activity provides additional protection against increased oxidative stress.
Vitamin C, for instance, the most powerful water-soluble antioxidant in human
blood plasma, acts as a regenerator for vitamin E in lipid systems (Niki et al., 1995).
b-Carotene might also play a role in such radical transfer chains (Truscott, 1996;
oohm et al., 1997). There is evidence from in vitro studies, that b-carotene regen-
erates tocopherol from the tocopheroxyl radical. The resulting carotenoid radical
cation may subsequently be repaired by vitamin C. Synergistic interactions against
UVA-induced photooxidative stress have been observed in cultured human fibro-
blasts when combinations of antioxidants were applied with b-carotene as main
component (B
oohm et al., 1998a,b). In comparison to the individual antioxidants,
vitamins E, C and b-carotene exhibited cooperative synergistic effects scavenging
reactive nitrogen species (B
oohm et al., 1998a,b). The cooperative interaction between
b-carotene and a-tocopherol was also examined in a membrane model (Palozza and
Krinsky, 1992). A combination of both lipophilic antioxidants resulted in an inhi-
bition of lipid peroxidation significantly greater than the sum of the individual in-
hibitions. Antioxidant activity of carotenoid mixtures was assayed in multilamellar
liposomes, measuring the inhibition of the formation of thiobarbituric acid-reactive
substances (Stahl et al., 1998). Mixtures were more effective than single compounds,
and the synergistic effect was most pronounced when lycopene or lutein was present.
The superior protection of mixtures may be related to specific positioning of different
carotenoids in membranes.
5. Photoprotection in humans
In biological systems, light exposure leads to the formation of reactive oxygen
species which are damaging to biomolecules and affect the integrity and stability of
subcellular structures, cells and tissues (Stahl and Sies, 2001; Krutmann, 2000).
Photooxidative processes play a role in the pathobiochemistry of several diseases of
light-exposed tissues, the eye and the skin.
Age-related macular degeneration is a major cause for irreversible blindness
among the elderly in the Western world and affects the macula lutea (yellow spot) of
the retina, the area of maximal visual acuity (Landrum and Bone, 2001). Lutein and
zeaxanthin are the pigments responsible for coloration of this tissue; other carote-
noids such as lycopene, a-carotene or b-carotene are not found in the macula lutea.
Epidemiological data support the concept that the macular pigment has a protective
role (Beatty et al., 2001). Protection against photooxidative processes has been re-
lated to the antioxidant activities of the macular carotenoids and/or their light fil-
tering effects.
The efficacy of carotenoids to filter blue light was investigated in unilamellar
liposomes (Junghans et al., 2001). Liposomes were loaded in the hydrophilic core
space with a fluorescent dye, excitable by blue light, and various carotenoids were
incorporated into the lipophilic membrane. The fluorescence emission in carotenoid-
containing liposomes was lower than in controls when exposed to blue light, indi-
cating a filter effect. In this model, lutein and zeaxanthin showed a better filtering
348 W. Stahl, H. Sies / Molecular Aspects of Medicine 24 (2003) 345–351
efficacy than b-carotene or lycopene. It was suggested that the more prominent ef-
ficacy of lutein and zeaxanthin is due to differences in the location of the incorpo-
rated molecules within the liposomal membrane. Such differences may also be a
reason why lutein and zeaxanthin can be incorporated into membranes in higher
amounts than other carotenoids like b-carotene or lycopene.
When skin is exposed to UV light, erythema is observed as an initial reaction.
There is evidence from in vitro and in vivo studies that b-carotene prevents photo-
oxidative damage and protects against sunburn (erythema solare) (Stahl and Sies,
2001). When b-carotene was applied alone or in combination with a-tocopherol for
12 weeks, erythema formation induced with a solar light simulator was significantly
diminished from week 8 on (Stahl et al., 2000). Such protective effects were also
achieved with a dietary intervention (Stahl et al., 2001): ingestion of tomato paste,
corresponding to a dose of 16 mg lycopene/day over 10 weeks, led to increases in
serum levels of lycopene and total carotenoids in skin. Erythema formation was
significantly lower in the group that took tomato paste as compared to the control.
Thus, protection against UV-light-induced erythema can be achieved by modulation
of the diet.
6. Conclusion
Carotenoids are efficient antioxidants protecting plants against oxidative damage.
They are also part of the antioxidant defense system in animals and humans. Due to
their unique structure it can be suggested that they possess specific tasks in the anti-
oxidant network such as protecting lipophilic compartments or scavenging reactive
species generated in photooxidative processes. They may further act as light filters
and prevent oxidative stress by diminishing light exposure. The possible role of
carotenoids as prooxidants and the implication of their prooxidant activity in ad-
verse reactions remains to be elucidated.
H.S. is a Fellow of the National Foundation of Cancer Research (NFCR),
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The green microalga Dunaliella salina hyperaccumulates β‐carotene in the chloroplast, which turns its cells orange. This does not occur in the sister species Dunaliella tertiolecta. However, the molecular mechanisms of β‐carotene hyperaccumulation were still unclear. Here, we discovered the reasons for β‐carotene hyperaccumulation by comparing the morphology, physiology, genome, and transcriptome between the carotenogenic D. salina and the noncarotenogenic D. tertiolecta after transfer to high light. The differences in photosynthetic capacity, cell growth, and the concentration of stored carbon suggest that these species regulate the supply and utilization of carbon differently. The number of β‐carotene‐containing plastid lipid globules increased in both species, but much faster and to a greater extent in D. salina than in D. tertiolecta. Consistent with the accumulation of plastid lipid globules, the expression of the methyl‐erythritol‐phosphate and carotenoid biosynthetic pathways increased only in D. salina, which explains the de novo synthesis of β‐carotene. In D. salina, the concomitantly upregulated expression of the carotene globule proteins suggests that hyperaccumulation of β‐carotene also requires a simultaneous increase in its sink capacity. Based on genomic analysis, we propose that D. salina has genetic advantages for routing carbon from growth to carotenoid metabolism.
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Background. In the global textile industry, cotton is a strategic fibre crop. It has a large impact on the industrial and agricultural economies of many countries. Sustainable cotton production is continuously threatened by the unpredictable changes in climate, specifically high temperatures. One of the main goals of contemporary cotton breeding programs is the production of high-yielding, heat-tolerant cotton cultivars with wide adaptation that can be grown throughout warming climate regions. Methods. The current study was designed to explore how heat stress impacts biochemical parameters that control the morpho-physiology of upland cotton. Two heat susceptible (FH-115 and NIAB-Kiran) and two heat tolerant (IUB-13 and GH-Mubarak) accessions were selected to develop filial and backcross generations. Heat tolerant ability of these generations and parental lines was assessed by determining viability of pollen grains, thermostability of cell membrane, levels of antioxidants and reactive oxygen species and yield related traits under both normal and high temperature environments in the field. Genetic control of these traits was assessed through generation mean analysis. Correlation and heterotic studies helped find the relationship among traits and best cross combination, respectively. Results. The data indicated that heat stress negatively impacted every plant attribute analysed. The IUB-13 × FH-115 cross performed best under both normal and high temperatures for yield, biochemical, and physiological attributes. Yield of seed cotton exhibited positive associations with antioxidant levels and pollen viability. Conclusions. The insights derived from this study will aid breeders in identifying traits for selection to develop cotton cultivars that can tolerate the existing challenging environmental conditions.
The effects of vitamin C (ascorbic acid), vitamin E (alpha-tocopherol), and beta-carotene as antioxidants and their cooperative action against the oxidation of lipid in solution, membranes, and lipoproteins have been studied and reviewed. Ascorbic acid and alpha-tocopherol act as potent, and probably the most important, hydrophilic and lipophilic antioxidants, respectively. They function at their own site individually and furthermore act synergistically. beta-Carotene has lower reactivity toward radicals than does alpha-tocopherol and acts as a weak antioxidant in solution. It is more lipophilic than alpha-tocopherol and is assumed to be present at the interior of membranes or lipoproteins, which enables it to scavenge radicals within the lipophilic compartment more efficiently than does alpha-tocopherol. The cooperative interaction between vitamin C and vitamin E may be quite probable, that of vitamin C and beta-carotene is improbable, whereas that between vitamin E and beta-carotene may be possible.
Considerable interest has been shown in the carotenoids for many years due to their wide ranging roles in photochemistry, photobiology and photomedicine and their possible use as a chemopreventative treatment for cancer. Studies about 20 years ago identified the triplet—triplet absorption of β-carotene; this work was of importance in understanding the protective role of these molecules in photosynthesis and bacterial photosynthesis and in porphyric disease treatment. Recently, attention has turned to the very weak fluorescence of these systems using picosecond measurements; results are related to the antenna role of carotenoids in photosynthesis. Photoisomerization continues to be studied with many of the recent developments based on pump-probe measurements using time-resolved resonance Raman spectroscopy for monitoring both the triplet state and the forbidden (1Ag−*) excited singlet state. Interest is also currently centred on the interaction of singlet oxygen with carotenoids; these studies are of value in photophysics (e.g. determination of the carotenoid lowest triplet energy level) and in photomedicine (e.g. evaluation of the use of carotenoids as chemopreventative drugs).
The bimolecular rate constants kq for quenching of singlet oxygen (1Δg state) by 26 different natural and novel synthetic carotenoids were determined at 37 °C in a mixture of chloroform and ethanol. The steady-state technique used involves the generation of 1O2 by thermal decomposition of disodium 3,3′-naphtalene-1,4-diyl-dipropionate endoperoxide (NDPO2) and the detection of its luminescence intensity at 1270 nm. Excitation energies (π,π*, 11Ag → 11Bu) and absorption maxima (430–590 nm) vary in the broadest range. Deeply coloured blue carotenoids are also included in the studies for the first time. An empirical correlation between the π,π* (11Ag → 11Bu) excitation energy and carotenoid structure (effective chain length Neff) was found: E(S) = 12642 cm−1 + 92027 cm−1 × 1/Neff. The quenching ability of the investigated carotenoids depends on the excitation energy of their transition at long wavelengths in a characteristic way showing as limiting factors either the thermal Arrhenius activation or the diffusion-controlled rate. This dependence and the suspected relationship between singlet E(S) and triplet E(T) energies, respectively, are discussed.
As a normal attribute of aerobic life, structural damage to organic compounds of a wide variety (DNA, proteins, carbohydrates and lipids) may occur as a consequence of oxidative reactions. Oxidative damage inflicted by reactive oxygen species has been called “oxidative stress”. Biological systems contain powerful enzymatic and nonenzymatic antioxidant systems, and oxidative stress denotes a shift in the prooxidant/antioxidant balance in favor of the former. Diverse biological processes such as inflammation, carcinogenesis, ageing, radiation damage and photobiological effects appear to involve reactive oxygen species. This field of research provides new perspectives in biochemical pharmacology, toxicology, radiation biochemistry as well as pathophysiology.