Lycopene Inhibits the Isomerization of β-Carotene during Quenching of Singlet Oxygen and Free RadicalsJ. Agric. Food Chem.


Thomas Heymann, Philipp Heinz, Marcus A. Glomb
Chemistry (all) / Agricultural and Biological Sciences (all)


Rape in marriage

Lee H. Bowker, o̊Dean of the Graduate School and Research

Max born medal and prize

The Institute of Physics


Lycopene Inhibits the Isomerization of β‑Carotene during Quenching of Singlet Oxygen and Free Radicals

Thomas Heymann, Philipp Heinz, and Marcus A. Glomb*

Food Chemistry, Institute of Chemistry, Martin-Luther-University Halle-Wittenberg, Kurt-Mothes-Strasse 2, 06120 Halle/Saale,

Germany *S Supporting Information

ABSTRACT: The present study aimed to investigate the influence of singlet oxygen and radical species on the isomerization of carotenoids. On the one hand, lycopene and β-carotene standards were incubated with 1,4-dimethylnaphthalene-1,4endoperoxide that produced singlet oxygen in situ. (13Z)- and (15Z)-β-carotene were preferentially generated at low concentrations of singlet oxygen, while high concentrations resulted in formation of (9Z)-β-carotene. The addition of different concentrations of lycopene led to the same isomerization progress of β-carotene, but resulted in a decreased formation of (9Z)-βcarotene and retarded degradation of (all-E)-β-carotene. On the other hand, isomerization of β-carotene and lycopene was induced by ABTS-radicals, too. As expected from the literature, chemical quenching was observed especially for lycopene, while physical quenching was preferred for β-carotene. Mixtures of β-carotene and lycopene resulted in a different isomerization progress compared to the separate β-carotene model. As long as lycopene was present, almost no isomerization of β-carotene was triggered; after that, strong formation of (13Z)-, (9Z)-, and (15Z)-β-carotene was initiated. In summary, lycopene protected βcarotene against isomerization during reactions with singlet oxygen and radicals. These findings can explain the pattern of carotenoid isomers analyzed in fruits and vegetables, where lycopene containing samples showed higher (all-E)/(9Z)-β-carotene ratios, and also in in vivo samples such as human blood plasma.

KEYWORDS: lycopene, β-carotene, singlet oxygen, radicals, isomerization, quenching ■ INTRODUCTION

Carotenoids are well-known as potent antioxidants against reactive species, such as free radicals or singlet oxygen.1,2 The high antioxidative capacity is closely associated with the elongated double bond backbone of these colored structures.

Conn et al. postulated that the ability to quench 1O2 depends on the number of double bonds, which makes lycopene the best singlet oxygen quencher of all natural carotenoids reported at this time.3 However, the antioxidative capacity has not been determined for all known carotenoids, thus there might be even more powerful structures compared to lycopene. In this context, carotenoids were linked to numerous beneficial effects on human health by minimizing oxidative damage, and thus were suggested as a prevention against prostate cancer or cardiovascular diseases.4 Moreover, some carotenoids, such as β-carotene, additionally have provitamin A activities that reflects another important aspect to human health, too.5

In principle, carotenoids can inactivate singlet oxygen or other reactive species through physical or chemical quenching (scavenging). Physical quenching is related to energy transfer reactions, where energy-rich species transfer their energy to the carotenoid molecule to reach an excited state. Subsequently, the carotenoid returns to its ground state by emitting thermal energy or by isomerization processes.6 Chemical quenching or scavenging always includes chemical reactions between carotenoid and oxidative species and results in formation of cleavage products, such as apo-carotenals or carotenoidendoperoxides. According to the literature, interactions between carotenoids and singlet oxygen are dominantly quenched physically, while chemical quenching seems to be just a minor side reaction.1,7 Surprisingly, there are almost no studies on isomerization processes triggered by singlet oxygen whereas a multitude of studies have investigated the formation of oxidative metabolites. Foote et al. already showed in 1970 that (15Z)-β-carotene was transferred to all-E during incubation with singlet oxygen.8 On the one hand, in vitro experiments using carotenoid solutions led to a variety of aldehydes and ketones during treatment with singlet oxygen.6

On the other hand, endoperoxides, epoxides, and lactones were also determined as carotenoid oxidation products.9 Reactions with radicals were reported to lead to a much higher degradation of carotenoids compared to physical quenching mechanisms.1

Only few studies illustrated possible synergistic effects between different antioxidants during quenching reactions; e.g., combinations of α-tocopherol and β-carotene resulted in a significantly stronger inhibition of lipid peroxidation than expected from individual inhibitions.10

Up to now, there has been a lack of knowledge concerning the isomerization process of carotenoids in vivo that could be induced by oxidative stress. Interestingly about 60% of total plasma lycopene was determined as (Z)-isomers (28% (5Z), 12% (13Z)/(15Z), 16% not specified Z),11 while (9Z)-βcarotene just occurred in trace amounts and (13Z) never exceeded 7% of total β-carotene.7 On the one hand, an

Received: January 21, 2015

Revised: March 12, 2015

Accepted: March 14, 2015

Published: March 24, 2015

Article © 2015 American Chemical Society 3279 DOI: 10.1021/acs.jafc.5b00377

J. Agric. Food Chem. 2015, 63, 3279−3287 increased bioavailability of (Z)-lycopenes caused by a better solubility in chylomicrons is often proposed to be the reason for this observation.12 On the other hand, various processes during digestion are hypothesized to trigger the isomerization of lycopene and β-carotene.13 Especially the gastric milieu is considered to be the main reason for the isomerization of carotenoids,14 because a strong formation of (Z)-isomers at gastric pH as well as at elevated physiological temperatures was observed in several studies.13,14 However, this cannot explain the dominant role of (all-E)-β-carotene in human plasma in the presence of only trace amounts of β-carotene isomers. Instead, enzymatic systems that could remove (Z)-isomers were discussed in the literature to form products such as (9Z)retinoic acid.7 Furthermore, the difference in the distribution of (Z)-lycopenes determined in various human tissues cannot be clarified by these hypotheses at all.14