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. 2023 Aug 23;12(9):1662.
doi: 10.3390/antiox12091662.

To Prevent Oxidative Stress, What about Protoporphyrin IX, Biliverdin, and Bilirubin?

Ana Martínez  1 , Isabel López-Rull  2 , Juan A Fargallo  3
Affiliations

To Prevent Oxidative Stress, What about Protoporphyrin IX, Biliverdin, and Bilirubin?

Ana Martínez et al. Antioxidants (Basel). .

Abstract

The pigments responsible for eggshell color and patterning in birds are protoporphyrin IX (PP) and biliverdin (BV). Both are involved in the catalytic degradation of the hemo group. Bilirubin (BR), another pigment, is produced when BV is broken down. PP, BV, and BR are free radical scavengers. In this study, we theoretically investigated the antioxidant capacities of these three biological meaningful molecules using Density Functional Theory calculations. First, two antioxidant mechanisms were analyzed for PP, BV, and BR: electron transfer and Hydrogen Atom Transfer. Second, since PP and BV interact with the calcium carbonate matrix of the eggshell, we analyzed the interaction of these pigments with Ca2+ and investigated their chelate compounds. Third, we explored the pro-oxidant properties of PP and BV, which have been proposed for PP when photoactivated to the triplet state, but not for BV. Our results show that PP, BV, and BR are just as good antiradical as other important natural pigments (carotenoids). Neither the antiradical properties of PP and BV nor the UV-visible spectra change due to the presence of calcium, suggesting that the signaling function of these pigments is not affected by the link with Ca2+. Finally, we found that both PP and BV (alone and when linked to Ca2+) can transfer energy from its triplet state to molecular-oxygen-producing singlet oxygen, indicating their pro-oxidant capacity. This investigation answers important questions about the function of these pigments, which may help to understand their influence on the reproductive success of birds.

Keywords: Donor Acceptor Map; microbial defense; oxidative stress; photoactivation; sexual selection.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Schematic representation of BV, PP, and BR.
Figure 2
Figure 2
Electron Donor Acceptor Map (DAM).
Figure 3
Figure 3
DAM of the molecules under study. Carotenoids (in yellow and red) are reported for comparison. The colors indicate the hue of the pigments. Values are in eV. Calculations were conducted in benzene to compare with previous results [34]. All molecules are in ground states (singlets).
Figure 4
Figure 4
Most stable dehydrogenated optimized structures of the molecules under study. The reactive position is indicated in red. The dissociation energy (ΔE) is also reported for comparison with previous results for carotenoids [31]. Calculations are at the M062x/LANL2DZ level.
Figure 5
Figure 5
Most stable BV-Ca and PP-Ca structures. Grey indicates carbon atoms, red is for oxygen atoms, nitrogen atoms are in blue color, green indicates calcium and white is for hydrogen atoms Binding energies are also reported.
Figure 6
Figure 6
DAM of the molecules under study including compounds with Ca2+. Carotenoids (in yellow and red) are reported for comparison. The colors indicate the hue of the pigments. Values in eV.
Figure 7
Figure 7
UV-visible spectra obtained with TDDFT using single-point calculations of the optimized geometries, at the same level of theory in benzene and water, to mimic nonpolar and polar environments.
See this image and copyright information in PMC

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