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Biologically active polymers from spontaneous carotenoid oxidation: a new frontier in carotenoid activity.

Johnston JB, Nickerson JG, Daroszewski J, Mogg TJ, Burton GW - PLoS ONE (2014)

Bottom Line: Results suggest an overall ability to prime innate immune function to more rapidly respond to subsequent microbial challenges.An underlying structural resemblance to sporopollenin, found in the outer shell of spores and pollen, may allow the polymer to modulate innate immune responses through interactions with the pattern recognition receptor system.Oxygen copolymer formation appears common to all carotenoids, is anticipated to be widespread, and the products may contribute to the health benefits of carotenoid-rich fruits and vegetables.

View Article: PubMed Central - PubMed

Affiliation: National Research Council of Canada, Charlottetown, Prince Edward Island, Canada.

ABSTRACT
In animals carotenoids show biological activity unrelated to vitamin A that has been considered to arise directly from the behavior of the parent compound, particularly as an antioxidant. However, the very property that confers antioxidant activity on some carotenoids in plants also confers susceptibility to oxidative transformation. As an alternative, it has been suggested that carotenoid oxidative breakdown or metabolic products could be the actual agents of activity in animals. However, an important and neglected aspect of the behavior of the highly unsaturated carotenoids is their potential to undergo addition of oxygen to form copolymers. Recently we reported that spontaneous oxidation of ß-carotene transforms it into a product dominated by ß-carotene-oxygen copolymers. We now report that the polymeric product is biologically active. Results suggest an overall ability to prime innate immune function to more rapidly respond to subsequent microbial challenges. An underlying structural resemblance to sporopollenin, found in the outer shell of spores and pollen, may allow the polymer to modulate innate immune responses through interactions with the pattern recognition receptor system. Oxygen copolymer formation appears common to all carotenoids, is anticipated to be widespread, and the products may contribute to the health benefits of carotenoid-rich fruits and vegetables.

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Related in: MedlinePlus

CD14 and TLR-4 staining in gut epithelial cells.Balb/c mice were not supplemented (control) or supplemented daily by oral gavage with OxC-beta (10 mg/kg). After 4 weeks, intestinal tissues were harvested and CD14 and TLR-4 expression was determined by immunocytochemistry. Increased CD14 (A) and TLR-4 (C) expression is readily apparent in epithelial cells in the OxC-beta-supplemented animals compared to the controls receiving vehicle alone (B and D, respectively). Arrows indicate the location of enterocytes within the cross section of microvilli. Magnification 40x.
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pone-0111346-g002: CD14 and TLR-4 staining in gut epithelial cells.Balb/c mice were not supplemented (control) or supplemented daily by oral gavage with OxC-beta (10 mg/kg). After 4 weeks, intestinal tissues were harvested and CD14 and TLR-4 expression was determined by immunocytochemistry. Increased CD14 (A) and TLR-4 (C) expression is readily apparent in epithelial cells in the OxC-beta-supplemented animals compared to the controls receiving vehicle alone (B and D, respectively). Arrows indicate the location of enterocytes within the cross section of microvilli. Magnification 40x.

Mentions: Flow cytometry confirms the earlier PCR assay results [17], showing up-regulation of TLR and CD14 expression. Treatment with OxC-beta increases plasma membrane content of TLRs and CD14 in several cultured cell types, including monocytes, fibroblasts and endothelial cells (Fig. 1). In monocytes OxC-beta (5.0 µM) significantly increases plasma membrane content of both CD14 and TLR-4 (1.7-fold for both), without altering TLR-2 levels (Fig. 1A). The effect on fibroblasts is more pronounced (Fig. 1B). OxC-beta (5.0 µM) induces increases in CD14 and TLR-4 of 3.9 and 3.1-fold, respectively. TLR-2 also increases significantly by 4.6-fold. CD14, TLR-4 and TLR-2 levels also increase significantly in endothelial cells (Fig. 2C): treatment with 5.0 µM OxC-beta produces increases of 3.3, 2.2 and 3.5-fold, respectively. These results indicate that the previously reported PCR gene expression results are reflected at the protein level.


Biologically active polymers from spontaneous carotenoid oxidation: a new frontier in carotenoid activity.

Johnston JB, Nickerson JG, Daroszewski J, Mogg TJ, Burton GW - PLoS ONE (2014)

CD14 and TLR-4 staining in gut epithelial cells.Balb/c mice were not supplemented (control) or supplemented daily by oral gavage with OxC-beta (10 mg/kg). After 4 weeks, intestinal tissues were harvested and CD14 and TLR-4 expression was determined by immunocytochemistry. Increased CD14 (A) and TLR-4 (C) expression is readily apparent in epithelial cells in the OxC-beta-supplemented animals compared to the controls receiving vehicle alone (B and D, respectively). Arrows indicate the location of enterocytes within the cross section of microvilli. Magnification 40x.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4216090&req=5

pone-0111346-g002: CD14 and TLR-4 staining in gut epithelial cells.Balb/c mice were not supplemented (control) or supplemented daily by oral gavage with OxC-beta (10 mg/kg). After 4 weeks, intestinal tissues were harvested and CD14 and TLR-4 expression was determined by immunocytochemistry. Increased CD14 (A) and TLR-4 (C) expression is readily apparent in epithelial cells in the OxC-beta-supplemented animals compared to the controls receiving vehicle alone (B and D, respectively). Arrows indicate the location of enterocytes within the cross section of microvilli. Magnification 40x.
Mentions: Flow cytometry confirms the earlier PCR assay results [17], showing up-regulation of TLR and CD14 expression. Treatment with OxC-beta increases plasma membrane content of TLRs and CD14 in several cultured cell types, including monocytes, fibroblasts and endothelial cells (Fig. 1). In monocytes OxC-beta (5.0 µM) significantly increases plasma membrane content of both CD14 and TLR-4 (1.7-fold for both), without altering TLR-2 levels (Fig. 1A). The effect on fibroblasts is more pronounced (Fig. 1B). OxC-beta (5.0 µM) induces increases in CD14 and TLR-4 of 3.9 and 3.1-fold, respectively. TLR-2 also increases significantly by 4.6-fold. CD14, TLR-4 and TLR-2 levels also increase significantly in endothelial cells (Fig. 2C): treatment with 5.0 µM OxC-beta produces increases of 3.3, 2.2 and 3.5-fold, respectively. These results indicate that the previously reported PCR gene expression results are reflected at the protein level.

Bottom Line: Results suggest an overall ability to prime innate immune function to more rapidly respond to subsequent microbial challenges.An underlying structural resemblance to sporopollenin, found in the outer shell of spores and pollen, may allow the polymer to modulate innate immune responses through interactions with the pattern recognition receptor system.Oxygen copolymer formation appears common to all carotenoids, is anticipated to be widespread, and the products may contribute to the health benefits of carotenoid-rich fruits and vegetables.

View Article: PubMed Central - PubMed

Affiliation: National Research Council of Canada, Charlottetown, Prince Edward Island, Canada.

ABSTRACT
In animals carotenoids show biological activity unrelated to vitamin A that has been considered to arise directly from the behavior of the parent compound, particularly as an antioxidant. However, the very property that confers antioxidant activity on some carotenoids in plants also confers susceptibility to oxidative transformation. As an alternative, it has been suggested that carotenoid oxidative breakdown or metabolic products could be the actual agents of activity in animals. However, an important and neglected aspect of the behavior of the highly unsaturated carotenoids is their potential to undergo addition of oxygen to form copolymers. Recently we reported that spontaneous oxidation of ß-carotene transforms it into a product dominated by ß-carotene-oxygen copolymers. We now report that the polymeric product is biologically active. Results suggest an overall ability to prime innate immune function to more rapidly respond to subsequent microbial challenges. An underlying structural resemblance to sporopollenin, found in the outer shell of spores and pollen, may allow the polymer to modulate innate immune responses through interactions with the pattern recognition receptor system. Oxygen copolymer formation appears common to all carotenoids, is anticipated to be widespread, and the products may contribute to the health benefits of carotenoid-rich fruits and vegetables.

Show MeSH
Related in: MedlinePlus