Uptake and Immunomodulatory Properties of Betanin, Vulgaxanthin I and Indicaxanthin towards Caco-2 Intestinal Cells

The present study aimed to compare the absorption and transport patterns of three main betalains, betanin, vulgaxanthin I and indicaxanthin, into intestinal epithelial cells and to assess their distinct molecular effects on inflammatory and redox-related cell signalling in association with their rad...

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Main Authors: Yunqing Wang, Ganwarige Sumali N. Fernando, Natalia N. Sergeeva, Nikolaos Vagkidis, Victor Chechik, Thuy Do, Lisa J. Marshall, Christine Boesch
Format: Article
Language:English
Published: MDPI AG 2022-08-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/11/8/1627
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author Yunqing Wang
Ganwarige Sumali N. Fernando
Natalia N. Sergeeva
Nikolaos Vagkidis
Victor Chechik
Thuy Do
Lisa J. Marshall
Christine Boesch
author_facet Yunqing Wang
Ganwarige Sumali N. Fernando
Natalia N. Sergeeva
Nikolaos Vagkidis
Victor Chechik
Thuy Do
Lisa J. Marshall
Christine Boesch
author_sort Yunqing Wang
collection DOAJ
description The present study aimed to compare the absorption and transport patterns of three main betalains, betanin, vulgaxanthin I and indicaxanthin, into intestinal epithelial cells and to assess their distinct molecular effects on inflammatory and redox-related cell signalling in association with their radial scavenging potencies. All three betalains showed anti-inflammatory effects (5–80 μM), reflected by attenuated transcription of pro-inflammatory mediators such as cyclooxygenase-2 and inducible NO-synthase. Concomitant increases in antioxidant enzymes such as heme oxygenase-1 were only observed for betanin. Moreover, betanin uniquely demonstrated a potent dose-dependent radical scavenging activity in EPR and cell-based assays. Results also indicated overall low permeability for the three betalains with <i>P</i><sub>app</sub> of 4.2–8.9 × 10<sup>−7</sup> cm s<sup>−1</sup>. Higher absorption intensities of vulgaxanthin and indicaxanthin may be attributed to smaller molecular sizes and greater lipophilicity. In conclusion, betanin, vulgaxanthin I and indicaxanthin have differentially contributed to lowering inflammatory markers and mitigating oxidative stress, implying the potential to ameliorate inflammatory intestinal disease. Compared with two betaxanthins, the greater efficacy of betanin in scavenging radical and promoting antioxidant response might, to some extent, compensate for its poorer absorption efficiency, as demonstrated by the Caco-2 cell model.
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spelling doaj.art-8dc083fd43c54367a7491e64ce4245152023-12-03T13:16:20ZengMDPI AGAntioxidants2076-39212022-08-01118162710.3390/antiox11081627Uptake and Immunomodulatory Properties of Betanin, Vulgaxanthin I and Indicaxanthin towards Caco-2 Intestinal CellsYunqing Wang0Ganwarige Sumali N. Fernando1Natalia N. Sergeeva2Nikolaos Vagkidis3Victor Chechik4Thuy Do5Lisa J. Marshall6Christine Boesch7School of Food Science and Nutrition, Faculty of Environment, University of Leeds, Leeds LS2 9JT, UKSchool of Food Science and Nutrition, Faculty of Environment, University of Leeds, Leeds LS2 9JT, UKSchool of Chemistry, Faculty of Engineering and Physical Sciences, University of Leeds, Leeds LS2 9JT, UKDepartment of Chemistry, University of York, York YO10 5DD, UKDepartment of Chemistry, University of York, York YO10 5DD, UKSchool of Dentistry, Faculty of Medicine and Health, University of Leeds, Leeds LS2 9LU, UKSchool of Food Science and Nutrition, Faculty of Environment, University of Leeds, Leeds LS2 9JT, UKSchool of Food Science and Nutrition, Faculty of Environment, University of Leeds, Leeds LS2 9JT, UKThe present study aimed to compare the absorption and transport patterns of three main betalains, betanin, vulgaxanthin I and indicaxanthin, into intestinal epithelial cells and to assess their distinct molecular effects on inflammatory and redox-related cell signalling in association with their radial scavenging potencies. All three betalains showed anti-inflammatory effects (5–80 μM), reflected by attenuated transcription of pro-inflammatory mediators such as cyclooxygenase-2 and inducible NO-synthase. Concomitant increases in antioxidant enzymes such as heme oxygenase-1 were only observed for betanin. Moreover, betanin uniquely demonstrated a potent dose-dependent radical scavenging activity in EPR and cell-based assays. Results also indicated overall low permeability for the three betalains with <i>P</i><sub>app</sub> of 4.2–8.9 × 10<sup>−7</sup> cm s<sup>−1</sup>. Higher absorption intensities of vulgaxanthin and indicaxanthin may be attributed to smaller molecular sizes and greater lipophilicity. In conclusion, betanin, vulgaxanthin I and indicaxanthin have differentially contributed to lowering inflammatory markers and mitigating oxidative stress, implying the potential to ameliorate inflammatory intestinal disease. Compared with two betaxanthins, the greater efficacy of betanin in scavenging radical and promoting antioxidant response might, to some extent, compensate for its poorer absorption efficiency, as demonstrated by the Caco-2 cell model.https://www.mdpi.com/2076-3921/11/8/1627betalainsavailabilityintestinal uptakeinflammationantioxidantCaco-2 cells
spellingShingle Yunqing Wang
Ganwarige Sumali N. Fernando
Natalia N. Sergeeva
Nikolaos Vagkidis
Victor Chechik
Thuy Do
Lisa J. Marshall
Christine Boesch
Uptake and Immunomodulatory Properties of Betanin, Vulgaxanthin I and Indicaxanthin towards Caco-2 Intestinal Cells
Antioxidants
betalains
availability
intestinal uptake
inflammation
antioxidant
Caco-2 cells
title Uptake and Immunomodulatory Properties of Betanin, Vulgaxanthin I and Indicaxanthin towards Caco-2 Intestinal Cells
title_full Uptake and Immunomodulatory Properties of Betanin, Vulgaxanthin I and Indicaxanthin towards Caco-2 Intestinal Cells
title_fullStr Uptake and Immunomodulatory Properties of Betanin, Vulgaxanthin I and Indicaxanthin towards Caco-2 Intestinal Cells
title_full_unstemmed Uptake and Immunomodulatory Properties of Betanin, Vulgaxanthin I and Indicaxanthin towards Caco-2 Intestinal Cells
title_short Uptake and Immunomodulatory Properties of Betanin, Vulgaxanthin I and Indicaxanthin towards Caco-2 Intestinal Cells
title_sort uptake and immunomodulatory properties of betanin vulgaxanthin i and indicaxanthin towards caco 2 intestinal cells
topic betalains
availability
intestinal uptake
inflammation
antioxidant
Caco-2 cells
url https://www.mdpi.com/2076-3921/11/8/1627
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