Bioavailability and provitamin A activity of neurosporaxanthin in mice

Abstract Various species of ascomycete fungi synthesize the carboxylic carotenoid neurosporaxanthin. The unique chemical structure of this xanthophyll reveals that: (1) Its carboxylic end and shorter length increase the polarity of neurosporaxanthin in comparison to other carotenoids, and (2) it con...

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Main Authors: Anthony P. Miller, Dámaso Hornero-Méndez, Sepalika Bandara, Obdulia Parra-Rivero, M. Carmen Limón, Johannes von Lintig, Javier Avalos, Jaume Amengual
Format: Article
Language:English
Published: Nature Portfolio 2023-10-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-023-05446-1
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author Anthony P. Miller
Dámaso Hornero-Méndez
Sepalika Bandara
Obdulia Parra-Rivero
M. Carmen Limón
Johannes von Lintig
Javier Avalos
Jaume Amengual
author_facet Anthony P. Miller
Dámaso Hornero-Méndez
Sepalika Bandara
Obdulia Parra-Rivero
M. Carmen Limón
Johannes von Lintig
Javier Avalos
Jaume Amengual
author_sort Anthony P. Miller
collection DOAJ
description Abstract Various species of ascomycete fungi synthesize the carboxylic carotenoid neurosporaxanthin. The unique chemical structure of this xanthophyll reveals that: (1) Its carboxylic end and shorter length increase the polarity of neurosporaxanthin in comparison to other carotenoids, and (2) it contains an unsubstituted β-ionone ring, conferring the potential to form vitamin A. Previously, neurosporaxanthin production was optimized in Fusarium fujikuroi, which allowed us to characterize its antioxidant properties in in vitro assays. In this study, we assessed the bioavailability of neurosporaxanthin compared to other provitamin A carotenoids in mice and examined whether it can be cleaved by the two carotenoid-cleaving enzymes: β-carotene-oxygenase 1 (BCO1) and 2 (BCO2). Using Bco1 −/− Bco2 −/− mice, we report that neurosporaxanthin displays greater bioavailability than β-carotene and β-cryptoxanthin, as evidenced by higher accumulation and decreased fecal elimination. Enzymatic assays with purified BCO1 and BCO2, together with feeding studies in wild-type, Bco1 −/− , Bco2 −/− , and Bco1 −/− Bco2 −/− mice, revealed that neurosporaxanthin is a substrate for either carotenoid-cleaving enzyme. Wild-type mice fed neurosporaxanthin displayed comparable amounts of vitamin A to those fed β-carotene. Together, our study unveils neurosporaxanthin as a highly bioavailable fungal carotenoid with provitamin A activity, highlighting its potential as a novel food additive.
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spelling doaj.art-e316ef235a0c4bf592f67e52d34fdd182023-11-20T10:36:15ZengNature PortfolioCommunications Biology2399-36422023-10-016111110.1038/s42003-023-05446-1Bioavailability and provitamin A activity of neurosporaxanthin in miceAnthony P. Miller0Dámaso Hornero-Méndez1Sepalika Bandara2Obdulia Parra-Rivero3M. Carmen Limón4Johannes von Lintig5Javier Avalos6Jaume Amengual7Department of Food Science and Human Nutrition, University of Illinois at Urbana-ChampaignDepartment of Food Phytochemistry, Instituto de la Grasa, CSICDepartment of Pharmacology, School of Medicine, Case Western Reserve UniversityDepartment of Genetics, Faculty of Biology, University of SevilleDepartment of Genetics, Faculty of Biology, University of SevilleDepartment of Pharmacology, School of Medicine, Case Western Reserve UniversityDepartment of Genetics, Faculty of Biology, University of SevilleDepartment of Food Science and Human Nutrition, University of Illinois at Urbana-ChampaignAbstract Various species of ascomycete fungi synthesize the carboxylic carotenoid neurosporaxanthin. The unique chemical structure of this xanthophyll reveals that: (1) Its carboxylic end and shorter length increase the polarity of neurosporaxanthin in comparison to other carotenoids, and (2) it contains an unsubstituted β-ionone ring, conferring the potential to form vitamin A. Previously, neurosporaxanthin production was optimized in Fusarium fujikuroi, which allowed us to characterize its antioxidant properties in in vitro assays. In this study, we assessed the bioavailability of neurosporaxanthin compared to other provitamin A carotenoids in mice and examined whether it can be cleaved by the two carotenoid-cleaving enzymes: β-carotene-oxygenase 1 (BCO1) and 2 (BCO2). Using Bco1 −/− Bco2 −/− mice, we report that neurosporaxanthin displays greater bioavailability than β-carotene and β-cryptoxanthin, as evidenced by higher accumulation and decreased fecal elimination. Enzymatic assays with purified BCO1 and BCO2, together with feeding studies in wild-type, Bco1 −/− , Bco2 −/− , and Bco1 −/− Bco2 −/− mice, revealed that neurosporaxanthin is a substrate for either carotenoid-cleaving enzyme. Wild-type mice fed neurosporaxanthin displayed comparable amounts of vitamin A to those fed β-carotene. Together, our study unveils neurosporaxanthin as a highly bioavailable fungal carotenoid with provitamin A activity, highlighting its potential as a novel food additive.https://doi.org/10.1038/s42003-023-05446-1
spellingShingle Anthony P. Miller
Dámaso Hornero-Méndez
Sepalika Bandara
Obdulia Parra-Rivero
M. Carmen Limón
Johannes von Lintig
Javier Avalos
Jaume Amengual
Bioavailability and provitamin A activity of neurosporaxanthin in mice
Communications Biology
title Bioavailability and provitamin A activity of neurosporaxanthin in mice
title_full Bioavailability and provitamin A activity of neurosporaxanthin in mice
title_fullStr Bioavailability and provitamin A activity of neurosporaxanthin in mice
title_full_unstemmed Bioavailability and provitamin A activity of neurosporaxanthin in mice
title_short Bioavailability and provitamin A activity of neurosporaxanthin in mice
title_sort bioavailability and provitamin a activity of neurosporaxanthin in mice
url https://doi.org/10.1038/s42003-023-05446-1
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