Pro-Inflammatory Effect of Gliadins and Glutenins Extracted from Different Wheat Cultivars on an In Vitro 3D Intestinal Epithelium Model

There is a need to assess the relationship between improved rheological properties and the immunogenic potential of wheat proteins. The present study aimed to investigate the in vitro effects of total protein extracts from three modern and two landrace <i>Triticum aestivum</i> commercial...

Full description

Bibliographic Details
Main Authors: Francesca Truzzi, Camilla Tibaldi, Anne Whittaker, Silvia Dilloo, Enzo Spisni, Giovanni Dinelli
Format: Article
Language:English
Published: MDPI AG 2020-12-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/22/1/172
_version_ 1797543426855534592
author Francesca Truzzi
Camilla Tibaldi
Anne Whittaker
Silvia Dilloo
Enzo Spisni
Giovanni Dinelli
author_facet Francesca Truzzi
Camilla Tibaldi
Anne Whittaker
Silvia Dilloo
Enzo Spisni
Giovanni Dinelli
author_sort Francesca Truzzi
collection DOAJ
description There is a need to assess the relationship between improved rheological properties and the immunogenic potential of wheat proteins. The present study aimed to investigate the in vitro effects of total protein extracts from three modern and two landrace <i>Triticum aestivum</i> commercial flour mixes, with significant differences in gluten strength (GS), on cell lines. Cytotoxicity and innate immune responses induced by wheat proteins were investigated using Caco-2 monocultures, two dimensional (2D) Caco-2/U937 co-cultures, and three dimensional (3D) co-cultures simulating the intestinal mucosa with Caco-2 epithelial cells situated above an extra-cellular matrix containing U937 monocytes and L929 fibroblasts. Modern wheat proteins, with increased GS, significantly reduced Caco-2 cell proliferation and vitality in monoculture and 2D co-cultures than landrace proteins. Modern wheat proteins also augmented Caco-2 monolayer disruption and tight junction protein, occludin, redistribution in 3D co-cultures. Release of interleukin-8 into the cell medium and increased U937 monocyte migration in both 2D and 3D co-cultures were similarly apparent. Immuno-activation of migrating U937 cells was evidenced from cluster of differentiation 14 (CD14) staining and CD11b-related differentiation into macrophages. The modern wheat proteins, with gluten polymorphism relatedness and increased GS, were shown to be more cytotoxic and immunogenic than the landrace wheat proteins.
first_indexed 2024-03-10T13:45:24Z
format Article
id doaj.art-4e0afe2d88314b4380489ec3de2a6a4b
institution Directory Open Access Journal
issn 1661-6596
1422-0067
language English
last_indexed 2024-03-10T13:45:24Z
publishDate 2020-12-01
publisher MDPI AG
record_format Article
series International Journal of Molecular Sciences
spelling doaj.art-4e0afe2d88314b4380489ec3de2a6a4b2023-11-21T02:39:55ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-12-0122117210.3390/ijms22010172Pro-Inflammatory Effect of Gliadins and Glutenins Extracted from Different Wheat Cultivars on an In Vitro 3D Intestinal Epithelium ModelFrancesca Truzzi0Camilla Tibaldi1Anne Whittaker2Silvia Dilloo3Enzo Spisni4Giovanni Dinelli5Department of Agricultural and Food Sciences, Alma Mater Studiorum–University of Bologna, 40127 Bologna, ItalyDepartment of Agricultural and Food Sciences, Alma Mater Studiorum–University of Bologna, 40127 Bologna, ItalyDepartment of Agricultural and Food Sciences, Alma Mater Studiorum–University of Bologna, 40127 Bologna, ItalyDepartment of Agricultural and Food Sciences, Alma Mater Studiorum–University of Bologna, 40127 Bologna, ItalyDepartment of Biological, Geological, and Environmental Sciences, Alma Mater Studiorum–University of Bologna, 40126 Bologna, ItalyDepartment of Agricultural and Food Sciences, Alma Mater Studiorum–University of Bologna, 40127 Bologna, ItalyThere is a need to assess the relationship between improved rheological properties and the immunogenic potential of wheat proteins. The present study aimed to investigate the in vitro effects of total protein extracts from three modern and two landrace <i>Triticum aestivum</i> commercial flour mixes, with significant differences in gluten strength (GS), on cell lines. Cytotoxicity and innate immune responses induced by wheat proteins were investigated using Caco-2 monocultures, two dimensional (2D) Caco-2/U937 co-cultures, and three dimensional (3D) co-cultures simulating the intestinal mucosa with Caco-2 epithelial cells situated above an extra-cellular matrix containing U937 monocytes and L929 fibroblasts. Modern wheat proteins, with increased GS, significantly reduced Caco-2 cell proliferation and vitality in monoculture and 2D co-cultures than landrace proteins. Modern wheat proteins also augmented Caco-2 monolayer disruption and tight junction protein, occludin, redistribution in 3D co-cultures. Release of interleukin-8 into the cell medium and increased U937 monocyte migration in both 2D and 3D co-cultures were similarly apparent. Immuno-activation of migrating U937 cells was evidenced from cluster of differentiation 14 (CD14) staining and CD11b-related differentiation into macrophages. The modern wheat proteins, with gluten polymorphism relatedness and increased GS, were shown to be more cytotoxic and immunogenic than the landrace wheat proteins.https://www.mdpi.com/1422-0067/22/1/172<i>Triticum aestivum</i>modern and old genotypestotal proteinsgluten strengthinnate immunitycytotoxicity
spellingShingle Francesca Truzzi
Camilla Tibaldi
Anne Whittaker
Silvia Dilloo
Enzo Spisni
Giovanni Dinelli
Pro-Inflammatory Effect of Gliadins and Glutenins Extracted from Different Wheat Cultivars on an In Vitro 3D Intestinal Epithelium Model
International Journal of Molecular Sciences
<i>Triticum aestivum</i>
modern and old genotypes
total proteins
gluten strength
innate immunity
cytotoxicity
title Pro-Inflammatory Effect of Gliadins and Glutenins Extracted from Different Wheat Cultivars on an In Vitro 3D Intestinal Epithelium Model
title_full Pro-Inflammatory Effect of Gliadins and Glutenins Extracted from Different Wheat Cultivars on an In Vitro 3D Intestinal Epithelium Model
title_fullStr Pro-Inflammatory Effect of Gliadins and Glutenins Extracted from Different Wheat Cultivars on an In Vitro 3D Intestinal Epithelium Model
title_full_unstemmed Pro-Inflammatory Effect of Gliadins and Glutenins Extracted from Different Wheat Cultivars on an In Vitro 3D Intestinal Epithelium Model
title_short Pro-Inflammatory Effect of Gliadins and Glutenins Extracted from Different Wheat Cultivars on an In Vitro 3D Intestinal Epithelium Model
title_sort pro inflammatory effect of gliadins and glutenins extracted from different wheat cultivars on an in vitro 3d intestinal epithelium model
topic <i>Triticum aestivum</i>
modern and old genotypes
total proteins
gluten strength
innate immunity
cytotoxicity
url https://www.mdpi.com/1422-0067/22/1/172
work_keys_str_mv AT francescatruzzi proinflammatoryeffectofgliadinsandgluteninsextractedfromdifferentwheatcultivarsonaninvitro3dintestinalepitheliummodel
AT camillatibaldi proinflammatoryeffectofgliadinsandgluteninsextractedfromdifferentwheatcultivarsonaninvitro3dintestinalepitheliummodel
AT annewhittaker proinflammatoryeffectofgliadinsandgluteninsextractedfromdifferentwheatcultivarsonaninvitro3dintestinalepitheliummodel
AT silviadilloo proinflammatoryeffectofgliadinsandgluteninsextractedfromdifferentwheatcultivarsonaninvitro3dintestinalepitheliummodel
AT enzospisni proinflammatoryeffectofgliadinsandgluteninsextractedfromdifferentwheatcultivarsonaninvitro3dintestinalepitheliummodel
AT giovannidinelli proinflammatoryeffectofgliadinsandgluteninsextractedfromdifferentwheatcultivarsonaninvitro3dintestinalepitheliummodel