Fibroblasts upregulate expression of adhesion molecules and promote lymphocyte retention in 3D fibroin/gelatin scaffolds

Bioengineered scaffolds are crucial components in artificial tissue construction. In general, these scaffolds provide inert three-dimensional (3D) surfaces supporting cell growth. However, some scaffolds can affect the phenotype of cultured cells, especially, adherent stromal cells, such as fibrobla...

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Main Authors: Maxim A. Nosenko, Anastasia M. Moysenovich, Anastasia Y. Arkhipova, Kamar-Sulu N. Atretkhany, Sergei A. Nedospasov, Marina S. Drutskaya, Mikhail M. Moisenovich
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2021-10-01
Series:Bioactive Materials
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Online Access:http://www.sciencedirect.com/science/article/pii/S2452199X21001249
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author Maxim A. Nosenko
Anastasia M. Moysenovich
Anastasia Y. Arkhipova
Kamar-Sulu N. Atretkhany
Sergei A. Nedospasov
Marina S. Drutskaya
Mikhail M. Moisenovich
author_facet Maxim A. Nosenko
Anastasia M. Moysenovich
Anastasia Y. Arkhipova
Kamar-Sulu N. Atretkhany
Sergei A. Nedospasov
Marina S. Drutskaya
Mikhail M. Moisenovich
author_sort Maxim A. Nosenko
collection DOAJ
description Bioengineered scaffolds are crucial components in artificial tissue construction. In general, these scaffolds provide inert three-dimensional (3D) surfaces supporting cell growth. However, some scaffolds can affect the phenotype of cultured cells, especially, adherent stromal cells, such as fibroblasts. Here we report on unique properties of 3D fibroin/gelatin materials, which may rapidly induce expression of adhesion molecules, such as ICAM-1 and VCAM-1, in cultured primary murine embryonic fibroblasts (MEFs). In contrast, two-dimensional (2D) fibroin/gelatin films did not show significant effects on gene expression profiles in fibroblasts as compared to 3D culture conditions. Interestingly, TNF expression was induced in MEFs cultured in 3D fibroin/gelatin scaffolds, while genetic or pharmacological TNF ablation resulted in diminished ICAM-1 and VCAM-1 expression by these cells. Using selective MAPK inhibitors, we uncovered critical contribution of JNK to 3D-induced upregulation of these adhesion molecules. Moreover, we observed ICAM-1/VCAM-1-dependent adhesion of lymphocytes to fibroblasts cultured in 3D fibroin/gelatin scaffolds, but not on 2D fibroin/gelatin films, suggesting functional reprogramming in stromal cells, when exposed to 3D environment. Finally, we observed significant infiltration of lymphocytes into 3D fibroin/gelatin, but not into collagen scaffolds in vivo upon subcapsular kidney implantation in mice. Together our data highlight the important features of fibroin/gelatin scaffolds, when they are produced as 3D sponges rather than 2D films, which should be considered when using these materials for tissue engineering.
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spelling doaj.art-5ac0732d43bc4ca3bb9757f6fd7a9e762024-04-16T19:03:17ZengKeAi Communications Co., Ltd.Bioactive Materials2452-199X2021-10-0161034493460Fibroblasts upregulate expression of adhesion molecules and promote lymphocyte retention in 3D fibroin/gelatin scaffoldsMaxim A. Nosenko0Anastasia M. Moysenovich1Anastasia Y. Arkhipova2Kamar-Sulu N. Atretkhany3Sergei A. Nedospasov4Marina S. Drutskaya5Mikhail M. Moisenovich6Center for Precision Genome Editing and Genetic Technologies for Biomedicine, Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, 119991, Russia; Corresponding author.Biological Faculty, Lomonosov Moscow State University, Moscow, 119991, RussiaBiological Faculty, Lomonosov Moscow State University, Moscow, 119991, Russia; Biological Faculty, Shenzhen MSU-BIT University, Shenzhen, 518172, ChinaCenter for Precision Genome Editing and Genetic Technologies for Biomedicine, Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, 119991, RussiaCenter for Precision Genome Editing and Genetic Technologies for Biomedicine, Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, 119991, Russia; Biological Faculty, Lomonosov Moscow State University, Moscow, 119991, Russia; Sirius University of Science and Technology, Federal Territory Sirius, Krasnodarsky Krai, 354340, RussiaCenter for Precision Genome Editing and Genetic Technologies for Biomedicine, Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, 119991, RussiaBiological Faculty, Lomonosov Moscow State University, Moscow, 119991, RussiaBioengineered scaffolds are crucial components in artificial tissue construction. In general, these scaffolds provide inert three-dimensional (3D) surfaces supporting cell growth. However, some scaffolds can affect the phenotype of cultured cells, especially, adherent stromal cells, such as fibroblasts. Here we report on unique properties of 3D fibroin/gelatin materials, which may rapidly induce expression of adhesion molecules, such as ICAM-1 and VCAM-1, in cultured primary murine embryonic fibroblasts (MEFs). In contrast, two-dimensional (2D) fibroin/gelatin films did not show significant effects on gene expression profiles in fibroblasts as compared to 3D culture conditions. Interestingly, TNF expression was induced in MEFs cultured in 3D fibroin/gelatin scaffolds, while genetic or pharmacological TNF ablation resulted in diminished ICAM-1 and VCAM-1 expression by these cells. Using selective MAPK inhibitors, we uncovered critical contribution of JNK to 3D-induced upregulation of these adhesion molecules. Moreover, we observed ICAM-1/VCAM-1-dependent adhesion of lymphocytes to fibroblasts cultured in 3D fibroin/gelatin scaffolds, but not on 2D fibroin/gelatin films, suggesting functional reprogramming in stromal cells, when exposed to 3D environment. Finally, we observed significant infiltration of lymphocytes into 3D fibroin/gelatin, but not into collagen scaffolds in vivo upon subcapsular kidney implantation in mice. Together our data highlight the important features of fibroin/gelatin scaffolds, when they are produced as 3D sponges rather than 2D films, which should be considered when using these materials for tissue engineering.http://www.sciencedirect.com/science/article/pii/S2452199X21001249BioengineeringCell adhesionArtificial lymphoid tissueMouse embryonic fibroblastsStromal cellsTNF
spellingShingle Maxim A. Nosenko
Anastasia M. Moysenovich
Anastasia Y. Arkhipova
Kamar-Sulu N. Atretkhany
Sergei A. Nedospasov
Marina S. Drutskaya
Mikhail M. Moisenovich
Fibroblasts upregulate expression of adhesion molecules and promote lymphocyte retention in 3D fibroin/gelatin scaffolds
Bioactive Materials
Bioengineering
Cell adhesion
Artificial lymphoid tissue
Mouse embryonic fibroblasts
Stromal cells
TNF
title Fibroblasts upregulate expression of adhesion molecules and promote lymphocyte retention in 3D fibroin/gelatin scaffolds
title_full Fibroblasts upregulate expression of adhesion molecules and promote lymphocyte retention in 3D fibroin/gelatin scaffolds
title_fullStr Fibroblasts upregulate expression of adhesion molecules and promote lymphocyte retention in 3D fibroin/gelatin scaffolds
title_full_unstemmed Fibroblasts upregulate expression of adhesion molecules and promote lymphocyte retention in 3D fibroin/gelatin scaffolds
title_short Fibroblasts upregulate expression of adhesion molecules and promote lymphocyte retention in 3D fibroin/gelatin scaffolds
title_sort fibroblasts upregulate expression of adhesion molecules and promote lymphocyte retention in 3d fibroin gelatin scaffolds
topic Bioengineering
Cell adhesion
Artificial lymphoid tissue
Mouse embryonic fibroblasts
Stromal cells
TNF
url http://www.sciencedirect.com/science/article/pii/S2452199X21001249
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