Label-Free Infrared Spectral Histology of Skin Tissue Part I: Impact of Lumican on Extracellular Matrix Integrity

Proteoglycans (PG) play an important role in maintaining the extracellular matrix (ECM) integrity. Lumican, a small leucine rich PG, is one such actor capable of regulating such properties. In this study, the integrity of the dermis of lumican-deleted Lum–/– vs. wild-type mice was investigated by co...

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Main Authors: Lise Nannan, Valérie Untereiner, Isabelle Proult, Camille Boulagnon-Rombi, Charlie Colin-Pierre, Ganesh D. Sockalingum, Stéphane Brézillon
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fcell.2020.00320/full
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spelling doaj-705a3fe75921405c901d753f161d554a2020-11-25T03:02:48ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2020-05-01810.3389/fcell.2020.00320527194Label-Free Infrared Spectral Histology of Skin Tissue Part I: Impact of Lumican on Extracellular Matrix IntegrityLise Nannan0Lise Nannan1Valérie Untereiner2Isabelle Proult3Isabelle Proult4Camille Boulagnon-Rombi5Camille Boulagnon-Rombi6Camille Boulagnon-Rombi7Charlie Colin-Pierre8Charlie Colin-Pierre9Charlie Colin-Pierre10Ganesh D. Sockalingum11Stéphane Brézillon12Stéphane Brézillon13Université de Reims Champagne-Ardenne, Laboratoire de Biochimie Médicale et Biologie Moléculaire, Reims, FranceCNRS UMR 7369, Matrice Extracellulaire et Dynamique Cellulaire, Reims, FranceUniversité de Reims Champagne-Ardenne, Cellular and Tissue Imaging Platform, Reims, FranceUniversité de Reims Champagne-Ardenne, Laboratoire de Biochimie Médicale et Biologie Moléculaire, Reims, FranceCNRS UMR 7369, Matrice Extracellulaire et Dynamique Cellulaire, Reims, FranceUniversité de Reims Champagne-Ardenne, Laboratoire de Biochimie Médicale et Biologie Moléculaire, Reims, FranceCNRS UMR 7369, Matrice Extracellulaire et Dynamique Cellulaire, Reims, FranceLaboratoire de Pathologie, Centre Hospitalier Universitaire de Reims, Reims, FranceUniversité de Reims Champagne-Ardenne, Laboratoire de Biochimie Médicale et Biologie Moléculaire, Reims, FranceCNRS UMR 7369, Matrice Extracellulaire et Dynamique Cellulaire, Reims, FranceBASF Beauty Care Solutions France SAS, Pulnoy, FranceUniversité de Reims Champagne-Ardenne, BioSpecT-BioSpectroscopie Translationnelle, EA7506, UFR de Pharmacie, Reims, FranceUniversité de Reims Champagne-Ardenne, Laboratoire de Biochimie Médicale et Biologie Moléculaire, Reims, FranceCNRS UMR 7369, Matrice Extracellulaire et Dynamique Cellulaire, Reims, FranceProteoglycans (PG) play an important role in maintaining the extracellular matrix (ECM) integrity. Lumican, a small leucine rich PG, is one such actor capable of regulating such properties. In this study, the integrity of the dermis of lumican-deleted Lum–/– vs. wild-type mice was investigated by conventional histology and by infrared spectral histology (IRSH). Infrared spectroscopy is a non-invasive, rapid, label-free and sensitive technique that allows to probe molecular vibrations of biomolecules present in a tissue. Our IRSH results obtained on control (WT, n = 3) and Lum–/– (n = 3) mice showed that different histological structures were identified by using K-means clustering and validated by hematoxylin eosin saffron (HES) staining. Furthermore, an important increase of the dermis thickness was observed in Lum–/– compared to WT mice. In terms of structural information, analysis of the spectral images also revealed an intra-group homogeneity and inter-group heterogeneity. In addition, type I collagen contribution was evaluated by HES and picrosirius red staining as well as with IRSH. Both techniques showed a strong remodeling of the ECM in Lum–/– mice due to the looseness of collagen fibers in the increased dermis space. These results confirmed the impact of lumican on the ECM integrity. The loss of collagen fibers organization due to the absence of lumican can potentially increase the accessibility of anti-cancer drugs to the tumor. These results are qualitatively interesting and would need further structural characterization of type I collagen fibers in terms of size, organization, and orientation.https://www.frontiersin.org/article/10.3389/fcell.2020.00320/fulllumicanextracellular matrixskin remodelinginfrared imaginghistology
collection DOAJ
language English
format Article
sources DOAJ
author Lise Nannan
Lise Nannan
Valérie Untereiner
Isabelle Proult
Isabelle Proult
Camille Boulagnon-Rombi
Camille Boulagnon-Rombi
Camille Boulagnon-Rombi
Charlie Colin-Pierre
Charlie Colin-Pierre
Charlie Colin-Pierre
Ganesh D. Sockalingum
Stéphane Brézillon
Stéphane Brézillon
spellingShingle Lise Nannan
Lise Nannan
Valérie Untereiner
Isabelle Proult
Isabelle Proult
Camille Boulagnon-Rombi
Camille Boulagnon-Rombi
Camille Boulagnon-Rombi
Charlie Colin-Pierre
Charlie Colin-Pierre
Charlie Colin-Pierre
Ganesh D. Sockalingum
Stéphane Brézillon
Stéphane Brézillon
Label-Free Infrared Spectral Histology of Skin Tissue Part I: Impact of Lumican on Extracellular Matrix Integrity
Frontiers in Cell and Developmental Biology
lumican
extracellular matrix
skin remodeling
infrared imaging
histology
author_facet Lise Nannan
Lise Nannan
Valérie Untereiner
Isabelle Proult
Isabelle Proult
Camille Boulagnon-Rombi
Camille Boulagnon-Rombi
Camille Boulagnon-Rombi
Charlie Colin-Pierre
Charlie Colin-Pierre
Charlie Colin-Pierre
Ganesh D. Sockalingum
Stéphane Brézillon
Stéphane Brézillon
author_sort Lise Nannan
title Label-Free Infrared Spectral Histology of Skin Tissue Part I: Impact of Lumican on Extracellular Matrix Integrity
title_short Label-Free Infrared Spectral Histology of Skin Tissue Part I: Impact of Lumican on Extracellular Matrix Integrity
title_full Label-Free Infrared Spectral Histology of Skin Tissue Part I: Impact of Lumican on Extracellular Matrix Integrity
title_fullStr Label-Free Infrared Spectral Histology of Skin Tissue Part I: Impact of Lumican on Extracellular Matrix Integrity
title_full_unstemmed Label-Free Infrared Spectral Histology of Skin Tissue Part I: Impact of Lumican on Extracellular Matrix Integrity
title_sort label-free infrared spectral histology of skin tissue part i: impact of lumican on extracellular matrix integrity
publisher Frontiers Media S.A.
series Frontiers in Cell and Developmental Biology
issn 2296-634X
publishDate 2020-05-01
description Proteoglycans (PG) play an important role in maintaining the extracellular matrix (ECM) integrity. Lumican, a small leucine rich PG, is one such actor capable of regulating such properties. In this study, the integrity of the dermis of lumican-deleted Lum–/– vs. wild-type mice was investigated by conventional histology and by infrared spectral histology (IRSH). Infrared spectroscopy is a non-invasive, rapid, label-free and sensitive technique that allows to probe molecular vibrations of biomolecules present in a tissue. Our IRSH results obtained on control (WT, n = 3) and Lum–/– (n = 3) mice showed that different histological structures were identified by using K-means clustering and validated by hematoxylin eosin saffron (HES) staining. Furthermore, an important increase of the dermis thickness was observed in Lum–/– compared to WT mice. In terms of structural information, analysis of the spectral images also revealed an intra-group homogeneity and inter-group heterogeneity. In addition, type I collagen contribution was evaluated by HES and picrosirius red staining as well as with IRSH. Both techniques showed a strong remodeling of the ECM in Lum–/– mice due to the looseness of collagen fibers in the increased dermis space. These results confirmed the impact of lumican on the ECM integrity. The loss of collagen fibers organization due to the absence of lumican can potentially increase the accessibility of anti-cancer drugs to the tumor. These results are qualitatively interesting and would need further structural characterization of type I collagen fibers in terms of size, organization, and orientation.
topic lumican
extracellular matrix
skin remodeling
infrared imaging
histology
url https://www.frontiersin.org/article/10.3389/fcell.2020.00320/full
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