{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T05:32:46Z","timestamp":1790487166540,"version":"4.1.0"},"reference-count":40,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2021,1,30]],"date-time":"2021-01-30T00:00:00Z","timestamp":1611964800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"BASF Beauty Care Solutions, Pulnoy","award":["PhD fellow"],"award-info":[{"award-number":["PhD fellow"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biomolecules"],"abstract":"<jats:p>The expression of glypicans in different hair follicle (HF) compartments and their potential roles during hair shaft growth are still poorly understood. Heparan sulfate proteoglycan (HSPG) distribution in HFs is classically investigated by conventional histology, biochemical analysis, and immunohistochemistry. In this report, a novel approach is proposed to assess hair histology and HSPG distribution changes in HFs at different phases of the hair growth cycle using infrared spectral imaging (IRSI). The distribution of HSPGs in HFs was probed by IRSI using the absorption region relevant to sulfation as a spectral marker. The findings were supported by Western immunoblotting and immunohistochemistry assays focusing on the glypican-1 expression and distribution in HFs. This study demonstrates the capacity of IRSI to identify the different HF tissue structures and to highlight protein, proteoglycan (PG), glycosaminoglycan (GAG), and sulfated GAG distribution in these structures. The comparison between anagen, catagen, and telogen phases shows the qualitative and\/or quantitative evolution of GAGs as supported by Western immunoblotting. Thus, IRSI can simultaneously reveal the location of proteins, PGs, GAGs, and sulfated GAGs in HFs in a reagent- and label-free manner. From a dermatological point of view, IRSI shows its potential as a promising technique to study alopecia.<\/jats:p>","DOI":"10.3390\/biom11020192","type":"journal-article","created":{"date-parts":[[2021,1,30]],"date-time":"2021-01-30T06:22:20Z","timestamp":1611987740000},"page":"192","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Hair Histology and Glycosaminoglycans Distribution Probed by Infrared Spectral Imaging: Focus on Heparan Sulfate Proteoglycan and Glypican-1 during Hair Growth Cycle"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5727-3665","authenticated-orcid":false,"given":"Charlie","family":"Colin-Pierre","sequence":"first","affiliation":[{"name":"Universit\u00e9 de Reims Champagne-Ardenne, Laboratoire de Biochimie M\u00e9dicale et Biologie Mol\u00e9culaire, 51097 Reims, France"},{"name":"CNRS UMR 7369, Matrice Extracellulaire et Dynamique Cellulaire-MEDyC, 51097 Reims, France"},{"name":"BASF Beauty Care Solutions France SAS, 54425 Pulnoy, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3360-0171","authenticated-orcid":false,"given":"Val\u00e9rie","family":"Untereiner","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Reims Champagne-Ardenne, PICT, 51097 Reims, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3160-4678","authenticated-orcid":false,"given":"Ganesh D.","family":"Sockalingum","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Reims Champagne-Ardenne, BioSpecT EA7506, UFR de Pharmacie, 51097 Reims, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1100-0885","authenticated-orcid":false,"given":"Nicolas","family":"Berth\u00e9l\u00e9my","sequence":"additional","affiliation":[{"name":"BASF Beauty Care Solutions France SAS, 54425 Pulnoy, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Louis","family":"Danoux","sequence":"additional","affiliation":[{"name":"BASF Beauty Care Solutions France SAS, 54425 Pulnoy, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vincent","family":"Bardey","sequence":"additional","affiliation":[{"name":"BASF Beauty Care Solutions France SAS, 54425 Pulnoy, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sol\u00e8ne","family":"Mine","sequence":"additional","affiliation":[{"name":"BASF Beauty Care Solutions France SAS, 54425 Pulnoy, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Jeanmaire","sequence":"additional","affiliation":[{"name":"BASF Beauty Care Solutions France SAS, 54425 Pulnoy, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurent","family":"Ramont","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Reims Champagne-Ardenne, Laboratoire de Biochimie M\u00e9dicale et Biologie Mol\u00e9culaire, 51097 Reims, France"},{"name":"CNRS UMR 7369, Matrice Extracellulaire et Dynamique Cellulaire-MEDyC, 51097 Reims, France"},{"name":"CHU de Reims, Service Biochimie-Pharmacologie-Toxicologie, 51097 Reims, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"St\u00e9phane","family":"Br\u00e9zillon","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Reims Champagne-Ardenne, Laboratoire de Biochimie M\u00e9dicale et Biologie Mol\u00e9culaire, 51097 Reims, France"},{"name":"CNRS UMR 7369, Matrice Extracellulaire et Dynamique Cellulaire-MEDyC, 51097 Reims, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,1,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1051\/medsci\/2006222138","article-title":"La vie r\u00e9v\u00e9l\u00e9e du follicule de cheveu humain","volume":"22","author":"Bernard","year":"2006","journal-title":"Med. Sci. (Paris)"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1007\/s11154-016-9389-5","article-title":"Beyond Acne: Current Aspects of Sebaceous Gland Biology and Function","volume":"17","author":"Zouboulis","year":"2016","journal-title":"Rev. Endocr. Metab. Disord."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/B978-0-12-405210-9.00001-1","article-title":"New Insights into Mechanisms of Stem Cell Daughter Fate Determination in Regenerative Tissues","volume":"300","author":"Sada","year":"2013","journal-title":"Int. Rev. Cell Mol. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1016\/j.jaad.2004.07.040","article-title":"Exogen Is an Active, Separately Controlled Phase of the Hair Growth Cycle","volume":"52","author":"Stenn","year":"2005","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1046\/j.1523-1747.2002.01842.x","article-title":"Exogen, Shedding Phase of the Hair Growth Cycle: Characterization of a Mouse Model","volume":"119","author":"Milner","year":"2002","journal-title":"J. Investig. Dermatol."},{"key":"ref_6","first-page":"55","article-title":"Donn\u00e9es r\u00e9centes sur la biologie du cheveu","volume":"4","author":"Bernard","year":"1996","journal-title":"Bull. Esthet. Dermatol. Cosmetol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1086\/physzool.24.1.30152098","article-title":"Critical Stages of Hair Development and Pigmentation in the Mouse","volume":"24","author":"Chase","year":"1951","journal-title":"Physiol. Zool."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1046\/j.0022-202x.2001.01377.x","article-title":"A Comprehensive Guide for the Accurate Classification of Murine Hair Follicles in Distinct Hair Cycle Stages","volume":"117","author":"Handjiski","year":"2001","journal-title":"J. Investig. Dermatol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1002\/jez.b.33","article-title":"Molecular Biology of Hair Morphogenesis: Development and Cycling","volume":"298","author":"Botchkarev","year":"2003","journal-title":"J. Exp. Zool. B Mol. Dev. Evol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1186\/gb-2008-9-5-224","article-title":"Glypicans","volume":"9","author":"Filmus","year":"2008","journal-title":"Genome Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"S104","DOI":"10.1177\/089686080702702s18","article-title":"Glycosaminoglycans and Proteoglycans: Overlooked Entities?","volume":"27","author":"Yung","year":"2007","journal-title":"Perit. Dial. Int."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"21305","DOI":"10.1074\/jbc.R800020200","article-title":"Biological Functions of the Small Leucine-Rich Proteoglycans: From Genetics to Signal Transduction","volume":"283","author":"Schaefer","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1161\/01.RES.0000159708.71142.c8","article-title":"Syndecans: New Kids on the Signaling Block","volume":"96","author":"Tkachenko","year":"2005","journal-title":"Circ. Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1016\/j.devcel.2010.02.015","article-title":"The Long-Range Activity of Hedgehog Is Regulated in the Apical Extracellular Space by the Glypican Dally and the Hydrolase Notum","volume":"18","author":"Ayers","year":"2010","journal-title":"Dev. Cell"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2911","DOI":"10.1083\/jcb.201605119","article-title":"Glypican-6 Promotes the Growth of Developing Long Bones by Stimulating Hedgehog Signaling","volume":"216","author":"Capurro","year":"2017","journal-title":"J. Cell Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1016\/j.devcel.2004.08.005","article-title":"Opposing Activities of Dally-like Glypican at High and Low Levels of Wingless Morphogen Activity","volume":"7","author":"Kreuger","year":"2004","journal-title":"Dev. Cell"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"G241","DOI":"10.1152\/ajpgi.00480.2012","article-title":"Heparan Sulfate on Intestinal Epithelial Cells Plays a Critical Role in Intestinal Crypt Homeostasis via Wnt\/\u03b2-Catenin Signaling","volume":"305","author":"Yamamoto","year":"2013","journal-title":"Am. J. Physiol. Gastrointest. Liver Physiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/j.bone.2013.04.013","article-title":"Regulation of Bone Morphogenetic Protein Signalling and Cranial Osteogenesis by Gpc1 and Gpc3","volume":"55","author":"Dwivedi","year":"2013","journal-title":"Bone"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1016\/j.cell.2014.02.057","article-title":"Transit-Amplifying Cells Orchestrate Stem Cell Activity and Tissue Regeneration","volume":"157","author":"Hsu","year":"2014","journal-title":"Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1016\/j.semcdb.2012.08.011","article-title":"Mesenchymal-Epithelial Interactions during Hair Follicle Morphogenesis and Cycling","volume":"23","author":"Sennett","year":"2012","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1111\/j.1365-2133.2007.08339.x","article-title":"Proteoglycan Expression Patterns in Human Hair Follicle","volume":"158","author":"Malgouries","year":"2008","journal-title":"Br. J. Dermatol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1097\/00000372-200212000-00005","article-title":"Syndecan-1 Is Strongly Expressed in the Anagen Hair Follicle Outer Root Sheath and in the Dermal Papilla but Expression Diminishes with Involution of the Hair Follicle","volume":"24","author":"Sanderson","year":"2002","journal-title":"Am. J. Dermatopathol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"25211","DOI":"10.1074\/jbc.M114.572511","article-title":"Heparan Sulfate Regulates Hair Follicle and Sebaceous Gland Morphogenesis and Homeostasis","volume":"289","author":"Gesteira","year":"2014","journal-title":"J. Biol. Chem."},{"key":"ref_24","unstructured":"R\u00e9dini, F. (2012). Characterization of Glycosaminoglycans by Tandem Vibrational Microspectroscopy and Multivariate Data Analysis. Proteoglycans: Methods and Protocols, Humana Press. Methods in Molecular Biology."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2293","DOI":"10.1007\/s00216-009-3140-y","article-title":"IR Spectroscopy Reveals Effect of Non-Cytotoxic Doses of Anti-Tumour Drug on Cancer Cells","volume":"395","author":"Draux","year":"2009","journal-title":"Anal. Bioanal. Chem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2215","DOI":"10.1039\/C4AN01884B","article-title":"Infrared Micro-Spectroscopy for Cyto-Pathological Classification of Esophageal Cells","volume":"140","author":"Townsend","year":"2015","journal-title":"Analyst"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2635","DOI":"10.1039\/C8AN01782D","article-title":"A Comparison of Mid-Infrared Spectral Regions on Accuracy of Tissue Classification","volume":"144","author":"Mittal","year":"2019","journal-title":"Analyst"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1002\/jbio.201200132","article-title":"Immunohistochemistry, Histopathology and Infrared Spectral Histopathology of Colon Cancer Tissue Sections","volume":"6","author":"Mosig","year":"2013","journal-title":"J Biophotonics"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1002\/jps.22288","article-title":"Rapid Characterization of Glycosaminoglycans Using a Combined Approach by Infrared and Raman Microspectroscopies","volume":"100","author":"Mainreck","year":"2011","journal-title":"J. Pharm. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"5795","DOI":"10.1007\/s00216-014-7994-2","article-title":"Glycosaminoglycan Profiling in Different Cell Types Using Infrared Spectroscopy and Imaging","volume":"406","author":"Untereiner","year":"2014","journal-title":"Anal. Bioanal. Chem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1007\/s10719-016-9743-6","article-title":"Implementation of Infrared and Raman Modalities for Glycosaminoglycan Characterization in Complex Systems","volume":"34","author":"Mohamed","year":"2017","journal-title":"Glycoconj. J."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1016\/S0733-8635(05)70387-9","article-title":"Whole Hair Follicle Culture","volume":"14","author":"Philpott","year":"1996","journal-title":"Dermatol. Clin."},{"key":"ref_33","unstructured":"Macqueen, J. Some Methods for Classification and Analysis of Multivariate Observations. Proceedings of the Fifth Berkeley Symposium on Mathematical Statistics and Probability, Beckeley, CA, USA."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"110693","DOI":"10.1016\/j.exger.2019.110693","article-title":"Decreased Expression of GPC1 in Human Skin Keratinocytes and Epidermis during Ageing","volume":"126","author":"Perrot","year":"2019","journal-title":"Exp. Gerontol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1038\/labinvest.2009.48","article-title":"Differential Expression of Stem-Cell-Associated Markers in Human Hair Follicle Epithelial Cells","volume":"89","author":"Inoue","year":"2009","journal-title":"Lab. Investig."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1111\/exd.13666","article-title":"Functional Anatomy of the Hair Follicle: The Secondary Hair Germ","volume":"27","author":"Panteleyev","year":"2018","journal-title":"Exp. Dermatol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1002\/bies.201300166","article-title":"Human Epithelial Hair Follicle Stem Cells and Their Progeny: Current State of Knowledge, the Widening Gap in Translational Research and Future Challenges","volume":"36","author":"Purba","year":"2014","journal-title":"Bioessays"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1111\/j.1600-0625.2008.00720.x","article-title":"Immunophenotyping of the Human Bulge Region: The Quest to Define Useful in Situ Markers for Human Epithelial Hair Follicle Stem Cells and Their Niche","volume":"17","author":"Kloepper","year":"2008","journal-title":"Exp. Dermatol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1111\/1523-1747.ep12873363","article-title":"Distribution of Two Basement Membrane Proteoglycans through Hair Follicle Development and the Hair Growth Cycle in the Rat","volume":"94","author":"Couchman","year":"1990","journal-title":"J. Investig. Dermatol."}],"container-title":["Biomolecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2218-273X\/11\/2\/192\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:17:27Z","timestamp":1760159847000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2218-273X\/11\/2\/192"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,30]]},"references-count":40,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["biom11020192"],"URL":"https:\/\/doi.org\/10.3390\/biom11020192","relation":{},"ISSN":["2218-273X"],"issn-type":[{"value":"2218-273X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,30]]}}}