{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:54:08Z","timestamp":1760147648887,"version":"build-2065373602"},"reference-count":27,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,2,21]],"date-time":"2023-02-21T00:00:00Z","timestamp":1676937600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"BASF Beauty Care Solutions"},{"name":"BASF\/CNRS (Centre national de la recherche scientifique)"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The expression of glypicans in different hair follicle (HF) compartments is still poorly understood. Heparan sulfate proteoglycans (HSPGs) distribution in HF is classically investigated by conventional histology, biochemical analysis, and immunohistochemistry. Our previous study proposed a novel approach to assess hair histology and glypican-1 (GPC1) distribution changes in the HF at different phases of the hair growth cycle using infrared spectral imaging (IRSI). We show in the present manuscript for the first time complementary data on the distribution of glypican-4 (GPC4) and glypican-6 (GPC6) in HF at different phases of the hair growth cycle using IR imaging. Findings were supported by Western blot assays focusing on the GPC4 and GPC6 expression in HFs. Like all proteoglycan features, the glypicans are characterized by a core protein to which sulfated and\/or unsulfated glycosaminoglycan (GAG) chains are covalently linked. Our study demonstrates the capacity of IRSI to identify the different HF tissue structures and to highlight protein, proteoglycan (PG), 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 blot. Thus, in one analysis, IRSI can simultaneously reveal the location of proteins, PGs, GAGs and sulfated GAGs in HFs in a chemical and label-free manner. From a dermatological point of view, IRSI may constitute a promising technique to study alopecia.<\/jats:p>","DOI":"10.3390\/ijms24054291","type":"journal-article","created":{"date-parts":[[2023,2,22]],"date-time":"2023-02-22T03:32:17Z","timestamp":1677036737000},"page":"4291","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Investigation of Glypican-4 and -6 by Infrared Spectral Imaging during the Hair Growth Cycle"],"prefix":"10.3390","volume":"24","author":[{"given":"Charlie","family":"Colin-Pierre","sequence":"first","affiliation":[{"name":"Laboratoire de Biochimie M\u00e9dicale et Biologie Mol\u00e9culaire, Universit\u00e9 de Reims Champagne-Ardenne, 51097 Reims, France"},{"name":"Matrice Extracellulaire et Dynamique Cellulaire-MEDyC, CNRS UMR 7369, 51097 Reims, France"},{"name":"BASF Beauty Care Solutions France SAS, 54425 Pulnoy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3360-0171","authenticated-orcid":false,"given":"Val\u00e9rie","family":"Untereiner","sequence":"additional","affiliation":[{"name":"PICT, Universit\u00e9 de Reims Champagne-Ardenne, 51097 Reims, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"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":[{"role":"author","vocabulary":"crossref"}]},{"given":"Laurent","family":"Ramont","sequence":"additional","affiliation":[{"name":"Laboratoire de Biochimie M\u00e9dicale et Biologie Mol\u00e9culaire, Universit\u00e9 de Reims Champagne-Ardenne, 51097 Reims, France"},{"name":"Matrice Extracellulaire et Dynamique Cellulaire-MEDyC, CNRS UMR 7369, 51097 Reims, France"},{"name":"Service Biochimie-Pharmacologie-Toxicologie, CHU de Reims, 51097 Reims, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"St\u00e9phane","family":"Br\u00e9zillon","sequence":"additional","affiliation":[{"name":"Laboratoire de Biochimie M\u00e9dicale et Biologie Mol\u00e9culaire, Universit\u00e9 de Reims Champagne-Ardenne, 51097 Reims, France"},{"name":"Matrice Extracellulaire et Dynamique Cellulaire-MEDyC, CNRS UMR 7369, 51097 Reims, France"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,21]]},"reference":[{"key":"ref_1","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_2","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_3","doi-asserted-by":"crossref","unstructured":"Colin-Pierre, C., Untereiner, V., Sockalingum, G.D., Berth\u00e9l\u00e9my, N., Danoux, L., Bardey, V., Mine, S., Jeanmaire, C., Ramont, L., and Br\u00e9zillon, S. (2021). Hair Histology and Glycosaminoglycans Distribution Probed by Infrared Spectral Imaging: Focus on Heparan Sulfate Proteoglycan and Glypican-1 during Hair Growth Cycle. Biomolecules, 11.","DOI":"10.3390\/biom11020192"},{"key":"ref_4","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_5","doi-asserted-by":"crossref","first-page":"8125081","DOI":"10.1155\/2020\/8125081","article-title":"Integral Roles of Specific Proteoglycans in Hair Growth and Hair Loss: Mechanisms behind the Bioactivity of Proteoglycan Replacement Therapy with Nourkrin\u00ae with Marilex\u00ae in Pattern Hair Loss and Telogen Effluvium","volume":"2020","author":"Wadstein","year":"2020","journal-title":"Dermatol. Res. Pract."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1177\/030006059101900208","article-title":"Imedeen for the Treatment of Degenerated Skin in Females","volume":"19","author":"Lassus","year":"1991","journal-title":"J. Int. Med. Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1177\/147323000603400508","article-title":"Nourkrin: Objective and Subjective Effects and Tolerability in Persons with Hair Loss","volume":"34","author":"Thom","year":"2006","journal-title":"J. Int. Med. Res."},{"key":"ref_8","first-page":"49","article-title":"Cosmetic Hair Treatments Improve Quality of Life in Women with Female Pattern Hair Loss","volume":"30","author":"Kingsley","year":"2012","journal-title":"J. Appl. Cosmetol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"9152","DOI":"10.1021\/acs.chemrev.8b00354","article-title":"Proteoglycan Chemical Diversity Drives Multifunctional Cell Regulation and Therapeutics","volume":"118","author":"Karamanos","year":"2018","journal-title":"Chem. Rev."},{"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":"85","DOI":"10.1038\/s41586-020-2498-z","article-title":"Glypicans Shield the Wnt Lipid Moiety to Enable Signalling at a Distance","volume":"585","author":"McGough","year":"2020","journal-title":"Nature"},{"key":"ref_12","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_13","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_14","doi-asserted-by":"crossref","first-page":"22936","DOI":"10.1074\/jbc.273.36.22936","article-title":"Heparan Sulfate Oligosaccharides Require 6-O-Sulfation for Promotion of Basic Fibroblast Growth Factor Mitogenic Activity","volume":"273","author":"Pye","year":"1998","journal-title":"J. Biol. Chem."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1369\/0022155420933709","article-title":"The Role of Glypicans in Cancer Progression and Therapy","volume":"68","author":"Li","year":"2020","journal-title":"J. Histochem. Cytochem. Off. J. Histochem. Soc."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1172\/JCI26043","article-title":"Characterization and Isolation of Stem Cell-Enriched Human Hair Follicle Bulge Cells","volume":"116","author":"Ohyama","year":"2006","journal-title":"J. Clin. Investig."},{"key":"ref_17","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_18","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_19","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_20","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_21","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/j.ydbio.2016.09.002","article-title":"Glypican4 Modulates Lateral Line Collective Cell Migration Non Cell-Autonomously","volume":"419","author":"Lush","year":"2016","journal-title":"Dev. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1863","DOI":"10.1002\/stem.1165","article-title":"Modulating Glypican4 Suppresses Tumorigenicity of Embryonic Stem Cells While Preserving Self-Renewal and Pluripotency","volume":"30","author":"Fico","year":"2012","journal-title":"Stem Cells"},{"key":"ref_23","first-page":"353","article-title":"Glypican-4 Is an FGF2-Binding Heparan Sulfate Proteoglycan Expressed in Neural Precursor Cells","volume":"219","author":"Hagihara","year":"2000","journal-title":"Dev. Dyn. Off. Publ. Am. Assoc. Anat."},{"key":"ref_24","first-page":"4919","article-title":"Glypican 4 Modulates FGF Signalling and Regulates Dorsoventral Forebrain Patterning in Xenopus Embryos","volume":"130","author":"Galli","year":"2003","journal-title":"Dev. Camb. Engl."},{"key":"ref_25","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":"Foitzik","year":"2001","journal-title":"J. Investig. Dermatol."},{"key":"ref_26","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_27","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."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/5\/4291\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:38:18Z","timestamp":1760121498000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/5\/4291"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,21]]},"references-count":27,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,3]]}},"alternative-id":["ijms24054291"],"URL":"https:\/\/doi.org\/10.3390\/ijms24054291","relation":{},"ISSN":["1422-0067"],"issn-type":[{"type":"electronic","value":"1422-0067"}],"subject":[],"published":{"date-parts":[[2023,2,21]]}}}