{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,2,21]],"date-time":"2025-02-21T14:08:47Z","timestamp":1740146927573,"version":"3.37.3"},"reference-count":54,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2023,3,31]],"date-time":"2023-03-31T00:00:00Z","timestamp":1680220800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100005825","name":"National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["CA-D-ETX-2152-H"],"award-info":[{"award-number":["CA-D-ETX-2152-H"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Protein profiling offers an effective approach to characterizing how far epidermis departs from normal in disease states. The present pilot investigation tested the hypothesis that protein expression in epidermal corneocytes is perturbed in the forehead of subjects exhibiting frontal fibrosing alopecia. To this end, samples were collected by tape stripping from subjects diagnosed with this condition and compared to those from asymptomatic control subjects and from those exhibiting androgenetic alopecia. Unlike the latter, which exhibited only 3 proteins significantly different from controls in expression level, forehead samples from frontal fibrosing alopecia subjects displayed 72 proteins significantly different from controls, nearly two-thirds having lower expression. The results demonstrate frontal fibrosing alopecia exhibits altered corneocyte protein expression in epidermis beyond the scalp, indicative of a systemic condition. They also provide a basis for quantitative measures of departure from normal by assaying forehead epidermis, useful in monitoring response to treatment while avoiding invasive biopsy.<\/jats:p>","DOI":"10.1371\/journal.pone.0283619","type":"journal-article","created":{"date-parts":[[2023,3,31]],"date-time":"2023-03-31T17:47:58Z","timestamp":1680284878000},"page":"e0283619","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":2,"title":["Protein profiling of forehead epidermal corneocytes distinguishes frontal fibrosing from androgenetic alopecia"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5699-6500","authenticated-orcid":true,"given":"Noreen","family":"Karim","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Paradi","family":"Mirmirani","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Blythe P.","family":"Durbin-Johnson","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David M.","family":"Rocke","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michelle","family":"Salemi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Brett S.","family":"Phinney","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2058-4405","authenticated-orcid":true,"given":"Robert H.","family":"Rice","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2023,3,31]]},"reference":[{"key":"pone.0283619.ref001","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1111\/exd.13756","article-title":"Corneocyte proteomics: Applications to skin biology and dermatology","volume":"27","author":"RH Rice","year":"2018","journal-title":"Exp Dermatol"},{"issue":"10","key":"pone.0283619.ref002","doi-asserted-by":"crossref","first-page":"e75355","DOI":"10.1371\/journal.pone.0075355","article-title":"Distinguishing ichthyoses by protein profiling","volume":"8","author":"RH Rice","year":"2013","journal-title":"PLoS One"},{"key":"pone.0283619.ref003","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.jprot.2019.04.007","article-title":"Proteomic manifestations of genetic defects in autosomal recessive congenital ichthyosis","volume":"201","author":"N Karim","year":"2019","journal-title":"J Proteomics"},{"key":"pone.0283619.ref004","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1074\/mcp.M500278-MCP200","article-title":"Proteome analysis of human hair shaft: From protein identification to posttranslational modification","volume":"5","author":"YJ Lee","year":"2006","journal-title":"Molec Cell Proteom"},{"key":"pone.0283619.ref005","doi-asserted-by":"crossref","first-page":"e506","DOI":"10.7717\/peerj.506","article-title":"Human hair shaft proteomic profiling: individual differences, site specificity and cuticle analysis","volume":"2","author":"CN Laatsch","year":"2014","journal-title":"PeerJ"},{"key":"pone.0283619.ref006","doi-asserted-by":"crossref","first-page":"6752","DOI":"10.1021\/pr1009349","article-title":"Proteomic analysis of human nail plate","volume":"9","author":"RH Rice","year":"2010","journal-title":"J Proteome Res"},{"issue":"2","key":"pone.0283619.ref007","doi-asserted-by":"crossref","first-page":"e1647","DOI":"10.1038\/cddis.2015.21","article-title":"Structural and biochemical changes underlying a keratoderma-like phenotype in mice lacking suprabasal AP1 transcription factor function","volume":"6","author":"EA Rorke","year":"2015","journal-title":"Cell Death Dis"},{"key":"pone.0283619.ref008","doi-asserted-by":"crossref","first-page":"2560","DOI":"10.1021\/acs.jproteome.6b00108","article-title":"Proteomic analysis of loricrin knockout mouse epidermis","volume":"15","author":"RH Rice","year":"2016","journal-title":"J Proteome Res"},{"key":"pone.0283619.ref009","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.jprot.2017.06.017","article-title":"Proteomic profiling of Pachyonychia congenita plantar callus","volume":"165","author":"RH Rice","year":"2017","journal-title":"J Proteomics"},{"key":"pone.0283619.ref010","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1111\/exd.13925","article-title":"Human stratum corneum proteomics reveals cross-linking of a broad spectrum of proteins in cornified envelopes","volume":"28","author":"N Karim","year":"2019","journal-title":"Exp Dermatol"},{"key":"pone.0283619.ref011","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1111\/exd.14130","article-title":"Hormonal regulation in male androgenetic alopecia\u2014Sex hormones and beyond","volume":"29","author":"S Heilmann-Heimbach","year":"2020","journal-title":"Exp Dermatol"},{"key":"pone.0283619.ref012","doi-asserted-by":"crossref","first-page":"14694","DOI":"10.1038\/ncomms14694","article-title":"Meta-analysis identifies novel risk loci and yields systematic insights into the biology of male-pattern baldness","volume":"8","author":"S Heilmann-Heimbach","year":"2017","journal-title":"Nature Communications"},{"key":"pone.0283619.ref013","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.clindermatol.2017.09.009","article-title":"Alopecia and the metabolic syndrome","volume":"36","author":"C Lie","year":"2018","journal-title":"Clin Dermatol"},{"key":"pone.0283619.ref014","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1080\/000155599750010238","article-title":"Quantitative and ultrastructural analysis of inflammatory infiltrates in male pattern alopecia","volume":"79","author":"H Sueki","year":"1999","journal-title":"Acta Derm Venereol"},{"key":"pone.0283619.ref015","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1159\/000489793","article-title":"Frontal fibrosing alopecia: an emerging epidemic","volume":"5","author":"P Mirmirani","year":"2019","journal-title":"Skin Appendage Disord"},{"key":"pone.0283619.ref016","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/j.jaad.2009.09.020","article-title":"Expanding the spectrum of frontal fibrosing alopecia: A unifying concept","volume":"63","author":"A-L Chew","year":"2010","journal-title":"J Am Acad Dermatol"},{"key":"pone.0283619.ref017","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.1111\/bjd.20567","article-title":"Guidelines for clinical trials of frontal fibrosing alopecia: consensus recommendations from the International FFA Cooperative Group (IFFACG)","volume":"185","author":"EA Olsen","year":"2021","journal-title":"Br J Dermatol"},{"key":"pone.0283619.ref018","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1111\/cup.13112","article-title":"Lichen planopilaris and frontal fibrosing alopecia cannot be differentiated by histopathology","volume":"45","author":"A Galvez-Canseco","year":"2018","journal-title":"Journal of Cutaneous Pathology"},{"key":"pone.0283619.ref019","doi-asserted-by":"crossref","first-page":"320","DOI":"10.18295\/squmj.2021.21.02.025","article-title":"Famial frontal fibrisong alopecia. Report of a case and systematic review of the literature","volume":"21","author":"C Cuenca-Barrales","year":"2021","journal-title":"Sultan Qaboos University Med J"},{"key":"pone.0283619.ref020","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1159\/000512039","article-title":"Frontal fibrosing alopecia: is there a link in relatives?","volume":"7","author":"SS Ocampo-Garza","year":"2021","journal-title":"Skin Appendage Disord"},{"key":"pone.0283619.ref021","doi-asserted-by":"crossref","first-page":"1150","DOI":"10.1038\/s41467-019-09117-w","article-title":"Genome-wide association study in frontal fibrosing alopecia identifies four susceptibility loci including HLA-B*07:02","volume":"10","author":"C Tziotzios","year":"2019","journal-title":"Nature Communications"},{"key":"pone.0283619.ref022","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/j.molmed.2018.03.007","article-title":"Lichen planopilaris and frontal fibrosing alopecia as model epithelial stem cell diseases","volume":"24","author":"MJ Harries","year":"2018","journal-title":"Trends Molec Med"},{"key":"pone.0283619.ref023","doi-asserted-by":"crossref","first-page":"10113","DOI":"10.1016\/j.xjidi.2022.100113","article-title":"Frontiers in lichen planopilaris and frontal fibrosing alopecia research: pathobiology progress and translational horizons","volume":"2","author":"MM Senna","year":"2022","journal-title":"JID Innovations"},{"key":"pone.0283619.ref024","doi-asserted-by":"crossref","first-page":"1243","DOI":"10.1038\/jid.2008.369","article-title":"Hair follicle stem cell-specific PPARgamma deletion causes scarring alopecia","volume":"129","author":"P Karnik","year":"2009","journal-title":"J Invest Dermatol"},{"key":"pone.0283619.ref025","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.clindermatol.2020.10.007","article-title":"Frontal fibrosing alopecia","volume":"39","author":"KLS Kerkemeyer","year":"2021","journal-title":"Clin Dermatol"},{"key":"pone.0283619.ref026","doi-asserted-by":"crossref","first-page":"1739","DOI":"10.1111\/jdv.14287","article-title":"Frontal fibrosing alopecia: clinical and prognostic classification","volume":"31","author":"OM Moreno-Arrones","year":"2017","journal-title":"Journal of the European Academy of Dermatology and Venereology"},{"key":"pone.0283619.ref027","doi-asserted-by":"crossref","first-page":"102309","DOI":"10.1016\/j.fsigen.2020.102309","article-title":"Age-related changes in hair shaft protein profiling and genetically variant peptides","volume":"47","author":"TJ Plott","year":"2020","journal-title":"Foren Sci Int: Genet"},{"key":"pone.0283619.ref028","doi-asserted-by":"crossref","first-page":"4193","DOI":"10.1021\/ac0498563","article-title":"A model for random sampling and estimation of relative protein abundance in shotgun proteomics","volume":"76","author":"H Liu","year":"2004","journal-title":"Analyt Chem"},{"key":"pone.0283619.ref029","doi-asserted-by":"crossref","first-page":"3550","DOI":"10.1021\/acs.jproteome.6b00308","article-title":"Comparing the diagnostic classification accuracy of iTRAQ, peak-area, spectral-counting, and emPAI methods for relative quantification in expression proteomics","volume":"15","author":"AA Dowle","year":"2016","journal-title":"J Proteome Res"},{"key":"pone.0283619.ref030","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.jprot.2015.11.011","article-title":"Benchmarking quantitative label-free LC-MS data processing workflows using a complex spiked proteomic standard dataset","volume":"132","author":"C Ramus","year":"2016","journal-title":"J Proteomics"},{"issue":"7","key":"pone.0283619.ref031","doi-asserted-by":"crossref","first-page":"e47","DOI":"10.1093\/nar\/gkv007","article-title":"limma powers differential expression analyses for RNA-sequencing and microarray studies","volume":"43","author":"ME Ritchie","year":"2015","journal-title":"Nucl Acids Res"},{"key":"pone.0283619.ref032","doi-asserted-by":"crossref","first-page":"R25","DOI":"10.1186\/gb-2010-11-3-r25","article-title":"A scaling normalization method for differential expression analysis of RNA-seq data","volume":"11","author":"MD Robinson","year":"2010","journal-title":"Genome Biol"},{"key":"pone.0283619.ref033","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the false discovery rate: A practical and powerful approach to multiple testing","volume":"57","author":"Y Benjamini","year":"1995","journal-title":"J Royal Stat Soc, Ser B"},{"volume-title":"Theory and Methods of Scaling","year":"1958","author":"WS Torgerson","key":"pone.0283619.ref034"},{"key":"pone.0283619.ref035","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1083\/jcb.200603161","article-title":"New consensus nomenclature for mammalian keratins","volume":"174","author":"J Schweizer","year":"2006","journal-title":"J Cell Biol"},{"key":"pone.0283619.ref036","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/j.jaad.2021.09.033","article-title":"Frontal fibrosing alopecia in men: a multicenter study of 39 patients","volume":"86","author":"A Lobato-Berezo","year":"2022","journal-title":"J Am Acad Dermatol"},{"issue":"10","key":"pone.0283619.ref037","doi-asserted-by":"crossref","first-page":"e372","DOI":"10.1111\/ijd.16313","article-title":"Clinical features and treatment outcomes of frontal fibrosing alopecia in men","volume":"61","author":"A Moussa","year":"2022","journal-title":"Int J Dermatol"},{"issue":"7","key":"pone.0283619.ref038","doi-asserted-by":"crossref","first-page":"e101937","DOI":"10.1371\/journal.pone.0101937","article-title":"Inhibition of keratinocyte differentiation by the synergistic effect of IL-17A, IL-22, IL-1\u03b1, TNF\u03b1 and oncostatin M","volume":"9","author":"H Rabeony","year":"2014","journal-title":"PLoS One"},{"key":"pone.0283619.ref039","doi-asserted-by":"crossref","first-page":"e9504","DOI":"10.7717\/peerj.9504","article-title":"Off-target effects of protein tyrosine phosphatase inhibitors on oncostatin M-treated human epidermal cells: the phosphatase targeting STAT1 remains unknown","volume":"8","author":"BV Hong","year":"2020","journal-title":"PeerJ"},{"key":"pone.0283619.ref040","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.jid.2021.05.033","article-title":"Nuclear IL-33 plays an important role in IL-31-mediated downregulation of FLG, keratin 1 and keratin 10 by regulating signal transducer and activator of transcription 3 activation in human keratinocytes","volume":"142","author":"X Dai","year":"2022","journal-title":"J Invest Dermatol"},{"key":"pone.0283619.ref041","doi-asserted-by":"crossref","first-page":"1240","DOI":"10.1001\/archdermatol.2011.261","article-title":"Lonely hair: A clue to the diagnosis of frontal fibrosing alopecia","volume":"147","author":"A Tosti","year":"2011","journal-title":"Arch Dermatol"},{"key":"pone.0283619.ref042","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.jbior.2015.11.004","article-title":"Phospholipase C \u03b41 in macrophages negatively regulates TLR4-induced proinflammatory cytokine production and Fc\u03b3 receptor-mediated phagocytosis","volume":"61","author":"K Kudo","year":"2016","journal-title":"Advances in Biological Regulation"},{"key":"pone.0283619.ref043","doi-asserted-by":"crossref","first-page":"912","DOI":"10.1016\/j.bbrc.2007.03.082","article-title":"Lack of phospholipase C-\u03b41 induces skin inflammation","volume":"356","author":"M Ichinohe","year":"2007","journal-title":"Biochem Biophys Res Commun"},{"issue":"6","key":"pone.0283619.ref044","doi-asserted-by":"crossref","first-page":"e39203","DOI":"10.1371\/journal.pone.0039203","article-title":"Alopecia in a viable phospholipase C delta 1 and phospholipase C delta 3 double mutant","volume":"7","author":"F Runkel","year":"2012","journal-title":"PLoS One"},{"key":"pone.0283619.ref045","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1096\/fj.07-9239com","article-title":"Phospholipase C-\u03b41 is an essential molecule downstream of Foxn1, the gene responsible for the nude mutation, in normal hair development","volume":"22","author":"Y Nakamura","year":"2008","journal-title":"FASEB J"},{"key":"pone.0283619.ref046","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1006\/excr.2001.5254","article-title":"Human calmodulin-like protein is an epithelial-specific protein regulated during keratinocyte differentiation","volume":"267","author":"MS Rogers","year":"2001","journal-title":"Exp Cell Res"},{"key":"pone.0283619.ref047","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.cellsig.2016.12.007","article-title":"Extracellular functions of 14-3-3 adaptor proteins","volume":"31","author":"A Kaplan","year":"2017","journal-title":"Cell Signaling"},{"key":"pone.0283619.ref048","doi-asserted-by":"crossref","first-page":"15977","DOI":"10.1073\/pnas.0508310102","article-title":"Identification of 14-3-3\u03c3 mutation causing cutaneous abnormality in repeated-epilation mutant mouse","volume":"102","author":"Q Li","year":"2005","journal-title":"Proc Natl Acad Sci USA"},{"key":"pone.0283619.ref049","doi-asserted-by":"crossref","first-page":"1210","DOI":"10.1038\/ng1652","article-title":"A mutation in stratifin is responsoble for the repeated epilation (Er) phenotype in mice","volume":"37","author":"BJ Herron","year":"2005","journal-title":"Nat Genet"},{"key":"pone.0283619.ref050","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.1111\/j.0022-202X.2004.22519.x","article-title":"Keratinocyte-releasable stratifin functions as a potent collagenase-stimulating factor in fibroblasts","volume":"122","author":"A Ghahary","year":"2004","journal-title":"J Invest Dermatol"},{"key":"pone.0283619.ref051","doi-asserted-by":"crossref","first-page":"6e20210518","DOI":"10.1084\/jem.20210518","article-title":"Ferroptosis in infection, inflammation, and immunity","volume":"218","author":"X Chen","year":"2021","journal-title":"J Exp Med"},{"key":"pone.0283619.ref052","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1038\/s41586-022-04717-x","article-title":"Group A Streptococcus induces GSDMA-dependent pyroptosis in keratinocytes","volume":"605","author":"DL LaRock","year":"2022","journal-title":"Nature"},{"key":"pone.0283619.ref053","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/B978-0-12-397863-9.00003-1","article-title":"Immunoproteasomes: structure, function, and antigen presentation","volume":"109","author":"DA Ferrington","year":"2012","journal-title":"Progress in Molecular Biology and Translational Science"},{"key":"pone.0283619.ref054","doi-asserted-by":"crossref","first-page":"24","DOI":"10.2174\/156652413804486214","article-title":"Functions of S100 proteins","volume":"13","author":"R Donato","year":"2013","journal-title":"Curr Molec Med"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0283619","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,17]],"date-time":"2024-10-17T13:26:55Z","timestamp":1729171615000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0283619"}},"subtitle":[],"editor":[{"given":"Michel","family":"Simon","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2023,3,31]]},"references-count":54,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2023,3,31]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0283619","relation":{},"ISSN":["1932-6203"],"issn-type":[{"type":"electronic","value":"1932-6203"}],"subject":[],"published":{"date-parts":[[2023,3,31]]}}}