{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T18:32:11Z","timestamp":1790620331193,"version":"4.1.0"},"reference-count":74,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2025,7,29]],"date-time":"2025-07-29T00:00:00Z","timestamp":1753747200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>The human skin microbiota, a complex community of bacterial, fungal, and viral organisms, plays a crucial role in maintaining skin homeostasis and regulating host-pathogen interactions. Dysbiosis within this microbial ecosystem has been implicated in various dermatological conditions, including acne vulgaris, psoriasis, seborrheic dermatitis, and atopic dermatitis. This review, for the first time, provides recent advancements in all four layers of omic technologies\u2014metagenomics, metatranscriptomics, metaproteomics, and metabolomics\u2014offering comprehensive insights into microbial diversity, in the context of functional skin modeling. Thus, this review explores the application of these omic tools to in vitro skin models, providing an integrated framework for understanding the molecular mechanisms underlying skin\u2013microbiota interactions in both healthy and pathological contexts. We highlight the importance of developing advanced in vitro skin models, including the integration of immune components and endothelial cells, to accurately replicate the cutaneous microenvironment. Moreover, we discuss the potential of these models to identify novel therapeutic targets, enabling the design of personalized treatments aimed at restoring microbial balance, reinforcing the skin barrier, and modulating inflammation. As the field progresses, the incorporation of multi-omic approaches into skin-microbiome research will be pivotal in unraveling the complex interactions between host and microbiota, ultimately advancing therapeutic strategies for skin-related diseases.<\/jats:p>","DOI":"10.3390\/microorganisms13081771","type":"journal-article","created":{"date-parts":[[2025,7,29]],"date-time":"2025-07-29T16:16:10Z","timestamp":1753805770000},"page":"1771","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Alternatives Integrating Omics Approaches for the Advancement of Human Skin Models: A Focus on Metagenomics, Metatranscriptomics, and Metaproteomics"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4317-2131","authenticated-orcid":false,"given":"Estibaliz","family":"Fern\u00e1ndez-Carro","sequence":"first","affiliation":[{"name":"Tissue Microenvironment (TME) Lab, Arag\u00f3n Institute of Engineering Research (I3A), University of Zaragoza, C\/Mariano Esquillor s\/n, 50018 Zaragoza, Spain"},{"name":"Department of Anatomy and Histology, Faculty of Medicine, University of Zaragoza, 50009 Zaragoza, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9155-0889","authenticated-orcid":false,"given":"Sophia","family":"Letsiou","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, University of West Attica, Ag. Spiridonos St. Egaleo, 12243 Athens, Greece"},{"name":"Department of Food Science and Technology, University of West Attica, Ag. Spiridonos St. Egaleo, 12243 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stella","family":"Tsironi","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, University of West Attica, Ag. Spiridonos St. Egaleo, 12243 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2313-1305","authenticated-orcid":false,"given":"Dimitrios","family":"Chaniotis","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, University of West Attica, Ag. Spiridonos St. Egaleo, 12243 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8666-622X","authenticated-orcid":false,"given":"Jes\u00fas","family":"Ciriza","sequence":"additional","affiliation":[{"name":"Tissue Microenvironment (TME) Lab, Arag\u00f3n Institute of Engineering Research (I3A), University of Zaragoza, C\/Mariano Esquillor s\/n, 50018 Zaragoza, Spain"},{"name":"Department of Anatomy and Histology, Faculty of Medicine, University of Zaragoza, 50009 Zaragoza, Spain"},{"name":"Institute for Health Research Arag\u00f3n (IIS Arag\u00f3n), Avda. San Juan Bosco, 13, 50009 Zargoza, Spain"},{"name":"Center of Bioengineering, Biomaterials and Nanomedicine, CIBER-BBN, 28029 Madrid, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5639-0528","authenticated-orcid":false,"given":"Apostolos","family":"Beloukas","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, University of West Attica, Ag. Spiridonos St. Egaleo, 12243 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,7,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Smythe, P., and Wilkinson, H.N. (2023). The Skin Microbiome: Current Landscape and Future Opportunities. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24043950"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1431","DOI":"10.1038\/ncomms2441","article-title":"The Microbiome Extends to Subepidermal Compartments of Normal Skin","volume":"4","author":"Nakatsuji","year":"2013","journal-title":"Nat. Commun."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1038\/nrmicro2537","article-title":"The Skin Microbiome","volume":"9","author":"Grice","year":"2011","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1038\/nrmicro.2017.157","article-title":"The Human Skin Microbiome","volume":"16","author":"Byrd","year":"2018","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"11971","DOI":"10.1073\/pnas.1002601107","article-title":"Delivery Mode Shapes the Acquisition and Structure of the Initial Microbiota across Multiple Body Habitats in Newborns","volume":"107","author":"Costello","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1038\/nm.4272","article-title":"Maturation of the Infant Microbiome Community Structure and Function across Multiple Body Sites and in Relation to Mode of Delivery","volume":"23","author":"Chu","year":"2017","journal-title":"Nat. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1186\/gm378","article-title":"Shifts in Human Skin and Nares Microbiota of Healthy Children and Adults","volume":"4","author":"Oh","year":"2012","journal-title":"Genome Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1016\/j.cell.2016.04.008","article-title":"Temporal Stability of the Human Skin Microbiome","volume":"165","author":"Oh","year":"2016","journal-title":"Cell"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1190","DOI":"10.1126\/science.1171700","article-title":"Topographical and Temporal Diversity of the Human Skin Microbiome","volume":"324","author":"Grice","year":"2009","journal-title":"Science"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"71","DOI":"10.2147\/PTT.S328439","article-title":"The Skin Microbiome and Its Role in Psoriasis: A Review","volume":"13","author":"Celoria","year":"2023","journal-title":"Psoriasis"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Martins, A.M., Ascenso, A., Ribeiro, H.M., and Marto, J. (2020). The Brain-Skin Connection and the Pathogenesis of Psoriasis: A Review with a Focus on the Serotonergic System. Cells, 9.","DOI":"10.3390\/cells9040796"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1111\/exd.14091","article-title":"An Update on the Microbiology, Immunology and Genetics of Seborrheic Dermatitis","volume":"29","author":"Adalsteinsson","year":"2020","journal-title":"Exp. Dermatol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1007\/s40266-022-00930-5","article-title":"Seborrheic Dermatitis in Older Adults: Pathogenesis and Treatment Options","volume":"39","author":"Sowell","year":"2022","journal-title":"Drugs Aging"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1111\/exd.13210","article-title":"Experimental Metagenomics and Ribosomal Profiling of the Human Skin Microbiome","volume":"26","author":"Ferretti","year":"2017","journal-title":"Exp. Dermatol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Sandhu, S.S., Pourang, A., and Sivamani, R.K. (2019). A Review of next Generation Sequencing Technologies Used in the Evaluation of the Skin Microbiome: What a Time to Be Alive. Dermatol. Online J., 25.","DOI":"10.5070\/D3257044797"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.jid.2021.07.159","article-title":"Deciphering the Role of Skin Surface Microbiome in Skin Health: An Integrative Multiomics Approach Reveals Three Distinct Metabolite\u2012Microbe Clusters","volume":"142","author":"Roux","year":"2022","journal-title":"JID"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Rusi\u00f1ol, L., and Puig, L. (2024). Multi-Omics Approach to Improved Diagnosis and Treatment of Atopic Dermatitis and Psoriasis. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25021042"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Guo, Y., Luo, L., Zhu, J., and Li, C. (2023). Multi-Omics Research Strategies for Psoriasis and Atopic Dermatitis. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24098018"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1128\/MMBR.68.4.669-685.2004","article-title":"Metagenomics: Application of Genomics to Uncultured Microorganisms","volume":"68","author":"Handelsman","year":"2004","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1016\/j.jid.2016.01.016","article-title":"Skin Microbiome Surveys Are Strongly Influenced by Experimental Design","volume":"136","author":"Meisel","year":"2016","journal-title":"JID"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e119","DOI":"10.1016\/j.jid.2016.07.045","article-title":"The Molecular Revolution in Cutaneous Biology: Investigating the Skin Microbiome","volume":"137","author":"Kong","year":"2017","journal-title":"JID"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"De Filippis, F., Laiola, M., Blaiotta, G., and Ercolini, D. (2017). Different Amplicon Targets for Sequencing-Based Studies of Fungal Diversity. Appl. Environ. Microbiol., 83.","DOI":"10.1128\/AEM.00905-17"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e23","DOI":"10.1016\/j.jid.2016.01.005","article-title":"Research Techniques Made Simple: Bacterial 16S Ribosomal RNA Gene Sequencing in Cutaneous Research","volume":"136","author":"Jo","year":"2016","journal-title":"JID"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Jovel, J., Patterson, J., Wang, W., Hotte, N., O\u2019Keefe, S., Mitchel, T., Perry, T., Kao, D., Mason, A.L., and Madsen, K.L. (2016). Characterization of the Gut Microbiome Using 16S or Shotgun Metagenomics. Front. Microbiol., 7.","DOI":"10.3389\/fmicb.2016.00459"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1016\/j.bbrc.2015.12.083","article-title":"Analysis of the Microbiome: Advantages of Whole Genome Shotgun versus 16S Amplicon Sequencing","volume":"469","author":"Ranjan","year":"2016","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Bashiardes, S., Zilberman-Schapira, G., and Elinav, E. (2016). Use of Metatranscriptomics in Microbiome Research. Bioinform. Biol. Insights, 10.","DOI":"10.4137\/BBI.S34610"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.resmic.2013.12.002","article-title":"The Future of Skin Metagenomics","volume":"165","author":"Mathieu","year":"2014","journal-title":"Res. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Gao, Z., Tseng, C., Strober, B.E., Pei, Z., and Blaser, M.J. (2008). Substantial Alterations of the Cutaneous Bacterial Biota in Psoriatic Lesions. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0002719"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Van Den Bossche, T., Verschaffelt, P., Moortele, T.V., Dawyndt, P., Martens, L., and Mesuere, B. (2023). Biodiversity Analysis of Metaproteomics Samples with Unipept: A Comprehensive Tutorial. Protein Bioinformatics, Humana.","DOI":"10.1007\/978-1-0716-4007-4_11"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Kelly, D., Yang, L., and Pei, Z. (2017). A Review of the Oesophageal Microbiome in Health and Disease. Methods in Microbiology, Academic Press Inc.","DOI":"10.1016\/bs.mim.2017.08.001"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1038\/nrmicro3451","article-title":"Sequencing and beyond: Integrating Molecular \u201comics\u201d for Microbial Community Profiling","volume":"13","author":"Franzosa","year":"2015","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Ben\u00edtez-P\u00e1ez, A., Belda-Ferre, P., Sim\u00f3n-Soro, A., and Mira, A. (2014). Microbiota Diversity and Gene Expression Dynamics in Human Oral Biofilms. BMC Genom., 15.","DOI":"10.1186\/1471-2164-15-311"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"3409","DOI":"10.1002\/pmic.201500183","article-title":"A Decade of Metaproteomics: Where We Stand and What the Future Holds","volume":"15","author":"Wilmes","year":"2015","journal-title":"Proteomics"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"9407","DOI":"10.1021\/acs.analchem.7b02224","article-title":"Deep Metaproteomics Approach for the Study of Human Microbiomes","volume":"89","author":"Zhang","year":"2017","journal-title":"Anal. Chem."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.jbiotec.2017.06.1201","article-title":"Challenges and Perspectives of Metaproteomic Data Analysis","volume":"261","author":"Heyer","year":"2017","journal-title":"J. Biotechnol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Van Den Bossche, T., Arntzen, M.\u00d8., Becher, D., Benndorf, D., Eijsink, V.G.H., Henry, C., Jagtap, P.D., Jehmlich, N., Juste, C., and Kunath, B.J. (2021). The Metaproteomics Initiative: A Coordinated Approach for Propelling the Functional Characterization of Microbiomes. Microbiome, 9.","DOI":"10.1186\/s40168-021-01176-w"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1111\/1462-2920.16238","article-title":"Metaproteomics to Understand How Microbiota Function: The Crystal Ball Predicts a Promising Future","volume":"25","author":"Armengaud","year":"2023","journal-title":"Environ. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1016\/j.tim.2017.11.002","article-title":"Human Gut Microbiome: Function Matters","volume":"26","author":"Wilmes","year":"2018","journal-title":"Trends Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"4299","DOI":"10.1111\/1462-2920.16028","article-title":"Taxonomical and Functional Changes in COVID-19 Faecal Microbiome Could Be Related to SARS-CoV-2 Faecal Load","volume":"24","author":"Grenga","year":"2022","journal-title":"Environ. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"D795","DOI":"10.1093\/nar\/gkab786","article-title":"GutMGene: A Comprehensive Database for Target Genes of Gut Microbes and Microbial Metabolites","volume":"50","author":"Cheng","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3424","DOI":"10.1002\/pmic.201400571","article-title":"Microbial Metaproteomics for Characterizing the Range of Metabolic Functions and Activities of Human Gut Microbiota","volume":"15","author":"Xiong","year":"2015","journal-title":"Proteomics"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"3077","DOI":"10.1007\/s00253-017-8215-7","article-title":"Metaproteomic Strategies and Applications for Gut Microbial Research","volume":"101","author":"Xiao","year":"2017","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Aguiar-Pulido, V., Huang, W., Suarez-Ulloa, V., Cickovski, T., Mathee, K., and Narasimhan, G. (2016). Metagenomics, Metatranscriptomics, and Metabolomics Approaches for Microbiome Analysis. Evol. Bioinform., 12s1.","DOI":"10.4137\/EBO.S36436"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Kuehne, A., Hildebrand, J., Soehle, J., Wenck, H., Terstegen, L., Gallinat, S., Knott, A., Winnefeld, M., and Zamboni, N. (2017). An Integrative Metabolomics and Transcriptomics Study to Identify Metabolic Alterations in Aged Skin of Humans in Vivo. BMC Genom., 18.","DOI":"10.1186\/s12864-017-3547-3"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/gigascience\/gix087","article-title":"Lipidomics Profiling Reveals the Role of Glycerophospholipid Metabolism in Psoriasis","volume":"6","author":"Zeng","year":"2017","journal-title":"Gigascience"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1111\/exd.14796","article-title":"LC\u2013MS Metabolomics Reveal Skin Metabolic Signature of Psoriasis Vulgaris","volume":"32","author":"Xiong","year":"2023","journal-title":"Exp. Dermatol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1016\/j.chom.2019.03.006","article-title":"Strain- and Species-Level Variation in the Microbiome of Diabetic Wounds Is Associated with Clinical Outcomes and Therapeutic Efficacy","volume":"25","author":"Kalan","year":"2019","journal-title":"Cell Host Microbe"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"100315","DOI":"10.1016\/j.xjidi.2024.100315","article-title":"Advances in Microengineered Platforms for Skin Research","volume":"5","author":"Teertam","year":"2025","journal-title":"JID Innov."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Barros, N.R., Kang, R., Kim, J., Ermis, M., Kim, H.-J., Dokmeci, M.R., and Lee, J. (2025). A Human Skin-on-a-Chip Platform for Microneedling-Driven Skin Cancer Treatment. Mater. Today Bio, 30.","DOI":"10.1016\/j.mtbio.2024.101399"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2609","DOI":"10.1039\/D4LC01010H","article-title":"Gut Microbe\u2013Skin Axis on a Chip for Reproducing the Inflammatory Crosstalk","volume":"25","author":"Ko","year":"2025","journal-title":"Lab Chip"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1111\/j.1574-6968.2007.01021.x","article-title":"Microbial Colonization of an in Vitro Model of a Tissue Engineered Human Skin Equivalent--a Novel Approach","volume":"279","author":"Holland","year":"2008","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1111\/exd.14268","article-title":"Development and Characterization of a 3D in Vitro Model Mimicking Acneic Skin","volume":"30","author":"Laclaverie","year":"2021","journal-title":"Exp. Dermatol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"329","DOI":"10.5582\/ddt.2018.01079","article-title":"Models for Acne: A Comprehensive Study","volume":"12","author":"Kanwar","year":"2018","journal-title":"Drug Discov. Ther."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2152","DOI":"10.1038\/jid.2013.21","article-title":"Propionibacterium Acnes Strain Populations in the Human Skin Microbiome Associated with Acne","volume":"133","author":"Tomida","year":"2013","journal-title":"J. Investig. Dermatol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1111\/j.0906-6705.2005.0285a.x","article-title":"What Is the Pathogenesis of Acne?","volume":"14","author":"Zouboulis","year":"2005","journal-title":"Exp. Dermatol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"eaal4651","DOI":"10.1126\/scitranslmed.aal4651","article-title":"Staphylococcus Aureus and Staphylococcus Epidermidis Strain Diversity Underlying Pediatric Atopic Dermatitis","volume":"9","author":"Byrd","year":"2017","journal-title":"Sci. Transl. Med."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.coi.2020.02.007","article-title":"Recent Advances in Atopic Dermatitis","volume":"66","author":"Ahn","year":"2020","journal-title":"Curr. Opin. Immunol."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Wu, X., Zhao, Y., Gu, Y., Li, K., Wang, X., and Zhang, J. (2021). Interferon-Lambda 1 Inhibits Staphylococcus Aureus Colonization in Human Primary Keratinocytes. Front. Pharmacol., 12.","DOI":"10.3389\/fphar.2021.652302"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"105150","DOI":"10.1016\/j.isci.2022.105150","article-title":"Wnt-Activating Human Skin Organoid Model of Atopic Dermatitis Induced by Staphylococcus Aureus and Its Protective Effects by Cutibacterium Acnes","volume":"25","author":"Jung","year":"2022","journal-title":"iScience"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"131","DOI":"10.2340\/00015555-1382","article-title":"A Comprehensive Pathophysiology of Dandruff and Seborrheic Dermatitis\u2014Towards a More Precise Definition of Scalp Health","volume":"93","author":"Schwartz","year":"2013","journal-title":"Acta Derm. Venereol."},{"key":"ref_61","first-page":"125","article-title":"Seborrheic Dermatitis: An Overview","volume":"74","author":"Schwartz","year":"2006","journal-title":"Am. Fam. Physician"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1038\/sj.jidsymp.5650049","article-title":"Malassezia Globosa and Restricta: Breakthrough Understanding of the Etiology and Treatment of Dandruff and Seborrheic Dermatitis through Whole-Genome Analysis","volume":"12","author":"Dawson","year":"2007","journal-title":"J. Investig. Dermatol. Symp. Proc."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"763","DOI":"10.1007\/s00403-014-1479-1","article-title":"Analysis of the Response of Human Keratinocytes to Malassezia Globosa and Restricta Strains","volume":"306","author":"Donnarumma","year":"2014","journal-title":"Arch. Dermatol. Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1111\/ics.12688","article-title":"Reproducing the Scalp Microbiota Community: Co-Colonization of a 3D Reconstructed Human Epidermis with C. Acnes and M. Restricta","volume":"43","author":"Meloni","year":"2021","journal-title":"Int. J. Cosmet. Sci."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"2100138","DOI":"10.1002\/adtp.202100138","article-title":"Recent Progress in Skin-on-a-Chip Platforms","volume":"5","author":"Cui","year":"2022","journal-title":"Adv. Ther."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Fernandez-Carro, E., Remacha, A.R., Orera, I., Lattanzio, G., Garcia-Barrios, A., del Barrio, J., Alcaine, C., and Ciriza, J. (2024). Human Dermal Decellularized ECM Hydrogels as Scaffolds for 3D In Vitro Skin Aging Models. Int. J. Mol. Sci., 25.","DOI":"10.20944\/preprints202403.0458.v1"},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Risue\u00f1o, I., Valencia, L., Jorcano, J.L., and Velasco, D. (2021). Skin-on-a-Chip Models: General Overview and Future Perspectives. APL Bioeng., 5.","DOI":"10.1063\/5.0046376"},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Pontiggia, L., Klar, A.S., Michalak-Micka, K., Moehrlen, U., and Biedermann, T. (2024). Isolation, Characterization, and Utilization of Human Skin Basal and Suprabasal Epidermal Stem Cells. Skin Stem Cells, Humana.","DOI":"10.1007\/7651_2024_551"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1853","DOI":"10.1002\/bit.27320","article-title":"Microfluidic Skin Chip with Vasculature for Recapitulating the Immune Response of the Skin Tissue","volume":"117","author":"Kwak","year":"2020","journal-title":"Biotechnol. Bioeng."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Ogai, K., Nagase, S., Mukai, K., Iuchi, T., Mori, Y., Matsue, M., Sugitani, K., Sugama, J., and Okamoto, S. (2018). A Comparison of Techniques for Collecting Skin Microbiome Samples: Swabbing Versus Tape-Stripping. Front. Microbiol., 9.","DOI":"10.3389\/fmicb.2018.02362"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"101498","DOI":"10.1016\/j.berh.2020.101498","article-title":"Methods in Microbiome Research: Past, Present, and Future","volume":"33","author":"Gotschlich","year":"2019","journal-title":"Best. Pract. Res. Clin. Rheumatol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1110","DOI":"10.1111\/1346-8138.15536","article-title":"Skin Microbiota in Health and Disease: From Sequencing to Biology","volume":"47","author":"Ederveen","year":"2020","journal-title":"J. Dermatol."},{"key":"ref_73","first-page":"119","article-title":"Advances in Bacterial Identification and Characterization: Methods and Applications","volume":"2","year":"2019","journal-title":"Microbiol. Metab. Biotechnol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.jid.2020.04.023","article-title":"Perspective and Consensus Opinion: Good Practices for Using Organotypic Skin and Epidermal Equivalents in Experimental Dermatology Research","volume":"141","author":"Ilic","year":"2021","journal-title":"JID"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/8\/1771\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T18:18:17Z","timestamp":1760033897000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/8\/1771"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,7,29]]},"references-count":74,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2025,8]]}},"alternative-id":["microorganisms13081771"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms13081771","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,7,29]]}}}