Background: A previous in vivo study analysing the volatilome—the complete set of volatile organic compounds (VOCs) emitted by an organism—identified 17 compounds that were increasingly released by the skin during psychological stress. Objective: As stress is known to accelerate skin ageing, and many VOCs have detrimental effects on the skin, we selected three of the 17 identified VOCs and assessed their effects following a single exposure to physiological doses. Materials and methods: Using reconstructed human epidermis, we focused on changes in the expression of genes and proteins related to inflammation, epidermal differentiation, and oxidative stress. Results: Each of the three VOCs induces changes in gene and protein expression. Two VOCs, heptadecane and 2,6,10,14-tetramethylpentadecane, induce inflammation and affect epidermal differentiation, although the specific markers influenced and the timing of these changes differ between the two compounds. The third VOC, 2-hydroxyethyl acetate, inhibits inflammation but increases the expression of genes and proteins involved in epidermal differentiation and oxidative stress defence. Conclusion: While each VOC has distinct effects, all impact functions critical to the proper functioning of the skin. These findings suggest that stress-modulated skin VOCs could be a, yet, unsuspected factor linking the brain and the skin and impacting skin functions.
References
[1]
Cumeras, R. (2017) Volatilome Metabolomics and Databases, Recent Advances and Needs. CurrentMetabolomics, 5, 79-89. https://doi.org/10.2174/2213235x05666170502103408
[2]
Amann, A., Costello, B.d.L., Miekisch, W., Schubert, J., Buszewski, B., Pleil, J., et al. (2014) The Human Volatilome: Volatile Organic Compounds (VOCs) in Exhaled Breath, Skin Emanations, Urine, Feces and Saliva. JournalofBreathResearch, 8, Article ID: 034001. https://doi.org/10.1088/1752-7155/8/3/034001
[3]
Drabińska, N., Flynn, C., Ratcliffe, N., Belluomo, I., Myridakis, A., Gould, O., et al. (2021) A Literature Survey of All Volatiles from Healthy Human Breath and Bodily Fluids: The Human Volatilome. JournalofBreathResearch, 15, Article ID: 034001. https://doi.org/10.1088/1752-7163/abf1d0
[4]
Gallagher, M., Wysocki, C.J., Leyden, J.J., Spielman, A.I., Sun, X. and Preti, G. (2008) Analyses of Volatile Organic Compounds from Human Skin. BritishJournalofDermatology, 159, 780-791. https://doi.org/10.1111/j.1365-2133.2008.08748.x
[5]
Havlíček, J., Fialová, J. and Roberts, S.C. (2017) Individual Variation in Body Odor. In: Buettner, A., Ed., SpringerHandbookofOdor, Springer, 125-126. https://doi.org/10.1007/978-3-319-26932-0_50
[6]
Sato, S., Sekine, Y., Kakumu, Y. and Hiramoto, T. (2020) Measurement of Diallyl Disulfide and Allyl Methyl Sulfide Emanating from Human Skin Surface and Influence of Ingestion of Grilled Garlic. ScientificReports, 10, Article No. 465. https://doi.org/10.1038/s41598-019-57258-1
[7]
Delgado-Povedano, M.M., Calderón-Santiago, M., Luque de Castro, M.D. and Priego-Capote, F. (2018) Metabolomics Analysis of Human Sweat Collected after Moderate Exercise. Talanta, 177, 47-65. https://doi.org/10.1016/j.talanta.2017.09.028
[8]
Duffy, E. and Morrin, A. (2019) Endogenous and Microbial Volatile Organic Compounds in Cutaneous Health and Disease. TrACTrendsinAnalyticalChemistry, 111, 163-172. https://doi.org/10.1016/j.trac.2018.12.012
[9]
Zhang, Z., Cai, J., Ruan, G. and Li, G. (2005) The Study of Fingerprint Characteristics of the Emanations from Human Arm Skin Using the Original Sampling System by SPME-GC/MS. JournalofChromatographyB, 822, 244-252. https://doi.org/10.1016/j.jchromb.2005.06.026
[10]
Duffy, E., Albero, G. and Morrin, A. (2018) Headspace Solid-Phase Microextraction Gas Chromatography-Mass Spectrometry Analysis of Scent Profiles from Human Skin. Cosmetics, 5, Article 62. https://doi.org/10.3390/cosmetics5040062
[11]
Sharma, A., Kumar, R. and Varadwaj, P. (2023) Smelling the Disease: Diagnostic Potential of Breath Analysis. MolecularDiagnosis&Therapy, 27, 321-347. https://doi.org/10.1007/s40291-023-00640-7
[12]
Moura, P.C., Raposo, M. and Vassilenko, V. (2023) Breath Volatile Organic Compounds (VOCs) as Biomarkers for the Diagnosis of Pathological Conditions: A Review. BiomedicalJournal, 46, Article ID: 100623. https://doi.org/10.1016/j.bj.2023.100623
[13]
Mitra, A., Choi, S., Boshier, P.R., Razumovskaya-Hough, A., Belluomo, I., Spanel, P., et al. (2022) The Human Skin Volatolome: A Systematic Review of Untargeted Mass Spectrometry Analysis. Metabolites, 12, Article 824. https://doi.org/10.3390/metabo12090824
[14]
Martin, H.J., Turner, M.A., Bandelow, S., Edwards, L., Riazanskaia, S. and Thomas, C.L.P. (2016) Volatile Organic Compound Markers of Psychological Stress in Skin: A Pilot Study. JournalofBreathResearch, 10, Article ID: 046012. https://doi.org/10.1088/1752-7155/10/4/046012
[15]
Tsukuda, M., Nishiyama, Y., Kawai, S. and Okumura, Y. (2019) Identifying Stress Markers in Skin Gases by Analysing Gas Collected from Subjects Undergoing the Trier Social Stress Test and Performing Statistical Analysis. JournalofBreathResearch, 13, Article ID: 036003. https://doi.org/10.1088/1752-7163/ab0903
[16]
Durán Acevedo, C.M., Carrillo Gómez, J.K. and Albarracín Rojas, C.A. (2021) Academic Stress Detection on University Students during COVID-19 Outbreak by Using an Electronic Nose and the Galvanic Skin Response. BiomedicalSignalProcessingandControl, 68, Article ID: 102756. https://doi.org/10.1016/j.bspc.2021.102756
[17]
Lucchi, G., Crépin, M., Chambaron, S., Peltier, C., Gilbert, L., Guéré, C., et al. (2024) Effects of Psychological Stress on the Emission of Volatile Organic Compounds from the Skin. ScientificReports, 14, Article No. 7238. https://doi.org/10.1038/s41598-024-57967-2
[18]
Chen, Y. and Lyga, J. (2014) Brain-Skin Connection: Stress, Inflammation and Skin Aging. Inflammation&Allergy-DrugTargets, 13, 177-190. https://doi.org/10.2174/1871528113666140522104422
[19]
Saif, G.A.B., Alotaibi, H.M., Alzolibani, A.A., Almodihesh, N.A., Albraidi, H.F., Alotaibi, N.M., et al. (2018) Association of Psychological Stress with Skin Symptoms among Medical Students. SaudiMedicalJournal, 39, 59-66. https://doi.org/10.15537/smj.2018.1.21231
[20]
Zhang, H., Wang, M., Zhao, X., Wang, Y., Chen, X. and Su, J. (2024) Role of Stress in Skin Diseases: A Neuroendocrine-Immune Interaction View. Brain, Behavior, andImmunity, 116, 286-302. https://doi.org/10.1016/j.bbi.2023.12.005
[21]
Anwar, S.S., Apolinar, M.A. and Ma, L. (2023) Perception, Understanding, and Association between Psychological Stress and Skin Aging: Quantitative Surveys of Asian Women Aged 18-34 Years, Dermatologists, and Psychologists in China and Japan. JournalofCosmeticDermatology, 22, 2297-2307. https://doi.org/10.1111/jocd.15732
[22]
Garg, A., Chren, M., Sands, L.P., Matsui, M.S., Marenus, K.D., Feingold, K.R., et al. (2001) Psychological Stress Perturbs Epidermal Permeability Barrier Homeostasis: Implications for the Pathogenesis of Stress-Associated Skin Disorders. ArchivesofDermatology, 137, 53-59. https://doi.org/10.1001/archderm.137.1.53
[23]
Choi, E., Brown, B.E., Crumrine, D., Chang, S., Man, M., Elias, P.M., et al. (2005) Mechanisms by Which Psychologic Stress Alters Cutaneous Permeability Barrier Homeostasis and Stratum Corneum Integrity. JournalofInvestigativeDermatology, 124, 587-595. https://doi.org/10.1111/j.0022-202x.2005.23589.x
[24]
Aberg, K.M., Radek, K.A., Choi, E., Kim, D., Demerjian, M., Hupe, M., et al. (2007) Psychological Stress Downregulates Epidermal Antimicrobial Peptide Expression and Increases Severity of Cutaneous Infections in Mice. JournalofClinicalInvestigation, 117, 3339-3349. https://doi.org/10.1172/jci31726
[25]
Kleyn, C.E., Schneider, L., Saraceno, R., Mantovani, C., Richards, H.L., Fortune, D.G., et al. (2008) The Effects of Acute Social Stress on Epidermal Langerhans’ Cell Frequency and Expression of Cutaneous Neuropeptides. JournalofInvestigativeDermatology, 128, 1273-1279. https://doi.org/10.1038/sj.jid.5701144
[26]
Dhabhar, F.S. (2009) Enhancing versus Suppressive Effects of Stress on Immune Function: Implications for Immunoprotection and Immunopathology. Neuroimmunomodulation, 16, 300-317. https://doi.org/10.1159/000216188
[27]
Herman, J.P. (2013) Neural Control of Chronic Stress Adaptation. FrontiersinBehavioralNeuroscience, 7, Article 61. https://doi.org/10.3389/fnbeh.2013.00061
[28]
Parrado, C., Mercado-Saenz, S., Perez-Davo, A., Gilaberte, Y., Gonzalez, S. and Juarranz, A. (2019) Environmental Stressors on Skin Aging. Mechanistic Insights. FrontiersinPharmacology, 10, Article 759. https://doi.org/10.3389/fphar.2019.00759
[29]
Krutmann, J., Schikowski, T., Morita, A. and Berneburg, M. (2021) Environmentally-induced (Extrinsic) Skin Aging: Exposomal Factors and Underlying Mechanisms. JournalofInvestigativeDermatology, 141, 1096-1103. https://doi.org/10.1016/j.jid.2020.12.011
[30]
Ishitsuka, Y. and Roop, D.R. (2020) Loricrin: Past, Present, and Future. InternationalJournalofMolecularSciences, 21, Article 2271. https://doi.org/10.3390/ijms21072271
[31]
Kim, Y. and Lim, K.M. (2021) Skin Barrier Dysfunction and Filaggrin. Archives of Pharmacal Research, 44, 36-48.
[32]
Rawlings, A.V. and Harding, C.R. (2004) Moisturization and Skin Barrier Function. DermatologicTherapy, 17, 43-48. https://doi.org/10.1111/j.1396-0296.2004.04s1005.x
[33]
Wood, L.C., Feingold, K.R., Sequeira‐Martin, S.M., Elias, P.M. and Grunfeld, C. (1994) Barrier Function Coordinately Regulates Epidermal IL-1 and IL-1 Receptor Antagonist mRNA Levels. ExperimentalDermatology, 3, 56-60. https://doi.org/10.1111/j.1600-0625.1994.tb00047.x
[34]
Wood, L.C., Elias, P.M., Calhoun, C., Tsai, J.C., Grunfeld, C. and Feingold, K.R. (1996) Barrier Disruption Stimulates Interleukin-1α Expression and Release from a Pre-Formed Pool in Murine Epidermis. JournalofInvestigativeDermatology, 106, 397-403. https://doi.org/10.1111/1523-1747.ep12343392
[35]
Bollag, W.B., Aitkens, L., White, J. and Hyndman, K.A. (2020) Aquaporin-3 in the Epidermis: More than Skin Deep. AmericanJournalofPhysiology-CellPhysiology, 318, C1144-C1153. https://doi.org/10.1152/ajpcell.00075.2020
[36]
Miao, L. and St. Clair, D.K. (2009) Regulation of Superoxide Dismutase Genes: Implications in Disease. FreeRadicalBiologyandMedicine, 47, 344-356. https://doi.org/10.1016/j.freeradbiomed.2009.05.018
[37]
Glorieux, C., Zamocky, M., Sandoval, J.M., Verrax, J. and Calderon, P.B. (2015) Regulation of Catalase Expression in Healthy and Cancerous Cells. FreeRadicalBiologyandMedicine, 87, 84-97. https://doi.org/10.1016/j.freeradbiomed.2015.06.017
[38]
Altobelli, G.G., Van Noorden, S., Balato, A. and Cimini, V. (2020) Copper/Zinc Superoxide Dismutase in Human Skin: Current Knowledge. FrontiersinMedicine, 7, Article 183. https://doi.org/10.3389/fmed.2020.00183
[39]
Dorr, M.M., Favre-Mercuret, M., Vié, K. and Fitoussi, R. (2024) Effects of B[a]P-UVA Co-Exposure on Epigenetic Marks of Isolated Skin Cells and Impact of an Arundodonax L. Extract of These Changes. JournalofCosmetics, DermatologicalSciencesandApplications, 14, 253-269. https://doi.org/10.4236/jcdsa.2024.143017
[40]
Nakai, K. and Tsuruta, D. (2021) What Are Reactive Oxygen Species, Free Radicals, and Oxidative Stress in Skin Diseases? InternationalJournalofMolecularSciences, 22, Article 10799. https://doi.org/10.3390/ijms221910799
