Skin Microbiome Modulates the Effect of Ultraviolet Radiation on Cellular Response and Immune Function
Open accessAbstract
The skin is colonized by a diverse microbiome intricately involved in various molecular and cellular processes within the skin and beyond. UV radiation is known to induce profound changes in the skin and modulate the immune response. However, the role of the microbiome in UV-induced immune suppression has been overlooked. By employing the standard model of contact hypersensitivity (using germ-free mice) we found diminished UV-induced systemic immune suppression in the presence of microbiome. Upon UV exposure, we found enhanced epidermal hyperplasia and neutrophilic infiltration in the presence and enhanced numbers of mast cells and monocyte or macrophages in the absence of microbiome. Transcriptome analysis revealed a predominant expression of cytokine genes related to pro-inflammatory milieu in the presence versus immunosuppressive milieu (with increased interleukin-10) in the absence of microbiome. Collectively, microbiome abrogates the immunosuppressive response to UV by modulating gene expression and cellular microenvironment of the skin.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Ultraviolet radiation alters the composition and activity of skin microbiota and modulates cellular response and immunological function.
“Ultraviolet radiation has been shown to alter the composition and activity of the microbiota, as well as modulate cellular response and immunological function”
From Skin protection from solar ultraviolet radiation using natural compounds: a review (2024) · cites this paper as Patra et al. 2019
The Introduction and Results (page unavailable) report that UV-B changes skin gene expression, cellular responses, and immune function, with effects that differ depending on whether a skin microbiome is present. They do not show that UV alters the composition or activity of the skin microbiota; the study compares mice with and without microbiomes rather than measuring UV-induced changes in the microbes. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn a mouse model of contact hypersensitivity and germ-free mice, the skin microbiome inhibited ultraviolet-induced immune suppression.
“Furthermore, a recent study on mice model of contact hypersensitivity and germ-free reported that the skin microbiome inhibited ultraviolet-induced immune suppression (Patra et al. 2019).”
From Skin protection from solar ultraviolet radiation using natural compounds: a review (2024) · cites this paper as Patra et al. 2019
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
de Waal Malefyt, R., Abrams, J., Bennett, B., Figdor, C. G., & de Vries, J. E. (1991) · The Journal of experimental medicine · doi:10.1084/jem.174.5.1209 · Cited by 3,762 · see citing works
Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide
Lande, R., Gregorio, J., Facchinetti, V., Chatterjee, B., Wang, Y.-H., Homey, B., Cao, W., Wang, Y.-H., Su, B., Nestle, F. O., et al. (2007) · Nature · doi:10.1038/nature06116 · Cited by 1,910 · see citing works
Commensal bacteria regulate Toll-like receptor 3–dependent inflammation after skin injury
Lai, Y., Di Nardo, A., Nakatsuji, T., Leichtle, A., Yang, Y., Cogen, A. L., Wu, Z.-R., Hooper, L. V., Schmidt, R. R., von Aulock, S., et al. (2009) · Nature Medicine · doi:10.1038/nm.2062 · Cited by 781 · see citing works
The Inflammasome Mediates UVB-Induced Activation and Secretion of Interleukin-1β by Keratinocytes
Feldmeyer, L., Keller, M., Niklaus, G., Hohl, D., Werner, S., & Beer, H.-D. (2007) · Current Biology · doi:10.1016/j.cub.2007.05.074 · Cited by 544 · see citing works
Activation of the IL-1β-Processing Inflammasome Is Involved in Contact Hypersensitivity
Watanabe, H., Gaide, O., Pétrilli, V., Martinon, F., Contassot, E., Roques, S., Kummer, J. A., Tschopp, J., & French, L. E. (2007) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700819 · Cited by 416 · see citing works
Skin-Resident T Cells Sense Ultraviolet Radiation–Induced Injury and Contribute to DNA Repair
MacLeod, A. S., Rudolph, R., Corriden, R., Ye, I., Garijo, O., & Havran, W. L. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1303297 · Cited by 77 · see citing works
Patra, V., Laoubi, L., Nicolas, J.-F., Vocanson, M., & Wolf, P. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00166 · Cited by 42 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 42
- Belkaid Y. Segre J.A. Dialogue between skin microbiota and immunity Science 346 2014 954 959 25414304
- Canesso M.C. Vieira A.T. Castro T.B. Schirmer B.G. Cisalpino D. Martins F.S. Rachid M.A. Nicoli J.R. Teixeira M.M. Barcelos L.S. Skin wound healing is accelerated and scarless in the absence of commensal microbiota J. Immunol. 193 2014 5171 5180 25326026
- Cebra J.J. Influences of microbiota on intestinal immune system development Am. J. Clin. Nutr. 69 1999 1046S 1051S 10232647
- Chen Y.E. Fischbach M.A. Belkaid Y. Skin microbiota-host interactions Nature 553 2018 427 436 29364286 PMC6075667
- Dawes J.M. Calvo M. Perkins J.R. Paterson K.J. Kiesewetter H. Hobbs C. Kaan T.K. Orengo C. Bennett D.L. McMahon S.B. CXCL5 mediates UVB irradiation-induced pain Sci. Transl. Med. 3 2011 90ra60 PMC3232447 21734176
- Doring G. The role of neutrophil elastase in chronic inflammation Am. J. Respir. Crit. Care Med. 150 1994 S114 S117 7952645
- Eden E. Navon R. Steinfeld I. Lipson D. Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists BMC Bioinformatics 10 2009 48 19192299 PMC2644678
- Enk C.D. Sredni D. Blauvelt A. Katz S.I. Induction of IL-10 gene expression in human keratinocytes by UVB exposure in vivo and in vitro J. Immunol. 154 1995 4851 4856 7722334
- Fisher M.S. Kripke M.L. Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis Proc. Natl. Acad. Sci. U S A 74 1977 1688 1692 300876 PMC430858
- Fourtanier A. Moyal D. Maccario J. Compan D. Wolf P. Quehenberger F. Cooper K. Baron E. Halliday G. Poon T. Measurement of sunscreen immune protection factors in humans: a consensus paper J. Invest. Dermatol. 125 2005 403 409 16117779
- Gallo R.L. Hooper L.V. Epithelial antimicrobial defence of the skin and intestine Nat. Rev. Immunol. 12 2012 503 516 22728527 PMC3563335
- Ghaly S. Kaakoush N.O. Lloyd F. Gordon L. Forest C. Lawrance I.C. Hart P.H. Ultraviolet Irradiation of skin alters the faecal microbiome independently of vitamin D in mice Nutrients 10 2018 1069 PMC6116187 30103486
- Glaser R. Navid F. Schuller W. Jantschitsch C. Harder J. Schroder J.M. Schwarz A. Schwarz T. UV-B radiation induces the expression of antimicrobial peptides in human keratinocytes in vitro and in vivo J. Allergy Clin. Immunol. 123 2009 1117 1123 19342087
- Harrison O.J. Linehan J.L. Shih H.Y. Bouladoux N. Han S.J. Smelkinson M. Sen S.K. Byrd A.L. Enamorado M. Yao C. Commensal-specific T cell plasticity promotes rapid tissue adaptation to injury Science 363 2019 eaat6280 30523076 PMC7304459
- Horton J.M. Gao Z. Sullivan D.M. Shopsin B. Perez-Perez G.I. Blaser M.J. The cutaneous microbiome in outpatients presenting with acute skin abscesses J. Infect. Dis. 211 2015 1895 1904 25583170 PMC4539909
- Jung E.S. Park H.M. Hyun S.M. Shon J.C. Singh D. Liu K.H. Whon T.W. Bae J.W. Hwang J.S. Lee C.H. The green tea modulates large intestinal microbiome and exo/endogenous metabolome altered through chronic UVB-exposure PLoS One 12 2017 e0187154 29117187 PMC5695601
- Kang K. Hammerberg C. Meunier L. Cooper K.D. CD11b+ macrophages that infiltrate human epidermis after in vivo ultraviolet exposure potently produce IL-10 and represent the major secretory source of epidermal IL-10 protein J. Immunol. 153 1994 5256 5264 7963579
- Kelly D.A. Young A.R. McGregor J.M. Seed P.T. Potten C.S. Walker S.L. Sensitivity to sunburn is associated with susceptibility to ultraviolet radiation–induced suppression of cutaneous cell–mediated immunity J. Exp. Med. 191 2000 561 566 10662801 PMC2195812
- Kolter J. Feuerstein R. Spoeri E. Gharun K. Elling R. Trieu-Cuot P. Goldmann T. Waskow C. Chen Z.J. Kirschning C.J. Streptococci engage TLR13 on myeloid cells in a site-specific fashion J. Immunol. 196 2016 2733 2741 26873993
- Kramer A. Green J. Pollard J. Jr. Tugendreich S. Causal analysis approaches in ingenuity pathway analysis Bioinformatics 30 2014 523 530 24336805 PMC3928520
- Lehtimaki S. Tillander S. Puustinen A. Matikainen S. Nyman T. Fyhrquist N. Savinko T. Majuri M.L. Wolff H. Alenius H. Absence of CCR4 exacerbates skin inflammation in an oxazolone-induced contact hypersensitivity model J. Invest. Dermatol. 130 2010 2743 2751 20631725
- Liu X. Huang H. Gao H. Wu X. Zhang W. Yu B. Dou X. Regulatory B cells induced by ultraviolet B through toll-like receptor 4 signalling contribute to the suppression of contact hypersensitivity responses in mice Contact Dermatitis 78 2018 117 130 29205369
- Maeda A. Beissert S. Schwarz T. Schwarz A. Phenotypic and functional characterization of ultraviolet radiation-induced regulatory T cells J. Immunol. 180 2008 3065 3071 18292529
- Meisel J.S. Sfyroera G. Bartow-McKenney C. Gimblet C. Bugayev J. Horwinski J. Kim B. Brestoff J.R. Tyldsley A.S. Zheng Q. Commensal microbiota modulate gene expression in the skin Microbiome 6 2018 20 29378633 PMC5789709
- Myles I.A. Fontecilla N.M. Valdez P.A. Vithayathil P.J. Naik S. Belkaid Y. Ouyang W. Datta S.K. Signaling via the IL-20 receptor inhibits cutaneous production of IL-1beta and IL-17A to promote infection with methicillin-resistant Staphylococcus aureus Nat. Immunol. 14 2013 804 811 23793061 PMC3721434
- Naik S. Bouladoux N. Linehan J.L. Han S.J. Harrison O.J. Wilhelm C. Conlan S. Himmelfarb S. Byrd A.L. Deming C. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature Nature 520 2015 104 108 25539086 PMC4667810
- Naik S. Bouladoux N. Wilhelm C. Molloy M.J. Salcedo R. Kastenmuller W. Deming C. Quinones M. Koo L. Conlan S. Compartmentalized control of skin immunity by resident commensals Science 337 2012 1115 1119 22837383 PMC3513834
- Nakaguma H. Kambara T. Yamamoto T. Rat ultraviolet ray B photodermatitis: an experimental model of psoriasis vulgaris Int. J. Exp. Pathol. 76 1995 65 73 7734340 PMC1997141
- Nakatsuji T. Chen T.H. Butcher A.M. Trzoss L.L. Nam S.J. Shirakawa K.T. Zhou W. Oh J. Otto M. Fenical W. A commensal strain of Staphylococcus epidermidis protects against skin neoplasia Sci. Adv. 4 2018 eaao4502 29507878 PMC5834004
- O'Neill C.A. Monteleone G. McLaughlin J.T. Paus R. The gut-skin axis in health and disease: a paradigm with therapeutic implications Bioessays 38 2016 1167 1176 27554239
- Patra V. Byrne S.N. Wolf P. The skin microbiome: is it affected by UV-induced immune suppression? Front. Microbiol. 7 2016 1235 27559331 PMC4979252
- Ridaura V.K. Bouladoux N. Claesen J. Chen Y.E. Byrd A.L. Constantinides M.G. Merrill E.D. Tamoutounour S. Fischbach M.A. Belkaid Y. Contextual control of skin immunity and inflammation by Corynebacterium J. Exp. Med. 215 2018 785 799 29382696 PMC5839758
- Schwarz T. The dark and the sunny sides of UVR-induced immunosuppression: photoimmunology revisited J. Invest. Dermatol. 130 2010 49 54 19626036
- Sells R.E. Hwang S.T. Paradoxical increase in skin inflammation in the absence of CCR4 J. Invest. Dermatol. 130 2010 2697 2699 21068732
- Sesto A. Navarro M. Burslem F. Jorcano J.L. Analysis of the ultraviolet B response in primary human keratinocytes using oligonucleotide microarrays Proc. Natl. Acad. Sci. U S A 99 2002 2965 2970 11867738 PMC122456
- Shen Y. Kim A.L. Du R. Liu L. Transcriptome analysis identifies the dysregulation of ultraviolet target genes in human skin cancers PLoS One 11 2016 e0163054 27643989 PMC5028058
- Supek F. Bosnjak M. Skunca N. Smuc T. REVIGO summarizes and visualizes long lists of gene ontology terms PLoS One 6 2011 e21800 21789182 PMC3138752
- Warde-Farley D. Donaldson S.L. Comes O. Zuberi K. Badrawi R. Chao P. Franz M. Grouios C. Kazi F. Lopes C.T. The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function Nucleic Acids Res. 38 2010 W214 W220 20576703 PMC2896186
- Willis C.R. Seamons A. Maxwell J. Treuting P.M. Nelson L. Chen G. Phelps S. Smith C.L. Brabb T. Iritani B.M. Interleukin-7 receptor blockade suppresses adaptive and innate inflammatory responses in experimental colitis J. Inflamm. (Lond.) 9 2012 39 23057802 PMC3551718
- Wolf P. Byrne S.N. Limon-Flores A.Y. Hoefler G. Ullrich S.E. Serotonin signalling is crucial in the induction of PUVA-induced systemic suppression of delayed-type hypersensitivity but not local apoptosis or inflammation of the skin Exp. Dermatol. 25 2016 537 543 26914366 PMC4927393
- Wolf P. Weger W. Patra V. Gruber-Wackernagel A. Byrne S.N. Desired response to phototherapy vs photoaggravation in psoriasis: what makes the difference? Exp. Dermatol. 25 2016 937 944 27376966
- Zeeuwen P.L. Kleerebezem M. Timmerman H.M. Schalkwijk J. Microbiome and skin diseases Curr. Opin. Allergy Clin. Immunol. 13 2013 514 520 23974680
Cited by
Sorted by citations
Neale, R. E., Barnes, P. W., Robson, T. M., Neale, P. J., Williamson, C. E., Zepp, R. G., Wilson, S. R., Madronich, S., Andrady, A. L., Heikkilä, A. M., et al. (2021) · Photochemical & Photobiological Sciences · doi:10.1007/s43630-020-00001-x · Cited by 225 · see citing works
Skin protection from solar ultraviolet radiation using natural compounds: a review
Verma, A., Zanoletti, A., Kareem, K. Y., Adelodun, B., Kumar, P., Ajibade, F. O., Silva, L. F. O., Phillips, A. J., Kartheeswaran, T., Bontempi, E., et al. (2024) · Environmental Chemistry Letters · doi:10.1007/s10311-023-01649-4 · Cited by 102 · see citing works
- Authors
- Patra, V., Wagner, K., Arulampalam, V., & Wolf, P.
- Affiliations
- Medical University of Graz (AT)
- Karolinska Institutet (SE)
- Corresponding author
- Wolf, Peter
- Venue
- iScience
- Publisher
- Elsevier BV
- Published
- 2019-05
- Volume
- 15
- Pages
- 211-222
- ISSN
- 2589-0042 (ISSN-L)
- PMC
- PMC6515114
- OpenAlex
- W2940791687
- Cited by
- 99
- References
- 7
- Citations by year
- 2026: 13 · 2025: 18 · 2024: 11 · 2023: 13 · 2022: 13 · 2021: 12 · 2020: 13 · 2019: 5 · 2018: 1
- FWCI
- 10.84
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- iScience (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Austrian Science Fund
- Topics
- Health Sciences › Medicine › Dermatology › Dermatology and Skin Diseases
- Health Sciences › Medicine › Dermatology › Skin Protection and Aging
- Health Sciences › Medicine › Dermatology › Contact Dermatitis and Allergies
- Keywords
- skin microbiome, ultraviolet radiation, contact hypersensitivity, germ-free mice, epidermal hyperplasia, neutrophil infiltration, mast cells, monocytes/macrophages, cytokine gene expression, IL-10, pro-inflammatory response, skin transcriptome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
