medsovetМедицинский СоветMeditsinskiy sovet = Medical Council2079-701X2658-5790REMEDIUM GROUP Ltd.10.21518/2079-701X-2019-17-168-176medsovet-4739Research ArticleДЕРМАТОЛОГИЯDERMATOLOGYМикробиом кожи: что нам известно сегодня?Skin microbiome: What is known today?https://orcid.org/0000-0003-4200-4598ЗахароваИ. Н.ZakharovaI. N.

Захарова Ирина Николаевна, доктор медицинских наук, профессор, заслуженный врач России, заведующая кафедрой педиатрии с курсом поликлинической педиатрии им. Г.Н. Сперанского

125993, Москва, ул. Баррикадная, д. 2/1, стр. 1

Irina N. Zakharova, Dr. of Sci. (Med), Professor, Honored Doctor of Russia, Head of the Department of Pediatrics with the course of polyclinic pediatrics named after G.N. Speransky

1, 2/1 Barrikadnaya St., Moscow 125993

kafedra25@yandex.ruhttps://orcid.org/0000-0002-9524-8724КасьяноваА. Н.Kas’yanovaA. N.

Касьянова Анна Николаевна, ассистент кафедры факультетской педиатрии

355017, Ставрополь, ул. Мира, д. 310

Anna N. Kas’yanova, Assistant of the Department of Pediatrics

310 Mira str., Stavropol, 355017

a.nicolaevnakasjanova@yandex.ruРоссийская медицинская академия непрерывного профессионального образованияРоссияRussian Medical Academy of Continuing Professional EducationRussian FederationСтавропольский государственный медицинский университетРоссияStavropol State Medical UniversityRussian Federation201924112019017168176Copyright © Захарова И.Н., Касьянова А.Н., 20192019Захарова И.Н., Касьянова А.Н.Zakharova I.N., Kas’yanova A.N.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.med-sovet.pro/jour/article/view/4739

Кожа человека представляет собой самый большой и в то же время сложный орган, который выполняет множество функций. Кожный барьер имеет решающее значение для выживания, предотвращая потерю влаги и проникновение инфекционных или токсических веществ. Кожа также является сложной средой обитания для разнообразных популяций микробиоты. Во время родов и последующего воздействия постнатальной среды кожа колонизируется множеством микробов, многие из которых являются комменсальными или симбиотическими. Полезные функции резидентной микробиоты включают ингибирование патогенных видов за счет различных механизмов, которые изучаются активным образом. В современных исследованиях все больше внимания уделяется изучению роли микробиома организма человека, включая микробиом кожи, в развитии ряда патологических заболеваний, как дерматологических, так и аллергических и инфекционных. Благодаря все более широкому распространению метода секвенирования гена 16S рРНК бактерий с каждым годом появляется все больше сведений о микробном составе различных систем организма, включая кожу. В обзоре представлены современные данные о составе здорового микробиома кожи, о его изменении на протяжении жизни человека, продемонстрированы некоторые механизмы его влияния на здоровье кожи и организма в целом. Отдельное внимание уделено понятию экологических ниш кожи, их особенностям и уникальному микробному составу. Также проанализирована роль нарушения состава микробиома в развитии ряда хронических воспалительных заболеваний кожи, включая атопический дерматит, псориаз и акне.

Human skin is the largest yet complex organ that performs many functions. The skin barrier is crucial for survival, preventing moisture loss and the entry of infectious or toxic substances. Skin is also a complex habitat for a diverse population of microbiota. During childbirth and subsequent exposure to the postnatal environment, the skin is colonized by many microbes, many of which are commensal or symbiotic. The useful functions of the resident microbiota include inhibition of pathogenic species through various mechanisms that are actively studied. Modern research is increasingly focused on the role of human microbiomes, including skin microbioms, in the development of a range of pathological diseases, including dermatological, allergic and infectious diseases. Due to the growing spread of the 16S rRNA bacteria gene sequencing method, more and more information on the microbial composition of various body systems, including the skin, is becoming available every year. The review presents current data on the composition of a healthy skin microbiome and its changes over the course of human’s life, and demonstrates some mechanisms of its effect on the health of the skin and the body as a whole. Special attention is paid to the concept of ecological niches of skin, their peculiarities and unique microbial composition. The role of microbiomal abnormalities in the development of a number of chronic inflammatory skin diseases, including atopic dermatitis, psoriasis and acne, was also analyzed.

микробиомкожавироматопический дерматитпсориазпробиотикилизатыдетиmicrobiomeskinviromeatopic dermatitispsoriasisprobioticslysateschildrenReferencesSender R., Fuchs S., Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14(8):e1002533. doi: 10.1371/journal.pbio.1002533.Sender R., Fuchs S., Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14(8):e1002533. doi: 10.1371/journal.pbio.1002533.Grice E.A., Kong H.H., Renaud G., Young A.C., NISC Comparative Sequencing Program, Bouffard G.G., Blakesley R.W., Wolfsberg T.G., Turner M.L., Segre J.A. A diversity profile of the human skin microbiota. Genome Res. 2008;18(7):1043-1050. doi: 10.1101/gr.075549.107.Grice E.A., Kong H.H., Renaud G., Young A.C., NISC Comparative Sequencing Program, Bouffard G.G., Blakesley R.W., Wolfsberg T.G., Turner M.L., Segre J.A. A diversity profile of the human skin microbiota. Genome Res. 2008;18(7):1043-1050. doi: 10.1101/gr.075549.107.Dominguez-Bello M.G., Costello E.K., Contreras M., Magris M., Hidalgo G., Fierer N., Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 2010;107(26):11971-11975. doi: 10.1073/pnas.1002601107.Dominguez-Bello M.G., Costello E.K., Contreras M., Magris M., Hidalgo G., Fierer N., Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 2010;107(26):11971-11975. doi: 10.1073/pnas.1002601107.Capone K.A., Dowd S.E., Stamatas G.N., Nikolovski J. Diversity of the human skin microbiome early in life. J Invest Dermatol. 2011;131(10):2026-2032. doi: 10.1038/jid.2011.168.Capone K.A., Dowd S.E., Stamatas G.N., Nikolovski J. Diversity of the human skin microbiome early in life. J Invest Dermatol. 2011;131(10):2026-2032. doi: 10.1038/jid.2011.168.Giacomoni P.U., Mammone T., Teri M. Genderlinked differences in human skin. J Dermatol Sci. 2009;55(3):144-149. doi: 10.1016/j.jdermsci.2009.06.001.Giacomoni P.U., Mammone T., Teri M. Genderlinked differences in human skin. J Dermatol Sci. 2009;55(3):144-149. doi: 10.1016/j.jdermsci.2009.06.001.Sander M.A., Sander M.S., Isaac-Renton J.L., Croxen M.A. The Cutaneous Microbiome: Implications for Dermatology Practice. J Cutan Med Surg. 2019:23(4):436-441. doi: 10.1177/1203475419839939.Sander M.A., Sander M.S., Isaac-Renton J.L., Croxen M.A. The Cutaneous Microbiome: Implications for Dermatology Practice. J Cutan Med Surg. 2019:23(4):436-441. doi: 10.1177/1203475419839939.Pammi M., O’Brien J.L., Ajami N.J., Wong M.C., Versalovic J., Petrosino J.F. Development of the cutaneous microbiome in the preterm infant: A prospective longitudinalstudy. PLoS One. 2017;12(4):e0176669. doi: 10.1371/journal.pone.0176669.Pammi M., O’Brien J.L., Ajami N.J., Wong M.C., Versalovic J., Petrosino J.F. Development of the cutaneous microbiome in the preterm infant: A prospective longitudinalstudy. PLoS One. 2017;12(4):e0176669. doi: 10.1371/journal.pone.0176669.Grice E.A., Segre J.A. The skin microbiome. Nat Rev Microbiol. 2011;(9):244-253. doi: 10.1038/nrmicro2537.Grice E.A., Segre J.A. The skin microbiome. Nat Rev Microbiol. 2011;(9):244-253. doi: 10.1038/nrmicro2537.Gao Z., Tseng C.H., Pei Z., Blaser M.J.Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci USA. 2007;(104):29272932. doi: 10.1073/pnas.0607077104.Gao Z., Tseng C.H., Pei Z., Blaser M.J.Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci USA. 2007;(104):29272932. doi: 10.1073/pnas.0607077104.Capone K.A., Dowd S.E., Stamatas G.N., Nikolovski J. Diversity of the human skin microbiome early in life. J Invest Dermatol. 2011;131(10):2026-2032. doi: 10.1038/jid.2011.168.Capone K.A., Dowd S.E., Stamatas G.N., Nikolovski J. Diversity of the human skin microbiome early in life. J Invest Dermatol. 2011;131(10):2026-2032. doi: 10.1038/jid.2011.168.Grice E.A., Kong H.H., Conlan S., Deming C.B., Davis J., Young A.C.; NISC Comparative Sequencing Program, Bouffard G.G., Blakesley R.W., Murray P.R., Green E.D., Turner M.L., Segre J.A. Topographical and temporal diversity of the human skin microbiome. Science. 2009;324(5931): 1190-1192. doi: 10.1126/science.1171700.Grice E.A., Kong H.H., Conlan S., Deming C.B., Davis J., Young A.C.; NISC Comparative Sequencing Program, Bouffard G.G., Blakesley R.W., Murray P.R., Green E.D., Turner M.L., Segre J.A. Topographical and temporal diversity of the human skin microbiome. Science. 2009;324(5931): 1190-1192. doi: 10.1126/science.1171700.Costello E.K., Lauber C.L., Hamady M., Fierer N., Gordon J.I., Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694-1697. doi: 10.1126/science.1177486.Costello E.K., Lauber C.L., Hamady M., Fierer N., Gordon J.I., Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694-1697. doi: 10.1126/science.1177486.Jo J.H., Kennedy E.A., Kong H.H. Topographical and physiological differences of the skin mycobiome in health and disease. Virulence. 2017;8(3):324-333. doi: 10.1080/21505594.2016.1249093.Jo J.H., Kennedy E.A., Kong H.H. Topographical and physiological differences of the skin mycobiome in health and disease. Virulence. 2017;8(3):324-333. doi: 10.1080/21505594.2016.1249093.Jo J.H., Deming C., Kennedy E.A., Conlan S., Polley E.C., Ng W.I.; NISC Comparative Sequencing Program, Segre J.A., Kong H.H. Diverse human skin fungal communities in children converge in adulthood. J Invest Dermatol. 2016;136(12):2356-2363. doi: 10.1016/j.jid.2016.05.130.Jo J.H., Deming C., Kennedy E.A., Conlan S., Polley E.C., Ng W.I.; NISC Comparative Sequencing Program, Segre J.A., Kong H.H. Diverse human skin fungal communities in children converge in adulthood. J Invest Dermatol. 2016;136(12):2356-2363. doi: 10.1016/j.jid.2016.05.130.Fierer N., Hamady M., Lauber C.L., Knight R. The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA. 2008;105(46):17994-17999. doi: 10.1073/pnas.0807920105.Fierer N., Hamady M., Lauber C.L., Knight R. The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA. 2008;105(46):17994-17999. doi: 10.1073/pnas.0807920105.Nakatsuji T., Chiang H.I., Jiang S.B., Nagarajan H., Zengler K., Gallo R.L. The microbiome extends to subepidermal compartments of normal skin. Nat Commun. 2013;(4):1431. doi: 10.1038/ncomms2441.Nakatsuji T., Chiang H.I., Jiang S.B., Nagarajan H., Zengler K., Gallo R.L. The microbiome extends to subepidermal compartments of normal skin. Nat Commun. 2013;(4):1431. doi: 10.1038/ncomms2441.Prast-Nielsen S., Tobin A.M., Adamzik K., Powles A., Hugerth L.W., Sweeney C., Kirby B., Engstrand L., Fry L. Investigation of the skin microbiome: swabs vs. biopsies. Br J Dermatol. 2019;28. doi: 10.1111/bjd.17691.Prast-Nielsen S., Tobin A.M., Adamzik K., Powles A., Hugerth L.W., Sweeney C., Kirby B., Engstrand L., Fry L. Investigation of the skin microbiome: swabs vs. biopsies. Br J Dermatol. 2019;28. doi: 10.1111/bjd.17691.Byrd A.L., Belkaid Y., Segre J.A. The human skin microbiome. Nat Rev Microbiol. 2018;16(3):143155. doi: 10.1038/nrmicro.2017.157.Byrd A.L., Belkaid Y., Segre J.A. The human skin microbiome. Nat Rev Microbiol. 2018;16(3):143155. doi: 10.1038/nrmicro.2017.157.Foulongne V., Sauvage V., Hebert C., Dereure O., Cheval J., Gouilh M.A., Pariente K., Segondy M., Burguiere A., Manuguerra J.-C., Caro V., Eloit M. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS One. 2012;7(6):e38499. doi: 10.1371/journal.pone.0038499.Foulongne V., Sauvage V., Hebert C., Dereure O., Cheval J., Gouilh M.A., Pariente K., Segondy M., Burguiere A., Manuguerra J.-C., Caro V., Eloit M. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS One. 2012;7(6):e38499. doi: 10.1371/journal.pone.0038499.Oh J., Byrd A.L., Deming C., Conlan S., NISC Comparative Sequencing Program, Kong H.H., Segre J.A. Biogeography and individuality shape function in the human skin metagenome. Nature. 2014;514(7520):59-64. doi: 10.1038/nature13786.Oh J., Byrd A.L., Deming C., Conlan S., NISC Comparative Sequencing Program, Kong H.H., Segre J.A. Biogeography and individuality shape function in the human skin metagenome. Nature. 2014;514(7520):59-64. doi: 10.1038/nature13786.Wylie K.M., Mihindukulasuriya K.A., Zhou Y., Sodergren E., Storch G.A., Weinstock G.M. Metagenomic analysis of doublestranded DNA viruses in healthy adults. BMC Biol. 2014;(12):71. doi: 10.1186/s12915-014-0071-7.Wylie K.M., Mihindukulasuriya K.A., Zhou Y., Sodergren E., Storch G.A., Weinstock G.M. Metagenomic analysis of doublestranded DNA viruses in healthy adults. BMC Biol. 2014;(12):71. doi: 10.1186/s12915-014-0071-7.Grice E.A. The intersection of microbiome and host at the skin interface: genomicand metagenomic-based insights. Genome Res. 2015;25(10):1514-1520. doi: 10.1101/gr.191320.115.Grice E.A. The intersection of microbiome and host at the skin interface: genomicand metagenomic-based insights. Genome Res. 2015;25(10):1514-1520. doi: 10.1101/gr.191320.115.Dreno B., Araviiskaia E., Berardesca E., Gontijo G., Sanchez V.M., Xiang L.F., Martin R., Bieber T. Microbiome in healthy skin, update for dermatologists. J Eur Acad Dermatol Venereol. 2016;30(12):2038-2047. doi: 10.1111/jdv.13965.Dreno B., Araviiskaia E., Berardesca E., Gontijo G., Sanchez V.M., Xiang L.F., Martin R., Bieber T. Microbiome in healthy skin, update for dermatologists. J Eur Acad Dermatol Venereol. 2016;30(12):2038-2047. doi: 10.1111/jdv.13965.Tomi N.S., Kranke B., Aberer E. Staphylococcal toxins in patients with psoriasis, atopic dermatitis, and erythroderma, and in healthy control subjects. J Am Acad Dermatol. 2005;(53):67–72. doi: 10.1016/j.jaad.2005.02.034.Tomi N.S., Kranke B., Aberer E. Staphylococcal toxins in patients with psoriasis, atopic dermatitis, and erythroderma, and in healthy control subjects. J Am Acad Dermatol. 2005;(53):67–72. doi: 10.1016/j.jaad.2005.02.034.Salava A., Lauerma A. Role of the skin microbiome in atopic dermatitis. Clin Transl Allergy. 2014;(4):33. doi: 10.1186/2045-7022-4-33.Salava A., Lauerma A. Role of the skin microbiome in atopic dermatitis. Clin Transl Allergy. 2014;(4):33. doi: 10.1186/2045-7022-4-33.Sanchez D.A., Nosanchuk J.D., Friedman A.J. The skin microbiome: is there a role in the pathogenesis of atopic dermatitis and psoriasis? J Drugs Dermatol. 2015;(14):127–130. Available at: https://www.ncbi.nlm.nih.gov/pubmed/25689807.Sanchez D.A., Nosanchuk J.D., Friedman A.J. The skin microbiome: is there a role in the pathogenesis of atopic dermatitis and psoriasis? J Drugs Dermatol. 2015;(14):127–130. Available at: https://www.ncbi.nlm.nih.gov/pubmed/25689807.Seite S., Bieber T. Barrier function and microbiotic dysbiosis in atopic dermatitis. Clin Cosmet Investig Dermatol. 2015;(8):479–483. doi: 10.2147/CCID.S91521.Seite S., Bieber T. Barrier function and microbiotic dysbiosis in atopic dermatitis. Clin Cosmet Investig Dermatol. 2015;(8):479–483. doi: 10.2147/CCID.S91521.Williams M.R., Gallo R.L. The role of the skin microbiome in atopic dermatitis. Current Allergy and Asthma Reports. 2015;15:65. doi: 10.1007/s11882-015-0567-4.Williams M.R., Gallo R.L. The role of the skin microbiome in atopic dermatitis. Current Allergy and Asthma Reports. 2015;15:65. doi: 10.1007/s11882-015-0567-4.Zeeuwen P.L., Kleerebezem M., Timmerman H.M., Schalkwijk J. Microbiome and skin diseases. Curr Opin Allergy Clin Immunol. 2013;(13):514–520. doi: 10.1097/ACI.0b013e328364ebeb.Zeeuwen P.L., Kleerebezem M., Timmerman H.M., Schalkwijk J. Microbiome and skin diseases. Curr Opin Allergy Clin Immunol. 2013;(13):514–520. doi: 10.1097/ACI.0b013e328364ebeb.Nakatsuji T., Chiang H.I., Jiang S.B., Nagarajan H., Zengler K., Gallo R.L. The microbiome extends to subepidermal compartments of normal skin. Nat Commun. 2013;(4):1431. doi: 10.1038/ncomms2441.Nakatsuji T., Chiang H.I., Jiang S.B., Nagarajan H., Zengler K., Gallo R.L. The microbiome extends to subepidermal compartments of normal skin. Nat Commun. 2013;(4):1431. doi: 10.1038/ncomms2441.Weyrich L.S., Dixit S., Farrer A.G., Cooper A.J. The skin microbiome: associations between altered microbial communities and disease. Australas J Dermatol. 2015;(56):268–274. doi: 10.1111/ajd.12253.Weyrich L.S., Dixit S., Farrer A.G., Cooper A.J. The skin microbiome: associations between altered microbial communities and disease. Australas J Dermatol. 2015;(56):268–274. doi: 10.1111/ajd.12253.Otto M. Staphylococcus epidermidis–the ‘accidental’ pathogen. Nat Rev Microbiol. 2009;(7):555–567. doi: 10.1038/nrmicro2182.Otto M. Staphylococcus epidermidis–the ‘accidental’ pathogen. Nat Rev Microbiol. 2009;(7):555–567. doi: 10.1038/nrmicro2182.Wang Y., Kuo S., Shu M., Yu J., Huang S., Dai A., Richard L.T., Huang G.C.-M. Staphylococcus epidermidis in the human skin microbiome mediates fermentation to inhibit the growth of Propionibacterium acnes: implications of probiotics in acne vulgaris. Appl Microbiol Biotechnol. 2014;(98):411–424. doi: 10.1007/s00253-013-5394-8.Wang Y., Kuo S., Shu M., Yu J., Huang S., Dai A., Richard L.T., Huang G.C.-M. Staphylococcus epidermidis in the human skin microbiome mediates fermentation to inhibit the growth of Propionibacterium acnes: implications of probiotics in acne vulgaris. Appl Microbiol Biotechnol. 2014;(98):411–424. doi: 10.1007/s00253-013-5394-8.Kong H.H., Segre J.A. Skin microbiome: looking back to move forward. J Invest Dermatol. 2012;132(3 Pt 2):933–939. doi: 10.1038/jid.2011.417.Kong H.H., Segre J.A. Skin microbiome: looking back to move forward. J Invest Dermatol. 2012;132(3 Pt 2):933–939. doi: 10.1038/jid.2011.417.Ladizinski B., McLean R., Lee K.C., Elpern D.J., Eron L. The human skin microbiome. Int J Dermatol. 2014;(53):1177–1179. doi: 10.1111/ijd.12609.Ladizinski B., McLean R., Lee K.C., Elpern D.J., Eron L. The human skin microbiome. Int J Dermatol. 2014;(53):1177–1179. doi: 10.1111/ijd.12609.Sanford J.A., Gallo R.L. Functions of the skin microbiota in health and disease. Semin Immunol. 2013;(25):370–377. doi: 10.1016/j.smim.2013.09.005.Sanford J.A., Gallo R.L. Functions of the skin microbiota in health and disease. Semin Immunol. 2013;(25):370–377. doi: 10.1016/j.smim.2013.09.005.Holmes A.D., Waite K.A., Chen M.C., Palaniswamy K., Wiser T.H., Draelos Z.D., Rafal E.S., Werschler W.P., Harvey A.E. Dermatological adverse events associated with topical brimonidine gel 0.33% in subjects with erythema of rosacea: a retrospective review of clinical studies. J Clin Aesthet Dermatol. 2015;(8):29–35.Holmes A.D., Waite K.A., Chen M.C., Palaniswamy K., Wiser T.H., Draelos Z.D., Rafal E.S., Werschler W.P., Harvey A.E. Dermatological adverse events associated with topical brimonidine gel 0.33% in subjects with erythema of rosacea: a retrospective review of clinical studies. J Clin Aesthet Dermatol. 2015;(8):29–35.Shu M., Wang Y., Yu J., Kuo S., Coda A., Jiang Y., Gallo R.L., Huang C.M. Fermentation of Propionibacterium acnes, a commensal bacterium in the human skin microbiome, as skin probiotics against methicillin-resistant Staphylococcus aureus. PLoS ONE. 2013;(8):e55380. doi: 10.1371/journal.pone.0055380.Shu M., Wang Y., Yu J., Kuo S., Coda A., Jiang Y., Gallo R.L., Huang C.M. Fermentation of Propionibacterium acnes, a commensal bacterium in the human skin microbiome, as skin probiotics against methicillin-resistant Staphylococcus aureus. PLoS ONE. 2013;(8):e55380. doi: 10.1371/journal.pone.0055380.Christensen G.J., Bruggemann H. Bacterial skin commensals and their role as host guardians. Benef Microbes. 2014;(5):201–215. doi: 10.3920/BM2012.0062.Christensen G.J., Bruggemann H. Bacterial skin commensals and their role as host guardians. Benef Microbes. 2014;(5):201–215. doi: 10.3920/BM2012.0062.Kostic A.D., Howitt M.R., Garrett W.S. Exploring host–microbiota interactions in animal models and humans. Genes Dev. 2013;(27):701–718. doi: 10.1101/gad.212522.112.Kostic A.D., Howitt M.R., Garrett W.S. Exploring host–microbiota interactions in animal models and humans. Genes Dev. 2013;(27):701–718. doi: 10.1101/gad.212522.112.Lai Y., Cogen A.L., Radek K.A., Park H.J., Macleod D.T., Leichtle A., Ryan A.F., Di Nardo A., Gallo R.L. Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. J Invest Dermatol. 2010;(130):2211– 2221. doi: 10.1038/jid.2010.123.Lai Y., Cogen A.L., Radek K.A., Park H.J., Macleod D.T., Leichtle A., Ryan A.F., Di Nardo A., Gallo R.L. Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. J Invest Dermatol. 2010;(130):2211– 2221. doi: 10.1038/jid.2010.123.Wang Z., MacLeod D.T., Di Nardo A. Commensal bacteria lipoteichoic acid increases skin mast cell antimicrobial activity against vaccinia viruses. J Immunol. 2012;(189):1551–1558. doi: 10.4049/jimmunol.1200471.Wang Z., MacLeod D.T., Di Nardo A. Commensal bacteria lipoteichoic acid increases skin mast cell antimicrobial activity against vaccinia viruses. J Immunol. 2012;(189):1551–1558. doi: 10.4049/jimmunol.1200471.Gallo R.L., Nakatsuji T. Microbial symbiosis with the innate immune defense system of the skin. J Invest Dermatol. 2011;(131):1974–1980. doi: 10.1038/jid.2011.182.Gallo R.L., Nakatsuji T. Microbial symbiosis with the innate immune defense system of the skin. J Invest Dermatol. 2011;(131):1974–1980. doi: 10.1038/jid.2011.182.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., Radek K.A., Huang C.M., Ryan A.F., Gallo R.L. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med. 2009;(15):1377– 1382. doi: 10.1038/nm.2062.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., Radek K.A., Huang C.M., Ryan A.F., Gallo R.L. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med. 2009;(15):1377– 1382. doi: 10.1038/nm.2062.Cogen A.L., Yamasaki K., Sanchez K.M., Dorschner R.A., Lai Y., MacLeod D.T., Torpey J.W., Otto M., Nizet V., Kim J.E., Gallo R.L. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J Invest Dermatol. 2010;(130):192–200. doi: 10.1038/jid.2009.243.Cogen A.L., Yamasaki K., Sanchez K.M., Dorschner R.A., Lai Y., MacLeod D.T., Torpey J.W., Otto M., Nizet V., Kim J.E., Gallo R.L. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J Invest Dermatol. 2010;(130):192–200. doi: 10.1038/jid.2009.243.Salava A., Lauerma A. Role of the skin microbiome in atopic dermatitis. Clin Transl Allergy. 2014;(4):33. doi: 10.1186/2045-7022-4-33.Salava A., Lauerma A. Role of the skin microbiome in atopic dermatitis. Clin Transl Allergy. 2014;(4):33. doi: 10.1186/2045-7022-4-33.Kong H.H., Oh J., Deming C., Conlan S., Grice E.A., Beatson M.A., Nomicos E., Polley E.C., Komarow H.D., NISC Comparative Sequence Program, Murray P.R., Turner M.L., Segre J.A. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 2012;22(5):850-859. doi: 10.1101/gr.131029.111.Kong H.H., Oh J., Deming C., Conlan S., Grice E.A., Beatson M.A., Nomicos E., Polley E.C., Komarow H.D., NISC Comparative Sequence Program, Murray P.R., Turner M.L., Segre J.A. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 2012;22(5):850-859. doi: 10.1101/gr.131029.111.Byrd A.L., Deming C., Cassidy S.K.B., Harrison O.J., Weng-Ian Ng, Conlan S., NISC Comparative Sequencing Program, Belkaid Y., Segre J.A., Kong H.H. Staphylococcus aureus and Staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis. Sci Transl Med. 2017; 9(397). doi: 10.1126/scitranslmed.aal4651.Byrd A.L., Deming C., Cassidy S.K.B., Harrison O.J., Weng-Ian Ng, Conlan S., NISC Comparative Sequencing Program, Belkaid Y., Segre J.A., Kong H.H. Staphylococcus aureus and Staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis. Sci Transl Med. 2017; 9(397). doi: 10.1126/scitranslmed.aal4651.Nakatsuji T., Gallo R.L. The role of the skin microbiome in atopic dermatitis. Ann Allergy Asthma Immunol. 2019;122(3):263-269. doi: 10.1016/j.anai.2018.12.003.Nakatsuji T., Gallo R.L. The role of the skin microbiome in atopic dermatitis. Ann Allergy Asthma Immunol. 2019;122(3):263-269. doi: 10.1016/j.anai.2018.12.003.Spaulding A.R., Salgado-Pabon W., Kohler P.L., Horswill A.R., Leung D.Y., Schlievert P.M. Staphylococcal and streptococcal superantigen exotoxins. Clin Microbiol Rev. 2013;(26):422-447. doi: 10.1128/CMR.00104-12.Spaulding A.R., Salgado-Pabon W., Kohler P.L., Horswill A.R., Leung D.Y., Schlievert P.M. Staphylococcal and streptococcal superantigen exotoxins. Clin Microbiol Rev. 2013;(26):422-447. doi: 10.1128/CMR.00104-12.Nakagawa S., Matsumoto M., Katayama Y., Oguma R., Wakabayashi S., Nygaard T., Saijo S., Inohara N., Otto M., Matsue H., Nunez G., Nakamura Y. Staphylococcus aureus Virulent PSMalpha Peptides Induce Keratinocyte Alarmin Release to Orchestrate IL-17Dependent Skin Inflammation. Cell Host Microbe. 2017;(22):667-677. doi: 10.1016/j.chom.2017.10.008.Nakagawa S., Matsumoto M., Katayama Y., Oguma R., Wakabayashi S., Nygaard T., Saijo S., Inohara N., Otto M., Matsue H., Nunez G., Nakamura Y. Staphylococcus aureus Virulent PSMalpha Peptides Induce Keratinocyte Alarmin Release to Orchestrate IL-17Dependent Skin Inflammation. Cell Host Microbe. 2017;(22):667-677. doi: 10.1016/j.chom.2017.10.008.Liu H., Archer N.K., Dillen C.A., Wang Y., Ashbaugh A.G., Ortines R.V., Kao T., Lee S.K., Cai S.S., Miller R.J., Marchitto M.C., Zhang E., Riggins D.P., Plaut R.D., Stibitz S., Geha R., Miller L.S. Staphylococcus aureus Epicutaneous Exposure Drives Skin Inflammation via IL-36-Mediated T Cell Responses. Cell Host Microbe. 2017;(22):653666 e655. doi: 10.1016/j.chom.2017.Liu H., Archer N.K., Dillen C.A., Wang Y., Ashbaugh A.G., Ortines R.V., Kao T., Lee S.K., Cai S.S., Miller R.J., Marchitto M.C., Zhang E., Riggins D.P., Plaut R.D., Stibitz S., Geha R., Miller L.S. Staphylococcus aureus Epicutaneous Exposure Drives Skin Inflammation via IL-36-Mediated T Cell Responses. Cell Host Microbe. 2017;(22):653666 e655. doi: 10.1016/j.chom.2017.Williams M.R., Nakatsuji T., Sanford J.A., Vrbanac A.F., Gallo R.L. Staphylococcus aureus Induces Increased Serine Protease Activity in Keratinocytes. J Invest Dermatol. 2017;(137):377384. doi: 10.1016/j.jid.2016.10.008.Williams M.R., Nakatsuji T., Sanford J.A., Vrbanac A.F., Gallo R.L. Staphylococcus aureus Induces Increased Serine Protease Activity in Keratinocytes. J Invest Dermatol. 2017;(137):377384. doi: 10.1016/j.jid.2016.10.008.Fahlen A., Engstrand L., Baker B.S., Powles A., Fry L. Comparison of bacterial microbiota in skin biopsies from normal and psoriatic skin. Arch Dermatol Res. 2012;304(1):15-22. doi: 10.1007/s00403-011-1189-x.Fahlen A., Engstrand L., Baker B.S., Powles A., Fry L. Comparison of bacterial microbiota in skin biopsies from normal and psoriatic skin. Arch Dermatol Res. 2012;304(1):15-22. doi: 10.1007/s00403-011-1189-x.Gomez-Moyano E., Crespo-Erchiga V., MartinezPilar L., Godoy Diaz D., Martinez-Garcia S., Lova Navarro M., Vera Casano A. Do Malassezia species play a role in exacerbation of scalp psoriasis? J Mycol Med. 2014;24(2):87-92. doi:10.1016/j.mycmed.2013.10.007.Gomez-Moyano E., Crespo-Erchiga V., MartinezPilar L., Godoy Diaz D., Martinez-Garcia S., Lova Navarro M., Vera Casano A. Do Malassezia species play a role in exacerbation of scalp psoriasis? J Mycol Med. 2014;24(2):87-92. doi:10.1016/j.mycmed.2013.10.007.Fitz-Gibbon S., Tomida S., Chiu B.H., Nguyen L., Du C., Liu M., Elashoff D., Erfe M.C., Loncaric A., Kim J., Modlin R.L., Miller J.F., Sodergren E., Craft N., Weinstock G.M., Li H. Propionibacterium acnes strain populations in the human skin microbiome associated with acne. J Invest Dermatol. 2013;133(9):2152-2160. doi: 10.1038/jid.2013.21.Fitz-Gibbon S., Tomida S., Chiu B.H., Nguyen L., Du C., Liu M., Elashoff D., Erfe M.C., Loncaric A., Kim J., Modlin R.L., Miller J.F., Sodergren E., Craft N., Weinstock G.M., Li H. Propionibacterium acnes strain populations in the human skin microbiome associated with acne. J Invest Dermatol. 2013;133(9):2152-2160. doi: 10.1038/jid.2013.21.Xu H., Li H. Acne, the Skin Microbiome, and Antibiotic Treatment. Am J Clin Dermatol. 2019;20(3):335-344. doi: 10.1007/s40257-01800417-3.Xu H., Li H. Acne, the Skin Microbiome, and Antibiotic Treatment. Am J Clin Dermatol. 2019;20(3):335-344. doi: 10.1007/s40257-01800417-3.Lise M., Mayer I., Silveira M. Use of probiotics in atopic dermatitis Rev Assoc Med Bras (1992). 2018;64(11):997-1001. doi: 10.1590/18069282.64.11.997.Lise M., Mayer I., Silveira M. Use of probiotics in atopic dermatitis Rev Assoc Med Bras (1992). 2018;64(11):997-1001. doi: 10.1590/18069282.64.11.997.Pringsheim E.G. The Vitreoscillaceae: a family of colorless, gliding, filamentous organisms. J Gen Microbiol. 1951;5:124–149. doi: 10.1099/00221287-5-1-124.Pringsheim E.G. The Vitreoscillaceae: a family of colorless, gliding, filamentous organisms. J Gen Microbiol. 1951;5:124–149. doi: 10.1099/00221287-5-1-124.Mahe Y.F., Perez M-J., Tacheau C., Fanchon C., Martin R., Rousset F., Seite S. A new Vitreoscilla filiformis extract grown on spa water enriched medium activates endogenous cutaneous antioxidant and antimicrobial defenses through a potential Toll-like receptor 2/protein kinase C, zeta transduction pathway. Clin Cosmet Investig Dermatol. 2013;(6):191–196. doi: 10.2147/CCID.S47324.Mahe Y.F., Perez M-J., Tacheau C., Fanchon C., Martin R., Rousset F., Seite S. A new Vitreoscilla filiformis extract grown on spa water enriched medium activates endogenous cutaneous antioxidant and antimicrobial defenses through a potential Toll-like receptor 2/protein kinase C, zeta transduction pathway. Clin Cosmet Investig Dermatol. 2013;(6):191–196. doi: 10.2147/CCID.S47324.Gueniche A., Knaudt B., Schuck E., Volz T., Bastien P., Martin R., Rocken M., Breton L., Biedermann T. Effects of nonpathogenic gram-negative bacterium Vitreoscilla filiformis lysate on atopic dermatitis: a prospective, randomized, double-blind, placebo-controlled clinical study. Br J Dermatol. 2008;159(6):1357-1363. doi: 10.1111/j.1365-2133.2008.08836.x.Gueniche A., Knaudt B., Schuck E., Volz T., Bastien P., Martin R., Rocken M., Breton L., Biedermann T. Effects of nonpathogenic gram-negative bacterium Vitreoscilla filiformis lysate on atopic dermatitis: a prospective, randomized, double-blind, placebo-controlled clinical study. Br J Dermatol. 2008;159(6):1357-1363. doi: 10.1111/j.1365-2133.2008.08836.x.

The authors declare that there are no conflicts of interest present.