Vestnik dermatologii i venerologiiVestnik dermatologii i venerologiiВестник дерматологии и венерологии0042-46092313-6294Rossijskoe Obschestvo Dermatovenerologov i Kosmetologov128210.25208/vdv1282REVIEWSОБЗОР ЛИТЕРАТУРЫReview ArticleDisorders of the skin microbiome in atopic dermatitis and psoriasisНарушения микробиома кожи при атопическом дерматите и псориазеhttps://orcid.org/0000-0002-8677-41678072-7935NikolaevaMarina Yu.НиколаеваМарина Юрьевна
Russian Federation

assistant lecturer

ассистент

lavrukhina.mary@yandex.ruhttps://orcid.org/0000-0002-8211-16651837-2098MonakhovKonstantin N.МонаховКонстантин Николаевич
Russian Federation

MD, Dr. Sci. (Med.), Professor

д.м.н., профессор

knmonakhov@mail.ruhttps://orcid.org/0000-0001-7610-60616807-7137SokolovskiyEvgeny V.СоколовскийЕвгений Владиславович
Russian Federation

MD, Dr. Sci. (Med.), Professor

д.м.н., профессор

s40@mail.ruFirst Pavlov State Medical University of Saint PetersburgПервый Санкт-Петербургский государственный медицинский университет им. академика И. П. Павлова2412202197633432409202129102021Copyright ©; 2021, Nikolaeva M.Y., Monakhov K.N., Sokolovskiy E.V.Copyright ©; 2021, Николаева М.Ю., Монахов К.Н., Соколовский Е.В.2021Nikolaeva M.Y., Monakhov K.N., Sokolovskiy E.V.Николаева М.Ю., Монахов К.Н., Соколовский Е.В.https://creativecommons.org/licenses/by/4.0https://vestnikdv.ru/jour/article/view/1282

The notion of skin microbiome encompasses a heterogeneous group of microorganisms that belong to various taxonomic units, such as bacteria, archaea, viruses, and fungi. The impact of these microbial community constituents upon the epidermal barrier condition, and upon the immune system functioning, is being intensely scrutinized. There is a particular interest in studying the role that the microorganisms of genus Staphylococcus spp. play in the course of physiological and pathological processes occurring in the skin. This review examines in detail the interaction of the microorganisms of genus Staphylococcus spp. with the microbial community constituents, as well as with the skin immune system in normal condition and in the condition associated with inflammatory dermatoses. There are also the data given on S. aureus pathogenicity factors, the data on the impact of this microorganism upon the course of atopic dermatitis, and upon the course of psoriasis. The review examines the role that coagulase-negative staphylococci, S. epidermidis in particular, play in maintaining the microbiome homeostasis. The review as well examines the impact of the skin microbiome upon the development and activity of the skin immune system, and upon maintaining the integrity of the epidermal barrier.

Понятие «микробиом кожи» охватывает гетерогенную группу микроорганизмов, принадлежащих к различным таксономическим единицам: бактерии, археи, вирусы и грибы. Влияние компонентов микробного сообщества на состояние эпидермального барьера, работу иммунной системы кожи активно изучается. Особый интерес представляет исследование роли микроорганизмов рода Staphylococcus spp. в течении физиологических и патологических процессов, протекающих в коже. В обзоре детально рассматривается взаимодействие микроорганизмов рода Staphylococcus spp. c компонентами микробного сообщества, иммунной системы кожи в норме и в ассоциации с воспалительными дерматозами. Приведены данные о факторах патогенности S. aureus, влиянии микроорганизма на течение атопического дерматита, псориаза. Рассматривается роль коагулаз-негативных стафилококков, в частности S. epidermidis, в поддержании гомеостаза микробиома, а также влияние на развитие и активность иммунной системы кожи, сохранение целостности эпидермального барьера.

skin microbiomeatopic dermatitispsoriasisмикробиом кожиатопический дерматитпсориазKong HH, Andersson B, Clavel T, Common JE, Jackson SA, Olson ND, et al. Performing Skin Microbiome Research: A Method to the Madness. J Invest Dermatol. 2017;137(3):561–568. doi: 10.1016/j.jid.2016.10.033Аравийская Е. Р., Соколовский Е. В. Микробиом: новая эра в изучении здоровой и патологически измененной кожи. Вестник дерматологии и венерологии. 2016;3:102–109 [Araviiskaia ER, Sokolovskiy EV. Microbiome: a new era in normal and pathological changes skin studies. Vestnik dermatologii i venerologii. 2016;3:102–109 (In Russ.)] doi: 10.25208/0042-4609-2016-92-3-102-109Byrd AL, Belkaid Y, Segre JA. The human skin microbiome. Nat Rev Microbiol. 2018;16(3):143–155. doi: 10.1038/nrmicro.2017.157Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol. 2011;9(4):244–253. doi: 10.1038/nrmicro2537. Erratum in: Nat Rev Microbiol. 2011;9(8):626.Powers CE, McShane DB, Gilligan PH, Burkhart CN, Morrell DS. Microbiome and pediatric atopic dermatitis. J Dermatol. 2015;42(12):1137–1142. doi: 10.1111/1346-8138.13072Pothmann A, Illing T, Wiegand C, Hartmann AA, Elsner P. The Microbiome and Atopic Dermatitis: A Review. Am J Clin Dermatol. 2019;20(6):749–761. doi: 10.1007/s40257-019-00467-1Paller AS, Kong HH, Seed P, Naik S, Scharschmidt TC, Gallo RL, et al. The microbiome in patients with atopic dermatitis. J Allergy Clin Immunol. 2019;143(1):26–35. doi: 10.1016/j.jaci.2018.11.015Drеno B. The microbiome, a new target for ecobiology in dermatology. Eur J Dermatol. 2019;29(S1):15–18. doi: 10.1684/ejd.2019.3535Zhang LJ, Gallo RL. Antimicrobial peptides. Curr Biol 2016;26:R14–9. doi: 10.1016/j.cub.2015.11.017Nakatsuji T, Gallo RL. The role of the skin microbiome in atopic dermatitis. Ann Allergy Asthma Immunol. 2019;122(3):263–269. doi: 10.1016/j.anai.2018.12.003Seiti Yamada Yoshikawa F, Feitosa de Lima J, Notomi Sato M, Álefe Leuzzi Ramos Y, Aoki V, Leao Orfali R. Exploring the Role of Staphylococcus Aureus Toxins in Atopic Dermatitis. Toxins (Basel). 2019;11(6):321. doi:10.3390/toxins11060321Пономаренко С. В. Микробиологические аспекты стафилококковой инфекции на современном этапе (обзор литературы). Annals of Mechnikov Institute. 2013;3:13–17 [Ponomarenko SV. Microbiological aspects of Staphylococcal infections today (literary rewiew). Annals of Mechnikov Institute. 2013;3:13–17 (In Russ.)]Iwamoto K, Moriwaki M, Miyake R, Hide M. Staphylococcus aureus in atopic dermatitis: Strain-specific cell wall proteins and skin immunity. Allergol Int. 2019;68(3):309–315. doi: 10.1016/j.alit.2019.02.006Kwiecinski J, Jin T, Josefsson E. Surface proteins of Staphylococcus aureus play an important role in experimental skin infection. APMIS. 2014;122(12):1240–1250. doi: 10.1111/apm.12295Cho SH, Strickland I, Boguniewicz M, Leung DY. Fibronectin and fibrinogen contribute to the enhanced binding of Staphylococcus aureus to atopic skin. J Allergy Clin Immunol. 2001;108(2):269–274. doi: 10.1067/mai.2001.117455Nakatsuji T, Chen TH, Two AM, Chun KA, Narala S, Geha RS, et al. Staphylococcus aureus exploits epidermal barrier defects in atopic dermatitis to trigger cytokine expression. J Invest Dermatol 2016;36(11):2192–2200. doi: 10.1016/j.jid.2016.05.127.Schlievert PM, Case LC, Strandberg KL, Abrams BB, Leung DY. Superantigen profile of Staphylococcus aureus isolates from patients with steroid-resistant atopic dermatitis. Clin Infect Dis. 2008;46(10):1562–1567. doi: 10.1086/586746Rudikoff D, Cohen SR, Scheinfeld N. Atopic dermatitis and eczematous disorders. CRC Press; 2014. p. 436.Tankersley A, Frank MB, Bebak M, Brennan R. Early effects of Staphylococcus aureus biofilm secreted products on inflammatory responses of human epithelial keratinocytes. J Inflamm (Lond). 2014;11:17 doi: 10.1186/1476-9255-11-17Dodds D, Bose JL, Deng MD, Dubé GR, Grossman TH, Kaiser A, et al. Controlling the Growth of the Skin Commensal Staphylococcus epidermidis Using d-Alanine Auxotrophy. mSphere. 2020;5(3):e00360-20. doi: 10.1128/mSphere.00360-20Flowers L, Grice EA. The Skin Microbiota: Balancing Risk and Reward. Cell Host Microbe. 2020;28(2):190–200. doi: 10.1016/j.chom.2020.06.017Brown MM, Horswill AR. Staphylococcus epidermidis-Skin friend or foe? PLoS Pathog. 2020;16(11):e1009026. doi: 10.1371/journal.ppat.1009026Stacy A, Belkaid Y. Microbial guardians of skin health. Science. 2019;363(6424):227–228. doi: 10.1126/science.aat4326Hwang J, Jaros J, Shi VY. Staphylococcus aureus in Atopic Dermatitis: Past, Present, and Future. Dermatitis. 2020;31(4):247–258. doi: 10.1097/DER.0000000000000589Chikindas ML, Weeks R, Drider D, Chistyakov VA, Dicks LM. Functions and emerging applications of bacteriocins. Curr Opin Biotechnol. 2018;49:23–28. doi: 10.1016/j.copbio.2017.07.011França A, Gaio V, Lopes N, Melo LDR. Virulence Factors in Coagulase-Negative Staphylococci. Pathogens. 2021;10(2):170. doi: 10.3390/pathogens10020170Williams MR, Costa SK, Zaramela LS, Khalil S, Todd DA, Winter HL, et al. Quorum sensing between bacterial species on the skin protects against epidermal injury in atopic dermatitis. Sci Transl Med. 2019;11(490):eaat8329. doi: 10.1126/scitranslmed.aat8329Naik S, Bouladoux N, Linehan JL, Han SJ, Harrison OJ, Wilhelm C, et al. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature. 2015;520(7545):104–148. doi: 10.1038/nature14052Simanski M, Erkens AS, Rademacher F, Harder J. Staphylococcus epidermidis-induced Interleukin-1 Beta and Human Beta-defensin-2 Expression in Human Keratinocytes is Regulated by the Host Molecule A20 (TNFAIP3). Acta Derm Venereol. 2019;99(2):181–187. doi: 10.2340/00015555-3073Constantinides MG, Link VM, Tamoutounour S, Wong AC, Perez-Chaparro PJ, Han SJ, et al. MAIT cells are imprinted by the microbiota in early life and promote tissue repair. Science. 2019;366(6464):eaax6624. doi: 10.1126/science.aax6624Toubal A, Nel I, Lotersztajn S, Lehuen A. Mucosal-associated invariant T cells and disease. Nat Rev Immunol. 2019;19(10):643–657. doi: 10.1038/s41577-019-0191-yNodake Y, Matsumoto S, Miura R, Honda H, Ishibashi G, Matsumoto S, et al. Pilot study on novel skin care method by augmentation with Staphylococcus epidermidis, an autologous skin microbe. A blinded randomized clinical trial. J Dermatol Sci. 2015;79(2):119–126. doi: 10.1016/j.jdermsci.2015.05.001David Boothe W, Tarbox JA, Tarbox MB. Atopic Dermatitis: Pathophysiology. In: Fortson E, Feldman S, Strowd L, editors. Management of Atopic Dermatitis. Advances in Experimental Medicine and Biology, vol 1027. Springer, Cham. doi: 10.1007/978-3-319-64804-0_3Рациональная фармакотерапия заболеваний кожи и инфекций, передаваемых половым путем / Под ред. Самцова А. В., Соколовского Е. В. Литтерра; 2021 г. 992 с. [Rational pharmacotherapy of skin disorders and venereal diseases. Litterra; 2021. p. 992 Ed. by Samtsov AV, Sokolovskiy EV. (In Russ.)]Torres T, Ferreira EO, Gonçalo M, Mendes-Bastos P, Selores M, Filipe P. Update on Atopic Dermatitis. Acta Med Port. 2019;32(9):606–613. doi: 10.20344/amp.11963Cabanillas B, Brehler AC, Novak N. Atopic dermatitis phenotypes and the need for personalized medicine. Curr Opin Allergy Clin Immunol. 2017;17(4):309–315 doi: 10.1097/ACI.0000000000000376.Li W, Yosipovitch G. The Role of the Microbiome and Microbiome-Derived Metabolites in Atopic Dermatitis and Non-Histaminergic Itch. Am J Clin Dermatol. 2020;21(Suppl 1):44–50. doi: 10.1007/s40257-020-00538-8Baurecht H, Ruhlemann MC, Rodriguez E, Thielking F, Harder I, Erkens AS, et al. Epidermal lipid composition, barrier integrity, and eczematous inflammation are associated with skin microbiome configuration. J Allergy Clin Immunol. 2018;141(5):1668–1676 e16. doi: 10.1016/j.jaci.2018.01.019Kraft MT, Prince BT. Atopic Dermatitis Is a Barrier Issue, Not an Allergy Issue. Immunol Allergy Clin North Am. 2019;39(4):507–519. doi: 10.1016/j.iac.2019.07.005Li S, Villarreal M, Stewart S, Choi J, Ganguli-Indra G, Babineau DC, et al. Altered composition of epidermal lipids correlates with Staphylococcus aureus colonization status in atopic dermatitis. Br J Dermatol. 2017;177(4):e125–e127. doi: 10.1111/bjd.15409Schittek B. The antimicrobial skin barrier in patients with atopic dermatitis. Curr Probl Dermatol. 2011;41:54–67. doi: 10.1159/000323296Holmes J, Fairclough LC, Todd I. Atopic dermatitis and autoimmunity: the occurrence of autoantibodies and their association with disease severity [published correction appears in Arch Dermatol Res. 2020;312(5):393].Arch Dermatol Res. 2019;311(3):141–162. doi:10.1007/s00403-019-01890-4Balato A, Cacciapuoti S, Di Caprio R, Marasca C, Masarà A, Raimondo A, et al. Human Microbiome: Composition and Role in Inflammatory Skin Diseases. Arch Immunol Ther Exp (Warsz). 2019;67(1):1–18. doi: 10.1007/s00005-018-0528-4Meylan P, Lang C, Mermoud S, Johannsen A, Norrenberg S, Hohl D, et al. Skin colonization by Staphylococcus aureus precedes the clinical diagnosis of atopic dermatitis in infancy. J Invest Dermatol 2017;137(12):2497–2504 doi: 10.1016/j.jid.2017.07.834Woo TE, Sibley CD. The emerging utility of the cutaneous microbiome in the treatment of acne and atopic dermatitis. J Am Acad Dermatol. 2020;82(1):222–228. doi: 10.1016/j.jaad.2019.08.078Byrd AL, Deming C, Cassidy SKB, Harrison OJ, Ng WI, Conlan S; NISC Comparative Sequencing Program, Belkaid Y, Segre JA, Kong HH. Staphylococcus aureus and Staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis. Sci Transl Med. 2017;9(397):eaal4651. doi: 10.1126/scitranslmed.aal4651.Edslev SM, Olesen CM, Nørreslet LB, Ingham AC, Iversen S, Lilje B, et al. Staphylococcal Communities on Skin Are Associated with Atopic Dermatitis and Disease Severity. Microorganisms. 2021;9(2):432. doi: 10.3390/microorganisms9020432Stalder JF, Fluhr JW, Foster T, Glatz M, Proksch E. The emerging role of skin microbiome in atopic dermatitis and its clinical implication. J Dermatolog Treat. 2019;30(4):357–364. doi: 10.1080/09546634.2018.1516030Leung DY, Harbeck R, Bina P, Reiser RF, Yang E, Norris DA, et al. Presence of IgE antibodies to staphylococcal exotoxins on the skin of patients with atopic dermatitis. Evidence for a new group of allergens. J Clin Invest. 1993;92(3):1374–1380. doi: 10.1172/JCI116711Strange P, Skov L, Lisby S, Nielsen PL, Baadsgaard O. Staphylococcal enterotoxin B applied on intact normal and intact atopic skin induces dermatitis. Arch Dermatol. 1996;132(1):27–33.Schlievert PM, Case LC, Strandberg KL, Abrams BB, Leung DY. Superantigen profile of Staphylococcus aureus isolates from patients with steroid-resistant atopic dermatitis. Clin Infect Dis. 2008;46(10):1562–1567.Hauk PJ, Hamid QA, Chrousos GP, Leung DY. Induction of corticosteroid insensitivity in human PBMCs by microbial superantigens. J Allergy Clin Immunol. 2000;105(4):782–787. doi: 10.1067/mai.2000.105807.Alexander H, Paller AS, Traidl-Hoffmann C, Beck LA, De Benedetto A, Dhar S, et al. The role of bacterial skin infections in atopic dermatitis: expert statement and review from the International Eczema Council Skin Infection Group. Br J Dermatol. 2020;182(6):1331–1342. doi: 10.1111/bjd.18643Ong PY. Recurrent MRSA skin infections in atopic dermatitis. J Allergy Clin Immunol Pract. 2014;2(4):396–399. doi: 10.1016/j.jaip.2014.04.007Nakatsuji T, Tong Y, Butcher A, Hayashi A, Chun K, Shafiq F, et al. Clinical improvement in atopic dermatitis following autologous application of microbiome therapy targeting Staphylococcus aureus. J Invest Dermatol 2018;138:S72Chang HW, Yan D, Singh R, Liu J, Lu X, Ucmak D, et al. Alteration of the cutaneous microbiome in psoriasis and potential role in Th17 polarization. Microbiome. 2018;6(1):154. doi: 10.1186/s40168-018-0533-1Потекаев Н. Н., Круглова Л. С. Псориатическая болезнь. Москва, 2014. 264 с. [Potekaev NN, Kruglova LS. Psoriatic disease. Moscow: 2014. p. 264. (In Russ.)]Tokuyama M, Mabuchi T. New Treatment Addressing the Pathogenesis of Psoriasis. Int J Mol Sci. 2020;21(20):7488. doi: 10.3390/ijms21207488Кубанов А. А., Бакулев А. Л., Глузмин М. И., Кохан М. М., Круглова Л. С., Руднева Н. С. и др. Цертолизумаба пэгол: новые возможности терапии среднетяжелого и тяжелого вульгарного псориаза. Вестник дерматологии и венерологии. 2019;95(5):50–57 [Kubanov AA, Bakulev AL, Gluzmin MI, Kokhan MM, Kruglova LS, Rudneva NS, et al. Certolizumab pegol: new opportunities for treatment of moderate to severe plaque psoriasis. Vestnik dermatologii i venerologii. 2019;95.50–57.(In Russ.)] doi:10.25208/0042-4609-2019-95-5-50-57Rendon A, Schäkel K. Psoriasis Pathogenesis and Treatment. Int J Mol Sci. 2019;20(6):1475. doi: 10.3390/ijms20061475Alekseyenko AV, Perez-Perez GI, De Souza A, Strober B, Gao Z, Bihan M, et al. Community differentiation of the cutaneous microbiota in psoriasis. Microbiome. 2013;1(1):31. doi: 10.1186/2049-2618-1-31Lewis DJ, Chan WH, Hinojosa T, Hsu S, Feldman SR. Mechanisms of microbial pathogenesis and the role of the skin microbiome in psoriasis: A review. Clin Dermatol. 2019;37(2):160–166. doi: 10.1016/j.clindermatol.2019.01.011Ng CY, Huang YH, Chu CF, Wu TC, Liu SH. Risks for Staphylococcus aureus colonization in patients with psoriasis: a systematic review and meta-analysis. Br J Dermatol. 2017;177(4):967–977. doi: 10.1111/bjd.15366Chen L, Li J, Zhu W, Kuang Y, Liu T, Zhang W, Chen X, et al. Skin and Gut Microbiome in Psoriasis: Gaining Insight Into the Pathophysiology of It and Finding Novel Therapeutic Strategies. Front Microbiol. 2020;11:589726. doi.org/10.3389/fmicb.2020.589726Niebuhr M, Scharonow H, Gathmann M, Mamerow D, Werfel T. Staphylococcal exotoxins are strong inducers of IL-22: A potential role in atopic dermatitis. J Allergy Clin Immunol. 2010;126(6):1176-83.e4. doi: 10.1016/j.jaci.2010.07.041Rodríguez-Cortes O, García-López ES, Cancino-Diaz ME. Peptidoglycan from Staphylococcus aureus has an anti-apoptotic effect in HaCaT keratinocytes mediated by the production of the cellular inhibitor of apoptosis protein-2. Microbiol Immunol. 2014;58(2):87–95. doi: 10.1111/1348-0421.12126