The role of the skin and intestinal microbiota in pathogenesis of some skin diseases in HIV-infected patients


DOI: https://dx.doi.org/10.18565/epidem.2019.9.1.107-14

Evdokimov E.Yu., Sundukov A.V., Gorelova E.A.

1 Central Research Institute of Epidemiology, Russian Federal Service for Supervision of Consumer Rights Protection and Human Well-Being, Moscow, Russia; 2 A.I. Yevdokimov Moscow State University of Medicine and Dentistry, Ministry of Health of Russia, Moscow, Russia
An analysis of the medical literature on the role of the skin and intestinal microbiota in the pathogenesis of some inflammatory skin diseases is presented. The effect of intestinal flora metabolites on the pathogenesis of certain dermatoses is described. Clinical and experimental data on the effect of specific bacterial communities on the pathogenesis of inflammation are presented; the role of interspecific interactions in the microbiota in the development of inflammatory dermatoses is discussed. The distinctive features of microbiotas in HIV-positive and HIV-negative patients suffering from seborrheic dermatitis, psoriasis and atopic dermatitis are presented.
Keywords: inflammatory dermatoses, skin and intestinal microbiota, HIV infection
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Literature

  1. Teruki Dainichi, Sho Hanakawa, Kenji Kabashima. Classification of inflammatory skin diseases: A proposal based on the disorders of the three-layered defense systems, barrier, innate immunity and acquired immunity. J. Dermatol. Sci. 2014; 76(2): 81–9.
  2. Nakamura M., Abrouk M., Farahnik B., Zhu T.H., Bhutani T. Psoriasis treatment in HIV-positive patients: a systematic review of systemic immunosuppressive therapies. Cutis 2018; 101(1): 38, 42, 56.
  3. Seed P.C. The human mycobiome. Cold Spring. Harb. Perspect Med. 2014; 5(5): a019810. DOI: 10.1101/cshperspect.a019810.
  4. Marrs T., Flohr C. The role of skin and gut microbiota in the development of atopic eczema. Br. J. Dermatol. 2016; 175(Suppl 2): 13–8. DOI: 10.1111/bjd.14907.
  5. 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 2016; 38(11): 1167–76. DOI: 10.1002/bies.201600008.
  6. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 2007; 104: 13780–5.
  7. Khalif I.L., Sheligin Yu.A. (eds.). [Atlas. Inflammatory bowel disease: diagnosis and treatment]. Saint-Petersburg: Gippokrat, 2017. 116 р. (In Russ.)
  8. Sonnenburg J.L., Backhed F. Diet-microbiota interactions as moderators of human metabolism. Nature 2016; 535: 56–64.
  9. Gensollen T., Iyer S.S., Kasper D.L., Blumberg R.S. How colonization by microbiota in early life shapes the immune system. Science 2016; 352: 539–44. DOI: 10.1126/science.aad9378.
  10. Remely M., Aumueller E., Merold C. Effects of short chain fatty acid producing bacteria on epigenetic regulation of FFAR3 in type 2 diabetes and obesity. Gene 2014; 537: 85–92.
  11. Loranskaya I.D., Khalif I.L., Boldyreva M.N., Kopaeva V.A. [Characteristics of microbiome in inflammatory bowel diseases]. Eksperimentalnaya i klinicheskaya gastroenterologiya 2018; 153(5): 104–11. (In Russ.).
  12. Miyazaki K., Masuoka N., Kano M., Iizuka R. Bifidobacterium fermented milk and galacto-oligosaccharides lead to improved skin health by decreasing phenols production by gut microbiota. Benef Microbes 2014; 5(2): 121–8.
  13. Osadchuk A.M., Davydkin I.L., Gritsenko T.A., Lebedeva E.A., Petrushin A.E. [The role of microbiota of the gastrointestinal tract in the development of diseases of internal organs] Eksperimentalnaya i klinicheskaya gastroenterologiya 2018; 153(5): 133–9. (In Russ.).
  14. Fouts D.E., Torralba M., Nelson K.E., Brenner D.A., Schnabl B. Bacterial translocation and changes in the intestinal microbiome in mouse models of liver disease. J. Hepatol. 2012; 56(6): 1283–92.
  15. Song H., Yoo Y., Hwang J., Na Y.C., Kim H.S. Faecalibacterium prausnitzii subspecies-level dysbiosis in the human gut microbiome underlying atopic dermatitis. J. Allergy Clin. Immunol. 2016; 137(3): 852–60.
  16. Lindberg M., Söderquist B. Atopic dermatitis and gut microbiota. Br. J. Dermatol. 2017; 176(2): 297–8.
  17. Scher J.U., Ubeda C., Artacho A., Attur M., Isaac S., Reddy S.M. et al. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol. 2015; 67: 128–39.
  18. Noureldein M.H., Eid A.A. Gut microbiota and mTOR signaling: insight on a new pathophysiological interaction. Microb. Pathog. 2018; 118: 98–104. DOI: 10.1016/j.micpath.2018.03.021.
  19. Duman H., Topal I. O., Kocaturk E., Duman M. A. (2016). Evaluation of anxiety, depression, and quality of life in patients with acne vulgaris, and quality of life in their families. DSI 34 6–9. 10.1016/j.dsi.2015.07.002.
  20. Gootenberg D.B., Paer J.M., Luevano J.-M., Kwona D.S. HIV-associated changes in the enteric microbial community: potential role in loss of homeostasis and development of systemic inflammation. Curr. Opin. Infect. Dis. 2017; 30(1): 31–43.
  21. Schuetz A., Deleage C., Sereti I., Rerknimitr R., Phanuphak N., Phuang-Ngern Y. et al. Initiation of ART during early acute HIV infection preserves mucosal Th17 function and reverses HIV-related immune activation. PLoS Pathog. 2014; 10: e1004543.
  22. Okoye A.A., Picker L.J. CD4+ T-cell depletion in HIV infection: mechanisms of immunological failure. Immunol. Rev. 2013; 254: 54–64.
  23. Yongjia Ji, Fengdi Zhang, Renfang Zhang, Yinzhong Shen, Li Liu, Jiangrong Wang et al. Changes in intestinal microbiota in HIV-1-infected subjects following cART initiation: influence of CD4+ T-cell count. Emerg. Microbes Infect. 2018; (7): 113. DOI: 10.1038/s41426-018-0117-y
  24. Aron-Wisnewsky J., Clement K. The gut microbiome, diet, and links to cardiometabolic and chronic disorders. Nat. Rev. Nephrol. 2016; (12): 169–81.
  25. Kosiewicz M.M., Dryden G.W., Chhabra A., Alard P. Relationship between gut microbiota and development of T-cell associated disease. FEBS Letters 2014; 588(22): 4195–206.
  26. Grice E.A., Segre J.A. The skin microbiome. Nat. Rev. Microbiol. 2011; (9), 244–53.
  27. Young J.P., Heung K.L. The role of skin and orogenital microbiota in protective immunity and chronic immune-mediated inflammatory disease. Front Immunol. 2017; (8): 1955. DOI: 10.3389/fimmu.2017.01955.
  28. Oh J., Byrd A.L., Park M., NISC Comparative Sequencing Program, Kong H.H., Segre J.A. Temporal stability of the human skin microbiome. Cell 2016; 165(4): 854–66. DOI: 10.1016/j.cell.2016.04.008.
  29. Scharschmidt T.C., Vasquez K.S., Truong H.A., Gearty S.V., Pauli M.L., Nosbaum A. et al. A Wave of regulatory T-cells into neonatal skin mediates tolerance to commensal microbes. Immunity 2015; 43: 1011–21.
  30. Nakatsuji T., Chen T.H., Narala S., Chun K.A., Two A.M., Yun T. et al. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci. Transl. Med. 2017; 9(378): pii: eaah4680. DOI: 10.1126/scitranslmed.aah4680.
  31. Kobayashi T., Glatz M., Horiuchi K., Kawasaki H., Akiyama H., Kaplan D.H. et al. Dysbiosis and Staphylococcus aureus colonization drives inflammation in atopic dermatitis. Immunity 2015; 42: 756–66.
  32. Li Z., Levast B., Madrenas J. Staphylococcus aureus downregulates IP-10 production and prevents Th1 cell recruitment. J. Immunol. 2017; 198(5): 1865–74. DOI: 10.4049/jimmunol.1601336.
  33. Kong H.H., Oh J., Deming C., Conlan S., Grice Е.А., Beatson M.A. et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 2012; 22(5): 850–9. DOI: 10.1101/gr.131029.111
  34. Kennedy E.A., Connolly J., Hourihane J.O., Fallon P.G., McLean W.H.I., Murray D. et al. Skin microbiome before development of atopic dermatitis: early colonization with commensal staphylococci at 2 months is associated with a lower risk of atopic dermatitis at 1 year. J. Allergy Clin. Immunol. 2017; 139(1): 166–72. DOI: 10.1016/j.jaci.2016.07.029.
  35. Byrd A.L., Belkaid Y., Segre J.A. The human skin microbiome. Nat. Rev. Microbiol. 2018; 16(3): 143–55. DOI: 10.1038/nrmicro.2017.157.
  36. Wollenberg M.S., Claesen J., Escapa I.F., Aldridge K.L., Fischbach M.A., Lemon K.P. Propionibacterium-produced coproporphyrin III induces Staphylococcus aureus aggregation and biofilm formation. MBio 2014; 5(4): e01286-14. DOI: 10.1128/mBio.01286-14.
  37. Nakamura Y., Oscherwitz J., Cease K.B., Chan S.M., Munoz-Planillo R., Hasegawa M. et al. Staphylococcus delta-toxin induces allergic skin disease by activating mast cells. Nature 2013; 503: 397–401.
  38. Bomar L., Brugger S.D., Yost B.H., Davies S.S., Lemon K.P. Corynebacterium accolens Releases Antipneumococcal Free Fatty Acids from Human Nostril and Skin Surface Triacylglycerols. MBio 2016; 7(1): e01725-15. DOI: 10.1128/mBio.01725-15.
  39. Johnson T., Kang D., Barnard E., Li H. Strain-Level Differences in Porphyrin Production and Regulation in Propionibacterium acnes Elucidate Disease Associations. mSphere 2016; 1(1): pii: e00023-15. DOI: 10.1128/mSphere.00023-15.
  40. Pace B.T., Lackner A.A., Porter E., Pahar B. The Role of Defensins in HIV Pathogenesis. Mediators Inflamm 2017; 2017: 5186904. http://dx.doi.org/10.1155/2017/5186904
  41. Shet A., Mathema B., Mediavilla J.R., Kishii K., Mehandru S., Jeane-Pierre P. et al. Colonization and subsequent skin and soft tissue infection due to methicillin-resistant Staphylococcus aureus in a cohort of otherwise healthy adults infected with HIV type 1. J. Infect. Dis. 2009; 200(1): 88–93.
  42. Pinto-Cardoso S., Klatt N.R., Reyes-Terána G.. Impact of antiretroviral drugs on the microbiome: unknown answers to important questions. Curr. Opin. HIV АIDS 2018; 13(1): 53–60.
  43. Rincón S., Celis A., Sopó L., Motta A., Cepero de García M.C. Malassezia yeast species isolated from patients with dermatologic lesions. Biomedica 2005; 25: 189–95.
  44. Bakhlykova E.A.. Filimonkova N.N.. Timokhina T.Kh.. Kurlovich N.A. [Skin microbiota in patients with psoriasis vulgaris and pustular psoriasis]. Vestnik dermatologii i venerologii 2016; (2): 47–54. (In Russ.). https://doi.org/10.25208/0042-4609-2016-0-2-47-54
  45. Fahlén 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.
  46. Gomez-Moyano E., Crespo-Erchiga V., Martínez-Pilar L., Godoy Diaz D., Martínez-García S., Lova Navarro M. et al. 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.
  47. Mukherjee P.K., Chandra J., Retuerto M., Sikaroodi M., Brown R.E., Jurevic R. Oral Mycobiome Analysis of HIV-Infected Patients: Identification of Pichia as an Antagonist of Opportunistic Fungi. PLoS Pathog. 2014; 10(3): e1003996.
  48. Tipton L., Müller C.L., Kurtz Z.D., Huang L., Kleerup E., Morris A. et al. Fungi stabilize connectivity in the lung and skin microbial ecosystems. Microbiome 2018; 6(1): 12. DOI: 10.1186/s40168-017-0393-0.


About the Autors

Evgeniy Y. Evdokimov, Cand. Med. Sci., Researcher, Clinical Department of Infectious Diseases, Central Research Institute of Epidemiology, Russian Federal Service for Supervision of Consumer Rights Protection and Human Well-Being, Moscow, Russia; е-mail: evdokimovevg@yandex.ru; ORCID: http//orcid.org/ 0000-0003-2694-8900
Aleksandr V. Sundukov, MD, Professor, Department of Infectious Diseases and Epidemiology, A.I. Evdokimov Moscow State University of Medicine and Dentistry, Ministry of Health of Russia, Moscow, Russia; e-mail: sunducov1961@mail.ru; ORCID: http//orcid.org/0000-0002-3798-7780
Elena A. Gorelova, Cand. Med. Sci., Researcher, Clinical Department of Infectious Diseases, Central Research Institute of Epidemiology, Russian Federal Service for Supervision of Consumer Rights Protection and Human Well-Being, Moscow, Russia; е-mail: doctorgorelovaea@yandex.ru; ORCID: http//orcid.org/ 0000-0002-3861-6375


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