Immunological and genetic features of pathogenetic association between psoriasis and colonic dysbiosis

Cover Page


Cite item

Full Text

Abstract

Psoriasis is a multifactorial systemic immune-associated disease. It is assumed that colonic dysbiosis may contribute to its development. In this review we provide the data on colonic dysbiosis in induction and progression of psoriatic inflammation assessing a role for bacterial species: Akkermansia muciniphila, Faecalibacterium prausnitzii and Escherichia coli. On one hand, these bacterial species indicate at state of dysbiotic bacterial communities, whereas on the other hand, they are functionally associated with triggering a chain of events inducing impaired intestinal barrier transforming into chronic inflammation in the colonic mucosa and systemic inflammation. Such a scenario leads to the altered systemic reactivity of innate and adaptive immune cells, impaired function of regulatory immune cells resulting in expansion of the autoreactive skin T-cells and induction of psoriatic inflammation due to molecular mimicry between persistent Streptococcus pyogenes and cutaneous antigens. The psoriatic process is envisioned as a comorbidity with inflammatory bowel diseases. Since dysbiotic changes in psoriasis and inflammatory bowel diseases (e.g. Crohn's disease) display similar features, these diseases might potentially proceed via a similar pathogenetic chain resulting from dysbiotic changes in intestinal microbiota towards impaired intestinal barrier, chronic systemic inflammation and altered anti-inflammatory immune arm. Therefore, the data on pathogenetic pathways of the diseases comorbid with psoriasis are able to uncover yet-unknown pathogenetic components for the latter. Psoriasis as a genetically-determined disease is currently believed to be associated with single nucleotide polymorphisms (SNP) in more than four hundred genes. A role for diverse SNPs in candidate genes involved in psoriasis pathogenetic chain in antigen processing and presentation, migration of immune cells, pro-inflammatory cytokine ligation and production is discussed. Crohn's disease is associated with single nucleotide polymorphisms of the genes encoding intestinal barrier proteins potentially underlying its functional deficiency. In connection with comorbidity and similarity between microbiota-associated pathogenetic psoriasis chain and inflammatory bowel diseases, it is possible to assume that such SNPs accounting for genetic defects in the intestinal barrier are manifested as dysbiotic changes in colonic bacterial community and contribute to progression not only of inflammatory bowel diseases, but psoriasis as well.

About the authors

A. A. Goncharov

Perm State Medical University named after academician E.A. Wagner

Author for correspondence.
Email: cool.alex919@yandex.ru
ORCID iD: 0000-0002-8099-8602

Aleksei A. Goncharov - PhD Student, Perm State Medical University named after academician E.A. Wagner.

614000, Perm, Petropavlovskaya str., 26.

Phone: +7 (950) 449-08-33 (mobile)

Россия

O. V. Dolgikh

Federal Scientific Center of Medical and Preventive Health Risk Management Technologies

Email: oleg@fcrisk.ru
ORCID iD: 0000-0003-4860-3145

PhD, MD (Medicine), Professor, Head of the Department of Immunobiological Diagnostic Methods, Federal Scientific Center of Medical and Preventive Health Risk ManagemenTechnologies.

Perm.

Россия

References

  1. Гумаюнова Н.Г., Потатуркина-Нестерова Н.И., Нестеров А.С. Состояние тонкокишечной микробиоты при псориатической болезни // Ульяновский медико-биологический журнал. 2016. № 3. С. 28—35.
  2. Кубанов А.А., Кубанова А.А., Карамова А.Э., Минеева А.А. Распространенность генетических факторов риска псориаза среди населения Российской Федерации // Вестник дерматологии и венерологии. 2014. № 6. С. 69—76. doi: 10.25208/0042-46092014-0-6-69-76
  3. Нестеров А.С., Гумаюнова Н.Г., Потатуркина-Нестерова Н.И., Пантелеев С.В., Шроль О.Ю. Патогенетически значимые изменения толстокишечной микробиоты при псориазе // Ульяновский медико-биологический журнал. 2016. № 1. С. 80-87.
  4. Песляк М.Ю. Модель патогенеза псориаза. Часть 1. Системный псориатический процесс. М.: MYPE, 2012. 94 с. doi: 10.13140/2.1.1848.2248
  5. Песляк М.Ю. Модель патогенеза псориаза. Часть 2. Локальный псориатический процесс. М.: MYPE, 2012. 116 с. doi: 10.13140/2.1.3290.0166
  6. Толмачова Н.В., Анисимова А.С. Современный взгляд на этиологию и патогенез псориаза // Фундаментальные исследования. 2015. № 1. С. 2118-2121.
  7. Arpaia N., Campbell C., Fan X., Dikiy S., van der Veeken J., deRoos P., Liu H., Cross J.R., Pfeffer K., Coffer P.J., Rudensky A.Y. Metabolites produced by commensal bacteria promote peripheral regulatory T cell generation. Nature, 2013, vol. 504, iss. 7480, pp. 451—455. doi: 10.1038/nature12726
  8. Ayala-Fontanez N., Soler D.C., McCormick T.S. Current knowledge on psoriasis and autoimmune diseases. Psoriasis: Targets and Therapy, 2016, vol. 6, pp. 7-32. doi: 10.2147/PTT.S64950
  9. Behrouzi A., Vaziri F., Riazi-Rad F., Amanzadeh A., Fateh A., Moshiri A., Khatami S., Siadat S.D. Comparative study of pathogenic and non-pathogenic Escherichia coli outer membrane vesicles and prediction of host-interactions with TLR signaling pathways. BMC Res. Notes, 2018, vol. 11: 539. doi: 10.1186/s13104-018-3648-3
  10. Bein A., Zilbershtein A., Golosovsky M., Davidov D., Schwartz B. LPS induces hyper-permeability of intestinal epithelial cells. J. Cell. Physiol., 2017, vol. 232, iss. 2, pp. 381-390. doi: 10.1002/jcp.25435
  11. Benhadou F., Mintoff D., Schnebert B., Thio H.B. Psoriasis and microbiota: a systematic review. Diseases, 2018, vol. 6, iss. 2. doi: 10.3390/diseases6020047
  12. Benhadou F., Mintoff D., del Marmol V. Psoriasis: Keratinocytes or immune cells — which is the trigger? Dermatology, 2019, vol. 235, no. 2, pp. 91-100. doi: 10.1159/000495291
  13. Beranek M., Zdenek F., Kremlacek J., Andrys C., Krejsek J., Hamakova K., Chmelarova M., Palicka V., Borska L. Changes in circulating cell-free DNA and nucleosomes in patients with exacerbated psoriasis. Arch Dermatol. Res., 2017, vol. 309, iss. 10, pp. 815-821. doi: 10.1007/s00403-017-1785-5
  14. Bovenschen H.J., van de Kerkhof P.C., van Erp P.E., Woestenenk R., Joosten I., Koenen H.J.P.M. Foxp3+ Regulatory T cells of psoriasis patients easily differentiate into IL-17A-producing cells and are found in lesional skin. J. Investig. Dermatol., 2011, vol. 131, iss. 9, pp. 1853-1860. doi: 10.1038/jid.2011.139
  15. De Jesus-Gil C., Ruiz-Romeu E., Ferran M., Chiriac A., Deza G., Hollo P., Celada A., Pujol R.M., Santamaria-Babi L.F. CLA+ T cell response to microbes in psoriasis. Front. Immunol., 2018, vol. 9. doi: 10.3389/fimmu.2018.01488
  16. Diani M., Altomare G., Reali E. T cell responses in psoriasis and psoriatic arthritis. Autoimmun. Rev., 2015, vol. 14, iss. 4, pp. 286292. doi: 10.1016/j.autrev.2014.11.012 doi: 10.1016/j.autrev.2014.11.012
  17. Ding Y., Xu J., Bromberg J.S. T regulatory cell migration during an immune response. Trends Immunol., 2012, vol. 33, iss. 4, pp. 174 -180. doi: 10.1016/j.it.2012.01.002
  18. Eiris N., Gonzalez-Lara L., Santos-Juanes J., Queiro R., Coto E., Coto-Segura P. Genetic variation at IL12B, IL23R and IL23A is associated with psoriasis severity, psoriatic arthritis and type 2 diabetes mellitus. J. Dermatol. Sci., 2014, vol. 75, iss. 3, pp. 167172. doi: 10.1016/j.jdermsci.2014.05.010
  19. Elder J.T., Bruce A.T., Gudjonsson J.E., Johnston A., Stuart P.E., Tejasvi T., Voorhees J.J., Abecasis C.R., Nair R.P. Molecular dissection of psoriasis: integrating genetics and biology. J. Investig. Dermatol., 2010, vol. 130, iss. 5, pp. 1213-1226. doi: 10.1038/jid.2009.319
  20. Ellinghaus E., Stuart P.E., Nair R.P., Ellinghaus E., Ding J., Tejasvi T., Gudjonsson J.E., Li Y., Weidinger S., Eberlein B., Gieger C., Wichmann H.E., Kunz M., Ike R., Krueger G.G., Bowcock A.M., Mrowietz U., Lim H.W., Voorhees J. J., Abecasis C.R., Weichenthal М., Franke А., Rahman Р., Gladman D.D., Elder J.T. Genome-wide asociation analysis identifies three psoriasis susceptibility loci. Nat. Genet., 2010, vol. 42, no. 11, pp. 1000—1005. doi: 10.1038/ng.693
  21. Ferreira-Halder C.V., de Sousa A.V.F., Andrade S.S. Action and function of Faecalibacterium prausnitzii in health and disease. Best Pract. Res. Clin. Gastroenterol., 2017, vol. 31, iss. 6, pp. 643—648. doi: 10.1016/j.bpg.2017.09.011
  22. Furnes O.S., FerencSipos G.M. Dysbiotic gut microbiome: a key element of Crohn's disease. Comp. Immunol. Microbiol. Infect. Dis, 2015, vol. 43, pp. 36- 49. doi: 10..1016/j.cimid.2015..10.005
  23. Fusco D.D., Dinallo V., Monteleone I., Laudisi F., Marafini I., Franze E., Di Grazia A., Dwairi R., Colantoni A., Ortenzi A., Stolfi C., Monteleone G. Metformin inhibits inflammatory signals in the gut by controlling AMPK and p38 MAP kinase activation. Clin. 5ci. (Lond.), 2018, vol. 132, iss. 11, pp. 1155-1168. doi: 10.1042/C520180167
  24. Ganguly D., Haak S., Sisirak V., Reizis B. The role of dendritic cells in autoimmunity. Nat. Rev. Immunol., 2013, vol. 13, iss. 8, pp. 566-577. doi: 10.1038/nri3477
  25. Garcia-Hernandez V., Quiros M., Nusrat A. Intestinal epithelial claudins: expression and regulation in homeostasis and inflammation. Ann. NY Acad. 5ci., 2017, vol. 1397, iss. 1, pp. 66- 79. doi: 10.1111/nyas.13360
  26. Georgescu S.R., Tampa M., Caruntu C., Sarbu M.I., Mitran C.I., Mitran M.I., Matei C., Constantin C., Neagu M. Advances in understanding the immunological pathways in psoriasis. Int. J. Mol. 5ci., 2019, vol. 20, iss. 3. doi: 10. 3390/ijms20030739
  27. Glas J., Seiderer J., Wagner J., Olszak T., Fries C., Tillack C., Friedrich M., Beigel F., Stallhofer J., Steib C., Wetzke M., Goke B., Ochsenkuhn T., Diegelmann J., Czamara D., Brand S. Analysis of IL12B gene variants in inflammatory bowel disease. PLo5 One, vol. 7, iss. 3: e34349. doi: 10.1371/journal.pone.0034349
  28. Goodman W.A., Levine A.D., Massari J.V., Sugiyama H., McCormick T.S., Cooper K.D. IL-6 signaling in psoriasis prevents immune suppression by regulatory T cells. J. Immunol., 2009, vol. 183, iss. 5, pp. 3170-3176. doi: 10.4049/jimmunol.0803721
  29. Grainger J., Daw J., Wemyss K. Systemic instruction of cell-mediated immunity by the intestinal microbiome [version 1; referees: 2 approved]. F1000Research 2018, 7(F1000 Faculty Rev). doi: 10.12688/f1000research.14633.1
  30. Guo J., Zhou X. Regulatory T cells turn pathogenic. Cell. Mol. Immunol., 2015, vol. 12, pp. 525-532. doi: 10.1038/cmi.2015.12
  31. Haines E.P. Is psoriasis a bowel disease? Successful treatment with bile acids and bioflavonoids suggests it is. Clin. Dermatol., 2018, vol. 36, iss. 3, pp. 376-389. doi: 10.1016/j.clindermatol.2018.03.011
  32. Huang L., Gao R., Yu N., Zhu Y., Ding Y., Qin H. Dysbiosis of gut microbiota was closely associated with psoriasis. 5ci. China Life 5ci., 2019, vol. 62, iss. 6, pp. 807-815. doi: 10.1007/s11427-018-9376-6
  33. Hubbard L.L. N., Moore B.B. IRAK-M regulation and function in host defense and immune homeostasis. Infect. Dis. Rep., 2010, vol. 2: e9. doi: 10.4081/idr.2010.e9
  34. Hugh J.M., Weinberg J.M. Update on the pathophysiology of psoriasis . Cutis, 2018, vol. 102, no. 55, pp. 6-12.
  35. Ichiyama K., Yoshida H., Wakabayashi Y., Chinen T., Saeki K., Nakaya M., Takaesu G., Hori S., Yoshimura A., Kobayashi T. Foxp3 inhibits RORgamma t-mediated IL-17A mRNA transcription through direct interaction with RORgamma t. J. Biol. Chem., 2008, vol. 283, pp. 17003-17008. doi: 10.1074/jbc.M801286200
  36. Jadali Z., Eslami M.B. T cell immune responses in psoriasis. Iran J. Allergy Asthma Immunol., 2014, vol. 13, no. 4, pp. 220-230.
  37. Javan M.R., Shahraki S., Safa A., Zamani M.R., Salmaninejad A., Aslani S. An interleukin 12 B single nucleotide polymorphism increases IL-12p40 production and is associated with increased disease susceptibility in patients with relapsing-remitting multiple sclerosis. Neurological Research, vol. 39, iss. 5, pp. 435- 441. doi: 10.1080/01616412.2017.1301623
  38. Kahlenberg J.M., Kaplan M.J. Little peptide, big effects: the role of LL-37 in inflammation and autoimmune disease. J. Immunol., 2013, vol. 191, iss. 10, pp. 4895-4901. doi: 10.4049/jimmunol.1302005
  39. Khasawneha A., Barathb S., Medgyesia B., Bekea G., Dajnokia Z., Gaspara K., Jeneia A., Pogacsasa L., Pazmandic K., Gaald J., Bacsic A., Szegedia A., Kapitany A. Myeloid but not plasmacytoid blood DCs possess Th1 polarizing and Th1/Th17 recruiting capacity in psoriasis. Immunol. Lett., 2017, vol. 189, pp. 109-113. doi: 10.1016/j.imlet.2017.04.005
  40. Kim T.G., Kim S.H., Lee M.G. The origin of skin dendritic cell network and its role in psoriasis. Int. J. Mol. 5ci., 2018, vol. 19: 42. doi: 10.3390/ijms19010042
  41. Komatsu N., Okamoto K., Sawa S., Nakashima T., Oh-hora M., Kodama T., Tanaka S., Bluestone J.A., Takayanagi H. Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis. Nat. Med., 2014, vol. 20, pp. 62-68. doi: 10.1038/nm.3432
  42. Kun-Ju Z., Zhu C.Y., Shi G., Fan Y.M. Meta-analysis of IL12B polymorphisms (rs3212227, rs6887695) with psoriasis and psoriatic arthritis. Rheumatol. Int., 2013, vol. 33, pp. 1785-1790. doi: 10.1007/s00296-012-2637-4
  43. Laurence M., Tan J., Vieira A.T., Leach K., Stanley D., Luong S., Maruya M., McKenzie C.I., Hijikata A., Wong C., Binge L., Thorburn A.N., Chevalier N., Ang C., Marino E., Robert R., Offermanns S., Teixeira M.M., Moore R.J., Flavell R.A., Fagarasan S., Mackay C.R. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat. Commun., 2015, vol. 6: 6734. doi: 10.1038/ncomms7734
  44. Liu J.Z., van Sommeren S., Huang H., Ng S.C., Alberts R., Takahashi A., Ripke S., Lee J.S., Jostins L., Shah T., Abedian S., Cheon J.H., Cho J., Dayani N.E., Franke L., Fuyuno Y., Hart A., Juyal R.C., Juyal G., Kim W.H., Morris A.P., Poustchi H., Newman W.G., Midha V., Orchard T.R., Vahedi H., Sood A., Sung J.Y., Malekzadeh R., Westra H.J., Yamazaki K., Yang S.K., Barrett J.C., Alizadeh B.Z., Parke M., Thelma B.K., Daly M.J., Kubo M., Anderson C.A., Weersma R.K. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat. Genet., 2015, vol. 47, pp. 979-986. doi: 10.1038/ng.3359
  45. Liu Y., Lagowski J., Gao S., Raymond J., White C.R., Kulesz-Martin M. Regulation of psoriatic chemokine CCL20 by E3 ligases Trim32 and Piasy in keratinocytes. J. Invest. Dermatol., 2010, vol. 130, pp. 1384-1390. doi: 10.1038/jid.2009.416
  46. Longman R.S., Yang Y., Diehl G.E., Kim S.V., Littman D.R. Microbiota: host interactions in mucosal homeostasis and systemic autoimmunity. Cold 5pring Harb. 5ymp. Quant. Biol., 2014, vol. 78, pp. 193-201. doi: 10.1101/sqb.2013.78.020081
  47. Lopez de Castro J.A. How ERAP1 and ERAP2 shape the peptidomes of disease-associated MHC-I proteins. Front. Immunol., 2018, vol. 9: 2463. doi: 10.3389/fimmu.2018.02463
  48. Mabuchi T., Chang T.W., Quinter S., Hwang S.T. Chemokine receptors in the pathogenesis and therapy of psoriasis. J. Dermatol. Sci., 2012, vol. 65, pp. 4-11. doi: 10.1016/j.jdermsci.2011.11.007
  49. Maciejewska-Radomska A., Szczerkowska-Dobosz A., Rębała K., Wysocka J., Roszkiewicz J., Szczerkowska Z., Placek W. Frequency of streptococcal upper respiratory tract infections and HLA-Cw*06 allele in 70 patients with guttate psoriasis from northern Poland. Postep. Derm. Alergol., 2015, vol. 32, pp. 455-458. doi: 10.5114/pdia.2014.40982
  50. Maeda Y., Kurakawa T., UmemotoE., Motooka D., Ito Y., Kazuyoshi Gotoh, Hirota K., Matsushita M., Furuta Y., Narazaki M., Sakaguchi N., KayamaH., Nakamura S., IidaT., Saeki Y., Kumanogoh A., Sakaguchi S., Takeda K. Dysbiosis contributes to arthritis development via activation of autoreactive T cells in the intestine. Arthritis Rheumatol., 2016, vol. 68, no. 11, pp. 2646-2661. doi: 10.1002/art.39783
  51. Mei-Jun Z., Sun X., Du M. AMPK in regulation of apical junctions and barrier function of intestinal epithelium. Tissue Barriers, 2018, vol. 6, 13 p. doi: 10.1080/21688370.2018.1487249
  52. Miao W., Wu X., Wang K., Wang W., Wang Y., Li Z., Liu J., Li L., Peng L. Sodium butyrate promotes reassembly of tight junctions in Caco-2 monolayers involving inhibition of MLCK/MLC2 pathway and phosphorylation of PKCe2. Int. J. Mol. Sci., 2016, vol. 17, iss. 10: 1696. doi: 10.3390/ijms17101696
  53. Micenkova L., Frankovicova L., Jabornlkova I., Bosak J., Dlte P., Smarda J., Vrba M., Sevclkova A., Kmetova M., Smajs D. Escherichia coli isolates from patients with inflammatory bowel disease: ExPEC virulence- and colicin-determinants are more frequent compared to healthy controls. Int. J. Med. Microbiol., 2018, vol. 308, iss. 5, pp. 498-504. doi: 10.1016/j.ijmm.2018.04.008
  54. Mobbs J.I., Illing P.T., Dudek N.L., Brooks A.G., Baker D.G., Purcell A.W., Rossjohn J., Vivian J.P. The molecular basis for peptide repertoire selection in the human leukocyte antigen (HLA) C*06:02 molecule. J. Biol. Chem., 2017, vol. 292, pp. 17203-17215. doi: 10.1074/jbc.M117.806976
  55. Morrison D.J., Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes, 2016, vol. 7, iss. 3, pp. 189-200. doi: 10.1080/19490976.2015.1134082
  56. Nair R.P., Duffin K.C., Helms C., Ding J., Stuart P.E., Goldgar D., Gudjonsson J.E., Li Y., Tejasvi T., Feng B.J., Ruether A., Schreiber S., Weichenthal M., Gladman D., Rahman P., Schrodi S.J., Prahalad S., Guthery S.L., Fischer J., Liao W., Kwok P.Y., Menter A., Lathrop G.M., Wise C.A., Begovich A.B., Voorhees J.J., Elder J.T., Krueger G.G., Bowcock A.M., Abecasis G.R. Genomewide scan reveals association of psoriasis with IL-23 and NF-kB pathways. Nat. Genet., 2009, vol. 41,pp. 199-204. doi: 10.1038/ng.311
  57. Nasrin G.M., Crowther N.J., Tikly M. Double trouble: psoriasis and cardiometabolic disorders. Cardiovasc. J. Afr., 2018, vol. 29, no. 3, pp. 189-194. doi: 10.5830/CVJA-2017-055
  58. Nighot M., Al-Sadi R., Guo S., Rawat M., Nighot P., Watterson M.D., Ma T.Y. Lipopolysaccharide-induced increase in intestinal epithelial tight permeability is mediated by Toll-like receptor 4/myeloid differentiation primary response 88 (MyD88) activation of myosin light chain kinase expression. Am. J. Pathol., 2017, vol. 187, no. 12, pp. 2698-2710. doi: 10.1016/j.ajpath.2017.08.005
  59. Noren E. Genetic variation of tight junction structures in intestinal inflammation. Thesis for Doctoral Degree (Ph.D.). Department of Medicine, Solna, 2016. 99 p.
  60. Ottman N., Geerlings S.Y., Aalvink S., de Vos W.M., Belzer C. Action and function of Akkermansia muciniphila in microbiome ecology, health and disease. Best Pract. Res. Clin. Gastroenterol., 2017, vol. 31, iss. 6, pp. 637-642. doi: 101016/j.bpg.2017.10.001
  61. Owczarczyk-Saczonek A., Czerwinska J., Placek W. The role of regulatory T cells and anti-inflammatory cytokines in psoriasis. Acta Dermatovenerol. APA, 2018, vol. 27, pp. 17-23. doi: 10.15570/actaapa.2018.4
  62. Parthasarathy A., Cross P.J., Dobson R.C. J., Adams L.E., Savka M.A., Hudson A.O. A three-ring circus: metabolism of the three proteogenic aromatic amino acids and their role in the health of plants and animals. Front. Mol. Biosci., 2018, vol. 5: 29. doi: 10.3389/fmolb.2018.00029
  63. Prinz J.C. Human leukocyte antigen-class I alleles and the autoreactive T cell response in psoriasis pathogenesis. Front. Immunol., 2018, vol. 9: 954. doi: 10.3389/fimmu.2018.00954
  64. Quiros M., Nusrat A. RhoGTPases, actomyosin signaling and regulation of the epithelial apical junctional complex. Semin. Cell. Dev Biol., 2014, vol. 36, pp. 194-203. doi: 10.1016/j.semcdb.2014.09.003
  65. Ramirez-Bosca A., Navarro-Lopez V., Martinez-Andres A., Such J., Frances R., Horga de la Parte J., Asm-Llorca M. Identification of bacterial DNA in the peripheral blood of patients with active psoriasis. JAMA Dermatol., 2015, vol. 151. doi: 10.1001/jamader-matol.2014.5585
  66. Rendon A., Schake K. Psoriasis pathogenesis and treatment. Int. J. Mol. Sci., 2019, vol. 20, iss. 6:1475. doi: 10.3390/ijms20061475
  67. Rodgers Laurel S., Beam M.T., Anderson J.M., Fanning A.S. Epithelial barrier assembly requires coordinated activity of multiple domains of the tight junction protein ZO-1. J. Cell. Sci., 2013, vol. 126, pp. 1565-1575. doi: 10.1242/jcs.113399
  68. Rowart P., Wu J., Caplan M.J., Jouret F. Implications of AMPK in the formation of epithelial tight junctions. Int. J. Mol. Sci., 2018, vol. 19, no. 7: 2040. doi: 10.3390/ijms19070040
  69. Sai M.J., Talukdar R., Subramanyam C., Vuyyuru H., Sasikala M., Reddy D.N. Role of the normal gut microbiota. World J. Gastroenterol., 2015, vol. 21, iss. 29, pp. 8787-8803. doi: 10.3748/wjg.v21.i29.8787
  70. Shapiro J., Cohen N.A., Shalev V., Uzan A., Koren O., Maharshak N. Psoriatic patients have a distinct structural and functional fecal microbiota compared with controls. J. Dermatol., 2019, vol. 46, iss. 7, pp. 595-603. doi: 10.1111/1346-8138.14933
  71. Sharm A., Adarsh M.B., Dogra S., Vaiphei K., Vaishnavi C., Sinha S.K. Evaluation of subclinical gut inflammation using faecal calprotectin levels and colonic mucosal biopsy in patients with psoriasis and psoriatic arthritis. Br. J. Dermatol., 2019, vol. 181, iss. 2, pp. 401-402. doi: 10.1111/bjd.17745
  72. Shimizu J., Suzuki N. Enhanced Th17 responses with intestinal dysbiosis in human allergic, inflammatory, and autoimmune diseases. Biomed. Res. Clin. Prac., 2016, vol. 1, pp. 58-61. doi: 10. 15761/BRCP.1000113
  73. Sikora M., Szcz M.C., Maciejewski C., Zaremba M., Waskiel A., Olszewska M., Rudnicka L. J. Dermatol., 2018, vol. 45, iss. 12, pp. 1468-1470. doi: 10.1111/1346-8138.14647
  74. Singh T.P., Zhang H.H., Borek I., Wolf P., Hedrick M.N., Singh S.P., Kelsall B.L., Clausen B.E., Farber J.M. Monocyte-derived inflammatory Langerhans cells and dermal dendritic cells mediate psoriasis-like inflammation. Nat. Commun., 2016, vol. 7: 13581. doi: 10.1038/ncomms13581
  75. Soler D.C., McCormick T.S. The dark side of regulatory T cells in psoriasis. J. Invest. Dermatol., 2011, vol. 131, iss. 9, pp. 1785— 1786. doi: 10.1038/jid.2011.200
  76. Sprouse M.L., Bates N.A., Felix K.M., Joyce Wu H.J. Impact of gut microbiota on gut — distal autoimmunity: a focus on T cells. Immunology, 2019, vol. 156, iss. 4, pp. 305—318. doi: 10.1111/imm.13037
  77. Stockenhuber K., Hegazy A.N., West N.R., Ilott N.E., Stockenhuber A., Bullers S.J., Thornton E.E., Arnold I.C., Tucci A., Waldmann H., Ogg G.S., Powrie F. Foxp3+ T reg cells control psoriasiform inflammation by restraining an IFN-I-driven CD8+ T cell response. J. Exp. Med., 2018, vol. 215, no. 8, pp. 1987—1998. doi: 10.1084/jem.20172094
  78. Strange A., Capon F., Spencer C.C., Knight J., Weale M.E., Allen M.H., Barton A., Band G., Bellenguez C., Bergboer J.G., Blackwell J.M., Bramon E., Bumpstead S.J., Casas J.P., Cork M.J., Corvin A., Deloukas P., Dilthey A., Duncanson A., Edkins S., Estivill X., Fitzgerald O., Freeman C., Giardina E., Gray E., Hofer A., Huffmeier U., Hunt S.E., Irvine A.D., Jankowski J., Kirby B., Langford C., Lascorz J., Leman J., Leslie S., Mallbris L., Markus H.S., Mathew C.G., McLean W.I., McManus R., Mossner R., Moutsianas L., Naluai A.T., Nestle F., Novelli G., Onoufriadis A., Palmer C.N., Perricone C., Pirinen M., Plomin R., Potter S.C., Pujol R.M., Rautanen A., Riveira-Munoz E., Ryan A.W., Salmhofer W., Samuelsson L., Sawcer S.J., Schalkwijk J., Smith C.H., Stahle M., Su Z., Tazi-Ahnini R., Traupe H., Viswanathan A.C., Warren R.B., Weger W., Wolk K., Wood N., Worthington J., Young S.H., Zeeuwen P.L., Hayday A., Burden A.D., Griffiths C., Kere J., Reis A., McVean G., Evans D.M., Brown M.A., Barker J.N., Peltonen L, Donnelly P., Trembath R.C. Genome-wide association study identifies new psoriasis susceptibility loci and an interaction between HLA-C and ERAP1. Nat. Genet., 2010, vol. 42, pp. 985-990. doi: 10.1038/ng.694
  79. Stuart P.E., Nair R.P., Tsoi L.C., Tejasvi T., Das S., Kang H.M., Ellinghaus E., Chandran V., Callis-Duffin K., Ike R., Li Y., Wen X., Enerback C., Gudjonsson J.E., Koks S., Kingo K., Esko T., Mrowietz U., Reis A., Wichmann H.E., Gieger C., Hoffmann P., Nothen M.M., Winkelmann J., Kunz M., Moreta E.G., Mease P.J., Ritchlin C.T., Bowcock A.M., Krueger G.G., Lim H.W., Weidinger S., Weichenthal M., Voorhees J.J., Rahman P., Gregersen P.K., Franke A., Gladman D.D., Abecasis G.R., Elder J.T. Genome-wide association analysis of psoriatic arthritis and cutaneous psoriasis reveals differences in their genetic architecture. Am. J. Hum. Genet., 2015, vol. 97, iss. 6, pp. 816-836. doi: 10.1016/j.ajhg.2015.10.019
  80. Tan L., Zhao S., Zhu W., Wu L., Li J., Shen M., Li L., Chen X., Peng C. The Akkermansia muciniphila is a gut microbiota signature in Psoriasis. Exp. Dermatol., 2018, vol. 27, iss. 2, pp. 144-149. doi: 10.1111/exd.13463
  81. Visser M.J. E., Kell D.B., Pretorius E. Bacterial dysbiosis and translocation in psoriasis vulgaris. Front. Cell. Infect. Microbiol., 2019, vol. 9: 7. doi: 10.3389/fcimb.2019.00007
  82. Wang L., Beier U.H., Akimova T., Dahiya S., Samanta R.H. A., Levine M.H., Hancock W.W. Histone/protein deacetylase inhibitor therapy for enhancement of Foxp3+ T-regulatory cell function posttransplantation. Am. J. Transplant., 2018, vol. 18, iss. 7, pp. 1596-1603. doi: 10.1111/ajt.14749
  83. Wang L., Yang L., Gao L., Gao T.W., Li W., Liu Y.F. A functional promoter polymorphism in monocyte chemoattractant pro-tein-1 is associated with psoriasis. Int. J. Immunogenet., 2008, vol. 35, iss. 1, pp. 45-49. doi: 10.1111/j.1744-313X.2007.00734.x
  84. Willems M., Dubois N., Musumeci L., Bours V., Robe P.A. IkBZ: an emerging player in cancer. Oncotarget, 2016, vol. 7, iss. 40, pp. 6631 0- 66322. doi: 10.18632/oncotarget.11624
  85. Xu K., Yang W.Y., Nanayakkara G.K., Shao Y., Yang F., Hu W., Choi E.T., Wang H., Yang X. GATA3, HDAC 6, and Bcl6 regulate Foxp3+ Treg plasticity and determine Treg conversion into either novel antigen-presenting cell-like Treg or Th1-Treg. Front. Immunol., 2018, vol. 9: 45. doi: 10.3389/fimmu.2018.00045
  86. Yang L., Li B., Dang E., Jin L., Fan X., Wang G. Impaired function of regulatory T cells in patients with psoriasis is mediated by phosphorylation of STAT3. J. Dermatol. Sci., 2016, vol. 81, iss. 2, pp. 85-92. doi: 10.1016/j.jdermsci.2015.11.007
  87. Yue C., Ma B., Zhao Y., Li Q., Li J. Lipopolysaccharide-induced bacterial translocation is intestine site-specific and associates with intestinal mucosal inflammation. Inflammation, 2012, vol. 35, no. 6, pp. 1880-1888. doi: 10.1007/s10753-012-9510-1
  88. Yunusbaeva M., Valiev R., Bilalov F., Sultanova Z., Sharipova L., Yunusbayev B. Psoriasis patients demonstrate HLA- Cw*06:02 allele dosagedependent T cell proliferation when treated with hair follicle-derived keratin 17 protein. Sci. Rep., 2018, vol. 8: 6098. doi: 10.1038/s41598-018-24491-z
  89. Zablotna M., Sobjanek M., Purzycka-Bohdan D., Szczerkowska-Dobosz A., Nedoszytko B., Nowicki R. The -2518 A/G MCP-1 and -403 G/A RANTES promoter gene polymorphisms are associated with psoriasis vulgaris. Clin. Exp. Dermatol., 2016, vol. 41, iss. 8, pp. 878-883. doi: 10.1111/ced.12937
  90. Zohdy M., Sharaf L.A., Abdelnaby S.E., Zalata K.R., Mohamed H.F. Paucity of forkhead box protein 3+ regulatory T-cells in psoriatic skin compared to other inflammatory dermatoses. Indian J. Dermatopathol. Diagn . Dermatol., 2016, vol. 3, iss. 2, pp. 52-56. doi: 10.4103/2349-6029.195220

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2020 Goncharov A.A., Dolgikh O.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies