The gut-skin axis: Investigating gut microbiota dysbiosis in pemphigus and bullous pemphigoid

1 Malik AM, Tupchong S, Huang S, Are A, Hsu S, Motaparthi K. An Updated Review of Pemphigus Diseases. Medicina (Kaunas). 2021 Oct 9;57(10):1080. Search in Google Scholar

2 Pratasava V, Sahni VN, Suresh A et al. Bullous Pemphigoid and Other Pemphigoid Dermatoses. Medicina (Kaunas). 2021 Oct 4;57(10):1061. Search in Google Scholar

3 Ghodsi SZ, Chams-Davatchi C, Daneshpazhooh M, Valikhani M, Esmaili N. Quality of life and psychological status of patients with pemphigus vulgaris using Dermatology Life Quality Index and General Health Questionnaires. J Dermatol. 2012 Feb;39(2):141-4. Search in Google Scholar

4 Kouris A, Platsidaki E, Christodoulou C et al. Quality of life, depression, anxiety and loneliness in patients with bullous pemphigoid. A case control study. An Bras Dermatol. 2016 Sep-Oct;91(5):601-603. Search in Google Scholar

5 Hammers CM, Stanley JR. Mechanisms of Disease: Pemphigus and Bullous Pemphigoid. Annu Rev Pathol. 2016 May 23;11:175-97. Search in Google Scholar

6 Yan L, Wang JM, Zeng K. Association between HLA-DRB1 polymorphisms and pemphigus vulgaris: a meta-analysis. Br J Dermatol. 2012 Oct;167(4):768-77. Search in Google Scholar

7 Moro F, Sinagra JLM, Salemme A, Fania L, Mariotti F, Pira A, Didona B, Di Zenzo G. Pemphigus: trigger and predisposing factors. Front Med (Lausanne). 2023 Dec 27;10:1326359. Search in Google Scholar

8 Moro F, Fania L, Sinagra JLM, Salemme A, Di Zenzo G. Bullous Pemphigoid: Trigger and Predisposing Factors. Biomolecules. 2020 Oct 10;10(10):1432. Search in Google Scholar

9 Shipman AR, Reddy H, Wojnarowska F. Association between the subepidermal autoimmune blistering diseases linear IgA disease and the pemphigoid group and inflammatory bowel disease: two case reports and literature review. Clin Exp Dermatol. 2012 Jul;37(5):461-8. Search in Google Scholar

10 Yoo JY, Groer M, Dutra SVO, Sarkar A, McSkimming DI. Gut Microbiota and Immune System Interactions. Microorganisms. 2020 Oct 15;8(10):1587. Search in Google Scholar

11 Huttenhower C, Kostic AD, Xavier RJ. Inflammatory bowel disease as a model for translating the microbiome. Immunity. 2014 Jun 19;40(6):843-54. Search in Google Scholar

12 Edwards CJ, Costenbader KH. Epigenetics and the microbiome: developing areas in the understanding of the aetiology of lupus. Lupus. 2014 May;23(6):505-6. Search in Google Scholar

13 van der Houwen TB, van Laar JAM, Kappen JH et al. Behçet’s Disease Under Microbiotic Surveillance? A Combined Analysis of Two Cohorts of Behçet’s Disease Patients. Front Immunol. 2020 Jun 12;11:1192. Search in Google Scholar

14 De Pessemier B, Grine L, Debaere M, Maes A, Paetzold B, Callewaert C. Gut-Skin Axis: Current Knowledge of the Interrelationship between Microbial Dysbiosis and Skin Conditions. Microorganisms. 2021 Feb 11;9(2):353. Search in Google Scholar

15 Buhaș MC, Gavrilaș LI, Candrea R et al. Gut Microbiota in Psoriasis. Nutrients. 2022 Jul 20;14(14):2970. Search in Google Scholar

16 Manos J. The human microbiome in disease and pathology. APMIS. 2022 Dec;130(12):690-705 Search in Google Scholar

17 Rinninella E, Raoul P, Cintoni M et al. What is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases. Microorganisms. 2019 Jan 10;7(1):14. Search in Google Scholar

18 Zheng D, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res (2020) 30(6):492–506. Search in Google Scholar

19 Mousa WK, Chehadeh F, Husband S. Microbial dysbiosis in the gut drives systemic autoimmune diseases. Front Immunol. 2022 Oct 20;13:906258. Search in Google Scholar

20 Petta I, Fraussen J, Somers V, Kleinewietfeld M. Interrelation of Diet, Gut Microbiome, and Autoantibody Production. Front Immunol. 2018 Mar 6;9:439. Search in Google Scholar

21 Szymula A, Rosenthal J, Szczerba BM, Bagavant H, Fu SM, Deshmukh US. T cell epitope mimicry between Sjögren’s syndrome Antigen A (SSA)/Ro60 and oral, gut, skin and vaginal bacteria. Clin Immunol. 2014 May-Jun;152(1-2):1-9. Search in Google Scholar

22 Rashid T, Ebringer A. Autoimmunity in Rheumatic Diseases Is Induced by Microbial Infections via Crossreactivity or Molecular Mimicry. Autoimmune Dis. 2012;2012:539282. Search in Google Scholar

23 O’Neill CA, Monteleone G, McLaughlin JT, Paus R. The gut-skin axis in health and disease: A paradigm with therapeutic implications. Bioessays. 2016 Nov;38(11):1167-1176. Search in Google Scholar

24 Ramírez-Boscá A, Navarro-López V, Martínez-Andrés A et al. Identification of Bacterial DNA in the Peripheral Blood of Patients With Active Psoriasis. JAMA Dermatol. 2015 Jun;151(6):6701. Search in Google Scholar

25 Fang H, Li Q, Wang G. The role of T cells in pemphigus vulgaris and bullous pemphigoid. Autoimmun Rev. 2020 Nov;19(11):102661. Search in Google Scholar

26 Shah AA, Sinha AA. Oxidative stress and autoimmune skin disease. Eur J Dermatol. 2013 Jan-Feb;23(1):5-13. Search in Google Scholar

27 Mitra S, De Sarkar S, Pradhan A et al. Levels of oxidative damage and proinflammatory cytokines are enhanced in patients with active vitiligo. Free Radic Res. 2017 Dec;51(11-12):986-994. Search in Google Scholar

28 Ni Q, Zhang P, Li Q, Han Z. Oxidative Stress and Gut Microbiome in Inflammatory Skin Diseases. Front Cell Dev Biol. 2022 Mar 7;10:849985. Search in Google Scholar

29 Liu X, van Beek N, Cepic A et al. The gut microbiome in bullous pemphigoid: implications of the gut-skin axis for disease susceptibility. Front Immunol. 2023 Nov 10;14:1212551. Search in Google Scholar

30 Guo Z, Yiu N, Hu Z et al. Alterations of fecal microbiome and metabolome in pemphigus patients. J Autoimmun. 2023 Dec;141:103108. Search in Google Scholar

31 De Filippis F, Pasolli E, Ercolini D. Newly Explored Faecalibacterium Diversity Is Connected to Age, Lifestyle, Geography, and Disease. Curr Biol. 2020 Dec 21;30(24):4932-4943.e4. Search in Google Scholar

32 Lopez-Siles M, Duncan SH, Garcia-Gil LJ, Martinez-Medina M. Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics. ISME J. 2017 Apr;11(4):841-852. Search in Google Scholar

33 Mahmud MR, Akter S, Tamanna SK et al. Impact of gut microbiome on skin health: gut-skin axis observed through the lenses of therapeutics and skin diseases. Gut Microbes. 2022 Jan-Dec;14(1):2096995. Search in Google Scholar

34 Sokol H, Pigneur B, Watterlot L et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008 Oct 28;105(43):16731-6. Search in Google Scholar

35 Carlsson AH, Yakymenko O, Olivier I et al. Faecalibacterium prausnitzii supernatant improves intestinal barrier function in mice DSS colitis. Scand J Gastroenterol. 2013 Oct;48(10):1136-44. Search in Google Scholar

36 Eppinga H, Sperna Weiland CJ, Thio Hb et al. Similar Depletion of Protective Faecalibacterium prausnitzii in Psoriasis and Inflammatory Bowel Disease, but not in Hidradenitis Suppurativa. J Crohns Colitis. 2016 Sep;10(9):1067-75 Search in Google Scholar

37 Thirion F, Guilly S, Fromentin S et al. Changes in Gut Microbiota of Patients with Atopic Dermatitis During Balneotherapy. Clin Cosmet Investig Dermatol. 2022 Feb 2;15:163-176. Search in Google Scholar

38 Huang S, Mao J, Zhou L, Xiong X, Deng Y. The imbalance of gut microbiota and its correlation with plasma inflammatory cytokines in pemphigus vulgaris patients. Scand J Immunol. 2019 Sep;90(3):e12799. Search in Google Scholar

39 Low L, Suleiman K, Shamdas M et al. Gut Dysbiosis in Ocular Mucous Membrane Pemphigoid. Front Cell Infect Microbiol. 2022 Apr 14;12:780354. Search in Google Scholar

40 Hu X, Wu Q, Fan Y et al. Identification of gut microbiota dysbiosis in bullous pemphigoid under different disease activity. Exp Dermatol. 2023 Dec;32(12):2149-2159. Search in Google Scholar

41 Liu R, Peng C, Jing D et al. Lachnospira is a signature of antihistamine efficacy in chronic spontaneous urticaria. Exp Dermatol. 2022 Feb;31(2):242-247. Search in Google Scholar

42 Nylund L, Nermes M, Isolauri E, Salminen S, de Vos WM, Satokari R. Severity of atopic disease inversely correlates with intestinal microbiota diversity and butyrate-producing bacteria. Allergy. 2015 Feb;70(2):241-4. Search in Google Scholar

43 Vacca M, Celano G, Calabrese FM, Portincasa P, Gobbetti M, De Angelis M. The Controversial Role of Human Gut Lachnospiraceae. Microorganisms. 2020 Apr 15;8(4):573. Search in Google Scholar

44 Boots AW, Haenen GR, Bast A. Health effects of quercetin: from antioxidant to nutraceutical. Eur J Pharmacol. 2008 May 13;585(2-3):325-37 Search in Google Scholar

45 Wang Y, Xia X, Zhou X et al. Association of gut microbiome and metabolites with onset and treatment response of patients with pemphigus vulgaris. Front Immunol. 2023 Apr 14;14:1114586. Search in Google Scholar

46 Litvak Y, Byndloss MX, Tsolis RM, Bäumler AJ. Dysbiotic Proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr Opin Microbiol. 2017 Oct;39:1-6. Search in Google Scholar

47 Mu Q, Kirby J, Reilly CM, Luo XM. Leaky Gut as a Danger Signal for Autoimmune Diseases. Front Immunol. 2017 May 23;8:598. Search in Google Scholar

48 Chalmers JR, Wojnarowska F, Kirtschig G et al. A randomised controlled trial to compare the safety, effectiveness and cost-effectiveness of doxycycline (200 mg/day) with that of oral prednisolone (0.5 mg/kg/ day) for initial treatment of bullous pemphigoid: the Bullous Pemphigoid Steroids and Tetracyclines (BLISTER) trial. Health Technol Assess. 2017 Mar;21(10):1-90. Search in Google Scholar

49 Mason JM, Chalmers JR, Godec T et al. U.K. Dermatology Clinical Trials Network BLISTER Study Group. Doxycycline compared with prednisolone therapy for patients with bullous pemphigoid: cost-effectiveness analysis of the BLISTER trial. Br J Dermatol. 2018 Feb;178(2):415-423. Search in Google Scholar

50 Han Z, Fan Y, Wu Q et al. Comparison of gut microbiota dysbiosis between pemphigus vulgaris and bullous pemphigoid. Int Immunopharmacol. 2024 Feb 15;128:111470. Search in Google Scholar

51 Nagpal R, Wang S, Ahmadi S et al. Human-origin probiotic cocktail increases short-chain fatty acid production via modulation of mice and human gut microbiome. Sci Rep. 2018 Aug 23;8(1):12649 Search in Google Scholar

52 Groeger D, O’Mahony L, Murphy EF et al. Bifidobacterium infantis 35624 modulates host inflammatory processes beyond the gut. Gut Microbes. 2013 Jul-Aug;4(4):325-39 Search in Google Scholar

53 Buhaș MC, Candrea R, Gavrilaș LI et al. Transforming Psoriasis Care: Probiotics and Prebiotics as Novel Therapeutic Approaches. Int J Mol Sci. 2023 Jul 7;24(13):11225. Search in Google Scholar

54 Umborowati MA, Damayanti D, Anggraeni S et al. The role of probiotics in the treatment of adult atopic dermatitis: a meta-analysis of randomized controlled trials. J Health Popul Nutr. 2022 Aug 17;41(1):37. Search in Google Scholar

55 Cesaroni I, Poteca H, Garrido A. The use of probiotic solution as supplement and restoring agent in some skin pathologies: Pemphigoid lesions, psoriasis, ulcerations and others. Proceedings of the Nutrition Society. 2013;72(OCE1):E23. Search in Google Scholar

56 Rungjang A, Meephansan J, Bing Thio H. Skin and gut microbiota in psoriasis: a systematic review. Hum Microbiome. 2021. Search in Google Scholar

57 Kim JH, Kim K, Kim W. Gut microbiota restoration through fecal microbiota transplantation: a new atopic dermatitis therapy. Exp Mol Med. 2021;53(5):907–916. Search in Google Scholar

58 Emtenani S, Hertl M, Schmidt E, Hudemann C. Mouse models of pemphigus: valuable tools to investigate pathomechanisms and novel therapeutic interventions. Front Immunol. 2023 Apr 27;14:1169947. Search in Google Scholar

59 Pollmann R, Eming R. Research Techniques Made Simple: Mouse Models of Autoimmune Blistering Diseases. J Invest Dermatol. 2017 Jan;137(1):e1-e6. Search in Google Scholar