Bacterial Metabolites: A Link between Gut Microbiota and Dermatological Diseases
Abstract
:1. Introduction
2. Short-Chain Fatty Acids
2.1. Atopic Dermatitis and Hypersensitivity Reactions
2.2. Psoriasis
2.3. Connective Tissue Diseases
3. Tryptophan Metabolites
3.1. Atopic Dermatitis and Hypersensitivity Reactions
3.2. Lupus
4. Trimethylamine (TMA) and Trimethylamine N-oxide (TMAO)
Dermatological Context
5. Future Perspectives
5.1. Prebiotics
5.2. Probiotics
5.3. Fecal Microbiota Transplantation
5.4. Postbiotics
References | Disease | Studied Model | Main Findings |
---|---|---|---|
Short-chain fatty acids (SCFAs) | |||
Schwarz et al. [61] | Psoriasis | imiquimod-induced psoriasis-like skin inflammation mouse model, skin biopsies from patients with psoriasis | Topical administration of sodium butyrate (SB) reduced symptoms of psoriasis-like skin inflammation Topical SB increased the number and activity of Treg cells, IL-10 transcription, and decreased IL-17 transcription in the skin of a mouse model SB increased the transcription of IL-10 and decreased the transcription of IL-6 and IL-17 in human skin biopsies |
Krejner et al. [62] | Psoriasis | skin biopsies from patients with psoriasis | Ex vivo treatment with SB caused a reduction in IL-17 and IL-6, and an upregulation of IL-10 transcription in skin biopsies Skin with psoriasis has decreased expression of GPR109a and GPR43, SB upregulates these receptors |
Rodríguez-Carrio et al. [67] | Systemic lupus erythematosus | 21 SLE patients, 25 healthy individuals | Fecal acetate and propionate are higher in patients with SLE compared to controls Dysbiosis in SLE patients |
Sanchez et al. [28] | Systemic lupus erythematosus | MRL/lpr and NZB/W F1 lupus-prone mice | Oral mixture of sodium butyrate and sodium propionate reduced local and systemic antibody responses Orally administered SCFAsT reduced lupus skin lesions and kidney pathology |
He et al. [68] | Systemic lupus erythematosus | MRL/lpr lupus-prone mice | Reduction in microbial diversity in the SLE mouse model Oral administration of SB reduced renal histopathological changes and increased microbiota diversity |
Patrone et al. [69] | Systemic sclerosis | 18 SSc patients, 9 healthy subjects | Dysbiosis manifested as a decrease in butyrate-producing genera more prominent in patients with gastrointestinal involvement |
Park et al. [71] | Systemic sclerosis | bleomycin-induced fibrosis mouse model of SSc, human dermal fibroblasts | SB administered orally or subcutaneously reduced bleomycin-induced dermal and lung fibrosis SB treatment inhibits TGF-β1-induced fibrotic responses in human dermal fibroblasts |
Reddel et al. [35] | Atopic dermatitis | 19 children with AD and 18 healthy individuals | AD was characterized by dysbiosis, especially manifested in the depletion of butyrate-producing bacteria |
Nylund et al. [36] | Atopic dermatitis | 28 infants with atopic dermatitis and 11 healthy infants | Less severe eczema was associated with increased butyrate-producing bacterial abundance and microbiome diversity |
Song et al. [39] | Atopic dermatitis | 90 patients with AD and 42 volunteers without AD | Decreased fecal level of butyrate and propionate in AD patients Some subspecies of Faecalibacterium prausnitzii are linked with AD |
Lee et al. [38] | Atopic dermatitis | 234 patients with mild to severe AD, 112 non-AD subjects | Diversity of the microbiota in moderate to severe AD was significantly lower than in non-AD Disordered gut microbiota development in AD was associated with dysregulated SCFA production |
Roduit et al. [40] | Atopic dermatitis | 301 one-year-old children | Children with the highest fecal levels of butyrate and propionate were less prone to atopic sensitization and were less likely to develop asthma between the ages of 3 and 6 Food allergies and allergic rhinitis were less common in children with the highest butyrate levels |
Cheng et al. [42] | Atopic dermatitis | 75 infants | Low fecal butyric acid was associated with an increased risk of developing atopic dermatitis, food sensitization, and wheezing up to 8 years old |
Gio-Batta et al. [44] | Atopic dermatitis | 65 infants | A lower level of valeric acid at 3 years of age was associated with a higher prevalence of atopic eczema at the age of 8 years |
Gio-Batta et al. [45] | Atopic dermatitis | 110 one-year-old children | Eczema at 13 years of age was inversely correlated with the amount of fecal valeric acid at 1 year of age |
Folkerts et al. [52] | Allergy | Human mast cells | Propionate and butyrate inhibited IgE- and non-IgE-dependent human mast cell degranulation |
Schwarz et al. [57] | Contact dermatitis | sensitized C57BL/6J mice | Sodium butyrate (SB) administered topically or subcutaneously inhibited both the elicitation phase and ongoing contact hypersensitivity response SB induced the anti-inflammatory response via an increase in the number of skin Treg cells and an increase in IL-10 transcription |
Trompette et al. [33] | Atopic dermatitis | atopic dermatitis-like skin inflammation mouse model | Fermentable fiber-rich diet or orally administered sodium butyrate alleviate systemic allergen sensitization and disease severity Oral butyrate stimulates terminal differentiation of epidermal keratinocytes and promotes skin barrier function |
Tryptophan metabolites | |||
Tsuji et al. [86] | Atopic dermatitis | normal human epidermal keratinocytes | The activation of AHR by tryptophane metabolite significantly increased filaggrin expression FICZ reversed the IL-4-induced downregulation in transcription and protein levels of filaggrin |
Aoki et al. [89] | UVB-induced skin damage | HR-1 mice, HaCaT keratinocytes | Topical application of indole-3-pyruvate reduced the severity of UVB-induced skin lesions, the augmentation of dermal thickness, and transepithelial water loss Suppression of the overproduction of IL-1b and IL-6 in response to UVB radiation in a mouse model Indole-3-pyruvate improved the survival rate and reduced the expression of IL-1b and IL-6 in UVB-exposed HaCaT keratinocytes |
Fang et al. [97] | Atopic dermatitis | 87 patients with atopic dermatitis, sensitized female C57BL/6 mice | Bifidobacterium longum probiotic treatment increased serum and fecal indole-3-carbaldehyde, significantly reduced AD symptoms Indole-3-carbaldehyde displayed a significant negative correlation with atopic dermatitis severity measured in both SCORAD and DLQI Oral administration of indole-3-carbaldehyde alleviated AD-like skin lesions in sensitized mice |
Yu et al. [81] | Atopic dermatitis | 19 patients with AD, 19 healthy volunteers, sensitized C57BL/6 and BALB/c mice | Decreased indole-3-aldehyde was observed in both lesional and non-lesional skin of AD patients Topical and orally administered indole-3-aldehyde attenuated MC903-induced AD-like dermatitis in mouse and decreased expression of IL-4, IL-5, IL-6, IL-13, and TSLP Topically administered indole-3-aldehyde reduced inflammatory cell infiltration in mice |
Kiyomatsu-Oda et al. [100] | Atopic dermatitis | NC/Nga mice, HaCaT cells and normal human epidermal keratinocytes (NHEKs) | Tryptophan metabolite FICZ improved symptoms of AD-like dermatitis, decreased TEWL, restored filaggrin expression, reduced the number of infiltrated mast cells, and reduced expression of IL-22 and IFN-γ genes in a mouse model FICZ upregulated expression and abundance of filaggrin in HaCaT and NHEKs cells |
Singh et al. [104] | Delayed-type hypersensitivity | Sensitized C57BL/6 mice | Topical administration of indole-3-carbinol and 3,3′-diindolylmethane alleviated symptoms, triggered induction of Tregs, and suppressed Th17 cells of delayed-type hypersensitivity in a mouse model FICZ exacerbated disease in a mouse model and suppressed Treg cells |
Shinde et al. [108] | Systemic lupus erythematosus | 48 patients with active SLE, 24 patients with SLE in remission, and 20 control subjects | Serum indole-3-propionic acid was significantly higher than in the control group |
Trimethylamine N-oxide (TMAO) | |||
Sikora et al. [127] | Psoriasis | 72 patients with psoriasis and 40 matched controls | In patients with psoriasis, serum TMAO was significantly higher than in the control group TMAO was found to be an independent predictor of cardiovascular risk |
Sun et al. [128] | Psoriasis | 180 patients with psoriasis, 60 healthy controls | Psoriatic patients had significantly higher serum levels of TMAO compared to controls TMAO had a positive correlation with PASI score |
Coras et al. [129] | Psoriatic arthritis | 38 patients with psoriatic arthritis | Serum TMAO demonstrated a significant correlation with indicators of disease activity for the skin and peripheral joints |
Barea et al. [130] | Hidradenitis suppurativa | 35 patients with hidradenitis suppurativa and 35 matched controls | Patients had increased serum TMAO levels compared to controls The level of circulating TMAO correlated positively with the HS Sartorius score also after adjustment for confounding factors Serum TMAO levels and PhA were the two primary indicators of the clinical severity of HS based on a linear regression model |
Li et al. [133] | Systemic lupus erythematosus | 17 patients with SLE and 17 healthy controls | Serum levels of trimethylamine N-oxide (TMAO) were found to be elevated in lupus patients compared to controls |
González-Correa et al. [134] | Systemic lupus erythematosus | Imiquimod-induced mouse model of SLE | Plasma TMAO concentrations were significantly elevated in the serum of active systemic lupus erythematosus patients |
Wu et al. [121] | Graft-versus-host disease | C57BL/6 and BALB/c mice | Induced by oral administration elevation of plasma TMAO was associated with worse course and survival of graft-versus-host disease |
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Stec, A.; Sikora, M.; Maciejewska, M.; Paralusz-Stec, K.; Michalska, M.; Sikorska, E.; Rudnicka, L. Bacterial Metabolites: A Link between Gut Microbiota and Dermatological Diseases. Int. J. Mol. Sci. 2023, 24, 3494. https://doi.org/10.3390/ijms24043494
Stec A, Sikora M, Maciejewska M, Paralusz-Stec K, Michalska M, Sikorska E, Rudnicka L. Bacterial Metabolites: A Link between Gut Microbiota and Dermatological Diseases. International Journal of Molecular Sciences. 2023; 24(4):3494. https://doi.org/10.3390/ijms24043494
Chicago/Turabian StyleStec, Albert, Mariusz Sikora, Magdalena Maciejewska, Karolina Paralusz-Stec, Milena Michalska, Ewa Sikorska, and Lidia Rudnicka. 2023. "Bacterial Metabolites: A Link between Gut Microbiota and Dermatological Diseases" International Journal of Molecular Sciences 24, no. 4: 3494. https://doi.org/10.3390/ijms24043494