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Faecalibacterium prausnitzii subspecies-level dysbiosis in the human gut microbiome underlying atopic dermatitis
Open accessAbstract
BACKGROUND: Atopic dermatitis (AD) is a serious global epidemic associated with a modern lifestyle. OBJECTIVE: Although aberrant interactions between gut microbes and the intestinal immune system have been implicated in this skin disease, the nature of the microbiome dysfunction underlying the disease remains unclear. METHODS: The gut microbiome from 132 subjects, including 90 patients with AD, was analyzed by using 16S rRNA gene and metagenome sequence analyses. Reference genomes from the Human Microbiome Project and the KEGG Orthology database were used for metagenome analyses. Short-chain fatty acids in fecal samples were compared by using gas chromatographic-mass spectrometric analyses. RESULTS: We show that enrichment of a subspecies of the major gut species Faecalibacterium prausnitzii is strongly associated with AD. In addition, the AD microbiome was enriched in genes encoding the use of various nutrients that could be released from damaged gut epithelium, reflecting a bloom of auxotrophic bacteria. Fecal samples from patients with AD showed decreased levels of butyrate and propionate, which have anti-inflammatory effects. This is likely a consequence of an intraspecies compositional change in F prausnitzii that reduces the number of high butyrate and propionate producers, including those related to the strain A2-165, a lack of which has been implicated in patients with Crohn disease. CONCLUSIONS: The data suggest that feedback interactions between dysbiosis in F prausnitzii and dysregulation of gut epithelial inflammation might underlie the chronic progression of AD by resulting in impairment of the gut epithelial barrier, which ultimately leads to aberrant TH2-type immune responses to allergens in the skin.
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“Gut dysbiosis has been observed in conditions such as atopic dermatitis [82].”
From Boosting the Photoaged Skin: The Potential Role of Dietary Components (2021) · cites this paper as [82]
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“Several studies have discovered that the content of short-chain fatty acids (SCFAs) such as propionate and butyrate in patients with AD is significantly lower than that in healthy individuals (40, 41).”
BackgroundPark, Y. M., Lee, S., Kang, M., Kim, B. S., Lee, M.-J., Jung, S. S., Yoon, J., Cho, H., Lee, E. M., Yang, S., et al. (2020) · Allergy Asthma and Immunology Research · doi:10.4168/aair.2020.12.2.322 · Cited by 100
Staphylococcus aureus and the Cutaneous Microbiota Biofilms in the Pathogenesis of Atopic Dermatitis
Domenico, E. G. D., Cavallo, I., Capitanio, B., Ascenzioni, F., Pimpinelli, F., Morrone, A., & Ensoli, F. (2019) · Microorganisms · doi:10.3390/microorganisms7090301 · Cited by 101
Dei‐Cas, I., Giliberto, F., Luce, L. N., Dopazo, H., & Steinhardt, A. P. (2020) · Scientific Reports · doi:10.1038/s41598-020-69537-3 · Cited by 100
Role of the Gut Microbiota in Atopic Dermatitis: A Systematic Review
Pedersen, E., Skov, L., Thyssen, J. P., & Jensen, P. (2018) · Acta Dermato Venereologica · doi:10.2340/00015555-3008 · Cited by 99
Next generation probiotics for human health: An emerging perspective
Jan, T., Negi, R., Sharma, B., Kumar, S., Singh, S., Rai, A. K., Shreaz, S., Rustagi, S., Chaudhary, N., Kaur, T., et al. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e35980 · Cited by 95
Emerging evidence of the role of gut microbiota in the development of allergic diseases
Sjödin, K. S., Vidman, L., Rydén, P., & West, C. E. (2016) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/aci.0000000000000277 · Cited by 91
Moon, J., Lee, A. R., Kim, H., Jhun, J., Lee, S.-Y., Choi, J. W., Jeong, Y., Park, M. S., Ji, G. E., Cho, M., et al. (2023) · Arthritis Research & Therapy · doi:10.1186/s13075-023-03118-3 · Cited by 97
“Faecalibacterium prausnitzii (formerly known as Fusobacterium prausnitzii) is an anaerobic gram-positive, non-spore-forming, acetate-consuming, butyrateproducing, and extremely oxygen-sensitive bacterium [20, 21].”
Systematic review of the association between short‐chain fatty acids and allergic diseases
Sasaki, M., Suaini, N. H. A., Afghani, J., Heye, K., O’Mahony, L., Venter, C., Lauener, R. P., Frei, R., & Roduit, C. (2024) · Allergy · doi:10.1111/all.16065 · Cited by 100
New Insights into the Diversity of the Genus Faecalibacterium
Benevides, L., Burman, S., Martin, R., Robert, V., Thomas, M., Miquel, S., Chain, F., Sokol, H., Bermudez-Humaran, L. G., Morrison, M., et al. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01790 · Cited by 86
“…samples of AD patients were enriched in those similar to strain L2-6 with respect to other strains of F. prausnitzii; they also proposed that strain L2-6 can be differentiated from other strains by the existence of a polycistronic region encoding GalNac uptake and metabolism (Song et al., 2016).”
BackgroundThe Prospects for the Therapeutic Implications of Genetically Engineered Probiotics
Mazhar, S. F., Afzal, M., Almatroudi, A., Munir, S., Ashfaq, U. A., Rasool, M., Raza, H., Munir, H. M. W., Rajoka, M. S. R., & Khurshid, M. (2020) · Journal of Food Quality · doi:10.1155/2020/9676452 · Cited by 90
Bacterial Metabolites: A Link between Gut Microbiota and Dermatological Diseases
Stec, A., Sikora, M., Maciejewska, M., Paralusz-Stec, K., Michalska, M. N., Sikorska, E., & Rudnicka, L. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043494 · Cited by 89
“Moreover, the microbiota in AD produce fewer SCFAs, particularly propionate and butyrate, which have been assessed in fecal samples [38,39].”
BackgroundDo an Altered Gut Microbiota and an Associated Leaky Gut Affect COVID-19 Severity?
Kim, H. S. (2021) · mBio · doi:10.1128/mbio.03022-20 · Cited by 86
“understand its influence on human health and disease (57, 58).”
BackgroundFecal Microbiome and Food Allergy in Pediatric Atopic Dermatitis: A Cross-Sectional Pilot Study
Fieten, K. B., Totté, J. E. E., Levin, E., Reyman, M., Meijer, Y., Knulst, A. C., Schuren, F. H. J., & Pasmans, S. G. M. A. (2018) · International Archives of Allergy and Immunology · doi:10.1159/000484897 · Cited by 87
Evolving trends in next-generation probiotics: a 5W1H perspective
Almeida, D., Machado, D., Andrade, J. C., Mendo, S., Gomes, A. M., & Freitas, A. C. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2019.1599812 · Cited by 92
“prausnitzii F6 (a low butyrate producer strain) in atopic dermatitis Case control studies (Song et al. 2016; Zheng et al. 2016; Candela et al. 2012)”
BackgroundRosacea and its association with enteral microbiota in Korean females
Nam, J., Yun, Y., Kim, H., Kim, H., Jung, H. J., Chang, Y., Ryu, S., Shin, H., Kim, H., & Kim, W. (2017) · Experimental Dermatology · doi:10.1111/exd.13398 · Cited by 84
Dokoshi, T., Chen, Y., Cavagnero, K. J., Rahman, G., Hakim, D., Brinton, S. L., Schwarz, H., Brown, E. A. R., O’Neill, A., Nakamura, Y., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-47072-3 · Cited by 88
“Although prior studies have observed dysbiosis in the gut microbiome of individuals with in fl am-matoryskindisease,ithadbeenassumedthatmicrobesinthegutwere in fl uencing the skin 28 – 30 .”
Microbiome in atopic dermatitis
Wollina, U. (2017) · Clinical Cosmetic and Investigational Dermatology · doi:10.2147/ccid.s130013 · Cited by 87
“41 Another study used microarray analysis of intestinal microbiome in infants with and without AD at 6 and 18 months of age.”
Puig‐Castellví, F., Pacheco‐Tapia, R., Deslande, M., Jia, M., Andrikopoulos, P., Chechi, K., Bonnefond, A., Froguel, P., & Dumas, M. (2023) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2023.117248 · Cited by 85
Mottin, V. H. M., & Suyenaga, E. S. (2018) · International Journal of Dermatology · doi:10.1111/ijd.13972 · Cited by 83
Comparative Analysis of the Microbiome across the Gut–Skin Axis in Atopic Dermatitis
Park, D. H., Kim, J. W., Park, H., & Hahm, D. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084228 · Cited by 82
“According to a recent study in Korea, significant dysbiosis (specifically an intraspecies compositional change) of a subspecies of Faecalibacterium prausnitzii was found in the fecal samples of patients with AD [9].”
BackgroundAge and fecal microbial strain-specific differences in patients with spondyloarthritis
Stoll, M. L., Weiss, P. F., Weiss, J. E., Nigrovic, P. A., Edelheit, B. S., Bridges, S., Danila, M. I., Spencer, C. H., Punaro, M., Schikler, K. N., et al. (2018) · Arthritis Research & Therapy · doi:10.1186/s13075-018-1510-6 · Cited by 75
“prausnitzii, such as L2/6, the A2-165 strain induces increased interleukin-10 production from peripheral blood mononuclear cells [16, 40] and has increased butyrate promoter activity [41].”
BackgroundRecent Advances on Microbiota Involvement in the Pathogenesis of Autoimmunity
Gianchecchi, E., & Fierabracci, A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020283 · Cited by 77
“[93] observed a significant correlation between the high abundance of F.”
BackgroundInfluentialMicrobial Dysbiosis Tunes the Immune Response Towards Allergic Disease Outcomes
Augustine, T., Kumar, M., Khodor, S. A., & van Panhuys, N. (2022) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-022-08939-9 · Cited by 77
“As the intestinal barrier function can be impaired in those patients [58], with impairment often being associ‐ ated with an enrichment of Fecalibacterium, in particular, Fecalibacterum prausnitzii, a non‐short chain fatty acid (SFCA)‐producing bacteria which is especially common in pediatric atopic dermatitis [59] and…”
BackgroundProbiotics: Protecting Our Health from the Gut
Varela-Trinidad, G. U., Domínguez-Díaz, C., Solórzano-Castanedo, K., Íñiguez-Gutiérrez, L., Hernández-Flores, T. D. J., & Fafutis‐Morris, M. (2022) · Microorganisms · doi:10.3390/microorganisms10071428 · Cited by 80
“In addition, AD patients have low levels of SCFAs, such as butyrate and propionate, due to a reduction in the number of bacteria producing these metabolites, which is associated with AD severity [141,142].”
BackgroundAtopic dermatitis: Pathophysiology, microbiota, and metabolome – A comprehensive review
Mohammad, S., Karim, M. R., Iqbal, S., Lee, J. H., Mathiyalagan, R., Kim, Y. J., Yang, D. U., & Yang, D. (2024) · Microbiological Research · doi:10.1016/j.micres.2023.127595 · Cited by 83
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The Role of Diet and Nutrition in Allergic Diseases
Zhang, P. (2023) · Nutrients · doi:10.3390/nu15173683 · Cited by 79
“Consistent with animal studies, dysbiosis characterized by the enrichment of Faecalibacterium prausnitzii and a reduced capacity for butyrate fermentation in the human gut microbiome has been found in patients with AD [84].”
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Manipulating Microbiota to Treat Atopic Dermatitis: Functions and Therapies
Alam, J., Xie, L., Yap, Y. A., Marques, F. Z., & Robert, R. (2022) · Pathogens · doi:10.3390/pathogens11060642 · Cited by 71
Metadata
- Authors
- Song, H., Yoo, Y., Hwang, J., Na, Y.-C., & Kim, H. S.
- Affiliations
- Korea University (KR)
- Korea Basic Science Institute (KR)
- Corresponding author
- Kim, Heenam Stanley
- Venue
- Journal of Allergy and Clinical Immunology
- Publisher
- Elsevier BV
- Published
- 2016-03
- Volume
- 137
- Issue
- 3
- Pages
- 852-860
- ISSN
- 0091-6749 (ISSN-L)
- OpenAlex
- W1822404940
- Cited by
- 416
- References
- 61
- Citations by year
- 2026: 27 · 2025: 40 · 2024: 64 · 2023: 57 · 2022: 43 · 2021: 55 · 2020: 28 · 2019: 28 · 2018: 39 · 2017: 18 · 2016: 16
- FWCI
- 10.71
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Allergy and Clinical Immunology (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- National Research Foundation of Korea
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Dermatology › Dermatology and Skin Diseases
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- atopic dermatitis, Faecalibacterium prausnitzii, gut dysbiosis, short-chain fatty acids, butyrate, propionate, intestinal epithelial barrier, Th2 immune response, Crohn's disease, intestinal immune regulation
- MeSH terms
- Eubacteriales, Gastrointestinal Microbiome, Dermatitis, Atopic, Feces, Female, Humans, Male, Models, Biological, Phylogeny, RNA, Ribosomal, 16S, Cluster Analysis, Sequence Analysis, DNA, Computational Biology, Metagenome, Metagenomics, Dysbiosis
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