Alteration of microbial composition in the skin and blood in vasculitis.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
15 09 2023
15 09 2023
Historique:
received:
17
05
2023
accepted:
07
09
2023
medline:
18
9
2023
pubmed:
16
9
2023
entrez:
15
9
2023
Statut:
epublish
Résumé
Vasculitis is a systemic autoimmune disease characterized by leukocyte infiltration into blood vessels. Various microorganisms have been associated with the pathogenesis of vasculitis; however, the causal microbial agents and underlying mechanisms are not fully understood, possibly because of the technical limitations of pathogen detection. In the present study, we characterized the microbiome profile of patients with cutaneous vasculitis using comprehensive metagenome shotgun sequencing. We found that the abundance of the SEN virus was increased in the affected skin and serum of patients with vasculitis compared to healthy donors. In particular, the abundance of SEN virus reads was increased in the sera of patients with cutaneous arteritis. Among the bacteria identified, Corynebacteriales was the most differentially associated with vasculitis. Linear discriminant analysis effect size also indicated differences in the microbial taxa between patients with vasculitis and healthy donors. These findings demonstrate that vasculitis is associated with considerable alteration of the microbiome in the blood and skin and suggest a role for the infectious trigger in vasculitis.
Identifiants
pubmed: 37714908
doi: 10.1038/s41598-023-42307-7
pii: 10.1038/s41598-023-42307-7
pmc: PMC10504252
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
15317Informations de copyright
© 2023. Springer Nature Limited.
Références
Jennette, J. C. et al. 2012 revised International Chapel Hill consensus conference nomenclature of vasculitides. Arthritis Rheum. 65, 1–11. https://doi.org/10.1002/art.37715 (2013).
doi: 10.1002/art.37715
pubmed: 23045170
Miyabe, Y., Miyabe, C., Iwai, Y. & Luster, A. D. Targeting the chemokine system in rheumatoid arthritis and vasculitis. Jma J. 3, 182–192. https://doi.org/10.31662/jmaj.2020-0019 (2020).
doi: 10.31662/jmaj.2020-0019
pubmed: 33150252
pmcid: 7590389
Watts, R. A. & Robson, J. Introduction, epidemiology and classification of vasculitis. Best Pract. Res. Clin. Rheumatol. 32, 3–20. https://doi.org/10.1016/j.berh.2018.10.003 (2018).
doi: 10.1016/j.berh.2018.10.003
pubmed: 30526896
Miyabe, C., Miyabe, Y., Miyata, R. & Ishiguro, N. Pathogens in vasculitis: Is it really idiopathic?. Jma J. 4, 216–224. https://doi.org/10.31662/jmaj.2021-0021 (2021).
doi: 10.31662/jmaj.2021-0021
pubmed: 34414315
pmcid: 8355637
Sugino, H., Sawada, Y. & Nakamura, M. IgA vasculitis: Etiology, treatment, biomarkers and epigenetic changes. Int. J. Mol. Sci. https://doi.org/10.3390/ijms22147538 (2021).
doi: 10.3390/ijms22147538
pubmed: 34445711
pmcid: 8396478
Shavit, E., Alavi, A. & Sibbald, R. G. Vasculitis-what do we have to know? A review of literature. Int. J. Low Extrem. Wounds 17, 218–226. https://doi.org/10.1177/1534734618804982 (2018).
doi: 10.1177/1534734618804982
pubmed: 30501545
Miyabe, C., Oda, T., Miyata, R., Miyabe, Y. & Ishiguro, N. Nephritis-associated plasmin receptor in the cutaneous vessels in IgA vasculitis. J. Dermatol. 50, 102–103. https://doi.org/10.1111/1346-8138.16574 (2023).
doi: 10.1111/1346-8138.16574
pubmed: 36151872
Ishiguro, N. & Kawashima, M. Cutaneous polyarteritis nodosa: A report of 16 cases with clinical and histopathological analysis and a review of the published work. J. Dermatol. 37, 85–93. https://doi.org/10.1111/j.1346-8138.2009.00752.x (2010).
doi: 10.1111/j.1346-8138.2009.00752.x
pubmed: 20175828
Trepo, C. & Guillevin, L. Polyarteritis nodosa and extrahepatic manifestations of HBV infection: the case against autoimmune intervention in pathogenesis. J. Autoimmun. 16, 269–274. https://doi.org/10.1006/jaut.2000.0502 (2001).
doi: 10.1006/jaut.2000.0502
pubmed: 11334492
Miyabe, C. et al. Am 80, a retinoic acid receptor agonist, ameliorates murine vasculitis through the suppression of neutrophil migration and activation. Arthritis Rheum. 65, 503–512. https://doi.org/10.1002/art.37784 (2013).
doi: 10.1002/art.37784
pubmed: 23203767
Miyabe, C. et al. A sphingosine 1-phosphate receptor agonist ameliorates animal model of vasculitis. Inflamm. Res. 66, 335–340. https://doi.org/10.1007/s00011-016-1018-y (2017).
doi: 10.1007/s00011-016-1018-y
pubmed: 27942751
Miyabe, C. et al. Abrogation of lysophosphatidic acid receptor 1 ameliorates murine vasculitis. Arthritis Res. Ther. 21, 191. https://doi.org/10.1186/s13075-019-1973-0 (2019).
doi: 10.1186/s13075-019-1973-0
pubmed: 31429784
pmcid: 6702724
Miyabe, C. et al. Dectin-2-induced CCL2 production in tissue-resident macrophages ignites cardiac arteritis. J. Clin. Invest. 129, 3610–3624. https://doi.org/10.1172/jci123778 (2019).
doi: 10.1172/jci123778
pubmed: 31169521
pmcid: 6715376
Hoffman, G. S. et al. The microbiome of temporal arteries. Pathog. Immun. 4, 21–38. https://doi.org/10.20411/pai.v4i1.270 (2019).
doi: 10.20411/pai.v4i1.270
pubmed: 30993251
pmcid: 6423729
Motooka, D., Nakamura, S., Hagiwara, K. & Nakaya, T. Viral detection by high-throughput sequencing. Methods Mol. Biol. 1236, 125–134. https://doi.org/10.1007/978-1-4939-1743-3_11 (2015).
doi: 10.1007/978-1-4939-1743-3_11
pubmed: 25287501
Boers, S. A., Jansen, R. & Hays, J. P. Understanding and overcoming the pitfalls and biases of next-generation sequencing (NGS) methods for use in the routine clinical microbiological diagnostic laboratory. Eur. J. Clin. Microbiol. Infect. Dis. 38, 1059–1070. https://doi.org/10.1007/s10096-019-03520-3 (2019).
doi: 10.1007/s10096-019-03520-3
pubmed: 30834996
pmcid: 6520317
Nakamura, S., Nakaya, T. & Iida, T. Metagenomic analysis of bacterial infections by means of high-throughput DNA sequencing. Exp. Biol. Med. (Maywood) 236, 968–971. https://doi.org/10.1258/ebm.2011.010378 (2011).
doi: 10.1258/ebm.2011.010378
pubmed: 21737580
Durazzi, F. et al. Comparison between 16S rRNA and shotgun sequencing data for the taxonomic characterization of the gut microbiota. Sci. Rep. 11, 3030. https://doi.org/10.1038/s41598-021-82726-y (2021).
doi: 10.1038/s41598-021-82726-y
pubmed: 33542369
pmcid: 7862389
Miyabe, C. et al. Immune checkpoint molecule expression is altered in the skin and peripheral blood in vasculitis. Sci. Rep. 11, 20019. https://doi.org/10.1038/s41598-021-99558-5 (2021).
doi: 10.1038/s41598-021-99558-5
pubmed: 34625602
pmcid: 8501116
Almaqati, T. et al. Molecular epidemiology of SEN virus among blood donors and renal dialysis patients. Acta Biomed. 93, e2022237. https://doi.org/10.23750/abm.v93i5.13005 (2022).
doi: 10.23750/abm.v93i5.13005
pubmed: 36300231
Akiba, J., Umemura, T., Alter, H. J., Kojiro, M. & Tabor, E. SEN virus: Epidemiology and characteristics of a transfusion-transmitted virus. Transfusion 45, 1084–1088. https://doi.org/10.1111/j.1537-2995.2004.00209.x (2005).
doi: 10.1111/j.1537-2995.2004.00209.x
pubmed: 15987351
Brogan, P. & Eleftheriou, D. Vasculitis update: Pathogenesis and biomarkers. Pediatr. Nephrol. 33, 187–198. https://doi.org/10.1007/s00467-017-3597-4 (2018).
doi: 10.1007/s00467-017-3597-4
pubmed: 28785984
Spertini, O., Kansas, G. S., Munro, J. M., Griffin, J. D. & Tedder, T. F. Regulation of leukocyte migration by activation of the leukocyte adhesion molecule-1 (LAM-1) selectin. Nature 349, 691–694. https://doi.org/10.1038/349691a0 (1991).
doi: 10.1038/349691a0
pubmed: 1705015
Somer, T. & Finegold, S. M. Vasculitides associated with infections, immunization, and antimicrobial drugs. Clin. Infect. Dis. 20, 1010–1036. https://doi.org/10.1093/clinids/20.4.1010 (1995).
doi: 10.1093/clinids/20.4.1010
pubmed: 7795045
Shibata, M. et al. The presence of a newly identified infectious agent (SEN virus) in patients with liver diseases and in blood donors in Japan. J. Infect. Dis. 184, 400–404. https://doi.org/10.1086/322050 (2001).
doi: 10.1086/322050
pubmed: 11471096
Pirouzi, A., Bahmani, M., Feizabadi, M. M. & Afkari, R. Molecular characterization of Torque teno virus and SEN virus co-infection with HIV in patients from Southern Iran. Rev. Soc. Bras. Med. Trop. 47, 275–279. https://doi.org/10.1590/0037-8682-0073-2014 (2014).
doi: 10.1590/0037-8682-0073-2014
pubmed: 25075476
Tauch, A., Fernández-Natal, I. & Soriano, F. A microbiological and clinical review on Corynebacterium kroppenstedtii. Int. J. Infect. Dis. 48, 33–39. https://doi.org/10.1016/j.ijid.2016.04.023 (2016).
doi: 10.1016/j.ijid.2016.04.023
pubmed: 27155209
Yamamuro, R., Hosokawa, N., Otsuka, Y. & Osawa, R. Clinical characteristics of corynebacterium bacteremia caused by different species, Japan, 2014–2020. Emerg. Infect. Dis. 27, 2981–2987. https://doi.org/10.3201/eid2712.210473 (2021).
doi: 10.3201/eid2712.210473
pubmed: 34812137
pmcid: 8632174
Ni, Q. et al. Gut microbial dysbiosis and plasma metabolic profile in individuals with vitiligo. Front. Microbiol. 11, 592248. https://doi.org/10.3389/fmicb.2020.592248 (2020).
doi: 10.3389/fmicb.2020.592248
pubmed: 33381090
pmcid: 7768019
Sánchez-Manubens, J. et al. Characterization of the nasopharyngeal microbiome in patients with Kawasaki disease. An. Pediatr. (Engl. Ed.) 97, 300–309. https://doi.org/10.1016/j.anpede.2022.08.001 (2022).
doi: 10.1016/j.anpede.2022.08.001
pubmed: 36241544
Shibata, M., Ezaki, T., Hori, M., Nagashima, M. & Morishima, T. Isolation of a Kawasaki disease-associated bacterial sequence from peripheral blood leukocytes. Pediatr. Int. 41, 467–473. https://doi.org/10.1046/j.1442-200x.1999.01115.x (1999).
doi: 10.1046/j.1442-200x.1999.01115.x
pubmed: 10530055
Chen, Y. E., Fischbach, M. A. & Belkaid, Y. Skin microbiota-host interactions. Nature 553, 427–436. https://doi.org/10.1038/nature25177 (2018).
doi: 10.1038/nature25177
pubmed: 29364286
pmcid: 6075667
Lu, J. et al. Metagenome analysis using the Kraken software suite. Nat. Protoc. 17, 2815–2839. https://doi.org/10.1038/s41596-022-00738-y (2022).
doi: 10.1038/s41596-022-00738-y
pubmed: 36171387
pmcid: 9725748
Wood, D. E., Lu, J. & Langmead, B. Improved metagenomic analysis with Kraken 2. Genome Biol. 20, 257. https://doi.org/10.1186/s13059-019-1891-0 (2019).
doi: 10.1186/s13059-019-1891-0
pubmed: 31779668
pmcid: 6883579
Kojima, H., Kaita, K. D., Zhang, M., Giulivi, A. & Minuk, G. Y. Genomic analysis of a recently identified virus (SEN virus) and genotypes D and H by polymerase chain reaction. Antiviral Res. 60, 27–33. https://doi.org/10.1016/s0166-3542(03)00133-5 (2003).
doi: 10.1016/s0166-3542(03)00133-5
pubmed: 14516918