The Extracellular Vesicles from the Commensal Staphylococcus Epidermidis ATCC12228 Strain Regulate Skin Inflammation in the Imiquimod-Induced Psoriasis Murine Model
Extracellular vesicles (EVs) are evaginations of the cytoplasmic membrane, containing nucleic acids, proteins, lipids, enzymes, and toxins. EVs participate in various bacterial physiological processes. <i>Staphylococcus epidermidis</i> interacts and communicates with the host skin. <i...
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MDPI AG
2021-12-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/22/23/13029 |
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| author | Fernando Gómez-Chávez Carlos Cedillo-Peláez Luis A. Zapi-Colín Guadalupe Gutiérrez-González Isaí Martínez-Torres Humberto Peralta Leslie Chavez-Galan Erick D. Avila-Calderón Araceli Contreras-Rodríguez Yaneth Bartolo-Aguilar Sandra Rodríguez-Martínez Mario E. Cancino-Diaz Juan C. Cancino-Diaz |
| author_facet | Fernando Gómez-Chávez Carlos Cedillo-Peláez Luis A. Zapi-Colín Guadalupe Gutiérrez-González Isaí Martínez-Torres Humberto Peralta Leslie Chavez-Galan Erick D. Avila-Calderón Araceli Contreras-Rodríguez Yaneth Bartolo-Aguilar Sandra Rodríguez-Martínez Mario E. Cancino-Diaz Juan C. Cancino-Diaz |
| author_sort | Fernando Gómez-Chávez |
| collection | DOAJ |
| description | Extracellular vesicles (EVs) are evaginations of the cytoplasmic membrane, containing nucleic acids, proteins, lipids, enzymes, and toxins. EVs participate in various bacterial physiological processes. <i>Staphylococcus epidermidis</i> interacts and communicates with the host skin. <i>S. epidermidis’</i> EVs may have an essential role in this communication mechanism, modulating the immunological environment. This work aimed to evaluate if <i>S. epidermidis’</i> EVs can modulate cytokine production by keratinocytes in vitro and in vivo using the imiquimod-induced psoriasis murine model. <i>S. epidermidis’</i> EVs were obtained from a commensal strain (ATC12228EVs) and a clinical isolated strain (983EVs). EVs from both origins induced IL-6 expression in HaCaT keratinocyte cultures; nevertheless, 983EVs promoted a higher expression of the pro-inflammatory cytokines VEGF-A, LL37, IL-8, and IL-17F than ATCC12228EVs. Moreover, in vivo imiquimod-induced psoriatic skin treated with ATCC12228EVs reduced the characteristic psoriatic skin features, such as acanthosis and cellular infiltrate, as well as VEGF-A, IL-6, KC, IL-23, IL-17F, IL-36γ, and IL-36R expression in a more efficient manner than 983EVs; however, in contrast, Foxp3 expression did not significantly change, and IL-36 receptor antagonist (IL-36Ra) was found to be increased. Our findings showed a distinctive immunological profile induction that is dependent on the clinical or commensal EV origin in a mice model of skin-like psoriasis. Characteristically, proteomics analysis showed differences in the EVs protein content, dependent on origin of the isolated EVs. Specifically, in ATCC12228EVs, we found the proteins glutamate dehydrogenase, ornithine carbamoyltransferase, arginine deiminase, carbamate kinase, catalase, superoxide dismutase, phenol-soluble β1/β2 modulin, and polyglycerol phosphate α-glucosyltransferase, which could be involved in the reduction of lesions in the murine imiquimod-induced psoriasis skin. Our results show that the commensal ATCC12228EVs have a greater protective/attenuating effect on the murine imiquimod-induced psoriasis by inducing IL-36Ra expression in comparison with EVs from a clinical isolate of <i>S. epidermidis</i>. |
| first_indexed | 2024-03-10T04:51:57Z |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T04:51:57Z |
| publishDate | 2021-12-01 |
| publisher | MDPI AG |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-1547862e066448fba71c1151979a0b732023-11-23T02:32:02ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-12-0122231302910.3390/ijms222313029The Extracellular Vesicles from the Commensal Staphylococcus Epidermidis ATCC12228 Strain Regulate Skin Inflammation in the Imiquimod-Induced Psoriasis Murine ModelFernando Gómez-Chávez0Carlos Cedillo-Peláez1Luis A. Zapi-Colín2Guadalupe Gutiérrez-González3Isaí Martínez-Torres4Humberto Peralta5Leslie Chavez-Galan6Erick D. Avila-Calderón7Araceli Contreras-Rodríguez8Yaneth Bartolo-Aguilar9Sandra Rodríguez-Martínez10Mario E. Cancino-Diaz11Juan C. Cancino-Diaz12Laboratorio de Enfermedades Osteoarticulares e Inmunológicas, Sección de Estudios de Posgrado e Investigación, Escuela Nacional de Medicina y Homeopatía, Instituto Politécnico Nacional, Mexico City 07320, MexicoLaboratorio de Inmunología Experimental, Instituto Nacional de Pediatría, Secretaría de Salud, Mexico City 04530, MexicoLaboratorio de Inmunidad Innata, Departamento de Inmunología, Escuela Nacional de Ciencias Biológicas-Instituto Politécnico Nacional, Mexico City 07340, MexicoLaboratorio de Inmunidad Innata, Departamento de Inmunología, Escuela Nacional de Ciencias Biológicas-Instituto Politécnico Nacional, Mexico City 07340, MexicoDepartamento de Inmunología, Unidad de Investigación, Instituto de Oftalmología Conde de Valenciana, Mexico City 06800, MexicoPrograma de Genómica Funcional de Procariotes, Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca 04510, MexicoLaboratory of Integrative Immunology, Instituto Nacional de Enfermedades Respiratorias Ismael Cosió Villegas, Mexico City 14080, MexicoLaboratorio de Inmunomicrobiología, Departamento Microbiología, Escuela Nacional de Ciencias Biológicas-Instituto Politécnico Nacional, Mexico City 11340, MexicoLaboratorio de Inmunomicrobiología, Departamento Microbiología, Escuela Nacional de Ciencias Biológicas-Instituto Politécnico Nacional, Mexico City 11340, MexicoUnidad Profesional Interdisciplinaria de Biotecnología del Instituto Politécnico Nacional (UPIBI-IPN), Mexico City 07340, MexicoLaboratorio de Inmunidad Innata, Departamento de Inmunología, Escuela Nacional de Ciencias Biológicas-Instituto Politécnico Nacional, Mexico City 07340, MexicoLaboratorio de Inmunidad Innata, Departamento de Inmunología, Escuela Nacional de Ciencias Biológicas-Instituto Politécnico Nacional, Mexico City 07340, MexicoLaboratorio de Inmunomicrobiología, Departamento Microbiología, Escuela Nacional de Ciencias Biológicas-Instituto Politécnico Nacional, Mexico City 11340, MexicoExtracellular vesicles (EVs) are evaginations of the cytoplasmic membrane, containing nucleic acids, proteins, lipids, enzymes, and toxins. EVs participate in various bacterial physiological processes. <i>Staphylococcus epidermidis</i> interacts and communicates with the host skin. <i>S. epidermidis’</i> EVs may have an essential role in this communication mechanism, modulating the immunological environment. This work aimed to evaluate if <i>S. epidermidis’</i> EVs can modulate cytokine production by keratinocytes in vitro and in vivo using the imiquimod-induced psoriasis murine model. <i>S. epidermidis’</i> EVs were obtained from a commensal strain (ATC12228EVs) and a clinical isolated strain (983EVs). EVs from both origins induced IL-6 expression in HaCaT keratinocyte cultures; nevertheless, 983EVs promoted a higher expression of the pro-inflammatory cytokines VEGF-A, LL37, IL-8, and IL-17F than ATCC12228EVs. Moreover, in vivo imiquimod-induced psoriatic skin treated with ATCC12228EVs reduced the characteristic psoriatic skin features, such as acanthosis and cellular infiltrate, as well as VEGF-A, IL-6, KC, IL-23, IL-17F, IL-36γ, and IL-36R expression in a more efficient manner than 983EVs; however, in contrast, Foxp3 expression did not significantly change, and IL-36 receptor antagonist (IL-36Ra) was found to be increased. Our findings showed a distinctive immunological profile induction that is dependent on the clinical or commensal EV origin in a mice model of skin-like psoriasis. Characteristically, proteomics analysis showed differences in the EVs protein content, dependent on origin of the isolated EVs. Specifically, in ATCC12228EVs, we found the proteins glutamate dehydrogenase, ornithine carbamoyltransferase, arginine deiminase, carbamate kinase, catalase, superoxide dismutase, phenol-soluble β1/β2 modulin, and polyglycerol phosphate α-glucosyltransferase, which could be involved in the reduction of lesions in the murine imiquimod-induced psoriasis skin. Our results show that the commensal ATCC12228EVs have a greater protective/attenuating effect on the murine imiquimod-induced psoriasis by inducing IL-36Ra expression in comparison with EVs from a clinical isolate of <i>S. epidermidis</i>.https://www.mdpi.com/1422-0067/22/23/13029<i>Staphylococcus epidermidis</i>extracellular vesiclespsoriasisskinimiquimodproteomics |
| spellingShingle | Fernando Gómez-Chávez Carlos Cedillo-Peláez Luis A. Zapi-Colín Guadalupe Gutiérrez-González Isaí Martínez-Torres Humberto Peralta Leslie Chavez-Galan Erick D. Avila-Calderón Araceli Contreras-Rodríguez Yaneth Bartolo-Aguilar Sandra Rodríguez-Martínez Mario E. Cancino-Diaz Juan C. Cancino-Diaz The Extracellular Vesicles from the Commensal Staphylococcus Epidermidis ATCC12228 Strain Regulate Skin Inflammation in the Imiquimod-Induced Psoriasis Murine Model International Journal of Molecular Sciences <i>Staphylococcus epidermidis</i> extracellular vesicles psoriasis skin imiquimod proteomics |
| title | The Extracellular Vesicles from the Commensal Staphylococcus Epidermidis ATCC12228 Strain Regulate Skin Inflammation in the Imiquimod-Induced Psoriasis Murine Model |
| title_full | The Extracellular Vesicles from the Commensal Staphylococcus Epidermidis ATCC12228 Strain Regulate Skin Inflammation in the Imiquimod-Induced Psoriasis Murine Model |
| title_fullStr | The Extracellular Vesicles from the Commensal Staphylococcus Epidermidis ATCC12228 Strain Regulate Skin Inflammation in the Imiquimod-Induced Psoriasis Murine Model |
| title_full_unstemmed | The Extracellular Vesicles from the Commensal Staphylococcus Epidermidis ATCC12228 Strain Regulate Skin Inflammation in the Imiquimod-Induced Psoriasis Murine Model |
| title_short | The Extracellular Vesicles from the Commensal Staphylococcus Epidermidis ATCC12228 Strain Regulate Skin Inflammation in the Imiquimod-Induced Psoriasis Murine Model |
| title_sort | extracellular vesicles from the commensal staphylococcus epidermidis atcc12228 strain regulate skin inflammation in the imiquimod induced psoriasis murine model |
| topic | <i>Staphylococcus epidermidis</i> extracellular vesicles psoriasis skin imiquimod proteomics |
| url | https://www.mdpi.com/1422-0067/22/23/13029 |
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