<i>Lentinula edodes</i> Cultured Extract and <i>Rouxiella badensis</i> subsp. <i>acadiensis</i> (Canan SV-53) Intake Alleviates Immune Deregulation and Inflammation by Modulating Signaling Pathways and Epigenetic Mechanisms
Puberty is a critical developmental period of life characterized by marked physiological changes, including changes in the immune system and gut microbiota development. Exposure to inflammation induced by immune stressors during puberty has been found to stimulate central inflammation and lead to im...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-09-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/24/19/14610 |
| _version_ | 1797575789321912320 |
|---|---|
| author | Roghayeh Shahbazi Hamed Yasavoli-Sharahi Nawal Alsadi Farzaneh Sharifzad Sandra Fang Cyrille Cuenin Vincent Cahais Felicia Fei-Lei Chung Zdenko Herceg Chantal Matar |
| author_facet | Roghayeh Shahbazi Hamed Yasavoli-Sharahi Nawal Alsadi Farzaneh Sharifzad Sandra Fang Cyrille Cuenin Vincent Cahais Felicia Fei-Lei Chung Zdenko Herceg Chantal Matar |
| author_sort | Roghayeh Shahbazi |
| collection | DOAJ |
| description | Puberty is a critical developmental period of life characterized by marked physiological changes, including changes in the immune system and gut microbiota development. Exposure to inflammation induced by immune stressors during puberty has been found to stimulate central inflammation and lead to immune disturbance at distant sites from the gut; however, its enduring effects on gut immunity are not well explored. Therefore, in this study, we used a pubertal lipopolysaccharides (LPS)-induced inflammation mouse model to mimic pubertal exposure to inflammation and dysbiosis. We hypothesized that pubertal LPS-induced inflammation may cause long-term dysfunction in gut immunity by enduring dysregulation of inflammatory signaling and epigenetic changes, while prebiotic/probiotic intake may mitigate the gut immune system deregulation later in life. To this end, four-week-old female Balb/c mice were fed prebiotics/probiotics and exposed to LPS in the pubertal window. To better decipher the acute and enduring immunoprotective effects of biotic intake, we addressed the effect of treatment on interleukin (IL)-17 signaling related-cytokines and pathways. In addition, the effect of treatment on gut microbiota and epigenetic alterations, including changes in microRNA (miRNA) expression and DNA methylation, were studied. Our results revealed a significant dysregulation in selected cytokines, proteins, and miRNAs involved in key signaling pathways related to IL-17 production and function, including IL-17A and F, IL-6, IL-1β, transforming growth factor-β (TGF-β), signal transducer and activator of transcription-3 (STAT3), p-STAT3, forkhead box O1 (FOXO1), and miR-145 in the small intestine of adult mice challenged with LPS during puberty. In contrast, dietary interventions mitigated the lasting adverse effects of LPS on gut immune function, partly through epigenetic mechanisms. A DNA methylation analysis demonstrated that enduring changes in gut immunity in adult mice might be linked to differentially methylated genes, including <i>Lpb</i>, <i>Rorc</i>, <i>Runx1</i>, <i>Il17ra</i>, <i>Rac1</i>, <i>Ccl5</i>, and <i>Il10</i>, involved in Th17 cell differentiation and IL-17 production and signaling. In addition, prebiotic administration prevented LPS-induced changes in the gut microbiota in pubertal mice. Together, these results indicate that following a healthy diet rich in prebiotics and probiotics is an optimal strategy for programming immune system function in the critical developmental windows of life and controlling inflammation later in life. |
| first_indexed | 2024-03-10T21:44:16Z |
| format | Article |
| id | doaj.art-fa62edf3a31e402e81a6724ae7180cd9 |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T21:44:16Z |
| publishDate | 2023-09-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-fa62edf3a31e402e81a6724ae7180cd92023-11-19T14:29:08ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-09-0124191461010.3390/ijms241914610<i>Lentinula edodes</i> Cultured Extract and <i>Rouxiella badensis</i> subsp. <i>acadiensis</i> (Canan SV-53) Intake Alleviates Immune Deregulation and Inflammation by Modulating Signaling Pathways and Epigenetic MechanismsRoghayeh Shahbazi0Hamed Yasavoli-Sharahi1Nawal Alsadi2Farzaneh Sharifzad3Sandra Fang4Cyrille Cuenin5Vincent Cahais6Felicia Fei-Lei Chung7Zdenko Herceg8Chantal Matar9Cellular and Molecular Medicine Department, Faculty of Medicine, University of Ottawa, Ottawa, ON K1H 8M5, CanadaCellular and Molecular Medicine Department, Faculty of Medicine, University of Ottawa, Ottawa, ON K1H 8M5, CanadaCellular and Molecular Medicine Department, Faculty of Medicine, University of Ottawa, Ottawa, ON K1H 8M5, CanadaDepartment of Urology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USATranslational Molecular Medicine Department, Faculty of Medicine, University of Ottawa, Ottawa, ON K1H 8M5, CanadaEpigenomics and Mechanisms Branch, International Agency for Research on Cancer (IARC), 25 Av. Tony Garnier, 69007 Lyon, FranceEpigenomics and Mechanisms Branch, International Agency for Research on Cancer (IARC), 25 Av. Tony Garnier, 69007 Lyon, FranceEpigenomics and Mechanisms Branch, International Agency for Research on Cancer (IARC), 25 Av. Tony Garnier, 69007 Lyon, FranceEpigenomics and Mechanisms Branch, International Agency for Research on Cancer (IARC), 25 Av. Tony Garnier, 69007 Lyon, FranceCellular and Molecular Medicine Department, Faculty of Medicine, University of Ottawa, Ottawa, ON K1H 8M5, CanadaPuberty is a critical developmental period of life characterized by marked physiological changes, including changes in the immune system and gut microbiota development. Exposure to inflammation induced by immune stressors during puberty has been found to stimulate central inflammation and lead to immune disturbance at distant sites from the gut; however, its enduring effects on gut immunity are not well explored. Therefore, in this study, we used a pubertal lipopolysaccharides (LPS)-induced inflammation mouse model to mimic pubertal exposure to inflammation and dysbiosis. We hypothesized that pubertal LPS-induced inflammation may cause long-term dysfunction in gut immunity by enduring dysregulation of inflammatory signaling and epigenetic changes, while prebiotic/probiotic intake may mitigate the gut immune system deregulation later in life. To this end, four-week-old female Balb/c mice were fed prebiotics/probiotics and exposed to LPS in the pubertal window. To better decipher the acute and enduring immunoprotective effects of biotic intake, we addressed the effect of treatment on interleukin (IL)-17 signaling related-cytokines and pathways. In addition, the effect of treatment on gut microbiota and epigenetic alterations, including changes in microRNA (miRNA) expression and DNA methylation, were studied. Our results revealed a significant dysregulation in selected cytokines, proteins, and miRNAs involved in key signaling pathways related to IL-17 production and function, including IL-17A and F, IL-6, IL-1β, transforming growth factor-β (TGF-β), signal transducer and activator of transcription-3 (STAT3), p-STAT3, forkhead box O1 (FOXO1), and miR-145 in the small intestine of adult mice challenged with LPS during puberty. In contrast, dietary interventions mitigated the lasting adverse effects of LPS on gut immune function, partly through epigenetic mechanisms. A DNA methylation analysis demonstrated that enduring changes in gut immunity in adult mice might be linked to differentially methylated genes, including <i>Lpb</i>, <i>Rorc</i>, <i>Runx1</i>, <i>Il17ra</i>, <i>Rac1</i>, <i>Ccl5</i>, and <i>Il10</i>, involved in Th17 cell differentiation and IL-17 production and signaling. In addition, prebiotic administration prevented LPS-induced changes in the gut microbiota in pubertal mice. Together, these results indicate that following a healthy diet rich in prebiotics and probiotics is an optimal strategy for programming immune system function in the critical developmental windows of life and controlling inflammation later in life.https://www.mdpi.com/1422-0067/24/19/14610gut microbiota<i>Lentinula edodes</i> myceliaprobiotic <i>Rouxiella badensis</i>interleukin-17FOXO1STAT3 |
| spellingShingle | Roghayeh Shahbazi Hamed Yasavoli-Sharahi Nawal Alsadi Farzaneh Sharifzad Sandra Fang Cyrille Cuenin Vincent Cahais Felicia Fei-Lei Chung Zdenko Herceg Chantal Matar <i>Lentinula edodes</i> Cultured Extract and <i>Rouxiella badensis</i> subsp. <i>acadiensis</i> (Canan SV-53) Intake Alleviates Immune Deregulation and Inflammation by Modulating Signaling Pathways and Epigenetic Mechanisms International Journal of Molecular Sciences gut microbiota <i>Lentinula edodes</i> mycelia probiotic <i>Rouxiella badensis</i> interleukin-17 FOXO1 STAT3 |
| title | <i>Lentinula edodes</i> Cultured Extract and <i>Rouxiella badensis</i> subsp. <i>acadiensis</i> (Canan SV-53) Intake Alleviates Immune Deregulation and Inflammation by Modulating Signaling Pathways and Epigenetic Mechanisms |
| title_full | <i>Lentinula edodes</i> Cultured Extract and <i>Rouxiella badensis</i> subsp. <i>acadiensis</i> (Canan SV-53) Intake Alleviates Immune Deregulation and Inflammation by Modulating Signaling Pathways and Epigenetic Mechanisms |
| title_fullStr | <i>Lentinula edodes</i> Cultured Extract and <i>Rouxiella badensis</i> subsp. <i>acadiensis</i> (Canan SV-53) Intake Alleviates Immune Deregulation and Inflammation by Modulating Signaling Pathways and Epigenetic Mechanisms |
| title_full_unstemmed | <i>Lentinula edodes</i> Cultured Extract and <i>Rouxiella badensis</i> subsp. <i>acadiensis</i> (Canan SV-53) Intake Alleviates Immune Deregulation and Inflammation by Modulating Signaling Pathways and Epigenetic Mechanisms |
| title_short | <i>Lentinula edodes</i> Cultured Extract and <i>Rouxiella badensis</i> subsp. <i>acadiensis</i> (Canan SV-53) Intake Alleviates Immune Deregulation and Inflammation by Modulating Signaling Pathways and Epigenetic Mechanisms |
| title_sort | i lentinula edodes i cultured extract and i rouxiella badensis i subsp i acadiensis i canan sv 53 intake alleviates immune deregulation and inflammation by modulating signaling pathways and epigenetic mechanisms |
| topic | gut microbiota <i>Lentinula edodes</i> mycelia probiotic <i>Rouxiella badensis</i> interleukin-17 FOXO1 STAT3 |
| url | https://www.mdpi.com/1422-0067/24/19/14610 |
| work_keys_str_mv | AT roghayehshahbazi ilentinulaedodesiculturedextractandirouxiellabadensisisubspiacadiensisicanansv53intakealleviatesimmunederegulationandinflammationbymodulatingsignalingpathwaysandepigeneticmechanisms AT hamedyasavolisharahi ilentinulaedodesiculturedextractandirouxiellabadensisisubspiacadiensisicanansv53intakealleviatesimmunederegulationandinflammationbymodulatingsignalingpathwaysandepigeneticmechanisms AT nawalalsadi ilentinulaedodesiculturedextractandirouxiellabadensisisubspiacadiensisicanansv53intakealleviatesimmunederegulationandinflammationbymodulatingsignalingpathwaysandepigeneticmechanisms AT farzanehsharifzad ilentinulaedodesiculturedextractandirouxiellabadensisisubspiacadiensisicanansv53intakealleviatesimmunederegulationandinflammationbymodulatingsignalingpathwaysandepigeneticmechanisms AT sandrafang ilentinulaedodesiculturedextractandirouxiellabadensisisubspiacadiensisicanansv53intakealleviatesimmunederegulationandinflammationbymodulatingsignalingpathwaysandepigeneticmechanisms AT cyrillecuenin ilentinulaedodesiculturedextractandirouxiellabadensisisubspiacadiensisicanansv53intakealleviatesimmunederegulationandinflammationbymodulatingsignalingpathwaysandepigeneticmechanisms AT vincentcahais ilentinulaedodesiculturedextractandirouxiellabadensisisubspiacadiensisicanansv53intakealleviatesimmunederegulationandinflammationbymodulatingsignalingpathwaysandepigeneticmechanisms AT feliciafeileichung ilentinulaedodesiculturedextractandirouxiellabadensisisubspiacadiensisicanansv53intakealleviatesimmunederegulationandinflammationbymodulatingsignalingpathwaysandepigeneticmechanisms AT zdenkoherceg ilentinulaedodesiculturedextractandirouxiellabadensisisubspiacadiensisicanansv53intakealleviatesimmunederegulationandinflammationbymodulatingsignalingpathwaysandepigeneticmechanisms AT chantalmatar ilentinulaedodesiculturedextractandirouxiellabadensisisubspiacadiensisicanansv53intakealleviatesimmunederegulationandinflammationbymodulatingsignalingpathwaysandepigeneticmechanisms |