Oral Probiotic VSL#3 Prevents Autoimmune Diabetes by Modulating Microbiota and Promoting Indoleamine 2,3-Dioxygenase-Enriched Tolerogenic Intestinal Environment
The gut microbiota modulates the autoimmune pathogenesis of type 1 diabetes (T1D) via mechanisms that remain largely unknown. The inflammasome components are innate immune sensors that are highly influenced by the gut environment and play pivotal roles in maintaining intestinal immune homeostasis. I...
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| Vydané v: | Journal of Diabetes Research Ročník 2016; číslo 2016; s. 1 - 12 |
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| Hlavní autori: | , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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Cairo, Egypt
Hindawi Publishing Corporation
01.01.2016
John Wiley & Sons, Inc Wiley |
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| ISSN: | 2314-6745, 2314-6753, 2314-6753 |
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| Abstract | The gut microbiota modulates the autoimmune pathogenesis of type 1 diabetes (T1D) via mechanisms that remain largely unknown. The inflammasome components are innate immune sensors that are highly influenced by the gut environment and play pivotal roles in maintaining intestinal immune homeostasis. In this study we show that modifications of the gut microbiota induced by oral treatment with Lactobacillaceae-enriched probiotic VSL#3, alone or in combination with retinoic acid (RA), protect NOD mice from T1D by affecting inflammasome at the intestinal level. In particular, we show that VSL#3 treatment inhibits IL-1β expression while enhancing release of protolerogenic components of the inflammasome, such as indoleamine 2,3-dioxygenase (IDO) and IL-33. Those modifications of the intestinal microenvironment in VSL#3-treated NOD mice modulate gut immunity by promoting differentiation of tolerogenic CD103+ DCs and reducing differentiation/expansion of Th1 and Th17 cells in the intestinal mucosa and at the sites of autoimmunity, that is, within the pancreatic lymph nodes (PLN) of VSL#3-treated NOD mice. Our data provide a link between dietary factors, microbiota composition, intestinal inflammation, and immune homeostasis in autoimmune diabetes and could pave the way for new therapeutic approaches aimed at changing the intestinal microenvironment with probiotics to counterregulate autoimmunity and prevent T1D. |
|---|---|
| AbstractList | The gut microbiota modulates the autoimmune pathogenesis of type 1 diabetes (T1D) via mechanisms that remain largely unknown. The inflammasome components are innate immune sensors that are highly influenced by the gut environment and play pivotal roles in maintaining intestinal immune homeostasis. In this study we show that modifications of the gut microbiota induced by oral treatment with Lactobacillaceae-enriched probiotic VSL#3, alone or in combination with retinoic acid (RA), protect NOD mice from T1D by affecting inflammasome at the intestinal level. In particular, we show that VSL#3 treatment inhibits IL-1
β
expression while enhancing release of protolerogenic components of the inflammasome, such as indoleamine 2,3-dioxygenase (IDO) and IL-33. Those modifications of the intestinal microenvironment in VSL#3-treated NOD mice modulate gut immunity by promoting differentiation of tolerogenic CD103
+
DCs and reducing differentiation/expansion of Th1 and Th17 cells in the intestinal mucosa and at the sites of autoimmunity, that is, within the pancreatic lymph nodes (PLN) of VSL#3-treated NOD mice. Our data provide a link between dietary factors, microbiota composition, intestinal inflammation, and immune homeostasis in autoimmune diabetes and could pave the way for new therapeutic approaches aimed at changing the intestinal microenvironment with probiotics to counterregulate autoimmunity and prevent T1D. The gut microbiota modulates the autoimmune pathogenesis of type 1 diabetes (T1D) via mechanisms that remain largely unknown. The inflammasome components are innate immune sensors that are highly influenced by the gut environment and play pivotal roles in maintaining intestinal immune homeostasis. In this study we show that modifications of the gut microbiota induced by oral treatment with Lactobacillaceae-enriched probiotic VSL#3, alone or in combination with retinoic acid (RA), protect NOD mice from T1D by affecting inflammasome at the intestinal level. In particular, we show that VSL#3 treatment inhibits IL-1β expression while enhancing release of protolerogenic components of the inflammasome, such as indoleamine 2,3-dioxygenase (IDO) and IL-33. Those modifications of the intestinal microenvironment in VSL#3-treated NOD mice modulate gut immunity by promoting differentiation of tolerogenic CD103+ DCs and reducing differentiation/expansion of Th1 and Th17 cells in the intestinal mucosa and at the sites of autoimmunity, that is, within the pancreatic lymph nodes (PLN) of VSL#3-treated NOD mice. Our data provide a link between dietary factors, microbiota composition, intestinal inflammation, and immune homeostasis in autoimmune diabetes and could pave the way for new therapeutic approaches aimed at changing the intestinal microenvironment with probiotics to counterregulate autoimmunity and prevent T1D. The gut microbiota modulates the autoimmune pathogenesis of type 1 diabetes (T1D) via mechanisms that remain largely unknown. The inflammasome components are innate immune sensors that are highly influenced by the gut environment and play pivotal roles in maintaining intestinal immune homeostasis. In this study we show that modifications of the gut microbiota induced by oral treatment with Lactobacillaceae-enriched probiotic VSL#3, alone or in combination with retinoic acid (RA), protect NOD mice from T1D by affecting inflammasome at the intestinal level. In particular, we show that VSL#3 treatment inhibits IL-1β expression while enhancing release of protolerogenic components of the inflammasome, such as indoleamine 2,3-dioxygenase (IDO) and IL-33. Those modifications of the intestinal microenvironment in VSL#3-treated NOD mice modulate gut immunity by promoting differentiation of tolerogenic [CD103.sup.+] DCs and reducing differentiation/expansion of Th1 and Th17 cells in the intestinal mucosa and at the sites of autoimmunity, that is, within the pancreatic lymph nodes (PLN) of VSL#3-treated NOD mice. Our data provide a link between dietary factors, microbiota composition, intestinal inflammation, and immune homeostasis in autoimmune diabetes and could pave the way for new therapeutic approaches aimed at changing the intestinal microenvironment with probiotics to counterregulate autoimmunity and prevent T1D. The gut microbiota modulates the autoimmune pathogenesis of type 1 diabetes (T1D) via mechanisms that remain largely unknown. The inflammasome components are innate immune sensors that are highly influenced by the gut environment and play pivotal roles in maintaining intestinal immune homeostasis. In this study we show that modifications of the gut microbiota induced by oral treatment with Lactobacillaceae-enriched probiotic VSL#3, alone or in combination with retinoic acid (RA), protect NOD mice from T1D by affecting inflammasome at the intestinal level. In particular, we show that VSL#3 treatment inhibits IL-1β expression while enhancing release of protolerogenic components of the inflammasome, such as indoleamine 2,3-dioxygenase (IDO) and IL-33. Those modifications of the intestinal microenvironment in VSL#3-treated NOD mice modulate gut immunity by promoting differentiation of tolerogenic CD103(+) DCs and reducing differentiation/expansion of Th1 and Th17 cells in the intestinal mucosa and at the sites of autoimmunity, that is, within the pancreatic lymph nodes (PLN) of VSL#3-treated NOD mice. Our data provide a link between dietary factors, microbiota composition, intestinal inflammation, and immune homeostasis in autoimmune diabetes and could pave the way for new therapeutic approaches aimed at changing the intestinal microenvironment with probiotics to counterregulate autoimmunity and prevent T1D.The gut microbiota modulates the autoimmune pathogenesis of type 1 diabetes (T1D) via mechanisms that remain largely unknown. The inflammasome components are innate immune sensors that are highly influenced by the gut environment and play pivotal roles in maintaining intestinal immune homeostasis. In this study we show that modifications of the gut microbiota induced by oral treatment with Lactobacillaceae-enriched probiotic VSL#3, alone or in combination with retinoic acid (RA), protect NOD mice from T1D by affecting inflammasome at the intestinal level. In particular, we show that VSL#3 treatment inhibits IL-1β expression while enhancing release of protolerogenic components of the inflammasome, such as indoleamine 2,3-dioxygenase (IDO) and IL-33. Those modifications of the intestinal microenvironment in VSL#3-treated NOD mice modulate gut immunity by promoting differentiation of tolerogenic CD103(+) DCs and reducing differentiation/expansion of Th1 and Th17 cells in the intestinal mucosa and at the sites of autoimmunity, that is, within the pancreatic lymph nodes (PLN) of VSL#3-treated NOD mice. Our data provide a link between dietary factors, microbiota composition, intestinal inflammation, and immune homeostasis in autoimmune diabetes and could pave the way for new therapeutic approaches aimed at changing the intestinal microenvironment with probiotics to counterregulate autoimmunity and prevent T1D. The gut microbiota modulates the autoimmune pathogenesis of type 1 diabetes (T1D) via mechanisms that remain largely unknown. The inflammasome components are innate immune sensors that are highly influenced by the gut environment and play pivotal roles in maintaining intestinal immune homeostasis. In this study we show that modifications of the gut microbiota induced by oral treatment with Lactobacillaceae-enriched probiotic VSL#3, alone or in combination with retinoic acid (RA), protect NOD mice from T1D by affecting inflammasome at the intestinal level. In particular, we show that VSL#3 treatment inhibits IL-1β expression while enhancing release of protolerogenic components of the inflammasome, such as indoleamine 2,3-dioxygenase (IDO) and IL-33. Those modifications of the intestinal microenvironment in VSL#3-treated NOD mice modulate gut immunity by promoting differentiation of tolerogenic CD103+ DCs and reducing differentiation/expansion of Th1 and Th17 cells in the intestinal mucosa and at the sites of autoimmunity, that is, within the pancreatic lymph nodes (PLN) of VSL#3-treated NOD mice. Our data provide a link between dietary factors, microbiota composition, intestinal inflammation, and immune homeostasis in autoimmune diabetes and could pave the way for new therapeutic approaches aimed at changing the intestinal microenvironment with probiotics to counterregulate autoimmunity and prevent T1D. |
| Audience | Academic |
| Author | Dolpady, Jayashree Canducci, Filippo Ferrarese, Roberto Sorini, Chiara Di Pietro, Caterina Clementi, Massimo Saita, Diego Cosorich, Ilaria Falcone, Marika |
| AuthorAffiliation | 1 Experimental Diabetes Unit, Diabetes Research Institute, Division of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific Institute, Via Olgettina 60, 20132 Milan, Italy 3 Department of Biotechnology and Life Sciences, University of Insubria, 21100 Varese, Italy 2 Microbiology Unit, IRCCS San Raffaele Scientific Institute, Via Olgettina 60, 20132 Milan, Italy |
| AuthorAffiliation_xml | – name: 3 Department of Biotechnology and Life Sciences, University of Insubria, 21100 Varese, Italy – name: 2 Microbiology Unit, IRCCS San Raffaele Scientific Institute, Via Olgettina 60, 20132 Milan, Italy – name: 1 Experimental Diabetes Unit, Diabetes Research Institute, Division of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific Institute, Via Olgettina 60, 20132 Milan, Italy |
| Author_xml | – sequence: 1 fullname: Falcone, Marika – sequence: 2 fullname: Canducci, Filippo – sequence: 3 fullname: Saita, Diego – sequence: 4 fullname: Ferrarese, Roberto – sequence: 5 fullname: Cosorich, Ilaria – sequence: 6 fullname: Di Pietro, Caterina – sequence: 7 fullname: Sorini, Chiara – sequence: 8 fullname: Dolpady, Jayashree – sequence: 9 fullname: Clementi, Massimo |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26779542$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2016 Jayashree Dolpady et al. COPYRIGHT 2015 John Wiley & Sons, Inc. Copyright © 2016 Jayashree Dolpady et al. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Copyright © 2016 Jayashree Dolpady et al. 2016 |
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| References | (16) 2004; 36 (33) 1987; 67 (27) 2011; 331 (23) 2014; 10 (4) 2011; 5 (6) 2008; 455 (29) 1998; 273 (30) 2012; 481 (13) 1986; 29 Lefrançois L. Lycke N. UNIT 3.19 isolation of mouse small intestinal intraepithelial lymphocytes, Peyer's Patch, and lamina propria cells Current Protocols in Immunology 2001 chapter 3 John Wiley & Sons 10.1002/0471142735.im0319s17 (19) 1997; 46 (26) 2008; 8 (41) 2007; 204 (11) 2004; 53 (37) 2005; 102 (38) 2009; 1165 (9) 2013; 2 (15) 2003; 52 (42) 2014; 40 (40) 2007; 204 (2) 2014; 146 (44) 2005; 102 (12) 2005; 48 (20) 2009; 47 (3) 2013; 11 (34) 2013; 34 (14) 1999; 28 (31) 2012; 5, article 18 (36) 2005; 23 (28) 2013; 500 (10) 1999; 276 (35) 2010; 59 (43) 2012; 123 (1) 2011; 473 (21) 2007; 137 (18) 1996; 45 (39) 2010; 53 (5) 2011; 6 (7) 2005; 48 (8) 2011; 479 (17) 2011; 60 (25) 2007; 2 (32) 2013; 4, article 181 (22) 2014; 9 22 44 23 24 25 26 27 28 29 30 31 32 11 12 34 13 35 14 36 15 37 16 38 17 39 18 19 1 2 3 4 5 6 7 8 40 41 20 42 43 |
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| SubjectTerms | Administration, Oral Age Factors Animals Autoimmunity Cellular Microenvironment Cytokines Diabetes Diabetes Mellitus, Type 1 - enzymology Diabetes Mellitus, Type 1 - immunology Diabetes Mellitus, Type 1 - microbiology Diabetes Mellitus, Type 1 - prevention & control Disease Models, Animal Flow cytometry Gastrointestinal Microbiome Homeostasis Hypotheses Indoleamine-Pyrrole 2,3,-Dioxygenase - immunology Indoleamine-Pyrrole 2,3,-Dioxygenase - metabolism Inflammasomes - immunology Inflammasomes - metabolism Interleukin-1beta - metabolism Interleukin-33 - metabolism Intestines - enzymology Intestines - immunology Intestines - microbiology Lactobacillaceae - growth & development Lactobacillaceae - immunology Lymphatic system Mice, Inbred NOD Microbiota Microbiota (Symbiotic organisms) Pathogenesis Probiotics Probiotics - administration & dosage Software Th1 Cells - immunology Th1 Cells - metabolism Th1 Cells - microbiology Th17 Cells - immunology Th17 Cells - metabolism Th17 Cells - microbiology Tretinoin - pharmacology Type 1 diabetes Vitamin A |
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| Title | Oral Probiotic VSL#3 Prevents Autoimmune Diabetes by Modulating Microbiota and Promoting Indoleamine 2,3-Dioxygenase-Enriched Tolerogenic Intestinal Environment |
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