Selective probiotic bacteria induce IL-10–producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell–specific intercellular adhesion molecule 3–grabbing nonintegrin
Lactobacilli are probiotic bacteria that are frequently tested in the management of allergic diseases or gastroenteritis. It is hypothesized that these probiotics have immunoregulatory properties and promote mucosal tolerance, which is in part mediated by regulatory T cells (Treg cells). On the basi...
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| Published in | Journal of Allergy and Clinical Immunology Vol. 115; no. 6; pp. 1260 - 1267 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York, NY
Mosby, Inc
01.06.2005
Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Lactobacilli are probiotic bacteria that are frequently tested in the management of allergic diseases or gastroenteritis. It is hypothesized that these probiotics have immunoregulatory properties and promote mucosal tolerance, which is in part mediated by regulatory T cells (Treg cells). On the basis of pathogenic or tissue-specific priming, dendritic cells (DC) acquire different T cell–instructive signals and drive the differentiation of naive T
H cells into either T
H1, T
H2, or regulatory effector T cells.
We studied in what way different species of lactobacilli prime human DCs for their ability to drive Treg cells.
Human monocyte-derived DCs were cultured
in vitro with lactobacilli of different species.
Two different species of lactobacilli,
Lactobacillus reuteri and
Lactobacillus casei, but not
Lactobacillus plantarum, prime monocyte-derived DCs to drive the development of Treg cells. These Treg cells produced increased levels of IL-10 and were capable of inhibiting the proliferation of bystander T cells in an IL-10–dependent fashion. Strikingly, both
L reuteri and
L casei, but not
L plantarum, bind the C-type lectin DC-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN). Blocking antibodies to DC-SIGN inhibited the induction of the Treg cells by these probiotic bacteria, stressing that ligation of DC-SIGN can actively prime DCs to induce Treg cells.
The targeting of DC-SIGN by certain probiotic bacteria might explain their beneficial effect in the treatment of a number of inflammatory diseases, including atopic dermatitis and Crohn's disease. |
|---|---|
| AbstractList | Background Lactobacilli are probiotic bacteria that are frequently tested in the management of allergic diseases or gastroenteritis. It is hypothesized that these probiotics have immunoregulatory properties and promote mucosal tolerance, which is in part mediated by regulatory T cells (Treg cells). On the basis of pathogenic or tissue-specific priming, dendritic cells (DC) acquire different T cell-instructive signals and drive the differentiation of naive T sub(H) cells into either T sub(H)1, T sub(H)2, or regulatory effector T cells. Objective We studied in what way different species of lactobacilli prime human DCs for their ability to drive Treg cells. Methods Human monocyte-derived DCs were cultured in vitro with lactobacilli of different species. Results Two different species of lactobacilli, Lactobacillus reuteri and Lactobacillus casei, but not Lactobacillus plantarum, prime monocyte-derived DCs to drive the development of Treg cells. These Treg cells produced increased levels of IL-10 and were capable of inhibiting the proliferation of bystander T cells in an IL-10-dependent fashion. Strikingly, both L reuteri and L casei, but not L plantarum, bind the C-type lectin DC-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN). Blocking antibodies to DC-SIGN inhibited the induction of the Treg cells by these probiotic bacteria, stressing that ligation of DC-SIGN can actively prime DCs to induce Treg cells. Conclusions The targeting of DC-SIGN by certain probiotic bacteria might explain their beneficial effect in the treatment of a number of inflammatory diseases, including atopic dermatitis and Crohn's disease. Lactobacilli are probiotic bacteria that are frequently tested in the management of allergic diseases or gastroenteritis. It is hypothesized that these probiotics have immunoregulatory properties and promote mucosal tolerance, which is in part mediated by regulatory T cells (Treg cells). On the basis of pathogenic or tissue-specific priming, dendritic cells (DC) acquire different T cell-instructive signals and drive the differentiation of naive T H cells into either T H 1, T H 2, or regulatory effector T cells. We studied in what way different species of lactobacilli prime human DCs for their ability to drive Treg cells. Human monocyte-derived DCs were cultured in vitro with lactobacilli of different species. Two different species of lactobacilli, Lactobacillus reuteri and Lactobacillus casei , but not Lactobacillus plantarum, prime monocyte-derived DCs to drive the development of Treg cells. These Treg cells produced increased levels of IL-10 and were capable of inhibiting the proliferation of bystander T cells in an IL-10-dependent fashion. Strikingly, both L reuteri and L casei , but not L plantarum , bind the C-type lectin DC-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN). Blocking antibodies to DC-SIGN inhibited the induction of the Treg cells by these probiotic bacteria, stressing that ligation of DC-SIGN can actively prime DCs to induce Treg cells. The targeting of DC-SIGN by certain probiotic bacteria might explain their beneficial effect in the treatment of a number of inflammatory diseases, including atopic dermatitis and Crohn's disease. BACKGROUNDLactobacilli are probiotic bacteria that are frequently tested in the management of allergic diseases or gastroenteritis. It is hypothesized that these probiotics have immunoregulatory properties and promote mucosal tolerance, which is in part mediated by regulatory T cells (Treg cells). On the basis of pathogenic or tissue-specific priming, dendritic cells (DC) acquire different T cell-instructive signals and drive the differentiation of naive T H cells into either T H 1, T H 2, or regulatory effector T cells.OBJECTIVEWe studied in what way different species of lactobacilli prime human DCs for their ability to drive Treg cells.METHODSHuman monocyte-derived DCs were cultured in vitro with lactobacilli of different species.RESULTSTwo different species of lactobacilli, Lactobacillus reuteri and Lactobacillus casei , but not Lactobacillus plantarum, prime monocyte-derived DCs to drive the development of Treg cells. These Treg cells produced increased levels of IL-10 and were capable of inhibiting the proliferation of bystander T cells in an IL-10-dependent fashion. Strikingly, both L reuteri and L casei , but not L plantarum , bind the C-type lectin DC-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN). Blocking antibodies to DC-SIGN inhibited the induction of the Treg cells by these probiotic bacteria, stressing that ligation of DC-SIGN can actively prime DCs to induce Treg cells.CONCLUSIONSThe targeting of DC-SIGN by certain probiotic bacteria might explain their beneficial effect in the treatment of a number of inflammatory diseases, including atopic dermatitis and Crohn's disease. Lactobacilli are probiotic bacteria that are frequently tested in the management of allergic diseases or gastroenteritis. It is hypothesized that these probiotics have immunoregulatory properties and promote mucosal tolerance, which is in part mediated by regulatory T cells (Treg cells). On the basis of pathogenic or tissue-specific priming, dendritic cells (DC) acquire different T cell–instructive signals and drive the differentiation of naive T H cells into either T H1, T H2, or regulatory effector T cells. We studied in what way different species of lactobacilli prime human DCs for their ability to drive Treg cells. Human monocyte-derived DCs were cultured in vitro with lactobacilli of different species. Two different species of lactobacilli, Lactobacillus reuteri and Lactobacillus casei, but not Lactobacillus plantarum, prime monocyte-derived DCs to drive the development of Treg cells. These Treg cells produced increased levels of IL-10 and were capable of inhibiting the proliferation of bystander T cells in an IL-10–dependent fashion. Strikingly, both L reuteri and L casei, but not L plantarum, bind the C-type lectin DC-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN). Blocking antibodies to DC-SIGN inhibited the induction of the Treg cells by these probiotic bacteria, stressing that ligation of DC-SIGN can actively prime DCs to induce Treg cells. The targeting of DC-SIGN by certain probiotic bacteria might explain their beneficial effect in the treatment of a number of inflammatory diseases, including atopic dermatitis and Crohn's disease. |
| Author | Kapsenberg, Martien L. van der Kleij, Desiree Yazdanbakhsh, Maria de Jong, Esther C. Wierenga, Eddy A. Engering, Anneke Schipper, Kim van Kooyk, Yvette Smits, Hermelijn H. van Capel, Toni M.M. Zaat, Bas A.J. |
| Author_xml | – sequence: 1 givenname: Hermelijn H. surname: Smits fullname: Smits, Hermelijn H. organization: From the Departments of Cell Biology and Histology – sequence: 2 givenname: Anneke surname: Engering fullname: Engering, Anneke organization: Department of Molecular Cell Biology and Immunology, VUMC Vrije Universiteit Medical Center, Amsterdam – sequence: 3 givenname: Desiree surname: van der Kleij fullname: van der Kleij, Desiree organization: Department of Parasitology, Leiden University Medical Center – sequence: 4 givenname: Esther C. surname: de Jong fullname: de Jong, Esther C. organization: From the Departments of Cell Biology and Histology – sequence: 5 givenname: Kim surname: Schipper fullname: Schipper, Kim organization: Medical Microbiology – sequence: 6 givenname: Toni M.M. surname: van Capel fullname: van Capel, Toni M.M. organization: From the Departments of Cell Biology and Histology – sequence: 7 givenname: Bas A.J. surname: Zaat fullname: Zaat, Bas A.J. organization: Medical Microbiology – sequence: 8 givenname: Maria surname: Yazdanbakhsh fullname: Yazdanbakhsh, Maria organization: Department of Parasitology, Leiden University Medical Center – sequence: 9 givenname: Eddy A. surname: Wierenga fullname: Wierenga, Eddy A. organization: From the Departments of Cell Biology and Histology – sequence: 10 givenname: Yvette surname: van Kooyk fullname: van Kooyk, Yvette organization: Department of Molecular Cell Biology and Immunology, VUMC Vrije Universiteit Medical Center, Amsterdam – sequence: 11 givenname: Martien L. surname: Kapsenberg fullname: Kapsenberg, Martien L. email: M.L.Kapsenberg@amc.uva.nl organization: From the Departments of Cell Biology and Histology |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=16927037$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/15940144$$D View this record in MEDLINE/PubMed |
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| Keywords | Human dendritic cell–specific intercellular adhesion molecule 3–grabbing nonintegrin bacteria MR Treg cell IL-10 PRR dendritic cells cfu DC-SIGN MF toll-like receptor TLR DC Probiotic Immunopathology Dendritic cell Cell function Intercellular adhesion molecule 3 Cytokine Cell adhesion molecule In vitro Immunology Antigen presenting cell Interleukin 10 T-Lymphocyte Bacteria Regulatory cell dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin |
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| PublicationTitle | Journal of Allergy and Clinical Immunology |
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| Snippet | Lactobacilli are probiotic bacteria that are frequently tested in the management of allergic diseases or gastroenteritis. It is hypothesized that these... Background Lactobacilli are probiotic bacteria that are frequently tested in the management of allergic diseases or gastroenteritis. It is hypothesized that... BACKGROUNDLactobacilli are probiotic bacteria that are frequently tested in the management of allergic diseases or gastroenteritis. It is hypothesized that... |
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| SubjectTerms | Antigens, CD - immunology bacteria Biological and medical sciences Cell Adhesion Molecules Cell Division Cells, Cultured dendritic cells Dendritic Cells - immunology dendritic cell–specific intercellular adhesion molecule 3–grabbing nonintegrin Fundamental and applied biological sciences. Psychology Fundamental immunology Human Humans IL-10 Immunopathology Interleukin-10 - biosynthesis Interleukin-10 - pharmacology Lactobacillus Lactobacillus casei Lactobacillus plantarum Lactobacillus reuteri Lectins, C-Type - immunology Medical sciences Monocytes - immunology Probiotics Species Specificity T-Lymphocytes - immunology toll-like receptor Up-Regulation |
| Title | Selective probiotic bacteria induce IL-10–producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell–specific intercellular adhesion molecule 3–grabbing nonintegrin |
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