Segmented Filamentous Bacteria Induce Divergent Populations of Antigen-Specific CD4 T Cells in the Small Intestine

CD4 T cells differentiate into RORγt/IL-17A-expressing cells in the small intestine following colonization by segmented filamentous bacteria (SFB). However, it remains unclear whether SFB-specific CD4 T cells can differentiate directly from naïve precursors, and whether their effector differentiation is solely directed towards the Th17 lineage. In this study, we used adoptive T cell transfer experiments and showed that naïve CD4 T cells can migrate to the small intestinal lamina propria (sLP) and differentiate into effector T cells that synthesize IL-17A in response to SFB colonization. Using single cell RT-PCR analysis, we showed that the progenies of SFB responding T cells are not uniform but composed of transcriptionally divergent populations including Th1, Th17 and follicular helper T cells. We further confirmed this finding using in vitro culture of SFB specific intestinal CD4 T cells in the presence of cognate antigens, which also generated heterogeneous population with similar features. Collectively, these findings indicate that a single species of intestinal bacteria can generate a divergent population of antigen-specific effector CD4 T cells, rather than it provides a cytokine milieu for the development of a particular effector T cell subset.

[1]  Mirang Kim,et al.  Dynamic Transcriptome, DNA Methylome, and DNA Hydroxymethylome Networks During T-Cell Lineage Commitment , 2018, Molecules and cells.

[2]  A. Sher,et al.  Memory-phenotype CD4+ T cells spontaneously generated under steady-state conditions exert innate TH1-like effector function , 2017, Science Immunology.

[3]  Yuichi Maeda,et al.  Role of Gut Microbiota in Rheumatoid Arthritis , 2017, Journal of clinical medicine.

[4]  P. Langella,et al.  Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria , 2017, Microbial Cell Factories.

[5]  D. Veale,et al.  Ex-Th17 (Nonclassical Th1) Cells Are Functionally Distinct from Classical Th1 and Th17 Cells and Are Not Constrained by Regulatory T Cells , 2017, The Journal of Immunology.

[6]  N. Tran,et al.  Gut Microbiota Drive Autoimmune Arthritis by Promoting Differentiation and Migration of Peyer's Patch T Follicular Helper Cells. , 2016, Immunity.

[7]  K. S. Kim,et al.  Dietary antigens limit mucosal immunity by inducing regulatory T cells in the small intestine , 2016, Science.

[8]  M. Hattori,et al.  Th17 Cell Induction by Adhesion of Microbes to Intestinal Epithelial Cells , 2015, Cell.

[9]  Ana I. Domingos,et al.  An IL-23R/IL-22 Circuit Regulates Epithelial Serum Amyloid A to Promote Local Effector Th17 Responses , 2015, Cell.

[10]  I. Ivanov,et al.  Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. , 2014, Immunity.

[11]  Jonathan L. Linehan,et al.  Focused Specificity of Intestinal Th17 Cells towards Commensal Bacterial Antigens , 2014, Nature.

[12]  C. Surh,et al.  Homeostatic proliferation of mature T cells. , 2013, Methods in molecular biology.

[13]  R. D. Hatton,et al.  Reciprocal interactions of the intestinal microbiota and immune system , 2012, Nature.

[14]  Veronica Sanchez-Freire,et al.  Microfluidic single-cell real-time PCR for comparative analysis of gene expression patterns , 2012, Nature Protocols.

[15]  J. Roderick,et al.  Notch Signaling Regulates Mouse and Human Th17 Differentiation , 2011, The Journal of Immunology.

[16]  S. Hapfelmeier,et al.  Intestinal bacterial colonization induces mutualistic regulatory T cell responses. , 2011, Immunity.

[17]  K. Honda,et al.  Induction of Colonic Regulatory T Cells by Indigenous Clostridium Species , 2011, Science.

[18]  S. Mazmanian,et al.  Has the Microbiota Played a Critical Role in the Evolution of the Adaptive Immune System? , 2010, Science.

[19]  Brigitta Stockinger,et al.  Effector T cell plasticity: flexibility in the face of changing circumstances , 2010, Nature Immunology.

[20]  Christophe Benoist,et al.  Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. , 2010, Immunity.

[21]  S. Mazmanian,et al.  Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota , 2010, Proceedings of the National Academy of Sciences.

[22]  C. Elson,et al.  Microbiota innate stimulation is a prerequisite for T cell spontaneous proliferation and induction of experimental colitis , 2010, The Journal of experimental medicine.

[23]  Dan R. Littman,et al.  Induction of Intestinal Th17 Cells by Segmented Filamentous Bacteria , 2009, Cell.

[24]  L. Hooper,et al.  Gut commensal bacteria direct a protective immune response against Toxoplasma gondii. , 2009, Cell host & microbe.

[25]  Chen Dong,et al.  T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. , 2008, Immunity.

[26]  J. Kolls,et al.  Th17 cells and mucosal host defense. , 2007, Seminars in immunology.

[27]  T. Macdonald,et al.  Immunity, Inflammation, and Allergy in the Gut , 2005, Science.

[28]  S. Targan,et al.  Bacterial flagellin is a dominant antigen in Crohn disease. , 2004, The Journal of clinical investigation.

[29]  A. Kelso Educating T cells: early events in the differentiation and commitment of cytokine-producing CD4+ and CD8+ T cells , 2004, Springer Seminars in Immunopathology.

[30]  A. Imaoka,et al.  Differential Roles of Segmented Filamentous Bacteria and Clostridia in Development of the Intestinal Immune System , 1999, Infection and Immunity.

[31]  R. Coffman,et al.  Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. , 1994, Immunity.

[32]  A. Beynen,et al.  Mono-association of mice with non-cultivable, intestinal, segmented, filamentous bacteria , 1991, Archives of Microbiology.