Helicobacter species are potent drivers of colonic T cell responses in homeostasis and inflammation

Jiani N. Chai, Yangqing Peng, Sunaina Rengarajan, Benjamin D. Solomon, Teresa L. Ai, Zeli Shen, Justin S.A. Perry, Kathryn A. Knoop, Takeshi Tanoue, Seiko Narushima, Kenya Honda, Charles O. Elson, Rodney D. Newberry, Thaddeus S. Stappenbeck, Andrew L. Kau, Daniel A. Peterson, James G. Fox, Chyi Song Hsieh

Research output: Contribution to journalArticle

30 Citations (Scopus)

Abstract

Specific gut commensal bacteria improve host health by eliciting mutualistic regulatory T (Treg) cell responses. However, the bacteria that induce effector T (Teff) cells during inflammation are unclear. We addressed this by analyzing bacterial-reactive T cell receptor (TCR) transgenic cells and TCR repertoires in a murine colitis model. Unexpectedly, we found that mucosal-associated Helicobacter species triggered both Treg cell responses during homeostasis and Teff cell responses during colitis, as suggested by an increased overlap between the Teff/Treg TCR repertoires with colitis. Four of six Treg TCRs tested recognized mucosal-associated Helicobacter species in vitro and in vivo. By contrast, the marked expansion of luminal Bacteroides species seen during colitis did not trigger a commensurate Teff cell response. Unlike other Treg cell-inducing bacteria, Helicobacter species are known pathobionts and cause disease in immunodeficient mice. Thus, our study suggests a model in which mucosal bacteria elicit context-dependent Treg or Teff cell responses to facilitate intestinal tolerance or inflammation.

Original languageEnglish
JournalScience immunology
Volume2
Issue number13
DOIs
Publication statusPublished - 2017 Jul 21
Externally publishedYes

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Eragrostis
Helicobacter
Regulatory T-Lymphocytes
Colitis
Homeostasis
Inflammation
T-Lymphocytes
T-Cell Antigen Receptor
Bacteria
Bacteroides
Health

ASJC Scopus subject areas

  • Medicine(all)

Cite this

Chai, J. N., Peng, Y., Rengarajan, S., Solomon, B. D., Ai, T. L., Shen, Z., ... Hsieh, C. S. (2017). Helicobacter species are potent drivers of colonic T cell responses in homeostasis and inflammation. Science immunology, 2(13). https://doi.org/10.1126/sciimmunol.aal5068

Helicobacter species are potent drivers of colonic T cell responses in homeostasis and inflammation. / Chai, Jiani N.; Peng, Yangqing; Rengarajan, Sunaina; Solomon, Benjamin D.; Ai, Teresa L.; Shen, Zeli; Perry, Justin S.A.; Knoop, Kathryn A.; Tanoue, Takeshi; Narushima, Seiko; Honda, Kenya; Elson, Charles O.; Newberry, Rodney D.; Stappenbeck, Thaddeus S.; Kau, Andrew L.; Peterson, Daniel A.; Fox, James G.; Hsieh, Chyi Song.

In: Science immunology, Vol. 2, No. 13, 21.07.2017.

Research output: Contribution to journalArticle

Chai, JN, Peng, Y, Rengarajan, S, Solomon, BD, Ai, TL, Shen, Z, Perry, JSA, Knoop, KA, Tanoue, T, Narushima, S, Honda, K, Elson, CO, Newberry, RD, Stappenbeck, TS, Kau, AL, Peterson, DA, Fox, JG & Hsieh, CS 2017, 'Helicobacter species are potent drivers of colonic T cell responses in homeostasis and inflammation', Science immunology, vol. 2, no. 13. https://doi.org/10.1126/sciimmunol.aal5068
Chai, Jiani N. ; Peng, Yangqing ; Rengarajan, Sunaina ; Solomon, Benjamin D. ; Ai, Teresa L. ; Shen, Zeli ; Perry, Justin S.A. ; Knoop, Kathryn A. ; Tanoue, Takeshi ; Narushima, Seiko ; Honda, Kenya ; Elson, Charles O. ; Newberry, Rodney D. ; Stappenbeck, Thaddeus S. ; Kau, Andrew L. ; Peterson, Daniel A. ; Fox, James G. ; Hsieh, Chyi Song. / Helicobacter species are potent drivers of colonic T cell responses in homeostasis and inflammation. In: Science immunology. 2017 ; Vol. 2, No. 13.
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