IL-10-producing CD4(+) T Cells Negatively Regulate Fucosylation of Epithelial Cells in the Gut

Overview

Journal Sci Rep

Specialty Science

Date 2015 Nov 3

PMID 26522513

Citations 15

Authors

Yoshiyuki Goto

Aayam Lamichhane

Mariko Kamioka

Shintaro Sato

Kenya Honda

Jun Kunisawa

Hiroshi Kiyono

Affiliations

Soon will be listed here.

Abstract

Fucosylated glycans on the surface of epithelial cells (ECs) regulate intestinal homeostasis by serving as attachment receptors and a nutrient source for some species of bacteria. We show here that epithelial fucosylation in the ileum is negatively regulated by IL-10-producing CD4(+) T cells. The number of fucosylated ECs was increased in the ileum of mice lacking T cells, especially those expressing αβ T cell receptor (TCR), CD4, and IL-10. No such effect was observed in mice lacking B cells. Adoptive transfer of αβTCR(+) CD4(+) T cells from normal mice, but not IL-10-deficient mice, normalized fucosylation of ECs. These findings suggest that IL-10-producing CD4(+) T cells contribute to the maintenance of the function of ECs by regulating their fucosylation.

Citing Articles

Reciprocal Interactions Between Regulatory T Cells and Intestinal Epithelial Cells.

Jiang Z, Wu C Front Immunol. 2022; 13:951339.

PMID: 35860233 PMC: 9289291. DOI: 10.3389/fimmu.2022.951339.

Targeting Interleukin-10 Restores Graft Microvascular Supply and Airway Epithelium in Rejecting Allografts.

Kazmi S, Khan M, Shamma T, Altuhami A, Ahmed H, Assiri A Int J Mol Sci. 2022; 23(3).

PMID: 35163192 PMC: 8836023. DOI: 10.3390/ijms23031269.

Finding the sweet spot: glycosylation mediated regulation of intestinal inflammation.

Brazil J, Parkos C Mucosal Immunol. 2021; 15(2):211-222.

PMID: 34782709 PMC: 8591159. DOI: 10.1038/s41385-021-00466-8.

IL-10 Mediated Immunomodulation Limits Subepithelial Fibrosis and Repairs Airway Epithelium in Rejecting Airway Allografts.

Khan M, Ashoor G, Shamma T, Alanazi F, Altuhami A, Kazmi S Cells. 2021; 10(5).

PMID: 34069395 PMC: 8158696. DOI: 10.3390/cells10051248.

Acceptive Immunity: The Role of Fucosylated Glycans in Human Host-Microbiome Interactions.

Kononova S, Litvinova E, Vakhitov T, Skalinskaya M, Sitkin S Int J Mol Sci. 2021; 22(8).

PMID: 33917768 PMC: 8068183. DOI: 10.3390/ijms22083854.

References

McGovern D, Jones M, Taylor K, Marciante K, Yan X, Dubinsky M . Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Hum Mol Genet. 2010; 19(17):3468-76. PMC: 2916706. DOI: 10.1093/hmg/ddq248. View

Flannigan K, Agbor T, Blackler R, Kim J, Khan W, Verdu E . Impaired hydrogen sulfide synthesis and IL-10 signaling underlie hyperhomocysteinemia-associated exacerbation of colitis. Proc Natl Acad Sci U S A. 2014; 111(37):13559-64. PMC: 4169975. DOI: 10.1073/pnas.1413390111. View

Terahara K, Nochi T, Yoshida M, Takahashi Y, Goto Y, Hatai H . Distinct fucosylation of M cells and epithelial cells by Fut1 and Fut2, respectively, in response to intestinal environmental stress. Biochem Biophys Res Commun. 2010; 404(3):822-8. DOI: 10.1016/j.bbrc.2010.12.067. View

Fu J, Wei B, Wen T, Johansson M, Liu X, Bradford E . Loss of intestinal core 1-derived O-glycans causes spontaneous colitis in mice. J Clin Invest. 2011; 121(4):1657-66. PMC: 3069788. DOI: 10.1172/JCI45538. View

Wacklin P, Makivuokko H, Alakulppi N, Nikkila J, Tenkanen H, Rabina J . Secretor genotype (FUT2 gene) is strongly associated with the composition of Bifidobacteria in the human intestine. PLoS One. 2011; 6(5):e20113. PMC: 3098274. DOI: 10.1371/journal.pone.0020113. View

Miyoshi J, Yajima T, Okamoto S, Matsuoka K, Inoue N, Hisamatsu T . Ectopic expression of blood type antigens in inflamed mucosa with higher incidence of FUT2 secretor status in colonic Crohn's disease. J Gastroenterol. 2011; 46(9):1056-63. DOI: 10.1007/s00535-011-0425-7. View

Pot C, Apetoh L, Kuchroo V . Type 1 regulatory T cells (Tr1) in autoimmunity. Semin Immunol. 2011; 23(3):202-8. PMC: 3178065. DOI: 10.1016/j.smim.2011.07.005. View

Lathrop S, Bloom S, Rao S, Nutsch K, Lio C, Santacruz N . Peripheral education of the immune system by colonic commensal microbiota. Nature. 2011; 478(7368):250-4. PMC: 3192908. DOI: 10.1038/nature10434. View

Vaishnava S, Yamamoto M, Severson K, Ruhn K, Yu X, Koren O . The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science. 2011; 334(6053):255-8. PMC: 3321924. DOI: 10.1126/science.1209791. View

10.

Smyth D, Cooper J, Howson J, Clarke P, Downes K, Mistry T . FUT2 nonsecretor status links type 1 diabetes susceptibility and resistance to infection. Diabetes. 2011; 60(11):3081-4. PMC: 3198057. DOI: 10.2337/db11-0638. View

11.

Goto Y, Kiyono H . Epithelial barrier: an interface for the cross-communication between gut flora and immune system. Immunol Rev. 2011; 245(1):147-63. DOI: 10.1111/j.1600-065X.2011.01078.x. View

12.

Thom S, Blackwell C, MacCallum C, WEIR D, Brettle R, Kinane D . Non-secretion of blood group antigens and susceptibility to infection by Candida species. FEMS Microbiol Immunol. 1989; 1(6-7):401-5. DOI: 10.1111/j.1574-6968.1989.tb02428.x. View

13.

Bosma M, Carroll A . The SCID mouse mutant: definition, characterization, and potential uses. Annu Rev Immunol. 1991; 9:323-50. DOI: 10.1146/annurev.iy.09.040191.001543. View

14.

Mombaerts P, Iacomini J, Johnson R, Herrup K, Tonegawa S, Papaioannou V . RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 1992; 68(5):869-77. DOI: 10.1016/0092-8674(92)90030-g. View

15.

Mukai T, Arihara K, Itoh H . Lectin-like activity of Lactobacillus acidophilus strain JCM 1026. FEMS Microbiol Lett. 1992; 77(1-3):71-4. DOI: 10.1016/0378-1097(92)90134-a. View

16.

Ding L, Linsley P, Huang L, Germain R, Shevach E . IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J Immunol. 1993; 151(3):1224-34. View

17.

Strober W, Ehrhardt R . Chronic intestinal inflammation: an unexpected outcome in cytokine or T cell receptor mutant mice. Cell. 1993; 75(2):203-5. DOI: 10.1016/0092-8674(93)80062-j. View

18.

Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W . Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993; 75(2):263-74. DOI: 10.1016/0092-8674(93)80068-p. View

19.

Bry L, Falk P, Midtvedt T, Gordon J . A model of host-microbial interactions in an open mammalian ecosystem. Science. 1996; 273(5280):1380-3. DOI: 10.1126/science.273.5280.1380. View

20.

Yamamoto K, Miwa T, Taniguchi H, Nagano T, Shimamura K, Tanaka T . Binding specificity of Lactobacillus to glycolipids. Biochem Biophys Res Commun. 1996; 228(1):148-52. DOI: 10.1006/bbrc.1996.1630. View