Literature DB >> 24515806

IL-13Rα2-bearing, type II NKT cells reactive to sulfatide self-antigen populate the mucosa of ulcerative colitis.

Ivan J Fuss1, Bharat Joshi2, Zhiqiong Yang1, Heba Degheidy2, Stefan Fichtner-Feigl3, Heitor de Souza4, Florian Rieder4, Franco Scaldaferri4, Anja Schirbel4, Melania Scarpa4, Gail West4, Chuli Yi1, Lili Xu1, Pamela Leland2, Michael Yao1, Peter Mannon1, Raj K Puri2, Claudio Fiocchi4, Warren Strober1.   

Abstract

OBJECTIVE: Previous studies have shown that ulcerative colitis (UC) is associated with the presence of lamina propria non-invariant (Type II) NKT cells producing IL-13 and mediating epithelial cell cytotoxicity. Here we sought to define the antigen(s) stimulating the NKT cells and to quantitate these cells in the UC lamina propria.
DESIGN: Detection of Type II NKT cells in UC lamina propria mononuclear cells (LPMC) with lyso-sulfatide loaded tetramer and quantum dot-based flow cytometry and staining. Culture of UC LPMCs with lyso-sulfatide glycolipid to determine sulfatide induction of epithelial cell cytotoxicity, IL-13 production and IL-13Rα2 expression. Blinded quantum dot-based phenotypic analysis to assess UC LPMC expression of IL-13Rα2, CD161 and IL-13.
RESULTS: Approximately 36% of UC LPMC were lyso-sulfatide tetramer positive, whereas few, if any, control LPMCs were positive. When tested, the positive cells were also CD3 and IL-13Rα2 positive. Culture of UC LPMC with lyso-sulfatide glycolipid showed that sulfatide stimulates UC LPMC production of IL-13 and induces UC CD161 LPMC-mediated cytotoxicity of activated epithelial cells; additionally, lyso-sulfatide induces enhanced expression of IL-13Rα2. Finally, blinded phenotypic analysis of UC LP MC using multicolour quantum dot-staining technology showed that approximately 60% of the LPMC bear both IL-13Rα2 and CD161 and most of these cells also produce IL-13.
CONCLUSIONS: These studies show that UC lamina propria is replete with Type II NKT cells responsive to lyso-sulfatide glycolipid and bearing IL-13Rα2. Since lyso-sulfatide is a self-antigen, these data suggest that an autoimmune response is involved in UC pathogenesis. Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://group.bmj.com/group/rights-licensing/permissions.

Entities:  

Keywords:  Cytokines; Inflammatory Bowel Disease; Intestinal T Cells; Ulcerative Colitis

Mesh:

Substances:

Year:  2014        PMID: 24515806      PMCID: PMC4782805          DOI: 10.1136/gutjnl-2013-305671

Source DB:  PubMed          Journal:  Gut        ISSN: 0017-5749            Impact factor:   23.059


  21 in total

1.  Oxazolone colitis, a Th2 colitis model resembling ulcerative colitis, is mediated by IL-13-producing NK-T cells.

Authors:  Frank Heller; Ivan J Fuss; Edward E Nieuwenhuis; Richard S Blumberg; Warren Strober
Journal:  Immunity       Date:  2002-11       Impact factor: 31.745

2.  Microbial exposure during early life has persistent effects on natural killer T cell function.

Authors:  Torsten Olszak; Dingding An; Sebastian Zeissig; Miguel Pinilla Vera; Julia Richter; Andre Franke; Jonathan N Glickman; Reiner Siebert; Rebecca M Baron; Dennis L Kasper; Richard S Blumberg
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3.  Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5.

Authors:  I J Fuss; M Neurath; M Boirivant; J S Klein; C de la Motte; S A Strong; C Fiocchi; W Strober
Journal:  J Immunol       Date:  1996-08-01       Impact factor: 5.422

4.  IL-13 signaling via IL-13R alpha2 induces major downstream fibrogenic factors mediating fibrosis in chronic TNBS colitis.

Authors:  Stefan Fichtner-Feigl; Cheryl A Young; Atsushi Kitani; Edward K Geissler; Hans-Jürgen Schlitt; Warren Strober
Journal:  Gastroenterology       Date:  2008-09-11       Impact factor: 22.682

5.  Multiple tissue-specific isoforms of sulfatide activate CD1d-restricted type II NKT cells.

Authors:  Maria Blomqvist; Sara Rhost; Susann Teneberg; Linda Löfbom; Thomas Osterbye; Manfred Brigl; Jan-Eric Månsson; Susanna L Cardell
Journal:  Eur J Immunol       Date:  2009-07       Impact factor: 5.532

6.  Presentation of the same glycolipid by different CD1 molecules.

Authors:  A Shamshiev; H-J Gober; A Donda; Z Mazorra; L Mori; G De Libero
Journal:  J Exp Med       Date:  2002-04-15       Impact factor: 14.307

7.  Sulfatide recognition by colonization factor antigen CS6 from enterotoxigenic Escherichia coli.

Authors:  Lena Jansson; Joshua Tobias; Catharina Jarefjäll; Michael Lebens; Ann-Mari Svennerholm; Susann Teneberg
Journal:  PLoS One       Date:  2009-02-16       Impact factor: 3.240

8.  Interleukin 13 mediates signal transduction through interleukin 13 receptor alpha2 in pancreatic ductal adenocarcinoma: role of IL-13 Pseudomonas exotoxin in pancreatic cancer therapy.

Authors:  Takeshi Shimamura; Toshio Fujisawa; Syed R Husain; Bharat Joshi; Raj K Puri
Journal:  Clin Cancer Res       Date:  2010-01-12       Impact factor: 13.801

9.  Prevention of autoimmunity by targeting a distinct, noninvariant CD1d-reactive T cell population reactive to sulfatide.

Authors:  Alex Jahng; Igor Maricic; Carlos Aguilera; Susanna Cardell; Ramesh C Halder; Vipin Kumar
Journal:  J Exp Med       Date:  2004-03-29       Impact factor: 14.307

10.  Receptor for interleukin (IL) 13 does not interact with IL4 but receptor for IL4 interacts with IL13 on human glioma cells.

Authors:  W Debinski; R Miner; P Leland; N I Obiri; R K Puri
Journal:  J Biol Chem       Date:  1996-09-13       Impact factor: 5.486

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Authors:  Heitor S P de Souza; Claudio Fiocchi
Journal:  Nat Rev Gastroenterol Hepatol       Date:  2015-12-02       Impact factor: 46.802

3.  Gene polymorphism linked to increased asthma and IBD risk alters gasdermin-B structure, a sulfatide and phosphoinositide binding protein.

Authors:  Kinlin L Chao; Liudmila Kulakova; Osnat Herzberg
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4.  Natural killer cell subsets in cerebrospinal fluid of patients with multiple sclerosis.

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Review 5.  Type II NKT cells: a distinct CD1d-restricted immune regulatory NKT cell subset.

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Review 6.  What rheumatologists need to know about innate lymphocytes.

Authors:  Mark A Exley; George C Tsokos; Kingston H G Mills; Dirk Elewaut; Ben Mulhearn
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Review 7.  Old and New Lymphocyte Players in Inflammatory Bowel Disease.

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Journal:  Dig Dis Sci       Date:  2017-12-23       Impact factor: 3.199

8.  Mucosal Expression of Type 2 and Type 17 Immune Response Genes Distinguishes Ulcerative Colitis From Colon-Only Crohn's Disease in Treatment-Naive Pediatric Patients.

Authors:  Michael J Rosen; Rebekah Karns; Jefferson E Vallance; Ramona Bezold; Amanda Waddell; Margaret H Collins; Yael Haberman; Phillip Minar; Robert N Baldassano; Jeffrey S Hyams; Susan S Baker; Richard Kellermayer; Joshua D Noe; Anne M Griffiths; Joel R Rosh; Wallace V Crandall; Melvin B Heyman; David R Mack; Michael D Kappelman; James Markowitz; Dedrick E Moulton; Neal S Leleiko; Thomas D Walters; Subra Kugathasan; Keith T Wilson; Simon P Hogan; Lee A Denson
Journal:  Gastroenterology       Date:  2017-01-26       Impact factor: 22.682

Review 9.  Roles of galactose 3'-O- sulfation in signaling.

Authors:  Rong Wang; Xing Zhong Wu
Journal:  Glycoconj J       Date:  2014-10-08       Impact factor: 2.916

10.  IL-13 receptor α2 stimulates human glioma cell growth and metastasis through the Src/PI3K/Akt/mTOR signaling pathway.

Authors:  Ming Tu; Wei Wange; Lin Cai; Penglei Zhu; Zhichao Gao; Weiming Zheng
Journal:  Tumour Biol       Date:  2016-09-14
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