Ubiquitin D is Upregulated by Synergy of Notch Signalling and TNF-α in the Inflamed Intestinal Epithelia of IBD Patients.


Journal

Journal of Crohn's & colitis
ISSN: 1876-4479
Titre abrégé: J Crohns Colitis
Pays: England
ID NLM: 101318676

Informations de publication

Date de publication:
30 Mar 2019
Historique:
pubmed: 6 11 2018
medline: 6 8 2019
entrez: 6 11 2018
Statut: ppublish

Résumé

The intestinal epithelium of inflammatory bowel disease [IBD] patients is exposed to various pro-inflammatory cytokines, most notably tumour necrosis factor alpha [TNF-α]. We have previously shown that the Notch signalling pathway is also upregulated in such an epithelium, contributing to intestinal epithelial cell [IEC] proliferation and regeneration. We aimed to reproduce such environment in vitro and explore the gene regulation involved. Human IEC cell lines or patient-derived organoids were used to analyse Notch- and TNF-α-dependent gene expression. Immunohistochemistry was performed to analyse expression of ubiquitin D [UBD] in various patient-derived intestinal tissues. In human IEC cell lines, we found that Notch signalling and TNF-α-induced NFκB signalling are reciprocally regulated to promote expression of a specific gene subset. Global gene expression analysis identified UBD to be one of the most highly upregulated genes, due to synergy of Notch and TNF-α. The synergistic expression of UBD was regulated at the transcriptional level, whereas the UBD protein had an extremely short half-life due to post-translational, proteasomal degradation. In uninflamed intestinal tissues from IBD patients, UBD expression was limited to IECs residing at the crypt bottom. In contrast, UBD-expressing IECs were seen throughout the crypt in inflamed tissues, indicating substantial induction by the local inflammatory environment. Analysis using patient-derived organoids consistently confirmed conserved Notch- and TNF-α-dependent expression of UBD. Notably, post-infliximab [IFX] downregulation of UBD reflected favourable outcome in IBD patients. We propose that UBD is a novel inflammatory-phase protein expressed in IECs, with a highly rapid responsiveness to anti-TNF-α treatment.

Sections du résumé

BACKGROUND AND AIMS OBJECTIVE
The intestinal epithelium of inflammatory bowel disease [IBD] patients is exposed to various pro-inflammatory cytokines, most notably tumour necrosis factor alpha [TNF-α]. We have previously shown that the Notch signalling pathway is also upregulated in such an epithelium, contributing to intestinal epithelial cell [IEC] proliferation and regeneration. We aimed to reproduce such environment in vitro and explore the gene regulation involved.
METHODS METHODS
Human IEC cell lines or patient-derived organoids were used to analyse Notch- and TNF-α-dependent gene expression. Immunohistochemistry was performed to analyse expression of ubiquitin D [UBD] in various patient-derived intestinal tissues.
RESULTS RESULTS
In human IEC cell lines, we found that Notch signalling and TNF-α-induced NFκB signalling are reciprocally regulated to promote expression of a specific gene subset. Global gene expression analysis identified UBD to be one of the most highly upregulated genes, due to synergy of Notch and TNF-α. The synergistic expression of UBD was regulated at the transcriptional level, whereas the UBD protein had an extremely short half-life due to post-translational, proteasomal degradation. In uninflamed intestinal tissues from IBD patients, UBD expression was limited to IECs residing at the crypt bottom. In contrast, UBD-expressing IECs were seen throughout the crypt in inflamed tissues, indicating substantial induction by the local inflammatory environment. Analysis using patient-derived organoids consistently confirmed conserved Notch- and TNF-α-dependent expression of UBD. Notably, post-infliximab [IFX] downregulation of UBD reflected favourable outcome in IBD patients.
CONCLUSION CONCLUSIONS
We propose that UBD is a novel inflammatory-phase protein expressed in IECs, with a highly rapid responsiveness to anti-TNF-α treatment.

Identifiants

pubmed: 30395194
pii: 5160030
doi: 10.1093/ecco-jcc/jjy180
doi:

Substances chimiques

Anti-Bacterial Agents 0
Gastrointestinal Agents 0
NF-kappa B 0
Receptors, Notch 0
Tumor Necrosis Factor-alpha 0
UBD protein, human 0
Ubiquitins 0
Infliximab B72HH48FLU
Doxycycline N12000U13O

Types de publication

Journal Article

Langues

eng

Pagination

495-509

Informations de copyright

Copyright © 2018 European Crohn’s and Colitis Organisation (ECCO). Published by Oxford University Press. All rights reserved. For permissions, please email: journals.permissions@oup.com.

Auteurs

Ami Kawamoto (A)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Sayaka Nagata (S)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Sho Anzai (S)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Junichi Takahashi (J)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Mao Kawai (M)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Minami Hama (M)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Daichi Nogawa (D)

Department of Comprehensive Pathology, Tokyo Medical and Dental University, Tokyo, Japan.

Kouhei Yamamoto (K)

Department of Comprehensive Pathology, Tokyo Medical and Dental University, Tokyo, Japan.

Reiko Kuno (R)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Kohei Suzuki (K)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Hiromichi Shimizu (H)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Yui Hiraguri (Y)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Shiro Yui (S)

Center for Stem Cell and Regenerative Medicine, Tokyo Medical and Dental University, Tokyo, Japan.

Shigeru Oshima (S)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Kiichiro Tsuchiya (K)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Tetsuya Nakamura (T)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.
Department of Advanced Therapeutics in GI Diseases, Tokyo Medical and Dental University, Tokyo, Japan.

Kazuo Ohtsuka (K)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Masanobu Kitagawa (M)

Department of Comprehensive Pathology, Tokyo Medical and Dental University, Tokyo, Japan.

Ryuichi Okamoto (R)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.
Center for Stem Cell and Regenerative Medicine, Tokyo Medical and Dental University, Tokyo, Japan.

Mamoru Watanabe (M)

Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH