Arrestin domain containing 3 promotes Helicobacter pylori-associated gastritis by regulating protease-activated receptor 1.


Journal

JCI insight
ISSN: 2379-3708
Titre abrégé: JCI Insight
Pays: United States
ID NLM: 101676073

Informations de publication

Date de publication:
06 08 2020
Historique:
received: 18 12 2019
accepted: 01 07 2020
pubmed: 8 7 2020
medline: 1 6 2021
entrez: 8 7 2020
Statut: epublish

Résumé

Arrestin domain containing 3 (ARRDC3) represents a newly discovered α-arrestin involved in obesity, inflammation, and cancer. Here, we demonstrate a proinflammation role of ARRDC3 in Helicobacter pylori-associated gastritis. Increased ARRDC3 was detected in gastric mucosa of patients and mice infected with H. pylori. ARRDC3 in gastric epithelial cells (GECs) was induced by H. pylori, regulated by ERK and PI3K-AKT pathways in a cagA-dependent manner. Human gastric ARRDC3 correlated with the severity of gastritis, and mouse ARRDC3 from non-BM-derived cells promoted gastric inflammation. This inflammation was characterized by the CXCR2-dependent influx of CD45+CD11b+Ly6C-Ly6G+ neutrophils, whose migration was induced via the ARRDC3-dependent production of CXCL2 by GECs. Importantly, gastric inflammation was attenuated in Arrdc3-/- mice but increased in protease-activated receptor 1-/- (Par1-/-) mice. Mechanistically, ARRDC3 in GECs directly interacted with PAR1 and negatively regulated PAR1 via ARRDC3-mediated lysosomal degradation, which abrogated the suppression of CXCL2 production and following neutrophil chemotaxis by PAR1, thereby contributing to the development of H. pylori-associated gastritis. This study identifies a regulatory network involving H. pylori, GECs, ARRDC3, PAR1, and neutrophils, which collectively exert a proinflammatory effect within the gastric microenvironment. Efforts to inhibit this ARRDC3-dependent pathway may provide valuable strategies in treating of H. pylori-associated gastritis.

Identifiants

pubmed: 32634127
pii: 135849
doi: 10.1172/jci.insight.135849
pmc: PMC7455081
doi:
pii:

Substances chimiques

ARRDC3 protein, human 0
ARRDC3 protein, mouse 0
Arrestins 0
Receptor, PAR-1 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Références

Cell Metab. 2011 Nov 2;14(5):671-83
pubmed: 21982743
Oncotarget. 2014 Jul 30;5(14):5798-807
pubmed: 25015565
Am J Respir Cell Mol Biol. 2010 Sep;43(3):269-75
pubmed: 19805483
Mol Immunol. 2011 Oct;49(1-2):64-74
pubmed: 21855149
Infect Immun. 2013 Aug;81(8):3035-44
pubmed: 23753627
Infect Immun. 2014 Jul;82(7):2881-9
pubmed: 24778119
FASEB J. 2004 Jan;18(1):218-20
pubmed: 14597566
Proc Natl Acad Sci U S A. 2011 Dec 13;108(50):E1372-80
pubmed: 22106258
Gastroenterology. 2017 Aug;153(2):420-429
pubmed: 28456631
Mucosal Immunol. 2015 May;8(3):683-95
pubmed: 25354317
Front Pharmacol. 2018 Nov 22;9:1347
pubmed: 30524287
Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14428-33
pubmed: 12391297
Am J Pathol. 2014 Aug;184(8):2297-309
pubmed: 24946011
Immunology. 2013 Dec;140(4):430-40
pubmed: 23859136
Curr Mol Med. 2017;17(3):221-229
pubmed: 28782483
Mol Biol Cell. 2015 Dec 15;26(25):4660-73
pubmed: 26490116
Gut. 2015 Sep;64(9):1368-78
pubmed: 25134787
Nat Immunol. 2010 Feb;11(2):136-40
pubmed: 20023662
Gastroenterology. 2016 Jan;150(1):64-78
pubmed: 26385073
Sci Rep. 2015 Dec 07;5:18117
pubmed: 26640170
N Engl J Med. 2010 Apr 29;362(17):1597-604
pubmed: 20427808
Mucosal Immunol. 2015 Jan;8(1):68-79
pubmed: 24866378
Sci Adv. 2019 Apr 03;5(4):eaau6547
pubmed: 30949574
J Biol Chem. 2018 Mar 2;293(9):3350-3362
pubmed: 29348172
EMBO Rep. 2010 Aug;11(8):605-11
pubmed: 20559325
Endocrinology. 2006 Feb;147(2):733-43
pubmed: 16269462
Infect Immun. 2008 Feb;76(2):551-61
pubmed: 18070899
Nat Immunol. 2008 Sep;9(9):970-80
pubmed: 18711434
PLoS Genet. 2010 Aug 19;6(8):e1001069
pubmed: 20808891
Science. 2000 Feb 25;287(5457):1497-500
pubmed: 10688800
Cell Death Dis. 2018 Apr 25;9(5):457
pubmed: 29691371
World J Gastroenterol. 2012 Sep 28;18(36):5101-5
pubmed: 23049221
Oncogene. 2010 Sep 9;29(36):5032-47
pubmed: 20603614
J Biol Chem. 2016 Jul 8;291(28):14510-25
pubmed: 27226565
J Pathol. 2015 Sep;237(1):85-97
pubmed: 25950520
Gastroenterology. 2010 Feb;138(2):573-82
pubmed: 19706295

Auteurs

Yu-Gang Liu (YG)

National Engineering Research Center of Immunological Products, Department of Microbiology and Biochemical Pharmacy, College of Pharmacy and Laboratory Medicine, Third Military Medical University, Chongqing, China.
Department of Clinical Laboratory, the General Hospital of Western Theater Command, Chengdu, Sichuan, China.

Yong-Sheng Teng (YS)

National Engineering Research Center of Immunological Products, Department of Microbiology and Biochemical Pharmacy, College of Pharmacy and Laboratory Medicine, Third Military Medical University, Chongqing, China.

Zhi-Guo Shan (ZG)

Department of General Surgery and Center of Minimal Invasive Gastrointestinal Surgery, Southwest Hospital, and.

Ping Cheng (P)

National Engineering Research Center of Immunological Products, Department of Microbiology and Biochemical Pharmacy, College of Pharmacy and Laboratory Medicine, Third Military Medical University, Chongqing, China.

Chuan-Jie Hao (CJ)

National Engineering Research Center of Immunological Products, Department of Microbiology and Biochemical Pharmacy, College of Pharmacy and Laboratory Medicine, Third Military Medical University, Chongqing, China.

Yi-Pin Lv (YP)

National Engineering Research Center of Immunological Products, Department of Microbiology and Biochemical Pharmacy, College of Pharmacy and Laboratory Medicine, Third Military Medical University, Chongqing, China.

Fang-Yuan Mao (FY)

National Engineering Research Center of Immunological Products, Department of Microbiology and Biochemical Pharmacy, College of Pharmacy and Laboratory Medicine, Third Military Medical University, Chongqing, China.

Shi-Ming Yang (SM)

Department of Gastroenterology, XinQiao Hospital, Third Military Medical University, Chongqing, China.

Weisan Chen (W)

La Trobe Institute of Molecular Science, La Trobe University, Bundoora, Victoria, Australia.

Yong-Liang Zhao (YL)

Department of General Surgery and Center of Minimal Invasive Gastrointestinal Surgery, Southwest Hospital, and.

Nan You (N)

Department of Hepatobiliary Surgery, XinQiao Hospital, Third Military Medical University, Chongqing, China.

Quan-Ming Zou (QM)

National Engineering Research Center of Immunological Products, Department of Microbiology and Biochemical Pharmacy, College of Pharmacy and Laboratory Medicine, Third Military Medical University, Chongqing, China.

Yuan Zhuang (Y)

National Engineering Research Center of Immunological Products, Department of Microbiology and Biochemical Pharmacy, College of Pharmacy and Laboratory Medicine, Third Military Medical University, Chongqing, China.

Articles similaires

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
Humans Meals Time Factors Female Adult

Classifications MeSH