TNF Receptor 1 Promotes Early-Life Immunity and Protects Against Colitis in Mice

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2020 Oct 21

PMID 33086075

Citations 11

Authors

Cambrian Y Liu

Sharon S Tam

Ying Huang

Philip E Dube

Rabea Alhosh

Nandini Girish

Shivesh Punit

Shirin Nataneli

Fan Li

Jeffrey M Bender

M Kay Washington

D Brent Polk

Affiliations

Soon will be listed here.

Abstract

Neutralization of tumor necrosis factor (TNF) represents a widely used therapeutic strategy for autoimmune diseases including inflammatory bowel disease (IBD). However, the fact that many patients with IBD are non-responsive to anti-TNF therapies suggests the need for a better understanding of TNF signaling in IBD. Here, we show that co-deletion of TNF receptor 1 (TNFR1, Tnfrsf1a) in the Il10 spontaneous colitis model exacerbates disease, resulting in very-early-onset inflammation after weaning. The disease can be interrupted by treatment with antibiotics. The single deletion of TNFR1 induces subclinical colonic epithelial dysfunction and mucosal immune abnormalities, including accumulation of neutrophils and depletion of B cells. During the pre-disease period (before weaning), both Tnfr1 and Il10Tnfr1 animals exhibit impaired expression of pro-inflammatory cytokines compared with wild-type and Il10 controls, respectively. Collectively, these results demonstrate the net anti-inflammatory functions of TNF/TNFR1 signaling through the regulation of colonic immune homeostasis in early life.

Citing Articles

PepT1-targeted nanodrug based on co-assembly of anti-inflammatory peptide and immunosuppressant for combined treatment of acute and chronic DSS-induced ColitiS.

Zhang D, Jiang L, Yu F, Yan P, Liu Y, Wu Y Front Pharmacol. 2024; 15:1442876.

PMID: 39211778 PMC: 11357942. DOI: 10.3389/fphar.2024.1442876.

Adipokines-A Cohort Prospective Study in Children with Severe Burns.

Badoiu S, Enescu D, Tatar R, Miricescu D, Stanescu-Spinu I, Greabu M Int J Mol Sci. 2024; 25(14).

PMID: 39062875 PMC: 11277113. DOI: 10.3390/ijms25147630.

Colitis-induced upregulation of tumor necrosis factor receptor-2 (TNFR2) terminates epithelial regenerative signaling to restore homeostasis.

Sharifkhodaei Z, Liu C, Girish N, Huang Y, Punit S, Washington M iScience. 2023; 26(10):107829.

PMID: 37736049 PMC: 10510063. DOI: 10.1016/j.isci.2023.107829.

Wound-healing plasticity enables clonal expansion of founder progenitor cells in colitis.

Liu C, Girish N, Gomez M, Kalski M, Bernard J, Simons B Dev Cell. 2023; 58(21):2309-2325.e7.

PMID: 37652012 PMC: 10872951. DOI: 10.1016/j.devcel.2023.08.011.

Deletion of Endogenous Neuregulin-4 Limits Adaptive Immunity During Interleukin-10 Receptor-Neutralizing Colitis.

Bernard J, Bucar E, Liu C, Katada K, Washington M, Schumacher M Inflamm Bowel Dis. 2023; 29(11):1778-1792.

PMID: 37265326 PMC: 10628918. DOI: 10.1093/ibd/izad092.

References

McGovern D, Kugathasan S, Cho J . Genetics of Inflammatory Bowel Diseases. Gastroenterology. 2015; 149(5):1163-1176.e2. PMC: 4915781. DOI: 10.1053/j.gastro.2015.08.001. View

Salzer E, Kansu A, Sic H, Majek P, Ikinciogullari A, Dogu F . Early-onset inflammatory bowel disease and common variable immunodeficiency-like disease caused by IL-21 deficiency. J Allergy Clin Immunol. 2014; 133(6):1651-9.e12. DOI: 10.1016/j.jaci.2014.02.034. View

Wang K, Han G, Dou Y, Wang Y, Liu G, Wang R . Opposite role of tumor necrosis factor receptors in dextran sulfate sodium-induced colitis in mice. PLoS One. 2013; 7(12):e52924. PMC: 3532169. DOI: 10.1371/journal.pone.0052924. View

Korzenik J, Larsen M, Nielsen J, Kjeldsen J, Norgard B . Increased risk of developing Crohn's disease or ulcerative colitis in 17 018 patients while under treatment with anti-TNFα agents, particularly etanercept, for autoimmune diseases other than inflammatory bowel disease. Aliment Pharmacol Ther. 2019; 50(3):289-294. DOI: 10.1111/apt.15370. View

Bianco A, Girardelli M, Tommasini A . Genetics of inflammatory bowel disease from multifactorial to monogenic forms. World J Gastroenterol. 2015; 21(43):12296-310. PMC: 4649114. DOI: 10.3748/wjg.v21.i43.12296. View

Scheer S, Medina T, Murison A, Taves M, Antignano F, Chenery A . Early-life antibiotic treatment enhances the pathogenicity of CD4 T cells during intestinal inflammation. J Leukoc Biol. 2016; 101(4):893-900. DOI: 10.1189/jlb.3MA0716-334RR. View

Singh V, Kumar M, Yeoh B, Xiao X, Saha P, Kennett M . Inhibition of Interleukin-10 Signaling Induces Microbiota-dependent Chronic Colitis in Apolipoprotein E Deficient Mice. Inflamm Bowel Dis. 2016; 22(4):841-52. PMC: 4792726. DOI: 10.1097/MIB.0000000000000699. View

Farmer M, Sundberg J, Bristol I, Churchill G, Li R, Elson C . A major quantitative trait locus on chromosome 3 controls colitis severity in IL-10-deficient mice. Proc Natl Acad Sci U S A. 2001; 98(24):13820-5. PMC: 61125. DOI: 10.1073/pnas.241258698. View

Redhu N, Bakthavatchalu V, Conaway E, Shouval D, Tsou A, Goettel J . Macrophage dysfunction initiates colitis during weaning of infant mice lacking the interleukin-10 receptor. Elife. 2017; 6. PMC: 5531923. DOI: 10.7554/eLife.27652. View

10.

Liu C, Xiao C, Fraser S, Lester H, Koos D . Electrophysiological characterization of Grueneberg ganglion olfactory neurons: spontaneous firing, sodium conductance, and hyperpolarization-activated currents. J Neurophysiol. 2012; 108(5):1318-34. PMC: 3544954. DOI: 10.1152/jn.00907.2011. View

11.

Murch S, Lamkin V, Savage M, Walker-Smith J, MacDonald T . Serum concentrations of tumour necrosis factor alpha in childhood chronic inflammatory bowel disease. Gut. 1991; 32(8):913-7. PMC: 1378961. DOI: 10.1136/gut.32.8.913. View

12.

Ebach D, Newberry R, Stenson W . Differential role of tumor necrosis factor receptors in TNBS colitis. Inflamm Bowel Dis. 2005; 11(6):533-40. DOI: 10.1097/01.mib.0000163698.34592.30. View

13.

Grasberger H, Gao J, Nagao-Kitamoto H, Kitamoto S, Zhang M, Kamada N . Increased Expression of DUOX2 Is an Epithelial Response to Mucosal Dysbiosis Required for Immune Homeostasis in Mouse Intestine. Gastroenterology. 2015; 149(7):1849-59. PMC: 4663159. DOI: 10.1053/j.gastro.2015.07.062. View

14.

Pierik M, Vermeire S, Steen K, Joossens S, Claessens G, Vlietinck R . Tumour necrosis factor-alpha receptor 1 and 2 polymorphisms in inflammatory bowel disease and their association with response to infliximab. Aliment Pharmacol Ther. 2004; 20(3):303-10. DOI: 10.1111/j.1365-2036.2004.01946.x. View

15.

Jostins L, Ripke S, Weersma R, Duerr R, McGovern D, Hui K . Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012; 491(7422):119-24. PMC: 3491803. DOI: 10.1038/nature11582. View

16.

Punit S, Dube P, Liu C, Girish N, Washington M, Polk D . Tumor Necrosis Factor Receptor 2 Restricts the Pathogenicity of CD8(+) T Cells in Mice With Colitis. Gastroenterology. 2015; 149(4):993-1005.e2. PMC: 4841683. DOI: 10.1053/j.gastro.2015.06.004. View

17.

Al Nabhani Z, Dulauroy S, Marques R, Cousu C, Al Bounny S, Dejardin F . A Weaning Reaction to Microbiota Is Required for Resistance to Immunopathologies in the Adult. Immunity. 2019; 50(5):1276-1288.e5. DOI: 10.1016/j.immuni.2019.02.014. View

18.

Kullberg M, Jankovic D, Feng C, Hue S, Gorelick P, McKenzie B . IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J Exp Med. 2006; 203(11):2485-94. PMC: 2118119. DOI: 10.1084/jem.20061082. View

19.

Walthall K, Cappon G, Hurtt M, Zoetis T . Postnatal development of the gastrointestinal system: a species comparison. Birth Defects Res B Dev Reprod Toxicol. 2005; 74(2):132-56. DOI: 10.1002/bdrb.20040. View

20.

Dube P, Punit S, Polk D . Redeeming an old foe: protective as well as pathophysiological roles for tumor necrosis factor in inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol. 2014; 308(3):G161-70. PMC: 4312954. DOI: 10.1152/ajpgi.00142.2014. View