Literature DB >> 20347817

Hypoxia-inducible factor signaling provides protection in Clostridium difficile-induced intestinal injury.

Simon A Hirota1, Kyla Fines, Jeffrey Ng, Danya Traboulsi, Josh Lee, Eikichi Ihara, Yan Li, William G Willmore, Daniel Chung, Melanie M Scully, Thomas Louie, Shaun Medlicott, Manigandan Lejeune, Kris Chadee, Glen Armstrong, Sean P Colgan, Daniel A Muruve, Justin A MacDonald, Paul L Beck.   

Abstract

BACKGROUND & AIMS: Clostridium difficile is the leading cause of nosocomial infectious diarrhea. Antibiotic resistance and increased virulence of strains have increased the number of C difficile-related deaths worldwide. The innate host response mechanisms to C difficile are not resolved; we propose that hypoxia-inducible factor (HIF-1) has an innate, protective role in C difficile colitis. We studied the impact of C difficile toxins on the regulation of HIF-1 and evaluated the role of HIF-1alpha in C difficile-mediated injury/inflammation.
METHODS: We assessed HIF-1alpha mRNA and protein levels and DNA binding in human mucosal biopsy samples and Caco-2 cells following exposure to C difficile toxins. We used the mouse ileal loop model of C difficile toxin-induced intestinal injury. Mice with targeted deletion of HIF-1alpha in the intestinal epithelium were used to assess the effects of HIF-1alpha signaling in response to C difficile toxin.
RESULTS: Mucosal biopsy specimens and Caco-2 cells exposed to C difficile toxin had a significant increase in HIF-1alpha transcription and protein levels. Toxin-induced DNA binding was also observed in Caco-2 cells. Toxin-induced HIF-1alpha accumulation was attenuated by nitric oxide synthase inhibitors. In vivo deletion of intestinal epithelial HIF-1alpha resulted in more severe, toxin-induced intestinal injury and inflammation. In contrast, stabilization of HIF-1alpha with dimethyloxallyl glycine attenuated toxin-induced injury and inflammation. This was associated with induction of HIF-1-regulated protective factors (such as vascular endothelial growth factor-alpha, CD73, and intestinal trefoil factor) and down-regulation of proinflammatory molecules such as tumor necrosis factor and Cxcl1.
CONCLUSIONS: HIF-1alpha protects the intestinal mucosa from C difficile toxins. The innate protective actions of HIF-1alpha in response to C difficile toxins be developed as therapeutics for C difficile-associated disease. Copyright 2010 AGA Institute. Published by Elsevier Inc. All rights reserved.

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Year:  2010        PMID: 20347817      PMCID: PMC3063899          DOI: 10.1053/j.gastro.2010.03.045

Source DB:  PubMed          Journal:  Gastroenterology        ISSN: 0016-5085            Impact factor:   22.682


  30 in total

1.  Role of tumor necrosis factor and nitric oxide in the cytotoxic effects of Clostridium difficile toxin A and toxin B on macrophages.

Authors:  A A Melo Filho; M H Souza; D M Lyerly; F Q Cunha; A A Lima; R A Ribeiro
Journal:  Toxicon       Date:  1997-05       Impact factor: 3.033

2.  Purification and characterization of toxins A and B of Clostridium difficile.

Authors:  N M Sullivan; S Pellett; T D Wilkins
Journal:  Infect Immun       Date:  1982-03       Impact factor: 3.441

3.  Stimulation of HIF-1alpha, HIF-2alpha, and VEGF by prolyl 4-hydroxylase inhibition in human lung endothelial and epithelial cells.

Authors:  Tiina M Asikainen; Aftab Ahmad; Barbara K Schneider; Wen-Bin Ho; Michael Arend; Mitchell Brenner; Volkmar Günzler; Carl W White
Journal:  Free Radic Biol Med       Date:  2005-04-15       Impact factor: 7.376

4.  Dextran sulfate sodium-induced colonic histopathology, but not altered epithelial ion transport, is reduced by inhibition of phosphodiesterase activity.

Authors:  N Diaz-Granados; K Howe; J Lu; D M McKay
Journal:  Am J Pathol       Date:  2000-06       Impact factor: 4.307

5.  Effect of Clostridium difficile toxin A on human intestinal epithelial cells: induction of interleukin 8 production and apoptosis after cell detachment.

Authors:  Y R Mahida; S Makh; S Hyde; T Gray; S P Borriello
Journal:  Gut       Date:  1996-03       Impact factor: 23.059

6.  IL-8 release and neutrophil activation by Clostridium difficile toxin-exposed human monocytes.

Authors:  J K Linevsky; C Pothoulakis; S Keates; M Warny; A C Keates; J T Lamont; C P Kelly
Journal:  Am J Physiol       Date:  1997-12

7.  Clostridium difficile toxins disrupt epithelial barrier function by altering membrane microdomain localization of tight junction proteins.

Authors:  A Nusrat; C von Eichel-Streiber; J R Turner; P Verkade; J L Madara; C A Parkos
Journal:  Infect Immun       Date:  2001-03       Impact factor: 3.441

8.  Clostridium difficile toxin B disrupts the barrier function of T84 monolayers.

Authors:  G Hecht; A Koutsouris; C Pothoulakis; J T LaMont; J L Madara
Journal:  Gastroenterology       Date:  1992-02       Impact factor: 22.682

9.  Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia.

Authors:  G T Furuta; J R Turner; C T Taylor; R M Hershberg; K Comerford; S Narravula; D K Podolsky; S P Colgan
Journal:  J Exp Med       Date:  2001-05-07       Impact factor: 14.307

10.  Toxin B is essential for virulence of Clostridium difficile.

Authors:  Dena Lyras; Jennifer R O'Connor; Pauline M Howarth; Susan P Sambol; Glen P Carter; Tongted Phumoonna; Rachael Poon; Vicki Adams; Gayatri Vedantam; Stuart Johnson; Dale N Gerding; Julian I Rood
Journal:  Nature       Date:  2009-03-01       Impact factor: 49.962

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  38 in total

1.  Clostridium difficile toxins induce VEGF-A and vascular permeability to promote disease pathogenesis.

Authors:  Jun Huang; Ciarán P Kelly; Kyriaki Bakirtzi; Javier A Villafuerte Gálvez; Dena Lyras; Steven J Mileto; Sarah Larcombe; Hua Xu; Xiaotong Yang; Kelsey S Shields; Weishu Zhu; Yi Zhang; Jeffrey D Goldsmith; Ishan J Patel; Joshua Hansen; Meijin Huang; Seppo Yla-Herttuala; Alan C Moss; Daniel Paredes-Sabja; Charalabos Pothoulakis; Yatrik M Shah; Jianping Wang; Xinhua Chen
Journal:  Nat Microbiol       Date:  2018-12-03       Impact factor: 17.745

Review 2.  Interactions between nitric oxide and hypoxia-inducible factor signaling pathways in inflammatory disease.

Authors:  Nels Olson; Albert van der Vliet
Journal:  Nitric Oxide       Date:  2011-01-01       Impact factor: 4.427

Review 3.  Hypoxia-inducible factors in physiology and medicine.

Authors:  Gregg L Semenza
Journal:  Cell       Date:  2012-02-03       Impact factor: 41.582

4.  Metabolic regulation of intestinal epithelial barrier during inflammation.

Authors:  Sean P Colgan; Valerie F Curtis; Jordi M Lanis; Louise E Glover
Journal:  Tissue Barriers       Date:  2015-04-03

5.  Hypoxia-inducible factor plays a gut-injurious role in intestinal ischemia reperfusion injury.

Authors:  Kolenkode B Kannan; Iriana Colorado; Diego Reino; David Palange; Qi Lu; Xiaofa Qin; Billy Abungu; Anthony Watkins; Francis J Caputo; Da-Zhong Xu; Gregg L Semenza; Edwin A Deitch; Rena Feinman
Journal:  Am J Physiol Gastrointest Liver Physiol       Date:  2010-12-23       Impact factor: 4.052

6.  Current Status of Nonantibiotic and Adjunct Therapies for Clostridium difficile Infection.

Authors:  Nuntra Suwantarat; David A Bobak
Journal:  Curr Infect Dis Rep       Date:  2011-02       Impact factor: 3.725

Review 7.  Oxygen metabolism and barrier regulation in the intestinal mucosa.

Authors:  Louise E Glover; J Scott Lee; Sean P Colgan
Journal:  J Clin Invest       Date:  2016-08-08       Impact factor: 14.808

Review 8.  Hypoxia-sensitive pathways in intestinal inflammation.

Authors:  Eric Brown; Cormac T Taylor
Journal:  J Physiol       Date:  2017-11-28       Impact factor: 5.182

Review 9.  Intestinal hypoxia and hypoxia-induced signalling as therapeutic targets for IBD.

Authors:  Sophie Van Welden; Andrew C Selfridge; Pieter Hindryckx
Journal:  Nat Rev Gastroenterol Hepatol       Date:  2017-08-30       Impact factor: 46.802

Review 10.  Hypoxia-dependent regulation of inflammatory pathways in immune cells.

Authors:  Cormac T Taylor; Glen Doherty; Padraic G Fallon; Eoin P Cummins
Journal:  J Clin Invest       Date:  2016-07-25       Impact factor: 14.808

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