Dietary iron enhances colonic inflammation and IL-6/IL-11-Stat3 signaling promoting colonic tumor development in mice
Chronic intestinal inflammation and high dietary iron are associated with colorectal cancer development. The role of Stat3 activation in iron-induced colonic inflammation and tumorigenesis was investigated in a mouse model of inflammation-associated colorectal cancer. Mice, fed either an iron-supple...
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Published in | PloS one Vol. 8; no. 11; p. e78850 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Public Library of Science
06.11.2013
Public Library of Science (PLoS) |
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Abstract | Chronic intestinal inflammation and high dietary iron are associated with colorectal cancer development. The role of Stat3 activation in iron-induced colonic inflammation and tumorigenesis was investigated in a mouse model of inflammation-associated colorectal cancer. Mice, fed either an iron-supplemented or control diet, were treated with azoxymethane and dextran sodium sulfate (DSS). Intestinal inflammation and tumor development were assessed by endoscopy and histology, gene expression by real-time PCR, Stat3 phosphorylation by immunoblot, cytokines by ELISA and apoptosis by TUNEL assay. Colonic inflammation was more severe in mice fed an iron-supplemented compared with a control diet one week post-DSS treatment, with enhanced colonic IL-6 and IL-11 release and Stat3 phosphorylation. Both IL-6 and ferritin, the iron storage protein, co-localized with macrophages suggesting iron may act directly on IL-6 producing-macrophages. Iron increased DSS-induced colonic epithelial cell proliferation and apoptosis consistent with enhanced mucosal damage. DSS-treated mice developed anemia that was not alleviated by dietary iron supplementation. Six weeks post-DSS treatment, iron-supplemented mice developed more and larger colonic tumors compared with control mice. Intratumoral IL-6 and IL-11 expression increased in DSS-treated mice and IL-6, and possibly IL-11, were enhanced by dietary iron. Gene expression of iron importers, divalent metal transporter 1 and transferrin receptor 1, increased and iron exporter, ferroportin, decreased in colonic tumors suggesting increased iron uptake. Dietary iron and colonic inflammation synergistically activated colonic IL-6/IL-11-Stat3 signaling promoting tumorigenesis. Oral iron therapy may be detrimental in inflammatory bowel disease since it may exacerbate colonic inflammation and increase colorectal cancer risk. |
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AbstractList | Chronic intestinal inflammation and high dietary iron are associated with colorectal cancer development. The role of Stat3 activation in iron-induced colonic inflammation and tumorigenesis was investigated in a mouse model of inflammation-associated colorectal cancer. Mice, fed either an iron-supplemented or control diet, were treated with azoxymethane and dextran sodium sulfate (DSS). Intestinal inflammation and tumor development were assessed by endoscopy and histology, gene expression by real-time PCR, Stat3 phosphorylation by immunoblot, cytokines by ELISA and apoptosis by TUNEL assay. Colonic inflammation was more severe in mice fed an iron-supplemented compared with a control diet one week post-DSS treatment, with enhanced colonic IL-6 and IL-11 release and Stat3 phosphorylation. Both IL-6 and ferritin, the iron storage protein, co-localized with macrophages suggesting iron may act directly on IL-6 producing-macrophages. Iron increased DSS-induced colonic epithelial cell proliferation and apoptosis consistent with enhanced mucosal damage. DSS-treated mice developed anemia that was not alleviated by dietary iron supplementation. Six weeks post-DSS treatment, iron-supplemented mice developed more and larger colonic tumors compared with control mice. Intratumoral IL-6 and IL-11 expression increased in DSS-treated mice and IL-6, and possibly IL-11, were enhanced by dietary iron. Gene expression of iron importers, divalent metal transporter 1 and transferrin receptor 1, increased and iron exporter, ferroportin, decreased in colonic tumors suggesting increased iron uptake. Dietary iron and colonic inflammation synergistically activated colonic IL-6/IL-11-Stat3 signaling promoting tumorigenesis. Oral iron therapy may be detrimental in inflammatory bowel disease since it may exacerbate colonic inflammation and increase colorectal cancer risk. |
Audience | Academic |
Author | Lawrance, Ian C Chua, Anita C G Ho, Desiree S Fu, S Kristine Forrest, Cynthia H Croft, Kevin D Klopcic, Borut R S Olynyk, John K Trinder, Debbie |
AuthorAffiliation | 4 Department of Histopathology, PathWest, Fremantle Hospital, Fremantle, Western Australia, Australia 8 Institute for Immunology and Infectious Diseases, Murdoch University, Murdoch, Western Australia, Australia 6 School of Medicine and Pharmacology, Royal Perth Hospital, University of Western Australia, Perth, Western Australia, Australia 9 Curtin Health Innovation Research Institute, Curtin University, Perth, Western Australia, Australia 7 Department of Gastroenterology, Fremantle Hospital, Fremantle, Western Australia, Australia 1 School of Medicine and Pharmacology, Fremantle Hospital, University of Western Australia, Fremantle, Western Australia, Australia 3 Centre for Inflammatory Bowel Diseases, Fremantle Hospital, Fremantle, Western Australia, Australia Juntendo University School of Medicine, Japan 5 School of Pathology and Laboratory Medicine, University of Western Australia, Perth, Western Australia, Australia 2 Western Australian Institute for Medical Research, Perth, Western Austral |
AuthorAffiliation_xml | – name: 8 Institute for Immunology and Infectious Diseases, Murdoch University, Murdoch, Western Australia, Australia – name: 9 Curtin Health Innovation Research Institute, Curtin University, Perth, Western Australia, Australia – name: Juntendo University School of Medicine, Japan – name: 6 School of Medicine and Pharmacology, Royal Perth Hospital, University of Western Australia, Perth, Western Australia, Australia – name: 2 Western Australian Institute for Medical Research, Perth, Western Australia, Australia – name: 3 Centre for Inflammatory Bowel Diseases, Fremantle Hospital, Fremantle, Western Australia, Australia – name: 7 Department of Gastroenterology, Fremantle Hospital, Fremantle, Western Australia, Australia – name: 4 Department of Histopathology, PathWest, Fremantle Hospital, Fremantle, Western Australia, Australia – name: 5 School of Pathology and Laboratory Medicine, University of Western Australia, Perth, Western Australia, Australia – name: 1 School of Medicine and Pharmacology, Fremantle Hospital, University of Western Australia, Fremantle, Western Australia, Australia |
Author_xml | – sequence: 1 givenname: Anita C G surname: Chua fullname: Chua, Anita C G organization: School of Medicine and Pharmacology, Fremantle Hospital, University of Western Australia, Fremantle, Western Australia, Australia ; Western Australian Institute for Medical Research, Perth, Western Australia, Australia – sequence: 2 givenname: Borut R S surname: Klopcic fullname: Klopcic, Borut R S – sequence: 3 givenname: Desiree S surname: Ho fullname: Ho, Desiree S – sequence: 4 givenname: S Kristine surname: Fu fullname: Fu, S Kristine – sequence: 5 givenname: Cynthia H surname: Forrest fullname: Forrest, Cynthia H – sequence: 6 givenname: Kevin D surname: Croft fullname: Croft, Kevin D – sequence: 7 givenname: John K surname: Olynyk fullname: Olynyk, John K – sequence: 8 givenname: Ian C surname: Lawrance fullname: Lawrance, Ian C – sequence: 9 givenname: Debbie surname: Trinder fullname: Trinder, Debbie |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24223168$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2013 Public Library of Science 2013 Chua et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2013 Chua et al 2013 Chua et al |
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DocumentTitleAlternate | Iron-Induced Colonic IL-6/IL-11-Stat3 Signaling |
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Notes | Conceived and designed the experiments: ACGC BRSK JKO ICL DT. Performed the experiments: ACGC BRSK DSH SKF KDC. Analyzed the data: ACGC BRSK DSH CHF ICL DT. Wrote the paper: ACGC JKO ICL DT. Interpretation of data: ACGC BRSK JKO ICL DT. Competing Interests: The authors have declared that no competing interests exist. |
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Snippet | Chronic intestinal inflammation and high dietary iron are associated with colorectal cancer development. The role of Stat3 activation in iron-induced colonic... |
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SubjectTerms | Anemia Animals Apoptosis Apoptosis - drug effects Azoxymethane Cancer Cation Transport Proteins - genetics Cation Transport Proteins - metabolism Cell proliferation Cell Proliferation - drug effects Colitis - chemically induced Colitis - genetics Colitis - metabolism Colon cancer Colonic Neoplasms - genetics Colonic Neoplasms - metabolism Colonoscopy Colorectal cancer Colorectal carcinoma Comparative analysis Cytokines Dextran Dextran Sulfate - toxicity Dextrans Diet Dietary supplements Divalent metal transporter-1 Drinking water Endoscopy Enzyme-Linked Immunosorbent Assay Epithelial cells Female Ferritin Gastroenterology Gastrointestinal diseases Gene expression Gene Expression Regulation, Neoplastic Health aspects Health risks Histology Homeostasis Hospitals Immunoblotting In Situ Nick-End Labeling Inflammation Inflammatory bowel disease Inflammatory bowel diseases Interleukin 11 Interleukin 6 Interleukin-11 - genetics Interleukin-11 - metabolism Interleukin-6 - genetics Interleukin-6 - metabolism Intestine Iron Iron, Dietary - adverse effects Macrophages Medical research Medicine Mice Mice, Inbred C57BL Mucosa Oxidative stress Pharmacology Phosphorylation Phosphorylation - drug effects Receptors, Transferrin - genetics Receptors, Transferrin - metabolism Reverse Transcriptase Polymerase Chain Reaction Rodents Signal Transduction Signaling Sodium Sodium sulfate Stat3 protein STAT3 Transcription Factor - metabolism Studies Sulfates Transferrin Tumor necrosis factor-TNF Tumorigenesis Tumors |
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Title | Dietary iron enhances colonic inflammation and IL-6/IL-11-Stat3 signaling promoting colonic tumor development in mice |
URI | https://www.ncbi.nlm.nih.gov/pubmed/24223168 https://www.proquest.com/docview/1449103876/abstract/ https://pubmed.ncbi.nlm.nih.gov/PMC3819375 https://doaj.org/article/37a9a9552b314a27866876ce169af7c4 http://dx.doi.org/10.1371/journal.pone.0078850 |
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