Role of Lymphatic Deficiency in the Pathogenesis and Progression of Inflammatory Bowel Disease to Colorectal Cancer in an Experimental Mouse Model.


Journal

Inflammatory bowel diseases
ISSN: 1536-4844
Titre abrégé: Inflamm Bowel Dis
Pays: England
ID NLM: 9508162

Informations de publication

Date de publication:
14 11 2019
Historique:
received: 14 03 2019
pubmed: 8 6 2019
medline: 25 6 2020
entrez: 8 6 2019
Statut: ppublish

Résumé

Inflammatory bowel disease (IBD) is characterized by chronic inflammation, which can progress to colorectal cancer, with duration of disease being the most important risk factor. Although many factors are involved, the pathogenic link between inflammation and cancer and the role played by the lymphatic system have not been fully investigated. This project uses lymphatic-deficient mice (Angiopoietin-2 [Ang2] knockout) to examine the lymphatic system in the progression of IBD to colorectal cancer. Angiopoietin-2 wild-type, heterozygote, and knockout mice received a single injection of the procarcinogen azoxymethane and had an IBD-promoting chemical irritant (dextran sodium sulfate) added to their drinking water over a 7-week period. We measured disease activity (weight loss, stool consistency, fecal occult blood) during the study and at sacrifice, collected blood for cytokine/biomarker (Ang2, interleukin [IL] 1-β, IL-6, tumor necrosis factor α [TNFα], and VEGF-C) enzyme-linked immunosorbent assay analysis, measured colon length, and assessed tumor burden. Ang2 knockout (KO) mice exhibited reduced (55%) survival vs wild-type (100%) and heterozygotes (91%; P < 0.01 and P < 0.0001, respectively). Most (>89%) mice developed tumors, and the incidence of colorectal cancer did not differ among the genotypes (P = 0.32). The tumor area was significantly increased in KO mice (P = 0.004). Of the biomarkers measured in the serum, Ang2 and TNF-α concentrations were significantly different among the genotypes (P = 3.35e-08 and P = 0.003 respectively). Disease activity was significantly increased in KO mice compared with wild-type and heterozygote mice (P = 0.033). Lymphatic deficiency, defective lymphangiogenesis, and impaired lymphatic-generated inflammation did not protect against clinical IBD or progression to colorectal cancer in this experimental model.

Sections du résumé

BACKGROUND
Inflammatory bowel disease (IBD) is characterized by chronic inflammation, which can progress to colorectal cancer, with duration of disease being the most important risk factor. Although many factors are involved, the pathogenic link between inflammation and cancer and the role played by the lymphatic system have not been fully investigated. This project uses lymphatic-deficient mice (Angiopoietin-2 [Ang2] knockout) to examine the lymphatic system in the progression of IBD to colorectal cancer.
METHODS
Angiopoietin-2 wild-type, heterozygote, and knockout mice received a single injection of the procarcinogen azoxymethane and had an IBD-promoting chemical irritant (dextran sodium sulfate) added to their drinking water over a 7-week period. We measured disease activity (weight loss, stool consistency, fecal occult blood) during the study and at sacrifice, collected blood for cytokine/biomarker (Ang2, interleukin [IL] 1-β, IL-6, tumor necrosis factor α [TNFα], and VEGF-C) enzyme-linked immunosorbent assay analysis, measured colon length, and assessed tumor burden.
RESULTS
Ang2 knockout (KO) mice exhibited reduced (55%) survival vs wild-type (100%) and heterozygotes (91%; P < 0.01 and P < 0.0001, respectively). Most (>89%) mice developed tumors, and the incidence of colorectal cancer did not differ among the genotypes (P = 0.32). The tumor area was significantly increased in KO mice (P = 0.004). Of the biomarkers measured in the serum, Ang2 and TNF-α concentrations were significantly different among the genotypes (P = 3.35e-08 and P = 0.003 respectively). Disease activity was significantly increased in KO mice compared with wild-type and heterozygote mice (P = 0.033).
CONCLUSIONS
Lymphatic deficiency, defective lymphangiogenesis, and impaired lymphatic-generated inflammation did not protect against clinical IBD or progression to colorectal cancer in this experimental model.

Identifiants

pubmed: 31173626
pii: 5512544
doi: 10.1093/ibd/izz112
pmc: PMC6855278
doi:

Substances chimiques

Angiopoietin-2 0
Angpt2 protein, mouse 0
Biomarkers 0
Tumor Necrosis Factor-alpha 0
Dextran Sulfate 9042-14-2
Azoxymethane MO0N1J0SEN

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1919-1926

Subventions

Organisme : NIDDK NIH HHS
ID : R01 DK109711
Pays : United States
Organisme : NHLBI NIH HHS
ID : R25 HL108837
Pays : United States

Informations de copyright

© 2019 Crohn’s & Colitis Foundation. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

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Auteurs

Sarah K Daley (SK)

Department of Pathology, University of Arizona, Tucson, Arizona.

Marlys H Witte (MH)

Department of Surgery, University of Arizona, Tucson, Arizona.

Jalicia Washington (J)

Department of Surgery, University of Arizona, Tucson, Arizona.

Michael Bernas (M)

Texas Christian University and University of North Texas Health Science Center School of Medicine, Fort Worth, Texas.

Pawel Kiela (P)

Department of Pediatrics, University of Arizona, Tucson, Arizona.

Jennifer Thorn (J)

Department of Pathology, University of Arizona, Tucson, Arizona.

Nathan Tanoue (N)

Department of Surgery, University of Arizona, Tucson, Arizona.

J Steven Alexander (JS)

Department of Molecular and Cellular Physiology, Louisiana Health Sciences Center-Shreveport, Louisiana.

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Classifications MeSH