Detection of Metabolic Alterations in Non-tumor Gastrointestinal Tissue of the ApcMin/+ Mouse by 1H MAS NMR Spectroscopy
Abstract
In this study, we have used metabolic profiling (metabolomics/metabonomics) via high resolution magic angle spinning (HRMAS) and solution state (1)H NMR spectroscopy to characterize small bowel and colon tissue from the Apc(Min/+) mouse model of early gastrointestinal (GI) tumorigenesis. Multivariate analysis indicated the presence of metabolic differences between the morphologically normal/non-tumor tissue from approximately 10 week-old Apc(Min/+) mice and their wild-type litter mates. The metabolic profile of isolated lamina propria and epithelial cells from the same groups could also be discriminated on the basis of genotype. Accounting for systematic variation in individual metabolite levels across different anatomical regions of the lower GI tract, the metabolic phenotype of Apc(Min/+) lamina propria tissue was defined by significant increases in the phosphocholine/glycerophosphocholine ratio (PC/GPC, +21%) and decreases in GPC (-25%) and the gut-microbial cometabolite dimethylamine (DMA, -40%) relative to wild type. In the whole tissue, elevated lactate (+15%) and myo-inositol (+19%) levels were detected. As the metabolic changes occurred in non-tumor tissue from animals of very low tumor burden (<2 polyps/animal), they are likely to represent the specific consequence of reduced Apc function and very early events in tumorigenesis. The observed increase in PC/GPC ratio has been previously reported with immortalisation and malignant transformation of cells and is consistent with the role of Apc as a tumor suppressor. Phospholipase A2, which hydrolyses phosphatidylcholine to Acyl-GPC, is a known modifier gene of the model phenotype (Mom1), and altered expression of choline phospholipid enzymes has been reported in gut tissue from Apc(Min/+) mice. These results indicate the presence of a metabolic phenotype associated with "field cancerization", highlighting potential biomarkers for monitoring disease progression, for early evaluation of response to chemoprevention, and for predicting the severity of the polyposis phenotype in the Apc(Min/+) model.
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Metabolic changes occur in premalignant colonic polyps in humans and mice, and some are retained in adenocarcinomas.
“Other studies in humans and mice report metabolic changes in premalignant colonic polyps, some of which are retained in adenocarcinomas (21, 22).”
From Metabolic reprogramming and cancer progression (2020) · cites this paper as [21]
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Wang, J.-Y., Zhang, X.-P., Zhou, H.-K., Cai, H.-X., Xu, J.-B., Xie, B.-G., Thiery, J.-P., & Zhou, W. (2024) · Figshare · doi:10.6084/m9.figshare.26723439
- Authors
- Backshall, A., Alferez, D., Teichert, F., Wilson, I. D., Wilkinson, R. W., Goodlad, R. A., & Keun, H. C.
- Affiliations
- University of Leicester (GB)
- Department of Biomolecular Medicine, Division of Surgery, Oncology, Reproductive Biology and Anaesthetics, Faculty of Medicine, Imperial College London, Sir Alexander Fleming Building, South Kensington, London, United Kingdom, SW7 2AZ, Cancer Research U.K., Lincoln’s Inn Fields, London, United Kingdom, WC2A 3PX, Cancer Biomarkers and Prevention Group, Dept of Cancer Studies and Molecular Medicine, University of Leicester, United Kingdom, AstraZeneca Pharmaceuticals, Alderley Park, Macclesfield, Cheshire,...
- Corresponding author
- Keun, Hector C.
- Venue
- Journal of Proteome Research
- Publisher
- American Chemical Society (ACS)
- Published
- 2009-01-21
- Volume
- 8
- Issue
- 3
- Pages
- 1423-1430
- ISSN
- 1535-3893 (ISSN-L)
- 1535-3907
- OpenAlex
- W2067544564
- Cited by
- 42
- References
- 47
- Citations by year
- 2025: 1 · 2024: 8 · 2021: 2 · 2020: 2 · 2019: 2 · 2018: 2 · 2017: 1 · 2015: 2 · 2014: 4 · 2013: 3 · 2012: 3
- FWCI
- 2.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Proteome Research (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- Biotechnology and Biological Sciences Research Council
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- field cancerization, dimethylamine, lactate, myo-inositol, lamina propria, phospholipase A2, colorectal polyps, metabolomics, biomarkers
- MeSH terms
- Animals, Cell Transformation, Neoplastic, Colon, Dimethylamines, Epithelial Cells, Gastrointestinal Neoplasms, Inositol, Intestine, Small, Mice, Inbred C57BL, Mucous Membrane, Magnetic Resonance Spectroscopy, Phosphorylcholine, Precancerous Conditions, Lactic Acid, Adenomatous Polyposis Coli Protein, Mice, Metabolomics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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