Decreased Triacylglycerol Content and Elevated Contents of Cell Membrane Lipids in Colorectal Cancer Tissue: A Lipidomic Study.

Adriana Mika,Wojciech Makarewicz,Adrian Perdyan,Ivan Liakh,Aleksandra Czumaj,Jarek Kobiela,Zbigniew Kaczynski,Krystian Adrych,Alicja Pakiet,Tomasz Sledzinski

doi:10.3390/jcm9041095

Adriana Mika, Wojciech Makarewicz + Show 8 more

Open Access

https://doi.org/10.3390/jcm9041095

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Abstract

Recent evidence suggests that lipid composition in cancer tissues may undergo multiple alterations. However, no comprehensive analysis of various lipid groups in colorectal cancer (CRC) tissue has been conducted thus far. To address the problem in question, we determined the contents of triacylglycerols (TG), an energetic substrate, various lipids necessary for cell membrane formation, among them phospholipids (phosphatidylcholine, phosphatidylethanolamine), sphingolipids (sphingomyelin) and cholesterol (free, esterified and total), and fatty acids included in complex lipids. 1H-nuclear magnetic resonance (1H-NMR) and gas chromatography-mass spectrometry (GC-MS) were used to analyze the lipid composition of colon cancer tissue and normal large intestinal mucosa from 25 patients. Compared with normal tissue, cancer tissues had significantly lower TG content, along with elevated levels of phospholipids, sphingomyelin, and cholesterol. Moreover, the content of oleic acid, the main component of TG, was decreased in cancer tissues, whereas the levels of saturated fatty acids and polyunsaturated fatty acids (PUFAs), which are principal components of polar lipids, were elevated. These lipidome rearrangements were associated with the overexpression of genes associated with fatty acid oxidation, and the synthesis of phospholipids and cholesterol. These findings suggest that reprogramming of lipid metabolism might occur in CRC tissue, with a shift towards increased utilization of TG for energy production and enhanced synthesis of membrane lipids, necessary for the rapid proliferation of cancer cells.

Highlights

Colorectal cancer (CRC) is one of the most common malignancies worldwide, and its incidence is still increasing [1,2,3,4]
CRC tissue contained higher levels of lipids serving as components of plasma membranes, such as phospholipids, sphingomyelin, and cholesterol, and had a lower content of TGs, the main source of energy in the cell
The present study suggest that this observation might be related to the fact that polyunsaturated fatty acids (PUFAs) are essential for the formation of cell membrane phospholipids during rapid proliferation of cancer cells

Summary

Introduction

Colorectal cancer (CRC) is one of the most common malignancies worldwide, and its incidence is still increasing [1,2,3,4]. Lipidomic studies can provide information about the biochemical role of lipids and their exact physiological functions, the problem is quite complex [5]. Based on the comparison of lipid metabolism in various physiological and pathological conditions, identification of critical structures, their functions and interactions with other lipids, proteins, and different metabolites, lipidomics may explain the role of these compounds in metabolic control [1]. Some authors have claimed a positive effect of supplementation with various lipids [2,6] or their main structural elements, fatty acids (FAs), in cancer patients [7]. The effects of FAs were shown to depend on the structural group they belong, as well as on their source (de novo synthesis, diet) [3]

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