Tuğçe Uygur1, Züleyha Pestil2, Oytun Erbaş1

1ERBAS Institute of Experimental Medicine, Illinois, USA & Gebze, Türkiye
2Pendik Veterinary Control Institute, İstanbul, Türkiye

Keywords: Cancer, cancer signaling pathways, cholesterol, high-density lipoprotein, low-density lipoprotein

Abstract

Cholesterol is a form of lipids, just as fats are and an essential component of cell membranes that are required for the synthesis of fat-soluble vitamins and steroid hormones such as estradiol, cortisol, progestins and testosterone, and bile acids. High-density lipoprotein and low-density lipoprotein (LDL), which are the most commonly known types of cholesterol, cause various diseases in the body. The LDL cholesterol raises the risk of breast, prostate, testicular, uterine, ovarian, and colorectal cancers and promotes cancer by activating several signaling pathways. This review discusse

Cancer, which originates from the Greek word karkinos, was found in mummies during the ancient Egyptian period (1600 BC). It is a disease that spreads worldwide.[1,2] According to 2017 data, a total of 180.288 cancer cases developed in Turkey.[3] Cancer, which occurs with the uncontrolled division and proliferation of cells, is a disease that occurs under the influence of genetic and environmental conditions.[4,5]

Cholesterol is an essential component of life and is maintained by a number of factors, including intracellular cholesterol levels, cholesterol synthesis, uptake, metabolism, and transport. Studies have shown that cholesterol plays a vital role in the formation and development of cancer and that high levels of cholesterol in the blood are associated with some types of cancer.[6-8]

CHOLESTEROL

Cholesterol, which is a type of fat; takes part in the production of hormones and vitamin D, cell membrane functions. Cholesterol also serves as a precursor to various steroid hormones and is involved in intracellular signal transduction. As one of its functions in cell signaling, recent evidence suggests that cholesterol plays an important role in regulating angiogenesis. It is produced by consuming milk and meat products in the body in the brain, adrenal glands, reproductive organs, intestine, and liver. In the cell, cholesterol is synthesized with the help of enzymes in the cytoplasm endoplasmic reticulum.[9-13]

Cholesterol biosynthesis occurs with the help of microsomes and peroxisomes, a mechanism called the Bloch and Kandutsch-Russell pathways, which involve a series of enzymatic reactions.[14-17] Several steps are required to convert acetyl coenzyme A (acetyl-CoA) into cholesterol, which is then involved in numerous biological roles. These steps include; acyl-CoA: cholesterol acyltransferase (ACAT), 3-hydroxy-3-methylglutaryl coenzyme A reductase (HMGCR), sterol O-acyltransferase, oxidative squalene cyclase (OSC), acyl-coenzyme A, sterol-O-Acyl transferases and adenosine triphosphate (ATP)-binding cassette transporter A-1. In vertebrate cells, lipid homeostasis is regulated by a set of membrane-bound transcription factors, sterol-regulatory element-binding proteins (SREBPs).[18]

The enzyme HMGCR is the rate-limiting enzyme of the cholesterol synthesis pathway.[19,20] ACAT1 is a tetrameric enzyme that converts two acetyl-CoA molecules into acetyl-CoA and CoA in the ketogenesis pathway.[21,22] Cholesterol synthesis begins with the two-carbon acetate group of acetyl-CoA.[23]

Two moles of acetyl-CoA combine to form acetoacetyl-CoA, followed by 3-hydroxy-3-methyl-glutaryl-CoA (HMG-CoA). In the following steps, cholesterol synthesis is completed with approximately 30 reactions that take place as a result of three stages. From the HMG-CoA formed in the first stage, mevalonate, the precursor of cholesterol, is formed by means of the HMG-CoA reductase enzyme. Here, the formation of mevalonate from HMG-CoA is the rate-limiting step, and HMG-CoA, the enzyme that catalyzes this reaction, acts as the reductase rate-limiting enzyme. In the second stage, squalene is formed from mevalonate. In the third stage, squalene follows two alternative pathways to create cholesterol, the Bloch pathway, and the Kandutsch–Russell pathway, and the cholesterol biosynthesis is completed.[23,24]

When cholesterol is in excess, it is stored as cholesterol esters (formed by the combination of fatty acids). Since it is insoluble in water, it binds to lipoproteins and circulates in the blood with the help of lipoproteins.[13] Both genetic and environmental factors affect the number of lipids and lipoproteins in the blood. Lipid concentrations increase as people age.[18]

Lipoproteins are macromolecular structures that contain a shell and nucleus consisting of phospholipids and free cholesterol. The polar part allows cholesterol to circulate in the blood as water communicates.[25]

Types of lipoproteins: low-density lipoprotein (LDL) (β mobility), very-low-density lipoprotein (VLDL;preβ mobility) and high-density lipoprotein (HDL; α mobility), chylomicrons.[26,27] High-density lipoprotein and LDL are the most widely known types of cholesterol.[27,28] Cholesterol is involved in the production of bile salts, and its overproduction causes excess fat absorption into the body.

Chylomicrons transport cholesterol from the small intestine to the liver. The majority of this transported cholesterol is taken in through food. When the amount decreases, it is produced in the liver. In order for the produced cholesterol and other lipids to be delivered to other tissues in the body, it is secreted into the blood in very VLDL (since it does not dissolve in water). As the cholesterol in the VLDL in the blood decreases and is transferred to the cells, the structure and density of VLDL change, first it turns into intermediate-density lipoprotein (IDL) and then into LDL. A high amount of LDL in the blood leads to the accumulation of these lipoproteins on the walls of arterial vessels, which causes clots, heart disease, and stroke.[29,30]

Blood cholesterol levels are affected by obesity, dietary habits, blood pressure imbalances, heredity, lipid metabolism disorder, diabetes, smoking and alcohol consumption, advanced age, lack of physical activity, estrogen deficiency, elevated fibrinogen, significant brain, heart, kidney, thyroid or vascular disease.[31-35]

THE RELATIONSHIP BETWEEN CHOLESTEROL AND CANCER

Dietary fat intake causes death in humans. High-fat consumption causes many chronic diseases such as obesity, cardiovascular diseases, some types of cancer, and type 2 diabetes.[36-40]

The most important features of cancer cells are the activation of oncogenes and the loss of tumor suppressors.[41] In the research, it is understood that cholesterol affects tumor development.[42] All types of fat, especially LDL, increase the risk of breast, testicular, uterine ovarian, and colorectal cancers.[36] Tumors must meet membrane biogenesis and biofunctional requirements in order to multiply. Cholesterol is also necessary for the membrane.[43]

An excess of lipids in the body increases the levels of reactive oxygen species (ROS), which causes the oxidation of intracellular LDL to oxidized low-density lipoproteins (ox-LDL). In addition, oxidative stress causes deoxyribonucleic acid (DNA) damage to carcinogenesis in cancers.[44,45] Low-density lipoprotein contains polyunsaturated fatty acids that can be oxidized by ROS (reactive oxygen species) and reactive nitrogen species (RNS) to produce lipid peroxides such as ox-LDL. Ox-LDL stimulates ROS production. Apolipoprotein B-100 (ApoB-100 ) is the protein component of LDL and is the best ligand for LDL receptor (LDLR). The residues of histidine, cysteine, tyrosine, and lysine in ApoB-100 are also oxidation targets of ROS and RNS, and oxidative modification of ApoB-100 can eliminate its function as an LDLR ligand. When ox-LDL are no longer recognized by LDLR, they can be identified and combined with scavenger receptors such as lectin-like oxidized LDL receptor-1 (LOX-1), scavenger receptor A, and the cluster of differentiation 36 (CD36). Ox-LDL is a well-known biomarker for cardiovascular disease and increases endothelial cell adhesion by activating oxidative stress and stimulating the expression of pro-inflammatory factors and adhesion molecules, as well as chemokines in vascular endothelial cells, leading to endothelial dysfunction. In recent years, more and more studies have focused on ox-LDL and cancers, and high levels of ox-LDL, as well as LOX-1, and CD36 have been found to be associated with increased risk of various cancers. Ox-LDL promotes epithelial-mesenchymal growth, and cytoplasmic transformation induces protective autophagy, activates inflammatories, and promotes the release of growth factors, cytokines, and other pro-inflammatory markers to stimulate oncogenic signals, resulting in cell mutations and chemotherapy resistance. Low-density lipoprotein may cause cancer by activating numerous signaling pathways; phosphatidylinositol 3-kinase/protein kinase B (PI3K/AKT), extracellular signal-regulated protein kinases (ERKs), Signal transducer and activator of transcription (STAT)-3, etc.[2,46-52]

The PI3K/Akt activation; PI3K family is divided into four classes: Three of the PI3K family phosphorylate lipids and one phosphorylates proteins. Class I of PI3K is divided into two subunits, p85 and p110. PI3K activation occurs by binding to the growth factor receptor (ERBB or epidermal growth factor (EGF). When PI3K is activated, the effect of p85 on p110 is reduced and it converts phosphatidylinositol-4,5-diphosphate (PIP2) to phosphatidylinositol-3,4,5-trisphosphate (PIP3). The increase in PIP3 (phosphatidyl inositol 1-4-5-triphosphate) causes an increase in AKT/AKT and ERK. phosphoinositide-dependent kinase 1 (PDK1) is activated by the binding of PIP3 to the pleckstrin homology (PH) domain at the C terminus of PDK1. Activated PDK1 phosphorylates AKT at thr/ser T308. Phosphorylation of T308 allows PDK2 to phosphorylate S473. Double phosphorylation of AKT at T308 and S473 activates AKT and stimulates cell cycle progression, survival, metabolism, and migration. AKT has three family members, AKT1, AKT2, and AKT3. Inactivation of AKT destroys Class I PI3K-induced survival. The most common PI3K mutations are E542K, E545K, and H104R.[53,54] PI3K/AKT regulates cancer cell growth by activating the mammalian target of rapamycin (mTOR), which can promote cholesterol synthesis and uptake by activating SREBPs. The mitogen-activated protein kinase (MAPK) pathway, consisting of the Ras-Raf-MEK-ERK signaling cascade is activated by the activation of ERBB2. Growth factor receptor-bound protein 2 (Grb2) contains the Src homology 2 (SH2) domain, which recognizes phosphorylated tyrosine sites in the active receptor. Grb2 binds to the guanine nucleotide exchange factor son of sevenless (SOS) through the SH3 domain. When the Grb2/SOS complex approaches the active receptor, SOS is activated and removes guanosine 5'-diphosphate (GDP) from the inactive Ras. The released Ras becomes active by binding to guanosine triphosphate (GTP). Ras/GTP) binds to Raf-1 and activates it. It also activates MEK-1 and MEK-2. For Ras proteins to become active, they must be localized to the membrane after post-translational regulation. In resting cells, Ras proteins are inactive (Ras-GDP) and act as nodes for signaling pathways. They activate MEK, ERK-1, and ERK-2 by phosphorylating them. ERK activation causes changes in cell physiology, cell cycle control, differentiation, migration, apoptosis, and angiogenesis.[54,55]

STAT3 activation causes the differentiation of cells and the proliferation of tumor cells. Activation of STAT3 leads to increased levels of anti-apoptotic proteins such as Bcl-xL, Bcl-2, and myeloid leukemia cell differentiation protein 1 in cancer cells and cell proliferation. STAT3 phosphorylates and activates survivin, vascular endothelial growth factor (VEGF), c-myc, cyclin D1, and matrix metalloproteinase (MMP) and enables cell proliferation.[56-61]

High blood cholesterol is a common comorbidity in obesity. Its impact as a risk factor for breast cancer is contradictory and it is unclear whether total, LDL, or HDL cholesterol contributes to the disease.[62,63]

In experimental studies, cancer cells have been shown to have an LDLR, They showed that HMG-CoA reductase HMGCR and sterol regulatory element-binding protein SREBPs exhibit deregulated transcriptional levels of several genes involved in cholesterol regulation and metabolism.[64-66]

Many cancer cells show high LDL receptor levels and increased LDL uptake.[67,68] In a breast cancer cell model known for its aggressive cell behavior (MDA-MB-231), the LDL receptor has been shown to be up-regulated and LDL stimulates cell migration.[69] Scavenger receptor-BI is also frequently overexpressed in tumors and is thought to contribute to increased HDL-cholesterol uptake in cancer cells.[67,70] In MDA-MB-231 cells, scavenger receptor-BI deficiency inhibits migration in vitro and tumor growth in vivo. [71] Liver X receptor (LXR) activation induced by 27-hydroxycholesterol accumulation promotes the development of highly aggressive basal breast carcinoma characterized by mesenchymal features.[72]

Excess fat accumulates in the liver and the liver enlarges due to fat accumulation and then inflammation begins in the fatty liver. If this situation continues for a long time, scar tissue forms in the liver, and eventually, cirrhosis occurs. If the cirrhosis problem progresses, it can cause cancer.[73,74] In a study, it was observed that serum cholesterol in the blood can cause increased expression of VEGF, MMP-2, and MMP-9 by activating the nuclear factor kappa B signaling pathway in hepatocellular carcinoma cells and cholesterol can cause inflammation.[6,75]

Studies have shown that the development of colorectal cancer is closely related to high fat intake in the diet and especially to cholesterol levels. It has been understood that high cholesterol levels cause colorectal cancer formation by the HMG-CoA mechanism.[76-79] It has been shown that LDL cholesterol is associated with colorectal cancer progression[79,80], HDL cholesterol is inversely associated with colorectal cancer risk[79,81], and total cholesterol and triglyceride levels are positively associated with increased colorectal cancer risk.[82-84]

The possible link between the incidence of pancreatic ductal adenocarcinoma (PDAC) and cholesterol metabolism has been demonstrated by epidemiologic studies showing high serum cholesterol and obesity as risk factors.[84,85] Rapid uptake and endogenous biosynthesis of cholesterol and phospholipids are a feature of oncogene-transformed cells.[85,86] PDAC causes increased expression of cholesterol synthesis genes, although this is not certain.[87] Cholesterol, its precursors, and/or metabolites may modulate the oncogenic functions of tumor cells to alter the disease course in early PDAC stages. For this reason, metabolites of cholesterol and other components of the cholesterol biosynthetic pathway are known to influence progression in some types of cancer.[72,88] A study examining the causal relationship between endogenous cholesterol metabolism and PDAC development and differentiation revealed that a metabolically determined PDAC differentiation duality is mediated by cholesterol-sensitive SREBP1-dependent transforming growth factor beta (TGFβ) expression, TGFβ receptor activation, and induction of a canonical Smad2/3 signaling pathway.[89]

Membrane rafts are heterogeneous and dynamic domains characterized by tight packing of lipids.[90] Signals critical for the survival and proliferation of prostate cancer (PCa) cells are transmitted through lipid rafts.[90,91] Studies have shown that some proteins critical for PCa growth and survival are regulated by lipid rafts and that changes in membrane cholesterol measurably affect the signals generated by these molecules.[92-94] Epidermal growth factor receptor (EGFR) in the lipid rafts of PCa cells is much more active and much more highly phosphorylated than the cohort of receptors in non-raft membranes, and cholesterol targeting by EGFR also disrupts downstream effectors.[95,96] The study also showed that a subpopulation of Akt present in rafts exhibits very different substrate specificity than non-raft Akt. This raft-localized Akt is inhibited by decreased cholesterol levels.[97] Signaling by LXRs down-regulates the level of phosphorylated Akt present in rafts, leading to PCa cell apoptosis, a process precipitated by LXR-stimulated cholesterol efflux and reversed by exogenous cholesterol addition. Collective data suggest that cholesterol regulates lipid dynamics, which in turn affects vital signaling pathways and acts to protect cells from apoptosis through the effects of increased cholesterol on lipids.[98,99]

Fatty acids and cholesterol are the two main types of lipids. Multiple fatty acids and enzymes involved in fatty acid metabolisms, such as fatty acid-binding protein 4, CD36, and stearoyl-CoA desaturase 1, significantly increase ovarian cancer proliferation, survival, drug resistance, and metastasis.[100-104] Proteins and enzymes highly expressed in cholesterol metabolism induce ovarian cancer progression; cholesterol and its derivatives also cause proliferation and chemo-resistance in ovarian cancer.[105-110]

In conclusion, the effect of LDL on the body causes various diseases. Excess LDL can cause heart disease, stroke, and cancer. It activates various signaling pathways and increases the risk of breast, prostate, testicular, uterine ovarian, and colorectal cancers.In addition, HDL eliminates cholesterol and tumor cells, which inhibits the growth and spread of tumors.

Cite this article as: Uygur T, Pestil Z, Erbaş O. Influence of Cholesterol on Cancer Progression. JEB Med Sci 2022;3(3):213-220.

Conflict of Interest

The authors declared no conflicts of interest with respect to the authorship and/or publication of this article.

Financial Disclosure

The authors received no financial support for the research and/or authorship of this article.

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