Role of apolipoprotein B-containing lipoproteins in the development of atherosclerosis Jan Borén MD, PhD
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1 Role of apolipoprotein B-containing lipoproteins in the development of atherosclerosis Jan Borén MD, PhD Our laboratory focuses on the role of apolipoprotein (apo) B- containing lipoproteins in normal and disturbed lipid metabolism and understanding the molecular mechanisms by which the apobcontaining lipoproteins exert their effect on the arterial wall. Our work spans multiple research disciplines: molecular biology, lipid biochemistry, genetically modified mice, whole organism physiology and multicompartment modeling of lipid metabolism in humans. AN ATHEROGENIC DYSLIPIDEMIA IN PATIENTS WITH TYPE 2 DIABETES Insulin resistance is a key feature of the metabolic syndrome and can lead to the development of type 2 diabetes. These conditions are today increasingly common, primarily because of the increased prevalence of a sedentary lifestyle and obesity. Insulin resistance and type 2 diabetes are characterized by dyslipidemia, which is a major risk factor for cardiovascular disease (CVD). This dyslipidemia is characterized by high levels of plasma triglycerides, low levels of high-density lipoprotein (HDL) cholesterol, the appearance of small, dense low-density lipoproteins (sdldl), and excessive postprandial lipemia. 1 Diabetic dyslipidemia frequently precedes type 2 diabetes, which may explain why macrovascular disease often develops long before the clinical diagnosis of diabetes. It is now recognized that the different components of diabetic dyslipidemia are not isolated abnormalities but are closely linked to each other metabolically. Furthermore, we have shown that diabetic dyslipidemia is initiated by the hepatic overproduction of large triglyceride-rich very low density lipoproteins (VLDL 1 ) (Figure 1). 1 It is therefore important to elucidate the mechanism for the increased production of VLDL 1 particles in patients with type 2 diabetes. We recently analyzed which features of type 2 diabetes and insulin resistance correlate with
2 VLDL 1 production, and revealed strong correlations with plasma glucose that are not apparent in the normal range of plasma glucose. 1 By extending our study to monitor liver fat, intraabdominal fat, subcutaneous fat and adiponectin, we showed that fasting insulin, plasma glucose, intra-abdominal fat and liver fat are closely associated with VLDL 1 - apob and VLDL 1 -triglyceride production. 2 However, in a multiple regression analysis, only liver fat and plasma glucose remain significant. 2 Once thought to be benign, fatty liver is now considered to be the hepatic component of the metabolic syndrome. We tested the relationship between liver fat and VLDL 1 production in subjects with a broad range of liver fat content. 3 This study confirmed that liver fat determines baseline VLDL 1 production, and it also showed that liver fat is associated with lack of VLDL 1 suppression in response to insulin: insulin downregulates VLDL 1 secretion in subjects with low liver fat, but fails to suppress VLDL 1 secretion in subjects with high liver fat, resulting in overproduction of VLDL 1 (Figure 1). 3 RETAINED ATHEROGENIC LIPOPROTEINS ARE RETAINED IN THE ARTERY WALL AND TAKEN UP BY MACROPHAGES Although it is well documented that elevated levels of LDL and other lipoproteins that contain apob cause increased atherosclerosis, the molecular and cellular mechanisms involved in the initiation of atherosclerosis have been under debate for many years and several hypotheses have been postulated. A few years ago we provided direct evidence to show that subendothelial retention of apob100-containing lipoproteins is the initiating event in atherogenesis, and that the atherogenicity of LDL is linked to their proteoglycan-binding activity (Figure 2). 4 Lipoproteins associate with artery wall proteoglycans via both direct and indirect interactions. Direct binding between LDL and proteoglycans involves an ionic interaction between basic amino acids in apob100 and negatively charged sulfate groups on the glycosaminoglycan (GAG) chains of proteoglycans. 4 Subendothelial retention of LDL can also be mediated by indirect binding to GAGs facilitated by bridging molecules, such as lipoprotein lipase (LPL). We recently investigated the importance of the direct binding of LDL-apoB to proteoglycans in the development of atherosclerosis over time, and assessed the role of LPL to facilitate LDL retention at later stages of development. 5 The results showed that although retention of LDL in the artery wall is initially governed by direct binding of LDL to proteoglycan
3 GAG chains, there is a shift to indirect binding when macrophages infiltrate the intima and secrete bridging molecules such as LPL. These bridging molecules act in concert or in parallel with proatherogenic modifications of the extracellular matrix and subendothelial modification of LDL, leading to accelerated retention of atherogenic lipoproteins and eventually development of advanced atherosclerotic lesions (Figure 3). 5 CONCLUSION Diabetic dyslipidemia is a cluster of potentially atherogenic lipid and lipoprotein abnormalities that are caused by an overproduction of large VLDL 1 particles. The dyslipidemia is linked to increased atherosclerosis. Despite the complexity of advanced atherosclerosis, there is a clear root cause the subendothelial retention of apob-containing lipoproteins which should continue to be a major focus of interventions to combat atherothrombotic vascular disease.
4 REFERENCES 1. Adiels M, Olofsson S-O, Taskinen MR and Borén J. Overproduction of VLDL particles is the hallmark of the dyslipidemia in the metabolic syndrome. Arterioscler Thromb Vasc Biol (in press). 2. Adiels M, Taskinen MR, Packard C, Caslake MJ, Soro A, Westerbacka J, Vehkavaara S, Häkkinen AM, Olofsson SO, Yki-Järvinen H and Borén J. Overproduction of large VLDL particles is driven by increase of liver fat content in man. Diabetologia 2006; 4: Adiels M, Westerbacka J, Soro-Paavonen A, Häkkinen A, Vehkavaara S, Caslake MJ, Packard C, Olofsson SO, Yki-Järvinen H, Taskinen MR and Borén J. Acute suppression of VLDL1 secretion rate by insulin is associated with hepatic fat content and insulin resistance. Diabetologia 2007; 50: Tabas I, Williams KJ and Borén J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis. Circulation 2007; 116: Gustafsson M, Levin M, Skålén K, Perman J, Fridén V, Jirholt P, Olofsson, SO, Fazio S, Linton MF, Semenkovich CF, Olivecrona G and Borén J. Retention of LDL in atherosclerotic lesions of the mouse: evidence for a role of lipoprotein lipase. Circulation Research. 2007; 101:
5 FIGURE LEGENDS Fig. 1. The assembly of VLDL involves a stepwise lipidation of the structural protein apob100 in the liver. This results in the formation of a VLDL 2 (i.e., the triglyceride-poor form of VLDL) by additional lipidation. The VLDL 2 particle can either be secreted from the cell or further lipidated to form VLDL 1. The conversion of VLDL 2 to VLDL 1 requires a bulk addition of triglycerides. Normally, insulin downregulates VLDL 1 secretion and increases VLDL 2 secretion, but in subjects with high liver fat this regulation is impaired resulting in overproduction of VLDL 1. Fig. 2. Lipoproteins normally flux into and out of the arterial wall by crossing the endothelium. The initial transport across the endothelium does not appear to be the rate limiting step, but rather the selective retention of lipoproteins probably determines the concentration and the susceptibility to modification of lipoproteins in the arterial wall. Following retention of LDL by proteoglycans of the intima, aggregated or otherwise modified LDL is avidly taken up by macrophages leading to foam cell formation. The conversion of macrophages to foam cells stimulates the release of LPL and other potentially atherogenic factors. Thus, retained lipoproteins can directly or indirectly provoke all known features of early lesions and, by stimulating local synthesis of proteoglycans and LPL, can accelerate further retention and aggregation. Fig. 3. The fatty streak is the earliest recognizable lesion of atherosclerosis and is caused by the aggregation of lipid-rich foam cells. The development of an atherosclerotic plaque indicates an advanced stage of atherosclerosis. Migration of vascular smooth muscle cells to the intima and the laying down of collagen fibers result in the formation of a protective fibrous cap over the lipid core. An atherosclerotic plaque may cause complications as a result of its size, reducing lumen diameter and blood flow, its tendency to rupture, or following its erosion. Plaque erosion or rupture occurs in plaques that are intrinsically vulnerable.
6 FIGURE 1 Insulin TG apob VLDL 2 VLDL 1 VLDL 2 FIGURE 2 LDL Monocyte Retention Foam cell formation
7 FIGURE 3 Fatty streak Normal Lipid-rich plaque Foam cells Thrombus Lipid core Fibrous cap
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