Articles |
From the Wallenberg Laboratory for Cardiovascular Research, Faculty of Medicine, University of Gothenburg, (E.H.-C., U.O., O.W., G.B., G.C.), and Astra Hässle AB, Preclinical Research Laboratories, Mölndal (G.C.), Sweden.
Correspondence to Germán Camejo, Astra Hässle AB, Preclinical Research Laboratories, Mölndal, S-431 83, Sweden.
Key Words: proteoglycans atherogenesis apoB lipoproteins
| ApoB Lipoproteins in the Intima and Atherosclerosis |
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However, deposition and colocalization with PGs in the intima do not explain why this phenomenon should be atherogenic. Deposits of cholesterol and cholesteryl esters in the interstitial intima originated from apoB lipoproteins could be direct cytotoxic agents initiating the tissue reaction in atheromas.18 19 Additionally, structurally modified apoB lipoproteins or their oxidative and hydrolytic products may be triggers of the tissue response associated with atherogenesis.20 Williams and Tabas,21 in what was termed "the response-to-retention hypothesis of early atherogenesis," recently discussed the general concepts of how apoB lipoprotein deposition in the intima may contribute to atherogenesis. Therefore, the present review is focused on the molecular aspects of the interaction of apoB lipoproteins with PGs of the intima and their potentially atherogenic cellular consequences.
| Molecular Basis for Entrapment of ApoB Lipoproteins in the Arterial Wall |
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Addition of hydrophobic segments of valine (V) and tryptophan (W) at the N- and C- terminals of the apoB-100 segment 3359-3367 (VVW-RLTRKRGLK-VVV) allowed its attachment on the surface of neutral liposomes, LDL, and VLDL. The liposomes, which show no affinity for GAGs, acquire this property when the peptide is attached. The complex liposome-peptide has a higher affinity for C6S than the isolated peptide. Furthermore, LDL and VLDL increase their affinity for C6S when additional peptide copies are bound to them.36 This behavior suggests that anchoring the GAG-binding segment to a polar lipid interface orients the Arg and Lys side chains for maximal interaction with the SO4- and COO- of the C6S. Recent data indicate that segments of apoB-100, 3147-3157 (SVKAQYKKNKHRKH) and 3359-3367 (RLTRKRGLK), may act cooperatively in the association with PGs and GAGs.37 These two segments, separated linearly by 202 amino acids, may be brought together by turns of the apoB-100 imposed by a disulfide bridge linking Cys(3167) and Cys(3297).31 Possibly apoB-100 becomes a better ligand for GAGs when the VLDL and LDL particles become smaller, because two or more positive segments coalesce in the particle's surface or become more exposed (Fig 1
).36 37 38
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| Arterial PGs That Can Interact With ApoB Lipoproteins |
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70% C6S, 20% C4S, and 10% DS and is defined as a CSPG. It fills the essentially acellular intima as an extended tridimensional network in association with hyaluronate and provides the compressive resilience of the vessel wall. Two small PGs, decorin and biglycan, with core proteins of 36 kD and two to three GAG chains of DS, exist also in the intimal interstitium and are involved in the correct organization of collagen fibers. These PGs are mostly products of smooth muscle cells of the media. The basement membrane of the endothelium contains perlecan, with a large multidomain core protein (
450 kD) and with three HS chains that interact with collagen type IV, vitronectin, and laminin. Syndecan is an additional PG associated with the plasma membrane of most cells, and it contains three to five CS and HS GAG chains attached to a 30-kD core protein. Its main function appears to be the accretion at the cell surface of growth factors, cytokines, lipases, and homeostasis factors that have GAG-binding segments. For a detailed discussion of vascular extracellular matrix, see the review by Wight.5 All PGs and sulfated GAGs can potentially interact with apoB lipoproteins, but the most studied is versican and the CS GAGs. During the proliferative phase of atherogenesis there is a marked increase in CSPG and most of the intima volume is occupied by the PGs and a collagen network.5 39 40 The CS and DS GAGs of lesion-prone regions of rabbits, pigeons, and humans have higher affinity for apoB lipoproteins than nonlesion-prone segments.41 42 43 Furthermore, the amount of LDL accumulated in aortas of hypercholesterolemic swine correlates with alterations of GAGs of the intima in lesion-prone regions.44 In humans, this increased affinity is caused by longer CS chains in versican.45 The origin of PG alterations of lesion-prone sites may be smooth muscle cells that begin to proliferate under the action of growth factors.46 47 This concept is supported by data showing that versican produced by proliferating human arterial smooth muscle cells in culture has a higher affinity for human LDL at physiological ionic composition and pH than that synthesized by nonproliferating cells.48 The above findings could explain the increased retention time of LDL and the higher net accumulation of LDL and Lp(a) measured in vivo and in vitro in lesion-prone regions of rabbit aorta that precedes lesion development.49 50 51 52 53
Small amounts of other active PGs, as heparin secreted by mast cells in the intima54 55 and CSPG, and heparan, secreted by macrophages, could also be important in complex formation with LDL in a growing lesion.56 Moreover, macrophages from human cell lines secrete hypersulfated CSPG with longer CS chains than before differentiation. The CSPG has high affinity for lipoprotein lipase.57 Such PGs could also increase the retention of apoB lipoproteins in the pericellular space via a ternary complex of PG, lipoprotein lipase, and LDL or directly as PG and LDL associations. In these complexes, Arg- and Lys-rich segments of apoB-100 also appear to be involved.58 59 60 61 62 Goldberg63 recently reviewed this interesting development in detail.
| Structural Alterations of ApoB Lipoproteins Induced by PGs |
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LDL-PG complexes in different states of aggregation can be isolated from human and rabbit lesions.11 76 77 In vitro, depending on pH and Ca2+ concentration, irreversible aggregates of LDL can be formed with CSPG.78 Increased time of residence of apoB lipoproteins by complex formation with PGs may also augment the chance for hydrolytic modifications by enzymes that reside in extracellular matrix or that can be secreted by cells of the intima. One of the earliest lipid alterations detected in apoB lipoproteins isolated from lesions is a reduction of the content of linoleic acid of phospholipids11 and of phosphatidylcholine content compared with plasma LDL.12 13 This finding indicates that an sPLA2 acts on the LDL in intima. Recently, Sartipy et al79 found sPLA2 in the extracellular matrix of human lesions, and the isolated enzyme used LDL phospholipids as substrates. Moreover, human sPLA2 binds efficiently to C6S, which increases its activity toward LDL. Possibly, by colocalization of the enzyme and the lipoprotein, the CSPG of the intima may potentiate the degradation of LDL phospholipids.79 80 These results are interesting because lysolecithin produced by sPLA2 may contribute to monocyte recruiting,81 reduce the production of nitric oxide,82 and promote cell proliferation, all actions thought to be atherogenic.83 An additional enzyme that could contribute to the atherogenicity of the LDL trapped in the intima is sphingomyelinase. This enzyme, acting on LDL sphingomyelin, could increase the lipoprotein ceramide content and lead to its aggregation. Ceramides produced focally can be cell-proliferation modulators.84
| Cellular Consequences of the Interaction of LDL With PGs |
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LDL, density 1.019 to 1.063 g/mL, is a heterogeneous population of particles.87 The arterial versican has maximal affinity for dense LDL particles with the highest apoB-100 relative content, the lowest content of phospholipids and free cholesterol in their surface monolayer, and that are the most basic (higher pI). The denser subfractions with higher affinity for versican, once complexed and dissociated, also show higher uptake and degradation by human macrophages than larger, lighter subfractions.38 We believe that because a smaller surface area of the particle is covered by phospholipids and free cholesterol, positive, PG-binding regions of apoB-100 become more accessible for the association (Fig 1
). PGs possibly select these particles over the larger ones, and they may also be more susceptible to the GAG-induced structural alterations discussed above, resulting in a higher uptake by cells.38 Small, dense LDL is more vulnerable to oxidative modifications.88 This factor could also contribute to the increased sensitivity to oxidation observed in versican and GAG-selected LDL subfractions.72 74
Vijayagopal et al89 used a different model to study the effect of association of LDL with PGs. Complexes of apoB lipoprotein and CS-rich PGs, obtained from lesions or formed in vivo, were incubated directly with cells. This procedure may represent the interaction of cells with irreversible aggregates in the intima. Both types of complex are taken up efficiently by foam cells from rabbit lesions and human monocyte-derived macrophages. Scavenger receptors are mostly involved in the uptake that leads to appreciable cholesterol and cholesteryl ester accumulation. Although the electrophoretic mobility of the complex was not reported, they probably were more negative than native LDL. The same laboratory found that the apoB lipoproteinPG complex in cocultures of macrophages and smooth muscle cells also was taken up efficiently and induced appreciable cholesteryl accumulation in both cells.90
The GAG-binding regions of LDL appear to be included in the extended apoB/E receptorbinding region of apoB-100.31 37 Therefore, pericellular GAGs in the liver and other tissues may serve as a thin layer of high capacity and low affinity for accretion of LDL. From this layer, the high-affinity apoB/E receptor may more efficiently take up the lipoproteins.91 In the intima, which is made of a thick PG layer, the extracellular distribution will be favored and may be one of the reasons intimal thickening precedes atherosclerosis and no lesions are present in vessels without intima.92 Fig 2
presents a diagram of the hypothetical scenario suggested by the discussed findings. ApoB lipoproteins with high affinity for PGs increase their residence time by the formation of permanent or transient complexes. This provides the opportunity for structural, hydrolytic, and oxidative modifications of the lipoproteins with consequences for the cells of the intima. Such processes may have a physiological function for utilization and disposal of apoB lipoproteins by the arterial wall. However, when an excess of particles with high affinity for PGs circulates and enters the intima, the disposal system may be insufficient and gives opportunity for the initiation of the inflammatory and degenerative steps of atherogenesis.21
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| Clinical Relevance of ApoB Lipoprotein Interactions With Arterial PGs |
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| Summary |
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| Selected Abbreviations and Acronyms |
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| Acknowledgments |
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Received January 8, 1997; accepted January 22, 1997.
| References |
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