Skip to content
BY-NC-ND 3.0 license Open Access Published by De Gruyter Open Access November 6, 2009

Collagen-bound LDL modifies endothelial cell adhesion to type V collagen: Implications for atherosclerosis

  • Stefan Lorkowski EMAIL logo , Jürgen Rauterberg , Bärbel Harrach-Ruprecht and David Troyer
From the journal Open Life Sciences

Abstract

Low density lipoprotein (LDL) is retained in the extracellular matrix of the arterial wall where it is considered to be atherogenic, but little is known about how cell adhesion to the matrix is affected by collagen-bound LDL. We tested the effect of native, oxidized and acetylated LDL reacted with adsorbed monomeric type I, III and V collagen on endothelial cell adhesion to collagen using a colorimetric adhesion assay. We found that none of the LDL species affected adhesion to type I and III collagen, but that collagen-bound native and acetylated LDL enhanced attachment to type V collagen, whereas bound oxidized LDL inhibited adhesion to this collagen. We therefore suggest that oxidized LDL associated with type V collagen in the arterial wall would favor de-endothelialization and contribute to atherogenesis and thrombosis.

[1] Hajjar D.P., Haberland M.E., Lipoprotein trafficking in vascular cells. Molecular Trojan horses and cellular saboteurs, J. Biol. Chem., 1997, 272, 22975–22978 http://dx.doi.org/10.1074/jbc.272.37.2297510.1074/jbc.272.37.22975Search in Google Scholar

[2] Chisolm G.M., Penn M.S., Oxidized Lipoproteins and Atherosclerosis, In: Fuster V., Ross R., Topol E.J., (Eds.), Atherosclerosis and Coronary Heart Disease, Lippincott Raven, Philadelphia, 1996 Search in Google Scholar

[3] Ross R., Cell biology of atherosclerosis, Annu. Rev. Physiol., 1995, 57, 791–804 http://dx.doi.org/10.1146/annurev.ph.57.030195.00404310.1146/annurev.ph.57.030195.004043Search in Google Scholar

[4] Thorne S.A., Abbot S.E., Winyard P.G., Blake D.R., Mills P.G., Extent of oxidative modification of low density lipoprotein determines the degree of cytotoxicity to human coronary artery cells, Heart, 1996, 75, 11–16 http://dx.doi.org/10.1136/hrt.75.1.1110.1136/hrt.75.1.11Search in Google Scholar

[5] Auerbach, B.J., Bisgaier, C.L., Wolle J., Saxena U., Oxidation of low density lipoproteins greatly enhances their association with lipoprotein lipase anchored to endothelial cell matrix, J. Biol. Chem., 1996, 271, 1329–1335 http://dx.doi.org/10.1074/jbc.271.3.132910.1074/jbc.271.3.1329Search in Google Scholar

[6] Edwards I.J., Goldberg I.J., Parks J.S., Xu H., Wagner W.D., Lipoprotein lipase enhances the interaction of low density lipoproteins with arteryderived extracellular matrix proteoglycans, J. Lipid Res., 1993, 34, 1155–1163 10.1016/S0022-2275(20)37703-8Search in Google Scholar

[7] Kaplan M., Aviram M., Oxidized LDL binding to a macrophage-secreted extracellular matrix, Biochem. Biophys. Res. Commun., 1997, 237, 271–276 http://dx.doi.org/10.1006/bbrc.1997.713010.1006/bbrc.1997.7130Search in Google Scholar

[8] Saxena U., Klein M.G., Vanni T.M., Goldberg I.J., Lipo-protein lipase increases low density lipoprotein retention by subendothelial cell matrix, J. Clin. Invest., 1992, 89, 373–380 http://dx.doi.org/10.1172/JCI11559510.1172/JCI115595Search in Google Scholar

[9] Tabas I., Li Y., Brocia R.W., Xu S.W., Swenson T.L., Williams K.J., Lipoprotein lipase and sphingomyelinase synergistically enhance the association of atherogenic lipoproteins with smooth muscle cells and extracellular matrix. A possible mechanism for low density lipoprotein and lipoprotein(a) retention and macrophage foam cell formation, J. Biol. Chem., 1993, 268, 20419–20432 10.1016/S0021-9258(20)80745-5Search in Google Scholar

[10] Pillarisetti S., Paka L., Obunike J.C., Berglund L., Goldberg I.J., Subendothelial retention of lipoprotein (a). Evidence that reduced heparan sulfate promotes lipoprotein binding to subendothelial matrix, J. Clin. Invest., 1997, 100, 867–874 http://dx.doi.org/10.1172/JCI11960210.1172/JCI119602Search in Google Scholar PubMed PubMed Central

[11] Pentikainen M.O., Oorni K., Lassila R., Kovanen P.T., The proteoglycan decorin links low density lipoproteins with collagen type I, J. Biol. Chem., 1997, 272, 7633–7638 http://dx.doi.org/10.1074/jbc.272.40.2528310.1074/jbc.272.40.25283Search in Google Scholar PubMed

[12] Hoover G.A., McCormick S., Kalant N., Interaction of native and cell-modified low density lipoprotein with collagen gel, Arteriosclerosis, 1988, 8, 525–534 10.1161/01.ATV.8.5.525Search in Google Scholar

[13] Kalant N., McCormick S., Parniak M.A., Effects of copper and histidine on oxidative modification of low density lipoprotein and its subsequent binding to collagen, Arterioscler. Thromb., 1991, 11, 1322–1329 10.1161/01.ATV.11.5.1322Search in Google Scholar

[14] Jimi S., Sakata N., Matunaga A., Takebayashi S., Low density lipoproteins bind more to type I and III collagens by negative charge-dependent mechanisms than to type IV and V collagens, Atherosclerosis, 1994, 107, 109–116 http://dx.doi.org/10.1016/0021-9150(94)90146-510.1016/0021-9150(94)90146-5Search in Google Scholar

[15] Greilberger J., Schmut O., Jurgens G., In vitro interactions of oxidatively modified LDL with type I, II, III, IV and V collagen, laminin, fibronectin, and poly-D-lysine, Arterioscler. Thromb. Vascular Biol., 1997, 17, 2721–2728 10.1161/01.ATV.17.11.2721Search in Google Scholar

[16] Takei A., Huang Y., Lopes-Virella M.F., Expression of adhesion molecules by human endothelial cells exposed to oxidized low density lipoprotein. Influences of degree of oxidation and location of oxidized LDL, Atherosclerosis, 2001, 154, 79–86 http://dx.doi.org/10.1016/S0021-9150(00)00465-210.1016/S0021-9150(00)00465-2Search in Google Scholar

[17] Rauterberg J., Allmann H., Henkel W., Fietzek P.P., Isolation and characterization of CNBr derived peptides of the alpha1 (III) chain of pepsinsolubilized calf skin collagen, Hoppe Seylers Z. Physiol. Chem., 1976, 357, 1401–1407 10.1515/bchm2.1976.357.2.1401Search in Google Scholar

[18] Rhodes R.K., Miller E.J., Physicochemical characterization and molecular organization of the collagen A and B chains, Biochemistry, 1978, 17, 3442–3448 http://dx.doi.org/10.1021/bi00610a00310.1021/bi00610a003Search in Google Scholar

[19] Kleinveld H.A., Hak-Lemmers H.L., Stalenhoef A.F., Demacker P.N., Improved measurement of lowdensity-lipoprotein susceptibility to copper-induced oxidation: application of a short procedure for isolating low-density lipoprotein, Clin. Chem., 1992, 38, 2066–2072 10.1093/clinchem/38.10.2066Search in Google Scholar

[20] Thomas C.E., Jackson R.L., Lipid hydroperoxide involvement in copper-dependent and independent oxidation of low density lipoproteins, J. Pharmacol. Exp. Ther., 1991, 256, 1182–1188 Search in Google Scholar

[21] Zhang M.Y., Lin R.C., Oxidative-modified and acetylated low-density lipoproteins differ in their effects on cholesterol synthesis and stimulate synthesis of apolipoprotein E in rat peritoneal macrophages by different mechanisms, Metabolism, 1994, 43, 1523–1530 http://dx.doi.org/10.1016/0026-0495(94)90011-610.1016/0026-0495(94)90011-6Search in Google Scholar

[22] Kueng W., Silber E., Eppenberger U., Quantification of cells cultured on 96-well plates, Anal. Biochem., 1989, 182, 16–19 http://dx.doi.org/10.1016/0003-2697(89)90710-010.1016/0003-2697(89)90710-0Search in Google Scholar

[23] De-Rijke Y.B., Biessen E.A., Vogelezang C.J., van-Berkel T.J., Binding characteristics of scavenger receptors on liver endothelial and Kupffer cells or modified low-density lipoproteins, Biochem. J., 1994, 304, 69–73 10.1042/bj3040069Search in Google Scholar

[24] Tanaka T., Nishikawa A., Tanaka Y., Nakamura H., Kodama T., Imanishi T., Doi T., Synthetic collagenlike domain derived from the macrophage scavenger receptor binds acetylated low-density lipoprotein in vitro, Protein Eng., 1996, 9, 307–313 http://dx.doi.org/10.1093/protein/9.3.30710.1093/protein/9.3.307Search in Google Scholar

[25] Lougheed M., Steinbrecher U.P., Mechanism of uptake of copper-oxidized low density lipoprotein in macrophages is dependent on its extent of oxidation, J. Biol. Chem., 1996, 271, 11798–11805 http://dx.doi.org/10.1074/jbc.271.20.1179810.1074/jbc.271.20.11798Search in Google Scholar

[26] Birk D.E., Fitch J.M., Babiarz J.P., Doane K.J., Linsenmayer T.F., Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter, J. Cell Sci., 1990, 95, 649–657 10.1242/jcs.95.4.649Search in Google Scholar

[27] Marchant J.K., Hahn R.A., Linsenmayer T.F., Birk D.E., Reduction of type V collagen using a dominant-negative strategy alters the regulation of fibrillogenesis and results in the loss of cornealspecific fibril morphology, J. Cell Biol., 1996, 135, 1415–1426 http://dx.doi.org/10.1083/jcb.135.5.141510.1083/jcb.135.5.1415Search in Google Scholar

[28] Hashimoto K., Hatai M., Yaoi Y., Inhibition of cell adhesion by type V collagen, Cell. Struct. Funct., 1991, 16, 391–397 http://dx.doi.org/10.1247/csf.16.39110.1247/csf.16.391Search in Google Scholar

[29] Saelman E.U., Nieuwenhuis H.K., Hese K.M., de-Groot P.G., Heijnen H.F., Sage E.H., et al., Platelet adhesion to collagen types I through VIII under conditions of stasis and flow is mediated by GPIa/IIa (alpha 2 beta 1-integrin), Blood, 1994, 83, 1244–1250 10.1182/blood.V83.5.1244.bloodjournal8351244Search in Google Scholar

[30] Sakata N., Jimi S., Takebayashi S., Marques M.A., Type V collagen represses the attachment, spread, and growth of porcine vascular smooth muscle cells in vitro, Exp. Mol. Pathol., 1992, 56, 20–36 http://dx.doi.org/10.1016/0014-4800(92)90020-C10.1016/0014-4800(92)90020-CSearch in Google Scholar

[31] Underwood P.A., Bean P.A., Whitelock J.M., Inhibition of endothelial cell adhesion and proliferation by extracellular matrix from vascular smooth muscle cells: role of type V collagen, Atherosclerosis, 1998, 141, 141–152 http://dx.doi.org/10.1016/S0021-9150(98)00164-610.1016/S0021-9150(98)00164-6Search in Google Scholar

[32] Ziats N.P., Anderson J.M., Human vascular endothelial cell attachment and growth inhibition by type V collagen, J. Vasc. Surg., 1993, 17, 710–718 http://dx.doi.org/10.1067/mva.1993.4073010.1067/mva.1993.40730Search in Google Scholar PubMed

[33] Murata K., Motoyama T., Collagen species in various sized human arteries and their changes with intimal proliferation, Artery, 1990, 17, 96–106 Search in Google Scholar

[34] Katsuda S., Okada Y., Minamoto T., Oda Y., Matsui Y., Nakanishi I., Collagens in human atherosclerosis. Immunohistochemical analysis using collagen typespecific antibodies, Arterioscler. Thromb., 1992, 12, 494–502 10.1161/01.ATV.12.4.494Search in Google Scholar

[35] Sage H., Pritzl P., Bornstein P., Characterization of cell matrix associated collagens synthesized by aortic endothelial cells in culture, Biochemistry, 1981, 20, 436–442 http://dx.doi.org/10.1021/bi00505a03210.1021/bi00505a032Search in Google Scholar

[36] Shekhonin B.V., Domogatsky S.P., Muzykantov V.R., Idelson G.L., Rukosuev V.S., Distribution of type I, III, IV and V collagen in normal and atherosclerotic human arterial wall: immunomorphological characteristics, Coll. Relat. Res., 1985, 5, 355–368 10.1016/S0174-173X(85)80024-8Search in Google Scholar

[37] Shekhonin B.V., Domogatsky S.P., Idelson G.L., Koteliansky V.E., Rukosuev V.S., Relative distribution of fibronectin and type I, III, IV, V collagens in normal and atherosclerotic intima of human arteries, Atherosclerosis, 1987, 67, 9–16 http://dx.doi.org/10.1016/0021-9150(87)90259-010.1016/0021-9150(87)90259-0Search in Google Scholar

[38] Van Zanten G.H., de Graaf S., Slootweg P.J., Heijnen H.F., Connolly T.M., de Groot P.G., Sixma J.J., Increased platelet deposition on atherosclerotic coronary arteries, J. Clin. Invest., 1994, 93, 615–632 http://dx.doi.org/10.1172/JCI11701410.1172/JCI117014Search in Google Scholar PubMed PubMed Central

[39] Virmani R., Kolodgie F.D., Burke A.P., Farb A., Schwartz S.M., Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions, Arterioscler. Thromb. Vasc. Biol., 2000, 20, 1262–1275 10.1161/01.ATV.20.5.1262Search in Google Scholar

Published Online: 2009-11-6
Published in Print: 2009-12-1

© 2009 Versita Warsaw

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Downloaded on 23.4.2024 from https://www.degruyter.com/document/doi/10.2478/s11535-009-0047-8/html
Scroll to top button