Artery Wall Interactions in Early Atherogenesis

  • Judith A. Berliner
  • Tripathi B. Rajavashisth
  • Mahamad Navab
  • Ali Andalibi
  • Susan Imes
  • Joy S. Frank
  • Mary C. Territo
  • Aldons J. Lusis
  • Alan M. Fogelman

Abstract

The early events in the development of the atherosclerotic lesion include lipoprotein entry, retention and modification in the artery wall, monocyte and lymphocyte recruitment into the subendothelial space, conversion of the monocytes into macrophage foam cells, and the migration of smooth muscle cells from the media into the subendothelial space where some become foam cells.1 In our laboratory we have considered these events to result from interactions between circulating lipoproteins and the cells and matrix of the artery wall. We have also considered the possibility that cell-cell interactions may have an important role in these events. In this chapter we will address lipoprotein transport, lipoprotein retention, monocyte recruitment, and conversion of monocytes into macrophages in the subendothelial space.

Keywords

Cholesterol Permeability Foam Heparin Fibril 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Ross, R., 1986, The pathogenesis of atherosclerosis—An update, N. Engl. J. Med. 314:488–500.PubMedCrossRefGoogle Scholar
  2. 2.
    Chobanian, A. V., Menzoian, J. O., Shipman, J., Heath, K., and Haudenschild, C. C., 1983, Effects of endothelial denudation and cholesterol feeding on in vivo transport of albumin, glucose, and water across rabbit carotid artery, Circ. Res. 53:805–814.PubMedCrossRefGoogle Scholar
  3. 3.
    Navab, M., Hough, G. P., Berliner, J. A., Frank, J. A., Fogelman, A. M., Haberland, M. E., and Edwards, P. A., 1986, Rabbit beta-migrating very low density lipoprotein increases endothelial macromolecular transport without altering electrical resistance, J. Clin. Invest. 78:389–397.PubMedCrossRefGoogle Scholar
  4. 4.
    Schwenke, D. C., and Carew, T. E., 1989, Initiation of atherosclerotic lesions in cholesterol-fed rabbits. I. Focal increases in arterial LDL concentration precede development of fatty streak lesions, Arteriosclerosis 9:895–907.PubMedCrossRefGoogle Scholar
  5. 5.
    Schwenke, D. C., and Carew, T. E., 1989, Initiation of atherosclerotic lesions in cholesterol-fed rabbits. II. Selective retention of LDL vs. selective increases in LDL permeability in susceptible sites of arteries, Arteriosclerosis 9:908–918.PubMedCrossRefGoogle Scholar
  6. 6.
    Wiklund, O., Carew, T. E., and Steinberg, D., 1984, Role of the low density lipoprotein receptor in penetration of low density lipoprotein into rabbit aortic wall, Arteriosclerosis 5:135–141.Google Scholar
  7. 7.
    Navab, M., Hough, G. P., Van Lenten, B. J., Berliner, J. A., and Fogelman, A. M., 1988, Low density lipoproteins transfer bacterial lipopolysaccharides across endothelial monolayers in a biologically active form, J. Clin. Invest. 81:601–605.PubMedCrossRefGoogle Scholar
  8. 8.
    Curran, R. G., and Crane, A. J., 1962, Mucopolysaccharides in the atheromatous aorta, J. Pathol. Bacteriol. 84:405–412.PubMedCrossRefGoogle Scholar
  9. 9.
    Hollander, W., 1976, Unified concept on the role of acid mucopolysaccharides and connective tissue proteins in the accumulation of lipids, lipoproteins and calcium in the atherosclerotic plaque, Exp. Mol. Pathol. 25:106–120.PubMedCrossRefGoogle Scholar
  10. 10.
    Iverius, P. H., 1972, The interaction between human plasma lipoprotein and connective tissue glycosamino-glycans, J. Biol. Chem. 247:2607–2613.PubMedGoogle Scholar
  11. 11.
    Srinivasan, S.R., Dolan, P., Radhakrishnamurthy, B., and Berenson, G. S., 1972, Isolation of lipoprotein-acid mucopolysaccharide complexes from fatty streaks of human aortas, Atherosclerosis 16:95–105.PubMedCrossRefGoogle Scholar
  12. 12.
    Srinivasan, S. R., Radhakrishnamurthy, B., and Berenson, G. S., 1975, Studies on the interaction of heparin with serum lipoproteins in the presence of Ca2+, Mg2+, and Mn2+, Arch. Biochem. Biophys. 170:334–342.PubMedCrossRefGoogle Scholar
  13. 13.
    Wight, T. N., and Ross, R., 1975, Proteoglycan in primate arteries, I. Ultrastructural localization and distribution in the intima, J. Cell Biol. 67:660–674.PubMedCrossRefGoogle Scholar
  14. 14.
    Wight, T. N., 1980, Vessel proteoglycans and thrombogenesis, in: Progress in Hemostasis and Thrombosis (T. H., Spaet, ed.), Grune & Stratton, New York, pp. 1–39.Google Scholar
  15. 15.
    Frank, J. S., and Fogelman, A. M., 1989, Ultrastructure of the intima in WHHL and cholesterol-fed rabbit aortas prepared by ultra-rapid freezing and freeze-etching, J. Lipid Res. 30:967–978.PubMedGoogle Scholar
  16. 16.
    Simionescu, N., Vasile, E., Lupu, F., Popescu, G., and Simionescu, M., 1986, Prelesional events in atherogenesis. Accumulation of extracellular cholesterol-rich liposomes in the arterial intima and cardiac valves of the hyperlipidemic rabbit, Am. J. Pathol. 123:109–125.PubMedGoogle Scholar
  17. 17.
    Mora, R., Lupu, F., and Simionescu, N., 1987, Prelesional events in atherogenesis. Colocalization of apolipoprotein B unesterified cholesterol and extracellular phospholipid liposomes in the aorta of hyperlipidemic rabbits, Arteriosclerosis 67:143–154.CrossRefGoogle Scholar
  18. 18.
    Goldstein, J. L., Ho, Y. K., Basu, S. K., and Brown, M. S., 1979, Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein producing massive cholesterol deposition, Proc. Natl. Acad. Sci. USA 76:333–337.PubMedCrossRefGoogle Scholar
  19. 19.
    Fogelman, A. M., Shechter, I., Seager, J., Hokom, M., Child, J. S., and Edwards, P. A., 1980, Malon-dialdehyde alteration of low-density lipoprotein leads to cholesteryl-ester accumulation in human monocyte macrophages, Proc. Natl. Acad. Sci. USA 77:2214–2218.PubMedCrossRefGoogle Scholar
  20. 20.
    Haberland, M. E., Fogelman, A. M., and Edwards, P. A., 1982, Specificity of receptor-mediated recognition of malondialdehyde-modified low density lipoproteins, Proc. Natl. Acad. Sci. USA 79:1712–1716.PubMedCrossRefGoogle Scholar
  21. 21.
    Havel, R. J., Kita, J., Kotite, L., Kane, J. P., Hamilton, R. L., Goldstein, J. L., and Brown, M. S., 1982, Concentration and composition of lipoproteins in blood plasma of the WHHL rabbit. An animal model of familial hypercholesterolemia, Arteriosclerosis 2:467–474.PubMedCrossRefGoogle Scholar
  22. 22.
    Mazzone, T., Lopez, C., and Bergstrasser, L., 1988, Modification of very low density lipoproteins leads to macrophage scavenger receptor uptake and cholesteryl ester deposition, Arteriosclerosis 7:191–196.Google Scholar
  23. 23.
    Haberland, M. E., Fong, D., and Cheng, L., 1988, Malondialdehyde-altered protein occurs in atheroma of Watanabe Heritable Hyperlipidemic rabbits, Science 241:215–218.PubMedCrossRefGoogle Scholar
  24. 24.
    Palinski, W., Rosenfeld, M. E., Yla-Herttuala, S., Gurtner, G. C., Socher, S. S., Butler, S. W., Parthasarathy, S., Carew, T. E., Steinberg, D., and Witztum, J. L., 1989, Low density lipoprotein undergoes oxidative modification in vivo, Proc. Natl. Acad. Sci. USA 86:1372–1376.PubMedCrossRefGoogle Scholar
  25. 25.
    Boyd, H. C., Gown, A.M., Wolfbauer, G., and Chait, A., 1989, Direct evidence for a protein recognized by a monoclonal antibody against oxidatively modified LDL in atherosclerotic lesions from a Watanabe Heritable Hyperlipidemic Rabbit, Am. J. Pathol. 135:815–826.PubMedGoogle Scholar
  26. 26.
    Hoff, H. F., Morel, D. W., Jurgens, G., Esterbauer, H., and Chisolm, G. M. III, 1987, Modification of LDL by 4-hydroxynonenal induces enhanced uptake by macrophages and cytotoxicity to proliferating fibroblasts, Arteriosclerosis 7:523a.Google Scholar
  27. 27.
    Suits, A. G., Chait, A., Aviram, M., and Heinecke, J. W., 1989, Phagocytosis of aggregated lipoprotein by macrophages: Low density lipoprotein receptor-dependent foam-cell formation, Proc. Natl. Acad. Sci. USA 86:2713–2717.PubMedCrossRefGoogle Scholar
  28. 28.
    Khoo, J. C., Miller, E., McLoughlin, P., and Steinberg, D., 1988, Enhanced macrophage uptake of low density lipoprotein after self aggregation, Arteriosclerosis 8:348–358.PubMedCrossRefGoogle Scholar
  29. 29.
    Wolfbauer, G., Glick, J. M., Minor, L. K., and Rothblat, G. H., 1986, Development of smooth muscle foam cell: Uptake of macrophage lipid inclusions, Proc. Natl. Acad. Sci. USA 83:7760–7764.PubMedCrossRefGoogle Scholar
  30. 30.
    Territo, M. C., Berliner, J. A., Almada, L., Ramirez, R., and Fogelman, A. M., 1989, ß-very low density lipoprotein pretreatment of endothelial monolayers increases monocyte adhesion, Arteriosclerosis 9:824–828.PubMedCrossRefGoogle Scholar
  31. 31.
    Morel, D. W., DiCorleto, P. E., and Chisolm, G. M., 1984, Endothelial and smooth muscle cells alter low density lipoprotein in vitro by free radical oxidation, Arteriosclerosis 4:357–364.PubMedCrossRefGoogle Scholar
  32. 32.
    Steinbrecher, U. S., Parthasarathy, S. P., Leake, D. S., Witztum, J. L., and Steinberg, D., 1984, Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids, Proc. Natl. Acad. Sci. USA 81:3883–3887.PubMedCrossRefGoogle Scholar
  33. 33.
    Heinecke, J. W., Rosen, H., and Chait, A., 1984, Iron and copper promote modification of LDL by human arterial smooth muscle cells, J. Clin. Invest. 74:1890–1894.PubMedCrossRefGoogle Scholar
  34. 34.
    Cathcart, M. K., Morel, D. W., and Chisolm, G. M., 1985, Monocytes and neutrophils oxidize low density lipoprotein making it cytotoxic, J. Leukocyte Biol. 38:341–350.PubMedGoogle Scholar
  35. 35.
    Steinberg, D., Parthasarathy, S. P., Carew, T. E., Khoo, J. C., and Witztum, J. L., 1989, Modifications of LDL that increase its atherogenicity, N. Engl. J. Med. 320:916–924.CrossRefGoogle Scholar
  36. 36.
    Kosugi, K., Morel, D. W., DiCorleto, P. E., and Chisolm, G. M., 1987, Toxicity of oxidized LDL to cultured fibroblasts is selective for S phase of the cell cycle, J. Cell. Physiol. 130:311–320.PubMedCrossRefGoogle Scholar
  37. 37.
    Berliner, J. A., Territo, M. C., Sevanian, A., Ramin, S., Kim, J. A., Bamshad, B., Esterson, M., and Fogelman, A. M., 1990, Minimally modified LDL stimulates monocyte endothelial interactions, J. Clin. Invest. 85:1260–1266.PubMedCrossRefGoogle Scholar
  38. 38.
    Quinn, M. T., Parthasarathy, S., Fong, L. G., and Steinberg, D., 1987, Oxidatively modified low density lipoproteins: A potential role in recruitment and retention of monocyte/macrophages during atherogenesis, Proc. Natl. Acad. Sci. USA 84:2995–2998.PubMedCrossRefGoogle Scholar
  39. 39.
    Lang, R. A., Metcalf, D., Cuthbertson, R. A., Lyons, I., Stanley, E., Kelso, A., Kannourakis, G., Williamson, D. J., Klintworth, G. K., Gonda, T. J., and Dunn, A. R., 1987, Transgenic mice expressing a hemopoietic growth factor gene (GM-CSF) develop accumulations of macrophages, blindness, and a fatal syndrome of tissue damage, Cell 51:675–686.PubMedCrossRefGoogle Scholar
  40. 40.
    Sieff, C.A., Niemeyer, C.M., and Faller, D. V., 1987, The production of hematopoietic growth factors by endothelial accessory cells, Blood Cells 13:65–74.PubMedGoogle Scholar
  41. 41.
    Segal, G. M., McCall, E., Stueve, T., and Bagby, G. C., Jr., 1987, Interleukin 1 stimulates endothelial cells to release multilineage human colony-stimulating activity, J. Immunol. 138:1722–1728.Google Scholar
  42. 42.
    Broudy, V. C., Kanshansky, K., Harlan, J. M., and Adamson, J. W., 1987, Interleukin 1 stimulates endothelial cells to produce granulocyte-macrophage colony-stimulating factor and granulocyte colony-stimulating factor, J. Immunol. 139:464–468.PubMedGoogle Scholar
  43. 43.
    Seelentag, W. K., Mermod, J. J., Montesano, R., and Vassalli, P., 1987, Additive effects of interleukin 1 and tumor necrosis factor-alpha on the accumulation of the three granulocyte and macrophage colony stimulating factor mRNAs in human endothelial cells, EMBO J. 6:2261–2265.PubMedGoogle Scholar
  44. 44.
    Griffin, J. D., Rambaldi, A., Vellenga, E., Young, D. C., Osapovicz, D., and Canistra, S. A., 1987, Secretion of interleukin-1 by myeloblasts leukemia cells in vitro induces endothelial cells to secrete colony stimulating factors, Blood 70:1218–1221.PubMedGoogle Scholar
  45. 45.
    Zsebom, M., Yuschenkoff, U. N., Schiffer, S., Chang, D., McCall, E., Dinarello, C. A., Brown, M. A., Altrock, B., and Bagby, G. C., Jr., 1988, Vascular endothelial cells and granulopoiesis: Interleukin-1 stimulates release of G-CSF and GM-CSF, Blood 71:99–103.Google Scholar
  46. 46.
    Malone, D. G., Pierce, J. H., Falko, J. P., and Metcalfe, D. D., 1988, Production of granulocyte-macrophage colony-stimulating factor by primary cultures of unstimulated rat microvascular endothelial cells, Blood 71:684–689.PubMedGoogle Scholar
  47. 47.
    Dainiak, N., Warren, H. B., Kreczko, Riordan, M. A., Feldman, I., Lawler, J., Cohen, A. M., and Davies, P. F., 1988, Acetylated lipoproteins impair erythroid growth factor release from endothelial cells, J. Clin. Invest. 81:834–843.PubMedCrossRefGoogle Scholar
  48. 48.
    Wang, J. M., Griffin, J. D., Rambaldi, A., Chen, Z. G., and Mantovani, A., 1988, Induction of monocyte migration by recombinant macrophage colony-stimulating factor, J. Immunol. 141:575–579.PubMedGoogle Scholar
  49. 49.
    Bussolino, F., Wang, J. M., Defilippi, P., Turrini, F., Sanavio, F., Edgell, C.-J. S., Aglietta, M., Arese, P., and Mantovani, A., 1989, Granulocyte- and granulocyte-macrophage-colony stimulating factors induce human endothelial cells to migrate and proliferate, Nature 337:471–473.PubMedCrossRefGoogle Scholar
  50. 50.
    Rajavashisth, T. B., Andalibi, A., Territo, M. C., Berliner, J. A., Navab, M., Fogelman, A. M., and Lusis, A. J., 1990, Modified low density lipoproteins induce endothelial cell expression of granulocyte and macrophage colony stimulating factors, Nature 344:254–257.PubMedCrossRefGoogle Scholar
  51. 51.
    Averill, L. E., Meagher, R. C., and Gerrity, R. G., 1989, Enhanced monocyte progenitor cell proliferation in bone marrow of hyperlipidemic swine, Am. J. Pathol. 135:369–377.PubMedGoogle Scholar
  52. 52.
    Navab, M., Hough, G. P., Stevenson, L. W., Drinkwater, D. C., Laks, H., and Fogelman, A. M., 1988, Monocyte migration into the subendothelial space of a co-culture of adult human aortic endothelial and smooth muscle cells, J. Clin. Invest. 82:1853–1863.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1992

Authors and Affiliations

  • Judith A. Berliner
    • 1
  • Tripathi B. Rajavashisth
    • 2
  • Mahamad Navab
    • 3
  • Ali Andalibi
    • 4
  • Susan Imes
    • 3
  • Joy S. Frank
    • 5
  • Mary C. Territo
    • 3
  • Aldons J. Lusis
    • 4
  • Alan M. Fogelman
    • 3
  1. 1.Department of PathologyUCLA School of MedicineLos AngelesUSA
  2. 2.Division of Medical GeneticsHarbor UCLA Medical CenterTorranceUSA
  3. 3.Department of MedicineUCLA School of MedicineLos AngelesUSA
  4. 4.Department of MicrobiologyUCLA School of MedicineLos AngelesUSA
  5. 5.Department of Medicine and PhysiologyUCLA School of MedicineLos AngelesUSA

Personalised recommendations