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. 1985 May;119(2):210–222.

Early atherogenesis in White Carneau pigeons. II. Ultrastructural and cytochemical observations.

W G Jerome, J C Lewis
PMCID: PMC1887902  PMID: 3993740

Abstract

The addition of cholesterol (0.5%) to the diet of White Carneau pigeons induces site specific, temporally predictable, atherosclerotic lesions. The earliest lesions, which occurred after 3 weeks, were small (less than 2500 sq mu in surface area) and were composed primarily of macrophage foam cells (94% of lesion volume). With a prolonged time on the diet the lesions expanded due to increases in the number and size of foam cells, increases in the amount of extracellular space, and influx of smooth muscle cells. Macrophage foam cells in advanced lesions composed 61% of the lesion volume, smooth muscle cells 25%, and extracellular space 14%. Concurrent with the alteration in the constituency of the lesion, redistribution of lipid within foam cells was noted. Lipid in small lesions was primarily cytoplasmic (88%), with the remaining 12% in acid-phosphatase-positive secondary lysosomes. In more advanced lesions, 34% of the lipid was cytoplastic and 66% was lysosomal. The changes in large lesions appeared to be a function of lesion age, because at the growing edge of large lesions both composition and lipid distribution resembled those of small early lesions.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams C. W., Bayliss O. B. Detection of macrophages in atherosclerotic lesions with cytochrome oxidase. Br J Exp Pathol. 1976 Feb;57(1):30–36. [PMC free article] [PubMed] [Google Scholar]
  2. Bass D. A., Lewis J. C., Szejda P., Cowley L., McCall C. E. Activation of lysosomal acid phosphatase of eosinophil leukocytes. Lab Invest. 1981 May;44(5):403–409. [PubMed] [Google Scholar]
  3. CLARKSON T. B., LOFLAND H. B. Effects of cholesterol-fat diets on pigeons susceptible and resistant to atherosclerosis. Circ Res. 1961 Jan;9:106–109. doi: 10.1161/01.res.9.1.106. [DOI] [PubMed] [Google Scholar]
  4. CLARKSON T. B., PRICHARD R. W., NETSKY M. G., LOFLAND H. B. Atherosclerosis in pigeons; its spontaneous occurrence and resemblance to human atherosclerosis. AMA Arch Pathol. 1959 Aug;68(2):143–147. [PubMed] [Google Scholar]
  5. Clarkson T. B., King J. S., Jr, Lofland H. B., Feldner M. A., Bullock B. C. Pathologic characteristics and composition of diet-aggravated atherosclerotic plaques during "regression". Exp Mol Pathol. 1973 Dec;19(3):267–283. doi: 10.1016/0014-4800(73)90059-2. [DOI] [PubMed] [Google Scholar]
  6. Faggiotto A., Ross R., Harker L. Studies of hypercholesterolemia in the nonhuman primate. I. Changes that lead to fatty streak formation. Arteriosclerosis. 1984 Jul-Aug;4(4):323–340. doi: 10.1161/01.atv.4.4.323. [DOI] [PubMed] [Google Scholar]
  7. Faggiotto A., Ross R. Studies of hypercholesterolemia in the nonhuman primate. II. Fatty streak conversion to fibrous plaque. Arteriosclerosis. 1984 Jul-Aug;4(4):341–356. doi: 10.1161/01.atv.4.4.341. [DOI] [PubMed] [Google Scholar]
  8. GEER J. C., McGILL H. C., Jr, STRONG J. P. The fine structure of human atherosclerotic lesions. Am J Pathol. 1961 Mar;38:263–287. [PMC free article] [PubMed] [Google Scholar]
  9. Gaton E., Wolman M. The role of smooth muscle cells and hematogenous macrophages in atheroma. J Pathol. 1977 Oct;123(2):123–128. doi: 10.1002/path.1711230208. [DOI] [PubMed] [Google Scholar]
  10. Gerrity R. G. The role of the monocyte in atherogenesis: I. Transition of blood-borne monocytes into foam cells in fatty lesions. Am J Pathol. 1981 May;103(2):181–190. [PMC free article] [PubMed] [Google Scholar]
  11. Hajjar D. P., Wight T. N., Smith S. C. Lipid accumulation and ultrastructural change within the aortic wall during early spontaneous atherogenesis. Am J Pathol. 1980 Sep;100(3):683–705. [PMC free article] [PubMed] [Google Scholar]
  12. Haley N. J., Shio H., Fowler S. Characterization of lipid-laden aortic cells from cholesterol-fed rabbits. I. Resolution of aortic cell populations by metrizamide density gradient centrifugation. Lab Invest. 1977 Sep;37(3):287–296. [PubMed] [Google Scholar]
  13. Hassler O. The origin of the cells constituting arterial intima thickening. An experimental autoradiographic study with the use of H3-thymidine. Lab Invest. 1970 Apr;22(4):286–293. [PubMed] [Google Scholar]
  14. Jerome W. G., Lewis J. C. Early atherogenesis in White Carneau pigeons. I. Leukocyte margination and endothelial alterations at the celiac bifurcation. Am J Pathol. 1984 Jul;116(1):56–68. [PMC free article] [PubMed] [Google Scholar]
  15. Jerome W. G., Lewis J. C., Taylor R. G., White M. S. Concurrent endothelial cell turnover and leukocyte margination in early atherosclerosis. Scan Electron Microsc. 1983;(Pt 3):1453–1459. [PubMed] [Google Scholar]
  16. Osborne-Pellegrin M. J., Weill D. "Spontaneous" endothelial injury in the rat caudal artery. Exp Mol Pathol. 1983 Aug;39(1):61–79. doi: 10.1016/0014-4800(83)90041-2. [DOI] [PubMed] [Google Scholar]
  17. PRICHARD R. W., CLARKSON T. B., GOODMAN H. O., LOFLAND H. B. AORTIC ATHEROSCLEROSIS IN PIGEONS AND ITS COMPLICATIONS. Arch Pathol. 1964 Mar;77:244–257. [PubMed] [Google Scholar]
  18. PRICHARD R. W., CLARKSON T. B., LOFLAND H. B., COODMAN H. O. PIGEON ATHEROSCLEROSIS. Am Heart J. 1964 May;67:715–717. doi: 10.1016/0002-8703(64)90348-5. [DOI] [PubMed] [Google Scholar]
  19. Peters T. J., De Duve C. Lysosomes of the arterial wall. II. Subcellular fractionation of aortic cells from rabbits with experimantal atheroma. Exp Mol Pathol. 1974 Apr;20(2):228–256. doi: 10.1016/0014-4800(74)90057-4. [DOI] [PubMed] [Google Scholar]
  20. Ross R., Glomset J. A. Atherosclerosis and the arterial smooth muscle cell: Proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science. 1973 Jun 29;180(4093):1332–1339. doi: 10.1126/science.180.4093.1332. [DOI] [PubMed] [Google Scholar]
  21. Ross R., Glomset J. A. The pathogenesis of atherosclerosis (second of two parts). N Engl J Med. 1976 Aug 19;295(8):420–425. doi: 10.1056/NEJM197608192950805. [DOI] [PubMed] [Google Scholar]
  22. Ross R., Wight T. N., Strandness E., Thiele B. Human atherosclerosis. I. Cell constitution and characteristics of advanced lesions of the superficial femoral artery. Am J Pathol. 1984 Jan;114(1):79–93. [PMC free article] [PubMed] [Google Scholar]
  23. Santerre R. F., Wight T. N., Smith S. C., Brannigan D. Spontaneous atherosclerosis in pigeons. A model system for studying metabolic parameters associated with atherogenesis. Am J Pathol. 1972 Apr;67(1):1–22. [PMC free article] [PubMed] [Google Scholar]
  24. Schaffner T., Taylor K., Bartucci E. J., Fischer-Dzoga K., Beeson J. H., Glagov S., Wissler R. W. Arterial foam cells with distinctive immunomorphologic and histochemical features of macrophages. Am J Pathol. 1980 Jul;100(1):57–80. [PMC free article] [PubMed] [Google Scholar]
  25. Shio H., Haley N. J., Fowler S. Characterization of lipid-laden aortic cells from cholesterol-fed rabbits. III. Intracellular localization of cholesterol and cholesteryl ester. Lab Invest. 1979 Aug;41(2):160–167. [PubMed] [Google Scholar]
  26. Stary H. C., Malinow M. R. Ultrastructure of experimental coronary artery atherosclerosis in cynomolgus macaques. A comparison with the lesions of other primates. Atherosclerosis. 1982 Jun;43(2-3):151–175. doi: 10.1016/0021-9150(82)90019-3. [DOI] [PubMed] [Google Scholar]
  27. Stefanovich V., Gore I. Cholesterol diet nd permeability of rabbit aorta. Exp Mol Pathol. 1971 Feb;14(1):20–29. doi: 10.1016/0014-4800(71)90049-9. [DOI] [PubMed] [Google Scholar]
  28. Stein O., Stein Y., Eisenberg S. A radioautographic study of the transport of 125 I-labeled serum lipoproteins in rat aorta. Z Zellforsch Mikrosk Anat. 1973 Mar 29;138(2):223–237. doi: 10.1007/BF00306609. [DOI] [PubMed] [Google Scholar]
  29. Still W. J. The topography of cholesterol-induced fatty streaks. Exp Mol Pathol. 1974 Jun;20(3):374–386. doi: 10.1016/0014-4800(74)90067-7. [DOI] [PubMed] [Google Scholar]
  30. Tesar G. E., Kottke B. A. Location and sequence of atherosclerotic plaque formation in white Carneau and show racer pigeons: reevaluation and redefinition. Arch Pathol Lab Med. 1978 Nov;102(11):581–586. [PubMed] [Google Scholar]
  31. Thomas W. A., Kim D. N., Lee K. T., Reiner J. M., Schmee J. Population dynamics of arterial cells during atherogenesis. XIII. Mitogenic and cytotoxic effects of a hyperlipidemic (HL) diet on cells in advanced lesions in the abdominal aortas of swine fed an HL diet for 270-345 days. Exp Mol Pathol. 1983 Dec;39(3):257–270. doi: 10.1016/0014-4800(83)90056-4. [DOI] [PubMed] [Google Scholar]
  32. Tracy R. E., Kissling G. E., Devaney K. O., Lopez C. R., Toca V. T., Gandia M. Spatial dispersion of foam cells in the human thoracic aorta. Lab Invest. 1983 Dec;49(6):693–701. [PubMed] [Google Scholar]
  33. Vos J., Aarnoudse M. W., Dijk F., Lamberts H. B. On the cellular origin and development of atheromatous plaques. A light and electron microscopic study of combined X-ray and hypercholesterolemia-induced atheromatosis in the carotid artery of the rabbit. Virchows Arch B Cell Pathol Incl Mol Pathol. 1983;43(1):1–16. doi: 10.1007/BF02932938. [DOI] [PubMed] [Google Scholar]
  34. Weibel E. R. Stereological principles for morphometry in electron microscopic cytology. Int Rev Cytol. 1969;26:235–302. doi: 10.1016/s0074-7696(08)61637-x. [DOI] [PubMed] [Google Scholar]
  35. Weibel E. R., Stäubli W., Gnägi H. R., Hess F. A. Correlated morphometric and biochemical studies on the liver cell. I. Morphometric model, stereologic methods, and normal morphometric data for rat liver. J Cell Biol. 1969 Jul;42(1):68–91. doi: 10.1083/jcb.42.1.68. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Werb Z., Cohn Z. A. Cholesterol metabolism in the macrophage. 3. Ingestion and intracellular fate of cholesterol and cholesterol esters. J Exp Med. 1972 Jan;135(1):21–44. doi: 10.1084/jem.135.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wolinsky H., Fowler S. Participation of lysosomes in atherosclerosis. N Engl J Med. 1978 Nov 23;299(21):1173–1178. doi: 10.1056/NEJM197811232992107. [DOI] [PubMed] [Google Scholar]

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