Skip to main content
NCBI home page
The American Journal of Pathology logoLink to The American Journal of Pathology
. 1992 Jan;140(1):179–191.

Ultrastructural localization of endogenous albumin in human aortic tissue by protein A-gold immunocytochemistry.

I Londoño 1, Y Leclerc 1, M Bendayan 1
PMCID: PMC1886237  PMID: 1731523

Abstract

The presence of endogenous plasma albumin in human aortas was demonstrated by immunocytochemical procedures. The protein A-gold approach, combining high resolution and specificity, was applied at the light and electron microscope levels to determine the in situ cellular and extracellular localization of albumin on tissue sections derived from normal and atherosclerotic human aortas. The distribution of albumin across the aortic wall interstitium was found to be uneven, with low to moderate staining intensities in the aortic subendothelial space, low intensities in the media, and high intensities around the vasa vasorum in the adventitia. Albumin was associated with collagen fibers as well as with the electron-dense material bordering the elastic laminae in both normal and pathologic tissues. Extracellular multilamellar structures were found to be characteristic of the necrotic areas of atherosclerotic aortas. These structures were intensely labeled for albumin, with the labeling being closely associated with the membranes. Numerous smooth muscle cell-derived and monocyte-derived foam cells were present in pathologic tissues, and some of their lysosomal compartments were labeled for albumin, suggesting an internalization and degradation of interstitial albumin by these cells.

Full text

PDF
179

Images in this article

183Figure 3
on p.183
183Figure 4
on p.183
182Figure 1
on p.182
182Figure 2
on p.182
185Figure 5
on p.185
185Figure 6
on p.185
186Figure 7
on p.186
187Figure 8
on p.187

Selected References

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

  1. Bell F. P., Adamson I. L., Schwartz C. J. Aortic endothelial permeability to albumin: focal and regional patterns of uptake and transmural distribution of 131I-albumin in the young pig. Exp Mol Pathol. 1974 Feb;20(1):57–68. doi: 10.1016/0014-4800(74)90043-4. [DOI] [PubMed] [Google Scholar]
  2. Bell F. P., Gallus A. S., Schwartz C. J. Focal and regional patterns of uptake and the transmural distribution of 131-I-fibrinogen in the pig aorta in vivo. Exp Mol Pathol. 1974 Apr;20(2):281–292. doi: 10.1016/0014-4800(74)90060-4. [DOI] [PubMed] [Google Scholar]
  3. Bocan T. M., Brown S. A., Guyton J. R. Human aortic fibrolipid lesions. Immunochemical localization of apolipoprotein B and apolipoprotein A. Arteriosclerosis. 1988 Sep-Oct;8(5):499–508. doi: 10.1161/01.atv.8.5.499. [DOI] [PubMed] [Google Scholar]
  4. Bratzler R. L., Chisolm G. M., Colton C. K., Smith K. A., Zilversmit D. B., Lees R. S. The distribution of labeled albumin across the rabbit thoracic aorta in vivo. Circ Res. 1977 Feb;40(2):182–190. doi: 10.1161/01.res.40.2.182. [DOI] [PubMed] [Google Scholar]
  5. Bundgaard M. Transport pathways in capillaries--in search of pores. Annu Rev Physiol. 1980;42:325–336. doi: 10.1146/annurev.ph.42.030180.001545. [DOI] [PubMed] [Google Scholar]
  6. Camejo G., Olofsson S. O., Lopez F., Carlsson P., Bondjers G. Identification of Apo B-100 segments mediating the interaction of low density lipoproteins with arterial proteoglycans. Arteriosclerosis. 1988 Jul-Aug;8(4):368–377. doi: 10.1161/01.atv.8.4.368. [DOI] [PubMed] [Google Scholar]
  7. Caro C. G., Lever M. J., Laver-Rudich Z., Meyer F., Liron N., Ebel W., Parker K. H., Winlove C. P. Net albumin transport across the wall of the rabbit common carotid artery perfused in situ. Atherosclerosis. 1980 Dec;37(4):497–511. doi: 10.1016/0021-9150(80)90057-x. [DOI] [PubMed] [Google Scholar]
  8. Chao F. F., Amende L. M., Blanchette-Mackie E. J., Skarlatos S. I., Gamble W., Resau J. H., Mergner W. T., Kruth H. S. Unesterified cholesterol-rich lipid particles in atherosclerotic lesions of human and rabbit aortas. Am J Pathol. 1988 Apr;131(1):73–83. [PMC free article] [PubMed] [Google Scholar]
  9. Coetzee J. H., Hattingh J., Mitchell G. Rat interstitial fluid proteins. Comp Biochem Physiol A Comp Physiol. 1982;72(1):173–178. doi: 10.1016/0300-9629(82)90028-7. [DOI] [PubMed] [Google Scholar]
  10. DUNCAN L. E., Jr, CORNFIELD J., BUCK K. Circulation of iodinated albumin through aortic and other connective tissues of the rabbit. Circ Res. 1958 May;6(3):244–255. doi: 10.1161/01.res.6.3.244. [DOI] [PubMed] [Google Scholar]
  11. Desjardins M., Bendayan M. Heterogenous distribution of type IV collagen, entactin, heparan sulfate proteoglycan, and laminin among renal basement membranes as demonstrated by quantitative immunocytochemistry. J Histochem Cytochem. 1989 Jun;37(6):885–897. doi: 10.1177/37.6.2723404. [DOI] [PubMed] [Google Scholar]
  12. Ehrenreich B. A., Cohn Z. A. The uptake and digestion of iodinated human serum albumin by macrophages in vitro. J Exp Med. 1967 Nov 1;126(5):941–958. doi: 10.1084/jem.126.5.941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fadnes H. O., Aukland K. Protein concentration and colloid osmotic pressure of interstitial fluid collected by the wick technique: analysis and evaluation of the method. Microvasc Res. 1977 Jul;14(1):11–25. doi: 10.1016/0026-2862(77)90137-6. [DOI] [PubMed] [Google Scholar]
  14. Fisher-Dzoga K., Jones R. M., Vesselinovitch D., Wissler R. W. Ultrastructural and immunohistochemical studies of primary cultures of aortic medial cells. Exp Mol Pathol. 1973 Apr;18(2):162–176. doi: 10.1016/0014-4800(73)90014-2. [DOI] [PubMed] [Google Scholar]
  15. Frank J. S., Fogelman A. M. Ultrastructure of the intima in WHHL and cholesterol-fed rabbit aortas prepared by ultra-rapid freezing and freeze-etching. J Lipid Res. 1989 Jul;30(7):967–978. [PubMed] [Google Scholar]
  16. Gerrity R. G., Cliff W. J. The aortic tunica intima in young and aging rats. Exp Mol Pathol. 1972 Jun;16(3):382–402. doi: 10.1016/0014-4800(72)90012-3. [DOI] [PubMed] [Google Scholar]
  17. Ghidoni J. J., O'Neal R. M. Recent advances in molecular pathology: a review ultrastructure of human atheroma. Exp Mol Pathol. 1967 Dec;7(3):378–400. doi: 10.1016/0014-4800(67)90049-4. [DOI] [PubMed] [Google Scholar]
  18. Ghinea N., Eskenasy M., Simionescu M., Simionescu N. Endothelial albumin binding proteins are membrane-associated components exposed on the cell surface. J Biol Chem. 1989 Mar 25;264(9):4755–4758. [PubMed] [Google Scholar]
  19. Ghitescu L., Fixman A., Simionescu M., Simionescu N. Specific binding sites for albumin restricted to plasmalemmal vesicles of continuous capillary endothelium: receptor-mediated transcytosis. J Cell Biol. 1986 Apr;102(4):1304–1311. doi: 10.1083/jcb.102.4.1304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ghitescu L., Galis Z., Simionescu M., Simionescu N. Differentiated uptake and transcytosis of albumin in successive vascular segments. J Submicrosc Cytol Pathol. 1988 Oct;20(4):657–669. [PubMed] [Google Scholar]
  21. Goldstein J. L., Brown M. S. The low-density lipoprotein pathway and its relation to atherosclerosis. Annu Rev Biochem. 1977;46:897–930. doi: 10.1146/annurev.bi.46.070177.004341. [DOI] [PubMed] [Google Scholar]
  22. Guyton J. R., Klemp K. F. The lipid-rich core region of human atherosclerotic fibrous plaques. Prevalence of small lipid droplets and vesicles by electron microscopy. Am J Pathol. 1989 Mar;134(3):705–717. [PMC free article] [PubMed] [Google Scholar]
  23. Hoff H. F., Heideman C. L., Gaubatz J. W., Scott D. W., Titus J. L., Gotto A. M., Jr Correlation of apolipoprotein B retention with the structure of atherosclerotic plaques from human aortas. Lab Invest. 1978 May;38(5):560–567. [PubMed] [Google Scholar]
  24. Holgate C. S., Jackson P., Cowen P. N., Bird C. C. Immunogold-silver staining: new method of immunostaining with enhanced sensitivity. J Histochem Cytochem. 1983 Jul;31(7):938–944. doi: 10.1177/31.7.6189883. [DOI] [PubMed] [Google Scholar]
  25. Hollander W., Colombo M. A., Kirkpatrick B., Paddock J. Soluble proteins in the human atherosclerotic plaque. With spectral reference to immunoglobulins, C3-complement component, alpha 1-antitrypsin and alpha 2-macroglobulin. Atherosclerosis. 1979 Dec;34(4):391–405. doi: 10.1016/0021-9150(79)90064-9. [DOI] [PubMed] [Google Scholar]
  26. Hollmann J., Schmidt A., von Bassewitz D. B., Buddecke E. Relationship of sulfated glycosaminoglycans and cholesterol content in normal and arteriosclerotic human aorta. Arteriosclerosis. 1989 Mar-Apr;9(2):154–158. doi: 10.1161/01.atv.9.2.154. [DOI] [PubMed] [Google Scholar]
  27. Hynes R. O., Yamada K. M. Fibronectins: multifunctional modular glycoproteins. J Cell Biol. 1982 Nov;95(2 Pt 1):369–377. doi: 10.1083/jcb.95.2.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hüttner I., Boutet M., More R. H. Studies on protein passage through arterial endothelium. I. Structural correlates of permeability in rat arterial endothelium. Lab Invest. 1973 Jun;28(6):672–677. [PubMed] [Google Scholar]
  29. Kao V. C., Wissler R. W. A study of the immunohistochemical localization of serum lipoproteins and other plasma proteins in human atherosclerotic lesions. Exp Mol Pathol. 1965 Oct;4(5):465–479. doi: 10.1016/0014-4800(65)90011-0. [DOI] [PubMed] [Google Scholar]
  30. Kilo C., Vogler N., Williamson J. R. Muscle capillary basement membrane changes related to aging and to diabetes mellitus. Diabetes. 1972 Aug;21(8):881–905. doi: 10.2337/diab.21.8.881. [DOI] [PubMed] [Google Scholar]
  31. Lever M. J., Jay M. T. Albumin and Cr-EDTA uptake by systemic arteries, veins, and pulmonary artery of rabbit. Arteriosclerosis. 1990 Jul-Aug;10(4):551–558. doi: 10.1161/01.atv.10.4.551. [DOI] [PubMed] [Google Scholar]
  32. Londoño I., Bendayan M. Distribution of endogenous albumin across the rat aortic wall as revealed by quantitative immunocytochemistry. Am J Anat. 1989 Dec;186(4):407–416. doi: 10.1002/aja.1001860410. [DOI] [PubMed] [Google Scholar]
  33. Londoño I., Bendayan M. Quantitative immunocytochemical studies of endogenous albumin in rat aortic endothelial and mesothelial cells. Biol Cell. 1990;69(3):161–169. doi: 10.1016/0248-4900(90)90342-z. [DOI] [PubMed] [Google Scholar]
  34. Mora R., Lupu F., Simionescu N. Prelesional events in atherogenesis. Colocalization of apolipoprotein B, unesterified cholesterol and extracellular phospholipid liposomes in the aorta of hyperlipidemic rabbit. Atherosclerosis. 1987 Oct;67(2-3):143–154. doi: 10.1016/0021-9150(87)90274-7. [DOI] [PubMed] [Google Scholar]
  35. Murata K., Motayama T., Kotake C. Collagen types in various layers of the human aorta and their changes with the atherosclerotic process. Atherosclerosis. 1986 Jun;60(3):251–262. doi: 10.1016/0021-9150(86)90172-3. [DOI] [PubMed] [Google Scholar]
  36. Packham M. A., Rowsell H. C., Jorgensen L., Mustard J. F. Localized protein accumulation in the wall of the aorta. Exp Mol Pathol. 1967 Oct;7(2):214–232. doi: 10.1016/0014-4800(67)90031-7. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Schnitzer J. E., Carley W. W., Palade G. E. Albumin interacts specifically with a 60-kDa microvascular endothelial glycoprotein. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6773–6777. doi: 10.1073/pnas.85.18.6773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Schwartz S. M., Benditt E. P. Studies on aortic intima. I. Structure and permeability of rat thoracic aortic intima. Am J Pathol. 1972 Feb;66(2):241–264. [PMC free article] [PubMed] [Google Scholar]
  40. Schwenke D. C., Carew T. E. Initiation of atherosclerotic lesions in cholesterol-fed rabbits. I. Focal increases in arterial LDL concentration precede development of fatty streak lesions. Arteriosclerosis. 1989 Nov-Dec;9(6):895–907. doi: 10.1161/01.atv.9.6.895. [DOI] [PubMed] [Google Scholar]
  41. 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 Sep;67(1):9–16. doi: 10.1016/0021-9150(87)90259-0. [DOI] [PubMed] [Google Scholar]
  42. Simionescu N., Vasile E., Lupu F., Popescu G., Simionescu M. Prelesional events in atherogenesis. Accumulation of extracellular cholesterol-rich liposomes in the arterial intima and cardiac valves of the hyperlipidemic rabbit. Am J Pathol. 1986 Apr;123(1):109–125. [PMC free article] [PubMed] [Google Scholar]
  43. Smith E. B., Staples E. M. Distribution of plasma proteins across the human aortic wall--barrier functions of endothelium and internal elastic lamina. Atherosclerosis. 1980 Dec;37(4):579–590. doi: 10.1016/0021-9150(80)90065-9. [DOI] [PubMed] [Google Scholar]
  44. Srinivasan S. R., Vijayagopal P., Dalferes E. R., Jr, Abbate B., Radhakrishnamurthy B., Berenson G. S. Low density lipoprotein retention by aortic tissue. Contribution of extracellular matrix. Atherosclerosis. 1986 Dec;62(3):201–208. doi: 10.1016/0021-9150(86)90094-8. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. Völker W., Schmidt A., Buddecke E. Cytochemical changes in a human arterial proteoglycan related to atherosclerosis. Atherosclerosis. 1989 Jun;77(2-3):117–130. doi: 10.1016/0021-9150(89)90073-7. [DOI] [PubMed] [Google Scholar]
  47. Walton K. W., Williamson N. Histological and immunofluorescent studies on the evolution of the human atheromatous plaque. J Atheroscler Res. 1968 Jul-Aug;8(4):599–624. doi: 10.1016/s0368-1319(68)80020-1. [DOI] [PubMed] [Google Scholar]
  48. Weinberg P. D. Application of fluorescence densitometry to the study of net albumin uptake by the rabbit aortic wall up- and downstream of intercostal ostia. Atherosclerosis. 1988 Nov;74(1-2):139–148. doi: 10.1016/0021-9150(88)90200-6. [DOI] [PubMed] [Google Scholar]
  49. Wight T. N. Cell biology of arterial proteoglycans. Arteriosclerosis. 1989 Jan-Feb;9(1):1–20. doi: 10.1161/01.atv.9.1.1. [DOI] [PubMed] [Google Scholar]
  50. Winlove C. P., Davis J., Baldwin A., Chabanel A. Effects of particle size and perfusate composition on the uptake of colloidal gold by the rabbit thoracic aorta perfused in situ. Atherosclerosis. 1982 Jul;44(1):99–111. doi: 10.1016/0021-9150(82)90056-9. [DOI] [PubMed] [Google Scholar]
  51. Winlove C. P., Parker K. H., Ewins A. R. The uptake of ions and neutral solutes by the artery and by artery wall preparations. Connect Tissue Res. 1988;18(2):83–93. doi: 10.3109/03008208809008061. [DOI] [PubMed] [Google Scholar]
  52. Woolf N., Pilkington T. R. The immunohistochemical demonstration of lipoproteins in vessel walls. J Pathol Bacteriol. 1965 Oct;90(2):459–463. doi: 10.1002/path.1700900213. [DOI] [PubMed] [Google Scholar]

Articles from The American Journal of Pathology are provided here courtesy of American Society for Investigative Pathology

RESOURCES