Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1975 Dec 1;67(3):863–885. doi: 10.1083/jcb.67.3.863

Segmental differentiations of cell junctions in the vascular endothelium. The microvasculature

PMCID: PMC2111645  PMID: 1202025

Abstract

Small vascular units consisting of an arteriole, its capillaries, and the emerging venule (ACV units) were identified in the rat omentum and mesentery. They were fixed in situ and processed for electron microscopy either as whole units or as dissected segments. Systematic examination of the latter (in thin sections, as well as in freeze- cleaved preparations) showed that the intercellular junctions of the vascular endothelium vary characteristically from one segment to another in the microvasculature. In arterioles, the endothelium has continuous and elaborate tight junctions with interpolated large gap junctions. The capillary endothelium is provided with tight junctions formed by either branching or staggered strands; gap junctions are absent at this level. The pericytic venules exhibit loosely organized endothelial junctions with discontinuous low-profile ridges and grooves, usually devoid of particles. No gap junctions were found in these vessels. The endothelium of muscular venules has the same type of junctions (discontinuous ridges and grooves of low profile); in addition, it displays isolated gap junctions of smaller size and lower frequency than in arterioles. The term communicating junction (macula communicans) is proposed as a substitute for gap junctions, since the latter is inappropriate, in general, and confusing in the special case of the vascular endothelium.

Full Text

The Full Text of this article is available as a PDF (9.6 MB).

Selected References

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

  1. Bruns R. R., Palade G. E. Studies on blood capillaries. I. General organization of blood capillaries in muscle. J Cell Biol. 1968 May;37(2):244–276. doi: 10.1083/jcb.37.2.244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Claude P., Goodenough D. A. Fracture faces of zonulae occludentes from "tight" and "leaky" epithelia. J Cell Biol. 1973 Aug;58(2):390–400. doi: 10.1083/jcb.58.2.390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Clementi F., Palade G. E. Intestinal capillaries. I. Permeability to peroxidase and ferritin. J Cell Biol. 1969 Apr;41(1):33–58. doi: 10.1083/jcb.41.1.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Connell C. J., Mercer K. L. Freeze-fracture appearance of the capillary endothelium in the cerebral cortex of mouse brain. Am J Anat. 1974 Aug;140(4):595–599. doi: 10.1002/aja.1001400412. [DOI] [PubMed] [Google Scholar]
  5. Drommer W. Feinstruktur der normalen Arteriolen und ihre Alterationen nach experimentallem Colitoxinschock im zentralen Nervensystem des Schweines. Acta Neuropathol. 1972;22(1):29–41. doi: 10.1007/BF00687548. [DOI] [PubMed] [Google Scholar]
  6. FARQUHAR M. G., PALADE G. E. Junctional complexes in various epithelia. J Cell Biol. 1963 May;17:375–412. doi: 10.1083/jcb.17.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fawcett D. W., Leak L. V., Heidger P. M., Jr Electron microscopic observations on the structural components of the blood-testis barrier. J Reprod Fertil Suppl. 1970;10:105–122. [PubMed] [Google Scholar]
  8. Friend D. S., Fawcett D. W. Membrane differentiations in freeze-fractured mammalian sperm. J Cell Biol. 1974 Nov;63(2 Pt 1):641–664. doi: 10.1083/jcb.63.2.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gilula N. B., Satir P. The ciliary necklace. A ciliary membrane specialization. J Cell Biol. 1972 May;53(2):494–509. doi: 10.1083/jcb.53.2.494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gore R. W. Mesenteric preparations for quantitative microcirculatory studies. Microvasc Res. 1973 May;5(3):368–375. doi: 10.1016/0026-2862(73)90052-6. [DOI] [PubMed] [Google Scholar]
  11. HAUSBERGER F. X., WIDELITZ M. M. Distribution of labeled erythrocytes in adipose tissue and muscle in the rat. Am J Physiol. 1963 Apr;204:649–652. doi: 10.1152/ajplegacy.1963.204.4.649. [DOI] [PubMed] [Google Scholar]
  12. Karnovsky M. J. The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J Cell Biol. 1967 Oct;35(1):213–236. doi: 10.1083/jcb.35.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. LANDIS E. M. HETEROPOROSITY OF THE CAPILLARY WALL AS INDICATED BY CINEMATOGRAPHIC ANALYSIS OF THE PASSAGE OF DYES. Ann N Y Acad Sci. 1964 Aug 27;116:765–773. doi: 10.1111/j.1749-6632.1964.tb52544.x. [DOI] [PubMed] [Google Scholar]
  14. Loewenstein W. R. Permeability of membrane junctions. Ann N Y Acad Sci. 1966 Jul 14;137(2):441–472. doi: 10.1111/j.1749-6632.1966.tb50175.x. [DOI] [PubMed] [Google Scholar]
  15. Lorber V., Rayns D. G. Cellular junctions in the tunicate heart. J Cell Sci. 1972 Jan;10(1):211–227. doi: 10.1242/jcs.10.1.211. [DOI] [PubMed] [Google Scholar]
  16. MAJNO G., PALADE G. E., SCHOEFL G. I. Studies on inflammation. II. The site of action of histamine and serotonin along the vascular tree: a topographic study. J Biophys Biochem Cytol. 1961 Dec;11:607–626. doi: 10.1083/jcb.11.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. MAYNARD E. A., SCHULTZ R. L., PEASE D. C. Electron microscopy of the vascular bed of rat cerebral cortex. Am J Anat. 1957 May;100(3):409–433. doi: 10.1002/aja.1001000306. [DOI] [PubMed] [Google Scholar]
  18. MUIR A. R., PETERS A. Quintuple-layered membrane junctions at terminal bars between endothelial cells. J Cell Biol. 1962 Feb;12:443–448. doi: 10.1083/jcb.12.2.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McNutt N. S., Weinstein R. S. Membrane ultrastructure at mammalian intercellular junctions. Prog Biophys Mol Biol. 1973;26:45–101. doi: 10.1016/0079-6107(73)90017-5. [DOI] [PubMed] [Google Scholar]
  20. Mohamed A. H., Waterhouse J. P., Friederici H. H. The fine structure of gingival terminal vascular bed. Microvasc Res. 1973 Sep;6(2):137–152. doi: 10.1016/0026-2862(73)90016-2. [DOI] [PubMed] [Google Scholar]
  21. Pietra G. G., Szidon J. P., Carpenter H. A., Fishman A. P. Bronchial venular leakage during endotoxin shock. Am J Pathol. 1974 Dec;77(3):387–406. [PMC free article] [PubMed] [Google Scholar]
  22. Plattner H., Miller F., Bachmann L. Membrane specializations in the form of regular membrane-to-membrane attachment sites in Paramecium. A correlated freeze-etching and ultrathin-sectioning analysis. J Cell Sci. 1973 Nov;13(3):687–719. doi: 10.1242/jcs.13.3.687. [DOI] [PubMed] [Google Scholar]
  23. Revel J. P., Karnovsky M. J. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol. 1967 Jun;33(3):C7–C12. doi: 10.1083/jcb.33.3.c7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rhodin J. A. The ultrastructure of mammalian arterioles and precapillary sphincters. J Ultrastruct Res. 1967 Apr;18(1):181–223. doi: 10.1016/s0022-5320(67)80239-9. [DOI] [PubMed] [Google Scholar]
  25. Rhodin J. A. Ultrastructure of mammalian venous capillaries, venules, and small collecting veins. J Ultrastruct Res. 1968 Dec;25(5):452–500. doi: 10.1016/s0022-5320(68)80098-x. [DOI] [PubMed] [Google Scholar]
  26. Satir B., Schooley C., Satir P. Membrane fusion in a model system. Mucocyst secretion in Tetrahymena. J Cell Biol. 1973 Jan;56(1):153–176. doi: 10.1083/jcb.56.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Simionescu M., Simionescu N., Palade G. E. Morphometric data on the endothelium of blood capillaries. J Cell Biol. 1974 Jan;60(1):128–152. doi: 10.1083/jcb.60.1.128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Simionescu N., Siminoescu M., Palade G. E. Permeability of muscle capillaries to small heme-peptides. Evidence for the existence of patent transendothelial channels. J Cell Biol. 1975 Mar;64(3):586–607. doi: 10.1083/jcb.64.3.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Simionescu N., Simionescu M., Palade G. E. Permeability of intestinal capillaries. Pathway followed by dextrans and glycogens. J Cell Biol. 1972 May;53(2):365–392. doi: 10.1083/jcb.53.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Simionescu N., Simionescu M., Palade G. E. Permeability of muscle capillaries to exogenous myoglobin. J Cell Biol. 1973 May;57(2):424–452. doi: 10.1083/jcb.57.2.424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Singer S. J., Nicolson G. L. The fluid mosaic model of the structure of cell membranes. Science. 1972 Feb 18;175(4023):720–731. doi: 10.1126/science.175.4023.720. [DOI] [PubMed] [Google Scholar]
  32. Staehelin L. A. Further observations on the fine structure of freeze-cleaved tight junctions. J Cell Sci. 1973 Nov;13(3):763–786. doi: 10.1242/jcs.13.3.763. [DOI] [PubMed] [Google Scholar]
  33. Staehelin L. A. Structure and function of intercellular junctions. Int Rev Cytol. 1974;39:191–283. doi: 10.1016/s0074-7696(08)60940-7. [DOI] [PubMed] [Google Scholar]
  34. TAKADA M. ELECTRON MICROSCOPIC OBSERVATIONS ON THE PASSAGE OF ELECTROLYTE SOLUTIONS AND TRYPAN BLUE FLUID THROUGH THE WALLS OF VENULES AND CAPILLARIES OF THE VENOUS SIDE. Nagoya Med J. 1963 Dec;9:113–123. [PubMed] [Google Scholar]
  35. Wade J. B., Karnovsky M. J. The structure of the zonula occludens. A single fibril model based on freeze-fracture. J Cell Biol. 1974 Jan;60(1):168–180. doi: 10.1083/jcb.60.1.168. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES