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J Cell Biol. 1963 May 1; 17(2): 375–412.
PMCID: PMC2106201



The epithelia of a number of glands and cavitary organs of the rat and guinea pig have been surveyed, and in all cases investigated, a characteristic tripartite junctional complex has been found between adjacent cells. Although the complex differs in precise arrangement from one organ to another, it has been regularly encountered in the mucosal epithelia of the stomach, intestine, gall bladder, uterus, and oviduct; in the glandular epithelia of the liver, pancreas, parotid, stomach, and thyroid; in the epithelia of pancreatic, hepatic, and salivary ducts; and finally, between the epithelial cells of the nephron (proximal and distal convolution, collecting ducts). The elements of the complex, identified as zonula occludens (tight junction), zonula adhaerens (intermediary junction), and macula adhaerens (desmosome), occupy a juxtaluminal position and succeed each other in the order given in an apical-basal direction. The zonula occludens (tight junction) is characterized by fusion of the adjacent cell membranes resulting in obliteration of the intercellular space over variable distances. Within the obliterated zone, the dense outer leaflets of the adjoining cell membranes converge to form a single intermediate line. A diffuse band of dense cytoplasmic material is often associated with this junction, but its development varies from one epithelium to another. The zonula adhaerens (intermediate junction) is characterized by the presence of an intercellular space (∼200 A) occupied by homogeneous, apparently amorphous material of low density; by strict parallelism of the adjoining cell membranes over distances of 0.2 to 0.5 µ; and by conspicuous bands of dense material located in the subjacent cytoplasmic matrix. The desmosome or macula adhaerens is also characterized by the presence of an intercellular space (∼240 A) which, in this case, contains a central disc of dense material; by discrete cytoplasmic plaques disposed parallel to the inner leaflet of each cell membrane; and by the presence of bundles of cytoplasmic fibrils converging on the plaques. The zonula occludens appears to form a continuous belt-like attachment, whereas the desmosome is a discontinuous, button-like structure. The zomula adhaerens is continuous in most epithelia but discontinuous in some. Observations made during experimental hemoglobinuria in rats showed that the hemoglobin, which undergoes enough concentration in the nephron lumina to act as an electron-opaque mass tracer, does not penetrate the intercellular spaces beyond the zonula occludens. Similar observations were made in pancreatic acini and ducts where discharged zymogen served as a mass tracer. Hence the tight junction is impervious to concentrated protein solutions and appears to function as a diffusion barrier or "seal." The desmosome and probably also the zonula adhaerens may represent intercellular attachment devices.

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Selected References

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  • FAWCETT DW. Intercellular bridges. Exp Cell Res. 1961;Suppl 8:174–187. [PubMed]
  • HAMA K. The fine structure of the desmosomes in frog mesothelium. J Biophys Biochem Cytol. 1960 Jun;7:575–578. [PMC free article] [PubMed]
  • WOOD RL. Intercellular attachment in the epithelium of Hydra as revealed by electron microscopy. J Biophys Biochem Cytol. 1959 Dec;6:343–352. [PMC free article] [PubMed]
  • PALADE GE, PORTER KR. Studies on the endoplasmic reticulum. I. Its identification in cells in situ. J Exp Med. 1954 Dec 1;100(6):641–656. [PMC free article] [PubMed]
  • BENNETT HS, LUFT JH, HAMPTON JC. Morphological classifications of vertebrate blood capillaries. Am J Physiol. 1959 Feb;196(2):381–390. [PubMed]
  • PEACHEY LD, RASMUSSEN H. Structure of the toad's urinary bladder as related to its physiology. J Biophys Biochem Cytol. 1961 Aug;10:529–553. [PMC free article] [PubMed]
  • MUIR AR, PETERS A. Quintuple-layered membrane junctions at terminal bars between endothelial cells. J Cell Biol. 1962 Feb;12:443–448. [PMC free article] [PubMed]
  • KAYE GI, PAPPAS GD. Studies on the cornea. I. The fine structure of the rabbit cornea and the uptake and transport of colloidal particles by the cornea in vivo. J Cell Biol. 1962 Mar;12:457–479. [PMC free article] [PubMed]
  • KAYE GI, PAPPAS GD, DONN A, MALLETT N. Studies on the cornea. II. The uptake and transport of colloidal particles by the living rabbit cornea in vitro. J Cell Biol. 1962 Mar;12:481–501. [PMC free article] [PubMed]
  • FARQUHAR MG, PALADE GE. Glomerular permeability. II. Ferritin transfer across the glomerular capillary wall in nephrotic rats. J Exp Med. 1961 Nov 1;114:699–716. [PMC free article] [PubMed]
  • PALAY SL, KARLIN LJ. An electron microscopic study of the intestinal villus. I. The fasting animal. J Biophys Biochem Cytol. 1959 May 25;5(3):363–372. [PMC free article] [PubMed]
  • FARQUHAR MG, WISSIG SL, PALADE GE. Glomerular permeability. I. Ferritin transfer across the normal glomerular capillary wall. J Exp Med. 1961 Jan 1;113:47–66. [PMC free article] [PubMed]
  • CAULFIELD JB. Effects of varying the vehicle for OsO4 in tissue fixation. J Biophys Biochem Cytol. 1957 Sep 25;3(5):827–830. [PMC free article] [PubMed]
  • LUFT JH. Permanganate; a new fixative for electron microscopy. J Biophys Biochem Cytol. 1956 Nov 25;2(6):799–802. [PMC free article] [PubMed]
  • LUFT JH. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. [PMC free article] [PubMed]
  • PARSONS DF. A simple method for obtaining increased contrast in araldite sections by using postfixation staining of tissues with potassium permanganate. J Biophys Biochem Cytol. 1961 Nov;11:492–497. [PMC free article] [PubMed]
  • WATSON ML. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958 Jul 25;4(4):475–478. [PMC free article] [PubMed]
  • WATSON ML. Reduction of heating artifacts in thin sections examined in the electron microscope. J Biophys Biochem Cytol. 1957 Nov 25;3(6):1017–1022. [PMC free article] [PubMed]
  • ROBERTSON JD. Ultrastructure of excitable membranes and the crayfish median-giant synapse. Ann N Y Acad Sci. 1961 Sep 6;94:339–389. [PubMed]
  • ROBERTSON JD. Structural alterations in nerve fibers produced by hypotonic and hypertonic solutions. J Biophys Biochem Cytol. 1958 Jul 25;4(4):349–364. [PMC free article] [PubMed]
  • PUCHTLER H, LEBLOND CP. Histochemical analysis of cell membranes and associated structures as seen in the intestinal epithelium. Am J Anat. 1958 Jan;102(1):1–31. [PubMed]
  • HORSTMANN E, KNOOP A. Elektronenmikroskopische Studien an der Epidermis. I. Rattenpfote. Z Zellforsch Mikrosk Anat. 1958;47(3):348–362. [PubMed]
  • KARRER HE. Cell interconnections in normal human cervical epithelium. J Biophys Biochem Cytol. 1960 Feb;7:181–184. [PMC free article] [PubMed]
  • MILLINGTON PF, FINEAN JB. Electron microscope studies of the structure of the microvilli on principal epithelial cells of rat jejunum after treatment in hypo- and hypertonic saline. J Cell Biol. 1962 Jul;14:125–139. [PMC free article] [PubMed]
  • RHODIN JA. The diaphragm of capillary endothelial fenestrations. J Ultrastruct Res. 1962 Apr;6:171–185. [PubMed]
  • TRUMP BF, BENDITT EP. Electron microscopic studies of human renal disease. Observations of normal visceral glomerular epithelium and its modification in disease. Lab Invest. 1962 Sep;11:753–781. [PubMed]
  • ROSENBLUTH J, PALAY SL. The fine structure of nerve cell bodies and their myelin sheaths in the eighth nerve ganglion of the goldfish. J Biophys Biochem Cytol. 1961 Apr;9:853–877. [PMC free article] [PubMed]
  • MOE H. The ultrastructure of Brunner's glands of the cat. J Ultrastruct Res. 1960 Oct;4:58–72. [PubMed]
  • KARRER HE. The striated musculature of blood vessels. II. Cell interconnections and cell surface. J Biophys Biochem Cytol. 1960 Sep;8:135–150. [PMC free article] [PubMed]
  • PETERS A. Plasma membrane contacts in the central nervous system. J Anat. 1962 Apr;96:237–248. [PMC free article] [PubMed]
  • DEVIS R, JAMES DW. Electron microscopic appearance of close relationships between adult guinea pig fibroblasts in tissue culture. Nature. 1962 May 19;194:695–696. [PubMed]
  • Dewey MM, Barr L. Intercellular Connection between Smooth Muscle Cells: the Nexus. Science. 1962 Aug 31;137(3531):670–672. [PubMed]
  • FAWCETT DW, SELBY CC. Observations on the fine structure of the turtle atrium. J Biophys Biochem Cytol. 1958 Jan 25;4(1):63–72. [PMC free article] [PubMed]
  • BUCK RC. The fine structure of endothelium of large arteries. J Biophys Biochem Cytol. 1958 Mar 25;4(2):187–190. [PMC free article] [PubMed]
  • WINDHAGER EE, WHITTEMBURY G, OKEN DE, SCHATZMANN HJ, SOLOMON AK. Single proximal tubules of the Necturus kidney. III. Dependence of H2O movement on NaCl concentration. Am J Physiol. 1959 Aug;197:313–318. [PubMed]
  • LEAF A. Some actions of neurohypophyseal hormones on a living membrane. J Gen Physiol. 1960 May;43:175–189. [PMC free article] [PubMed]
  • MERCER EH. An electron microscopic study of Amoeba proteus. Proc R Soc Lond B Biol Sci. 1959 Mar 17;150(939):216–232. [PubMed]
  • Steiner JW, Carruthers JS. Studies on the Fine Structure of the Terminal Branches of the Biliary Tree: I. The Morphology of Normal Bile Canaliculi, Bile Pre-ductules (Ducts of Hering) and Bile Ductules. Am J Pathol. 1961 Jun;38(6):639–661. [PMC free article] [PubMed]
  • MOVAT HZ, STEINER JW. Studies of nephrotoxic nephritis. I. The fine structure of the glomerulus of the dog. Am J Clin Pathol. 1961 Oct;36:289–305. [PubMed]

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