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Studies on blood capillaries. I. General organization of blood capillaries in muscle.

The Journal of Cell Biology, 01 May 1968, 37(2):244-276
https://doi.org/10.1083/jcb.37.2.244 PMID: 5656394 PMCID: PMC2107413

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Abstract 

THE WALL OF THE BLOOD CAPILLARIES OF SKELETAL MUSCLES (DIAPHRAGM, TONGUE, HIND LEGS) AND MYOCARDIUM OF THE RAT, GUINEA PIG, AND HAMSTER CONSISTS OF THREE CONSECUTIVE LAYERS OR TUNICS: the endothelium (inner layer), the basement membrane with its associated pericytes (middle layer), and the adventitia (outer layer). The flattened cells of the endothelium have a characteristic, large population of cytoplasmic vesicles which, within the attenuated periphery of the cells, may attain a maximum frequency of 120/micro(2) of cell front and occupy approximately 18% of the cytoplasmic volume; these values decrease as the cells thicken toward the perikaryon. The vesicles are 650-750 A in over-all diameter and are bounded by typical unit membranes. They occur as single units or are fused to form short chains of two to three vesicles. Each configuration may lie entirely within the cytoplasm or open onto the cell surface. In the latter case, the unit membrane of the vesicle is continuous, layer by layer, with the plasmalemma. Chains of vesicles opening simultaneously on both the blood and tissue fronts of the endothelial tunic have not been observed either in sections or in a tridimensional reconstruction of a sector of endothelial cell cytoplasm. Adjacent endothelial cells are closely apposed to one another and appear to be joined over a large part of their margins, possibly over their entire perimeter, by narrow belts of membrane fusion (zonulae occludentes). Except for tongue capillaries, patent intercellular gaps are rare or absent. The middle layer is formed by a continuous basement membrane ( approximately 500 A thick) and by pericytes which lie in between leaflets of this membrane. The tips of the pericyte pseudopodia penetrate through the inner leaflet of the basement membrane and join the endothelium in maculae occludentes. The adventitia is a discontinuous layer comprising cellular (macrophages, fibroblasts, mast cells) and extracellular (fibrils, amorphous matrix) elements. The same general type of construction appears to be used along the entire length of the capillary.

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J Cell Biol. 1968 May 1; 37(2): 244–276.
PMCID: PMC2107413
PMID: 5656394

STUDIES ON BLOOD CAPILLARIES

I. General Organization of Blood Capillaries in Muscle
Romaine R. Bruns and George E. Palade
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Abstract

The wall of the blood capillaries of skeletal muscles (diaphragm, tongue, hind legs) and myocardium of the rat, guinea pig, and hamster consists of three consecutive layers or tunics: the endothelium (inner layer), the basement membrane with its associated pericytes (middle layer), and the adventitia (outer layer). The flattened cells of the endothelium have a characteristic, large population of cytoplasmic vesicles which, within the attenuated periphery of the cells, may attain a maximum frequency of 120/µ2 of cell front and occupy ~18% of the cytoplasmic volume; these values decrease as the cells thicken toward the perikaryon. The vesicles are 650–750 A in over-all diameter and are bounded by typical unit membranes. They occur as single units or are fused to form short chains of two to three vesicles. Each configuration may lie entirely within the cytoplasm or open onto the cell surface. In the latter case, the unit membrane of the vesicle is continuous, layer by layer, with the plasmalemma. Chains of vesicles opening simultaneously on both the blood and tissue fronts of the endothelial tunic have not been observed either in sections or in a tridimensional reconstruction of a sector of endothelial cell cytoplasm. Adjacent endothelial cells are closely apposed to one another and appear to be joined over a large part of their margins, possibly over their entire perimeter, by narrow belts of membrane fusion (zonulae occludentes). Except for tongue capillaries, patent intercellular gaps are rare or absent. The middle layer is formed by a continuous basement membrane (~500 A thick) and by pericytes which lie in between leaflets of this membrane. The tips of the pericyte pseudopodia penetrate through the inner leaflet of the basement membrane and join the endothelium in maculae occludentes. The adventitia is a discontinuous layer comprising cellular (macrophages, fibroblasts, mast cells) and extracellular (fibrils, amorphous matrix) elements. The same general type of construction appears to be used along the entire length of the capillary.

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Selected References

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  • BENNETT HS, LUFT JH, HAMPTON JC. Morphological classifications of vertebrate blood capillaries. Am J Physiol. 1959 Feb;196(2):381–390. [Abstract] [Google Scholar]
  • PALADE GE. Blood capillaries of the heart and other organs. Circulation. 1961 Aug;24:368–388. [Abstract] [Google Scholar]
  • Bruns RR, Palade GE. Studies on blood capillaries. II. Transport of ferritin molecules across the wall of muscle capillaries. J Cell Biol. 1968 May;37(2):277–299. [Europe PMC free article] [Abstract] [Google Scholar]
  • PALADE GE. A study of fixation for electron microscopy. J Exp Med. 1952 Mar;95(3):285–298. [Europe PMC free article] [Abstract] [Google Scholar]
  • Farquhar MG, Palade GE. Cell junctions in amphibian skin. J Cell Biol. 1965 Jul;26(1):263–291. [Europe PMC free article] [Abstract] [Google Scholar]
  • LUFT JH. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. [Europe PMC free article] [Abstract] [Google Scholar]
  • WATSON ML. The use of carbon films to support tissue sections for electron microscopy. J Biophys Biochem Cytol. 1955 Mar;1(2):183–184. [Europe PMC free article] [Abstract] [Google Scholar]
  • KARNOVSKY MJ. Simple methods for "staining with lead" at high pH in electron microscopy. J Biophys Biochem Cytol. 1961 Dec;11:729–732. [Europe PMC free article] [Abstract] [Google Scholar]
  • WATSON ML. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958 Jul 25;4(4):475–478. [Europe PMC free article] [Abstract] [Google Scholar]
  • WEIBEL ER, KNIGHT BW. A MORPHOMETRIC STUDY ON THE THICKNESS OF THE PULMONARY AIR-BLOOD BARRIER. J Cell Biol. 1964 Jun;21:367–396. [Europe PMC free article] [Abstract] [Google Scholar]
  • FLOREY HW, POOLE JC, MEEK GA. Endothelial cells and cement lines. J Pathol Bacteriol. 1959 Apr;77(2):625–636. [Abstract] [Google Scholar]
  • MUIR AR, PETERS A. Quintuple-layered membrane junctions at terminal bars between endothelial cells. J Cell Biol. 1962 Feb;12:443–448. [Europe PMC free article] [Abstract] [Google Scholar]
  • 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • DROCHMANS P. [Morphology of glycogen. Electron microscopic study of the negative stains of particulate glycogen]. J Ultrastruct Res. 1962 Apr;6:141–163. [Abstract] [Google Scholar]
  • SLAUTTERBACK DB. CYTOPLASMIC MICROTUBULES. I. HYDRA. J Cell Biol. 1963 Aug;18:367–388. [Europe PMC free article] [Abstract] [Google Scholar]
  • THEG DE. CYTOPLASMIC MICROTUBULES IN DIFFERENT ANIMAL CELLS. J Cell Biol. 1964 Nov;23:265–275. [Europe PMC free article] [Abstract] [Google Scholar]
  • HAMA K. On the existence of filamentous structures in endothelial cells of the amphibian capillary. Anat Rec. 1961 Mar;139:437–441. [Abstract] [Google Scholar]
  • MOORE DH, RUSKA H. The fine structure of capillaries and small arteries. J Biophys Biochem Cytol. 1957 May 25;3(3):457–462. [Europe PMC free article] [Abstract] [Google Scholar]
  • RHODIN JA. Fine structure of vascular walls in mammals with special reference to smooth muscle component. Physiol Rev Suppl. 1962 Jul;5:48–87. [Abstract] [Google Scholar]
  • RHODIN JA. The diaphragm of capillary endothelial fenestrations. J Ultrastruct Res. 1962 Apr;6:171–185. [Abstract] [Google Scholar]
  • Elfvin LG. The ultrastructure of the capillary fenestrae in the adrenal medulla of the rat. J Ultrastruct Res. 1965 Jun;12(5):687–704. [Abstract] [Google Scholar]
  • PORTER KR, PALADE GE. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J Biophys Biochem Cytol. 1957 Mar 25;3(2):269–300. [Europe PMC free article] [Abstract] [Google Scholar]
  • YAMADA E. The fine structure of the gall bladder epithelium of the mouse. J Biophys Biochem Cytol. 1955 Sep 25;1(5):445–458. [Europe PMC free article] [Abstract] [Google Scholar]
  • 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • ROTH TF, PORTER KR. YOLK PROTEIN UPTAKE IN THE OOCYTE OF THE MOSQUITO AEDES AEGYPTI. L. J Cell Biol. 1964 Feb;20:313–332. [Europe PMC free article] [Abstract] [Google Scholar]
  • ROSENBLUTH J, WISSIG SL. THE DISTRIBUTION OF EXOGENOUS FERRITIN IN TOAD SPINAL GANGLIA AND THE MECHANISM OF ITS UPTAKE BY NEURONS. J Cell Biol. 1964 Nov;23:307–325. [Europe PMC free article] [Abstract] [Google Scholar]
  • SCHOEFL GI. STUDIES ON INFLAMMATION. III. GROWING CAPILLARIES: THEIR STRUCTURE AND PERMEABILITY. Virchows Arch Pathol Anat Physiol Klin Med. 1963 Nov 8;337:97–141. [Abstract] [Google Scholar]
  • Rhodin JA. The ultrastructure of mammalian arterioles and precapillary sphincters. J Ultrastruct Res. 1967 Apr;18(1):181–223. [Abstract] [Google Scholar]
  • WATSON M. Observations on a granule associated with chromatin in the nuclei of cells of rat and mouse. J Cell Biol. 1962 Apr;13:162–167. [Europe PMC free article] [Abstract] [Google Scholar]
  • FARQUHAR MG, PALADE GE. Junctional complexes in various epithelia. J Cell Biol. 1963 May;17:375–412. [Europe PMC free article] [Abstract] [Google Scholar]
  • FAWCETT DW. Intercellular bridges. Exp Cell Res. 1961;Suppl 8:174–187. [Abstract] [Google Scholar]
  • FAWCETT DW. Physiologically significant specializations of the cell surface. Circulation. 1962 Nov;26:1105–1132. [Abstract] [Google Scholar]
  • KARRER HE. Electron microscopic study of the phagocytosis process in lung. J Biophys Biochem Cytol. 1960 Apr;7:357–366. [Europe PMC free article] [Abstract] [Google Scholar]
  • Cohn ZA, Hirsch JG, Fedorko ME. The in vitro differentiation of mononuclear phagocytes. IV. The ultrastructure of macrophage differentiation in the peritoneal cavity and in culture. J Exp Med. 1966 Apr 1;123(4):747–756. [Europe PMC free article] [Abstract] [Google Scholar]
  • ROSS R, BENDITT EP. Wound healing and collagen formation. I. Sequential changes in components of guinea pig skin wounds observed in the electron microscope. J Biophys Biochem Cytol. 1961 Dec;11:677–700. [Europe PMC free article] [Abstract] [Google Scholar]
  • MOVAT HZ, FERNANDO NV. The fine structure of connective tissue. I. The fibroblast. Exp Mol Pathol. 1962 Dec;1:509–534. [Abstract] [Google Scholar]
  • FERNANDO NV, MOVAT HZ. THE FINE STRUCTURE OF CONNECTIVE TISSUE. III. THE MAST CELL. Exp Mol Pathol. 1963 Oct;31:450–463. [Abstract] [Google Scholar]
  • HURLEY JV, XEROS N. Electron microscopic observations on the emigration of leucocytes. Aust J Exp Biol Med Sci. 1961 Dec;39:609–623. [Abstract] [Google Scholar]
  • FERNANDO NV, MOVAT HZ. THE FINE STRUCTURE OF THE TERMINAL VASCULAR BED. III. THE CAPILLARIES. Exp Mol Pathol. 1964 Apr;34:87–97. [Abstract] [Google Scholar]
  • ZAMBONI L, PEASE DC. The vascular bed of red bone marrow. J Ultrastruct Res. 1961 Mar;5:65–85. [Abstract] [Google Scholar]
  • SUTER ER, MAJNO G. ULTRASTRUCTURE OF THE JOINT CAPSULE IN THE RAT: PRESENCE OF TWO KINDS OF CAPILLARIES. Nature. 1964 May 30;202:920–921. [Abstract] [Google Scholar]
  • MAYNARD EA, SCHULTZ RL, PEASE DC. Electron microscopy of the vascular bed of rat cerebral cortex. Am J Anat. 1957 May;100(3):409–433. [Abstract] [Google Scholar]
  • MARCHESI VT, FLOREY HW. Electron micrographic observations on the emigration of leucocytes. Q J Exp Physiol Cogn Med Sci. 1960 Oct;45:343–348. [Abstract] [Google Scholar]
  • KARRER HE. The ultrastructure of mouse lung; general architecture of capillary and alveolar walls. J Biophys Biochem Cytol. 1956 May 25;2(3):241–252. [Europe PMC free article] [Abstract] [Google Scholar]
  • WOLFF J. [Contributions to the ultrastructure of the capillaries in the normal cerebral cortex]. Z Zellforsch Mikrosk Anat. 1963;60:409–431. [Abstract] [Google Scholar]
  • RENKIN EM. TRANSPORT OF LARGE MOLECULES ACROSS CAPILLARY WALLS. Physiologist. 1964 Feb;60:13–28. [Abstract] [Google Scholar]
  • TORMEY JM. DIFFERENCES IN MEMBRANE CONFIGURATION BETWEEN OSMIUM TETROXIDE-FIXED AND GLUTARALDEHYDE-FIXED CILIARY EPITHELIUM. J Cell Biol. 1964 Dec;23:658–664. [Europe PMC free article] [Abstract] [Google Scholar]
  • ROSENBLUTH J. Contrast between osmium-fixed and permanganate-fixed toad spinal ganglia. J Cell Biol. 1963 Jan;16:143–157. [Europe PMC free article] [Abstract] [Google Scholar]
  • Loewenstein WR. Permeability of membrane junctions. Ann N Y Acad Sci. 1966 Jul 14;137(2):441–472. [Abstract] [Google Scholar]
  • PAPPENHEIMER JR, RENKIN EM, BORRERO LM. Filtration, diffusion and molecular sieving through peripheral capillary membranes; a contribution to the pore theory of capillary permeability. Am J Physiol. 1951 Oct;167(1):13–46. [Abstract] [Google Scholar]
  • MAJNO G, PALADE GE. Studies on inflammation. 1. The effect of histamine and serotonin on vascular permeability: an electron microscopic study. J Biophys Biochem Cytol. 1961 Dec;11:571–605. [Europe PMC free article] [Abstract] [Google Scholar]
  • MAJNO G, PALADE GE, SCHOEFL GI. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • RHODIN J, DALHAMN T. Electron microscopy of collagen and elastin in lamina propria of the tracheal muscosa of rat. Exp Cell Res. 1955 Oct;9(2):371–375. [Abstract] [Google Scholar]
  • KARRER HE. An electron microscope study of the aorta in young and in aging mice. J Ultrastruct Res. 1961 Mar;5:1–27. [Abstract] [Google Scholar]
  • Kefalides NA, Winzler RJ. The chemistry of glomerular basement membrane and its relation to collagen. Biochemistry. 1966 Feb;5(2):702–713. [Abstract] [Google Scholar]
  • DISCHE RM, PAPPAS GD, GRAUER A, DISCHE Z. THE CARBOHYDRATE OF BASEMENT MEMBRANES OF HUMAN KIDNEY GLOMERULI. Biochem Biophys Res Commun. 1965 Jun 18;20:63–70. [Abstract] [Google Scholar]
  • MACHER E, VOGELL W. [Electron microscopic studies on the skin capillaries]. Dermatologica. 1962;124:110–128. [Abstract] [Google Scholar]
  • KUWABARA T, COGAN DG. Retinal vascular patterns. VI. Mural cells of the retinal capillaries. Arch Ophthalmol. 1963 Apr;69:492–502. [Abstract] [Google Scholar]
  • DEWEY MM, BARR L. A STUDY OF THE STRUCTURE AND DISTRIBUTION OF THE NEXUS. J Cell Biol. 1964 Dec;23:553–585. [Europe PMC free article] [Abstract] [Google Scholar]
  • BARR L, DEWEY MM, BERGER W. PROPAGATION OF ACTION POTENTIALS AND THE STRUCTURE OF THE NEXUS IN CARDIAC MUSCLE. J Gen Physiol. 1965 May;48:797–823. [Europe PMC free article] [Abstract] [Google Scholar]
  • BENNETT MV, ALJURE E, NAKAJIMA Y, PAPPAS GD. Electrotonic junctions between teleost spinal neurons: electrophysiology and ultrastructure. Science. 1963 Jul 19;141(3577):262–264. [Abstract] [Google Scholar]
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