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Three-dimensional organization of the plasmalemmal vesicular system in directly frozen capillaries of the rete mirabile in the swim bladder of the eel

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Summary

Several recent studies comparing chemically fixed and cryofixed endothelium have indicated that glutaraldehyde fixation may result in increases in the population of “vesicles” in the cytoplasm. Other reports based on ultrathin serial-section reconstruction of chemically fixed endothelium have revealed that the vesicular system is comprised of interconnected membranous compartments, which are ultimately continuous with either cell surface but do not extend across the endothelial cell. In this study, we have investigated the three-dimensional organization of the vesicular system in directly frozen, freeze-substituted capillaries of the rete mirabile from the swim bladder of the eel, specifically using the same block of embedded capillaries in which frozen capillaries had previously been found to contain less “vesicles” than chemically fixed capillaries. The results show that essentially all vesicles remain inter-connected with each other and are part of two separate sets of invaginations from the luminal and abluminal cell surface like in chemically fixed tissue. Any increase in vesicle number resulting from glutaraldehyde fixation does not affect the overall three-dimensional organization of the vesicular system in these endothelial cells.

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References

  • Bridgman PC, Reese TS (1984) The structure of cytoplasm in directly frozen cultured cells. I. Filamentous meshworks and the cytoplasmic ground substance. J Cell Biol 99:1655–1668

    Google Scholar 

  • Buchanan R, Wagner RC, Andrews BS, Frøkjær-Jensen J (1988) Effect of section thickness on the morphological characterization of the vesicular system in endothelial cells. Microvasc Res (in press)

  • Bundgaard M (1987) Tubular invaginations in cerebral endothelium and their relation to smooth-surfaced cisternae in hagfish (Myxine glutinosa). Cell Tissue Res 249:359–365

    Google Scholar 

  • Bundgaard M, Frøkjær-Jensen J, Crone C (1979) Endothelial plasmalemmal vesicles as elements in a system of branching invaginations from the cell surface. Proc Natl Acad Sci USA 76:6439–6442

    Google Scholar 

  • Bundgaard M, Hagman P, Crone C (1983) The three-dimensional organization of plasmalemmal vesicular profiles in the endothelium of rat heart capillaries. Microvasc Res 25:358–368

    Google Scholar 

  • Casley-Smith JR (1981) Freeze-substitution observations on the endothelium, and the passage of ions. Microcirculation 1:79–109

    Google Scholar 

  • Frøkjær-Jensen J (1980) Three-dimensional organization of plasmalemmal vesicles in endothelial cells. An analysis by serial sectioning of frog mesenteric capillaries. J Ultrastruct Res 73:9–20

    Google Scholar 

  • Frøkjær-Jensen J (1983) The plasmalemmal vesicular system in capillary endothelium. Conventional electron microscopic (EM) thin sections compared with the picture arising from ultrathin (≈140 Å) serial sectioning. Prog Appl Microcirc 1:17–34

    Google Scholar 

  • Frøkjær-Jensen J (1984) The plasmalemmal vesicular system in striated muscle capillaries and in pericytes. Tissue Cell 16:31–42

    Google Scholar 

  • Frøkjær-Jensen J (1985) The continuous capillary. Structure and Function. Biol Skr Dan Vid Selsk 25:209–253

    Google Scholar 

  • Frøkjær-Jensen J, Reese TS (1985) Three-dimensional organization of the plasmalemmal vesicular system in directly frozen, freezesubstituted frog mesenteric capillaries. J Physiol (London) 371:84P [Abstract]

    Google Scholar 

  • Haraldsson B, Johansson BR (1985) Changes in transcapillary exchange induced by perfusion fixation with glutaraldehyde, followed by measurements of capillary filtration coefficient, diffusion capacity and albumin clearance. Acta Physiol Scand 124:99–106

    Google Scholar 

  • Heuser JE, Reese TS, Dennis MJ, Jan Y, Jan L, Evans L (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol 81:275–300

    Google Scholar 

  • Jennings MA, Florey L (1967) An investigation of some properties of endothelium related to capillary permeability. Proc R Soc Lond [Biol] 167:39–63

    Google Scholar 

  • Kobayashi S (1970) Ferritin labeling in the fixed muscle capillary. A doubt on the tracer-experiments as the basis for the vesicular transport theory. Arch Histol Jpn 32:81–86

    Google Scholar 

  • Mazzone RW, Kornblau SM (1981) Pinocytotic vesicles in the endothelium of rapidly frozen rabbit lung. Microvasc Res 21:193–211

    Google Scholar 

  • McGuire PG, Twietmeyer TA (1983) Morphology of rapidly frozen aortic endothelial cells. Glutaraldehyde fixation increases the number of caveolae. Circ Res 53:424–429

    Google Scholar 

  • Nagy Z, Pettigrew KD, Meiselman S, Brightman MW (1987) Cerebral vessels cryofixed after hyperosmosis or cold injury in normothermic and hypothermic frogs. Brain Res (in press)

  • Noguchi Y, Shibata Y, Yamamoto T (1987) Endothelial vesicular system in rapid-frozen muscle capillaries revealed by serial sectioning and deep etching. Anat Rec 217:355–360

    Google Scholar 

  • Palade GE (1953) Fine structure of blood capillaries. J Appl Phys 24:1424 [Abstract]

    Google Scholar 

  • Palade GE, Bruns RR (1968) Structural modulations of plasmalemmal vesicles. J Cell Biol 37:633–649

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–213

    Article  CAS  PubMed  Google Scholar 

  • Rippe B, Kamiya A, Folkow B (1979) Transcapillary passage of albumin, effects of tissue cooling and of increases in filtration and plasma colloid osmotic pressure. Acta Physiol Scand 105:171–187

    Google Scholar 

  • Rippe B, Haraldsson B (1986) Capillary permeability in rat hindquarters as determined by estimations of capillary reflection coefficients. Acta Physiol Scand 127:289–303

    Google Scholar 

  • Robinson JM, Hoover RL, Karnovsky MJ (1984) Vesicle (caveolae) number is reduced in cultured endothelial cells prepared for electron microscopy by rapid-freezing. J Cell Biol 99:287a [Abstract]

    Google Scholar 

  • Simionescu M, Simionescu N (1984) Ultrastructure of the microvascular wall: functional correlations. In: Renkin EM, Michel CC (eds) Handbook of Physiology vol IV, The Cardiovascular System. American Physiological Society, Washington, USA, pp 41–101

    Google Scholar 

  • Simionescu N, Simionescu M, Palade GE (1975) Permeability of muscle capillaries to small heme-peptides. Evidence for the existence of patent transendothelial channels. J Cell Biol 64:586–607

    Google Scholar 

  • Taylor AE, Granger DN (1984) Exchange of macromolecules across the circulation. In: Renkin EM, Michel CC (eds) Handbook of Physiology, vol IV, The Cardiovascular System. American Physiological Society, Washington, USA, pp 467–520

    Google Scholar 

  • Wagner RC, Andrews SB (1985) Ultrastructure of the vesicular system in rapidly frozen capillary endothelium of the rete mirabile. J Ultrastruct Res 90:172–182

    Google Scholar 

  • Wagner RC, Robinson CS (1984) High-voltage electron microscopy of capillary endothelial vesicles. Microvasc Res 28:197–205

    Google Scholar 

  • Wolff JR (1967) On the meaning of vesiculation in capillary endothelium. Angiologica 4:64–68

    Google Scholar 

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Frøkjær-Jensen, J., Wagner, R.C., Andrews, S.B. et al. Three-dimensional organization of the plasmalemmal vesicular system in directly frozen capillaries of the rete mirabile in the swim bladder of the eel. Cell Tissue Res. 254, 17–24 (1988). https://doi.org/10.1007/BF00220012

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