Skip to main content
Log in

Ultrastructural aspects of the choroid plexus epithelium as revealed by the rapid-freezing and deep-etching techniques

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

By use of rapid freezing with a nitrogen-cooled propane jet, differentiating epithelial cells of the choroid plexus can be studied without chemical and embedding procedures. The cytological features of the developing choroidal cells were investigated in chick embryos and three-week-old-chicks. After cryofixation, the material was fractured, deep-etched and rotary shadowed. Fractures of the Golgi apparatus reveal the particulate structure of the saccule membranes and show that the intracisternal surfaces are covered by particles which protrude into the intracisternal space. The inner membranes of mitochondrial cristae are characteristically covered by stalked particles; the intracristal space is collapsed. The endoplasmic reticulum possesses globular particles that occupy the width of the membrane, as well as granules and filament-like structures in its cisternae. The adherent ribosomes demonstrated by deep-etching consist of aggregated subunits. New aspects of the structure of the nuclear envelope and the pore complex are described. The circumference of the pore complex is formed by intramembranous aggregated particles in an octagonal symmetrical arrangement. The structure of the cilia and the ciliary necklace can be studied in their three-dimensional aspects, e.g., the structure of doublets and their relation to the cytomembrane. The junctional complexes of choroid epithelial cells differentiated both nexus and zonula occludens simultaneously. Tight junctions consist of isolated arrays of particles, which do not form fibrils in cryofixed material. Gap junctions are not always hexagonally arranged, are devoid of a crystalline form and occasionally show the presence of pits in the protoplasmic face.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aaronson RP, Blobel G (1974) On the attachment of the nuclear pore complex. J Cell Biol 62:746–754

    PubMed  Google Scholar 

  • Branton D (1966) Fracture faces of frozen membranes. Proc Natl Acad Sci USA 55:1048–1056

    PubMed  Google Scholar 

  • Chalcroft JP, Bullivant S (1970) An interpretation of liver cell membrane and junction structure based on observation of freeze-fracture replicas of both sides of the fracture. J Cell Biol 47:49–60

    PubMed  Google Scholar 

  • Dermietzel R, Meller K, Tetzlaff W, Waelsch M (1977) In vivo and in vitro formation of the junctional complex in choroid epithelium. A freeze-etching study. Cell Tissue Res 181:427–441

    PubMed  Google Scholar 

  • ElgsaeterA, Espevik T, Kopstad G (1980) Rapid freezing of freezeetch specimens. In: Bailey GW (ed) 38th Ann. Proceedings of the Electron Microscopy Society of America. San Francisco, California p 752–755

  • Espevik T, Elgsaeter A (1981) In situ liquid propane jet-freezing and freeze-etching of monolayer cell cultures. J Microsc 123:105–110

    PubMed  Google Scholar 

  • Farquhar MG, Palade GE (1981) The Golgi apparatus (complex) — (1954–1981) — from artifact to center stage. J Cell Biol 91:77s-103s

    PubMed  Google Scholar 

  • Fernandez-Moran H (1962) Cell-membrane ultrastructure. Low-temperature electron microscopy and X-ray diffraction studies of lipoprotein components in lamellar systems. Circulation 24 Suppl.: 1039–1074

    Google Scholar 

  • Fernandez-Moran H, Oda T, Blair PV, Green DE (1964) A macromolecular repeating unit of mitochondrial structure and function. J Cell Biol 22:63–100

    PubMed  Google Scholar 

  • Franke WW (1970) On the universality of nuclear pore complex structure. Z Zellforsch 105:405–429

    PubMed  Google Scholar 

  • Franke WW, Scheer U (1970) The ultrastructure of the nuclear envelope of amphibian oocytes: A reinvestigation. I. The mature oocyte. J Ultrastruct Res 30:288–316

    PubMed  Google Scholar 

  • Franke WW, Scheer U (1974) Structures and functions of the nuclear envelope. In: Busch H (ed) The cell nucleus, Vol 1 Academic Press New York-London p 219–347

    Google Scholar 

  • Franke WW, Scheer U, Krohne G, Jarasch E-D (1981) The nuclear envelope and the architecture of the nuclear periphery. J Cell Biol 91:39s-50s

    PubMed  Google Scholar 

  • Goodenough UW, Heuser JE (1982) Substructure of the outer dynein arm. J Cell Biol 95:798–815

    PubMed  Google Scholar 

  • Heuser JE (1977) Synaptic vesicle exocytosis revealed in quickfrozen frog neuromuscular junctions treated with 4-aminopyridine and given a single electrical shock. In: Cowan WM, Ferrendelli JA (eds) Approaches to the cell biology of neurons. Society for Neuroscience Bethesda, Maryland p 215–239

    Google Scholar 

  • Heuser JE, Kirschner MW (1980) Filament organization revealed in platinum replicas of freeze-dried cytoskeletons. J Cell Biol 86:212–234

    PubMed  Google Scholar 

  • Heuser JE, Salpeter SR (1979) Organization of acetylcholine receptors in quick-frozen, deep-etched, and rotary-replicated torpedo postsynaptic membrane. J Cell Biol 82:150–173

    PubMed  Google Scholar 

  • Heuser JE, Reese TS, Landis DMD (1974) Functional changes in frog neuromuscular junctions studied with freeze-fracture. J Neurocytol 3:109–131

    PubMed  Google Scholar 

  • Heuser JE, Reese TS, Landis DMD (1975) Preservation of synaptic structure by rapid freezing. Cold Spring Harbor Symp Quant Biol 40:17–24

    Google Scholar 

  • Hirokawa N (1982) The intramembrane structure of tight junctions: An experimental analysis of the single-fibril and two-fibril models using the quick-freeze method. J Ultrastruct Res 80:288–301

    PubMed  Google Scholar 

  • Hirokawa N, Heuser JE (1982a) Internal and external differentiations of the postsynaptic membrane at the neuromuscular junction. J Neurocytol 11:487–510

    PubMed  Google Scholar 

  • Hirokawa N, Heuser J (1982b) The inside and outside of gapjunction membranes visualized by deep etching. Cell 30:395–406

    PubMed  Google Scholar 

  • Hirokawa N, Lewis G, Tilney LG, Fujiwara K, Heuser JE (1982) Organization of actin, myosin, and intermediate filaments in the brush border of intestinal epithelial cells. J Cell Biol 94:425–443

    PubMed  Google Scholar 

  • Kartenbeck J, Zentgraf H, Scheer U, Franke WW (1971) The nuclear envelope in freeze-etching. Adv Anat Embryol Cell Biol 45:1–55

    Google Scholar 

  • Kreibich G, Ulrich BL, Sabatini DD (1978a) Proteins of rough microsomal membranes related to ribosome binding. I. Identification of ribophorins I and II, membrane proteins characteristic of rough microsomes. J Cell Biol 77:464–587

    PubMed  Google Scholar 

  • Kreibich G, Czako-Graham M, Grebenau R, Mok W, Rodriguez-Boulan E, Sabatini DD (1978b) Characterization of the ribosomal binding site in rat liver rough microsomes: ribophorins I and II, two integral membrane proteins related to ribosome binding. J Supramol Struct 8:279–302

    PubMed  Google Scholar 

  • Landis DMD, Reese TS (1983) Cytoplasmic organization in cerebellar dendritic spines. J Cell Biol 97:1169–1178

    PubMed  Google Scholar 

  • McIntyre JA, Gilula NB, Karnovsky MJ (1974) Cryoprotectantinduced redistribution of intramembranous particles in mouse lymphocytes. J Cell Biol 60:192–203

    PubMed  Google Scholar 

  • Margaritis LH, Elgsaeter A, Branton D (1977) Rotary replication for freeze-etching. J Cell Biol 72:47–56

    PubMed  Google Scholar 

  • Meller K (1983) Ultrastructural aspects of rapid-frozen, deepetched and rotary-shadowed synaptosomes. Cell Tissue Res 231:347–355

    PubMed  Google Scholar 

  • Meller K (1984) The ultrastructure of the developing inner and outer segments of the photoreceptors of chick embryo retina as revealed by the rapid-freezing and deep-etching techniques. Anat Embryol 169:141–150

    PubMed  Google Scholar 

  • Meller K, Wagner HH (1968a) Die Feinstruktur des Plexus chorioideus in Gewebekulturen. Z Zellforsch 86:98–110

    PubMed  Google Scholar 

  • Meller K, Wagner HH (1968b) Vergleichende elektronenmikroskopische Untersuchungen des Plexus chorioideus der Maus in vivo und in vitro. Z Zellforsch 91:507–518

    PubMed  Google Scholar 

  • Meller K, Wechsler W (1965) Elektronenmikroskopische Untersuchung der Entwicklung der telencephalen Plexus chorioides des Huhnes. Z Zellforsch 65:420–444

    PubMed  Google Scholar 

  • Mestres P, Meller K, Breipohl W (1973) Elektronenmikroskopische Befunde zum cell coat unter normalen und experimentellen Bedingungen. Verh Anat Ges 67:489–494

    Google Scholar 

  • Moor H (1971) Recent progress in the freeze-etching technique. Phil Trans Roy Soc Lond B 261:121–131

    Google Scholar 

  • Moor H, Kistler J, Müller M (1976) Freezing in a propane jet. Experientia 32:805

    Google Scholar 

  • Morre DJ, Vigil EL (1979) Membrane differentiation within Golgi apparatus of rat hepatocytes. J Ultrastruct Res 68:317–324

    PubMed  Google Scholar 

  • Ojakian GK, Kreibich G, Sabatini DD (1977) Mobility of ribosomes bound to microsomal membranes. A freeze-etch and thin-section electron microscope study of the structure and fluidity of the rough endoplasmic reticulum. J Cell Biol 72:530–551

    PubMed  Google Scholar 

  • Peracchia C (1980) Structural correlates of gap junction permeation. Int Rev Cytol 66:81–146

    PubMed  Google Scholar 

  • Pinto da Silva P, Kachar B (1980) Quick freezing vs. chemical fixation: capture and identification of membrane fusion intermediates. Cell Biol Int Rep 4:625–641

    PubMed  Google Scholar 

  • Pinto da Silva P, Kachar B (1982) On tight-junction structure. Cell 28:441–450

    PubMed  Google Scholar 

  • Rambourg A, Hernandez W, Leblond CP (1969) Detection of complex carbohydrates in the Golgi apparatus of rat cells. J Cell Biol 40:395–414

    PubMed  Google Scholar 

  • Rash JE (1983) The rapid-freeze technique in neurobiology. Trends Neurosci 6:208–212

    Google Scholar 

  • Raviola E, Goodenough DA, Raviola G (1980) Structure of rapidly frozen gap junctions. J Cell Biol 87:273–279

    PubMed  Google Scholar 

  • Roberts K, Northcote DH (1971) Ultrastructure of the nuclear envelope; structural aspects of the interphase nucleus of sycamore suspension culture cells. Microsc Acta 71:102–120

    PubMed  Google Scholar 

  • Roof DJ, Heuser JE (1982) Surfaces of rod photoreceptor disk membranes: Integral membrane components. J Cell Biol 95:487–500

    PubMed  Google Scholar 

  • Schnapp BJ, Reese TS (1982) Cytoplasmic structure in rapid-frozen axons. J Cell Biol 94:667–679

    PubMed  Google Scholar 

  • Staehelin LA (1973) Further observations on the fine structure of freeze-cleaved tight junctions. J Cell Sci 13:763–786

    PubMed  Google Scholar 

  • Staehelin LA (1974) Structure and function of intercellular junctions. Int Rev Cytol 39:191–283

    PubMed  Google Scholar 

  • Unwin PNT, Milligan RA (1982) A large particle associated with the perimeter of the nuclear pore complex. J Cell Biol 93:63–75

    PubMed  Google Scholar 

  • Usukura J, Yamada E (1981) Molecular oganization of the rod outer segment. A deep-etching study with rapid freezing using unfixed frog retina. Biomed Res 2:177–193

    Google Scholar 

  • Van Deurs B, Luft JH (1979) Effects of glutaraldehyde fixation on the structure of tight junctions. A quantitative freeze-fracture analysis. J Ultrastruct Res 68:160–172

    PubMed  Google Scholar 

  • Van Harreveld A, Crowell J (1964) Electron microscopy after rapid freezing on a metal surface and substitution fixation. Anat Rec 149:381–386

    PubMed  Google Scholar 

  • Wade JB, Karnovsky MJ (1974) The structure of the zonula occludens. A single fibril model based on freeze-fracture. J Cell Biol 60:168–180

    PubMed  Google Scholar 

  • Wartiovaara J, Branton D (1970) Visualization of ribosomes by freeze-etching. Exp Cell Res 61:403–406

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This work was supported by a grant from the Ministerium für Wissenschaft und Forschung des Landes Nordrhein-Westfalen (II B5-FA 7470). The author thanks E. Descher, R. Hardt and K. Donberg for their excellent assistance and C. Bloch for her great help in preparing this manuscript.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meller, K. Ultrastructural aspects of the choroid plexus epithelium as revealed by the rapid-freezing and deep-etching techniques. Cell Tissue Res. 239, 189–201 (1985). https://doi.org/10.1007/BF00214919

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00214919

Key words

Navigation