Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Protein synthesis and transport by the rat choroid plexus and ependyma

An autoradiographic study

  • 40 Accesses

  • 27 Citations

Summary

Light (LM-ARG) and electron microscope (EM-ARG) autoradiographs were prepared from immature rat choroid plexus and ependyma at 5, 10, 30, and 60 min and 16 h following intraperitoneal administration of [3H]- labeled amino acid mixtures. Intracellular protein synthesis and transport were ascertained in lateral and fourth ventricle choroid plexus epithelium by quantitative EM-ARG at the several post-injection intervals. ARG were also prepared from choroid plexuses cultured for one day, pulse labeled for one hour and reincubated for various periods in nonradioactive media. Significant labeling of both attached and free apical protrusions (blebs) was observed in both choroid plexus and ependyma in vivo and in choroid plexus in vitro. This phenomenon was interpreted as a physiologically significant mechanism for protein transport (apocrine secretion) by epithelia into the cerebrospinal fluid (CSF).

Zusammenfassung

Licht- (LM-ARG) und elektronenmikroskopische (EMARG) Autoradiographien des Plexus chorioideus und des Ependyms von jungen Ratten wurden nach der Injektion von Tritium-markierten Aminosäuren angefertigt. Die Ratten wurden in Zeitabständen von 5, 10, 30, 60 min und 16 h getötet. Intracelluläre Proteinsynthese und Transport wurden im Plexus chorioideus der lateralen und des vierten Ventrikels mit quantitativer Autoradiographie bestimmt. Autoradiographische Experimente wurden auch an kultiviertem Plexus chorioideus-Gewebe durchgeführt. Diese Serie wurde nach eintägigem Wachstum in vitro für 1 h mit 3H-Phenylalanin markiert, anschließend gewaschen und für weitere Zeitperioden kultiviert. Hohe Inkorporation der markierten Substanzen wurde in gestielten und freien “blebs” des Plexus chorioideus und des Ependyms in vivo und des Plexus chorioideus in vitro gefunden. Dieses Ergebnis wurde als ein physiologisch bedeutender Mechanismus des Protein-Transportes (apokrine Sekretion) von den Epithelzellen in den Liquor cerebrospinalis gedeutet.

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

References

  1. Agnew WF, Yuen TGH (1975) Electron microscope autoradiographic localization of [3H] proline and [3H] palmitic acid in the choroid plexus. Brain Res 93:343–348

  2. Agnew WF, Yuen TGH, Achtyl TR (1979) Ultrastructural observations suggesting apocrine secretion in the choroid plexus: a comparative study. Neurol Res (in publication)

  3. Agnew WF, Yuen TGH, Cheng JT, Alvarez RB (1978) Does apocrine secretion occur in the choroid plexus? Soc Neurosci Abstr 4:329

  4. Arregui A, Iversen LL (1978) Angiotensin-converting enzyme: Presence of high activity in choroid plexus of mammalian brain. Eur J Pharmacol 52:147–150

  5. Aumüller G, Adler G (1979) Experimental studies of apocrine secretion in the dorsal prostate epithelium of the rat. Cell Tissue Res 198:145–158

  6. Azzam NA, Choudhury SR, Donohue JM (1978) Changes in the surface fine structure of choroid plexus epithelium following chronic acetazolamide treatment. J Anat 127:333–342

  7. Becker NH, Sutton CH (1963) Pathologic features of the choroid plexus. 1. Cytochemical effects of hypervitaminosis A. Am J Pathol 43:1017–1025

  8. Bock E (1973) Nonplasma proteins in cerebrospinal fluid. Scand J Immunol I:119–124

  9. Booz KH (1975) Secretory phenomena at the ependyma of the third ventricle of the embryonic rat. Anat Embryol 147:143–157

  10. Brightman MW (1967) The intracerebral movement of proteins injected into blood and cerebrospinal fluid of mice. Progr Brain Res 29:19–37

  11. Caruthers JS, Lorenzo AV (1974) In vitro studies on the uptake and incorporation of natural amino acids in rabbit choroid plexus. Brain Res 73:35–50

  12. Clausen J (1961) Proteins in normal cerebrospinal fluid not found in serum. Proc Soc Exp Biol 107:170–172

  13. Collins P, Morriss GM (1975) Changes in the surface features of choroid plexus of the rat following the administration of acetazolamide and other drugs which affect CSF secretion. J Anat 120:571–579

  14. Davis DA, Milhorat TH (1975) The blood-brain barrier of the rat choroid plexus. Anat Rec 181:779–790

  15. Davis DA, Milhorat TH, Lloyd Jr BJ (1973) Fine structural localization of intravenously injected cytochrome C in the porcine choroid plexus. In: Arceneaux CJ (ed) Proceedings of the Electron Microscopy Society of America. Claitors Publishing Division, Baton Rouge

  16. Davson H (1967) Physiology of the cerebrospinal fluid. Davson H (ed) Little Brown and Co, Boston, Mass.

  17. Dohrmann GL (1970) The choroid plexus: A historical review. Brain Res 18:197–218

  18. Dohrmann GJ, Herdson PB (1969) Lobated nuclei in epithelial cells of the choroid plexus of young mice. J Ultrastruct Res 29:218–223

  19. Edvinsson L, Nielson KC, Owman Ch, West KA (1974) Adrenergic innervation of the mammalian choroid plexus. Am J Anat 139:299–308

  20. Feeney L, Wissig SL (1972) A biochemical and radioautographic analysis of protein secretion by thyroid lobes incubated in vitro. J Cell Biol 53:510–522

  21. Fisher RG, Copenhauer JH Jr (1959) The metabolic activity of the choroid plexus. J Neurosurg 16:2167–175

  22. Flickinger CJ (1974) Synthesis, intracellular transport, and release of secretory protein in the seminal vesicle of the rat, as studied by electron microscope radioautography. Anat Rec 180:407–426

  23. Gonzalez-Santander R (1979) Electron-microscopic study of the secretion of the ependymal cells in the domestic cat (ependymin-β cells). Acta Anat 103:266–277

  24. Hetzel W (1978) Ependyma and ependymal protrusions of the lateral ventricles of the rabbit brain. Cell Tissue Res 192:475–488

  25. Hochwald GM, Pepe AJ, Thorbecke GJ (1967) Trace proteins in biological fluids. IV. Physicochemical properties and sites of formation of γ-trace and β-trace proteins. Proc Soc Exp Biol Med 124:961–966

  26. Kaluza JS, Burstone MS, Klatzo I (1964) Enzyme histochemistry of the chick choroid plexus. Acta Neuropathol (Berl) 3:480–489

  27. Kobayashi H (1975) Absorption of cerebrospinal fluid by ependymal cells of median eminence. In: Knigge KM, Scott DE, Kobayashi H, Ishii G (eds) Brain Endocrine Interaction. II. The ventricular system in neuroendocrine mechanisms. S. Karger Basel AG

  28. Kumar K, Anand Kumar TC (1975) The habenular ependyma: A neuroendocrine component of the epithalamus in the rhesus monkey. In: Stumpf WE, Grant LD (eds) Anatomical Neuroendocrinology. S Karger, Basel

  29. Leonhardt H, Lindner E (1967) Marklose Nervenfasern im III. und IV. Ventrikel des Kaninchen- und Katzengehirns. Z Zellforsch 78:1–18

  30. Lettré H, Pawelatz N (1966) Probleme der elektronenmikroskopischen Autoradiographie. Naturwissenschaften 53:268–271

  31. Lindvall M, Edvinsson L, Owman Ch (1978) Sympathetic nervous control of the cerebral spinal fluid production from the choroid plexus. Science 201:176–178

  32. Link H, Zettervall O, Blennow G (1972) Individual cerebrospinal fluid (CSF) proteins in the evaluation of increased CSF total protein. J Neurol 203:119–132

  33. Lowenthal A, Noppe M, Ghevens J, Karcher D (1978) α-albumin (glial fibrillary acidic protein) in normal and pathological human brain and cerbrospinal fluid. J Neurol 219:87–91

  34. Maxwell DS, Pease DC (1956) The electron microscopy of the choroid plexus. J Biophys Biochem Cytol 2:467–476

  35. Meldolesi J (1974) Secretory mechanisms in pancreatic acinar cells. Role of the cytoplasmic membranes. In: Ceccarelli B, Clementi F, Meldolesi J (eds) Advances in Cytopharmacology. Raven Press, New York, Vol 2

  36. Milhorat TH, Davis DA, Hammock MK (1975) Localization of ouabain-sensitive Na-K-ATPase in frog, rabbit and rat choroid plexus. Brain Res 99:170–174

  37. Møllgård K, Saunders NR (1977) A possible transepithelial pathway via endoplasmic reticulum in foetal sheep choroid plexus. Proc R Soc Lond (Biol) 199:321–326

  38. Nathanson JA (1979) β-adrenergic-sensitive adenylate cyclase in secretory cells of choroid plexus. Science 204:843–844

  39. Nilsson K, Olsson J (1978) Analysis for cerebrospinal fluid proteins by isoelectric focusing on polyacrylamide gel: Methodological aspects and normal values, with special reference to the alkaline region. Clin Chem 24:1134–1139

  40. Nyland H, Matre R (1978) Fcγ receptors in human choroid plexus. Acta Pathol Microbiol Scand Sect C 86:141–143

  41. Olsson JE, Link H (1973) Distribution of serum proteins and beta-trace protein within the nervous system. J Neurochem 20:837–846

  42. Peters A (1974) The surface fine structure of the choroid plexus and ependymal lining of the rat lateral ventricle. J Neurocytol 3:99–108

  43. Peters T Jr, Ashley CA (1967) An artefact in radioautography due to binding of free acids to tissues by fixatives. J Cell Biol 33:53–60

  44. Quinton PM, Wright EM, Tormey J McD (1973) Localization of sodium pumps in the choroid plexus epithelium. J Cell Biol 58:724–730

  45. Rapoport SI, Pettigrew KD (1979) A heterogeneous, pore-vesicle membrane model for protein transfer from blood to cerebrospinal fluid. Microv Res 18:105–119

  46. Santolaya PC, Rodiguez-Echandia EL (1968) The surface of the choroid plexus cells under normal and experimental conditions. Z Zellforsch 92:43–51

  47. Schliep G, Felgenhauer K (1978) Serum-CSF protein gradients, the blood-CSF barrier and the local immuno response. J Neurol 218:77–96

  48. Scott DE, Krobisch-Dudley G (1975) Ultrastructural analysis of the mammalian median eminence. I. Morphological correlates of transependymal transport. In: Knigge KM, Scott DE, Kobayashi K, Ishii (eds) Brain-Endocrine Interaction II. The ventricular system in neuroendocrine mechanisms. Karger, Basel

  49. Scott DE, Krobisch-Dudley G, Knigge KM (1974) The ventricular system in neuroendocrine mechanisms. II. In vivo monoamine transport by ependyma of the median eminence. Cell Tissue Res 154:1–16

  50. Selinger Z, Sharoni Y, Schramm M (1974) Modification of the secretory granule during secretion in the rat parotid gland. In: Ceccarelli B, Clementi F, Meldolesi J (eds) Advances in Cytopharmacology. Raven Press, New York, Vol 2

  51. Shelton E, Mowczko WE (1978) Membrane blisters: A fixation artifact; a study in fixation for scanning electron microscopy. Scanning 1:166–173

  52. Simpson JF, Tourtellotte WW, Kokmen E, Parker JA, Itabashi HH (1969) Fluorescent protein tracing in multiple sclerosis brain tissue. Arch Neurol 20:373–377

  53. Stumpf WE, Hellreich MA, Aumüller G, Lamb JC, Sar M (1977) The collicular recess organ: Evidence for structural and secretory specialization of the ventricular lining in the collicular recess. Cell Tissue Res 184:29–44

  54. Tennyson VM, Pappas GD (1961) Electron microscope studies of the developing telencephalic choroid plexus in normal and hydrocephalie rabbits. In: Fields W, Desmond M (eds) Disorders of the Developing Nervous System. CC Thomas, Springfield

  55. Van Deurs B (1978a) Horseradish peroxidase uptake into the rat choroid plexus epithelium, with special reference to the lysosomal system. J Ultrastruct Res 62:155–167

  56. Van Deurs B (1978b) Microperoxidase uptake into the rat choroid plexus epithelium. J Ultrastruct Res 62:168–180

  57. Walsh RJ, Posner BI, Kopriwa BM, Brawer JR (1979) Prolactin binding sites in the rat brain. Science 201:1041–1042

  58. Weisner B (1977) Gleichzeitige Bestimmung von Immunoglobulin G and Albumin in Ventrikelliquor und Serum. Nervenarzt (Berlin) 48:684–687

  59. Yuen TGH, Agnew WF (1978) Ultrastructural alterations during choroid plexus incubations. Exp Neurol 60:96–115

  60. Yuen TGH, Agnew WF, Carregal EJA (1975) Lysosomal handling of tellurium by the choroid plexus following chronic administration: An ultrastructural study. Exp Neurol 47:213–228

  61. Young RW (1973) The role of the Golgi complex in sulfate metabolism. J Cell Biol 57:175–189

Download references

Author information

Correspondence to Dr. William F. Agnew.

Additional information

The authors thank Mr. J.T. Cheng for technical assistance, and Mrs. Dee Whiting for typing the manuscript

This study was supported in part by N.I.H. Research Grant NS 12906

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Agnew, W.F., Alvarez, R.B., Yuen, T.G.H. et al. Protein synthesis and transport by the rat choroid plexus and ependyma. Cell Tissue Res. 208, 261–281 (1980). https://doi.org/10.1007/BF00234876

Download citation

Key words

  • Choroid plexus
  • Ependyma
  • Apocrine secretion
  • Protein synthesis
  • Electron microscope autoradiography