Cell and Tissue Research

, Volume 199, Issue 3, pp 415–429 | Cite as

The smooth endoplasmic reticulum in neurohypophysial axons of the rat: Possible involvement in transport, storage and release of neurosecretory material

  • G. Alonso
  • I. Assenmacher
Article
Accepted:

Summary

The intra-axonal organization of the smooth endoplasmic reticulum was studied in the neurohypophysis of rats during and after water deprivation. Parallel to conventional electron microscopy, the material was treated with a double impregnation staining technique specifically designed to contrast the intracellular membranous system. In conventionally stained ultrathin sections from severely dehydrated rats most axons appeared to be free of membranous organelles, whereas corresponding axons treated with the double-impregnation technique generally exhibited a highly developed system of smooth endoplasmic reticulum. In axonal endings, both techniques revealed a profusion of microvesicles in intimate relationship with tubular elements of the smooth endoplasmic reticulum. In short-term (12 h) rehydrated rats, a similarly developed system of smooth endoplasmic reticulum was still observed at all axonal levels with both procedures. After 24 to 48 h of rehydration the tubules of the smooth endoplasmic reticulum exhibited, in double impregnated material, numerous dilatations which resembled the adjacent neurosecretory granules. In conventionally stained ultrathin sections, an accumulation of electron dense material occurred within tubules of the smooth endoplasmic reticulum in the more proximal axonal segments, while in the more terminal segments, which contained numerous elongated granules, membrane continuity was frequently observed between newly formed granules and the smooth endoplasmic reticulum. After 7 days of rehydration the general pattern of the axonal smooth endoplasmic reticulum was comparable to that in untreated rats. These results are discussed in the light of a suggested involvement of the axonal smooth endoplasmic reticulum in the non-granular transport of neurosecretory material in connection with (1) storage in distally formed granules, and (2) release via microvesicles.

Key words

Hypothalamo-neurohypophysial system (rat) Axoplasmic transport Smooth endoplasmic reticulum Neurosecretory granules Microvesicles 
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References

  1. Alonso, G.: L'innervation catécholaminergique du système hypothalamo-posthypophysaire. Etude chez le Rat par radioautographie à haute résolution. C.R. Acad. Sci. [D] (Paris) 277, 2769–2771 (1973)Google Scholar
  2. Alonso, G., Assenmacher, I.: The smooth endoplasmic reticulum in neurosecretory axons of the rat neurohypophysis. Biol. Cell. 32, 203–206 (1978a)Google Scholar
  3. Alonso, G., Assenmacher, I.: Electron microscopic study of the orthograde axonal transport of horseradish peroxidase in the supraoptico-neurohypophysial tract of the rat. Cell Tissue Res. 194, 525–531 (1978b)Google Scholar
  4. Alonso, G., Assenmacher, I.: Sur l'origine des granules et microvésicules dans les axones neurosécrétoires. J. Physiol. (Paris) (1978c, in press)Google Scholar
  5. Alonso, G., Assenmacher, I.: Three-dimensional organization of the endoplasmic reticulum in supraoptic neurons of the rat. Ultrastructural functional correlation. Brain Res. (1979, in press)Google Scholar
  6. Boudier, J.A.: Formation et évolution des vacuoles autophagiques dans les axones neurosécréteurs et leurs terminaisons chez le Rat. Biol. Cell. 31, 45–50 (1978)Google Scholar
  7. Boudier, J.A., Picard, D.: Granulolysis in neurosecretory neurons of the rat supraoptico- posthypophysial system. Cell. Tissue Res. 172, 39–58 (1976)Google Scholar
  8. Boudier, J.L., Boudier, J.A., Picard, D.: Ultrastructure du lobe postérieur de l'hypophyse du Rat et ses modifications au cours de l'excrétion de vasopressine. Z. Zellforsch. 108, 357–379 (1970)Google Scholar
  9. Boudier, J.A., Cau, P., Massacrier, A., Boudier, J.L.: Approche morphométrique de la distribution du matériel hormonal dans les axones de la posthypophyse du Rat. J. Physiol. (Paris) (1978, in press)Google Scholar
  10. Douglas, W.W., Nagasawa, J., Schulz, R.A.: Electron microscopic studies on the mechanism of secretion of posterior pituitary hormones and significance of microvesicles (synaptic vesicles). In: Subcellular organization and function of endocrine tissues. Heller and Lederis, eds., pp. 353–378. New York-Cambridge University Press 1971Google Scholar
  11. Droz, B., Boyenwal, J.: Le réticulum endoplasmique des axones: son rôle probable dans le transport axoplasmique des phospholipides membranaires. J. Microsc. Biol. Cell. 23, 45–46a (1975)Google Scholar
  12. Droz, B., Koenig, H.L., Rambourg, A.: Transport intracytoplasmique de macromolécules et réticulum endoplasmique lisse: cas du flux axonal rapide. J. Microsc. 20, 45a (1974)Google Scholar
  13. Droz, B., Rambourg, A., Koenig, H.L.: The smooth endoplasmic reticulum: structure and role in the renewal of axonal membrane and synaptic vesicles by fast axonal transport. Brain Res. 93, 1–13 (1975)Google Scholar
  14. Gainer, H., Sarne, Y., Brownstein, M.J.: Biosynthesis and axonal transport of rat neurohypophysial proteins and peptides. J. Cell. Biol. 73, 366–381 (1977)Google Scholar
  15. Jones, C.W., Pickering, B.T.: Comparison of the effects of water deprivation and sodium chloride imbibition on the hormone content of the neurohypophysis of rat. J. Physiol. (Lond.) 203, 449–458 (1969)Google Scholar
  16. Kalimo, H.: Ultrastructural studies of the hypothalamic neurosecretory neurons of the rat. III. Paraventricular and supraoptic neurons during lactation and dehydration. Cell Tissue Res. 163, 151–168 (1975)Google Scholar
  17. Kekki, M., Attila, U., Talanti, S.: The kinetics of 35S-labelled cysteine in the hypothalamicneurohypophyseal neurosecretory system of the dehydrated rat. Cell Tissue Res. 158, 439–450 (1975)Google Scholar
  18. Krisch, B.: Different populations of granules and their distinction in the hypothalamoneurohypophysial tract of the rat under various experimental conditions. II. The median eminence. Cell Tissue Res. 160, 231–261 (1975)Google Scholar
  19. Lavail, M.W., Lavail, J.H.: Retrograde intra-axonal transport of horseradish peroxidase in retinal ganglion cells of the chick. Brain. Res. 85, 273–280 (1975)Google Scholar
  20. Livingston, A.: Morphology of the perivascular regions of the rat neural lobe in relation to hormone release. Cell Tissue Res. 159, 551–561 (1975)Google Scholar
  21. Miller, M., Moses, A.M.: Radioimmunoassay of vasopressin with a comparison of immunological and biological activity in the rat posterior pituitary. Endocrinology 84, 557–562 (1969)Google Scholar
  22. Moses, A.M., Miller, M.: Accumulation and release of pituitary vasopressin in rats heterozygous for hypothalamic diabetes insipidus. Endocrinology 86, 34–41 (1970)Google Scholar
  23. Nagasawa, J., Douglas, W.W., Schulz, R.A.: Micropinocytocic origin of coated and smooth microvesicles (“synaptic vesicles”) in neurosecretory terminals of posterior pituitary glands demonstrated by incorporation of horseradish peroxidase. Nature 232, 341–342 (1971)Google Scholar
  24. Norström, A., Sjöstrand, J.: Effect of salt loading, thirst and water loading on transport and turn-over of neurohypophysial proteins of the rat. J. Endocrinol. 52, 87–105 (1972)Google Scholar
  25. Pilgrim, C.: Morphologische und funktionelle Untersuchungen zur Neurosekretbildung. Enzymhistochemische, autoradiographische und elektronenmikroskopische Beobachtungen an Ratten unter osmotischer Belastung. Ergeb. Anat. Entwickl. Gesch. 41, 1–79 (1969)Google Scholar
  26. Price, P., Fisher, A.W.: Electron microscopic study of retrograde axonal transport of horseradish peroxidase in the supraoptico-hypophysial tract in the rat. J. Anat. 125, 137–147 (1978)Google Scholar
  27. Reinhardt, H.F., Henning, L.Ch., Rohr, H.P.: Morphometrisch-ultrastrukturelle Untersuchungen am Hypophysenhinterlappen der Ratte nach Dehydratation. Z. Zellforsch. 102, 182–192 (1969)Google Scholar
  28. Rougon-Rapuzzi, G., Cau, P., Boudier, J.A., Cupo, A.: Evolution of vasopressin levels in the hypothalamo-posthypophysial system of the rat during rehydration following water deprivation. Correlation with ultrastructural aspects in the posterior lobe. Neuroendocrinology 27, 46–62 (1978)Google Scholar
  29. Santolaya, R.C., Bridges, T.E., Lederis, K.: Elementary granules, small vesicles and exocytosis in the rat neurohypophysis after acute haemorrhage. Z. Zellforsch. 125, 277–288 (1972)Google Scholar
  30. Smith, U.: The origin of small vesicles in neurosecretory axons. Tissue Cell 2, 427–433 (1970)Google Scholar
  31. Sotelo, C., Riche, D.: Smooth endoplasmic reticulum and the retrograde and fast orthograde transport of horseradish peroxidase in the nigro-striatal-nigral-loop. Anat. Embryol. (Berl.) 146, 209–218 (1974)Google Scholar
  32. Stoeckel, M.E., Hindelang-Gertner, C., Dellman, H.D., Porte, A., Stutinsky, F.: Subcellular localization of calcium in the mouse hypophysis. I. Calcium distribution in the adeno- and neurohypophysis under normal conditions. Cell Tissue Res. 157, 307–322 (1975)Google Scholar
  33. Theodosis, D., Dreyfuss, J.J., Orci, L.: Two classes of microvesicles in the neurohypophysis. Brain Res. 123, 159–161 (1977)Google Scholar
  34. Thiéry, G., Rambourg, A.: A new staining technique for studying thick sections in electron microscope. J. Microscopic Biol. Cell. 26, 103–106 (1976)Google Scholar
  35. Young, T.K., Van Dyke, H.B.: Depletion of vasopressin and ocytocin in the posterior lobe of the pituitary gland of the rat. J. Endocrinol. 40, 337–342 (1968)Google Scholar

Copyright information

© Springer-Verlag 1979

Authors and Affiliations

  • G. Alonso
    • 1
  • I. Assenmacher
    • 1
  1. 1.Laboratoire de NeuroendocrinologieUniversité de Montpellier IIMontpellierFrance

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