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Glycoprotein secretion in the hypothalamo-neurohypophyseal system of the rat

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Summary

Although the secretory products of the hypothalamoneurohypophyseal system are not glycoproteins, synthesis and migration of these macromolecules occur within its secretory neurons. After being labeled with 3H-fucose in the Golgi apparatus, newly synthesized glycoproteins migrate to secretion granules, lysosomes and the plasma membrane of the secretory neurons, as demonstrated by quantitative electron-microscopic radioautography. Secretion granules bearing newly synthesized glycoproteins migrate to the pars nervosa, the labeling pattern of which was studied in rats killed from 4 h to 14 days after the isotope injection. Most of the silver grains were observed to overly the secretory axons. Labeling of pituicytes was negligible and the number of silver grains over the perivascular spaces was about 10% of the total at certain postinjection intervals. In the secretory axons, most of the silver grains were seen to overly the secretion granules. The proportion of silver grains over the different portions of the secretory axons changed with time. At the longer intervals, the percentage of silver grains increased over the nerve swellings (including Herring bodies) and decreased concomitantly in the undilated portions of the axons and in the nerve endings. This labeling pattern conforms with observations on the secretion products. Water deprivation increased the release of neurosecretion as well as glycoproteins from the pars nervosa. However, glycoproteins inside the Herring bodies were not easily releasible. There was a parallel decrease in the amount of secretion granules and 3H-fucose-labeled glycoproteins indicating that the glycoproteins are predominantly a constituent of the granule content. Some newly synthesized glycoproteins were probably also used in the renewal of the axonal membrane. The labeling of smooth vesicles in nerve endings was discussed. In conclusion, most of the glycoproteins synthesized in the perikarion of the hypothalamic secretory neurons migrate inside secretion granules along the axon to the pars nervosa where they are secreted.

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References

  1. Acher R (1976) Les neurophysines. Aspects moléculaires et cellulaires. Biochimie 58:895–911

  2. Barka T, Andersen PJ (1963) Histochemistry. Theory, practice, and bibliography. Hoeber Medical Division. Harper & Row Publishers Inc New York, pp 65–95

  3. Bennett G (1978) Synthesis and migration of glycoproteins in cells of rat thymus, as shown by radioautography after 3H-fucose injection. Am J Anat 152:223–256

  4. Bennett G, Leblond CP (1977) Biosynthesis of the glycoproteins present in plasma membrane, lysosomes and secretory materials, as visualized by radioautography. Histochem J 9:393–417

  5. Bennett G, Di Giamberardino L, Koenig HL, Droz B (1973) Axonal migration of protein and glycoprotein to nerve endings. II. Radioautographic analysis of the renewal of glycoproteins in nerve endings of chicken ciliary ganglion after intracerebral injection of (3H)-fucose and (3H)-glucosamine. Brain Res 60:129–146

  6. Bennett G, Leblond CP, Haddad A (1974) Migration of glycoprotein from the Golgi apparatus to the surface of various cell types as shown by radioautography after labeled fucose injection into rats. J Cell Biol 60:258–284

  7. Cameron ML, Steele JE (1959) Simplified aldehyde-fuchsin staining of neurosecretory cells. Stain Technol 34:265–266

  8. Chalkley HW (1943) Method for the quantitative morphologic analysis of tissues. J Natl Canc Inst 4:47–53

  9. Cross BA, Dyball REJ, Dyer RG, Jones CW, Lincoln DW, Morris JF, Pickering BT (1975) Endocrine neurons. Rec Prog Horm Res 31:243–294

  10. Douglas WW, Nagasawa J, Schulz R (1971) Electron microscopic studies on the mechanism of secretion of posterior pituitary hormones and significance of microvesicles (“synaptic vesicles”): evidence of secretion by exocytosis and formation of microvesicles as a by-product of this process. Mem Soc Endocrinol 19:353–378

  11. Dreifuss JJ (1975) A review on neurosecretory granules: their contents and mechanisms of release. Ann NY Acad Sci 248:184–201

  12. Droz B, Koenig HL, DiGiamberardino L (1973) Axonal migration of protein and glycoprotein to nerve endings. I. Radioautographic analysis of the renewal of protein in nerve endings of chicken ciliary ganglion after intracerebral injection of (3H)-lysine. Brain Res 60:93–127

  13. Gainer H, Sarne Y, Brownstein J (1977) Biosynthesis and axonal transport of rat neurohypophysial proteins and peptides. J Cell Biol 73:366–381

  14. Gold RZ (1962) On comparing multinomial probabilities. School of Aerospace Medicine. USAF Aerospace Medical Division (AFSC). Brooks Air Force Base, Texas, USA, pp 62–81

  15. Goldstone A, Koenig H (1972) Biosynthesis of lysosomal glycoproteins in rat kidney. Life Sci 11:511–523

  16. Haddad A, Bennett G, Leblond CP (1977 a) Formation and turnover of plasma membrane glycoproteins in kidney tubules of young rats and adult mice, as shown by radioautography after an injection of 3H-fucose. Am J Anat 148:241–274

  17. Haddad A, Pelletier G, Marchi F, Brasileiro ILG (1977b) Light microscope radioautographic study of glycoprotein secretion in the hypothalamic-neurohypophysial system of the rat after L-fucose-3H injection. Cell Tissue Res 177:67–79

  18. Heap PF, Jones CW, Morris JF, Pickering BT (1975) Movement of neurosecretory product through the anatomical compartments of the neural lobe of the pituitary gland. An electron microscopic autoradiographic study. Cell Tissue Res 156:483–497

  19. Holwerda DA (1972) A glycopeptide from the posterior lobe of pig pituitaries. 2. Primary structure. Eur J Biochem 28:340–346

  20. Hvas S, Thorn NA (1973) Hexosamine and heparin in homogenate and subcellular fractions from bovine neurohypophysis. Acta Endocrinol (Kbh.) 74:209–214

  21. Jones CW, Swann RW (1974) Incorporation of tritiated sugars into rat neural lobe components. J Endocrinol 63:53P-54P

  22. Jones CW, Swann RW (1975) A glycoprotein in the neurosecretory granules of the neurohypophysis. J Physiol (Lond) 245:45P

  23. Kalimo H (1978) Ultrastructural aspects of the hypothalamic neurosecretion. Acta Endocrinol (Kbh) 89:(Suppl 220), 13

  24. Kent C, Williams MA (1974) The nature of hypothalamo-neurohypophyseal neurosecretion in the rat. A study by light and electron microscope autoradiography. J Cell Biol 60:554–570

  25. Kodama Y, Fujita H (1975) Some findings on the fine structure of the neurohypophysis in dehydrated and pitressin-treated mice. Arch Histol Jpn 38:121–131

  26. Kopriwa BM (1973) A reliable standardised method for ultrastructural electron microscopic radioautography. Histochimie 37:1–17

  27. Kopriwa BM, Huckins C (1972) A method for the use of Zenker-formol fixation and the Periodic Acid Schiff staining technique in light microscopic radioautography. Histochimie 32:231–244

  28. Kurosumi K (1977) Morphological and morphometric studies on the ultrastructural changes during the active release of neurosecretory substance from the neurohypophyseal nerve terminals in dehydrated rats. Arch Histol Jpn 40:225–242

  29. Leblond CP, Bennett G (1974) Elaboration and turnover of cell coat glycoproteins. In: Moscona AA (ed) The cell surface in development. Proc 7th Internat Meet Dev Biol, New York, pp 29–49

  30. Marchi F, Haddad A, Pelletier G (In preparation) Glycoprotein biosynthesis in the neurointermidiate lobe of pituitary gland of mice and rats, as shown by radioautography after an intravenous injection of 3H-fucose

  31. Martinez-Rodriguez R, Toledano A, Garcia-Segura LM, Gonzales-Elorriaga M, Gamonal A, DiazGozales P, Agustin M, Rodriguez-Ganzales C (1976) Mucopolysaccharides in hypothalamic neurons of the rat. J Anat (Lond) 121:231–239

  32. Nadler NJ (1971) The interpretation of grain counts in electron microscope radioautography. J Cell Biol 49:877–882

  33. Nagasawa J (1977) Exocytosis: the common release mechanism of secretory granules in glandular cells, neurosecretory cells, neurons and paraneurons. Arch Histol Jpn 40 (Suppl):31–47

  34. Nordman JJ, Morris JF (1976) Membrane retrieval at neurosecretory axon endings. Nature 261:723–725

  35. Nordström A (1975) Axonal transport and turnover of neurohypophyseal proteins in the rat. Ann N Y Acad Sci 248:46–63

  36. Pickering BT (1978) The neurosecretory neurone: A model system for the study of secretion. Essays Biochem 14:45–81

  37. Pilgrim Ch, Wagner HJ (1975a) Glycoprotein metabolism in the hypothalamus of rat: significance of glial cells. Histochemistry 45:289–297

  38. Pilgrim Ch, Wagner HJ (1975b) Synthese und Transport von Glycoprotein im hypothalamoneurohypophysären System von Ratten. Verh Anat Ges 69:685–689

  39. Reisert I, Pilgrim Ch (1979) Metabolism of glycoconjugates in hypothalamic neurons and glial cells: comparison of incorporation of 3H-fucose and 3H-N-acetylmannosamine by electron microscopic autoradioautography. Cell Tissue Res 196:135–145

  40. Richard Ph, Freund-Mercier MJ, Moos F (1978) Les neurones hypothalamiques ayant une fonction endocrine. Indentification, localisation, caractéristiques électrophysiologiques et contrôle hormonal. J Physiol (Paris) 74:61–112

  41. Roux M (1970) Etude histoautoradiographic de l'incorporation de D-glucose-6–3H dans l'hypothalamus neurosécrétoire et le lobe nerveux de l'hypophyse chez la Souris albino normale et déshydratée. CR Acad Sci (Paris) 270:717–720

  42. Schachter H (1978) Glycoprotein biosynthesis. In: Horowitz MI, Pigman W (eds) The Glycoconjugates. Academic Press, New York, Vol II, pp 87–181

  43. Schantz A, Scheeler A (1965) Iron-hematoxylin and safranin O as a polychrome stain for Epon sections. Stain Technol 40:279–282

  44. Snedecor GW, Cochran WG (1972) Statistical methods. The Iowa State University Press. Ames, Iowa, USA. 6th edition, pp 285–288

  45. Sturgess J, Moscarello M, Schachter H (1978) The structure and biosynthesis of membrane glycoproteins. In: Current Topics in Membranes and Transport. Academic Press, New York, Vol 2, pp 16–105

  46. Swann RW, Pickering BT (1976) Incorporation of radioactive precursors into the membrane and contents of the neurosecretory granules of the rat neurohypophysis as a method of studying their fate. J Endocrinol 68:95–108

  47. Tasso F (1973) Localisation cytochimique ultrastructurale de glycoprotéines dans les granules neurosécrétoires de la post-hypophyse du rat. J Microsc 18:115–118

  48. Tasso F, Rua S (1975) Etude cytochimique ultrastructurale des glycoprotéines dans le complex hypothalamo-post-hypophysaire du rat. Arch Anat Microsc Morphol Exp 64:247–260

  49. Tasso F, Picard D, Dreifuss JJ (1976) Ultrastructural identification of granules containing oxytocin and vasopressin. Nature 260:621–622

  50. Tasso F, Rua S, Picard D (1977) Cytochemical duality of neurosecretory material in the hypothalamoposthypophysial system of the rat as related to hormonal content. Cell Tissue Res 180:11–29

  51. Theodosis DT, Dreifuss JJ, Orci L (1978) A freeze-fracture study of membrane events during neurohypophysial secretion. J Cell Biol 78:542–553

  52. Vilhardt H, Baker RV, Hope DB (1975) Isolation and protein composition of membranes of neurosecretory vesicles and plasma membranes from the neural lobe of the bovine pituitary gland. Biochem J 148:57–65

  53. Whur P, Hersovics A, Leblond CP (1969) Radioautographic visualization of the incorporation of galactose-3H and mannose-3H by rat thyroids in vitro in relation to the stages of thyroglobulin synthesis. J Cell Biol 43:289–311

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Correspondence to Dr. Antonio Haddad.

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Haddad, A., Guaraldo, S.P., Pelletier, G. et al. Glycoprotein secretion in the hypothalamo-neurohypophyseal system of the rat. Cell Tissue Res. 209, 399–422 (1980). https://doi.org/10.1007/BF00234755

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Key words

  • Hypothalamus
  • Neurohypophysis
  • Glycoprotein
  • 3H-fucose