Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1973 Apr 1;57(1):88–108. doi: 10.1083/jcb.57.1.88

AXONAL AGRANULAR RETICULUM AND SYNAPTIC VESICLES IN CULTURED EMBRYONIC CHICK SYMPATHETIC NEURONS

Saul Teichberg 1, Eric Holtzman 1
PMCID: PMC2108948  PMID: 4347980

Abstract

Cultured chick embryonic sympathetic neurons contain an extensive axonal network of sacs and tubules of agranular reticulum. The reticulum is also seen branching into networks in axon terminals and varicosities. The axonal reticulum and perikaryal endoplasmic reticulum resemble one another in their content of cytochemically demonstrable enzyme activities (G6Pase and IDPase) and in their characteristic membrane thicknesses (narrower than plasma membrane or some Golgi membranes). From the reticulum, both along the axon and at terminals, there appear to form dense-cored vesicles ranging in size from 400 to 1,000 Å in diameter. These vesicles behave pharmacologically and cytochemically like the classes of large and small catecholamine storage vesicles found in several adrenergic systems; for example, they can accumulate exogenous 5-hydroxydopamine. In addition, dense-cored vesicles at the larger (1,000 Å) end of the size spectrum appear to arise within perikaryal membrane systems associated with the Golgi apparatus; this is true also of very large (800–3,500 Å) dense-cored vesicles found in some perikarya.

Full Text

The Full Text of this article is available as a PDF (2.3 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abrahams S. J., Holtzman E. Secretion and endocytosis in insulin-stimulated rat adrenal medulla cells. J Cell Biol. 1973 Feb;56(2):540–558. doi: 10.1083/jcb.56.2.540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BORNSTEIN M. B. Reconstituted rattail collagen used as substrate for tissue cultures on coverslips in Maximow slides and roller tubes. Lab Invest. 1958 Mar-Apr;7(2):134–137. [PubMed] [Google Scholar]
  3. Banks P., Mayor D., Tomlinson D. R. Further evidence for the involvement of microtubules in the intra-axonal movement of noradrenaline storage granules. J Physiol. 1971 Dec;219(3):755–761. doi: 10.1113/jphysiol.1971.sp009688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bloom F. E., Barrnett R. J. Fine structural localization of noradrenaline in vesicles of autonomic nerve endings. Nature. 1966 May 7;210(5036):599–601. doi: 10.1038/210599a0. [DOI] [PubMed] [Google Scholar]
  5. Bloom F. E., Iversen L. L., Schmitt F. O. Macromolecules in synaptic function. Neurosci Res Program Bull. 1970 Sep;8(4):325–455. [PubMed] [Google Scholar]
  6. Bondareff W. Submicroscopic morphology of granular vesicles in sympathetic nerves of rat pineal body. Z Zellforsch Mikrosk Anat. 1965 Jul 15;67(2):211–218. doi: 10.1007/BF00344470. [DOI] [PubMed] [Google Scholar]
  7. Brimijoin S. Transport and turnover of dopamine- -hydroxylase (EC 1.14.2.1) in sympathetic nerves of the rat. J Neurochem. 1972 Sep;19(9):2183–2193. doi: 10.1111/j.1471-4159.1972.tb05127.x. [DOI] [PubMed] [Google Scholar]
  8. Bunge M. B., Bunge R. P., Peterson E. R. The onset of synapse formation in spinal cord cultures as studied by electron microscopy. Brain Res. 1967 Dec;6(4):728–749. doi: 10.1016/0006-8993(67)90129-1. [DOI] [PubMed] [Google Scholar]
  9. Burdman J. A. Uptake of (3H)catecholamines by chick embryo sympathetic ganglia in tissue culture. J Neurochem. 1968 Nov;15(11):1321–1323. doi: 10.1111/j.1471-4159.1968.tb05910.x. [DOI] [PubMed] [Google Scholar]
  10. Coon H. G. Clonal stability and phenotypic expression of chick cartilage cells in vitro. Proc Natl Acad Sci U S A. 1966 Jan;55(1):66–73. doi: 10.1073/pnas.55.1.66. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dahlström A. Axoplasmic transport (with particular respect to adrenergic neurons). Philos Trans R Soc Lond B Biol Sci. 1971 Jun 17;261(839):325–358. doi: 10.1098/rstb.1971.0064. [DOI] [PubMed] [Google Scholar]
  12. Dallner G., Siekevitz P., Palade G. E. Biogenesis of endoplasmic reticulum membranes. I. Structural and chemical differentiation in developing rat hepatocyte. J Cell Biol. 1966 Jul;30(1):73–96. doi: 10.1083/jcb.30.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. De Potter W. P., Chubb I. W. The turnover rate of noradrenergic vesicles. Biochem J. 1971 Nov;125(1):375–376. doi: 10.1042/bj1250375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. De Potter W. P. Noradrenaline storage particles in splenic nerve. Philos Trans R Soc Lond B Biol Sci. 1971 Jun 17;261(839):313–317. doi: 10.1098/rstb.1971.0062. [DOI] [PubMed] [Google Scholar]
  15. England J. M., Goldstein M. N. The uptake and localization of catecholamines in chick embryo sympathetic neurons in tissue culture. J Cell Sci. 1969 May;4(3):677–691. doi: 10.1242/jcs.4.3.677. [DOI] [PubMed] [Google Scholar]
  16. Eränkö O., Eränkö L., Hill C. E., Burnstock G. Hydrocortisone-induced increase in the number of small intensely fluorescent cells and their histochemically demonstrable catecholamine content in cultures of sympathetic ganglia of the newborn rat. Histochem J. 1972 Jan;4(1):49–58. doi: 10.1007/BF01005268. [DOI] [PubMed] [Google Scholar]
  17. Farquhar M. G., Bainton D. F., Baggiolini M., de Duve C. Cytochemical localization of acid phosphatase activity in granule fractions from rabbit polymorphonuclear leukocytes. J Cell Biol. 1972 Jul;54(1):141–156. doi: 10.1083/jcb.54.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fillenz M. The innervation of the cat spleen. Proc R Soc Lond B Biol Sci. 1970 Jan 20;174(1037):459–468. doi: 10.1098/rspb.1970.0005. [DOI] [PubMed] [Google Scholar]
  19. Flickinger C. J. The development of Golgi complexes and their dependence upon the nucleus inmebae. J Cell Biol. 1969 Nov;43(2):250–262. doi: 10.1083/jcb.43.2.250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. GOLDFISCHER S., ESSNER E., NOVIKOFF A. B. THE LOCALIZATION OF PHOSPHATASE ACTIVITIES AT THE LEVEL OF ULTRASTRUCTURE. J Histochem Cytochem. 1964 Feb;12:72–95. doi: 10.1177/12.2.72. [DOI] [PubMed] [Google Scholar]
  21. Geffen L. B., Livett B. G. Synaptic vesicles in sympathetic neurons. Physiol Rev. 1971 Jan;51(1):98–157. doi: 10.1152/physrev.1971.51.1.98. [DOI] [PubMed] [Google Scholar]
  22. Geffen L. B., Ostberg A. Distribution of granular vesicles in normal and constricted sympathetic neurones. J Physiol. 1969 Oct;204(3):583–592. doi: 10.1113/jphysiol.1969.sp008933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Goldfischer S., Essner E., Schiller B. Nucleoside diphosphatase and thiamine pyrophosphatase activities in the endoplasmic reticulum and golgi apparatus. J Histochem Cytochem. 1971 Jun;19(6):349–360. doi: 10.1177/19.6.349. [DOI] [PubMed] [Google Scholar]
  24. Gray E. G. The question of relationship between Golgi vesicles and synaptic vesicles in Octopus neurons. J Cell Sci. 1970 Jul;7(1):189–201. doi: 10.1242/jcs.7.1.189. [DOI] [PubMed] [Google Scholar]
  25. HERS H. G., BERTHET J., BERTHET L., DE DUVE C. Le système hexose-phosphatasique. III. Localisation intra-cellulaire des ferments par centrifugation fractionnée. Bull Soc Chim Biol (Paris) 1951;33(1-2):21–41. [PubMed] [Google Scholar]
  26. Holtzman E. Cytochemical studies of protein transport in the nervous system. Philos Trans R Soc Lond B Biol Sci. 1971 Jun 17;261(839):407–421. doi: 10.1098/rstb.1971.0075. [DOI] [PubMed] [Google Scholar]
  27. Holtzman E., Dominitz R. Cytochemical studies of lysosomes, golgi apparatus and endoplasmic reticulum in secretion and protein uptake by adrenal medulla cells of the rat. J Histochem Cytochem. 1968 May;16(5):320–336. doi: 10.1177/16.5.320. [DOI] [PubMed] [Google Scholar]
  28. Holtzman E., Freeman A. R., Kashner L. A. Stimulation-dependent alterations in peroxidase uptake at lobster neuromuscular junctions. Science. 1971 Aug 20;173(3998):733–736. doi: 10.1126/science.173.3998.733. [DOI] [PubMed] [Google Scholar]
  29. Holtzman E., Novikoff A. B. Lysomes in the rat sciatic nerve following crush. J Cell Biol. 1965 Dec;27(3):651–669. doi: 10.1083/jcb.27.3.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Holtzman E., Novikoff A. B., Villaverde H. Lysosomes and GERL in normal and chromatolytic neurons of the rat ganglion nodosum. J Cell Biol. 1967 May;33(2):419–435. doi: 10.1083/jcb.33.2.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Holtzman E., Peterson E. R. Uptake of protein by mammalian neurons. J Cell Biol. 1969 Mar;40(3):863–869. doi: 10.1083/jcb.40.3.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hökfelt T., Dahlström A. Effects of two mitosis inhibitors (colchicine and vinblastine) on the distribution and axonal transport of noradrenaline storage particles, studied by fluorescence and electron microscopy. Z Zellforsch Mikrosk Anat. 1971;119(4):460–482. doi: 10.1007/BF00455243. [DOI] [PubMed] [Google Scholar]
  33. Hökfelt T. Distribution of noradrenaline storing particles in peripheral adrenergic neurons as revealed by electron microscopy. Acta Physiol Scand. 1969 Aug;76(4):427–440. doi: 10.1111/j.1748-1716.1969.tb04488.x. [DOI] [PubMed] [Google Scholar]
  34. Kapeller K., Mayor D. The accumulation of noradrenaline in constricted sympathetic nerves as studied by fluorescence and electron microscopy. Proc R Soc Lond B Biol Sci. 1967 Mar 28;167(1008):282–292. doi: 10.1098/rspb.1967.0027. [DOI] [PubMed] [Google Scholar]
  35. Kasa P. Acetylcholinesterase transport in the central and peripheral nervous tissue: the role of tubules in the enzyme transport. Nature. 1968 Jun 29;218(5148):1265–1267. doi: 10.1038/2181265a0. [DOI] [PubMed] [Google Scholar]
  36. Kebabian J. W., Greengard P. Dopamine-sensitive adenyl cyclase: possible role in synaptic transmission. Science. 1971 Dec 24;174(4016):1346–1349. doi: 10.1126/science.174.4016.1346. [DOI] [PubMed] [Google Scholar]
  37. Korneliussen H. Ultrastructure of normal and stimulated motor endplates with comments on the origin and fate of synaptic vesicles. Z Zellforsch Mikrosk Anat. 1972;130(1):28–57. doi: 10.1007/BF00306993. [DOI] [PubMed] [Google Scholar]
  38. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lentz T. L. Vesicle and granule content of sympathetic ganglion cells during limb regeneration of the newt Triturus. Z Zellforsch Mikrosk Anat. 1969;102(4):447–458. doi: 10.1007/BF00335487. [DOI] [PubMed] [Google Scholar]
  40. Nichols B. A., Bainton D. F., Farquhar M. G. Differentiation of monocytes. Origin, nature, and fate of their azurophil granules. J Cell Biol. 1971 Aug;50(2):498–515. doi: 10.1083/jcb.50.2.498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Norberg K. A., Ritzén M., Ungerstedt U. Histochemical studies on a special catecholamine-containing cell type in sympathetic ganglia. Acta Physiol Scand. 1966 Jul-Aug;67(3):260–270. doi: 10.1111/j.1748-1716.1966.tb03311.x. [DOI] [PubMed] [Google Scholar]
  42. Novikoff P. M., Novikoff A. B., Quintana N., Hauw J. J. Golgi apparatus, GERL, and lysosomes of neurons in rat dorsal root ganglia, studied by thick section and thin section cytochemistry. J Cell Biol. 1971 Sep;50(3):859–886. doi: 10.1083/jcb.50.3.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. OSINCHAK J. ELECTRON MICROSCOPIC LOCALIZATION OF ACID PHOSPHATASE AND THIAMINE PYROPHOSPHATASE ACTIVITY IN HYPOTHALAMIC NEUROSECRETORY CELLS OF THE RAT. J Cell Biol. 1964 Apr;21:35–47. doi: 10.1083/jcb.21.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Ochs S. Fast transport of materials in mammalian nerve fibers. Science. 1972 Apr 21;176(4032):252–260. doi: 10.1126/science.176.4032.252. [DOI] [PubMed] [Google Scholar]
  45. PALAY S. L., PALADE G. E. The fine structure of neurons. J Biophys Biochem Cytol. 1955 Jan;1(1):69–88. doi: 10.1083/jcb.1.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. PALAY S. L. The morphology of synapses in the central nervous system. Exp Cell Res. 1958;14(Suppl 5):275–293. [PubMed] [Google Scholar]
  47. ROSENBLUTH J. Subsurface cisterns and their relationship to the neuronal plasma membrane. J Cell Biol. 1962 Jun;13:405–421. doi: 10.1083/jcb.13.3.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. SABATINI D. D., BENSCH K., BARRNETT R. J. Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J Cell Biol. 1963 Apr;17:19–58. doi: 10.1083/jcb.17.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Smith A. D. Secretion of proteins (chromogranin A and dopamine -hydroxylase) from a sympathetic neuron. Philos Trans R Soc Lond B Biol Sci. 1971 Jun 17;261(839):363–370. doi: 10.1098/rstb.1971.0066. [DOI] [PubMed] [Google Scholar]
  50. Smith D. S. On the significance of cross-bridges between microtubules and synaptic vesicles. Philos Trans R Soc Lond B Biol Sci. 1971 Jun 17;261(839):395–405. doi: 10.1098/rstb.1971.0074. [DOI] [PubMed] [Google Scholar]
  51. Sotelo C., Palay S. L. Altered axons and axon terminals in the lateral vestibular nucleus of the rat. Possible example of axonal remodeling. Lab Invest. 1971 Dec;25(6):653–671. [PubMed] [Google Scholar]
  52. Tranzer J. P., Thoenen H. Electronmicroscopic localization of 5-hydroxydopamine (3,4,5-trihydroxy-phenyl-ethylamine), a new 'false' sympathetic transmitter. Experientia. 1967 Sep 15;23(9):743–745. doi: 10.1007/BF02154151. [DOI] [PubMed] [Google Scholar]
  53. VAN BREEMEN V. L., ANDERSON E., REGER J. F. An attempt to determine the origin of synaptic vesicles. Exp Cell Res. 1958;14(Suppl 5):153–167. [PubMed] [Google Scholar]
  54. VENABLE J. H., COGGESHALL R. A SIMPLIFIED LEAD CITRATE STAIN FOR USE IN ELECTRON MICROSCOPY. J Cell Biol. 1965 May;25:407–408. doi: 10.1083/jcb.25.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. WATSON M. L. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958 Jul 25;4(4):475–478. doi: 10.1083/jcb.4.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. WOLFE D. E., POTTER L. T., RICHARDSON K. C., AXELROD J. Localizing tritiated norepinephrine in sympathetic axons by electron microscopic autoradiography. Science. 1962 Oct 19;138(3538):440–442. doi: 10.1126/science.138.3538.440. [DOI] [PubMed] [Google Scholar]
  57. Weinshilboum R. M., Thoa N. B., Johnson D. G., Kopin I. J., Axelrod J. Proportional release of norepinephrine and dopamine- -hydroxylase from sympathetic nerves. Science. 1971 Dec 24;174(4016):1349–1351. doi: 10.1126/science.174.4016.1349. [DOI] [PubMed] [Google Scholar]
  58. Whaley W. G., Dauwalder M., Kephart J. E. Golgi apparatus: influence on cell surfaces. Science. 1972 Feb 11;175(4022):596–599. doi: 10.1126/science.175.4022.596. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES