Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1971 Sep 1;50(3):859–886. doi: 10.1083/jcb.50.3.859

GOLGI APPARATUS, GERL, AND LYSOSOMES OF NEURONS IN RAT DORSAL ROOT GANGLIA, STUDIED BY THICK SECTION AND THIN SECTION CYTOCHEMISTRY

Phyllis M Novikoff 1, Alex B Novikoff 1, Nelson Quintana 1, Jean-Jacques Hauw 1
PMCID: PMC2108306  PMID: 4329159

Abstract

New insights into the ultrastructure and phosphatase localizations of Golgi apparatus and GERL, and into the probable origin of lysosomes in the neurons of fetal dorsal root ganglia and the small neurons of adult ganglia have come from studying thick (0.5–1.0 µ) as well as thin (up to 500 A) sections by conventional electron microscopy. Tilting the thick specimens, by a goniometer stage, has helped to increase our understanding of the three-dimensional aspects of the Golgi apparatus and GERL. One Golgi element, situated at the inner aspect of the Golgi stack, displays thiamine pyrophosphatase and nucleoside diphosphatase activities. This element exhibits regular geometric arrays (hexagons) of interconnected tubules without evidence of a flattened portion (saccule or cisterna). In contrast, GERL shows acid phosphatase activity and possesses small cisternal portions and anastomosing tubules. Lysosomes appear to bud from GERL. Osmium deposits, following prolonged osmication, are found in the outer Golgi element. Serial 0.5-µ and thin sections of thiamine pyrophosphatase-incubated material demonstrate that, in the neurons studied, the Golgi apparatus is a continuous network coursing through the cytoplasm. Serial thick sections of acid phosphatase-incubated tissue suggest that GERL is also a continuous structure throughout the cytoplasm. Tubules of smooth endoplasmic reticulum, possibly part of GERL, extend into the polygonal compartments of the inner Golgi element. The possible physiological significance of a polygonal arrangement of a phosphatase-rich Golgi element in proximity to smooth ER is considered. A tentative diagram of the Golgi stack and associated endoplasmic reticulum in these neurons has been drawn.

Full Text

The Full Text of this article is available as a PDF (3.0 MB).

Selected References

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

  1. Bainton D. F., Farquhar M. G. Differences in enzyme content of azurophil and specific granules of polymorphonuclear leukocytes. II. Cytochemistry and electron microscopy of bone marrow cells. J Cell Biol. 1968 Nov;39(2):299–317. doi: 10.1083/jcb.39.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bainton D. F., Farquhar M. G. Origin of granules in polymorphonuclear leukocytes. Two types derived from opposite faces of the Golgi complex in developing granulocytes. J Cell Biol. 1966 Feb;28(2):277–301. doi: 10.1083/jcb.28.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barland P., Smith C., Hamerman D. Localization of hyaluronic acid in synovial cells by radioautography. J Cell Biol. 1968 Apr;37(1):13–26. doi: 10.1083/jcb.37.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beams H. W., Kessel R. G. The Golgi apparatus: structure and function. Int Rev Cytol. 1968;23:209–276. doi: 10.1016/s0074-7696(08)60273-9. [DOI] [PubMed] [Google Scholar]
  5. Bennett G., Leblond C. P. Formation of cell coat material for the whole surface of columnar cells in the rat small intestine, as visualized by radioautography with L-fucose-3H. J Cell Biol. 1970 Aug;46(2):409–416. doi: 10.1083/jcb.46.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Claude A. Growth and differentiation of cytoplasmic membranes in the course of lipoprotein granule synthesis in the hepatic cell. I. Elaboration of elements of the Golgi complex. J Cell Biol. 1970 Dec;47(3):745–766. doi: 10.1083/jcb.47.3.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cunningham W. P., Morré D. J., Mollenhauer H. H. Structure of isolated plant Golgi apparatus revealed by negative staining. J Cell Biol. 1966 Feb;28(2):169–179. doi: 10.1083/jcb.28.2.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dauwalder M., Whaley W. G., Kephart J. E. Phosphatases and differentiation of the Golgi apparatus. J Cell Sci. 1969 Mar;4(2):455–497. doi: 10.1242/jcs.4.2.455. [DOI] [PubMed] [Google Scholar]
  9. Droz B. Elaboration de glycoproteines dans l'appareil de Golgi des cellules hépatiques chez le rat; étude radioautographique en microscopie électronique après injection de glactose-3H. C R Acad Sci Hebd Seances Acad Sci D. 1966 Apr 18;262(16):1766–1768. [PubMed] [Google Scholar]
  10. FRIEND D. S., MURRAY M. J. OSMIUM IMPREGNATION OF THE GOLGI APPARATUS. Am J Anat. 1965 Jul;117:135–149. doi: 10.1002/aja.1001170109. [DOI] [PubMed] [Google Scholar]
  11. Farquhar M. G., Palade G. E. Cell junctions in amphibian skin. J Cell Biol. 1965 Jul;26(1):263–291. doi: 10.1083/jcb.26.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fleischer B., Fleischer S., Ozawa H. Isolation and characterization of Golgi membranes from bovine liver. J Cell Biol. 1969 Oct;43(1):59–79. doi: 10.1083/jcb.43.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Flickinger C. J. Fenestrated cisternae in the Golgi apparatus of the epididymis. Anat Rec. 1969 Jan;163(1):39–53. doi: 10.1002/ar.1091630105. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Flickinger C. J. The pattern of growth of the Golgi complex during the fetal and postnatal development of the rat epididymis. J Ultrastruct Res. 1969 May;27(3):344–360. doi: 10.1016/s0022-5320(69)80022-5. [DOI] [PubMed] [Google Scholar]
  16. Friend D. S. Cytochemical staining of multivesicular body and golgi vesicles. J Cell Biol. 1969 Apr;41(1):269–279. doi: 10.1083/jcb.41.1.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Friend D. S., Farquhar M. G. Functions of coated vesicles during protein absorption in the rat vas deferens. J Cell Biol. 1967 Nov;35(2):357–376. doi: 10.1083/jcb.35.2.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Friend D. S. The fine structure of Brunner's glands in the mouse. J Cell Biol. 1965 Jun;25(3):563–576. doi: 10.1083/jcb.25.3.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Goldfischer S., Novikoff A. B., Albala A., Biempica L. Hemoglobin uptake by rat hepatocytes and its breakdown within lysosomes. J Cell Biol. 1970 Mar;44(3):513–529. doi: 10.1083/jcb.44.3.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Grove S. N., Bracker C. E., Morré D. J. Cytomembrane differentiation in the endoplasmic reticulum-Golgi apparatus-vesicle complex. Science. 1968 Jul 12;161(3837):171–173. doi: 10.1126/science.161.3837.171. [DOI] [PubMed] [Google Scholar]
  21. Herzog V., Miller F. Die Lokalisation endogener Peroxydase in der Glandula parotis der Ratte. Z Zellforsch Mikrosk Anat. 1970;107(3):403–420. [PubMed] [Google Scholar]
  22. 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]
  23. Jamieson J. D., Palade G. E. Intracellular transport of secretory proteins in the pancreatic exocrine cell. II. Transport to condensing vacuoles and zymogen granules. J Cell Biol. 1967 Aug;34(2):597–615. doi: 10.1083/jcb.34.2.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. KESSEL R. G., BEAMS H. W. AN UNUSUAL CONFIGURATION OF THE GOLGI COMPLEX IN PIGMENT-PRODUCING "TEST" CELLS OF THE OVARY OF THE TUNICATE, STYELA. J Cell Biol. 1965 Apr;25:55–67. doi: 10.1083/jcb.25.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. MANTON I. On a reticular derivative from Golgi bodies in the meristem of Anthroceros. J Biophys Biochem Cytol. 1960 Sep;8:221–231. doi: 10.1083/jcb.8.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. MOLLENHAUER H. H., WHALEY W. G. An observation on the functioning of the Golgi apparatus. J Cell Biol. 1963 Apr;17:222–225. doi: 10.1083/jcb.17.1.222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ma M. H., Biempica L. The normal human liver cell. Cytochemical and ultrastructural studies. Am J Pathol. 1971 Mar;62(3):353–390. [PMC free article] [PubMed] [Google Scholar]
  29. Maul G. G., Brinkley B. R. The golgi apparatus during mitosis in human melanoma cells in vitro. Cancer Res. 1970 Sep;30(9):2326–2335. [PubMed] [Google Scholar]
  30. Maul G. G., Brumbaugh J. A. On the possible function of coated vesicles in melanogenesis of the regenerating fowl feather. J Cell Biol. 1971 Jan;48(1):41–48. doi: 10.1083/jcb.48.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Maul G. G. On the relationship between the Golgi apparatus and annulate lamellae. J Ultrastruct Res. 1970 Feb;30(3):368–384. doi: 10.1016/s0022-5320(70)80069-7. [DOI] [PubMed] [Google Scholar]
  32. Miller F., Herzog V. Die Lokalisation von Peroxydase und saurer Phosphatase in eosinophilen Leukocyten während der Reifung. Elek. Elektronenmikroskopisch-cytochemische Untersuchungen am Knochenmark von Ratte und Kaninchen. Z Zellforsch Mikrosk Anat. 1969;97(1):84–110. [PubMed] [Google Scholar]
  33. Morre J., Merlin L. M., Keenan T. W. Localization of glycosyl transferase activities in a Golgi apparatus-rich fraction isolated from rat liver. Biochem Biophys Res Commun. 1969 Nov 20;37(5):813–819. doi: 10.1016/0006-291x(69)90964-4. [DOI] [PubMed] [Google Scholar]
  34. NOVIKOFF A. B., ESSNER E. Pathological changes in cytoplasmic organelles. Fed Proc. 1962 Nov-Dec;21:1130–1142. [PubMed] [Google Scholar]
  35. NOVIKOFF A. B., ESSNER E., QUINTANA N. GOLGI APPARATUS AND LYSOSOMES. Fed Proc. 1964 Sep-Oct;23:1010–1022. [PubMed] [Google Scholar]
  36. NOVIKOFF A. B., GOLDFISCHER S. Nucleosidediphosphatase activity in the Golgi apparatus and its usefulness for cytological studies. Proc Natl Acad Sci U S A. 1961 Jun 15;47:802–810. doi: 10.1073/pnas.47.6.802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Novikoff A. B., Albala A., Biempica L. Ultrastructural and cytochemical observations on B-16 and Harding-Passey mouse melanomas. The origin of premelanosomes and compound melanosomes. J Histochem Cytochem. 1968 May;16(5):299–319. doi: 10.1177/16.5.299. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Palade G. E. Structure and function at the cellular level. JAMA. 1966 Nov 21;198(8):815–825. [PubMed] [Google Scholar]
  40. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rambourg A. L'appareil de Golgi: examen en microscopie électronique de coupes épaisses (0,5-1 mu), colorées par le mélange chlorhydrique-phosphotungstique. C R Acad Sci Hebd Seances Acad Sci D. 1969 Nov 24;269(21):2125–2127. [PubMed] [Google Scholar]
  42. 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]
  43. Schachter H., Jabbal I., Hudgin R. L., Pinteric L., McGuire E. J., Roseman S. Intracellular localization of liver sugar nucleotide glycoprotein glycosyltransferases in a Golgi-rich fraction. J Biol Chem. 1970 Mar 10;245(5):1090–1100. [PubMed] [Google Scholar]
  44. Smith R. E., Farquhar M. G. Modulation in nucleoside diphosphatase activity of mammotrophic cells of the rat adenohypophysis during secretion. J Histochem Cytochem. 1970 Apr;18(4):237–250. doi: 10.1177/18.4.237. [DOI] [PubMed] [Google Scholar]
  45. Stenn K., Bahr G. F. Specimen damage caused by the beam of the transmission electron microscope, a correlative reconsideration. J Ultrastruct Res. 1970 Jun;31(5-6):526–550. doi: 10.1016/s0022-5320(70)90167-x. [DOI] [PubMed] [Google Scholar]
  46. Wagner R. R., Cynkin M. A. Enzymatic transfer of 14C-glucosamine from UDP-N-acetyl-14C-glucosamine to endogenous acceptors in a Golgi apparatus-rich fraction from liver. Biochem Biophys Res Commun. 1969 Apr 10;35(1):139–143. doi: 10.1016/0006-291x(69)90495-1. [DOI] [PubMed] [Google Scholar]
  47. Whur P., Herscovics A., Leblond C. P. 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. 1969 Nov;43(2):289–311. doi: 10.1083/jcb.43.2.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Yamazaki M., Hayaishi O. Allosteric properties of nucleoside diphosphatase and its identity with thiamine pyrophosphatase. J Biol Chem. 1968 Jun 10;243(11):2934–2942. [PubMed] [Google Scholar]

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

RESOURCES