Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1976 Aug;73(8):2781–2787. doi: 10.1073/pnas.73.8.2781

The endoplasmic reticulum: a cytochemist's view (a review).

A B Novikoff
PMCID: PMC430742  PMID: 183210

Abstract

Enzyme cytochemistry has been used, at the light and electron microscope levels, to "mark" cytoplasmic organelles of mammalian cells. Catalase cytochemistry permitted identification of microperoxisomes, apparently ubiquitous organelles that are attached by numerous slender connections to the endoplasmic reticulum. Thiamine pyrophosphatase and acid phosphatase cytochemistry can be used to distinguish between the Golgi apparatus and a specialized acid-phosphatase-rich region of smooth endoplasmic reticulum (ER) that appears to be involved in: (a) the formation of lysosomes and melanin granules: (b) the processing and packaging of secretory materials in endocrine and exocrine cells; and (c) the metabolism of lipid. The acronym GERL has been given to this region of smooth ER because it is located at the inner or "trans" aspect of the Golgi apparatus and because it appears to produce various types of Lysosomes.

Full text

PDF
2781

Images in this article

2782Image
on p.2782
2784Image
on p.2784
2786Image
on p.2786

Selected References

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

  1. Bentfeld M. E., Bainton D. F. Cytochemical localization of lysosomal enzymes in rat megakaryocytes and platelets. J Clin Invest. 1975 Dec;56(6):1635–1649. doi: 10.1172/JCI108246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boutry J. M., Nivikoff A. B. Cytochemical studies on golgi apparatus, GERL, and lysosomes in neurons of dorsal root ganglia in mice. Proc Natl Acad Sci U S A. 1975 Feb;72(2):508–512. doi: 10.1073/pnas.72.2.508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brumbaugh J. A. The ultrastructural effects of the I and S loci upon black-red melanin differentiation in the fowl. Dev Biol. 1971 Mar;24(3):392–412. doi: 10.1016/0012-1606(71)90088-1. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Decker R. S. Lysosomal packaging in differentiating and degenerating anuran lateral motor column neurons. J Cell Biol. 1974 Jun;61(3):599–612. doi: 10.1083/jcb.61.3.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ehrenreich J. H., Bergeron J. J., Siekevitz P., Palade G. E. Golgi fractions prepared from rat liver homogenates. I. Isolation procedure and morphological characterization. J Cell Biol. 1973 Oct;59(1):45–72. doi: 10.1083/jcb.59.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eppig J. J., Jr, Dumont J. N. Cytochemical localization of tyrosinase activity in pigmented epithelial cells of Rana pipiens and Xenopus laevis larvae. J Ultrastruct Res. 1972 May;39(3):397–410. doi: 10.1016/s0022-5320(72)90031-7. [DOI] [PubMed] [Google Scholar]
  8. Essner E., Oliver C. Lysosome formation in hepatocytes of mice with Chèdiak-Higashi syndrome. Lab Invest. 1974 May;30(5):597–607. [PubMed] [Google Scholar]
  9. Ganote C. E., Rosenthal A. S., Moses H. L., Tice L. W. Lead and phosphate as sources of artifact in nucleoside phosphatase histochemistry. J Histochem Cytochem. 1969 Oct;17(10):641–650. doi: 10.1177/17.10.641. [DOI] [PubMed] [Google Scholar]
  10. Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
  11. Hayashi H., Sternlieb I. Lipolysosomes in human hepatocytes. Ultrastructural and cytochemical studies of patients with Wilson's disease. Lab Invest. 1975 Jul;33(1):1–7. [PubMed] [Google Scholar]
  12. 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]
  13. Ide C. The development of melanosomes in the pigment epithelium of the chick embryo. Z Zellforsch Mikrosk Anat. 1972;131(2):171–186. doi: 10.1007/BF00306925. [DOI] [PubMed] [Google Scholar]
  14. Leuenberger P. M., Novikoff A. B. Studies on microperoxisomes. VII. Pigment epithelial cells and other cell types in the retina of rodents. J Cell Biol. 1975 May;65(2):324–334. doi: 10.1083/jcb.65.2.324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Maul G. G. Golgi-melanosome relationship in human melanoma in vitro. J Ultrastruct Res. 1969 Jan;26(1):163–176. doi: 10.1016/s0022-5320(69)90042-2. [DOI] [PubMed] [Google Scholar]
  17. Maul G. G., Romsdahl M. M. Ultrastructural comparison of two human malignant melanoma cell lines. Cancer Res. 1970 Nov;30(11):2782–2790. [PubMed] [Google Scholar]
  18. Moses H. L., Rosenthal A. S., Beaver D. L., Schuffman S. S. Lead ion and phosphatase histochemistry. II. Effect of adenosine triphosphate hydrolysis by lead ion on the histochemical localization of adenosine triphosphatase activity. J Histochem Cytochem. 1966 Oct;14(10):702–710. doi: 10.1177/14.10.702. [DOI] [PubMed] [Google Scholar]
  19. NOVIKOFF A. B., ESSNER E. Pathological changes in cytoplasmic organelles. Fed Proc. 1962 Nov-Dec;21:1130–1142. [PubMed] [Google Scholar]
  20. 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]
  21. NOVIKOFF A. B., HEUS M. A microsomal nucleoside diphosphatase. J Biol Chem. 1963 Feb;238:710–716. [PubMed] [Google Scholar]
  22. NOVIKOFF A. B., SHIN W. Y., DRUCKER J. Mitochondrial localization of oxidative enzymes: staining results with two tetrazolium salts. J Biophys Biochem Cytol. 1961 Jan;9:47–61. doi: 10.1083/jcb.9.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nehemiah J. L., Novikoff A. B. Unusual lysosomes in hamster hepatocytes. Exp Mol Pathol. 1974 Dec;21(3):398–423. doi: 10.1016/0014-4800(74)90105-1. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Novikoff A. B. Enzyme localizations with Gomori type lead phosphate procedures: real or artifact. J Histochem Cytochem. 1970 May;18(5):366–367. doi: 10.1177/18.5.366. [DOI] [PubMed] [Google Scholar]
  26. Novikoff A. B. Enzyme localizations with Wachstein-Meisel procedures: real or artifact. J Histochem Cytochem. 1967 Jun;15(6):353–354. doi: 10.1177/15.6.353. [DOI] [PubMed] [Google Scholar]
  27. Novikoff A. B., Goldfischer S. Visualization of peroxisomes (microbodies) and mitochondria with diaminobenzidine. J Histochem Cytochem. 1969 Oct;17(10):675–680. doi: 10.1177/17.10.675. [DOI] [PubMed] [Google Scholar]
  28. Novikoff A. B., Novikoff P. M., Davis C., Quintana N. Studies on microperoxisomes. II. A cytochemical method for light and electron microscopy. J Histochem Cytochem. 1972 Dec;20(12):1006–1023. doi: 10.1177/20.12.1006. [DOI] [PubMed] [Google Scholar]
  29. Novikoff A. B., Novikoff P. M., Davis C., Quintana N. Studies on microperoxisomes. V. Are microperoxisomes ubiquitous in mammalian cells? J Histochem Cytochem. 1973 Aug;21(8):737–755. doi: 10.1177/21.8.737. [DOI] [PubMed] [Google Scholar]
  30. Novikoff A. B., Novikoff P. M. Microperoxisomes. J Histochem Cytochem. 1973 Nov;21(11):963–966. doi: 10.1177/21.11.963. [DOI] [PubMed] [Google Scholar]
  31. Novikoff A. B. Their phosphatase controversy: Love's labours lost. J Histochem Cytochem. 1970 Dec;18(12):916–917. doi: 10.1177/18.12.916. [DOI] [PubMed] [Google Scholar]
  32. Novikoff A. B., Yam A., Novikoff P. M. Cytochemical study of secretory process in transplantable insulinoma of syrian golden hamster. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4501–4505. doi: 10.1073/pnas.72.11.4501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Novikoff P. M., Novikoff A. B. Peroxisomes in absorptive cells of mammalian small intestine. J Cell Biol. 1972 May;53(2):532–560. doi: 10.1083/jcb.53.2.532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Novikoff P. M., Roheim P. S., Novikoff A. B., Edelstein D. Production and prevention of fatty liver in rats fed clofibrate and orotic acid diets containing sucrose. Lab Invest. 1974 Jun;30(6):732–750. [PubMed] [Google Scholar]
  36. Palade G. Intracellular aspects of the process of protein synthesis. Science. 1975 Aug 1;189(4200):347–358. doi: 10.1126/science.1096303. [DOI] [PubMed] [Google Scholar]
  37. Rosenthal A. S., Moses H. L., Beaver D. L., Schuffman S. S. Lead ion and phosphatase histochemistry. I. Nonenzymatic hydrolysis of nucleoside phosphates by lead ion. J Histochem Cytochem. 1966 Oct;14(10):698–701. doi: 10.1177/14.10.698. [DOI] [PubMed] [Google Scholar]
  38. Rosenthal A. S., Moses H. L., Ganote C. E. Interpretation of phosphatase cytochemical data. J Histochem Cytochem. 1970 Dec;18(12):915–915. doi: 10.1177/18.12.915. [DOI] [PubMed] [Google Scholar]
  39. Vigil E. L. Structure and function of plant microbodies. Subcell Biochem. 1973;2(3):237–285. [PubMed] [Google Scholar]
  40. Wake K. Development of vitamin A-rich lipid droplets in multivesicular bodies of rat liver stellate cells. J Cell Biol. 1974 Nov;63(2 Pt 1):683–691. doi: 10.1083/jcb.63.2.683. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES