Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1978 Jul 1;78(1):131–151. doi: 10.1083/jcb.78.1.131

Secretory kinetics in the follicular cells of silkmoths during eggshell formation

PMCID: PMC2110171  PMID: 566758

Abstract

Procedures for quantitative autoradiography were used for studying the process of secretion of eggshell (chorion) proteins in the follicular epithelium of silkmoths. The method was based on photometric measurements of the reflectance of vertically illuminated autoradiographic silver grains. Results were analyzed and plotted by computer. Secretory kinetics were also determined by analysis of labeled proteins in physically separated epithelium and chorion. Rapid accumulation of radioactivity into "clumps" visualized by light microscope autoradiography and evidence from preliminary electron microscope autoradiography indicate that, within 2 min from the time of synthesis, labeled chorion proteins move to Golgi regions scattered throughout the cytoplasm. The proteins begin to accumulate in the apical area 10-20 min later and to be discharged from the cell. The time for half-secretion is 20-25 min, and discharge is essentially complete 30-50 min after labeling. At the developmental stages examined, the kinetics of secretion appear to be similar for all proteins. Within the chorion the proteins rapidly assume a characteristic distribution, which varies for different developmental stages. Two relatively slow steps have been identified in secretion, associated with residence in Golgi regions and in the cell apex, respectively. By contrast, translocation of proteins across the cell and deposition of discharged proteins in the chorion are rapid steps.

Full Text

The Full Text of this article is available as a PDF (4.0 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. Segregation and packaging of granule enzymes in eosinophilic leukocytes. J Cell Biol. 1970 Apr;45(1):54–73. doi: 10.1083/jcb.45.1.54. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. CARO L. G., VAN TUBERGEN R. P., KOLB J. A. High-resolution autoradiography. I. Methods. J Cell Biol. 1962 Nov;15:173–188. doi: 10.1083/jcb.15.2.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Castle J. D., Jamieson J. D., Palade G. E. Radioautographic analysis of the secretory process in the parotid acinar cell of the rabbit. J Cell Biol. 1972 May;53(2):290–311. doi: 10.1083/jcb.53.2.290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. GRACE T. D. Establishment of four strains of cells from insect tissues grown in vitro. Nature. 1962 Aug 25;195:788–789. doi: 10.1038/195788a0. [DOI] [PubMed] [Google Scholar]
  7. GULLBERG J. E. A new change-over optical system and a direct recording microscope for quantitative autoradiography. Exp Cell Res. 1957;13(Suppl 4):222–230. [PubMed] [Google Scholar]
  8. Grayson S., Berry S. J. Synthesis and intracellular transport of protein by the colleterial gland of the cecropia silkmoth. Dev Biol. 1974 May;38(1):150–156. doi: 10.1016/0012-1606(74)90265-6. [DOI] [PubMed] [Google Scholar]
  9. HOWLING D. H., FITZGERALD P. J. The nature, significance, and evaluation of the Schwarzschild-Villiger (SV) effect in photometric procedures. J Biophys Biochem Cytol. 1959 Dec;6:313–337. doi: 10.1083/jcb.6.3.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jamieson J. D., Palade G. E. Intracellular transport of secretory proteins in the pancreatic exocrine cell. I. Role of the peripheral elements of the Golgi complex. J Cell Biol. 1967 Aug;34(2):577–596. doi: 10.1083/jcb.34.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Jamieson J. D., Palade G. E. Synthesis, intracellular transport, and discharge of secretory proteins in stimulated pancreatic exocrine cells. J Cell Biol. 1971 Jul;50(1):135–158. doi: 10.1083/jcb.50.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kafatos F. C., Regier J. C., Mazur G. D., Nadel M. R., Blau H. M., Petri W. H., Wyman A. R., Gelinas R. E., Moore P. B., Paul M. The eggshell of insects: differentiation-specific proteins and the control of their synthesis and accumulation during development. Results Probl Cell Differ. 1977;8:45–145. doi: 10.1007/978-3-540-37332-2_2. [DOI] [PubMed] [Google Scholar]
  14. Kopriwa B. M. The influence of development on the number and appearance of silver grains in electron microscopic radioautography. J Histochem Cytochem. 1967 Sep;15(9):501–515. doi: 10.1177/15.9.501. [DOI] [PubMed] [Google Scholar]
  15. Kraehenbuhl J. P., Jamieson J. D. Solid-phase conjugation of ferritin to Fab-fragments of immunoglobulin G for use in antigen localization on thin sections. Proc Natl Acad Sci U S A. 1972 Jul;69(7):1771–1775. doi: 10.1073/pnas.69.7.1771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Neely J. E., Combs J. W. Variation in the autoradiographic technique: I. Emulsion-developer combinations assessed by photometric measurement of single silver grains. J Histochem Cytochem. 1976 Oct;24(10):1057–1064. doi: 10.1177/24.10.977937. [DOI] [PubMed] [Google Scholar]
  17. Neutra M., Leblond C. P. Radioautographic comparison of the uptake of galactose-H and glucose-H3 in the golgi region of various cells secreting glycoproteins or mucopolysaccharides. J Cell Biol. 1966 Jul;30(1):137–150. doi: 10.1083/jcb.30.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Neutra M., Leblond C. P. Synthesis of the carbohydrate of mucus in the golgi complex as shown by electron microscope radioautography of goblet cells from rats injected with glucose-H3. J Cell Biol. 1966 Jul;30(1):119–136. doi: 10.1083/jcb.30.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Paul M., Goldsmith M. R., Hunsley J. R., Kafatos F. C. Specific protein synthesis in cellular differentiation. Production of eggshell proteins by silkmoth follicular cells. J Cell Biol. 1972 Dec;55(3):653–680. doi: 10.1083/jcb.55.3.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Paul M., Kafaots F. C. Specific protein synthesis in cellular differentiation. II. The program of protein synthetic changes during chorion formation by slikmoth follicles, and its implementation in organ culture. Dev Biol. 1975 Jan;42(1):141–159. doi: 10.1016/0012-1606(75)90320-6. [DOI] [PubMed] [Google Scholar]
  21. REVEL J. P., HAY E. D. AN AUTORADIOGRAPHIC AND ELECTRON MICROSCOPIC STUDY OF COLLAGEN SYNTHESIS IN DIFFERENTIATING CARTILAGE. Z Zellforsch Mikrosk Anat. 1963 Oct 8;61:110–144. doi: 10.1007/BF00341524. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. ROGERS A. W. A simple photometric device for the quantitation of silver grains in autoradiographs of tissue sections. Exp Cell Res. 1961 Aug;24:228–239. doi: 10.1016/0014-4827(61)90425-6. [DOI] [PubMed] [Google Scholar]
  24. Ross R., Benditt E. P. Wound healing and collagen formation. V. Quantitative electron microscope radioautographic observations of proline-H3 utilization by fibroblasts. J Cell Biol. 1965 Oct;27(1):83–106. doi: 10.1083/jcb.27.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Scheele G. A., Palade G. E. Studies on the guinea pig pancreas. Parallel discharge of exocrine enzyme activities. J Biol Chem. 1975 Apr 10;250(7):2660–2670. [PubMed] [Google Scholar]
  26. Tartakoff A. M., Jamieson J. D., Scheele G. A., Palade G. E. Studies on the pancreas of the guinea pig. Parallel processing and discharge of exocrine proteins. J Biol Chem. 1975 Apr 10;250(7):2671–2677. [PubMed] [Google Scholar]
  27. 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]
  28. Yund M. A., Yund E. W., Kafatos F. C. A computer method for analysis of radioactivity data from single and double labeled experiments. Biochem Biophys Res Commun. 1971 May 21;43(4):717–722. doi: 10.1016/0006-291x(71)90674-7. [DOI] [PubMed] [Google Scholar]

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

RESOURCES