Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1968 Mar 1;36(3):453–483. doi: 10.1083/jcb.36.3.453

PROTEIN UPTAKE INTO MULTIVESICULAR BODIES AND STORAGE GRANULES IN THE FAT BODY OF AN INSECT

M Locke 1, Janet V Collins 1
PMCID: PMC2107381  PMID: 5645544

Abstract

The fat body in Calpodes ethlius (Lepidoptera, Hesperiidae) takes up protein from the blood throughout the larval stage before pupation. Depending upon the phase of development, the protein appears in multivesicular bodies, in large storage granules, and in structures of intermediate form. There are three phases in the 8 days of the last larval stage; the first devoted to growth (molting to 66 hr), the second to synthesis for storage or export (M + 66 to M + 156 hr), and the third to preparation for pupation (M + 156 to pupation at M + 192 hr). From M + O to M + 156 and from M + 180 to M + 188 hr, protein is taken up into multivesicular bodies. Larger MVB's form a continuous series with the protein granules formed from M + 162 to M + 180 hr. Blood proteins increase in concentration and amount from M + 66 to M + 156 hr at the same time as the fat body cells have a high rate of incorporation of amino acids and a structure appropriate for protein synthesis. During granule formation, both amino acid incorporation and blood protein concentration decrease. Since foreign proteins injected into the blood appear in the granules, they are probably made mainly from sequestered blood. Protein uptake involves two stages: concentration between the cells, and ingestion in pinocytotic vesicles. The vesicles fuse to become MVB's or storage granules, depending upon their rates of growth and the addition of lytic enzymes. Since MVB's do not accumulate in the fat body and since many of them contain acid phosphatase and appear empty, they are presumed to be concerned in protein turnover.

Full Text

The Full Text of this article is available as a PDF (3.2 MB).

Selected References

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

  1. BISHOP G. H. Nuclear and cytoplasmic changes in fat body cells of the queen bee during metamorphosis. J Exp Zool. 1958 Apr;137(3):501–525. doi: 10.1002/jez.1401370308. [DOI] [PubMed] [Google Scholar]
  2. BUTTERWORTH F. M., BODENSTEIN D., KING R. C. ADIPOSE TISSUE OF DROSOPHILA MELANOGASTER. I. AN EXPERIMENTAL STUDY OF LARVAL FAT BODY. J Exp Zool. 1965 Mar;158:141–153. doi: 10.1002/jez.1401580203. [DOI] [PubMed] [Google Scholar]
  3. CURTIS A. S. Area and volume measurements by random sampling methods. Med Biol Illus. 1960 Oct;10:261–266. [PubMed] [Google Scholar]
  4. Christiansen R. G., Marshall J. M. A study of phagocytosis in the ameba Chaos chaos. J Cell Biol. 1965 Jun;25(3):443–457. doi: 10.1083/jcb.25.3.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. De Duve C., Wattiaux R. Functions of lysosomes. Annu Rev Physiol. 1966;28:435–492. doi: 10.1146/annurev.ph.28.030166.002251. [DOI] [PubMed] [Google Scholar]
  6. EASTON J. M., GOLDBERG B., GREEN H. Demonstration of surface antigens and pinocytosis in mammalian cells with ferritin-antibody conjugates. J Cell Biol. 1962 Feb;12:437–443. doi: 10.1083/jcb.12.2.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. FARQUHAR M. G., PALADE G. E. Segregation of ferritin in glomerular protein absorption droplets. J Biophys Biochem Cytol. 1960 Apr;7:297–304. doi: 10.1083/jcb.7.2.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. FAWCETT D. W. SURFACE SPECIALIZATIONS OF ABSORBING CELLS. J Histochem Cytochem. 1965 Feb;13:75–91. doi: 10.1177/13.2.75. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. HOLTZER H., HOLTZER S. The in vitro uptake of fluorescein labelled plasma proteins. I. Mature cells. C R Trav Lab Carlsberg. 1960;31:373–408. [PubMed] [Google Scholar]
  11. Locke M., Collins J. V. Protein uptake in multivesicular bodies in the molt-intermolt cycle of an insect. Science. 1967 Jan 27;155(3761):467–469. doi: 10.1126/science.155.3761.467. [DOI] [PubMed] [Google Scholar]
  12. Locke M., Collins J. V. Sequestration of protein by the fat body of an insect. Nature. 1966 Apr 30;210(5035):552–553. doi: 10.1038/210552a0. [DOI] [PubMed] [Google Scholar]
  13. Locke M. The structure and formation of the cuticulin layer in the epicuticle of an insect, Calpodes ethlius (Lepidoptera, Hesperiidae). J Morphol. 1966 Apr;118(4):461–494. doi: 10.1002/jmor.1051180403. [DOI] [PubMed] [Google Scholar]
  14. MILLER F., PALADE G. E. LYTIC ACTIVITIES IN RENAL PROTEIN ABSORPTION DROPLETS. AN ELECTRON MICROSCOPICAL CYTOCHEMICAL STUDY. J Cell Biol. 1964 Dec;23:519–552. doi: 10.1083/jcb.23.3.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Maddrell S. H., Treherne J. E. A neural fat-body sheath in a phytophagous insect (Carausius morosus). Nature. 1966 Jul 9;211(5045):215–216. doi: 10.1038/211215a0. [DOI] [PubMed] [Google Scholar]
  16. Miller A. T., Jr, Hale D. M., Alexander K. D. Histochemical studies on the uptake of horseradish peroxidase by rat kidney slices. J Cell Biol. 1965 Nov;27(2):305–312. doi: 10.1083/jcb.27.2.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. PALAY S. L. The fine structure of secretory neurons in the preoptic nucleus of the goldish (Carassius auratus). Anat Rec. 1960 Dec;138:417–443. doi: 10.1002/ar.1091380404. [DOI] [PubMed] [Google Scholar]
  18. Price G. M., Bosman T. The electrophoretic separation of proteins isolated from the larva of the blowfly, Calliphora erythrocephala. J Insect Physiol. 1966 Jul;12(7):741–745. doi: 10.1016/0022-1910(66)90026-6. [DOI] [PubMed] [Google Scholar]
  19. Price G. M. The in vitro incorporation of [U-14C] valine into fat body protein of the larva of the blowfly, Calliphora erythrocephala. J Insect Physiol. 1966 Jul;12(7):731–740. doi: 10.1016/0022-1910(66)90025-4. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. ROSENBLUTH J., WISSIG S. L. THE DISTRIBUTION OF EXOGENOUS FERRITIN IN TOAD SPINAL GANGLIA AND THE MECHANISM OF ITS UPTAKE BY NEURONS. J Cell Biol. 1964 Nov;23:307–325. doi: 10.1083/jcb.23.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. ROTH T. F., PORTER K. R. YOLK PROTEIN UPTAKE IN THE OOCYTE OF THE MOSQUITO AEDES AEGYPTI. L. J Cell Biol. 1964 Feb;20:313–332. doi: 10.1083/jcb.20.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. RYSER H., CAULFIELD J. B., AUB J. C. Studies on protein uptake by isolated tumor cells. I. Electron microscopic evidence of ferritin uptake by Ehrlich ascites tumor cells. J Cell Biol. 1962 Aug;14:255–268. doi: 10.1083/jcb.14.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. SHIGEMATSU H. Synthesis of blood protein by the fat body in the silkworm, Bombyx mori L. Nature. 1958 Sep 27;182(4639):880–882. doi: 10.1038/182880b0. [DOI] [PubMed] [Google Scholar]
  25. SOTELO J. R., PORTER K. R. An electron microscope study of the rat ovum. J Biophys Biochem Cytol. 1959 Mar 25;5(2):327–342. doi: 10.1083/jcb.5.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. STRAUS W. FACTORS AFFECTING THE CYTOCHEMICAL REACTION OF PEROXIDASE WITH BENZIDINE AND THE STABILITY OF THE BLUE REACTION PRODUCT. J Histochem Cytochem. 1964 Jun;12:462–469. doi: 10.1177/12.6.462. [DOI] [PubMed] [Google Scholar]
  27. STRAUS W. FACTORS AFFECTING THE STATE OF INJECTED HORSERADISH PEROXIDASE IN ANIMAL TISSUES AND PROCEDURES FOR THE STUDY OF PHAGOSOMES AND PHAGO-LYSOSOMES. J Histochem Cytochem. 1964 Jun;12:470–480. doi: 10.1177/12.6.470. [DOI] [PubMed] [Google Scholar]
  28. Stay B. Protein uptake in the oocytes of the cecropia moth. J Cell Biol. 1965 Jul;26(1):49–62. doi: 10.1083/jcb.26.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. VON GAUDECKER UBER DEN FORMWECHSEL EINIGER ZELLORGANELLE BEI DER BILDUNG DER RESERVESTOFFE IM FETTKOERPER VON DROSOPHILA-LARVEN. Z Zellforsch Mikrosk Anat. 1963 Oct 8;61:56–95. [PubMed] [Google Scholar]

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

RESOURCES