Abstract
The secretion of insulin by the pancreatic B-cell involves a passage of the newly synthetized (pro)insulin polypeptides across the Golgi apparatus, at the trans pole of which secretory proteins are released as a population of secretory granules characterized by a clathrinlike coat on segments of their limiting membrane. When the conversion of radiolabeled proinsulin to insulin was inhibited by replacing arginine and lysine with the aminoacid analogs, canavanine and thialysine, the nonconverted radioactive material remained associated with Golgi- derived, coated secretory granules. The coat was characterized as clathrin-containing by immunocytochemistry. Under analog treatment, the noncoated, storage secretory granules did not become markedly labeled during the pulse-chase experiment. These data are compatible with the hypothesis that in normal conditions, the maturation of the coated compartment into noncoated granules is linked to the effective conversion of the prohormone.
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- Armbruster B. L., Carlemalm E., Chiovetti R., Garavito R. M., Hobot J. A., Kellenberger E., Villiger W. Specimen preparation for electron microscopy using low temperature embedding resins. J Microsc. 1982 Apr;126(Pt 1):77–85. doi: 10.1111/j.1365-2818.1982.tb00358.x. [DOI] [PubMed] [Google Scholar]
- 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]
- Docherty K., Steiner D. F. Post-translational proteolysis in polypeptide hormone biosynthesis. Annu Rev Physiol. 1982;44:625–638. doi: 10.1146/annurev.ph.44.030182.003205. [DOI] [PubMed] [Google Scholar]
- Farquhar M. G., Palade G. E. The Golgi apparatus (complex)-(1954-1981)-from artifact to center stage. J Cell Biol. 1981 Dec;91(3 Pt 2):77s–103s. doi: 10.1083/jcb.91.3.77s. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Halban P. A. Inhibition of proinsulin to insulin conversion in rat islets using arginine and lysine analogs. Lack of effect on rate of release of modified products. J Biol Chem. 1982 Nov 25;257(22):13177–13180. [PubMed] [Google Scholar]
- Halban P. A., Wollheim C. B., Blondel B., Renold A. E. Long-term exposure of isolated pancreatic islets to mannoheptulose: evidence for insulin degradation in the beta cell. Biochem Pharmacol. 1980 Oct 1;29(19):2625–2633. doi: 10.1016/0006-2952(80)90077-5. [DOI] [PubMed] [Google Scholar]
- Lacy P. E., Kostianovsky M. Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes. 1967 Jan;16(1):35–39. doi: 10.2337/diab.16.1.35. [DOI] [PubMed] [Google Scholar]
- Louvard D., Morris C., Warren G., Stanley K., Winkler F., Reggio H. A monoclonal antibody to the heavy chain of clathrin. EMBO J. 1983;2(10):1655–1664. doi: 10.1002/j.1460-2075.1983.tb01640.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Merisko E. M., Farquhar M. G., Palade G. E. Coated vesicle isolation by immunoadsorption on Staphylococcus aureus cells. J Cell Biol. 1982 Mar;92(3):846–857. doi: 10.1083/jcb.92.3.846. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noe B. D. Inhibition of islet prohormone to hormone conversion by incorporation of arginine and lysine analogs. J Biol Chem. 1981 May 25;256(10):4940–4946. [PubMed] [Google Scholar]
- Orci L. A portrait of the pancreatic B-cell. The Minkowski Award Lecture delivered on July 19, 1973, during the 8th Congress of the International Diabetes Federation, held in Brussels, Belgium. Diabetologia. 1974 Jun;10(3):163–187. doi: 10.1007/BF00423031. [DOI] [PubMed] [Google Scholar]
- Orci L., Halban P., Amherdt M., Ravazzola M., Vassalli J. D., Perrelet A. A clathrin-coated, Golgi-related compartment of the insulin secreting cell accumulates proinsulin in the presence of monensin. Cell. 1984 Nov;39(1):39–47. doi: 10.1016/0092-8674(84)90189-2. [DOI] [PubMed] [Google Scholar]
- Orci L., Like A. A., Amherdt M., Blondel B., Kanazawa Y., Marliss E. B., Lambert A. E., Wollheim C. B., Renold A. E. Monolayer cell culture of neonatal rat pancreas: an ultrastructural and biochemical study of functioning endocrine cells. J Ultrastruct Res. 1973 May;43(3):270–297. doi: 10.1016/s0022-5320(73)80039-5. [DOI] [PubMed] [Google Scholar]
- Patzelt C., Labrecque A. D., Duguid J. R., Carroll R. J., Keim P. S., Heinrikson R. L., Steiner D. F. Detection and kinetic behavior of preproinsulin in pancreatic islets. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1260–1264. doi: 10.1073/pnas.75.3.1260. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pearse B. M. Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1255–1259. doi: 10.1073/pnas.73.4.1255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roth J., Bendayan M., Orci L. Ultrastructural localization of intracellular antigens by the use of protein A-gold complex. J Histochem Cytochem. 1978 Dec;26(12):1074–1081. doi: 10.1177/26.12.366014. [DOI] [PubMed] [Google Scholar]
- Steiner D. F., Docherty K., Carroll R. Golgi/granule processing of peptide hormone and neuropeptide precursors: a minireview. J Cell Biochem. 1984;24(2):121–130. doi: 10.1002/jcb.240240204. [DOI] [PubMed] [Google Scholar]
- Steiner D. F., Kemmler W., Tager H. S., Peterson J. D. Proteolytic processing in the biosynthesis of insulin and other proteins. Fed Proc. 1974 Oct;33(10):2105–2115. [PubMed] [Google Scholar]
- Stäubli W., Schweizer W., Suter J., Weibel E. R. The proliferative response of hepatic peroxidomes of neonatal rats to treatment with SU-13 437 (nafenopin). J Cell Biol. 1977 Sep;74(3):665–689. doi: 10.1083/jcb.74.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]