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PMID: 2138058 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Cell-free protein sorting to the regulated and constitutive secretory pathways.

Cell ·Vol. 60 ·No. 5 ·1990-03-09 ·Pages 837-47

Tooze SA, Huttner WB

Abstract

To elucidate the mechanism of secretory granule formation, we here identify the first intermediate in this process, the immature secretory granule, in the neuroendocrine cell line PC12 and demonstrate the packaging of a regulated secretory protein, secretogranin II, to immature secretory granules in a cell-free system. The formation of immature secretory granules was as fast (t1/2 approximately 5 min) as that of constitutive secretory vesicles identified by the presence of a rapidly secreted heparan sulfate proteoglycan. Using the cell-free system, the formation of post-Golgi secretory vesicles was found to be dependent upon ATP. Two distinct populations of vesicles were formed: immature secretory granules containing secretogranin II and constitutive secretory vesicles containing the heparan sulfate proteoglycan. These results show that in a cell-free system, a constitutive and a regulated secretory protein are sorted upon exit from the trans-Golgi network.

MeSH Terms
Adenosine Triphosphate/metabolism Adrenal Gland Neoplasms Animals Cell Line Cell-Free System Chondroitin Sulfate Proteoglycans/genetics Cytoplasmic Granules/metabolism,ultrastructure Glycosaminoglycans/genetics Golgi Apparatus/metabolism,ultrastructure Heparan Sulfate Proteoglycans Heparitin Sulfate/genetics Kinetics Microscopy, Electron Pheochromocytoma Protein Processing, Post-Translational Proteoglycans/genetics
Chemicals
Chondroitin Sulfate Proteoglycans Glycosaminoglycans Heparan Sulfate Proteoglycans Proteoglycans Adenosine Triphosphate Heparitin Sulfate
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Tooze S A
European Molecular Biology Laboratory, Heidelberg, Federal Republic of Germany.
Huttner W B
References (37)
37 references, click to expand
  1. Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation.
    Cell. 1983 Aug;34(1):233-43 PMID: 6883510
  2. Reconstitution of an endocytic fusion event in a cell-free system.
    Cell. 1985 Dec;43(3 Pt 2):643-52 PMID: 4075403
  3. A polarized epithelial cell mutant deficient in translocation of UDP-galactose into the Golgi complex.
    J Biol Chem. 1988 Nov 5;263(31):16283-90 PMID: 3141404
  4. Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine.
    Cell. 1984 Dec;39(2 Pt 1):405-16 PMID: 6498939
  5. Intracellular transport and packaging of prolactin: a quantitative electron microscope autoradiographic study of mammotrophs dissociated from rat pituitaries.
    Endocrinology. 1978 Jan;102(1):296-311 PMID: 743954
  6. The primary structure of human secretogranin II, a widespread tyrosine-sulfated secretory granule protein that exhibits low pH- and calcium-induced aggregation.
    J Biol Chem. 1989 Jul 15;264(20):12009-15 PMID: 2745426
  7. Secretogranins I and II: two tyrosine-sulfated secretory proteins common to a variety of cells secreting peptides by the regulated pathway.
    J Cell Biol. 1985 Nov;101(5 Pt 1):1999-2011 PMID: 4055903
  8. The major tyrosine-sulfated protein of the bovine anterior pituitary is a secretory protein present in gonadotrophs, thyrotrophs, mammotrophs, and corticotrophs.
    J Cell Biol. 1985 Mar;100(3):928-37 PMID: 3972902
  9. Clathrin-coated vesicular transport of secretory proteins during the formation of ACTH-containing secretory granules in AtT20 cells.
    J Cell Biol. 1986 Sep;103(3):839-50 PMID: 3017997
  10. Chromogranins A, B, and C: widespread constituents of secretory vesicles.
    Ann N Y Acad Sci. 1987;493:120-34 PMID: 3296906
  11. Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi.
    Annu Rev Biochem. 1987;56:829-52 PMID: 3304148
  12. The effect of alpha-latrotoxin on the neurosecretory PC12 cell line: electron microscopy and cytotoxicity studies.
    Neuroscience. 1983 Nov;10(3):1011-24 PMID: 6646424
  13. Mechanism of compartmentation of secretory proteins: transport of exocrine pancreatic proteins across the microsomal membrane.
    J Cell Biol. 1980 Dec;87(3 Pt 1):611-28 PMID: 7462318
  14. Studies on the biosynthesis of cartilage proteoglycan in a model system of cultured chondrocytes from the Swarm rat chondrosarcoma.
    J Cell Biochem. 1984;26(4):261-78 PMID: 6530407
  15. Inhibition of tyrosine sulfation in the trans-Golgi retards the transport of a constitutively secreted protein to the cell surface.
    J Cell Biol. 1988 Nov;107(5):1655-67 PMID: 3182933
  16. Amyloid beta protein precursor is possibly a heparan sulfate proteoglycan core protein.
    Science. 1988 Jul 8;241(4862):223-6 PMID: 2968652
  17. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor.
    Proc Natl Acad Sci U S A. 1976 Jul;73(7):2424-8 PMID: 1065897
  18. Constitutive and regulated secretion of proteins.
    Annu Rev Cell Biol. 1987;3:243-93 PMID: 3318877
  19. The trans Golgi network: sorting at the exit site of the Golgi complex.
    Science. 1986 Oct 24;234(4775):438-43 PMID: 2945253
  20. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples.
    Anal Biochem. 1978 Jun 15;87(1):206-10 PMID: 98070
  21. Pathways of protein secretion in eukaryotes.
    Science. 1985 Oct 4;230(4721):25-32 PMID: 2994224
  22. Sorting of progeny coronavirus from condensed secretory proteins at the exit from the trans-Golgi network of AtT20 cells.
    J Cell Biol. 1987 Sep;105(3):1215-26 PMID: 2821011
  23. Tyrosine-O-sulfated proteins of PC12 pheochromocytoma cells and their sulfation by a tyrosylprotein sulfotransferase.
    J Biol Chem. 1983 Sep 25;258(18):11326-34 PMID: 6577005
  24. The molecular function of adrenal chromaffin granules: established facts and unresolved topics.
    Neuroscience. 1986 Jun;18(2):261-90 PMID: 2942794
  25. Tyrosine sulfation is a trans-Golgi-specific protein modification.
    J Cell Biol. 1987 Dec;105(6 Pt 1):2655-64 PMID: 3121635
  26. The trans-most cisternae of the Golgi complex: a compartment for sorting of secretory and plasma membrane proteins.
    Cell. 1987 Dec 24;51(6):1039-51 PMID: 2826013
  27. Determination and occurrence of tyrosine O-sulfate in proteins.
    Methods Enzymol. 1984;107:200-23 PMID: 6390090
  28. Isolation of exocytic carrier vesicles from BHK cells.
    Cell. 1989 Aug 25;58(4):719-27 PMID: 2504496
  29. Condensation-sorting events in the rough endoplasmic reticulum of exocrine pancreatic cells.
    J Cell Biol. 1989 Jul;109(1):35-50 PMID: 2745555
  30. Relationship between NGF-mediated volume increase and "priming effect" in fast and slow reacting clones of PC12 pheochromocytoma cells. Role of cAMP.
    Exp Cell Res. 1983 Apr 15;145(1):179-90 PMID: 6303817
  31. Release of putative exocytic transport vesicles from perforated MDCK cells.
    EMBO J. 1988 Dec 20;7(13):4075-85 PMID: 3243273
  32. Progress in unraveling pathways of Golgi traffic.
    Annu Rev Cell Biol. 1985;1:447-88 PMID: 3916320
  33. Demonstration of an extensive trans-tubular network continuous with the Golgi apparatus stack that may function in glycosylation.
    Cell. 1985 Nov;43(1):287-95 PMID: 3000603
  34. Chondroitin sulfate and heparan sulfate proteoglycans of PC12 pheochromocytoma cells.
    J Biol Chem. 1989 Jul 5;264(19):11436-43 PMID: 2525557
  35. The Golgi apparatus (complex)-(1954-1981)-from artifact to center stage.
    J Cell Biol. 1981 Dec;91(3 Pt 2):77s-103s PMID: 7033246
  36. An antibody against secretogranin I (chromogranin B) is packaged into secretory granules.
    J Cell Biol. 1989 Jul;109(1):17-34 PMID: 2663878
  37. Protein sorting among two distinct export pathways occurs from the content of maturing exocrine storage granules.
    J Cell Biol. 1987 Dec;105(6 Pt 1):2675-84 PMID: 3500952
Article Info
Journal
Cell
Abbr.
Cell
ISSN
0092-8674
Published
1990-03-09
Pages
837-47
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC7125605
Subset
IM
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