DOI: 10.1083/jcb.143.7.1831. Homotypic Fusion of Immature Secretory Granules during Maturation in a Cell-free Assay

Homotypic Fusion of Immature Secretory Granules during Maturation in a Cell-free Assay

10.1083/jcb.143.7.1831

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

The biogenesis of secretory granules embodies several morphological and biochemical changes. In particular, in neuroendocrine cells maturation of secretory granules is characterized by an increase in size which has been proposed to reflect homotypic fusion of immature secretory granules (ISGs). Here we describe an assay that provides the first biochemical evidence for such a fusion event and allows us to analyze its regulation. The assay reconstitutes homotypic fusion between one population of ISGs containing a [35S]sulfate-labeled substrate, secretogranin II (SgII), and a second population containing the prohormone convertase PC2. Both substrate and enzyme are targeted exclusively to ISGs. Fusion is measured by quantification of a cleavage product of SgII produced by PC2. With this assay we show that fusion only occurs between ISGs and not between ISGs and MSGs, is temperature dependent, and requires ATP and GTP and cytosolic proteins. NSF (N-ethylmaleimide–sensitive fusion protein) is amongst the cytosolic proteins required, whereas we could not detect a requirement for p97. The ability to reconstitute ISG fusion in a cell-free assay is an important advance towards the identification of molecules involved in the maturation of secretory granules and will increase our understanding of this process.

Bibliography

UrbÃ©, S., Page, L. J., & Tooze, S. A. (1998). Homotypic Fusion of Immature Secretory Granules during Maturation in a Cell-free Assay. The Journal of Cell Biology, 143(7), 1831â1844.

Authors 3

Sylvie Urbé (first)
Lesley J. Page (additional)
Sharon A. Tooze (additional)

References 67 Referenced 64

10.1016/0092-8674(95)90269-4 / Cell / The formation of Golgi stacks from vesiculated Golgi membranes requires two distinct fusion events by Acharya (1995)
10.1083/jcb.129.3.577 / J Cell Biol / Reconstitution of vesiculated Golgi membranes into stacks of cisternae: requirement of NSF in stack formation by Acharya (1995)
10.1074/jbc.273.17.10317 / J Biol Chem / Seven novel mammalian SNARE proteins localize to distinct membrane compartments by Advani (1998)
10.1016/0014-5793(91)81438-E / FEBS (Fed Eur Biochem Soc) Lett / Trimeric G-proteins of the trans-Golgi network are involved in the formation of constitutive secretory vesicles and immature secretory granules by Barr (1991)
10.1016/S0021-9258(18)42170-9 / J Biol Chem / Identification of the type 2 proinsulin processing endopeptidase as PC2, a member of the eukaryote subtilisin family by Bennett (1992)
10.1073/pnas.85.21.7852 / Proc Natl Acad Sci USA / Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport by Block (1988)
10.1038/387133a0 / Nature / Protein transport A fusion of new ideas by Bock (1997)
10.1091/mbc.8.7.1261 / Mol Biol Cell / Syntaxin 6 functions in trans Golgi network vesicle trafficking by Bock (1997)
10.1146/annurev.cb.03.110187.001331 / Annu Rev Cell Biol / Constitutive and regulated secretion of proteins by Burgess (1987)
10.1083/jcb.127.3.693 / J Cell Biol / Transport via the regulated secretory pathway in semi-intact PC12 cells: role of intra-cisternal calcium and pH in the transport and sorting of secretogranin II by Carnell (1994)
10.1083/jcb.138.3.495 / J Cell Biol / Phospholipase D stimulates release of nascent secretory vesicles from the trans-Golgi network by Chen (1997)
10.1016/0092-8674(90)90482-T / Cell / SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast by Clary (1990)
10.1083/jcb.119.6.1469 / J Cell Biol / In vitro reactions of vacuole inheritance in Saccharomyces cerevisiae. by Conradt (1992)
10.1016/S0092-8674(00)81860-7 / Cell / Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpefatmice by Cool (1997)
10.1016/0092-8674(85)90236-3 / Cell / Reconstitution of an endocytic fusion event in a cell-free system by Davey (1985)
10.1016/S0021-9258(18)68754-X / J Biol Chem / In vitro fusion of endosomes following receptor-mediated endocytosis by Diaz (1988)
10.1038/339398a0 / Nature / Vesicle fusion following receptor-mediated endocytosis requires a protein active in Golgi transport by Diaz (1989)
10.1042/bj3100777 / Biochem J / Characterization of the endopeptidase PC2 activity towards SgII in stably transfected PC12 cells by Dittié (1995)
10.1083/jcb.132.4.523 / J Cell Biol / The AP-1 adaptor complex binds to immature secretory granules from PC12 cells, and is regulated by ADP- ribosylation factor by Dittié (1996)
10.1093/emboj/16.16.4859 / EMBO (Eur Mol Biol Organ) J / Interaction of furin in immature secretory granules from neuroendocrine cells with the AP-1 adaptor complex is modulated by casein kinase II phosphorylation by Dittié (1997)
10.1091/mbc.7.12.2019 / Mol Biol Cell / Distinct cellular locations of the syntaxin family of proteins in rat pancreatic acinar cells by Gaisano (1996)
10.1093/nar/16.24.11811 / Nucl Acids Res / The primary structure of rat secretogranin II deduces from a cDNA sequence by Gerdes (1988)
10.1016/S0962-8924(98)01272-0 / Trends Cell Biol / A new beat for the SNARE drum by Götte (1998)
10.1002/j.1460-2075.1986.tb04615.x / EMBO (Eur Mol Biol Organ) J / Reconstitution of vesicle fusions occurring in endocytosis with a cell-free system by Gruenberg (1986)
10.1016/S0014-4827(83)80019-6 / Exp Cell Res / Relationship between NGF-mediated volume increase and “priming effect” in fast and slow reacting clones of PC12 pheochromocytoma cells by Heumann (1983)
10.1074/jbc.272.44.27532 / J Biol Chem / Proinsulin targeting to the regulated pathway is not impaired in carboxypeptidase E-deficient Cpefat/Cpefatmice by Irminger (1997)
10.1074/jbc.272.44.27737 / J Biol Chem / A novel assay reveals a role for soluble N-ethylmaleimide-sensitive fusion attachment protein in mannose 6-phosphate receptor transport from endosomes to the trans-Golgi network by Itin (1997)
10.1083/jcb.141.2.359 / J Cell Biol / Mannose 6-phosphate receptors are sorted from immature secretory granules via adaptor protein AP-1, clathrin, and syntaxin 6-positive vesicles by Klumperman (1998)
10.1038/40411 / Nature / p47 is a cofactor for p97-mediated membrane fusion by Kondo (1997)
10.1083/jcb.126.1.77 / J Cell Biol / Distinct molecular mechanisms for protein sorting within immature secretory granules of pancreatic β-cells by Kuliawat (1994)
10.1083/jcb.137.3.595 / J Cell Biol / Differential sorting of lysosomal enzymes out of the regulated secretory pathway in pancreatic β-cells by Kuliawat (1997)
10.1046/j.1471-4159.1998.70010374.x / J Neurochem / Proteolytic processing of chromogranin B and secretogranin II by prohormone convertases by Laslop (1998)
10.1016/0092-8674(95)90268-6 / Cell / Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes by Latterich (1995)
10.1016/S0021-9258(17)44421-8 / J Biol Chem / Tyrosine-O-sulfated proteins of PC12 pheochromocytoma cells and their sulfation by a tyrosylprotein sulfotransferase by Lee (1983)
10.1016/S0092-8674(00)81084-3 / Cell / Sec18p (NSF)-driven release of Sec17p (α-SNAP) can precede docking and fusion of yeast vacuoles by Mayer (1996)
10.1016/0092-8674(95)90018-7 / Cell / Enigma variations: protein mediators of membrane fusion by Mellman (1995)
10.1083/jcb.124.1.33 / J Cell Biol / Differential trafficking of soluble and integral membrane secretory granule-associated proteins by Milgram (1994)
10.1038/387199a0 / Nature / Homotypic vacuolar fusion mediated by t-and v-SNAREs by Nichols (1997)
{'key': '2023072900364860100_B39', 'first-page': '35', 'article-title': 'Two membrane-bound forms of tyrosylprotein sulfotransferase as revealed by phase partitioning in Triton X-114', 'volume': '58', 'author': 'Niehrs', 'year': '1992', 'journal-title': 'Eur J Cell Biol'} / Eur J Cell Biol / Two membrane-bound forms of tyrosylprotein sulfotransferase as revealed by phase partitioning in Triton X-114 by Niehrs (1992)
10.1038/377544a0 / Nature / A role for phosphatidylinositol transfer protein in secretory vesicle formation by Ohashi (1995)
10.1083/jcb.126.5.1149 / J Cell Biol / pH-independent and -dependent cleavage of proinsulin in the same secretory vesicle by Orci (1994)
10.1016/S0092-8674(00)81129-0 / Cell / Organelle membrane fusion: a novel function for the syntaxin homolog Ufe1p in ER membrane fusion by Patel (1998)
10.1016/0092-8674(95)90270-8 / Cell / An NSF-like ATPase, p97, and NSF mediate cisternal regrowth from mitotic Golgi fragments by Rabouille (1995)
10.1083/jcb.129.3.605 / J Cell Biol / Reassembly of Golgi stacks from mitotic Golgi fragments in a cell-free system by Rabouille (1995)
10.1016/S0092-8674(00)81128-9 / Cell / Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro by Rabouille (1998)
10.1242/jcs.110.17.2079 / J Cell Sci / NSF is required for transport from early to late endosomes by Robinson (1997)
10.1091/mbc.5.7.773 / Mol Biol Cell / Multiple N-ethylmaleimide-sensitive components are required for endosomal vesicle fusion by Rodriguez (1994)
10.1038/372055a0 / Nature / Mechanisms of intracellular protein transport by Rothman (1994)
10.1083/jcb.91.1.240 / J Cell Biol / High resolution analysis of the secretory pathway in mammotrophs of the rat anterior pituitary by Salpeter (1981)
10.1083/jcb.31.2.319 / J Cell Biol / Lysosome function in the regulation of the secretory process in cells of the anterior pituitary gland by Smith (1966)
10.1016/0092-8674(93)90376-2 / Cell / A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion by Sollner (1993)
10.1016/0960-9822(91)90198-6 / Curr Biol / Prohormone convertases revealed at last by Steiner (1991)
10.1016/S0960-9822(06)00247-8 / Curr Biol / Protein secretion: puzzling receptors by Thiele (1997)
10.1016/0014-5793(91)80805-D / FEBS (Fed Eur Biochem Soc) Lett / Biogenesis of secretory granules Implications arising from the immature secretory granule in the regulated pathway of secretion by Tooze (1991)
10.1016/S0167-4889(98)00059-7 / Biochim Biophys Acta / Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells by Tooze (1998)
10.1016/0092-8674(90)90097-X / Cell / Cell-free protein sorting to the regulated and constitutive secretory pathways by Tooze (1990)
10.1083/jcb.115.6.1491 / J Cell Biol / Characterization of the immature secretory granule, an intermediate in granule biogenesis by Tooze (1991)
10.1074/jbc.272.21.13479 / J Biol Chem / A Rab GTPase is required for homotypic assembly of the endoplasmic reticulum by Turner (1997)
10.1042/bj3210065 / Biochem J / pH-dependent processing of secretogranin II by the endopeptidase PC2 in isolated immature secretory granules by Urbé (1997)
10.1016/S0167-4889(97)00050-5 / Biochim Biophys Acta / Formation of secretory vesicles in the biosynthetic pathway by Urbé (1997)
10.1083/jcb.139.3.665 / J Cell Biol / Homotypic lysosome fusion in macrophages: analysis using an in vitro assay by Ward (1997)
10.1016/S0092-8674(00)81404-X / Cell / SNAREpins: minimal machinery for membrane fusion by Weber (1998)
10.1083/jcb.108.5.1589 / J Cell Biol / Binding of an N-ethylmaleimide–sensitive fusion protein to golgi membranes requires both a soluble protein(s) and an integral membrane protein by Weidman (1989)
10.1038/362353a0 / Nature / SNAP family of NSF attachment proteins includes a brain- specific isoform by Whiteheart (1993)
10.1016/S0962-8924(00)88948-5 / Trends Cell Biol / SNAPs and NSF: general members of the fusion apparatus by Whiteheart (1995)
10.1016/S0167-4889(97)00039-6 / Biochim Biophys Acta / The roles of NSF, SNAPs and SNAREs during membrane fusion by Woodman (1997)
10.1111/j.1432-1033.1988.tb13972.x / Eur J Biochem / Fusion between vesicles from the pathway of receptor-mediated endocytosis in a cell-free system by Woodman (1988)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:45 p.m.)
Deposited	2 years, 1 month ago (July 28, 2023, 8:37 p.m.)
Indexed	11 months, 3 weeks ago (Sept. 8, 2024, 6:15 a.m.)
Issued	26 years, 8 months ago (Dec. 28, 1998)
Published	26 years, 8 months ago (Dec. 28, 1998)
Published Online	26 years, 8 months ago (Dec. 28, 1998)
Published Print	26 years, 8 months ago (Dec. 28, 1998)

Funders 0

None

BibTeX

@article{Urb__1998, title={Homotypic Fusion of Immature Secretory Granules during Maturation in a Cell-free Assay}, volume={143}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.143.7.1831}, DOI={10.1083/jcb.143.7.1831}, number={7}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Urbé, Sylvie and Page, Lesley J. and Tooze, Sharon A.}, year={1998}, month=dec, pages={1831–1844} }

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      "volume": "273",
      "author": "Advani",
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      "article-title": "Trimeric G-proteins of the trans-Golgi network are involved in the formation of constitutive secretory vesicles and immature secretory granules",
      "volume": "294",
      "author": "Barr",
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      "journal-title": "FEBS (Fed Eur Biochem Soc) Lett"
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      "first-page": "15229",
      "DOI": "10.1016/S0021-9258(18)42170-9",
      "article-title": "Identification of the type 2 proinsulin processing endopeptidase as PC2, a member of the eukaryote subtilisin family",
      "volume": "267",
      "author": "Bennett",
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      "journal-title": "J Biol Chem"
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      "article-title": "Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport",
      "volume": "85",
      "author": "Block",
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      "journal-title": "Proc Natl Acad Sci USA"
    },
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      "first-page": "133",
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      "article-title": "Protein transport A fusion of new ideas",
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      "year": "1997",
      "journal-title": "Nature"
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    },
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      "first-page": "2019",
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      "volume": "7",
      "author": "Gaisano",
      "year": "1996",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "2023072900364860100_B22",
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      "first-page": "11811",
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      "volume": "16",
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      "author": "Irminger",
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      "author": "Klumperman",
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      "author": "Kuliawat",
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      "volume": "70",
      "author": "Laslop",
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      "volume": "258",
      "author": "Lee",
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      "volume": "124",
      "author": "Milgram",
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      "author": "Nichols",
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      "author": "Ohashi",
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      "volume": "5",
      "author": "Rodriguez",
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      "volume": "91",
      "author": "Salpeter",
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      "author": "Thiele",
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      "author": "Tooze",
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      "volume": "321",
      "author": "Urb\u00e9",
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