Pro-hormone Secretogranin II Regulates Dense Core Secretory Granule Biogenesis in Catecholaminergic Cells
Processes underlying the formation of dense core secretory granules (DCGs) of neuroendocrine cells are poorly understood. Here, we present evidence that DCG biogenesis is dependent on the secretory protein secretogranin (Sg) II, a member of the granin family of pro-hormone cargo of DCGs in neuroendo...
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| Veröffentlicht in: | The Journal of biological chemistry 2010-03, Vol.285 (13), p.10030-10043 |
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| creator | Courel, Maïté Soler-Jover, Alex Rodriguez-Flores, Juan L. Mahata, Sushil K. Elias, Salah Montero-Hadjadje, Maïté Anouar, Youssef Giuly, Richard J. O'Connor, Daniel T. Taupenot, Laurent |
| description | Processes underlying the formation of dense core secretory granules (DCGs) of neuroendocrine cells are poorly understood. Here, we present evidence that DCG biogenesis is dependent on the secretory protein secretogranin (Sg) II, a member of the granin family of pro-hormone cargo of DCGs in neuroendocrine cells. Depletion of SgII expression in PC12 cells leads to a decrease in both the number and size of DCGs and impairs DCG trafficking of other regulated hormones. Expression of SgII fusion proteins in a secretory-deficient PC12 variant rescues a regulated secretory pathway. SgII-containing dense core vesicles share morphological and physical properties with bona fide DCGs, are competent for regulated exocytosis, and maintain an acidic luminal pH through the V-type H+-translocating ATPase. The granulogenic activity of SgII requires a pH gradient along this secretory pathway. We conclude that SgII is a critical factor for the regulation of DCG biogenesis in neuroendocrine cells, mediating the formation of functional DCGs via its pH-dependent aggregation at the trans-Golgi network. |
| doi_str_mv | 10.1074/jbc.M109.064196 |
| format | Article |
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Here, we present evidence that DCG biogenesis is dependent on the secretory protein secretogranin (Sg) II, a member of the granin family of pro-hormone cargo of DCGs in neuroendocrine cells. Depletion of SgII expression in PC12 cells leads to a decrease in both the number and size of DCGs and impairs DCG trafficking of other regulated hormones. Expression of SgII fusion proteins in a secretory-deficient PC12 variant rescues a regulated secretory pathway. SgII-containing dense core vesicles share morphological and physical properties with bona fide DCGs, are competent for regulated exocytosis, and maintain an acidic luminal pH through the V-type H+-translocating ATPase. The granulogenic activity of SgII requires a pH gradient along this secretory pathway. We conclude that SgII is a critical factor for the regulation of DCG biogenesis in neuroendocrine cells, mediating the formation of functional DCGs via its pH-dependent aggregation at the trans-Golgi network.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.M109.064196</identifier><identifier>PMID: 20061385</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Catecholamines - metabolism ; Cell Biology ; Cell/Exocytosis ; Cell/pH ; Cell/Secretion ; Cellular Biology ; Chlorocebus aethiops ; Chromaffin ; Chromaffin Granules - metabolism ; COS Cells ; Gene Silencing ; Genetic Vectors ; Hydrogen-Ion Concentration ; Life Sciences ; Methods/Fluorescence ; Neuroendocrine Cells - metabolism ; PC12 Cells ; Protein/Chimeras ; Protein/Intracellular Trafficking ; Rats ; Recombinant Fusion Proteins - metabolism ; RNA, Small Interfering - metabolism ; Secretogranin II - metabolism ; Secretory Vesicles - metabolism ; Subcellular Organelles/Vesicles ; Subcellular Processes</subject><ispartof>The Journal of biological chemistry, 2010-03, Vol.285 (13), p.10030-10043</ispartof><rights>2010 © 2010 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2010 by The American Society for Biochemistry and Molecular Biology, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c574t-2b70a342b368bf77a3690ec1cddd0e4819dda06693f15dcd93d606963effa8393</citedby><cites>FETCH-LOGICAL-c574t-2b70a342b368bf77a3690ec1cddd0e4819dda06693f15dcd93d606963effa8393</cites><orcidid>0000-0002-3215-4325 ; 0000-0001-8859-893X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2843166/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2843166/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20061385$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://normandie-univ.hal.science/hal-02334607$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Courel, Maïté</creatorcontrib><creatorcontrib>Soler-Jover, Alex</creatorcontrib><creatorcontrib>Rodriguez-Flores, Juan L.</creatorcontrib><creatorcontrib>Mahata, Sushil K.</creatorcontrib><creatorcontrib>Elias, Salah</creatorcontrib><creatorcontrib>Montero-Hadjadje, Maïté</creatorcontrib><creatorcontrib>Anouar, Youssef</creatorcontrib><creatorcontrib>Giuly, Richard J.</creatorcontrib><creatorcontrib>O'Connor, Daniel T.</creatorcontrib><creatorcontrib>Taupenot, Laurent</creatorcontrib><title>Pro-hormone Secretogranin II Regulates Dense Core Secretory Granule Biogenesis in Catecholaminergic Cells</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>Processes underlying the formation of dense core secretory granules (DCGs) of neuroendocrine cells are poorly understood. 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Here, we present evidence that DCG biogenesis is dependent on the secretory protein secretogranin (Sg) II, a member of the granin family of pro-hormone cargo of DCGs in neuroendocrine cells. Depletion of SgII expression in PC12 cells leads to a decrease in both the number and size of DCGs and impairs DCG trafficking of other regulated hormones. Expression of SgII fusion proteins in a secretory-deficient PC12 variant rescues a regulated secretory pathway. SgII-containing dense core vesicles share morphological and physical properties with bona fide DCGs, are competent for regulated exocytosis, and maintain an acidic luminal pH through the V-type H+-translocating ATPase. The granulogenic activity of SgII requires a pH gradient along this secretory pathway. We conclude that SgII is a critical factor for the regulation of DCG biogenesis in neuroendocrine cells, mediating the formation of functional DCGs via its pH-dependent aggregation at the trans-Golgi network.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>20061385</pmid><doi>10.1074/jbc.M109.064196</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-3215-4325</orcidid><orcidid>https://orcid.org/0000-0001-8859-893X</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Catecholamines - metabolism Cell Biology Cell/Exocytosis Cell/pH Cell/Secretion Cellular Biology Chlorocebus aethiops Chromaffin Chromaffin Granules - metabolism COS Cells Gene Silencing Genetic Vectors Hydrogen-Ion Concentration Life Sciences Methods/Fluorescence Neuroendocrine Cells - metabolism PC12 Cells Protein/Chimeras Protein/Intracellular Trafficking Rats Recombinant Fusion Proteins - metabolism RNA, Small Interfering - metabolism Secretogranin II - metabolism Secretory Vesicles - metabolism Subcellular Organelles/Vesicles Subcellular Processes |
| title | Pro-hormone Secretogranin II Regulates Dense Core Secretory Granule Biogenesis in Catecholaminergic Cells |
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