Home LiteratureArticle Details
PMID: 15975913 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

dGRASP localization and function in the early exocytic pathway in Drosophila S2 cells.

Molecular biology of the cell ·Vol. 16 ·No. 9 ·2005-09-00 ·Pages 4061-72

Kondylis V, Spoorendonk KM, Rabouille C

Abstract

The de novo model for Golgi stack biogenesis predicts that membrane exiting the ER at transitional ER (tER) sites contains and recruits all the necessary molecules to form a Golgi stack, including the Golgi matrix proteins, p115, GM130, and GRASP65/55. These proteins leave the tER sites faster than Golgi transmembrane resident enzymes, suggesting that they act as a template nucleating the formation of the Golgi apparatus. However, the localization of the Golgi matrix proteins at tER sites is only shown under conditions where exit from the ER is blocked. Here, we show in Drosophila S2 cells, that dGRASP, the single Drosophila homologue of GRASP65/55, localizes both to the Golgi membranes and the tER sites at steady state and that the myristoylation of glycine 2 is essential for the localization to both compartments. Its depletion for 96 h by RNAi gave an effect on the architecture of the Golgi stacks in 30% of the cells, but a double depletion of dGRASP and dGM130 led to the quantitative conversion of Golgi stacks into clusters of vesicles and tubules, often featuring single cisternae. This disruption of Golgi architecture was not accompanied by the disorganization of tER sites or the inhibition of anterograde transport. This shows that, at least in Drosophila, the structural integrity of the Golgi stacks is not required for efficient transport. Overall, dGRASP exhibits a dynamic association to the membrane of the early exocytic pathway and is involved in Golgi stack architecture.

MeSH Terms
Animals Autoantigens Cell Line Drosophila Proteins/metabolism,physiology Endoplasmic Reticulum/ultrastructure Exocytosis/physiology Golgi Apparatus/metabolism,ultrastructure Golgi Matrix Proteins Membrane Proteins/metabolism,physiology
Chemicals
Autoantigens Drosophila Proteins GRASP65 protein, Drosophila Golgi Matrix Proteins Golgin subfamily A member 2 Membrane Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Kondylis Vangelis
The Cell Microscopy Centre, Department of Cell Biology and Institute of Biomembranes, University Medical Centre Utrecht, AZU, 3584CX Utrecht, The Netherlands.
Spoorendonk Kirsten M
Rabouille Catherine
References (59)
59 references, click to expand
  1. The GM130 and GRASP65 Golgi proteins cycle through and define a subdomain of the intermediate compartment.
    Nat Cell Biol. 2001 Dec;3(12):1101-13 PMID: 11781572
  2. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER.
    Cell. 1989 Mar 10;56(5):801-13 PMID: 2647301
  3. Ras signalling on the endoplasmic reticulum and the Golgi.
    Nat Cell Biol. 2002 May;4(5):343-50 PMID: 11988737
  4. Fragmentation and dispersal of the pericentriolar Golgi complex is required for entry into mitosis in mammalian cells.
    Cell. 2002 May 3;109(3):359-69 PMID: 12015985
  5. Golgi biogenesis in Toxoplasma gondii.
    Nature. 2002 Aug 1;418(6897):548-52 PMID: 12152082
  6. Can the Golgi form de novo?
    Nat Rev Mol Cell Biol. 2002 Aug;3(8):615-9 PMID: 12154372
  7. De novo formation of transitional ER sites and Golgi structures in Pichia pastoris.
    Nat Cell Biol. 2002 Oct;4(10):750-6 PMID: 12360285
  8. Golgi architecture and inheritance.
    Annu Rev Cell Dev Biol. 2002;18:379-420 PMID: 12142281
  9. Tomographic evidence for continuous turnover of Golgi cisternae in Pichia pastoris.
    Mol Biol Cell. 2003 Jun;14(6):2277-91 PMID: 12808029
  10. A direct role for GRASP65 as a mitotically regulated Golgi stacking factor.
    EMBO J. 2003 Jul 1;22(13):3279-90 PMID: 12839990
  11. A novel role for dp115 in the organization of tER sites in Drosophila.
    J Cell Biol. 2003 Jul 21;162(2):185-98 PMID: 12876273
  12. Golgins in the structure and dynamics of the Golgi apparatus.
    Curr Opin Cell Biol. 2003 Aug;15(4):405-13 PMID: 12892780
  13. Persistence of Golgi matrix distribution exhibits the same dependence on Sar1p activity as a Golgi glycosyltransferase.
    Traffic. 2003 Sep;4(9):631-41 PMID: 12911817
  14. Capacity of the golgi apparatus for biogenesis from the endoplasmic reticulum.
    Mol Biol Cell. 2003 Dec;14(12):5011-8 PMID: 14565973
  15. Gene replacement reveals that p115/SNARE interactions are essential for Golgi biogenesis.
    Proc Natl Acad Sci U S A. 2004 Feb 3;101(5):1253-6 PMID: 14736916
  16. Autolytic activation and localization in Schneider cells (S2) of calpain B from Drosophila.
    Biochem J. 2004 Mar 1;378(Pt 2):299-305 PMID: 14614768
  17. Isolation of a matrix that binds medial Golgi enzymes.
    J Cell Biol. 1994 Feb;124(4):405-13 PMID: 8106542
  18. Syntaxin 5 regulates endoplasmic reticulum to Golgi transport.
    J Biol Chem. 1994 Nov 25;269(47):29363-6 PMID: 7961911
  19. The organization of endoplasmic reticulum export complexes.
    J Cell Biol. 1996 Oct;135(1):19-35 PMID: 8858160
  20. The vesicle docking protein p115 binds GM130, a cis-Golgi matrix protein, in a mitotically regulated manner.
    Cell. 1997 May 2;89(3):445-55 PMID: 9150144
  21. GRASP65, a protein involved in the stacking of Golgi cisternae.
    Cell. 1997 Oct 17;91(2):253-62 PMID: 9346242
  22. gp25L/emp24/p24 protein family members of the cis-Golgi network bind both COP I and II coatomer.
    J Cell Biol. 1998 Feb 23;140(4):751-65 PMID: 9472029
  23. Mapping the interaction between GRASP65 and GM130, components of a protein complex involved in the stacking of Golgi cisternae.
    EMBO J. 1998 Jun 15;17(12):3258-68 PMID: 9628863
  24. Complex proteolytic processing acts on Delta, a transmembrane ligand for Notch, during Drosophila development.
    Mol Biol Cell. 1998 Jul;9(7):1709-23 PMID: 9658166
  25. KDEL receptor (Erd2p)-mediated retrograde transport of the cholera toxin A subunit from the Golgi involves COPI, p23, and the COOH terminus of Erd2p.
    J Cell Biol. 1998 Nov 2;143(3):601-12 PMID: 9813083
  26. Intracellular localization and in vivo trafficking of p24A and p23.
    J Cell Sci. 1999 Feb;112 ( Pt 4):537-48 PMID: 9914165
  27. Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae.
    J Cell Biol. 1999 Apr 5;145(1):69-81 PMID: 10189369
  28. Molecular techniques for detection, species differentiation, and phylogenetic analysis of microsporidia.
    Clin Microbiol Rev. 1999 Apr;12(2):243-85 PMID: 10194459
  29. Quantitative aspects of immunogold labeling in embedded and nonembedded sections.
    Methods Mol Biol. 1999;117:125-44 PMID: 10327403
  30. A role for the vesicle tethering protein, p115, in the post-mitotic stacking of reassembling Golgi cisternae in a cell-free system.
    J Cell Biol. 1999 Jul 12;146(1):57-70 PMID: 10402460
  31. GRASP55, a second mammalian GRASP protein involved in the stacking of Golgi cisternae in a cell-free system.
    EMBO J. 1999 Sep 15;18(18):4949-60 PMID: 10487747
  32. mRNA localization and ER-based protein sorting mechanisms dictate the use of transitional endoplasmic reticulum-golgi units involved in gurken transport in Drosophila oocytes.
    Mol Biol Cell. 2004 Dec;15(12):5306-17 PMID: 15385627
  33. Mapping the functional domains of the Golgi stacking factor GRASP65.
    J Biol Chem. 2005 Feb 11;280(6):4921-8 PMID: 15576368
  34. Plk1 docking to GRASP65 phosphorylated by Cdk1 suggests a mechanism for Golgi checkpoint signalling.
    EMBO J. 2005 Feb 23;24(4):753-65 PMID: 15678101
  35. p125 is localized in endoplasmic reticulum exit sites and involved in their organization.
    J Biol Chem. 2005 Mar 18;280(11):10141-8 PMID: 15623529
  36. Convergence of cell cycle regulation and growth factor signals on GRASP65.
    J Biol Chem. 2005 Jun 17;280(24):23048-56 PMID: 15834132
  37. YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3zeta.
    J Cell Biol. 2004 Mar 29;164(7):1009-20 PMID: 15037601
  38. Golgi duplication in Trypanosoma brucei.
    J Cell Biol. 2004 May 10;165(3):313-21 PMID: 15138289
  39. Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells.
    Plant Cell. 2004 Jul;16(7):1753-71 PMID: 15208385
  40. Molecular basis for Golgi maintenance and biogenesis.
    Curr Opin Cell Biol. 2004 Aug;16(4):364-72 PMID: 15261668
  41. Sec34p, a protein required for vesicle tethering to the yeast Golgi apparatus, is in a complex with Sec35p.
    J Cell Biol. 1999 Nov 15;147(4):729-42 PMID: 10562277
  42. ER to Golgi transport: Requirement for p115 at a pre-Golgi VTC stage.
    J Cell Biol. 1999 Dec 13;147(6):1205-22 PMID: 10601335
  43. Golgi membranes are absorbed into and reemerge from the ER during mitosis.
    Cell. 1999 Dec 10;99(6):589-601 PMID: 10612395
  44. Potential role for protein kinases in regulation of bidirectional endoplasmic reticulum-to-Golgi transport revealed by protein kinase inhibitor H89.
    Mol Biol Cell. 2000 Aug;11(8):2577-90 PMID: 10930455
  45. The effect of Golgi depletion on exocytic transport.
    Nat Cell Biol. 2000 Nov;2(11):840-6 PMID: 11056540
  46. Kinase signaling initiates coat complex II (COPII) recruitment and export from the mammalian endoplasmic reticulum.
    J Biol Chem. 2000 Nov 17;275(46):35673-6 PMID: 11001944
  47. The p115-interactive proteins GM130 and giantin participate in endoplasmic reticulum-Golgi traffic.
    J Biol Chem. 2001 Jan 26;276(4):2693-700 PMID: 11035033
  48. ER export: public transportation by the COPII coach.
    Curr Opin Cell Biol. 2001 Aug;13(4):438-43 PMID: 11454450
  49. Biogenesis of Golgi stacks in imaginal discs of Drosophila melanogaster.
    Mol Biol Cell. 2001 Aug;12(8):2308-27 PMID: 11514618
  50. Evidence that Golgi structure depends on a p115 activity that is independent of the vesicle tether components giantin and GM130.
    J Cell Biol. 2001 Oct 15;155(2):227-38 PMID: 11591729
  51. Evidence that the entire Golgi apparatus cycles in interphase HeLa cells: sensitivity of Golgi matrix proteins to an ER exit block.
    J Cell Biol. 2001 Nov 12;155(4):543-55 PMID: 11696556
  52. Maintenance of Golgi structure and function depends on the integrity of ER export.
    J Cell Biol. 2001 Nov 12;155(4):557-70 PMID: 11706049
  53. The Sec34/35 Golgi transport complex is related to the exocyst, defining a family of complexes involved in multiple steps of membrane traffic.
    Dev Cell. 2001 Oct;1(4):527-37 PMID: 11703943
  54. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi.
    Nature. 2001 Nov 22;414(6862):450-3 PMID: 11719806
  55. A GRASP55-rab2 effector complex linking Golgi structure to membrane traffic.
    J Cell Biol. 2001 Dec 10;155(6):877-83 PMID: 11739401
  56. Golgi matrix proteins interact with p24 cargo receptors and aid their efficient retention in the Golgi apparatus.
    J Cell Biol. 2001 Dec 10;155(6):885-91 PMID: 11739402
  57. Direct targeting of cis-Golgi matrix proteins to the Golgi apparatus.
    J Cell Sci. 2001 Nov;114(Pt 22):4105-15 PMID: 11739642
  58. Dynamic nucleation of Golgi apparatus assembly from the endoplasmic reticulum in interphase hela cells.
    Traffic. 2004 Aug;5(8):595-605 PMID: 15260829
  59. Caspase-mediated cleavage of the stacking protein GRASP65 is required for Golgi fragmentation during apoptosis.
    J Cell Biol. 2002 Feb 4;156(3):495-509 PMID: 11815631
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2005-09-00
Epub
2005-00-22
Pages
4061-72
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1196319
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com