Home LiteratureArticle Details
PMID: 1730750 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Assembly and disassembly of the Golgi complex: two processes arranged in a cis-trans direction.

The Journal of cell biology ·Vol. 116 ·No. 1 ·1992-01-00 ·Pages 69-83

Alcalde J, Bonay P, Roa A, Vilaro S, Sandoval IV

Abstract

We have studied the disassembly and assembly of two morphologically and functionally distinct parts of the Golgi complex, the cis/middle and trans cisterna/trans network compartments. For this purpose we have followed the redistribution of three cis/middle- (GMPc-1, GMPc-2, MG 160) and two trans- (GMPt-1 and GMPt-2) Golgi membrane proteins during and after treatment of normal rat kidney (NRK) cells with brefeldin A (BFA). BFA induced complete disassembly of the cis/middle- and trans-Golgi complex and translocation of GMPc and GMPt to the ER. Cells treated for short times (3 min) with BFA showed extensive disorganization of both cis/middle- and trans-Golgi complexes. However, complete disorganization of the trans part required much longer incubations with the drug. Upon removal of BFA the Golgi complex was reassembled by a process consisting of three steps: (a) exist of cis/middle proteins from the ER and their accumulation into vesicular structures scattered throughout the cytoplasm; (b) gradual relocation and accumulation of the trans proteins in the vesicles containing the cis/middle proteins; and (c) assembly of the cisternae, and reconstruction of the Golgi complex within an area located in the vicinity of the centrosome from which the ER was excluded. Reconstruction of the cis/middle-Golgi complex occurred under temperature conditions inhibitory of the reorganization of the trans-Golgi complex, and was dependent on microtubules. Reconstruction of the trans-Golgi complex, disrupted with nocodazole after selective fusion of the cis/middle-Golgi complex with the ER, occurred after the release of cis/middle-Golgi proteins from the ER and the assembly of the cis/middle cisternae.

MeSH Terms
Animals Anti-Bacterial Agents/pharmacology Brefeldin A Cells, Cultured Cyclopentanes/pharmacology Endoplasmic Reticulum/drug effects,ultrastructure Ethylmaleimide/pharmacology Golgi Apparatus/drug effects,physiology,ultrastructure Kidney Membrane Proteins/analysis,metabolism Microtubules/physiology,ultrastructure Rats Temperature
Chemicals
Anti-Bacterial Agents Cyclopentanes Membrane Proteins Brefeldin A Ethylmaleimide
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Alcalde J
Centro de Biologia Molecular, Facultad de Ciencias, Universidad Autónoma de Madrid, Spain.
Bonay P
Roa A
Vilaro S
Sandoval I V
References (79)
79 references, click to expand
  1. Sorting within the regulated secretory pathway occurs in the trans-Golgi network.
    J Cell Biol. 1990 Jan;110(1):1-12 PMID: 2295680
  2. Compartmentation of asparagine-linked oligosaccharide processing in the Golgi apparatus.
    J Cell Biol. 1983 Jul;97(1):270-5 PMID: 6223041
  3. Early and late functions associated with the Golgi apparatus reside in distinct compartments.
    Proc Natl Acad Sci U S A. 1981 Dec;78(12):7453-7 PMID: 6801652
  4. Role of microtubules in the distribution of the Golgi apparatus: effect of taxol and microinjected anti-alpha-tubulin antibodies.
    Proc Natl Acad Sci U S A. 1983 Jul;80(14):4286-90 PMID: 6136036
  5. Role of microtubules in the organization and localization of the Golgi apparatus.
    J Cell Biol. 1984 Jul;99(1 Pt 2):113s-118s PMID: 6146626
  6. Transport of protein between cytoplasmic membranes of fused cells: correspondence to processes reconstituted in a cell-free system.
    J Cell Biol. 1984 Jul;99(1 Pt 1):248-59 PMID: 6429157
  7. Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface.
    Cell. 1984 Sep;38(2):535-49 PMID: 6432345
  8. A rat monoclonal antibody reacting specifically with the tyrosylated form of alpha-tubulin. I. Biochemical characterization, effects on microtubule polymerization in vitro, and microtubule polymerization and organization in vivo.
    J Cell Biol. 1983 Nov;97(5 Pt 1):1467-75 PMID: 6415068
  9. Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets.
    Proc Natl Acad Sci U S A. 1983 Dec;80(23):7224-8 PMID: 6359165
  10. Newly synthesized G protein of vesicular stomatitis virus is not transported to the cell surface during mitosis.
    J Cell Biol. 1983 Nov;97(5 Pt 1):1623-8 PMID: 6355124
  11. Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound.
    Proc Natl Acad Sci U S A. 1982 Apr;79(8):2603-7 PMID: 7045867
  12. The site of incorporation of sialic acid residues into glycoproteins and the subsequent fates of these molecules in various rat and mouse cell types as shown by radioautography after injection of [3H]N-acetylmannosamine. I. Observations in hepatocytes.
    J Cell Biol. 1981 Jan;88(1):1-15 PMID: 7204482
  13. Mitosis in rat thyroid epithelial cells in vivo. I. Ultrastructural changes in cytoplasmic organelles during the mitotic cycle.
    J Ultrastruct Res. 1979 Jan;66(1):53-77 PMID: 423323
  14. Cytochemical contributions to differentiating GERL from the Golgi apparatus.
    Histochem J. 1977 Sep;9(5):525-51 PMID: 198392
  15. Dynamics of the Golgi apparatus: membrane differentiation and membrane flow.
    Int Rev Cytol Suppl. 1977;(5):61-188 PMID: 340403
  16. Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum.
    J Cell Biol. 1989 Jul;109(1):61-72 PMID: 2745557
  17. Blockade by brefeldin A of intracellular transport of secretory proteins in mouse pituitary cells: effects on the biosynthesis of thyrotropin and free alpha-subunits.
    Endocrinology. 1988 Mar;122(3):912-20 PMID: 2449343
  18. 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
  19. Brefeldin A causes disassembly of the Golgi complex and accumulation of secretory proteins in the endoplasmic reticulum.
    J Biol Chem. 1988 Dec 5;263(34):18545-52 PMID: 3192548
  20. Novel blockade by brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes.
    J Biol Chem. 1986 Aug 25;261(24):11398-403 PMID: 2426273
  21. Brefeldin A arrests the intracellular transport of a precursor of complement C3 before its conversion site in rat hepatocytes.
    FEBS Lett. 1987 Apr 6;214(1):135-8 PMID: 3569512
  22. Semi-intact cells permeable to macromolecules: use in reconstitution of protein transport from the endoplasmic reticulum to the Golgi complex.
    Cell. 1987 Aug 14;50(4):523-34 PMID: 3038335
  23. Differential subcompartmentation of terminal glycosylation in the Golgi apparatus of intestinal absorptive and goblet cells.
    J Biol Chem. 1986 Oct 25;261(30):14307-12 PMID: 3095318
  24. Assembly of asparagine-linked oligosaccharides.
    Annu Rev Biochem. 1985;54:631-64 PMID: 3896128
  25. 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
  26. Two integral membrane proteins located in the cis-middle and trans-part of the Golgi system acquire sialylated N-linked carbohydrates and display different turnovers and sensitivity to cAMP-dependent phosphorylation.
    J Cell Biol. 1987 Jul;105(1):215-27 PMID: 3301866
  27. Exit of newly synthesized membrane proteins from the trans cisterna of the Golgi complex to the plasma membrane.
    J Cell Biol. 1985 Sep;101(3):949-64 PMID: 2863275
  28. A new type of coated vesicular carrier that appears not to contain clathrin: its possible role in protein transport within the Golgi stack.
    Cell. 1986 Jul 18;46(2):171-84 PMID: 2872969
  29. 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
  30. Intracellular movement of cell surface receptors after endocytosis: resialylation of asialo-transferrin receptor in human erythroleukemia cells.
    J Cell Biol. 1985 Mar;100(3):826-34 PMID: 2982885
  31. A mitotic form of the Golgi apparatus in HeLa cells.
    J Cell Biol. 1987 Apr;104(4):865-74 PMID: 3104351
  32. Vesicular transport between the endoplasmic reticulum and the Golgi stack requires the NEM-sensitive fusion protein.
    Nature. 1989 Jun 1;339(6223):397-8 PMID: 2542798
  33. Parathyroid hormone biosynthesis. Correlation of conversion of biosynthetic precursors with intracellular protein migration as determined by electron microscope autoradiography.
    J Cell Biol. 1979 Mar;80(3):715-31 PMID: 457765
  34. Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy.
    J Histochem Cytochem. 1974 Dec;22(12):1077-83 PMID: 4374474
  35. Golgi apparatus, GERL, and lysosomes of neurons in rat dorsal root ganglia, studied by thick section and thin section cytochemistry.
    J Cell Biol. 1971 Sep;50(3):859-86 PMID: 4329159
  36. The endoplasmic reticulum: a cytochemist's view (a review).
    Proc Natl Acad Sci U S A. 1976 Aug;73(8):2781-7 PMID: 183210
  37. Intracellular aspects of the process of protein synthesis.
    Science. 1975 Aug 1;189(4200):347-58 PMID: 1096303
  38. The golgi apparatus during mitosis in human melanoma cells in vitro.
    Cancer Res. 1970 Sep;30(9):2326-35 PMID: 5475479
  39. Brefeldin A, a drug that blocks secretion, prevents the assembly of non-clathrin-coated buds on Golgi cisternae.
    Cell. 1991 Mar 22;64(6):1183-95 PMID: 2004424
  40. Intracellular accumulation and oligosaccharide processing of alkaline phosphatase under disassembly of the Golgi complex caused by brefeldin A.
    Eur J Biochem. 1990 Dec 27;194(3):805-10 PMID: 2269302
  41. A coat subunit of Golgi-derived non-clathrin-coated vesicles with homology to the clathrin-coated vesicle coat protein beta-adaptin.
    Nature. 1991 Jan 17;349(6306):215-20 PMID: 1898984
  42. Identification of an intermediate compartment involved in protein transport from endoplasmic reticulum to Golgi apparatus.
    Eur J Cell Biol. 1990 Dec;53(2):185-96 PMID: 1964413
  43. The rate of bulk flow from the Golgi to the plasma membrane.
    Cell. 1990 Oct 19;63(2):259-67 PMID: 2208286
  44. Evidence that luminal ER proteins are sorted from secreted proteins in a post-ER compartment.
    EMBO J. 1988 Apr;7(4):913-8 PMID: 3402439
  45. The trans Golgi network: sorting at the exit site of the Golgi complex.
    Science. 1986 Oct 24;234(4775):438-43 PMID: 2945253
  46. Brefeldin A implicates egress from endoplasmic reticulum in class I restricted antigen presentation.
    Nature. 1989 May 18;339(6221):223-6 PMID: 2785645
  47. Targeting and processing of glycophorins in murine erythroleukemia cells: use of brefeldin A as a perturbant of intracellular traffic.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):6992-6 PMID: 2780556
  48. The dynamic nature of the Golgi complex.
    J Cell Biol. 1989 Feb;108(2):277-97 PMID: 2537312
  49. Dissection of a single round of vesicular transport: sequential intermediates for intercisternal movement in the Golgi stack.
    Cell. 1989 Feb 10;56(3):357-68 PMID: 2536591
  50. The response of the Golgi complex to microtubule alterations: the roles of metabolic energy and membrane traffic in Golgi complex organization.
    J Cell Biol. 1989 Nov;109(5):2081-8 PMID: 2681225
  51. A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast.
    Nature. 1989 Jun 1;339(6223):355-9 PMID: 2657434
  52. Reduced temperature does not prevent transport of lysosomal integral membrane proteins from endoplasmic reticulum and through the Golgi system to lysosomes.
    Eur J Biochem. 1989 Aug 1;183(2):407-12 PMID: 2788083
  53. Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack.
    Cell. 1989 Jul 28;58(2):329-36 PMID: 2752426
  54. Vesicle fusion following receptor-mediated endocytosis requires a protein active in Golgi transport.
    Nature. 1989 Jun 1;339(6223):398-400 PMID: 2725659
  55. MG-160. A novel sialoglycoprotein of the medial cisternae of the Golgi apparatus [published eeratum appears in J Biol Chem 1989 Mar 5;264(7):4264].
    J Biol Chem. 1989 Jan 5;264(1):646-53 PMID: 2909545
  56. Identification, by a monoclonal antibody, of a 53-kD protein associated with a tubulo-vesicular compartment at the cis-side of the Golgi apparatus.
    J Cell Biol. 1988 Nov;107(5):1643-53 PMID: 3182932
  57. Presence of an autoantibody against a Golgi cisternal membrane protein in the serum and cerebrospinal fluid from a patient with idiopathic late onset cerebellar ataxia.
    J Neuroimmunol. 1988 Mar;17(4):287-99 PMID: 3339121
  58. Recycling of transferrin receptors in A431 cells is inhibited during mitosis.
    EMBO J. 1984 Oct;3(10):2217-25 PMID: 6209129
  59. Sequential intermediates in the pathway of intercompartmental transport in a cell-free system.
    Cell. 1984 Dec;39(3 Pt 2):525-36 PMID: 6096009
  60. Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi.
    Annu Rev Biochem. 1987;56:829-52 PMID: 3304148
  61. 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
  62. Fragmentation and partitioning of the Golgi apparatus during mitosis in HeLa cells.
    EMBO J. 1987 Nov;6(11):3239-46 PMID: 3428259
  63. The rate of bulk flow from the endoplasmic reticulum to the cell surface.
    Cell. 1987 Jul 17;50(2):289-300 PMID: 3594573
  64. Biosynthesis, glycosylation, movement through the Golgi system, and transport to lysosomes by an N-linked carbohydrate-independent mechanism of three lysosomal integral membrane proteins.
    J Biol Chem. 1986 Dec 15;261(35):16755-63 PMID: 3782140
  65. Progress in unraveling pathways of Golgi traffic.
    Annu Rev Cell Biol. 1985;1:447-88 PMID: 3916320
  66. The Golgi apparatus remains associated with microtubule organizing centers during myogenesis.
    J Cell Biol. 1985 Aug;101(2):630-8 PMID: 3894380
  67. Compartmentation of the Golgi complex: brefeldin-A distinguishes trans-Golgi cisternae from the trans-Golgi network.
    J Cell Biol. 1990 Sep;111(3):893-9 PMID: 2167898
  68. Identification by anti-idiotype antibodies of an intracellular membrane protein that recognizes a mammalian endoplasmic reticulum retention signal.
    Nature. 1990 Jun 7;345(6275):495-502 PMID: 2161500
  69. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway.
    Cell. 1990 Mar 9;60(5):821-36 PMID: 2178778
  70. Role of microtubules in the organisation of the Golgi apparatus.
    Cell Motil Cytoskeleton. 1990;15(2):67-70 PMID: 2178782
  71. The confined function model of the Golgi complex: center for ordered processing of biosynthetic products of the rough endoplasmic reticulum.
    Int Rev Cytol. 1983;85:221-52 PMID: 6363328
  72. Cells injected with guanosine 5'-[alpha, beta-methylene]triphosphate, an alpha, beta-nonhydrolyzable analog of GTP, show anomalous patterns of tubulin polymerization affecting cell translocation, intracellular movement, and the organization of Golgi elements.
    Proc Natl Acad Sci U S A. 1983 Apr;80(7):1938-41 PMID: 6572952
  73. Intercompartmental transport in the Golgi complex is a dissociative process: facile transfer of membrane protein between two Golgi populations.
    J Cell Biol. 1984 Jul;99(1 Pt 1):260-71 PMID: 6539782
  74. Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line.
    J Cell Biol. 1982 Jun;93(3):576-82 PMID: 6811596
  75. THE ULTRASTRUCTURE OF A MAMMALIAN CELL DURING THE MITOTIC CYCLE.
    J Cell Biol. 1964 Jun;21:429-63 PMID: 14189913
  76. Forskolin inhibits and reverses the effects of brefeldin A on Golgi morphology by a cAMP-independent mechanism.
    J Cell Biol. 1991 Feb;112(4):567-77 PMID: 1847146
  77. Beta-COP, a 110 kd protein associated with non-clathrin-coated vesicles and the Golgi complex, shows homology to beta-adaptin.
    Cell. 1991 Feb 8;64(3):649-65 PMID: 1840503
  78. Guanine nucleotides modulate the effects of brefeldin A in semipermeable cells: regulation of the association of a 110-kD peripheral membrane protein with the Golgi apparatus.
    J Cell Biol. 1991 Feb;112(4):579-88 PMID: 1993732
  79. Immunocytochemical visualization of the Golgi apparatus in several species, including human, and tissues with an antiserum against MG-160, a sialoglycoprotein of rat Golgi apparatus.
    J Histochem Cytochem. 1990 Jul;38(7):957-63 PMID: 2355176
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1992-01-00
Pages
69-83
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2289264
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