Home LiteratureArticle Details
PMID: 8573789 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The organization of the endoplasmic reticulum and the intermediate compartment in cultured rat hippocampal neurons.

Molecular biology of the cell ·Vol. 6 ·No. 10 ·1995-10-00 ·Pages 1315-32

Krijnse-Locker J, Parton RG, Fuller SD, Griffiths G, Dotti CG

Abstract

The boundaries of the organelles of the biosynthetic endomembrane system are still controversial. In this paper we take advantage of the unique architectural organization of neurons to investigate the localization of a spectrum of compartment-specific markers with the goal of defining the location of the rough endoplasmic reticulum (ER), smooth ER, intermediate compartment, and the Golgi complex. Markers of the rough ER (signal sequence receptor), Golgi complex (mannosidase II), and the trans Golgi network (TGN38) were essentially restricted to the cell body and the initial segment of one of the cell's dendrites. In contrast the cytochemical reaction product for glucose 6 phosphate, a classical ER marker, in addition to staining ER structures in the cell body also reacted with smooth ER elements that extended into both axons and dendrites. These peripheral smooth ER elements also reacted at the immunofluorescence level for ER marker 3-hydroxy-3-methylglutaryl-coenzyme A reductase, as well as for calnexin and protein disulfide isomerase. We also analyzed the location of rab1, rab2, p58, the KDEL receptor, and beta-subunit of coatomer. These intermediate compartment markers were found predominantly in the cell body but also extended to the proximal parts of the dendrites. Collectively, our data argue that the ER of hippocampal neurons consists of functionally and spatially distinct and separated domains, and they stress the power of the hippocampal neuron system for investigations of the organization of the ER by light microscopy.

MeSH Terms
Animals Biological Transport Biomarkers/analysis Cell Compartmentation Cells, Cultured Endoplasmic Reticulum, Rough/chemistry,ultrastructure Endoplasmic Reticulum, Smooth/chemistry,ultrastructure Golgi Apparatus/chemistry,ultrastructure Hippocampus/chemistry,cytology Membrane Proteins/analysis Microscopy, Fluorescence Neurons/chemistry,ultrastructure Rats Semliki forest virus Viral Proteins/analysis,biosynthesis
Chemicals
Biomarkers Membrane Proteins Viral Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Krijnse-Locker J
Cell Biology Programm, European Molecular Biology Laboratory, Heidelberg, Germany.
Parton R G
Fuller S D
Griffiths G
Dotti C G
References (67)
67 references, click to expand
  1. 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
  2. The G protein of vesicular stomatitis virus has free access into and egress from the smooth endoplasmic reticulum of UT-1 cells.
    J Cell Biol. 1990 Mar;110(3):625-35 PMID: 2155242
  3. Photocrosslinking demonstrates proximity of a 34 kDa membrane protein to different portions of preprolactin during translocation through the endoplasmic reticulum.
    FEBS Lett. 1989 Nov 6;257(2):263-8 PMID: 2583273
  4. Membrane biogenesis in the sprouting neuron. I. Selective transfer of newly synthesized phospholipid into the growing neurite.
    J Cell Biol. 1983 Oct;97(4):1038-42 PMID: 6194160
  5. Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus.
    J Cell Biol. 1994 Jul;126(1):41-52 PMID: 8027184
  6. The neuronal endomembrane system. II. The multiple forms of the Golgi apparatus cis element.
    J Neurosci. 1985 Dec;5(12):3124-34 PMID: 3908622
  7. Localization of the Lys, Asp, Glu, Leu tetrapeptide receptor to the Golgi complex and the intermediate compartment in mammalian cells.
    J Cell Biol. 1994 Dec;127(6 Pt 1):1557-74 PMID: 7798312
  8. Polarized distribution of the trans-Golgi network marker TGN38 during the in vitro development of neocortical neurons: effects of nocodazole and brefeldin A.
    Eur J Neurosci. 1994 Sep 1;6(9):1453-65 PMID: 8000569
  9. Endoplasmic reticulum: a dynamic patchwork of specialized subregions.
    Mol Biol Cell. 1992 Oct;3(10):1067-72 PMID: 1421566
  10. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments.
    Cell. 1990 Jul 27;62(2):317-29 PMID: 2115402
  11. The Golgi complex: in vitro veritas?
    Cell. 1992 Mar 6;68(5):829-40 PMID: 1547485
  12. Biogenesis of the crystalloid endoplasmic reticulum in UT-1 cells: evidence that newly formed endoplasmic reticulum emerges from the nuclear envelope.
    J Cell Biol. 1986 Jun;102(6):2158-68 PMID: 3711144
  13. 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
  14. Folding and assembly of viral membrane proteins.
    Virology. 1993 Apr;193(2):545-62 PMID: 8460475
  15. The neuronal endoplasmic reticulum: its cytochemistry and contribution to the endomembrane system. I. Cell bodies and dendrites.
    J Histochem Cytochem. 1983 Sep;31(9):1077-88 PMID: 6309951
  16. Semliki forest virus mutants with temperature-sensitive transport defect of envelope proteins.
    Virology. 1980 Jan 30;100(2):229-45 PMID: 7352369
  17. Molecular dissection of the secretory pathway.
    Nature. 1992 Jan 30;355(6359):409-15 PMID: 1734280
  18. Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture.
    Cell. 1990 Jul 13;62(1):63-72 PMID: 2163770
  19. Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks.
    J Cell Biol. 1993 May;121(3):521-41 PMID: 8486734
  20. Four intracisternal calcium-binding glycoproteins from rat liver microsomes with high affinity for calcium. No indication for calsequestrin-like proteins in inositol 1,4,5-trisphosphate-sensitive calcium sequestering rat liver vesicles.
    J Biol Chem. 1989 Oct 15;264(29):17494-501 PMID: 2793869
  21. 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
  22. A chaperone with a sweet tooth.
    Curr Biol. 1993 Dec 1;3(12):884-6 PMID: 15335825
  23. Localization of the small GTP-binding protein rab1p to early compartments of the secretory pathway.
    J Cell Sci. 1995 Apr;108 ( Pt 4):1541-52 PMID: 7615674
  24. Rab1 and Ca2+ are required for the fusion of carrier vesicles mediating endoplasmic reticulum to Golgi transport.
    J Cell Biol. 1994 Apr;125(2):239-52 PMID: 8163543
  25. 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
  26. The endoplasmic reticulum calcium-binding protein of 55 kDa is a novel EF-hand protein retained in the endoplasmic reticulum by a carboxyl-terminal His-Asp-Glu-Leu motif.
    J Biol Chem. 1994 Jul 22;269(29):19142-50 PMID: 8034671
  27. Beta-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo.
    Cell. 1993 Jul 16;74(1):71-82 PMID: 8334707
  28. Distribution of the intermediate elements operating in ER to Golgi transport.
    J Cell Sci. 1991 Nov;100 ( Pt 3):415-30 PMID: 1808196
  29. The neuronal endomembrane system. III. The origins of the axoplasmic reticulum and discrete axonal cisternae at the axon hillock.
    J Neurosci. 1985 Dec;5(12):3135-44 PMID: 3878394
  30. The endoplasmic reticulum as a protein-folding compartment.
    Trends Cell Biol. 1992 Aug;2(8):227-31 PMID: 14731479
  31. The neuronal endoplasmic reticulum: its cytochemistry and contribution to the endomembrane system. II. Axons and terminals.
    J Comp Neurol. 1984 Dec 1;230(2):231-48 PMID: 6210310
  32. Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38).
    Biochem J. 1990 Aug 15;270(1):97-102 PMID: 2204342
  33. Molecular cloning, characterization, subcellular localization and dynamics of p23, the mammalian KDEL receptor.
    J Cell Biol. 1993 Jan;120(2):325-38 PMID: 8380600
  34. Protein transport. Signals and salvage sequences.
    Nature. 1987 May 7-13;327(6117):17-8 PMID: 3574462
  35. Biosynthesis and modification of Golgi mannosidase II in HeLa and 3T3 cells.
    J Biol Chem. 1985 Jun 10;260(11):6654-62 PMID: 3922977
  36. The identity of the calcium-storing, inositol 1,4,5-trisphosphate-sensitive organelle in non-muscle cells: calciosome, endoplasmic reticulum ... or both?
    Trends Neurosci. 1991 Jul;14(7):310-4 PMID: 1719679
  37. Biosynthesis of membrane lipids in rat axons.
    J Cell Biol. 1991 Nov;115(4):1061-8 PMID: 1955456
  38. Internalization of lectins in neuronal GERL.
    J Cell Biol. 1977 Apr;73(1):1-13 PMID: 856827
  39. Disruption of endoplasmic reticulum to Golgi transport leads to the accumulation of large aggregates containing beta-COP in pancreatic acinar cells.
    Mol Biol Cell. 1993 Apr;4(4):413-24 PMID: 8507897
  40. Retention of unassembled components of integral membrane proteins by calnexin.
    Science. 1994 Jan 21;263(5145):387-90 PMID: 8278814
  41. Viral glycoproteins at different stages of intracellular transport can be distinguished using monoclonal antibodies.
    Eur J Cell Biol. 1983 Sep;31(2):315-24 PMID: 6196197
  42. Endoplasmic reticulum resident protein of 90 kilodaltons associates with the T- and B-cell antigen receptors and major histocompatibility complex antigens during their assembly.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4734-8 PMID: 1584811
  43. Protein folding in the cell.
    Nature. 1992 Jan 2;355(6355):33-45 PMID: 1731198
  44. Control of protein exit from the endoplasmic reticulum.
    Annu Rev Cell Biol. 1989;5:1-23 PMID: 2688704
  45. Ultrastructural analysis of crystalloid endoplasmic reticulum in UT-1 cells and its disappearance in response to cholesterol.
    J Cell Sci. 1983 Sep;63:1-20 PMID: 6685129
  46. GTP-binding mutants of rab1 and rab2 are potent inhibitors of vesicular transport from the endoplasmic reticulum to the Golgi complex.
    J Cell Biol. 1992 Nov;119(4):749-61 PMID: 1429835
  47. Antibodies to rat pancreas Golgi subfractions: identification of a 58-kD cis-Golgi protein.
    J Cell Biol. 1987 Nov;105(5):2021-9 PMID: 3316245
  48. Axonal and dendritic endocytic pathways in cultured neurons.
    J Cell Biol. 1992 Oct;119(1):123-37 PMID: 1527164
  49. The neuronal endomembrane system. I. Direct links between rough endoplasmic reticulum and the cis element of the Golgi apparatus.
    J Neurosci. 1985 Dec;5(12):3111-23 PMID: 3878393
  50. 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
  51. Cytochemistry of Golgi fractions prepared from rat liver.
    J Cell Biol. 1974 Jan;60(1):8-25 PMID: 4358430
  52. Replication of coronavirus MHV-A59 in sac- cells: determination of the first site of budding of progeny virions.
    Eur J Cell Biol. 1984 Mar;33(2):281-93 PMID: 6325194
  53. Hepatitis B surface antigen assembles in a post-ER, pre-Golgi compartment.
    J Cell Biol. 1992 Sep;118(6):1305-20 PMID: 1522109
  54. Isolation, characterization, and expression of cDNAs encoding murine alpha-mannosidase II, a Golgi enzyme that controls conversion of high mannose to complex N-glycans.
    J Cell Biol. 1991 Dec;115(6):1521-34 PMID: 1757461
  55. Axonal agranular reticulum and synaptic vesicles in cultured embryonic chick sympathetic neurons.
    J Cell Biol. 1973 Apr;57(1):88-108 PMID: 4347980
  56. Heterogeneous distribution of the cAMP receptor protein RII in the nervous system: evidence for its intracellular accumulation on microtubules, microtubule-organizing centers, and in the area of the Golgi complex.
    J Cell Biol. 1986 Jul;103(1):189-203 PMID: 3522603
  57. Immunocytochemical analysis of the transfer of vesicular stomatitis virus G glycoprotein from the intermediate compartment to the Golgi complex.
    J Cell Biol. 1992 Jul;118(1):43-50 PMID: 1320035
  58. Dissection of the Golgi complex. I. Monensin inhibits the transport of viral membrane proteins from medial to trans Golgi cisternae in baby hamster kidney cells infected with Semliki Forest virus.
    J Cell Biol. 1983 Mar;96(3):835-50 PMID: 6682112
  59. Intralumenal sarcoplasmic reticulum Ca(2+)-binding proteins.
    Semin Cell Biol. 1990 Aug;1(4):265-75 PMID: 2103513
  60. Intracellular Ca2+ stores in chicken Purkinje neurons: differential distribution of the low affinity-high capacity Ca2+ binding protein, calsequestrin, of Ca2+ ATPase and of the ER lumenal protein, Bip.
    J Cell Biol. 1991 May;113(4):779-91 PMID: 1827445
  61. Segregation of the signal sequence receptor protein in the rough endoplasmic reticulum membrane.
    Eur J Cell Biol. 1990 Dec;53(2):197-202 PMID: 1964414
  62. Localization of Sed5, a putative vesicle targeting molecule, to the cis-Golgi network involves both its transmembrane and cytoplasmic domains.
    J Cell Biol. 1994 Oct;127(2):357-71 PMID: 7929581
  63. Beta-COP localizes mainly to the cis-Golgi side in exocrine pancreas.
    J Cell Biol. 1993 Apr;121(1):49-59 PMID: 8458872
  64. The identification of proteins in the proximity of signal-anchor sequences during their targeting to and insertion into the membrane of the ER.
    J Cell Biol. 1991 Apr;113(1):35-44 PMID: 1848866
  65. 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
  66. The endoplasmic reticulum-Golgi intermediate compartment.
    Curr Opin Cell Biol. 1992 Aug;4(4):600-8 PMID: 1419041
  67. Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from the RER to the Golgi complex requires only one vesicular transport step.
    J Cell Biol. 1994 Jan;124(1-2):55-70 PMID: 8294506
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
DOI
10.1091/mbc.6.10.1315
Published
1995-10-00
Pages
1315-32
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC301290
Subset
IM
External Links
PubMed source DOI: 10.1091/mbc.6.10.1315 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2