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Golgi Structure in Three Dimensions: Functional Insights from the Normal Rat Kidney Cell

Ladinsky, Mark S. and Mastronarde, David N. and McIntosh, J. Richard and Howell, Kathryn E. and Staehelin, L. Andrew (1999) Golgi Structure in Three Dimensions: Functional Insights from the Normal Rat Kidney Cell. Journal of Cell Biology, 144 (6). pp. 1135-1149. ISSN 0021-9525. PMCID PMC2150572. doi:10.1083/jcb.144.6.1135. https://resolver.caltech.edu/CaltechAUTHORS:20191106-105056628

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Abstract

Three-dimensional reconstructions of portions of the Golgi complex from cryofixed, freeze-substituted normal rat kidney cells have been made by dual-axis, high-voltage EM tomography at ∼7-nm resolution. The reconstruction shown here (∼1 × 1 × 4 μm³) contains two stacks of seven cisternae separated by a noncompact region across which bridges connect some cisternae at equivalent levels, but none at nonequivalent levels. The rest of the noncompact region is filled with both vesicles and polymorphic membranous elements. All cisternae are fenestrated and display coated buds. They all have about the same surface area, but they differ in volume by as much as 50%. The trans-most cisterna produces exclusively clathrin-coated buds, whereas the others display only nonclathrin coated buds. This finding challenges traditional views of where sorting occurs within the Golgi complex. Tubules with budding profiles extend from the margins of both cis and trans cisternae. They pass beyond neighboring cisternae, suggesting that these tubules contribute to traffic to and/or from the Golgi. Vesicle-filled “wells” open to both the cis and lateral sides of the stacks. The stacks of cisternae are positioned between two types of ER, cis and trans. The cis ER lies adjacent to the ER-Golgi intermediate compartment, which consists of discrete polymorphic membranous elements layered in front of the cis-most Golgi cisterna. The extensive trans ER forms close contacts with the two trans-most cisternae; this apposition may permit direct transfer of lipids between ER and Golgi membranes. Within 0.2 μm of the cisternae studied, there are 394 vesicles (8 clathrin coated, 190 nonclathrin coated, and 196 noncoated), indicating considerable vesicular traffic in this Golgi region. Our data place structural constraints on models of trafficking to, through, and from the Golgi complex.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1083/jcb.144.6.1135DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2150572PubMed CentralArticle
ORCID:
AuthorORCID
Ladinsky, Mark S.0000-0002-1036-3513
Additional Information:© 1999 Rockefeller University Press. After the Initial Publication Period, RUP will grant to the public the non-exclusive right to copy, distribute, or display the Article under a Creative Commons Attribution-Noncommercial-Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/legalcode, or updates thereof. Submitted: 3 December 1998; Revision received 1 February 1999. We thank Jim Kremer for taking tilt series micrographs and for software development improvements. This work was supported by grant RR00592 to J.R. McIntosh from the National Center for Research Resources of the National Institutes of Health (NIH), and by NIH grants GM18639 to L.A. Staehelin and GM42629 to K.E. Howell.
Funders:
Funding AgencyGrant Number
NIHRR00592
NIHGM18639
NIHGM42629
Subject Keywords:Golgi; membrane traffic; cryofixation; electron microscopy; tomography
Issue or Number:6
PubMed Central ID:PMC2150572
DOI:10.1083/jcb.144.6.1135
Record Number:CaltechAUTHORS:20191106-105056628
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20191106-105056628
Official Citation:Golgi Structure in Three Dimensions: Functional Insights from the Normal Rat Kidney Cell. Mark S. Ladinsky, David N. Mastronarde, J. Richard McIntosh, Kathryn E. Howell, L. Andrew Staehelin. The Journal of Cell Biology Mar 1999, 144 (6) 1135-1149; DOI: 10.1083/jcb.144.6.1135
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:99693
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:06 Nov 2019 19:14
Last Modified:16 Nov 2021 17:48

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