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

doi:10.1083/jcb.144.6.1135

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© The Rockefeller University Press, 0021-9525/1999//1135 $5.00
The Journal of Cell Biology, Volume 144, Number 6, , 1999 1135-1149

Regular Articles

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, and L. Andrew Staehelin

^* Laboratory for Three-Dimensional Fine Structure and Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309-0347; and Department of Cellular and Structural Biology University of Colorado School of Medicine, Denver, Colorado 80262-1111

Three-dimensional reconstructions of portions of the Golgi complexfrom cryofixed, freeze-substituted normal rat kidney cells havebeen made by dual-axis, high-voltage EM tomography at $~$ 7-nmresolution. The reconstruction shown here ( $~$ 1 x 1 x 4 µm³)contains two stacks of seven cisternae separated by a noncompactregion across which bridges connect some cisternae at equivalentlevels, but none at nonequivalent levels. The rest of the noncompactregion is filled with both vesicles and polymorphic membranous elements. All cisternae are fenestrated and display coatedbuds. They all have about the same surface area, but they differin volume by as much as 50%. The trans-most cisterna producesexclusively clathrin-coated buds, whereas the others displayonly nonclathrin coated buds. This finding challenges traditionalviews of where sorting occurs within the Golgi complex. Tubules with budding profiles extend from the margins of both cisand trans cisternae. They pass beyond neighboring cisternae,suggesting that these tubules contribute to traffic to and/orfrom the Golgi. Vesicle-filled "wells" open to both the cisand lateral sides of the stacks. The stacks of cisternae arepositioned between two types of ER, cis and trans. The cisER lies adjacent to the ER-Golgi intermediate compartment, whichconsists of discrete polymorphic membranous elements layeredin 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 betweenER and Golgi membranes. Within 0.2 µm of the cisternaestudied, there are 394 vesicles (8 clathrin coated, 190 nonclathrincoated, and 196 noncoated), indicating considerable vesiculartraffic in this Golgi region. Our data place structural constraintson models of trafficking to, through, and from the Golgi complex.

Key Words: Golgi • membrane traffic • cryofixation • electron microscopy • tomography

Abbreviations used in this paper: 2-D, 2-dimensional; CGN, cis-Golgi network; ERGIC, ER-Golgi intermediate compartment; HVEM, high-voltage electron microscopy; NCR, noncompact region; NRK, normal rat kidney; VTC, vesicular tubular cluster.

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