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NB Cole, N Sciaky, A Marotta, J Song and J Lippincott-Schwartz
Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, USA.
Microtubule disruption has dramatic effects on the normal centrosomal localization of the Golgi complex, with Golgi elements remaining as competent functional units but undergoing a reversible "fragmentation" and dispersal throughout the cytoplasm. In this study we have analyzed this process using digital fluorescence image processing microscopy combined with biochemical and ultrastructural approaches. After microtubule depolymerization, Golgi membrane components were found to redistribute to a distinct number of peripheral sites that were not randomly distributed, but corresponded to sites of protein exit from the ER. Whereas Golgi enzymes redistributed gradually over several hours to these peripheral sites, ERGIC-53 (a protein which constitutively cycles between the ER and Golgi) redistributed rapidly (within 15 minutes) to these sites after first moving through the ER. Prior to this redistribution, Golgi enzyme processing of proteins exported from the ER was inhibited and only returned to normal levels after Golgi enzymes redistributed to peripheral ER exit sites where Golgi stacks were regenerated. Experiments examining the effects of microtubule disruption on the membrane pathways connecting the ER and Golgi suggested their potential role in the dispersal process. Whereas clustering of peripheral pre-Golgi elements into the centrosomal region failed to occur after microtubule disruption, Golgi-to-ER membrane recycling was only slightly inhibited. Moreover, conditions that impeded Golgi-to-ER recycling completely blocked Golgi fragmentation. Based on these findings we propose that a slow but constitutive flux of Golgi resident proteins through the same ER/Golgi cycling pathways as ERGIC-53 underlies Golgi Dispersal upon microtubule depolymerization. Both ERGIC-53 and Golgi proteins would accumulate at peripheral ER exit sites due to failure of membranes at these sites to cluster into the centrosomal region. Regeneration of Golgi stacks at these peripheral sites would re-establish secretory flow from the ER into the Golgi complex and result in Golgi dispersal.
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O. W. Rossanese, J. Soderholm, B. J. Bevis, I. B. Sears, J. O'Connor, E. K. Williamson, and B. S. Glick Golgi Structure Correlates with Transitional Endoplasmic Reticulum Organization in Pichia pastoris and Saccharomyces cerevisiae J. Cell Biol., April 5, 1999; 145(1): 69 - 81. [Abstract] [Full Text] [PDF]
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C. H. George, J. M. Kendall, and W. H. Evans Intracellular Trafficking Pathways in the Assembly of Connexins into Gap Junctions J. Biol. Chem., March 26, 1999; 274(13): 8678 - 8685. [Abstract] [Full Text] [PDF]
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C Roghi and V. Allan Dynamic association of cytoplasmic dynein heavy chain 1a with the Golgi apparatus and intermediate compartment J. Cell Sci., January 12, 1999; 112(24): 4673 - 4685. [Abstract] [PDF]
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M del Valle, Y Robledo, and I. Sandoval Membrane flow through the Golgi apparatus: specific disassembly of the cis-Golgi network by ATP depletion J. Cell Sci., January 11, 1999; 112(22): 4017 - 4029. [Abstract] [PDF]
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B. Storrie, J. White, S. Rottger, E. H.K. Stelzer, T. Suganuma, and T. Nilsson Recycling of Golgi-resident Glycosyltransferases through the ER Reveals a Novel Pathway and Provides an Explanation for Nocodazole-induced Golgi Scattering J. Cell Biol., December 14, 1998; 143(6): 1505 - 1521. [Abstract] [Full Text] [PDF]
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H. Palokangas, M. Ying, K. Väänänen, and J. Saraste Retrograde Transport from the Pre-Golgi Intermediate Compartment and the Golgi Complex Is Affected by the Vacuolar H+-ATPase Inhibitor Bafilomycin A1 Mol. Biol. Cell, December 1, 1998; 9(12): 3561 - 3578. [Abstract] [Full Text]
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S. Duvet, L. Cocquerel, A. Pillez, R. Cacan, A. Verbert, D. Moradpour, C. Wychowski, and J. Dubuisson Hepatitis C Virus Glycoprotein Complex Localization in the Endoplasmic Reticulum Involves a Determinant for Retention and Not Retrieval J. Biol. Chem., November 27, 1998; 273(48): 32088 - 32095. [Abstract] [Full Text] [PDF]
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D. S. Nelson, C. Alvarez, Y.-s. Gao, R. Garcia-Mata, E. Fialkowski, and E. Sztul The Membrane Transport Factor TAP/p115 Cycles between the Golgi and Earlier Secretory Compartments and Contains Distinct Domains Required for Its Localization and Function J. Cell Biol., October 19, 1998; 143(2): 319 - 331. [Abstract] [Full Text] [PDF]
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A. T. Fullerton, M.-Y. Bau, P. A. Conrad, and G. S. Bloom In Vitro Reconstitution of Microtubule Plus End-directed, GTPgamma S-sensitive Motility ofGolgi Membranes Mol. Biol. Cell, October 1, 1998; 9(10): 2699 - 2714. [Abstract] [Full Text]
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J. Dietrich, T. Backstrom, J. P. H. Lauritsen, J. Kastrup, M. D. Christensen, F. von Bulow, E. Palmer, and C. Geisler The Phosphorylation State of CD3gamma Influences T Cell Responsiveness and Controls T Cell Receptor Cycling J. Biol. Chem., September 11, 1998; 273(37): 24232 - 24238. [Abstract] [Full Text] [PDF]
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C. Pous, K. Chabin, A. Drechou, L. Barbot, T. Phung-Koskas, C. Settegrana, M.L. Bourguet-Kondracki, M. Maurice, D. Cassio, M. Guyot, et al. Functional Specialization of Stable and Dynamic Microtubules in Protein Traffic in WIF-B Cells J. Cell Biol., July 13, 1998; 142(1): 153 - 165. [Abstract] [Full Text] [PDF]
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J. F. Presley, C. Smith, K. Hirschberg, C. Miller, N. B. Cole, K. J. M. Zaal, and J. Lippincott-Schwartz Golgi Membrane Dynamics Mol. Biol. Cell, July 1, 1998; 9(7): 1617 - 1626. [Full Text]
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D. T. Shima, N. Cabrera-Poch, R. Pepperkok, and G. Warren An Ordered Inheritance Strategy for the Golgi Apparatus: Visualization of Mitotic Disassembly Reveals a Role for the Mitotic Spindle J. Cell Biol., May 18, 1998; 141(4): 955 - 966. [Abstract] [Full Text] [PDF]
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A. Harada, Y. Takei, Y. Kanai, Y. Tanaka, S. Nonaka, and N. Hirokawa Golgi Vesiculation and Lysosome Dispersion in Cells Lacking Cytoplasmic Dynein J. Cell Biol., April 6, 1998; 141(1): 51 - 59. [Abstract] [Full Text] [PDF]
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G. S. Bloom and L. S.B. Goldstein Cruising along Microtubule Highways: How Membranes Move through the Secretory Pathway J. Cell Biol., March 23, 1998; 140(6): 1277 - 1280. [Full Text] [PDF]
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S. A. Jesch and A. D. Linstedt The Golgi and Endoplasmic Reticulum Remain Independent during Mitosis in HeLa Cells Mol. Biol. Cell, March 1, 1998; 9(3): 623 - 635. [Abstract] [Full Text]
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N. B. Cole, J. Ellenberg, J. Song, D. DiEuliis, and J. Lippincott-Schwartz Retrograde Transport of Golgi-localized Proteins to the ER J. Cell Biol., January 12, 1998; 140(1): 1 - 15. [Abstract] [Full Text] [PDF]
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D Drecktrah, P de Figueiredo, R. Mason, and W. Brown Retrograde trafficking of both Golgi complex and TGN markers to the ER induced by nordihydroguaiaretic acid and cyclofenil diphenol J. Cell Sci., January 4, 1998; 111(7): 951 - 965. [Abstract] [PDF]
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W. Yang and B. Storrie Scattered Golgi Elements during Microtubule Disruption Are Initially Enriched in Trans-Golgi Proteins Mol. Biol. Cell, January 1, 1998; 9(1): 191 - 207. [Abstract] [Full Text]
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M. Maceyka and C. E. Machamer Ceramide Accumulation Uncovers a Cycling Pathway for the cis-Golgi Network Marker, Infectious Bronchitis Virus M Protein J. Cell Biol., December 15, 1997; 139(6): 1411 - 1418. [Abstract] [Full Text] [PDF]
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M. Rojo, R. Pepperkok, G. Emery, R. Kellner, E. Stang, R. G. Parton, and J. Gruenberg Involvement of the Transmembrane Protein p23 in Biosynthetic Protein Transport J. Cell Biol., December 1, 1997; 139(5): 1119 - 1135. [Abstract] [Full Text] [PDF]
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N. Sciaky, J. Presley, C. Smith, K. J.M. Zaal, N. Cole, J. E. Moreira, M. Terasaki, E. Siggia, and J. Lippincott-Schwartz Golgi Tubule Traffic and the Effects of Brefeldin A Visualized in Living Cells J. Cell Biol., December 1, 1997; 139(5): 1137 - 1155. [Abstract] [Full Text] [PDF]
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J. K. Burkhardt, C. J. Echeverri, T. Nilsson, and R. B. Vallee Overexpression of the Dynamitin (p50) Subunit of the Dynactin Complex Disrupts Dynein-dependent Maintenance of Membrane Organelle Distribution J. Cell Biol., October 20, 1997; 139(2): 469 - 484. [Abstract] [Full Text] [PDF]
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