J. Cell Biol., Volume 141, Number 4, May 18, 1998 955-966

An Ordered Inheritance Strategy for the Golgi Apparatus: Visualization of Mitotic Disassembly Reveals a Role for the Mitotic Spindle

David T. Shima,^* Noemí Cabrera-Poch,^* Rainer Pepperkok, and Graham Warren^*

^* Cell Biology Laboratory, and  Light Microscopy Laboratory, Imperial Cancer Research Fund, London WC2A 3PX, United Kingdom

During mitosis, the ribbon of the Golgi apparatus is transformed into dispersed tubulo-vesicular membranes, proposed to facilitate stochastic inheritance of this low copy number organelle at cytokinesis. Here, we have analyzed the mitotic disassembly of the Golgi apparatus in living cells and provide evidence that inheritance is accomplished through an ordered partitioning mechanism. Using a Sar1p dominant inhibitor of cargo exit from the endoplasmic reticulum (ER), we found that the disassembly of the Golgi observed during mitosis or microtubule disruption did not appear to involve retrograde transport of Golgi residents to the ER and subsequent reorganization of Golgi membrane fragments at ER exit sites, as has been suggested. Instead, direct visualization of a green fluorescent protein (GFP)-tagged Golgi resident through mitosis showed that the Golgi ribbon slowly reorganized into 1-3-µm fragments during G2/early prophase. A second stage of fragmentation occurred coincident with nuclear envelope breakdown and was accompanied by the bulk of mitotic Golgi redistribution. By metaphase, mitotic Golgi dynamics appeared to cease. Surprisingly, the disassembly of mitotic Golgi fragments was not a random event, but involved the reorganization of mitotic Golgi by microtubules, suggesting that analogous to chromosomes, the Golgi apparatus uses the mitotic spindle to ensure more accurate partitioning during cytokinesis.

CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

This article has been cited by other articles:

• Wei, J.-H., Seemann, J. (2009). The mitotic spindle mediates inheritance of the Golgi ribbon structure. JCB 184: 391-397 [Abstract] [Full Text]  
• Goss, J. W., Toomre, D. K. (2008). Both daughter cells traffic and exocytose membrane at the cleavage furrow during mammalian cytokinesis. JCB 181: 1047-1054 [Abstract] [Full Text]  
• de Graffenried, C. L., Ho, H. H., Warren, G. (2008). Polo-like kinase is required for Golgi and bilobe biogenesis in Trypanosoma brucei. JCB 181: 431-438 [Abstract] [Full Text]  
• Tang, D., Mar, K., Warren, G., Wang, Y. (2008). Molecular Mechanism of Mitotic Golgi Disassembly and Reassembly Revealed by a Defined Reconstitution Assay. J. Biol. Chem. 283: 6085-6094 [Abstract] [Full Text]  
• Yilmaz Dejgaard, S., Murshid, A., Dee, K. M., Presley, J. F. (2007). Confocal Microscopy-based Linescan Methodologies for Intra-Golgi Localization of Proteins. J. Histochem. Cytochem. 55: 709-719 [Abstract] [Full Text]  
• Iinuma, T., Shiga, A., Nakamoto, K., O'Brien, M. B., Aridor, M., Arimitsu, N., Tagaya, M., Tani, K. (2007). Mammalian Sec16/p250 Plays a Role in Membrane Traffic from the Endoplasmic Reticulum. J. Biol. Chem. 282: 17632-17639 [Abstract] [Full Text]  
• Gaietta, G. M., Giepmans, B. N. G., Deerinck, T. J., Smith, W. B., Ngan, L., Llopis, J., Adams, S. R., Tsien, R. Y., Ellisman, M. H. (2006). Golgi twins in late mitosis revealed by genetically encoded tags for live cell imaging and correlated electron microscopy. Proc. Natl. Acad. Sci. USA 103: 17777-17782 [Abstract] [Full Text]  
• Eisman, R. C., Stewart, N., Miller, D., Kaufman, T. C. (2006). centrosomin's beautiful sister (cbs) encodes a GRIP-domain protein that marks Golgi inheritance and functions in the centrosome cycle inDrosophila. J. Cell Sci. 119: 3399-3412 [Abstract] [Full Text]  
• Arasaki, K., Taniguchi, M., Tani, K., Tagaya, M. (2006). RINT-1 Regulates the Localization and Entry of ZW10 to the Syntaxin 18 Complex. Mol. Biol. Cell 17: 2780-2788 [Abstract] [Full Text]  
• Altan-Bonnet, N., Sougrat, R., Liu, W., Snapp, E. L., Ward, T., Lippincott-Schwartz, J. (2006). Golgi Inheritance in Mammalian Cells Is Mediated through Endoplasmic Reticulum Export Activities. Mol. Biol. Cell 17: 990-1005 [Abstract] [Full Text]  
• Poteryaev, D., Squirrell, J. M., Campbell, J. M., White, J. G., Spang, A. (2005). Involvement of the Actin Cytoskeleton and Homotypic Membrane Fusion in ER Dynamics in Caenorhabditis elegans. Mol. Biol. Cell 16: 2139-2153 [Abstract] [Full Text]  
• daSilva, L. L.P., Snapp, E. L., Denecke, J., Lippincott-Schwartz, J., Hawes, C., Brandizzi, F. (2004). Endoplasmic Reticulum Export Sites and Golgi Bodies Behave as Single Mobile Secretory Units in Plant Cells. Plant Cell 16: 1753-1771 [Abstract] [Full Text]  
• Axelsson, M. A. B., Warren, G. (2004). Rapid, Endoplasmic Reticulum-independent Diffusion of the Mitotic Golgi Haze. Mol. Biol. Cell 15: 1843-1852 [Abstract] [Full Text]  
• Cha, H., Smith, B. L., Gallo, K., Machamer, C. E., Shapiro, P. (2004). Phosphorylation of golgin-160 by mixed lineage kinase 3. J. Cell Sci. 117: 751-760 [Abstract] [Full Text]  
• Fan, J., Beck, K. A. (2004). A role for the spectrin superfamily member Syne-1 and kinesin II in cytokinesis. J. Cell Sci. 117: 619-629 [Abstract] [Full Text]  
• Husain, M., Moss, B. (2003). Evidence against an Essential Role of COPII-Mediated Cargo Transport to the Endoplasmic Reticulum-Golgi Intermediate Compartment in the Formation of the Primary Membrane of Vaccinia Virus. J. Virol. 77: 11754-11766 [Abstract] [Full Text]  
• Diao, A., Rahman, D., Pappin, D. J.C., Lucocq, J., Lowe, M. (2003). The coiled-coil membrane protein golgin-84 is a novel rab effector required for Golgi ribbon formation. JCB 160: 201-212 [Abstract] [Full Text]  
• Moreno, R. D., Schatten, G., Ramalho-Santos, J. (2002). Golgi Apparatus Dynamics During Mouse Oocyte In Vitro Maturation: Effect of the Membrane Trafficking Inhibitor Brefeldin A. Biol. Reprod. 66: 1259-1266 [Abstract] [Full Text]  
• Yoshimura, S.-i., Nakamura, N., Barr, F. A., Misumi, Y., Ikehara, Y., Ohno, H., Sakaguchi, M., Mihara, K. (2002). Direct targeting of cis-Golgi matrix proteins to the Golgi apparatus. J. Cell Sci. 114: 4105-4115 [Abstract] [Full Text]  
• Seemann, J., Pypaert, M., Taguchi, T., Malsam, J., Warren, G. (2002). Partitioning of the Matrix Fraction of the Golgi Apparatus During Mitosis in Animal Cells. Science 295: 848-851 [Abstract] [Full Text]  
• Nagahama, M., Usui, S., Shinohara, T., Yamaguchi, T., Tani, K., Tagaya, M. (2002). Inactivation of G{alpha}z causes disassembly of the Golgi apparatus. J. Cell Sci. 115: 4483-4493 [Abstract] [Full Text]  
• Jokitalo, E., Cabrera-Poch, N., Warren, G., Shima, D. T. (2001). Golgi clusters and vesicles mediate mitotic inheritance independently of the endoplasmic reticulum. JCB 154: 317-330 [Abstract] [Full Text]  
• Chabin-Brion, K., Marceiller, J., Perez, F., Settegrana, C., Drechou, A., Durand, G., Pous, C. (2001). The Golgi Complex Is a Microtubule-organizing Organelle. Mol. Biol. Cell 12: 2047-2060 [Abstract] [Full Text]  
• Jesch, S. A., Lewis, T. S., Ahn, N. G., Linstedt, A. D. (2001). Mitotic Phosphorylation of Golgi Reassembly Stacking Protein 55 by Mitogen-activated Protein Kinase ERK2. Mol. Biol. Cell 12: 1811-1817 [Abstract] [Full Text]  
• Fontijn, R. D., Goud, B., Echard, A., Jollivet, F., van Marle, J., Pannekoek, H., Horrevoets, A. J. G. (2001). The Human Kinesin-Like Protein RB6K Is under Tight Cell Cycle Control and Is Essential for Cytokinesis. Mol. Cell. Biol. 21: 2944-2955 [Abstract] [Full Text]  
• Lu, Z., Joseph, D., Bugnard, E., Zaal, K. J. M., Ralston, E. (2001). Golgi Complex Reorganization during Muscle Differentiation: Visualization in Living Cells and Mechanism. Mol. Biol. Cell 12: 795-808 [Abstract] [Full Text]  
• Walenta, J. H., Didier, A. J., Liu, X., Kramer, H. (2001). The Golgi-associated Hook3 Protein Is a Member of a Novel Family of Microtubule-binding Proteins. JCB 152: 923-934 [Abstract] [Full Text]  
• Voorn-Brouwer, T., Kragt, A., Tabak, H. F., Distel, B. (2001). Peroxisomal membrane proteins are properly targeted to peroxisomes in the absence of COPI- and COPII-mediated vesicular transport. J. Cell Sci. 114: 2199-2204 [Abstract] [Full Text]  
• Todorow, Z., Spang, A., Carmack, E., Yates, J., Schekman, R. (2000). Active recycling of yeast Golgi mannosyltransferase complexes through the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 10.1073/pnas.250472397v1 [Abstract] [Full Text]  
• Hammond, A. T., Glick, B. S. (2000). Dynamics of Transitional Endoplasmic Reticulum Sites in Vertebrate Cells. Mol. Biol. Cell 11: 3013-3030 [Abstract] [Full Text]  
• Nebenführ, A., Frohlick, J. A., Staehelin, L. A. (2000). Redistribution of Golgi Stacks and Other Organelles during Mitosis and Cytokinesis in Plant Cells. Plant Physiol. 124: 135-152 [Abstract] [Full Text]  
• Okamoto, C. T., McKinney, J., Jeng, Y. Y. (2000). Clathrin in mitotic spindles. Am. J. Physiol. Cell Physiol. 279: C369-C374 [Abstract] [Full Text]  
• Lee, T. H., Linstedt, A. D. (2000). Potential Role for Protein Kinases in Regulation of Bidirectional Endoplasmic Reticulum-to-Golgi Transport Revealed by Protein Kinase Inhibitor H89. Mol. Biol. Cell 11: 2577-2590 [Abstract] [Full Text]  
• Gerez, L., Mohrmann, K., van Raak, M., Jongeneelen, M., Zhou, X. Z., Lu, K. P., van der Sluijs, P. (2000). Accumulation of rab4GTP in the Cytoplasm and Association with the Peptidyl-Prolyl Isomerase Pin1 during Mitosis. Mol. Biol. Cell 11: 2201-2211 [Abstract] [Full Text]  
• Nelson, W. J. (2000). W(h)ither the Golgi during Mitosis?. JCB 149: 243-248 [Abstract] [Full Text]  
• Lowe, M., Gonatas, N. K., Warren, G. (2000). The Mitotic Phosphorylation Cycle of the cis-Golgi Matrix Protein GM130. JCB 149: 341-356 [Abstract] [Full Text]  
• Kano, F., Takenaka, K., Yamamoto, A., Nagayama, K., Nishida, E., Murata, M. (2000). MEK and Cdc2 Kinase Are Sequentially Required for Golgi Disassembly in MDCK Cells by the Mitotic Xenopus Extracts. JCB 149: 357-368 [Abstract] [Full Text]  
• Terasaki, M. (2000). Dynamics of the Endoplasmic Reticulum and Golgi Apparatus during Early Sea Urchin Development. Mol. Biol. Cell 11: 897-914 [Abstract] [Full Text]  
• Robertson, A. M., Allan, V. J. (2000). Brefeldin A-dependent Membrane Tubule Formation Reconstituted In Vitro Is Driven by a Cell Cycle-regulated Microtubule Motor. Mol. Biol. Cell 11: 941-955 [Abstract] [Full Text]  
• Seemann, J., Jokitalo, E. J., Warren, G. (2000). The Role of the Tethering Proteins p115 and GM130 in Transport through the Golgi Apparatus In Vivo. Mol. Biol. Cell 11: 635-645 [Abstract] [Full Text]  
• Hauri, H., Kappeler, F, Andersson, H, Appenzeller, C (2000). ERGIC-53 and traffic in the secretory pathway. J. Cell Sci. 113: 587-596 [Abstract]  
• Lin, C.-C., Love, H. D., Gushue, J. N., Bergeron, J. J.M., Ostermann, J. (1999). ER/Golgi Intermediates Acquire Golgi Enzymes by Brefeldin A-Sensitive Retrograde Transport In Vitro. JCB 147: 1457-1472 [Abstract] [Full Text]  
• Drecktrah, D., Brown, W. J. (1999). Phospholipase A2 Antagonists Inhibit Nocodazole-induced Golgi Ministack Formation: Evidence of an ER Intermediate and Constitutive Cycling. Mol. Biol. Cell 10: 4021-4032 [Abstract] [Full Text]  
• Rogers, S. L., Karcher, R. L., Roland, J. T., Minin, A. A., Steffen, W., Gelfand, V. I. (1999). Regulation of Melanosome Movement in the Cell Cycle by Reversible Association with Myosin V. JCB 146: 1265-1276 [Abstract] [Full Text]  
• Thieblemont, N., Wright, S. D. (1999). Transport of Bacterial Lipopolysaccharide to the Golgi Apparatus. JEM 190: 523-534 [Abstract] [Full Text]  
• Shorter, J., Warren, G. (1999). A Role for the Vesicle Tethering Protein, p115, in the Post-mitotic Stacking of Reassembling Golgi Cisternae in a Cell-free System. JCB 146: 57-70 [Abstract] [Full Text]  
• Juin, P., Hueber, A.-O., Littlewood, T., Evan, G. (1999). c-Myc-induced sensitization to apoptosis is mediated through cytochrome c release. Genes Dev. 13: 1367-1381 [Abstract] [Full Text]  
• de Figueiredo, P., Polizotto, R. S., Drecktrah, D., Brown, W. J. (1999). Membrane Tubule-mediated Reassembly and Maintenance of the Golgi Complex Is Disrupted by Phospholipase A2 Antagonists. Mol. Biol. Cell 10: 1763-1782 [Abstract] [Full Text]  
• Füllekrug, J., Suganuma, T., Tang, B. L., Hong, W., Storrie, B., Nilsson, T. (1999). Localization and Recycling of gp27 (hp24gamma 3): Complex Formation with Other p24 Family Members. Mol. Biol. Cell 10: 1939-1955 [Abstract] [Full Text]  
• Lee, T. H., Linstedt, A. D. (1999). Osmotically Induced Cell Volume Changes Alter Anterograde and Retrograde Transport, Golgi Structure, and COPI Dissociation. Mol. Biol. Cell 10: 1445-1462 [Abstract] [Full Text]  
• Shugrue, C., Kolen, E., Peters, H, Czernik, A, Kaiser, C, Matovcik, L, Hubbard, A., Gorelick, F (1999). Identification of the putative mammalian orthologue of Sec31P, a component of the COPII coat. J. Cell Sci. 112: 4547-4556 [Abstract]  
• Roghi, C, Allan, V. (1999). Dynamic association of cytoplasmic dynein heavy chain 1a with the Golgi apparatus and intermediate compartment. J. Cell Sci. 112: 4673-4685 [Abstract]  
• Farmaki, T, Ponnambalam, S, Prescott, A., Clausen, H, Tang, B., Hong, W, Lucocq, J. (1999). Forward and retrograde trafficking in mitotic animal cells. ER-Golgi transport arrest restricts protein export from the ER into COPII-coated structures. J. Cell Sci. 112: 589-600 [Abstract]  
• Jackson, M., Simpson, J., Girod, A, Pepperkok, R, Roberts, L., Lord, J. (1999). The KDEL retrieval system is exploited by Pseudomonas exotoxin A, but not by Shiga-like toxin-1, during retrograde transport from the Golgi complex to the endoplasmic reticulum. J. Cell Sci. 112: 467-475 [Abstract]  
• Storrie, B., White, J., Rottger, S., Stelzer, E. H.K., Suganuma, T., Nilsson, T. (1998). Recycling of Golgi-resident Glycosyltransferases through the ER Reveals a Novel Pathway and Provides an Explanation for Nocodazole-induced Golgi Scattering. JCB 143: 1505-1521 [Abstract] [Full Text]  
• Presley, J. F., Smith, C., Hirschberg, K., Miller, C., Cole, N. B., Zaal, K. J. M., Lippincott-Schwartz, J. (1998). Golgi Membrane Dynamics. Mol. Biol. Cell 9: 1617-1626 [Full Text]  
• Gaulin, J.-F., Fiset, A., Fortier, S., Faure, R. L. (2000). Characterization of Cdk2-Cyclin E Complexes in Plasma Membrane and Endosomes of Liver Parenchyma. INSULIN-DEPENDENT REGULATION. J. Biol. Chem. 275: 16658-16665 [Abstract] [Full Text]  
• Todorow, Z., Spang, A., Carmack, E., Yates, J., Schekman, R. (2000). Active recycling of yeast Golgi mannosyltransferase complexes through the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 97: 13643-13648 [Abstract] [Full Text]  
• Puthenveedu, M. A., Linstedt, A. D. (2001). Evidence that Golgi structure depends on a p115 activity that is independent of the vesicle tether components giantin and GM130. JCB 155: 227-238 [Abstract] [Full Text]  

Home | Help | Feedback | Subscriptions | Archive | Search | Table of Contents