Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells

doi:10.1083/jcb.126.3.661

This Article

	Full Text (PDF, 4345K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Fath, K. R.
	Articles by Burgess, D. R.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Fath, K. R.
	Articles by Burgess, D. R.


Social Bookmarking

	What's this?

ARTICLES

Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells

KR Fath, GM Trimbur and DR Burgess
Department of Biological Sciences, University of Pittsburgh, Pennsylvania 15260.

Microtubules (MT) are required for the efficient transport of membranes from the trans-Golgi and for transcytosis of vesicles from the basolateral membrane to the apical cytoplasm in polarized epithelia. MTs in these cells are primarily oriented with their plus ends basally near the Golgi and their minus-ends in the apical cytoplasm. Here we report that isolated Golgi and Golgi-enriched membranes from intestinal epithelial cells possess the actin based motor myosin-I, the MT minus- end-directed motor cytoplasmic dynein and its in vitro motility activator dynactin (p150/Glued). The Golgi can be separated into stacks, possessing features of the Golgi cisternae, and small membranes enriched in the trans-Golgi network marker TGN 38/41. Whereas myosin-I is present on all membranes in the Golgi fraction, dynein is present only on the small membrane fraction. Dynein, like myosin-I, is associated with membranes as a cytoplasmic peripheral membrane protein. Dynein and myosin-I coassociate with membranes that bind to MTs and cross-link actin filaments and MTs in a nucleotide-dependent manner. We propose that cytoplasmic dynein moves Golgi membranes along MTs to the cell cortex where myosin-I provides local delivery through the actin- rich cytoskeleton to the apical membrane.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Levy, J. R., Holzbaur, E. L. F. (2008). Dynein drives nuclear rotation during forward progression of motile fibroblasts. J. Cell Sci. 121: 3187-3195 [Abstract] [Full Text]
Tyska, M. J., Mackey, A. T., Huang, J.-D., Copeland, N. G., Jenkins, N. A., Mooseker, M. S. (2005). Myosin-1a Is Critical for Normal Brush Border Structure and Composition. Mol. Biol. Cell 16: 2443-2457 [Abstract] [Full Text]
Tyska, M. J., Mooseker, M. S. (2004). A role for myosin-1A in the localization of a brush border disaccharidase. JCB 165: 395-405 [Abstract] [Full Text]
Duran, J. M., Valderrama, F., Castel, S., Magdalena, J., Tomas, M., Hosoya, H., Renau-Piqueras, J., Malhotra, V., Egea, G. (2003). Myosin Motors and Not Actin Comets Are Mediators of the Actin-based Golgi-to-Endoplasmic Reticulum Protein Transport. Mol. Biol. Cell 14: 445-459 [Abstract] [Full Text]
Romagnoli, S., Cai, G., Cresti, M. (2003). In Vitro Assays Demonstrate That Pollen Tube Organelles Use Kinesin-Related Motor Proteins to Move along Microtubules. Plant Cell 15: 251-269 [Abstract] [Full Text]
Susalka, S. J., Nikulina, K., Salata, M. W., Vaughan, P. S., King, S. M., Vaughan, K. T., Pfister, K. K. (2002). The Roadblock Light Chain Binds a Novel Region of the Cytoplasmic Dynein Intermediate Chain. J. Biol. Chem. 277: 32939-32946 [Abstract] [Full Text]
Shigematsu, S., Khan, A. H., Kanzaki, M., Pessin, J. E. (2002). Intracellular Insulin-Responsive Glucose Transporter (GLUT4) Distribution But Not Insulin-Stimulated GLUT4 Exocytosis and Recycling Are Microtubule Dependent. Mol. Endocrinol. 16: 1060-1068 [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]
Ravkov, E. V., Compans, R. W. (2001). Hantavirus Nucleocapsid Protein Is Expressed as a Membrane-Associated Protein in the Perinuclear Region. J. Virol. 75: 1808-1815 [Abstract] [Full Text]
Habermann, A, Schroer, T., Griffiths, G, Burkhardt, J. (2001). Immunolocalization of cytoplasmic dynein and dynactin subunits in cultured macrophages: enrichment on early endocytic organelles. J. Cell Sci. 114: 229-240 [Abstract]
Cai, G., Romagnoli, S., Moscatelli, A., Ovidi, E., Gambellini, G., Tiezzi, A., Cresti, M. (2000). Identification and Characterization of a Novel Microtubule-Based Motor Associated with Membranous Organelles in Tobacco Pollen Tubes. Plant Cell 12: 1719-1736 [Abstract] [Full Text]
Brendza, R. P., Sheehan, K. B., Turner, F.R., Saxton, W. M. (2000). Clonal Tests of Conventional Kinesin Function during Cell Proliferation and Differentiation. Mol. Biol. Cell 11: 1329-1343 [Abstract] [Full Text]
De Matteis, M., Morrow, J. (2000). Spectrin tethers and mesh in the biosynthetic pathway. J. Cell Sci. 113: 2331-2343 [Abstract]
Martel, V, Vignoud, L, Dupe, S, Frachet, P, Block, M., Albiges-Rizo, C (2000). Talin controls the exit of the integrin alpha 5 beta 1 from an early compartment of the secretory pathway. J. Cell Sci. 113: 1951-1961 [Abstract]
Ku, N.-O., Zhou, X., Toivola, D. M., Omary, M. B. (1999). The cytoskeleton of digestive epithelia in health and disease. Am. J. Physiol. Gastrointest. Liver Physiol. 277: G1108-G1137 [Abstract] [Full Text]
Stephens, D. J., Banting, G. (1999). Direct Interaction of the trans-Golgi Network Membrane Protein, TGN38, with the F-actin Binding Protein, Neurabin. J. Biol. Chem. 274: 30080-30086 [Abstract] [Full Text]
Escalante-Ochoa, C., Ducatelle, R., Charlier, G., De Vos, K., Haesebrouck, F. (1999). Significance of Host Cell Kinesin in the Development of Chlamydia psittaci. Infect. Immun. 67: 5441-5446 [Abstract] [Full Text]
Itin, C., Ulitzur, N., Mühlbauer, B., Pfeffer, S. R. (1999). Mapmodulin, Cytoplasmic Dynein, and Microtubules Enhance the Transport of Mannose 6-Phosphate Receptors from Endosomes to the Trans-Golgi Network. Mol. Biol. Cell 10: 2191-2197 [Abstract] [Full Text]
Heimann, K., Percival, J. M., Weinberger, R., Gunning, P., Stow, J. L. (1999). Specific Isoforms of Actin-binding Proteins on Distinct Populations of Golgi-derived Vesicles. J. Biol. Chem. 274: 10743-10750 [Abstract] [Full Text]
Lee, S., Wisniewski, J. C., Dentler, W. L., Asai, D. J. (1999). Gene Knockouts Reveal Separate Functions for Two Cytoplasmic Dyneins in Tetrahymena thermophila. Mol. Biol. Cell 10: 771-784 [Abstract] [Full Text]
Vaughan, K., Tynan, S., Faulkner, N., Echeverri, C., Vallee, R. (1999). Colocalization of cytoplasmic dynein with dynactin and CLIP-170 at microtubule distal ends. J. Cell Sci. 112: 1437-1447 [Abstract]
Wu, X., Bowers, B., Rao, K., Wei, Q., Hammer, J. A. III (1998). Visualization of Melanosome Dynamics within Wild-Type and Dilute Melanocytes Suggests a Paradigm for Myosin V Function In Vivo. JCB 143: 1899-1918 [Abstract] [Full Text]
Buss, F., Kendrick-Jones, J., Lionne, C., Knight, A. E., Cote, G. P., Paul Luzio, J. (1998). The Localization of Myosin VI at the Golgi Complex and Leading Edge of Fibroblasts and Its Phosphorylation and Recruitment into Membrane Ruffles of A431 Cells after Growth Factor Stimulation. JCB 143: 1535-1545 [Abstract] [Full Text]
HAMM-ALVAREZ, S. F., SHEETZ, M. P. (1998). Microtubule-Dependent Vesicle Transport: Modulation of Channel and Transporter Activity in Liver and Kidney. Physiol. Rev. 78: 1109-1129 [Abstract] [Full Text]
Priddle, H., Hemmings, L., Monkley, S., Woods, A., Patel, B., Sutton, D., Dunn, G. A., Zicha, D., Critchley, D. R. (1998). Disruption of the Talin Gene Compromises Focal Adhesion Assembly in Undifferentiated but Not Differentiated Embryonic Stem Cells. JCB 142: 1121-1133 [Abstract] [Full Text]
Tai, A. W., Chuang, J.-Z., Sung, C.-H. (1998). Localization of Tctex-1, a Cytoplasmic Dynein Light Chain, to the Golgi Apparatus and Evidence for Dynein Complex Heterogeneity. J. Biol. Chem. 273: 19639-19649 [Abstract] [Full Text]
Zegers, M. M.�P., Zaal, K. J.�M., van IJzendoorn, S. C.�D., Klappe, K., Hoekstra, D. (1998). Actin Filaments and Microtubules are Involved in Different Membrane Traffic Pathways That Transport Sphingolipids to the Apical Surface of Polarized HepG2 Cells. Mol. Biol. Cell 9: 1939-1949 [Abstract] [Full Text]
Harada, A., Takei, Y., Kanai, Y., Tanaka, Y., Nonaka, S., Hirokawa, N. (1998). Golgi Vesiculation and Lysosome Dispersion in Cells Lacking Cytoplasmic Dynein. JCB 141: 51-59 [Abstract] [Full Text]
Ihrke, G., Martin, G. V., Shanks, M. R., Schrader, M., Schroer, T. A., Hubbard, A. L. (1998). Apical Plasma Membrane Proteins and Endolyn-78 Travel through a Subapical Compartment in Polarized WIF-B Hepatocytes. JCB 141: 115-133 [Abstract] [Full Text]
Jontes, J. D., Ostap, E. M., Pollard, T. D., Milligan, R. A. (1998). Three-dimensional Structure of Acanthamoeba castellanii Myosin-IB (MIB) Determined by Cryoelectron Microscopy of Decorated Actin Filaments. JCB 141: 155-162 [Abstract] [Full Text]
Lillie, S.H., Brown, S.S. (1998). Smy1p, a Kinesin-related Protein That Does Not Require Microtubules. JCB 140: 873-883 [Abstract] [Full Text]
Lantz, V. A., Miller, K. G. (1998). A Class VI Unconventional Myosin Is Associated with a Homologue of a Microtubule-binding Protein, Cytoplasmic Linker Protein-170, in Neurons and at the Posterior Pole of Drosophila Embryos. JCB 140: 897-910 [Abstract] [Full Text]
Criswell, P. S., Asai, D. J. (1998). Evidence for Four Cytoplasmic Dynein Heavy Chain Isoforms in Rat Testis. Mol. Biol. Cell 9: 237-247 [Abstract] [Full Text]
Ahmad, F. J., Echeverri, C. J., Vallee, R. B., Baas, P. W. (1998). Cytoplasmic Dynein and Dynactin Are Required for the Transport of Microtubules into the Axon. JCB 140: 391-401 [Abstract] [Full Text]
Fath, K. R., Trimbur, G. M., Burgess, D. R. (1997). Molecular Motors and a Spectrin Matrix Associate with Golgi Membranes In Vitro. JCB 139: 1169-1181 [Abstract] [Full Text]
Burkhardt, J. K., Echeverri, C. J., Nilsson, T., Vallee, R. B. (1997). Overexpression of the Dynamitin (p50) Subunit of the Dynactin Complex Disrupts Dynein-dependent Maintenance of Membrane Organelle Distribution. JCB 139: 469-484 [Abstract] [Full Text]
Nascimento, A. A.C., Amaral, R. G., Bizario, J. C.S., Larson, R. E., Espreafico, E. M. (1997). Subcellular Localization of Myosin-V in the B16 Melanoma Cells, a Wild-type Cell Line for the dilute Gene. Mol. Biol. Cell 8: 1971-1988 [Abstract] [Full Text]
Steffen, W., Karki, S., Vaughan, K. T., Vallee, R. B., Holzbaur, E. L.F., Weiss, D. G., Kuznetsov, S. A. (1997). The Involvement of the Intermediate Chain of Cytoplasmic Dynein in Binding the Motor Complex to Membranous Organelles of Xenopus Oocytes. Mol. Biol. Cell 8: 2077-2088 [Abstract] [Full Text]
Bi, G.-Q., Morris, R. L., Liao, G., Alderton, J. M., Scholey, J. M., Steinhardt, R. A. (1997). Kinesin- and Myosin-driven Steps of Vesicle Recruitment for Ca2+-regulated Exocytosis. JCB 138: 999-1008 [Abstract] [Full Text]
Musch, A., Cohen, D., Rodriguez-Boulan, E. (1997). Myosin II Is Involved in the Production of Constitutive Transport Vesicles from the TGN. JCB 138: 291-306 [Abstract] [Full Text]
Maples, C. J., Ruiz, W. G., Apodaca, G. (1997). Both Microtubules and Actin Filaments Are Required for Efficient Postendocytotic Traffic of the Polymeric Immunoglobulin Receptor in Polarized Madin-Darby Canine Kidney Cells. J. Biol. Chem. 272: 6741-6751 [Abstract] [Full Text]
Huber, C, Saffrich, R, Anton, M, Passreiter, M, Ansorge, W, Gorgas, K, Just, W (1997). A heterotrimeric G protein-phospholipase A2 signaling cascade is involved in the regulation of peroxisomal motility in CHO cells. J. Cell Sci. 110: 2955-2968 [Abstract]
Ikonen, E, de Almeid, J., Fath, K., Burgess, D., Ashman, K, Simons, K, Stow, J. (1997). Myosin II is associated with Golgi membranes: identification of p200 as nonmuscle myosin II on Golgi-derived vesicles. J. Cell Sci. 110: 2155-2164 [Abstract]
Fan, S., Ready, D. (1997). Glued participates in distinct microtubule-based activities in Drosophila eye development. Development 124: 1497-1507 [Abstract]
Temesvari, L. A., Bush, J. M., Peterson, M. D., Novak, K. D., Titus, M. A., Cardelli, J. A. (1996). Examination of the endosomal and lysosomal pathways in Dictyostelium discoideum myosin I mutants. J. Cell Sci. 109: 663-673 [Abstract]
Pfister, K. K., Salata, M. W., Dillman, J. F. III, Vaughan, K. T., Vallee, R. B., Torre, E., Lye, R. J. (1996). Differential Expression and Phosphorylation of the 74-kDa Intermediate Chains of Cytoplasmic Dynein in Cultured Neurons and Glia. J. Biol. Chem. 271: 1687-1694 [Abstract] [Full Text]
Criswell, P., Ostrowski, L., Asai, D. (1996). A novel cytoplasmic dynein heavy chain: expression of DHC1b in mammalian ciliated epithelial cells. J. Cell Sci. 109: 1891-1898 [Abstract]
Karki, S., Holzbaur, E. L. F. (1995). Affinity Chromatography Demonstrates a Direct Binding between Cytoplasmic Dynein and the Dynactin Complex. J. Biol. Chem. 270: 28806-28811 [Abstract] [Full Text]
Wolenski, J., Cheney, R., Mooseker, M., Forscher, P (1995). In vitro motility of immunoadsorbed brain myosin-V using a Limulus acrosomal process and optical tweezer-based assay. J. Cell Sci. 108: 1489-1496 [Abstract]
Evans, L., Lee, A., Bridgman, P., Mooseker, M. (1988). Vesicle-associated brain myosin-V can be activated to catalyze actin-based transport. J. Cell Sci. 111: 2055-2066 [Abstract]