Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution

Journal of Cell Biology

Volumn 139, Issue 2, 1997, Pages 469-484

  Burkhardt, Janis K ^a,b   Echeverri, Christophe J ^c   Nilsson, Tommy ^b   Vallee, Richard B ^c  

^a UNIVERSITY OF CHICAGO   (United States)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREFELDIN A; DYNEIN ADENOSINE TRIPHOSPHATASE; GALACTOSYLTRANSFERASE; MEMBRANE PROTEIN; MICROTUBULE PROTEIN; N ACETYLGLUCOSAMINYLTRANSFERASE; NOCODAZOLE; PROTEIN SUBUNIT; SIALYLTRANSFERASE; TRANSFERRIN RECEPTOR;

ARTICLE; CELL MEMBRANE; CELL ORGANELLE; CELLULAR DISTRIBUTION; CENTROMERE; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; GENE OVEREXPRESSION; GOLGI COMPLEX; HUMAN; HUMAN CELL; INTERPHASE; LYSOSOME; MICROTUBULE ASSEMBLY; PRIORITY JOURNAL;

ANTIGENS, CD; BIOLOGICAL MARKERS; CYTOSKELETON; DYNEIN ATPASE; ENDOSOMES; GOLGI APPARATUS; HELA CELLS; HUMANS; INTRACELLULAR MEMBRANES; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MACROMOLECULAR SUBSTANCES; MANNOSE-BINDING LECTINS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NOCODAZOLE; ORGANELLES; RECEPTORS, PEPTIDE; RECOMBINANT PROTEINS;

EID: 0030727535     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.2.469     Document Type: Article

References (75)

1. Allan, V. 1995. Protein phosphatase 1 regulates the cytoplasmic dynein-driven formation of endoplasmic reticulum networks in vitro. J Cell Biol. 128:879-891.
2. Allanm, V. 1996. Motor proteins: a dynamic duo. Curr. Biology. 6:630-633.
3. Baumgart, E., A. Völkl, T. Hashimoto, and H.D. Fahimi. 1989. Biogenesis of peroxisomes: immunocytochemical investigation of peroxisomal membrane proteins in proliferating rat liver peroxisomes and in catalase-negative loops. J. Cell Biol. 108:2221-2231.
4. Blocker, A., F.F. Severin, J.K. Burkhardt, J.B. Bingham, H. Yu, J.-C. Olivio, T.A. Schroer, A.A. Hyman, and G. Griffiths. 1997. Molecular requirements for bi-directional movement of phagosomes along microtubules. J. Cell Biol. 137:113-129.
5. Bomsel, M., R. Parton, S.A. Kuznetsov, T.A. Schroer, and J. Gruenberg. 1990. Microtubule-and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells. Cell. 62:719-731.
6. Burkhardt, J.K. 1996. In search of membrane receptors for microtubule-based motors. Is kinectin a kinesin receptor? Trends Cell Biol. 6:127-131.
7. Burkhardt, J.K., F.A. Wiebel, S. Hester, and Y. Argon. 1993. The giant organelles in beige and Chediak-Higashi fibroblasts are derived from late endosomes and mature lysosomes. J. Exp. Med. 178:1845-1856.
8. Clark, S.W., and D.I. Meyer. 1994. ACT3: a putative centractin homologue in S. crevisiae is required for proper orientation of the mitotic spindle. J. Cell Biol. 127:129-138.
9. Cole, N.B., N. Sciaky, A. Marotta, J. Song, and J. Lippincott-Schwartz. 1996. Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell. 7:631-650.
10. Corthesy Theulaz, I., A. Pauloin, and S.R. Pfeffer. 1992. Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J. Cell Biol. 118:1333-1345.
11. Echeverri, C.J., B.M. Paschal, K.T. Vaughan, and R.B. Vallee. 1996. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J. Cell Biol. 132:617-633.
12. Elluru, R.G., G.S. Bloom, and S.T. Brady. 1995. Fast axonal transport of kinesin in the rat visual system: functionality of kinesin heavy chain isoforms. Mol. Biol. Cell. 6:21-40.
13. Eshel, D., L.A. Urrestarazu, S. Vissers, J.C. Jauniaux, J.C. van Vliet-Reedijk, R.J. Planta, and I.R. Gibbons. 1993. Cytoplasmic dynein is required for normal nuclear segregation in yeast. Proc. Nat. Acad. Sci. USA. 90:11172-11176.
14. Evan, G.I., G.K. Lewis, G. Ramsay, and J.M. Bishop. 1985. Isolation of monoclonal antibodies specific for the human c-myc proto-oncogene product. Mol. Cell Biol. 5:3610-3616.
15. Fath, K.R., G.M. Trimbur, and D.R. Burgess. 1994. Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells. J. Cell Biol. 126:661-675.
16. Feiguin, F., A. Ferreira, K.S. Kosik, and A. Caceres. 1994. Kinesin-mediated organelle translocation revealed by specific cellular manipulations. J. Cell Biol. 127:1021-1039.
17. Fukuda, M. 1991. Lysosomal membrane glycoproteins. Structure, biosynthesis, and intracellular trafficking. J. Biol. Chem. 266:21327-21330.
18. Griffiths, G. 1993. Fine Structure Immunocytochemistry. Springer Verlag, Berlin. 459.
19. Heald, R., R. Tournebize, T. Blank, R. Sandaltzopoulos, P. Becker, A. Hyman, and E. Karsenti. 1996. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature (Lond.). 382:420-425.
20. Heuser, J. 1989. Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH. J. Cell Biol. 108:855-864.
21. Ho, W.C., V.J. Allan, G. van Meer, E.G. Berger, and T.E. Kreis. 1989. Reclustering of scattered Golgi elements occurs along microtubules. Eur. J. Cell Biol. 48:250-263.
22. Hollenbeck, P. 1996. The pattern and mechanism of mitochondrial transport in axons. Frontiers Biosci. 1:91-102.
23. Hollenbeck, P.J., and J.A. Swanson. 1990. Radial extension of macrophage tubular lysosomes supported by kinesin. Nature (Lond.). 346:864-866.
24. Holleran, E., M. Tokito, S. Karki, and E. Holzbaur. 1996. Centractin (Arp1) associates with spectrin revealing a potential mechanism to link dynactin to intracellular organelles. J. Cell Biol. 135:1815-1829.
25. Holzbaur, E.L., J.A. Hammarback, B.M. Paschal, N.G. Kravit, K.K. Pfister, and R.B. Vallee. 1991. Homology of a 150K cytoplasmic dynein-associated polypeptide with the Drosophila gene Glued. Nature (Lond.). 351:579-583.
26. Houliston, E., and R.P. Elinson. 1991. Evidence for the involvement of microtubules, ER, and kinesin in the cortical rotation of fertilized frog eggs. J. Cell Biol. 114:1017-1028.
27. Huebers, H.A., and C.A. Finch. 1987. The physiology of transferrin and transferrin receptors. Physiol. Rev. 67:520-582.
28. Karki, S., and E.L. Holzbaur. 1995. Affinity chromatogiaphy demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J. Biol. Chem. 270:28806-28811.
29. r 78,000 intermediate chain of Chlamydomonas outer arm dynein interacts with alpha-tubulin in situ. J. Biol. Chem. 266:8401-8407.
30. King, S.M., and G.B. Witman. 1990. Localization of an intermediate chain of outer arm dynein by immunoelectron microscopy. J. Biol. Chem. 265:19807-19811.
31. Klausner, R.D., J.G. Donaldson, and J. Lippincott-Schwartz. 1992. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116:1071-1080.
32. Knapp, P.E., and J.A. Swanson. 1990. Plasticity of the tubular lysosomal compartment in macrophages. J. Cell Sci. 95:433-439.
33. Kumar, J., H. Yu, and M.P. Sheetz. 1995. Kinectin, an essential anchor for kinesin-driven vesicle motility. Science (Wash. DC). 267:1834-1837.
34. Lin. S.X., and C.A. Collins. 1993. Regulation of the intracellular distribution of cytoplasmic dynein by serum factors and calcium. J. Cell Science. 105:579-588.
35. Lin, S.X., K.L. Ferro, and C.A. Collins. 1994. Cytoplasmic dynein undergoes intracellular redistribution concomitant with phosphorylation of the heavy chain in response to serum starvation and okadaic acid. J. Cell Biol. 127: 1009-1019.
36. Lippincott-Schwartz, J., N.B. Cole, A. Marotta, P.A. Conrad, and G.S. Bloom. 1995. Kinesin is the motor for microtubule-mediated Golgi-to-ER membrane traffic. J. Cell Biol. 128:293-306.
37. Luzio, J.P., B. Brake, G. Banting, K.E. Howell, P. Braghetta, and K.K. Stanley. 1990. Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38). Biochem. J. 270:97-102.
38. Matteoni, R., and T.E. Kreis. 1987. Translocation and clustering of endosomes and lysosomes depends on microtubules. J. Cell Biol. 105:1253-1265.
39. McGrail, M., J. Gepner, A. Silvanovich, S. Ludmann, M. Serr, and T.S. Hays. 1995. Regulation of cytoplasmic dynein function in vivo by the Drosophila glued complex. J. Cell Biol. 131:411-425.
40. McGraw, T.E., K.W. Dunn, and F.R. Maxfield. 1993. Isolation of a temperature-sensitive variant Chinese hamster ovary cell line with a morphologically altered endocytic recycling compartment. J. Cell Physiol. 155:579-594.
41. Merdes, A., K. Ramyar, J.D. Vechio, and D.W. Cleveland. 1996. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell. 87:447-458.
42. Meyerowitz, E., and D. Kankel. 1978. A genetic analysis of visual system development in Drosophila melanogaster. Dev. Biol. 62:112-142.
43. Moremen, K.W., and P.W. Robbins. 1991. Isolation, characterization, and expression of cDNAs encoding murine α-mannosidase II, a Golgi enzyme that controls conversion of high mannose to complex N-glycans. J. Cell Biol. 115: 1521-1534.
44. Muhua, L., T.S. Karpova, and J.A. Cooper. 1994. A yeast actin-related protein homologous to that in vertebrate dynactin complex is important for spindle orientation and nuclear migration. Cell. 78:669-679.
45. Nakata, T., and N. Hirokawa. 1995. Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde Iysosome membrane transport. J. Cell Biol. 131:1039-1053.
46. Nangaku, M., R. Sato-Yoshitake, Y. Okada, Y. Noda, R. Takemura, H. Yamazaki, and N. Hirokawa. 1994. KIF1B, a novel microtubule plus enddirected monomeric motor protein for transport of mitochondria. Cell. 79: 1209-1220.
47. Nilsson, T., M.H. Hoe, P. Slusarewicz, C. Rabouille, R. Watson, F. Hunte, G. Watzele, E.G. Berger, and G. Warren. 1994. Kin recognition between medial Golgi enzymes in HeLa cells. EMBO J. 13:562-574.
48. Paschal, B.M., E.L. Holzbaur, K.K. Pfister, S. Clark, D.I. Meyer, and R.B. Vallee. 1993. Characterization of a 50-kDa polypeptide in cytoplasmic dynein preparations reveals a complex with p150GLUED and a novel actin. J. Biol. Chem. 268:15318-15323.
49. Paschal, B.M., and R.B. Vallee. 1987. Retrograde transport by the microtubule-associated protein MAP 1C. Nature (Lond.). 330:181-183.
50. Pavelka, M., and A. Ellinger. 1983. Effect of colchicine on the Golgi complex of rat pancreatic acinar cells. J. Cell Biol. 97:737-748.
51. Plamann, M., P.F. Minke, J.H. Tinsley, and K.S. Bruno. 1994. Cytoplasmic dynein and actin-relaled protein Arp1 are required for normal nuclear distribution in filamentous fungi. J. Cell Biol. 127:139-149.
52. Plough, H., and P. Ives. 1935. Induction of mutations by high temperature in Drosophila. Genetics. 20:42-69.
53. Rabouille, C, N. Hui, F. Hunte, R. Kieckbusch, E.G. Berger, G. Warren, and T. Nilsson. 1995. Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J. Cell Sci. 108:1617-1627.
54. Rapp. S., R. Saffrich, M. Anton, U. Jakle, W. Ansorge, K. Gorgas, and W.W. Just. 1996. Microtubule-based peroxisome movement. J. Cell Sci. 109:837-849.
55. Reaves, B., M. Horn, and G. Banting. 1993. TGN38/41 recycles between the cell surface and the TGN: brefeldin A affects its rate of return to the TGN. Mol. Biol. Cell 4:93-105.
56. 2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J. Cell Biol. 137:1-12.
57. Schafer, D.A., S.R. Gill, J.A. Cooper, J.E. Heuser, and T.A. Schroer. 1994. Ul-trastructural analysis of the dynactin complex: an actin-related protein is a component of a filament that resembles F-actin. J. Cell Biol. 126:403-412.
58. Schrader, M., J. Burkhardt, E. Baumgart, G. Lüers, H. Spring, A. Völkl, and H. Fahimi. 1996. Interaction of peroxisomes with microtubules. Tubular and spherical peroxisomes in HepG2 cells and their alterations induced by microtubule-active drugs. Eur. J. Cell Biol. 69:24-35.
59. Schroer, T.A. 1996. Structure and function of dynactin. Sem. Cell Devel. Biol. 7: 321-328.
60. Schroer, T.A., and M.P. Sheetz. 1991. Two activators of microtubule-based vesicle transport. J. Cell Biol. 115:1309-1318.
61. Schweizer, A., J.A. Fransen, K. Matter, T.E. Kreis, L. Ginsel, and H.P. Hauri. 1990. Identification of an intermediate compartment involved in protein transport from endoplasmic reticulum to Golgi apparatus. Eur. J. Cell Biol. 53:185-196.
62. Sönnichsen, B., J. Füllekrug, P. Nguyen Van, P. Diekmann, D.G. Robinson, and G. Mieskes. 1994. Retention and retrieval: two mechanisms cooperate to maintain calreticulin in the endoplasmic reticulum. J. Cell Sci. 107:2705-2717.
63. Steffen, W., J.L. Hodgkinson, and G. Wiche. 1996. Immunogold localization of the intermediate chain localization within the complex of cytoplasmic dynein. J. Struct. Biol. 117:227-235.
64. Steuer, E.R., L. Wordeman, T.A. Schroer, and M.P. Sheetz. 1990. Localization of cytoplasmic dynein to mitotic spindles and kinetochores [see comments]. Nature (Lond.). 345:266-268.
65. Terasaki, M., L.B. Chen, and K. Fujiwara. 1986. Microtubules and the endoplasmic reticulum are highly interdependent structures. J. Cell Biol. 103: 1557-1568.
66. Thyberg, J., and S. Moskalewski. 1985. Microtubules and the organization of the Golgi complex. Exp. Cell Res. 159:1-16.
67. Toyoshima, I., H. Yu, E.R. Steuer, and M.P. Sheetz. 1992. Kinectin, a major kinesin-binding protein on ER. J. Cell Biol. 118:1121-1131.
68. Vaisberg, E.A., P.M. Grissom, and J.R. McIntosh. 1996. Mammalian cells express three distinct dynein heavy chains that are localized to different cytoplasmic organelles. J. Cell. Biol. 133:831-842.
69. Vallee, R.B., K.T. Vaughan, and C.J. Echeverri. 1995. Targeting of cytoplasmic dynein to membranous organelles and kinetochores. Cold Spring Harbor Symp. Quant. Biol. 60:803-811.
70. Vallee, R., and M.P. Sheetz. 1996. Targeting of motor proteins. Science (Wash. DC). 271:1539-1544.
71. Vaughan, K.T., and R.B. Vallee. 1995. Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued. J. Cell Biol. 131:1507-1516.
72. Waterman-Storer, C.M., S. Karki, and E.L. Holzbaur. 1995. The p150Glued component of the dynactin complex binds to both microtubules and the actin-related protein centractin (Arp-1). Proc. Natl. Acad. Sci. USA. 92:1634-1638.
73. Wiemer, E.A., T. Wentzel, T.J. Deerinck, M.H. Ellisman, and S. Subramani. 1997. Visualization of the peroxisomal compartment in living mammalian cells: dynamic behavior and association with microtubules. J. Cell Biol. 136:71-80.
74. Xiang, X., S.M. Beckwith, and N.R. Morris. 1994. Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA. 91:2100-2104.
75. Yu. H., I. Toyoshima, E.R. Steuer, and M.P. Sheetz. 1992. Kinesin and cytoplasmic dynein binding to brain microsomes. J. Biol. Chem. 267:20457-20464.